    [From the U.S. Government Printing Office, www.gpo.gov]

      SYMPOSIA SERIES FOR UNDERSEA RESEARCH NOAA'S UNDERSEA RESEARCH PROGRAM
      VOL. 3 NO. 1, 1985
                                                     Coasaal �~ne
                                                     introreat:cn

    : The Ecology

      of Coral Reefs

                U. S. DEPARTMENT OF COMMERCE NOAA
                COASTAL SEREVICES CENTER
                2234 SOUTH HOBSON AVENUE   ---,
                CHARLEStON, SC 29405-24137 '

       ~i~i
       - '

       US DEPARTMENT
       OF COMMERCE  -
       Nationai Oceanic   and
       Atmospheric Administration

             -I                                                '-a.--~j

    SYMPOSIA SERIES FOR UNDERSEA RESEARCH
    NOAA'S UNDERSEA RESEARCH PROGRAM, VOL. 3 NO. 1, 1985

    The Ecology

    of Coral Reefs

    Results of a Workshop on Coral Reef
    Ecology held by the American Society
    of Zoologists, Philadelphia, Pennsylvania,
    December 1983

    Edited by
    Marjorie L. Reaka
    Department of Zoology
    University of Maryland
    College Park, Maryland 20742
    Washington, D.C.
    September 1985

    U.S. DEPARTMENT OF COMMERCE
    Malcolm Baldrige, Secretary
    National Oceanic and Atmospheric Administration
    Anthony J. Calio, Deputy Administrator
    Oceanic and Atmospheric Research
    Ned A. Ostenso, Assistant Administrator
    Office of Undersea Research
    Elliott Finkle, Director

                         Symposia Series for Undersea Research

        The National Oceanic and Atmospheric Administration's (NOAA) Office Of
    Undersea Research provides manned undersea facilities and other research support
    for investigations of aquatic environments in the areas of biological, geological,
    and ecological research. There are currently five national undersea research
    facilities which operate under cooperative agreements between universities and
    NOAA. These facilities are located at: the West Indies Laboratory of Fairleigh
    Dickinson University, the University of North Carolina at Wilmington, the
    University of Connecticut at Avery Point, the University of Southern California,
    and the University of Hawaii.

         NOAA's Office of Undersea Research provides facilities for scientists to
    conduct research supporting NOAA's mission objectives in the areas of: marine
    fisheries, marine pollution, sea floor properties and processes, and ocean
    services.

         Since its inception, NOAA also has encouraged and supported the use of
    submersibles to perform in-situ underwater observations and data gathering.
    Many shallow-water submersible missions have been supported, including the use
    of the Johnson Sea-Link, the Nekton-Ganmma, and the Mermaid, as well as deep-water
    missions using the Alvin. The goals of the submersible programs are to support
    the research requirements of NOAA's major program elements and its Sea GrantW
    College system.

         This Symposia Series for Undersea Research has been developed specifically
    to provide a pu Ishi~ng me~Tim for national symposia whose contents have addressed
    topics related to undersea research activities. Additional information concerning
    this series and other activities of NOAA's Office of Undersea Research may be
    obtained by contacting:

                            Director
                            NOAA's Office of Undersea Research
                            Mail Stop R/SE2
                            6010 Executive Boulevard, Roomi 805
                            Rockville, MD   20852

    Photo Credits: Color photographs are from Bruce Nyden, Marjorie Reaka, Phillip
                    Lobel, or the Office of Undersea Research.

                                            ii

                                  TABLE OF CONTENTS

    Chapter I.  INTRODUCTION. Marjorie L. Reaka ............................ 1

    Chapter II.   RESULTS OF A WORKSHOP ON CORAL REEF ECOLOGY:  SYNTHESES
                  OF DISCUSSION SECTIONS ......................................7

                  Overview: The Dynamics of Recruitment in Coral Reef
                    Organisms. William N. McFarland ..........................9

                  Growth and Life History Patterns of Coral Reef Organisms:
                    A Discussion Group Summary and Overview. Ronald H.
                    Karlson ................................................. 17

                  Overview: Coral Reef Community Structure and Function.
                    Mark A. Hixon ... .......................................... 27

                  Some Thoughts on the Past, Present, and Future of Studies on
                    Coral Reef Community Metabolism.  S. V. Smith ............. 33

    Chapter III. CONTRIBUTED PAPERS .......................................... 35

                  Recruitment of Young Coral Reef Fishes From the Plankton.
                    William N. McFarland and John C. Ogden .................... 37

                  Pelagic Duration, Dispersal, and the Distribution of Indo-
                    Pacific Coral-Reef Fishes. Edward B. Brothers and
                    Ronald E. Thresher ........................................ 53

                  Diurnal Periodicity of Spawning Activity by the Hamlet Fish,
                    Hypoplectrus guttavarius (Serranidae). Phillip S.
                    Lobel and Steve Neudecker ................................. 71

                  Patterns of Reproduction in Small Jamaican Brittle Stars:
                    Fission and Brooding Predominate. Ronald H. Emson,
                    Philip V. Mladenov and lain C. Wilkie ..................... 87

                  Reef Zooplankton Collected Along a Depth Gradient at
                    Discovery Bay, Jamaica.  Sharon L. Ohlhorst ............... 101

                  Temporal Patterns of Zooplankton Migration. Sharon L.
                    Ohlhorst and W. David Liddell ............................. 117

                  Field Analysis of the Dominance Hierarchy of the Bicolor
                    Damselfish Stegastes partitus (Poey) (Pisces: Poma-
                    centridae). Yvonne Sa3ovy .............................. 129

                  A Comparison of Fore and Back Reef Populations of Diadema
                    antillarum Philippi and Eupomacentrus planifrons
                    Cuvier at St. Croix, U.S. Virgin Islands. C. Lance
                    Robinson and Ann Houston Williams ......................... 139

    Carbonate Sediment Production by the Rock-Boring Urchin
      Echinometra lucunter and Associated Endolithic
      Infauna at Black Rock, Little Bahama Bank.  Charles
      M. Hoskin and John K. Reed ................................    151

    Highly Productive Eastern Caribbean Reefs:  Synergistic
      Effects of Biological, Chemical, Physical, and
      Geological Factors. Walter H. Adey and Robert S.
      Steneck ...................................................    163

    Studies on the Bio-Optics of Coral Reefs.  Phillip Dustan ...  189

    Preliminary Studies of Denitrification on a Coral Reef.
      Sybil P. Seitzinger and Christopher F. D'Elia .............    199

                                CHAPTER I: INTRODUCTION

                                   Marjorie L. Reaka
                                 Department of Zoology
                               The Universit of Maryland
                             College Park, Maryland  20742

         This volume presents the results of a workshop on the ecology of coral
    reefs that was held at the American Society of Zoologists meetings in Philadel-
    phia, December 1983. The workshop, which included four symposium presentations,
    four discussion sections, and presentations of undersea research facilities by
    NOAA's Office of Undersea Research, was sponsored by the Division of Ecology of
    the ASZ. The four symposium talks and discussion sections addressed the topics
    of growth and life history patterns, recruitment, community organization, and
    community metabolism in coral reef systems. The workshop was unusually well
    attended (attendance in the Ecology Division of the ASZ was 30% higher than in
    previous years and two additional contributed paper sessions in the Division
    of Ecology were devoted specifically to coral reef ecology), and vigorous group
    discussions continued well into the night. The objective of the workshop was
    to focus attention on what we do and do not know about the ecology of coral
    reefs, particularly along depth gradients, and to assess the most important
    directions for future research on coral reefs.

         A previous volume in this series (Reaka, 1983), containing symposium
    presentations and contributed papers in each of the four topical areas, was
    made available at the Coral Reef Workshop. The present volume presents the
    main conclusions derived from the discussion sections (Chapter II) and additional
    contributed papers on the ecology of coral reefs (Chapter III).

         In Chapter II, the discussion leaders summarize the topics discussed and
    the conclusions reached in each discussion section.  William McFarland points
    out that astonishingly little is known about recruitment in coral reef species.
    He identifies some of the reasons for our lack of knowledge in this area, not
    the least of which is the prevalence of planktonic larvae in reef organisms.
    The production of hundreds to millions of tiny dispersing planktotrophic larvae
    distinguishes marine animals from those in every other major environment.
    Furthermore, the incidence of species with long-lived planktotrophic larvae is
    inversely related to latitude (Thorson, 1950; Mileikovsky, 1971), so that, in
    contrast to marine communities from high latitudes, the vast majority of coral
    reef species produce planktonic dispersing young.  This phenomenon has profound
    implications for the population dynamics, community organization, and even
    evolutionary patterns of marine species compared to those in terrestrial or
    fresh water environments. In marine species thousands of recruits may occur in
    local areas in some years but not in others; planktonic larvae may settle in
    their parent population, may be carried to distant habitable sites, or even may
    be swept out to sea without any favorable substrate having been encountered.
    McFarland discusses several mechanisms that enhance the predictability of local
    recruitment on coral reefs, including the timing and dynamics of reproduction,
    currents or eddies that may return larvae to their parent populations, and
    behavioral patterns of the larvae and settling juveniles themselves. These

                                          I

    mechanisms, as well as fine scale observations of the larvae of species from
    different reef habitats, deserve extensive research before we will understand
    this critically important aspect of the biology of coral reef organisms.

         Ronald Karlson summarizes the conclusions of his discussion section on a
    related topic, life history patterns. An emerging body of research demonstrates
    that the observed growth rates, form, and longevity of corals along depth
    gradients result from complex interactions between physical (e.g., light and
    wave disturbance) and biotic variables. Recent research shows that sublethal
    phenomena such as injuries due to physical and biotic agents have significant
    implications for growth and reproduction in many sessile reef organisms.  These
    processes can vary significantly in different habitats. This discussion group
    also addressed the important topic of ecological and evolutionary patterns in
    solitary vs. colonial organisms on coral reefs. The importance of fission,
    fusion, and fragmentation (and thus of colony size) in both solitary and colonial
    species received particular attention as a productive avenue for future research.

         Mark Hixon lead the discussion section on community structure and function.
    Coral reef ecologists have been in the forefront of the debate on whether
    communities are organized by stable predictable processes or whether they
    merely represent independent populations in shifting states of disequilibria.
    One of the reasons that disequilibrium and stochastic processes have been so
    apparent in coral reef communities may be because dispersing, feeding larvae
    engender unpredictable recruitment. However, recent research also has demon-
    strated the importance of irregular catastrophic perturbations, such as storms
    (e.g., Woodley, et al., 1981), population outbreaks (e.g., Birkeland, 1982), or
    diseases (e.g., Lessios, et al., 1984) in the organization of coral reef communi-
    ties. One of these events-, th-e mass mortality of Caribbean sea urchin populations,W
    was ongoing at the time of the workshop and was a major topic of discussion.
    Although the causes and mechanisms of this outbreak still are not well under-
    stood, Mixon identifies the heuristic value of this "natural experiment" which
    has removed a major herbivore over large local and geographical areas of reefs.
    This discussion lead to an evaluation of a more deterministic process, herbivory
    by urchins vs. fishes, on reefs; this discussion centered on how human activities
    such as fishing in certain well studied localities can affect our interpretations
    of the past and present organization of reef communities. Although terrestrial
    and fresh water ecologists have been concerned about the effects of human inter-
    vention on natural communities for some time, the pervasiveness of this problem
    in coral reef communities has attracted attention only recently. Hixon argues
    that one of the most critical needs for future research is for experimental
    manipulations and long term comparative studies.

         The discussion section on community metabolism was led by Stephen Smith.
    Smith shows how this field has developed from a focus on oxygen and carbon flux
    to studies of the physical, chemical, and biological variables that control
    metabolism of the reef ecosystem. The discussion addressed how the quantity and
    quality of available nutrients affect productivity, how nutrient flux between sub-
    communities can affect nutrient balance of the overall reef ecosystem, and how new
    technological approaches can improve our ability to measure community metabolism.
    Smith stresses that a holistic approach, including comparisons with other ecosys-
    tems, will represent important avenues for future research in this area.

            Chapter III includes contributed papers whose topics span those covered
    Win the four discussion groups. McFarland and Ogden provide a comprehensive
       review of recruitment in coral reef fishes and evaluate the various hypotheses
       advanced to account for the presence of planktonic larvae. They conclude that
       both reduced predation on young and enhanced dispersal favor the development of
       long-lived larvae which migrate offshore from local reefs. Due to the hetero-
       geneity in patterns of larval development, however, these authors note that the
       relative importance of these selective factors must vary among different species
       of reef fishes. Brothers and Thresher evaluate the relationship between larval
       durations and the extent of the geographic distributions in 115 species of ree'
       fishes. Their study yields the new and interesting result that, if larval
       durations are < about 45 days, the size of the geographic range (usually an
       indication of dispersal patterns) is not correlated with length of larval life.
       Larvae which have pelagic phases longer than 45 days, however, all have broad
       distributions and can transgress oceanic barriers at least occasionally. This
       work, then, has important implications for patterns of colonization and biogeog-
       raphy. Lobel and Neudecker analyze another aspect of reproductive biology of
       reef fishes that can influence dispersal of larvae on reefs:  the timing and
       location of spawning. They describe and compare courtship in several species
       of hamlets. These fishes spawn at dusk over specific high reef structures,
       which may reduce predation and facilitate dispersal of eggs. The time and
       duration of spawning is influenced by depth and/or lunar phase as well as
       simulated attacks by predators. Emson, Mladenov, and Wilkie provide information
       on a different aspect of reproductive biology in a reef invertebrate. Various
       modes of asexual reproduction, including fission, are well known in a number of
    .   relatively sessile invertebrate phyla.  However, these authors demonstrate that
       fission represents the major method of reproduction in many small species of
       motile brittle stars associated with algae and sea grass in lagoonal habitats.
       Many of these ophiuroids also apparently produce dispersing planktonic larvae,
       an unexpected phenomenon because small size usually is associated with brooding.
       These results again have implications for patterns of recruitment and maintenance
       of local populations.

            Both meroplankton (the larvae of benthic reef organisms) and holoplankton
        (organisms that spend their entire life in the plankton) exhibit diel vertical
       migrations that are likely to influence their tendency to disperse in currents
       and their susceptibility to predation. The long term study reported by Ohlhorst
       also suggests that other factors, such as preceding rain and lunar effects,I
       can influence abundance of zooplankton above the reef. Ohlhorst further demon-
        strates that numbers of zooplankton decline significantly with increased depth,
        and that even in the shallow areas these plankton can provide relatively little
        of the metabolic requirements for sessile reef organisms. Using frequent
        collections throughout the day and night, Ohlhorst and Liddell provide the
        first precise documentation of a predawn surge in abundance of plankton over
        the reef that complements the postsunset peak of emergence known for these
        organisms. A swarming holoplanktonic copepod usually W~as the most common
        zooplankter in both Jamaica and St. Croix, althoukgh other taxa, including
        meroplankters, became prominent during the hours around sunset. These papers
        therefore are related to the topics of dispersal and reproductive biology
        discussed above but also bear on community organization and energy flow among
        different components of the reef community.

                                             3

         The following three papers in the volume deal with damselfishes and/or
    urchins on reefs.  The territorial activities of damselfishes are known to be I
    significant for the structure and productivity of reef communities (e.g.,
    Brawley and Adey, 1977; Hixon, 1983; and others). Sadovy studied the detailed
    dominance relations among individuals of bicolored damselfish in the field.
    Her results showed a linear, size-dependent dominance hierarchy in these fish
    and revealed some interesting similarities and differences between field and
    otherwise comparable laboratory studies.  Robinson and Williams compare population
    characteristics of threespot damselfish and urchins (Diadema) in shallow back
    reef and fore reef environments. They found that urchins are larger, occur in
    lower densities, and are found higher in coral branches on the back reef than
    on the fore reef; in contrast, damselfish live at higher densities, have larger
    lawns, and exhibit less aggression toward urchins on the fore reef than on the
    back reef. Urchins may remain small and close to the substrate on the shallow
    fore reef because high wave action inhibits their grazing; thus interference
    between urchins and damselfish is less strong when mediated by disturbance on
    the fore reef than in more benign conditions on the back reef. Examining
    another species of urchin with a different but very significant impact on the
    structure of reefs, Hoskin and Reed use carefully controlled experimental
    methods to estimate the rates of bioerosion of carbonate substrates by urchins
    (Echinometra) and other burrowing infauna. These urchins excavate approximately
    8.9 g substrate/m2/day (9 tons/year for the population), while the remaining
    infauna produces about 5 g sediment/m2/day (6.5 tons/year). This study illus-
    trates the tremendous amount of sediment that is produced and transported in
    benthic reef communities. Scouring and burial by this sediment must represent
    one of the most important agents influencing the structure and dynamics of reef
    communities, yet the significance of these processes for community organization
    are almost unstudied. In addition, this study provides new data on the sources
    and rates of degradation of reef substrates, a significant aspect of long term
    morphogenesis and diagenesis of reefs. This paper therefore provides a link
    between the papers on community organization and those on community metabolism.

         Adey and Steneck show how reef productivity is related to substrate
    complexity and surface area, light and water flow, and abundance of turf algae.
    They demonstrate that all of these factors can be understood in the context of
    geological development of the reefs. Using upstream/downstream flow respirometry
    techniques on reefs in three different stages of geological development in St.
    Croix, these authors provide good evidence for some of the highest rates of
    primary productivity reported for any marine environment. Dustan explores a
    different method of assessing primary productivity.  He provides initial data
    on the spectral intensities of light impinging on, absorbed, and reflected by
    different substrates. Dustan suggests that much can be learned about the photo-
    biology of reef organisms using these nondestructive bio-optical sampling
    techniques and indicates that we may be able to estimate primary productivity
    over vast tracts of previously inaccessible reefs if optical signals from these
    reefs can be detected from orbiting spacecraft.  Although we are in the initial
    stages of interpreting these data, such new technological approaches offer the
    promise of measuring and understanding productivity on a global scale.  Seitzinger
    and D'Elia present data on another new and potentially important aspect of
    community metabolism on reefs.  While nitrogen fixation on reefs has received
    well deserved attention, Seitzinger and D'Elia show that some reef habitats, in
    particular dead coral heads and sediments, may be the sites of extensive denitri-

                                                                                        4
                                            4

                                          ERRATA
         Several typographical errors were inadvertently included in our publication
    of The Ecology of Deep and Shallow Coral Reefs [Symp. Ser. Undersea Res., Vol.
    1(1T 71983], anwe wouTlike totake this opportunity to correct them.

         For Chornesky, E. A., and S. L. Williams, "Distribution of Sweeper Tentacles
    on Montastrea cavernosa, p. 61, par. 3, line 15 should read "or after contact
    and recognition;" p. 63, caption for figure 1 should read "For M. annularis,
    change in number of polyps."

         For Wolf, N. G., E. B. Bermingham, and M. L. Reaka, "Relationships Between
    Fishes and Mobile Benthic Invertebrates on Coral Reefs," p. 69, the address of
    E. B. Bermingham should read "Department of Molecular and Population Genetics;"
    p. 72, line 3 should read "Although fewer planktivores were recorded on C than
    on A reefs."

         For Hay, M. E., and T. Goertemiller, "Between-Habitat Differences in
    Herbivore Impact on Caribbean Coral Reefs," p. 100, par. 4, line 3 should read
    "and 12.8% versus 1% on Lighthouse (fig. 1);" p. 101, par. 2, lines 10-11 should
    read "or motility in sea urchin sperm (Norris and Fenical 1982, Paul and Fenical
    1983). The polyphenolic compounds produced by Turbinaria."

         For Szmant-Froelich, A., "Functional Aspects of Nutrient Cycling on Coral
    Reefs," p. 136, Table 1, DIN should be TDN.

                                              6

    fication, whereby NO2 and N03 are lost from the system as atmospheric N2. Such
    studies make important contributions to Smith's goal of understanding the
    overall balance of nutrient flow within and between major components of reef
    communities.

         Many people have contributed to the successful completion of this volume.
    Thanks are especially extended to the authors for their fine contributions and
    cooperation throughout the editing process. In addition, the reviewers of
    these papers are gratefully acknowledged for contributing their time and
    criticisms, all of which improved the volume.  Completion of this symposium
    volume would have been impossible without the expert typing and editorial
    assistance of Ms. Marcia Collie, Staff Assistant from NOAA's Office of Undersea
    Research; her cooperation, advice, and assistance through all the stages of
    publication are acknowledged with heartfelt thanks.  Similarly, publication was
    made possible through NOAA's Office of Undersea Research, and the support of
    Mr. William Busch and Mr. Elliott Finkle throughout this endeavor are sincerely
    appreciated.  Lastly, I thank my husband, Stephen, and our two little blonde
    boys, Alexei and Erik, for their sunshine and enthusiasm.

                                    LITERATURE CITED

    Birkeland, C.  1982.  "Terrestrial Runoff as a Cause of Outbreaks of Acanthaster
       planci (Echinodermata: Asteroidea)." Mar. Biol. 69:175-185.

    Brawley, S. H., and W. H. Adey.  1977.  "Territorial Behavior of Threespot
       Damselfish (Eupomacentrus planifrons) Increases Reef Algal Biomass and
       Productivity."  Environ. Biol.  Fish. 2:45-51.

    Hixon, M. A.  1983.  "Fish Grazing and Community Structure of Reef Corals and
       Algae:  A Synthesis of Recent Studies," pp. 79-87.  In:  M. L. Reaka (ed.),
       The EcologY of Deep and Shallow Coral Reefs.  Symp. Ser. Undersea Res., Vol.
       T7).  NOAA Undersea Res. Progr., Rockville, Md.

    Lessios, H. A., D. R. Robertson, and J. D. Cubit.  1984.  "Spread of Diadema
       Mass Mortality Through the Caribbean." Science 226:335-337.

    Mileikovsky, S. A.  1971.  "Types of Larval Development in Marine Bottom
       Invertebrates, Their Distribution and Ecological Significance: A Re-
       Evaluation." Mar. Biol. 10:390-404.

    Reaka, M. L., ed.  1983.  The Ecology of Deep  and Shallow Coral Reefs.  Symp.
       Ser. Undersea Res., VolI(1).  NOAUnde-rsea Res. Progr., Rockville, Md.
       149 pp.

    Thorson, G. 1950. "Reproductive and Larval Ecology of Marine Bottom
       Invertebrates." Biol. Rev. 25:1-45.

    Woodley, J. D., E. A. Chornesky, P. A. Clifford, J. B. C. Jackson, L. S. Kaufman,
       N. Knowlton, J. C. Lang, M. P. Pearson, J. W. Porter, M. C. Rooney, K. W.
       Rylaarsdam, V. J. Tunnicliffe, C. M. Wahle, J. L. Wulff, A. S. G. Curtis, M.
       D. Dallmeyer, B. P. Jupp, M. A. R. Koehl, J. Neigel, and E. M. Sides. 1981.
        "Hurricane Allen's Impact on Jamaican Coral Reefs."  Science 214:749-755.

                                             5

                    CHAPTER II:  RESULTS OF A WORKSHOP ON CORAL REEF ECOLOGY:  SYNTHESES

    ion  OF DISCUSSION SECTIONS

    les

    d    I
    1    1                                            Figure 1

                     Coral reefs have been tremendously important in the history of human
                civilizations.  Reefs support fisheries and provide protected embayments that
                are essential for food and commerce in coastal cultures.  It is critical that
                we understand the biological dynamics responsible for the formation and
                degradation of these systems in order to preserve and manage their resources.
                NOAA's underwater habitat, HYDROLAB (fig. 1), has (continued on next page)

                  Figure 2                                                         Figure 3
                                                    7

                                                                                 iN"

                                                           Figure 5

           Figure 4

    allowed scientists to conduct experimental field studies on reproduction,
    recruitment, population dynamics, and community organization of coral reef
    communities that would have been impossible without the extended diving time
    made possible through saturation techniques. Here divers study the factors
    that influence recruitment of fishes and invertebrates (figs. 2, 3, 4), many
    of them important fisheries and food stocks, on artificial reefs where large
    predators and grazers are excluded or allowed access. These facilities also
    have allowed extended study of the life histories, growth, and species inter-
    actions of the major structural agents on reefs, corals and sponges (fig. 5).
    The AEGIR, NOAA's mobile underwater habitat that will replace HYDROLAB in 1986,
    also is shown here (fig. 6).

                                       Figure 6
                                           8

            discussion section that spawning is a variable act within and between species
            a nd an activity that involves considerable behavioral plasticity. If the
            function of casting eggs into the plankton is to rapidly remove them from reef
           predators, then doing so at dusk (as many fish do) would seem safest.  The fact
           that many fish do not spawn at dusk may relate to the presence of favorable
           currents that flush the eggs rapidly offshore and out of the reach of abundant
           small reef predators. Unfortunately, few papers deal simultaneously with
           spawning and local currents (McFarland and Ogden, 1985). As a result, it is
           rather difficult to resolve the differences that exist between species (see
           Robertson, 1983, for spawning variation in several acanthurids).

                 Although recruitment from the plankton occurs at the end of the larval
           stage, knowing how and when potential propagules are introduced into the plankton
           is essential for understanding recruitment because the spawning act initiates
           the recruitment process. The difficulties identified above-could be partly
           resolved by an integrated study in a local area of the seasonal, monthly, and
           diel spawnings of many different species of coral reef fishes. Evaluating the
           function~s) of differential spawning amongst the various species will require
           that the observations be tightly coupled with analysis of local currents (for
           example, Robertson, 1983). If this is accomplished in severa~l different areas,
           it should be possible to sort out the trade-offs that different species invoke
           in order to "safely" deliver young to the plankton.

                 Once spawned, the eggs of coral reef fishes usually hatch within a day
           (Thresher, 1984). Although most coral reef fish eggs and larvae are flushed
           offshore, in some circumstances the eggs and larvae are entrained within lagoons
           (apparently by local currents). Because eggs and very young larvae cannot swim
    *      ~~and orient actively (Leis and Rennis, 1983), it is generally assumed that, when
           at sea, larvae are widely dispersed (through diffusional and other processes).
           As pointed out by Lobel during the discussion, similarly sized larvae of the
           same species often are taken in the same plankton hauls. In addition, newly
           recruited fish larvae often appear on reef sites in small groups of 3 or more
           fish (e.g., pempherids, high hats, grunts, etc.), but may also recruit as
           individuals, as noted by McFarland at the discussion. The question arose,
           therefore, as to how valid is the assumption of wide dispersion of individuals
           at sea? There was general agreement that little is really known about the
           distribution and dispersion of the eggs and larvae of individual species at sea
           (but see Leis and Goldman, 1984, for a beginning). Shapiro's paper in volume I
           of these proceedings develops a model which suggests that the dispersion of
           eggs resulting from a single spawning act will retain reasonable cohesiveness
           (after 24 hours of drift in a current; this varies depending on assumed
           conditions, but could yield as many as I post-.hatchling in each adjacent m3 of
           water). If newly hatched larvae can swim actively and are mutually attracted,
           it is at least possible that in the first few days they might form cohesive
           aggregations. Shapiro's thesis specifically suggests the possibility that
           young recruiting reef fishes may, in some instances, be kin. Tests of this
           hypothesis can involve electrophoretic analysis of recent recruits that occur
           in cohesive groups. A more immediate test involves the aging of all recruits
           in a group by use of the otolith aging technique (Brothers and Thresher, 1985;
           Victor, 1983). If spawned simultaneously and dispersed as a group, the
           cohesiveness of which is retained by active behaviors by individuals in the

                                                 to

             OVERVIEW: THE DYNAMICS OF RECRUITMENT IN CORAL REEF ORGANISMS

                                  William N. McFarland
                           Section of Ecology and Systemnatics
                            Division of Biological Sciences
                                   Cornell University
                                Ithaca, New York 14853

          In her introduction to volume 1 of these proceedings, Marjorie Reaka
    states, "The second set of papers addresses the issue about which we probably
    know the least in coral reef ecology:  what factors control recruitment?"  One
    must conclude from the three contributed papers in volume I of these proceedings
    (Lobel and Robinson, 1983; Shapiro, 1983; Victor, 1983) and the papers in the
    present volume (Brothers and Thresher, 1985; Lobel and Neudecker, 1985; McFarland
    and Ogden, 1985) that data on reproduction, larval development, and recruitment
    are sparse. This is astonishing when we consider that almost all coral reef
    fishes, and a great majority of tropical invertebrates too, cast their eggs and
    larvae into the plankton where they must survive and grow before they can settle
    again to the reef as juveniles.

          The discussion held on December 27, 1983, at the ASZ meeting in Philadelphia,
    dwelled on two aspects of recruitment, what we actually know and what we need
    to know to better understand the dynamics of reef recruitment.  About 20 par-
    ticipants were involved in the discussion.  Here I will summarize the more
    important trends of the discussion.

          Given the ubiquity of a planktonic larval phase in so many coral reef0
    organisms, why is so little known about recruitment? The answer is multiple.
    The eggs and larvae of most reef organisms are small, translucent, and difficult
    to identify to species.  They are extremely hard to maintain and study in
    captivity because they are fragile and nutritional requirements often are
    either unknown or difficult to adequately provide.  In addition, only over the
    last decade have newer techniques (e.g., otolith aging, increased use of SCUBA
    and saturation diving for observations, improved methods for measuring currents,
    etc.) become accessible to reef biologists.  The paper by McFarland and Ogden
    (this proceeding) addresses what is known about why so many fishes cast their
    eggs and larvae into the plankton.  They conclude that there is yet no definitive
    answer; that the function of a pelagic larval phase for one reef organism may
    not apply to another species; that in most species multiple functions prevail;
    and that avoiding predation and dispersal appear to be the most important
    factors that favor long-lived planktonic larvae.  In addition, the times of
    spawning in most reef species are poorly known.  In recent years, however,
    considerable effort has been placed on in situ observations of where and when
    reef fish spawn.  Lobel and Neudecker's-pape-r(this volume) describes spawning
    in a hamlet (Hypoplectrus guttavaius) and also reviews important papers on
    reproduction in other specTies of ishes.  Although many reef species spawn at
    specific *spawning sites and during a rush toward the surface, the time of
    spawning is variable, often occurring in the late afternoon and dusk (Lobel and
     Neudecker, 1985). However, spawning also often occurs during midday or midafter-
     noon (Colin, 1982; Robertson, 1983). It was the general conclusion in the

                                           9

    .    ~group, then each recruit in the group should be of the same daily age.  This
          specific experiment has not yet been performed.

                As tantalizing as the possibility of kinship in recruits may be, a larger
          related question prevails. What do larval fishes do when at sea? It is
         axiomatic that they feed and grow, but beyond that the discussion group agreed
          that the behaviors of larval reef fishes remain virtually unknown. Quantitative
          data on the behaviors of a variety of species of reef fishes are crucial to
          understanding the recruitment process. Answers will not be easy nor rapidly
          forthcoming, for they must involve careful, stratified plankton sampling to
          determine vertical distributions (at different times of the day), and also mus-c
          include specific experiments in the laboratory and on shipboard to assess the
          responses of fish larvae to various stimuli. The investigations are greatly
          complicated by larval growth. Because most reef fish larvae spend from I to 6
         weeks and in some instances up to 15 weeks at sea (Brothers and Thresher, this
          volume), behaviors must change as the larvae grow. It is critical, therefore,
          to also evaluate the ontogeny of larval behaviors. The central importance of
          such studies to the overall process of tropical fish recruitment, however,
          should motivate investigators to overcome the difficulties that the study of
          larval fish behavior presents. Especially in this area will creative and
          imaginative investigations help, for they will provide short cuts to what
          otherwise would be a prolonged undertaking. The lead provided by researchers
          studying larval fish behaviors in temperate waters, fortunately, can be of
          great assistance in getting started (e.g., Blaxter and Hunter, 1982; Lasker,
          1981; on clupeoid fishes).

                Since the classic demonstrations of Johannes Schmidt (1922) that the
          leptocephalus larvae of the European eel can drift at sea for not only months
          but in some instances for more than a year, the duration of larval life of
          fishes has provoked constant interest. Knowing how long a larva can exist at
          sea has been particularly important in explaining long-distance transport of
          reef fishes, e.g., the presence of Indo-Pacific reef species in the eastern
          Pacific (Brothers and Thresher, this proceeding). The problem has been frustra-
          ting because of the lack of methods to age larvae. The "invention" of the
          daily otolith aging technique (Panella, 1971; Brothers, et al., 1976) and the
          "discovery" of a transitional check mark in the otolith increments that approxi-
          mate settlement of the larvae from the plankton to the reef substrate (Brothers
          and McFarland, 1981; Brothers, et al., 1983; Victor, 1983) have revolutionized
          the aging of larval fishes and, as a consequence, estimating the duration of
          larval life of reef fishes. Brothers and Thresher's paper (this proceeding)
          examines 115 species of Pacific reef fishes. Interestingly, over 80% of these
          fishes have fairly short larval lives (< 45 days). All fishes with pelagic
          larval durations in excess of 45 days are widely distributed (as expected). We
          recognized that the use of otolith aging is an innovation that will assi-st in
          providing answers to many questions concerning recruitment. Already we have a
          better understanding of the lengths of larval life for a considerable number of
          species. In some species the length of larval life can be restricted to only a
          few days (e.g., French grunts, as noted by McFarland during the discussion) or
          can encompass a highly variable number of days (from a short number to many
          days and may show a strongly skewed distribution toward fewer days; Victor
      *   noted during the discussion that this is the case for some wrasses).  Given the

    novelty of the otolith aging techn~ique, a general warning was sounded that care
    should be taken with generalizations. Nevertheless, it was agreed that few
    studies on fish recruitment could effectively proceed without the use of this
    revealing technique.

          The paper by Lo-bel and Robinson (1983) re~viewed attempts to relate larval
    drift to mesoscale disturbances in the near surface waters, e.g., local current
    gy res .For many years various authors have invoked changes in local currents
    or even steady current conditions to explain how spawning, larval duration,
    and settlement are integrated to sustain local populations of fishes (Emery,
    1972; Johannes, 1978, 1980; Sale, 1970). It is only over thie last decade,
    however, that oceanographers have begun to develop instrumentation that allows
    ready determination of local current eddies, shears, etc., on a sufficiently
    small scale to be useful in biological investigations (see, for example,
    Robinson, 1983). Techniques include radio-tracked drogues, expendable rapid
    acting bathythermographs, current meters, and satellite infrared imagery. As
    deployed in Hawaii, the initial data appear to support the concept that larvae
    spawned at a particular site can drift in gyres (at certain times of the year
    only) and could be returned close to their point of departure in times coin-
    cident with the general length of larval life. We agreed that it was crucial
    that local current regimes in various areas of the tropics must be carefully
    measured at different times of the year and during all phases of the lunar
    month if the potential drift paths of eggs and larvae are to be ascertained.
    However, as indicated, daily changes in larval behaviors and the ability to
    swim and orient can place fishes in different local current regimes. It is
    possible, therefore, that active directed behaviors (such as vertical movements)~
    could increase the chance(s) that fishes will be dispersed to suitable reefW
    habitats for colonization. Thus, it is critical that subsurface currents as
    well as surface currents be measured.

          As crucial as the measurements of currents are, they must be coupled to
    ongoing investigations of spawning, egg and larval distribution, and larval
    behaviors if they are to result in meaningful conclusions for understanding
    recruitment dynamics in the tropics.

          As indicated by McFarland and Ogden (this proceeding) data on the actual
    settlement of reef fishes are sparse. Observations of settlement on a given
    day usually record the presence of recruits on a specific reef site, from which
    they were absent the previous day. Daily observations of this sort are useful
    in establishing recruitment cycles, but they reveal little about actual settle-
    ment behaviors of local reef fish. Do most reef fish larvae settle at night,
    or is there die] variation? And if so, are settlement behaviors species specific
    or plastic? What specific factors trigger settlement, and what attributes of a
    reef are attractive to each species? Answers to these questions will not yield
    to casual observation. As an example, during the discussion I indicated that
    newly recruited French grunts repeatedly established themselves on the same
    small coral heads and never recruited on closely adjacent heads that had similar
    configurations.  Choice of a site might, thus, be resolved not only by appropriate
    substrate requirements but also by microscale differences in currents, as noted
    by Lobel. To know exactly what factors control site selection by new recruits
    will require carefully controlled manipulative experiments for a broad spectrum
    of reef species.  Answers are critical before generalizations can be made:  if W

                                           12

    settlement is to a large degree passive and succeeds only because currents
    carry larvae over reefs, then the process can be considered somewhat stochastic;
    if, however, searching and testing behaviors, such as vertical movements in the
    water column (as observed in many invertebrate reef plankters; see McFarland
    and Ogden, this volume, for specific references), are widely utilized by larvae
    to identify suitable substrates on which to settle, then recruitment can be
    considered as an active determined process. However, even if fish larvae do
    actively 'search' for specific substrate as they settle from the plankton, or
    soon after, their success in establishing themselves can be negatively affected
    by the presence of previously settled juveniles (Shulman, et al., 1983). As a
    result, even if the act of settlement is deterministic forea-E'-larva, the
    overall success of individual recruits is infused with a large element of
    chance (e.g., being in a current that favors transport to native habitat,
    arriving in a region of native habitat at the appropriate time of day to avoid
    predation, actually finding an appropriate and 'empty' settlement site within
    the native habitat). In a very real sense, therefore, settlement can be viewed
    as partly determined and partly stochastic.  Because we remain largely ignorant
    of the details of the settlement process, and because recruitment is central to
    understanding coral reef fish community structure (see Helfman, 1978, for review),
    generalizations about the proximal and ultimate causes of the high species diver-
    sity of fishes associated with coral reefs remain, at best, first approximations.

          Although innumerable problems require solution to understand recruitment
    dynamics in coral reef organisms, it was generally concluded that rapid progress
    would result by focusing attention on four general areas:  (1) the timing and
    dynamics of reproduction:  where, when, and how often; (2) investigation of the
    fine scale horizontal, vertical, and diel distribution of larvae over a time
    frame that spans reproduction through recruitment; (3) coincident fine scale
    measures of local current regimes (at varied depths); and (4) descriptive and
    experimental investigations of the behaviors of larval coral reef organisms.
    Furthermore, it is not enough to study only one species, although individual
    researchers will be hard pressed to examine more than one at a time.

          Because of the necessary broad scope of recruitment studies, the research
    will involve planktologists, fish biologists, invertebrate biologists,
    behaviorists, and physical oceanographers. As a result, interdisciplinary
    collaborations will be a requirement in understanding and solving tropical
    recruitment processes.

                                    LITERATURE CITED

    Blaxter, J. H. S., and J. R. Hunter. 1982. "The Biology of the Clupeoid
       Fishes." Adv. Mar. Biol. 20:1-223.

    Brothers, E. B., C. P. Matthews, and R. Lasker. 1976. "Daily Growth Increments
       in Otoliths From Larval and Adult Fishes." Fish. Bull. 74:1-8.

    Brothers, E. B., and W. N. McFarland. 1981. "Correlations Between Otolith
       Microstructure, Growth, and Life History Transitions in Newly Recruited
       French Grunts (Haemulon flavolineatum (Desmarest), Haemulidae)." In: R.
       Lasker and J. Blaxter (eds.), Early Life History of Fish, II.  Rapp. P-V.
       Reun. Cons. Int.  Explor. Mer.:-7T37.

                                            13

    Brothers, E. B., D. McB. Williams, and P. F. Sale.  1983.  "Length of Larval
      Life in Twelve Families of Fishes at 'One Tree Lagoon,' Great Barrier Reef,
      Australia." Mar. Biol. 76:319-324.

    Brothers, E. B., and R. E. Thresher. 1985. "Pelagic Duration, Dispersal, and
       the Distribution of Indo-Pacific Coral-Reef Fishes," pp. 53-69. In: M. L.
       Reaka (ed.), The Ecology of Coral Reefs, Symp. Ser. Undersea Res., Vol. 3(1).
       NOAA Undersea Res. Progr., Rockvil-eMd.

    Colin, P. L. 1982. "Aspects of the Spawning of Western Atlantic Reef Fishes,"
       pp. 69-78. In: G. R. Huntsman, W. R. Nicholson, and W. W. Fox (eds.), The
       Biological Basis for Reef Fishery Management.  NOAA Tech. Memo NMFS-SEFC-T,
       Nat. Mar. FTis. Serv., Beaufort, NC.

    Emery, A. R. 1972. "Eddy Formation From an Oceanic Island: Ecological
       Effects." Carib. J. Sci. 12:121-128.

    Helfman, G. S. 1978. "Patterns of Community Structure in Fishes: Summary and
       Overview." Environ. Biol. Fish. 3:129-148.

    Johannes, R. E. 1980. "Using Knowledge of the Reproductive Behavior of Reef
       and Lagoon Fishes to Improve Fishing Yields." In: J. E. Bardach, J. J.
       Magnuson, R. C. May, and J. M. Reinhart (eds.),-lFish Behavior and Its Use in
       the Capture and Culture of Fishes.  Proc. 5th Int.enter Living Auat. Resource
       Managemt., Minila, Philippines. 512 pp.

    Lasker, R., ed.  1981.  Marine Fish Larvae.  Univ. Wash. Press, Seattle.  131 pp@

    Leis, J. M., and B. Goldman.  1984.  "A Preliminary Distributional Study of Fish
       Larvae Near a Ribbon Reef in the Great Barrier Reef." Coral Reefs, 2:197-203.

    Leis, J. M., and D. S. Rennis.  1983.  The Larvae of Indo-Pacific Coral Reef
       Fishes.  Univ. Hawaii Press, Honolulu'.  26   pp.

    Lobel, P. S., and S. Neudecker.  1985.  "Diurnal Periodicity of Spawning Activity
       by the Hamlet Fish, Hypoplectrus guttavarius (Serranidae)," pp. 71-86. In:
       M. L. Reaka (ed.), The Ecology of Coral Reefs, Symp. Ser. Undersea Res.,
       Vol. 3(1).  NOAA Uned'ersea Res. Fogr., Rockville, Md.

    Lobel, P. S., and A. R. Robinson.  1983.  "Reef Fishes at Sea:  Ocean Currents
       and the Advection of Larvae," pp. 29-38.  In:  M. L. Reaka (ed.), The Ecology
       of Deep and Shallow Coral Reefs, Symp. Ser. Undersea Res., Vol. 1(TT.  NOAA
       Undersea Res. Progr., Rockville, Md.

    McFarland, W. N., and J. C. Ogden.  1985.  "Recruitment of Young Coral Reef
       Fishes From the Plankton," pp. 37-51.  In:  M. L. Reaka (ed.), The Ecology of
       Coral Reefs, Symp. Ser. Undersea Res., Vol. 3(1).  NOAA Undersea Res. Progr.,
       RockviTTe, Md.

    Panella, G.  1971.  "Fish Otoliths:  Daily Growth Layers and Periodical Patterns."
       Science 173:1124-1127.

                                           14

    Robertson, D. R.  1983.  "On the Spawning Behavior and Spawning Cycles of Eight
       Surgeon Fishes (Acanthuridae) From the Indo-Pacific." Environ. Biol. Fish.
      9:193-223.

    Robinson, A. R., ed. 1983. "Overview and Summary of Eddy Science. 1.1 Eddy
      Currents in the Ocean," pp. 3-15.  In:  Eddies in Marine Science.  Springer-
      Verlag, Berlin.

    Sale, P. F. 1970. "Distribution of Larval Acanthuridae off Hawaii." Copeia
       4:765-766.

    Schmidt, J. 1922. "The Breeding Places of the Eel." Phil. Trans. Roy. Soc.
      Lond., Ser. B, 211:179-208.

    Shapiro, D. Y. 1983. "On the Possibility of Kin Groups in Coral Reef Fishes,"
      pp. 39-46. In: M. L. Reaka (ed.), The Ecology of Deep and Shallow Coral
      Reefs, Symp. Ser. Undersea Res., Vol. (1). NOAXUndersea Res. Progr.,
       Rockville, Md.

    Shulman, M. J., J. C. Ogden, J. P. Ebersole, W. N. McFarland, S. L. Miller, and
       N. G. Wolf. 1983. "Priority Effects in the Recruitment of Juvenile Coral
       Reef Fishes." Ecology 64:1508-1513.

    Thresher, R. E. 1984. Reproduction in Reef Fishes. Tropical Fish Hobbyist,
       Neptune City, NJ.  399 pp.

    Victor, B. C. 1983. "Settlement and Larval Metamorphosis Produce Distinct
       Marks on the Otoliths of the Slippery Dick, Halichoeres bivattatus," pp. 47-52.
       In: M. L. Reaka (ed.), The Ecology of Deep and Shallow Coral Reefs, Symp. Ser.
       Undersea Res., Vol. 1(1).NOAA Undersea  es.7rogr., Roc-'  '     lleF.

                                           15

              GROWTH AND LIFE HISTORY PATTERNS OF CORAL REEF ORGANISMS:
                       A DISCUSSION GROUP SUMMARY AND OVERVIEW

                                   Ronald H. Karlson
                         Ecology and Organismic Biology Program
                           School of Life and Health Sciences
                                 University of Delaware
                                Newark, Delaware 19716

          I would like to take this opportunity to thank all who attended our late
    evening discussion group. Although it would have been impossible for us to
    deal with all major taxa of coral reef organisms, we discussed a reasonably
    diverse array of colonial organisms and a group of solitary echinoderms.
    Taxonomic areas of research and a partial list of participants include actinians
    (Sebens), bryozoans (Jackson), corals (Brakel, Highsmith, Hughes, Hunter,
    Jackson), echinoderms (Highsmith, Keller, Levitan, Mladenov), gorgonians
    (Harvell, Lasker, Wahle), sponges (Harvell, Pomponi, Suchanek), and zoanthids
    (Karlson, Sebens, Suchanek).

          Six short presentations by Brakel, Hughes, Suchanek, Wahle, Karlson, and
    Mladenov were given in our discussion session. Each was followed by questions
    and/or discussion. Each presentation dealt with variability in one or more of
    the following: growth form, growth rate, overgrowth frequency, fecundity,
    survivorship, colonial integrity, or reproductive mode.  We also discussed size-
    specific variation in life histories, fission, fusion, and brooding in coral
    reef invertebrates.

          Brakel's presentation dealt with depth-related variation in the growth
    form of Porites astreoides (Brakel, 1983). He noted that much of the literature
    dealing with coral growth form suggests that there may be a simple monotonic
    relationship between colony shape and depth. Brakel's analysis indicates that
    flattened colonies are typical of high-energy, shallow water habitats and of
    low-light, deep water habitats. Between these two extremes, wave energy and
    light set upper limits on morphological variation and are not good predictors
    of mean morphological parameters.

          Three additional citations to those given by Brakel (1983) on the general
    relationship between colony morphology and depth are Fricke and Schuhmacher
    (1983), Chappell (1980), and Stearn (1982). The first is an interesting paper
    on photoadaptations in deep hermatypic corals found down to 145 m. They noted
    the prevalence of flat hermatypes in deep water and a great diversity of growth
    forms in shallow water. This pattern was not observed for ahermatypic corals.
    Chappell (1980) discussed the effects of light and wave stress on coral growth
    form and rate and extended these effects to include the growth of coral reefs.
    Stearn (1982) critically reviewed the analysis of growth form in corals and
    stromatoporoids. He, like Brakel, concluded that the relationship between
    growth form and environmental variables is quite complex due to the influences
    of genetic and developmental processes.

          The presentation by Hughes (1983) dealt with coral growth rates as well
    as life history variation over a depth range. The major point of this presentation

                                            17

    was that net coral growth rates do not vary much with depth.  Although
    calcification rates decrease with increasing depth, rates of injury to colonies _
    are much higher in shallow water. This results in several examples of deep
    corals at 35 or 55 m growing faster than corals of the same species at 10 or
    20 m. These data suggest that we should exercise caution when using calcifica-
    tion rates to evaluate coral reef growth.

          In our third presentation, Suchanek discussed the relative abundances and
    interaction frequencies of corals and demosponges over a 40 m depth range
    (Suchanek, et al., 1983). He emphasized the high frequency of demosponge-coral
    interactions at-40 m and the increasing prevalence of demosponges as aggressive
    spatial competitors with increasing depth. Aggressive interactions in shallow
    water involved encrusting gorgonians, hydrocorals, and zoanthids.

          The effect of spatial competition on coral or demosponge growth, depth
    distribution, and life history variation remains to be determined. Even though
    deep hermatypic corals experience relatively low injury rates, a significant
    amount of this injury is caused by sponge overgrowth (Hughes, 1983; Suchanek,
    et al., 1983; Hughes and Jackson, in review). Lang (1974) has previously noted
    FiFe prevalence of demosponges in deep fore-reef (below 55 m) and island slope
    zones off Discovery Bay, Jamaica. Hermatypic corals growing under light-limited
    conditions near their lower distributional limit may be more susceptible to
    overgrowth by demosponges than corals growing at shallower depths.

          Wahle presented his data on the relationship between injury, colony size,
    and life history variation in the gorgonian Plexaura homomalla (Wahle, 1983). *
    Between-colony analysis of variation in fecundity indicated that only colonies
    taller than 20 cm contained eggs. Natural and experimentally induced injuries
    to large female colonies resulted in physiologically isolated colony branches
    which exhibited size-related variation in fecundity. This work demonstrates
    that: 1) "colony size and not age controls both onset and continuation of
    gametogenesis"; 2) "injury can subtly reduce fecundity without noticeably
    affecting (colony) size"; and 3) injuries can alter the level of colony integrity
    and "create mosaics of different life history stages coexisting within the same
    colony."

          My own presentation dealt with an analysis of divergent life history
    patterns in Zoanthus sociatus and Z. solanderi.  Since these data do not appear
    elsewhere, I present them here in more detail than that given to the other five
    presentations. Both of these zoanthids are very common at several locations
    throughout the Caribbean Sea.  These sessile colonial organisms generally
    inhabit shallow subtidal and lower intertidal zones where they occasionally are
    exposed to extreme wave action (e.g., Hurricane Allen, see Woodley, et al.,
     1981) or to desiccation (Sebens, 1982a; Fadallah, et al., 1984). Boi-i species
    may successfully escape from such extremes by dispersing gametes and/or fragmented
     clusters of adult polyps.

           Highsmith (1982) has suggested that fragmentation is an important part of
     the life history of many corals, and that one characteristic typical of
     fragmenting species is delayed sexual reproduction.  The data in table 1 were
     collected from 101 zoanthid colonies to determine if either Z. sociatus, Z.
     solanderi, or both species delay sexual reproduction.  Both species have been    _

        Table 1.--The frequency of fertile polyps in four colony size classes of
           Z. sociatus and Z. solanderi. Colonies were collected in June, 1983,
           at Discovery Bay, Jamaica. Numbers of colonies are given in parentheses.

    Colony
    size                        Polyp
    class                    condition       Z. sociatus      Z. solanderi          2
                                                    _       _                  ~~~~~~x2

    A.  < 20 polyps          fertile              0                  8            9.44
                            nonfertile        227 (N=31)         188 (N=40)    p < 0.005

    B.  20 < 40 polyps       fertile              0                 22            22.12
                            nonfertile        103 (N=4)           92 (N=4)      p < 0.001

    C.  40 < 60 polyps        fertile             0                  9            11.63
                            nonfertile         58 (N=1)           40 (N=1)      p < 0.001

    D.  very large           fertile            105                179            26.93
        (subsamples          nonfertile        395 (N=10)         321 (N=10)    p < 0.001
        = 50 polyps
        per colony)

    E.  < 60 polyps          fertile              0 (N=36)          39 (N=45)    21.36
        very large           fertile           105 (N=10)          179 (N=10)    p < 0.001

    observed to fragment either as clusters of loose polyps, analogous to the "polyp
    balls" reported by Rosen and Taylor (1969), or as polyps attached to shifting
    rubble. The fact that fragmentation occurs, however, does not demonstrate that
    it is adaptive or an important life history characteristic.

          The frequency of fertile polyps in ten extremely large colonies of Z.
    sociatus and Z. solanderi was 21% and 36%, respectively (table 10). These-were
    sampled during their peak reproductive season, as indicated by Karlson (1981,
    and unpub. data). None of the polyps in 36 small colonies (< 60 polyps) of Z.
    sociatus were fertile; 11% of the polyps in 45 small colonies of Z. solanderi
    were fertile (table 1E). All three small colony size classes exhi ited
    significantly higher frequencies of fertile polyps for Z. solanderi than for Z.
    sociatus (table 1A, B, and C). The absence of fertile polyps in small Z.
    sociatus colonies suggests that this species delays sexual reproduction while
    Z. solanderi does not.

          Further examination of the 81 small zoanthid colonies (< 60 polyps)
    revealed another significant difference between these two species. Colonial
    growth in zoanthids commonly occurs by the budding of new individuals from
    stolons. These stolonal connections can degenerate over time (West, 1979),
    resulting in very loosely organized colonies with extremely low levels of
    integration and asynchronous sexual reproduction (e.g., table 1D).  As a measure

                                             19

                  Table 2.--Group size as a measure of colonial integrity

    Colony
    size                            Group size
    class             Z. sociatus                  Z. solanderi                  t-test

    < 20       X = 3.6 polyps per group           2.3 polyps per group
    polyps     Range = 1 - 13                      1 - 8                          3.68
               n = 63 groups in 31 colonies       84 groups in 40 colonies       p < 0.001

    20 < 40    X = 6.9                             2.3
    polyps     Range = 1 - 27                      1 - 5                           4.40
               n = 15 in 4 colonies               49 in 4 colonies                p < 0.001

    40 < 60    X = 5.3                             2.7
    polyps     Range = 1 - 30                      1 - 5                           1.25
               n = 11 in 1 colony                 18 in 1 colony                  N.S.

      of colonial integrity, I have counted the number of unconnected polyp groups
      and the number of polyps within each group. There were a total of 89 polyp
      groups within 36 colonies of Z. sociatus and 151 polyp groups within 45 colonies
      of Z. solanderi (table 2). Z3anthus solanderi had significantly fewer polyps
      pergroup than did Z. sociatus in the two smallest colony size classes.  The
      maximum number of polyps per group was also much higher in Z. sociatus than Z.
      solanderi.

            These significant differences in polyps per group may have important life
      history implications. Variation at this low level of colonial integrity is
      likely to influence the size of colony fragments and the size frequency
      distribution of zoanthid colonies. Among colonial species, survivorship,
      fecundity, fragmentation, and fusion are highly dependent on colony size (e.g.,
      Hughes and Jackson, 1980, and ms. in review; Buss, 1980, 1981; Sebens, 1982b;
      Hughes, 1984). Small fragments of Z. sociatus colonies have higher mortality
      rates than do fragments of the same size for L. solanderi (Sebens, 1982a;
      Karlson, in preparation). In addition, small colonies of Z. sociatus are
      nonreproductive (table 1).  The high level of colonial integrity in Z. sociatus
      suggests a benefit to large group (and colony) size in this species and,
      conversely, a cost (e.g., lower survivorship) associated with small size.
      There appears to be little cost to small size in Z. solanderi.  This zoanthid
      is more resistant to predation than Z. sociatus (�e-bens, 1982a) and does not
      delay sexual reproduction.  Low colonial integrity in Z. solanderi is likely to
      enhance fragmentation of small clusters of polyps.  Higher colonial integrity
      in Z. sociatus may enhance production of larger clusters by fragmentation or,
      alternatively, it may enhance resistance to fragmentation.

             In our last presentation, Mladenov briefly reviewed some of the life
       history characteristics of seven shallow-water Jamaican ophiuroids.  All of the

                                             20

    species studied were small cryptic forms.  Three species were fissiparous (see
    also Mladenov, et al., 1983) and produced relatively small eggs; two of these
    broadcast "exceedingly small numbers of larvae." Two non-fissiparous species
    produce and brood a small number of relatively large eggs which undergo direct
    devel opment.

          Mladenov noted that of approximately 2,000 extant ophiuroid species, only
    57 are known brooders (Hendler, 1979) and 37 undergo fission (Emson and Wilkie,
    1980; Emson, et al., 1985). While 65% of those exhibiting fissiparity and
    12% of the brooders are found in the tropics, brooders like Amphipholis squamata
    and fissiparous species like Ophiactis savignyl are among the most widespread
    and abundant" tropical ophiuroids. At Discovery Bay, the three fissiparous
    ophiuroid species were numerically dominant. Emson, et al. (1985) speculate
    that populations of these species have been "maintain~e  almost solely by asexual
    reproduction."

          Among colonial species, growth, fission, fusion, and fragmentation are
    important asexual life history processes (e.g., Bak and Engel, 1979; Hughes and
    Jackson, 1980; Karlson, 1980, 1983; Bothwell, 1981; Tunnicliffe, 1981; Lasker,
    1983; Rylaarsdam, 1983; Hughes, 1984).  More critical evaluation of the importance
    of sexual reproduction to these colonial species is currently underway.  There
    has been a relatively recent increase in this particular research area.  At the
    Third International Coral Reef Symposium held in 1977, there were no presentations
    on this topic.  Four years later at the Fourth International Coral Reef Symposium,
    there were six such presentations (Bothwell, unpub. data; Karlson, 1981; Kojis
    and Quinn, 1981; Richmond, 1981; Van Moorsel, 1981; Yamazato, et al., 1981).
    Data from the Van Moorsel presentation have now been published--Van Moorsel,
    1983). An excellent review of this subject dealing with over 100 scleractinian
    coral species has also just been published by Fadallah (1983); also see Harrison,
    et al. (1984). Fadalallah (1983) and Szmant-Froelich, et al. (1983) suggest the
    neTeior further work on reproductive cycles, reproductive modes, relative
    fecundity, and reproductive effort in order to satisfactorily evaluate the
    importance of sex to coral reef organisms. At this point we know virtually
    nothing about the relationship between reproductive effort and the actual input
    of settled larvae into adult populations; this point also is stressed by
    McFarland (1985).

          The original purpose of this discussion group was to compare growth and
    life history patterns of solitary and colonial organisms on shallow and deep
    reefs. We did, in part, deal with depth-related variation in coral growth
    form, growth rate, and life history patterns. Furthermore, we briefly discussed
    some general differences and similarities between colonial and solitary species
    (see Jackson, 1977). The remarkable success of fissiparous echinoderms and
    colonial corals, sponges, gorgonians, and zoanthids has been noted. This is
    suggestive of some level of evolutionary convergence favoring asexual strategies
    even in solitary organisms. My own work with zoanthids emphasized low colonial
    integrity in two very successful species. These species may be more similar to
    aggregating solitary organisms (e.g., barnacles, anemones, polychaetes, and
    mussels) than to more highly organized colonial forms. One curious and
    potentially significant difference between solitary and colonial organisms is
    the ability of colonial species to fuse (Teissier, 1929; Stephenson, 1931;
    Schijfsma, 1939; Ivker, 1972; Hughes and Jackson, 1980; Buss, 1982). It is

                                            21

    generally thought that fusion, whether it occurs between clonemates or non-
    clonemates, results in the formation of a larger colony with higher survivorship_
    and/or fecundity (Hughes and Jackson, in review). It also results in a level
    of physiological continuity which even aggregating solitary organisms cannot
    mimic. Variation in colonial integrity and the adaptive significance of
    fragmentation and fusion among colonial species would appear, then, to be an
    interesting new direction for future exploration.

                                    LITERATURE CITED

    Bak, R. P. M., and M. S. Engel. 1979. "Distribution, Abundance, and Survival
       of Juvenile Hermatypic Corals (Scleractinia) and the Importance of Life
       History Strategies in the Parent Coral Community." Mar. Biol. 54:341-352.

    Bothwell, A. M. 1981. "Fragmentation, a Means of Asexual Reproduction and
       Dispersal in the Coral Genus Acropora (Scleractinia: Astrocoeniida:
       Acroporidae) - A Preliminary Report." Proc. 4th Int. Coral Reef Symp.
       2:137-144.

    Brakel, W. H. 1983. "Depth-Related Changes in the Colony Form of the Reef
       Coral Porites astreoides," pp. 21-26. In: M. L. Reaka (ed.), The Ecology of
       Deep and Shallow Coral Reefs.  Symp. Ser. Undersea Res., Vol. 1i7.  NOAA
       Unhdersea Res. Progr., Rockville, Md.

    Buss, L. W.  1980.  "Competitive Intransitivity and Size-Frequency Distributions
       of Interacting Populations."  Proc. Nat. Acad. Sci. USA 77:5355-5359.

    Buss, L. W. 1981. "Group Living, Competition, and the Evolution of Cooperation
       in a Sessile Invertebrate." Science 213:1012-1014.

    Buss, L. W. 1982. "Somatic Cell Parasitism and the Evolution of Somatic Tissue
       Compatibility." Proc. Nat. Acad. Sci. USA 79:5337-5341.

    Chappell, J. 1980. "Coral Morphology, Diversity, and Reef Growth." Nature
       286:249-252.

    Emson, R. H., and I. C. Wilkie. 1980. "Fission and Autotomy in Echinoderms."
       Oceanogr. Mar. Biol. Ann. Rev. 18:155-250.

    Emson, R. H., P. V. Mladenov, and I. C. Wilkie. 1985. "Patterns of Reproduction
       in Small Jamaican Brittle Stars: Fission and Brooding Strategies Predominate,"
       pp. 87-100. In: M. L. Reaka (ed.), The Ecology of Coral Reefs, Symp. Ser.
       Undersea Res., Vol. 3(1).  NOAA Undersea Res. Progr., Rockville, Md.

    Fadlallah, Y. H. 1983. "Sexual Reproduction, Development and Larval Biology
       in Scleratinian Corals: A Review." Coral Reefs 2:129-150.

    Fadlallah, Y. H., R. H. Karlson, and K. P. Sebens. 1984. "A Comparative Study
       of Sexual Reproduction in Three Species of Panamanian Zoanthids
       (Coelenterata:Anthozoa)."  Bull. Mar. Sci. 35:80-89.                                0

                                            22

    *_     Fricke, H. W., and H. Schuhmacher.  1983.  "The Depth Limits of Red Sea Stony
             Corals:  An Ecophysiological Problem (a Deep Diving Survey by Submersible)."
             Mar. Ecol. 4:163-194.

          Harrison, P. L., R. C. Babcock, G. D. Bull, J. K. Oliver, C. C. Wallace, and B.
             L. Willis. 1984. "Mass Spawning in Tropical Reef Corals." Science
             223:1186-1189.

          Hendler, G.  1979.  "Reproductive Periodicity of Ophiuroids (Echinodermata:
             Ophiuroidea) on the Atlantic and Pacific Coasts of Panama," pp. 145-156.
             In:  S. E. Stancyk (ed.), Reproductive Ecology of Marine Invertebrates.  The
             Belle W. Baruch Library in Marine Science, Number 9.  Univ. S. Carolina
             Press, Columbia.

          Highsmith, R. C.  1982.  "Reproduction by Fragmentation in Corals."  Mar. Ecol.
             Prog. Ser. 7:207-226.

          Hughes, T. 1983. "Life Histories and Growth of Corals Over a Depth Gradient,"
             pp. 17-20. In: M. L. Reaka (ed.), The Ecology of Deep and Shallow Coral
             Reefs, Symp. Ser. Undersea Res., Vol. 1(1).  NOAA-Undersea Res. Prog.,
             Rockville, Md.

          Hughes, T. P. 1984. "Population Dynamics Based on Individual Size Rather Than
             Age: A General Model With a Reef Coral Example." Amer. Nat. 123:778-795.

          Hughes, T. P., and J. B. C. Jackson. 1980. "Do Corals Lie About Their Age?
             Some Demographic Consequences of Partial Mortality, Fission, and Fusion."
             Science 209:713-715.

          Hughes, T. P., and J. B. C. Jackson. In review. "Population Dynamics and Life
             Histories of Foliaceous Corals."  Submitted to Ecol. Monogr.

          Ivker, F. B. 1972. "A Hierarchy of Histo-Incompatibility in Hydractinia
             echinata." Biol. Bull. 143:162-174.

          Jackson, J. B. C. 1977. "Competition on Marine Hard Substrata: The Adaptive
             Significance of Solitary and Colonial Strategies." Amer. Nat. 111:743-767.

          Karlson, R. H. 1980. "Alternative Competitive Strategies in a Periodically
             Disturbed Habitat." Bull. Mar. Sci. 30:894-900.

          Karlson, R. H. 1981. "Reproductive Patterns in Zoanthus spp. from Discovery
             Bay, Jamaica." Proc. 4th Int. Coral Reef Symp. 2:699-704.

          Karlson, R. H.  1983.  "Disturbance and Monopolization of a Spatial Resource by
             Zoanthus sociatus (Coelenterata, Anthozoa)." Bull. Mar. Sci. 33:118-131.

          Kojis, B. L., and N. J. Quinn. 1981. "Reproductive Strategies in Four Species
             of Porites (Scleractinia)." Proc. 4th Int. Coral Reef. Symp. 2:145-152.

          Lang, J. C.  1974.  "Biological Zonation at the Base of a Reef."  Amer. Sci.
     *s ~62:272-281.

                                                  23

    Lasker, H. R.  1983.  "Vegetative Reproduction in the Octocoral Briereum
      asbestinum (Pallas)."  J. Exp. Mar. Biol. Ecol. 72:157-169.

    McFarland, W. N. 1985. "Overview: The Dynamics of Recruitment in Coral Reef
      Organisms," pp. 9-15. In: M. L. Reaka (ed.), The Ecology of Coral Reefs,
       Symp. Ser. Undersea Res., Vol. 3(1).  NOAA Undersea Res. Progr., Rockville,
      Md.

    Mladenov, P. V., R. H. Emson, L. V. Colpitts, and I. C. Wilkie. 1983. "Asexual
      Reproduction in the West Indian Brittle Star Ophiocomella ophiactoides (H.
      L. Clark) (Echinodermata: Ophiuroidea)."  J. Exp. Mar. Biol. Ecol. 72:1-23.

    Richmond, R. 1981. "Energetic Considerations in the Dispersal of Pocillopora
       damicornis (Linnaeus) planulae.  Proc. 4th Int. Coral Reef S 2mp._21T53-156,

    Rosen, B. R., and J. D. Taylor. 1969. "Reef Coral From Aldabra: New Mode of
       Reproduction." Science 166:119-121.

    Rylaarsdam, K. W. 1983. "Life Histories and Abundance of Colonial Corals on
       Jamaican Reefs." Mar. Ecol. Prog. Ser. 13:249-260.

    Schijfsma, K. 1939. "Preliminary Notes on Early Stages in the Growth of
       Colonies of Hydractinia echinata (Flem.)." Arch. Neerland. Zool. 4:93-102.

    Sebens, K. P. 1982a. "Distribution and Spatial Patterns of Zoanthids in the
       Coral Reef Flat Community at Galeta, Panama: The Effects of Desiccation and
       Predation."  Bull. Mar. Sci. 32:316-335.

    Sebens, K. P. 1982b. "Competition for Space: Growth Rate, Reproductive
       Output, and Escape in Size." Amer. Nat. 120:189-197.

    Steam, C. W. 1982. The Shapes of Paleozoic and Modern Reef-Builders: A
       Critical Review." Paleobiology 8:228-241.

    Stephenson, T. A. 1931. "Development and Formation of Colonies of Pocillopora
       and Porites."  Great Barrier Reef Expeditions, Sci. Rpts. 3:113-134.

    Suchanek, T. H., R. C. Carpenter, J. D. Witman, and C. 0. Harvell. 1983.
       "Sponges as Important Space Competitors in Deep Caribbean Coral Reef
       Communities," pp. 55-60.  In:  M. L. Reaka (ed.), The Ecology of Deep and
       Shallow Coral Reefs, Symp.Ter. Undersea Res., Vol. 1(1).  NOAUndersea
       Res. Progr., Rockville, Md.

    Szmant-Froelich, A., L. Riggs, and M. Reutter.  1983.  "Sexual Reproduction in
       Caribbean Reef Corals." Amer. Zool. 23:961, abstract no. 513.

    Teissier, G. 1929.  "L'Origine Multiple de Certaines Colonies d'Hydractinia
       echinata (Fleming) et ses Consequences Possibles."  Bull. Soc. Zool. France
       54:645-647.

    Tunnicliffe, V. J. 1981. "Breakage and Propagation of the Stony Coral Acropora
       cervicornis."  Proc. Nat. Acad. Sci. USA 78:2427-2431.

                                            24

    Van Moorsel, G. W. N. M. 1981. "Different Reproductive Strategies in Two
      Closely Related Stony Corals (Agaricia, Scleractinia)." Proc. 4th Int.
       Coral Reef Symp. 2:193 (abstract).

    Van Moorsel, G. W. N. M. 1983. "Reproductive Strategies in Two Closely Related
       Stony Corals (Agaricia, Scleractinia)." Mar. Ecol. Prog. Ser. 13:273-283.

    Wahle, C. M. 1983. "The Roles of Age, Size, and Injury in Sexual Reproduction
       Among Jamaican Gorgonians." Amer. Zool. 23:961, abstract no. 514.

    West, D. A. 1979. "Symbiotic Zoanthids (Anthozoa: Cnidaria) of Puerto Rico."
       Bull. Mar. Sci. 29:253-271.

    Woodley, J. D., E. A. Chornesky, P. A. Clifford, J. B. C. Jackson, L. S. Kaufman,
       N. Knowlton, J. C. Lang, M. P. Pearson, J. W. Porter, M. C. Rooney, K. W.
       Rylaarsdam, V. J. Tunnicliffe, C. M. Wahle, J. L. Wulff, A. S. G. Curtis,
       M. D. Dallmeyer, B. P. Jupp, M. A. R. Koehl, J. Neigel, and E. M. Sides.
       1981. "Hurricane Allen's Impact on Jamaican Coral Reefs." Science
       214:749-755.

    Yamazato, K. M. Sato, and H. Yamashiro.  1981.  "Reproductive Biology of an
       Alcyonacean Coral, Lobophytum crassum Marenzeller." Proc. 4th Int. Coral
       Reef Symp. 2:671-678.

                                            25

                 OVERVIEW: CORAL REEF COMMUNITY STRUCTURE AND FUNCTION

                                     Mark A. Hixon
                               Department of Zoology and
                                College of Oceanography
                                Oregon State University
                                Corvallis, Oregon 97331

          This paper summarizes an open discussion session which took place during
    the "Coral Reef Ecology Workshop" held at the annual meeting of~the American
    Society of Zoologists in Philadelphia on December 27, 1983. Due to either
    sampling error or a genuine bias in current research emphasis, most of the
    participants in this session studied herbivory and grazing patterns on reefs.
    Consequently, most of the discussion centered around two related topics: (1)
    the recently discovered mass mortality of urchins in the Caribbean and (2) the
    relative importance of urchins vs. fishes in structuring benthic reef communities
    in areas facing different fishing pressures. A third more general topic was
    discussed briefly toward the end of the session: approaches to research on the
    community structure of reef systems.  I will cover each of these topies in
    turn, extending discussion on the final topic with an overview of future needs
    in the study of coral reef communities.

                          MASS MORTALITY OF CARIBBEAN URCHINS
          One of the major herbivores on Caribbean reefs is the long-spined urchin
    Diadema antillarum. In November 1983, a letter published in Science reported
    unprecedented mass mortalities of this species that were sweeping the Caribbean
    (Lessios, et al., 1983). Haris Lessios (Smithsonian Tropical Research Institute)
    attended the session and provided both a description of the effects of the
    apparent pathogen (the origin or nature of which was currently unknown) and
    an updated account of the spread of the calamity.

          The apparent disease runs a 4- to 5-day course, beginning with the urchins
    emerging from coral cover and climbing up any available substrate. The urchins
    then discolor, gradually lose their attachment capabilities, and ultimately
    lose their spines and die. Up to 98% mortality has been reported in some
    populations, with apparently resistant individuals remaining. Curiously, no
    other species of urchin has been affected.

          The outbreak was first noted near the Caribbean entrance of the Panama
    Canal in January 1983. Urchin mortalities were observed subsequently in
    Colombia, Costa Rica, and Grand Cayman by June; in Jamaica, Belize, Cancun
    (Mexico), and Key Largo (Florida) by July; in the Bahamas by August; in the Dry
    Tortugas and Bermuda by September; in Grand Turk and Haiti by October; and
    throughout the Greater and Lesser Antilles, including Curacao, Bonnaire, and
    part of the coast of Venezuela, between November 1983 and January 1984.

          Initially, the spread of the die-off appeared to follow prevailing ocean
    currents.  However, certain exceptions, such as the outbreak in Barbados in
    October (a full month or two before the remainder of the Antilles), suggested a

                                           27

    more complex situation. At present, Lessios reports that the entire Caribbean
    except for much of Venezuela, Tobago, and the area between Guadaloupe and the
    British Virgin Islands, has been affected, although these areas could be affected
    by the time this report is published.

          Mark Hay (University of North Carolina at Chapel Hill) noted that, despite
    the die-off of Diadema in the Florida Keys, algal abundance on reefs there was
    not unusually high 2 months after the die-off. He suggested that either herbivorou
    fishes were sufficiently abundant to check algal growth or 2 months may not
    have been enough time to detect a noticeable change.

          Douglas Morrison (University of Georgia) summarized his quantitative data
    on the effects of the die-off on a Jamaican reef.  Mean densities of urchins I
    year before the die-off were about 15 per m2 at 5 m depth and about 2 per m2 at
    16 m. Several months after the die-off, mean densities had declined to about 1
    per m2 at 5 m depth, and no urchins were apparent at 16 m.  After the urchin die-
    off at the shallow site, the coverage of crustose coralline algae (an indicator
    of high grazing intensity) declined from 45% to about 18%.  Replacing the coral-
    lines, coverage by fleshy macroalgae quadrupled (from 7% to about 28%) and coverage
    by filamentous algae nearly tripled. These patterns were corroborated by earlier
    urchin-removal experiments conducted before the die-off; in the experimental
    absence of grazing, crustose corallines were replaced by upright macroalgae.
    In contrast, the die-off had little apparent effect upon algal growth at the
    deep site, where urchin densities were normally low, and macroalgal abundance
    remained relatively high (73% cover). The macroalgae that increased in abundance
    at the shallow site are known to be resistant to fish grazing but not to urchi
    grazing. These included members of the genera Lobophora, Caulerpa, and DictyoW

          Whatever its cause, the mass mortality of Diadema throughout the Caribbean
    provides an excellent (although uncontrolled) "naturaFexperiment" for determining
    the impact of urchins on entire reef systems. Where adequate baseline data are
    available, observations following the die-off will test the widespread applicabilit
    of previous experimental analyses of small patch-reef systems (e.g., Ogden, et al.,
    1973) and help to resolve the controversy discussed in the next section.

                    ARE URCHINS IMPORTANT GRAZERS ON UNFISHED REEFS?

          Hay summarized a study that was in press at the time of the workshop
    (Hay, 1984). He noted that most of the studies of the impact of urchin grazing
    on reef benthos have occurred at two sites: Teague Bay, St. Croix (e.g., Ogden,
    et al., 1973) and Discovery Bay, Jamaica (e.g., Sammarco, 1980). Such studies
    ~ve--Ted some to believe that urchins are the most important grazers on "typical"
    coral reefs. However, Hay suggested that these particular sites are atypical
    in that they have been heavily fished, indirectly resulting in unusually high
    densities of urchins which have been freed from predation by (and perhaps
    competition with) fishes. Using pieces of the seagrass Thalassia testudinum as
    a field bioassay for the intensity of herbivory on macrophytes, he found that
    eight lightly fished sites scattered throughout the Caribbean (including Salt
    River on St. Croix) showed decreasing grazing intensity with increasing depth
    and that almost all herbivory was due to fishes. Moreover, urchin abundances
    were low at these sites.  In contrast, Haiti and Teague Bay on St. Croix, bothF

                                            28

            heavily fished areas, showed the traditional opposite patterns. Hixon added
            that Hay's general observation that urchins are Often rare where large urchin-
            eating fishes are abundant is evident on Hawaiian reefs. Where fishing is
            prohibited on marine reserves, such as Hanauma Bay and Coconut Island on Oahu,
            urchins appear to be relatively rare.

                  Hay stressed that his major point was that many patterns documented on
            human-impacted reefs may be recent, having prevailed only for the past few hundred
            years. Because herbivory by fishes may select for different evolutionary responses
            in algae than herbivory by urchins, attempts to extract evolutionary implications
            from ecological data gathered on heavily fished reefs is not justified.

                  Les Kaufman (New England Aquarium) objected to a number of Hay's assertions,
            particularly the idea that urchins on heavily fished reefs necessarily are
            freed from predation by fishes. He took issue with Hay's data which indicated,
            on one hand, a decrease in grazing intensity with increased depth at Salt River
            on St. Croix but, on the other hand, an increase in grazing intensity with
            increased depth at nearby Teague Bay on the same island. Based on his diving
            experience at these sites, Kaufman felt that both areas supported fishes capable
            of eating urchins. Thus, other factors besides the overall abundance of fishes
            may explain the patterns that Hay attributed to fishing pressure. Further,
            Kaufman felt that Hay failed to consider the importance of juvenile mortality
            in urchin populations. He suggested that predation by wrasses on juvenile
            urchins may be considerable on heavily fished reefs, such as Teague Bay (St.
            Croix) and Discovery Bay (Jamaica), so that fishing pressure on larger fish
    *       ~~species may not ultimately affect urchin densities.

                  Substantial discussion centered on the adequacy of Thalassia as a bioassay
            of grazing intensity. Robert Carpenter (University of Georgia) suggested that
            different measures of grazing could produce different depth profiles of grazing
            intensity (see also Steneck, 1983). Carpenter felt that the Thalassia technique
            measured mostly parrotfish grazing and that a more general measure of grazing
            is provided by counting the number of herbivore bites per unit reef area. Hixon
            agreed, noting that bite marks by fishes from different families (e.g., parrotfishes
            vs. surgeonfishes) can be individually identified and counted on flat substrates
            (e.g., Hixon and Brostoff, 1983). Morrison also concurred and suggested that,
            instead of Thalassia, a food readily consumed by all herbivores should be used
            to measure overall grazing intensity. Based on his own and other's work,
            Morrison indicated that filamentous algae seem to be preferred by urchins and
            nearly all herbivorous fishes (especially parrotfishes and damselfishes).

                  Sara Lewis (Duke University) noted that some algal species (e.g., Lobophora
            variegata) are differentially susceptible to grazing on different reefs. She
            suggested that these within-species differences may represent geographical
            variation in the development of plant defensive compounds. Hay agreed, noting
            that herbivory on a local level possibly could induce the production of chemical
            defenses. He went on to stress the problem of interpreting data from herbivore
            food-preference observations. Data on food preferences provide information on
            the responses of herbivores to different plants, but not necessarily on the
            selective pressure that herbivores impose upon the plants. Clearly, more
            information will be required to elucidate the reciprocal interactions between
            reef herbivores and algae.

                                                    29

                      STUDYING COMMUNITY STRUCTURE IN REEF SYSTEMS

          Eldredge Bermingham (University of Georgia) introduced this general topic
    toward the end of the session by suggesting what he believed to be a major
    problem with coral reef community ecology. He felt that reef ecologists were
    often academic descendants of bird ecologists, but failed to follow their
    ornithological forefathers' passion for detailed natural history data. He
    stressed that lack of solid baseline data on coral reefs inhibits our ability
    to understand these systems.

          Both John Ebersole (University of Massachusetts at Boston) and Hixon
    agreed in turn that detailed observational data are essential for any convincing
    ecological study. In particular, long-term baseline data illustrating the
    constancy or variability of observed patterns are needed. However, Hixon
    questioned whether most (or even many) reef ecologists were academic descendants
    of bird ecologists and, more importantly, noted that reef ecologists have
    conducted far more rigorous experimental studies than most bird ecologists.
    This disparity is understandable. On one hand, many terrestrial systems
    (especially many avian communities) are amenable to long-term observation but
    not to experimental manipulation. On the other hand, most coral reefs are both
    geographically distant from most research institutions and difficult to observe
    for long periods due to diving constraints. However, some reef systems are
    small enough or the associated organisms sedentary enough to allow direct
    experimentation, as evidenced by the papers in this symposium. Moreover,
    artificial reefs constructed from either natural or manmade materials allow
    researchers to rigidly control the age and structure of reef habitats, allowing
    powerful experimental designs (e.g., Shulman, et al., 1983; Fitz,,et al., 1983;1W
    Wolf, et al., 1983).

                                SYNTHESIS AND PROSPECTUS

          It seem~s appropriate to close this paper with an overview of our future
    needs in the'study of coral reef communities. It is clear that, despite the
    knowledge that has accrued since the first professional ecologists donned SCUBA
    gear in the 1950's, we have only begun to scratch the surface of the complexities
    of coral reef systems. The number of research possibilities is infinite; the
    field is wide open. Thus, rather than suggesting what we need to study in
    particular, I would like to review the ideas suggested during this workshop on
    how we might improve future studies.

          Based an criticisms leveled at current studies and pleas for future changes
    aired at various times during this workshop, three basic needs are evident.
    First, the complexities of coral-reef community structure cannot be elucidated
    without more extensive use of properly controlled field experiments. This
    suggestion is not new (e.g., Connell, 1974), and many reef ecologists have
    embraced experimentation enthusiastically. However, any experiment, no matter
    how elegantly designed and executed, cannot stand alone.  As discussed above,
    detailed observational knowledge of a system is essential before field experiments
    can be properly interpreted.

          This brings us to a second need:  long-tern field studies.  Because
    (1) most coral reefs are located far from universities and other research

                                            30

    institutions, (2) most researchers cannot spend large blocks of time away from
    home, and (3) travel costs are becoming prohibitive, few current studies have
    followed long-term variations in reef systems. Moreover, current policy dictates
    that most research grants are limited to durations of several years at most.
    The net result is that most ecological studies are relatively static "snapshots"
    of intrinsically dynamic systems. Thus, our ability to understand the long -
    range consequences of various ecological interactions, and especially major
    environmental events (such as the urchin die-off discussed above), becomes
    severely limited. Likens (1983) recently has characterized the establishment
    and funding of long-term ecological studies in general to be a major priority
    for the future. Perhaps reef systems will one day be included in the National
    Science Foundation's Long-Term Ecological Research Program. In any event, the
    establishment and funding of facilities for detailed studies in prescribed local
    areas (such as NOAA's HYDROLAB in Salt River Canyon, St. Croix) or in local
    regions (such as NOAA's MAKALI'I submersible program in Hawaii and Johnston
    Island, the JOHNSON SEA-LINK submersible program in Florida and the Bahamas,
    and the submersible now available at the Discovery Bay Marine Laboratory,
    Jamaica) represent important first steps toward obtaining long-term data on
    deep reef systems.

          The third need is for future studies to include several study areas in
    order to determine the ubiquity of observed patterns. Most present studies
    occur at single sites, making widespread generalizations about coral reefs
    based on a single study tenuous at best (although this fact rarely stops us).
    This problem can be rectified by a single project being conducted at a number
    of locations, either sequentially by a single research team or simultaneously
    by several teams using standardized methods. Present controversies, such as
    the importance of urchins as grazers discussed above, could be resolved by such
    an approach. NOAAs proposal to establish a saturation facility which can be
    moved among different geographical locations for comparative surveys of reef
    biota and processes should facilitate standardized studies.

          Unfortunately, enacting these last two proposals may require changes in
    the current policies of granting agencies. The present system seems geared
    toward a fast-turnover "results-now" policy. While programs such as HYDROLAB
    provide the potential for long-tern studies of reef systems, few such facilities
    exist presently, precluding detailed comparative studies among a number of
    study sites. In any case, should the majority of reef ecologists concur that
    these needs are important, long-term observational and experimental studies
    over wide areas will be realized eventually.

                                    ACKNOWLEDGMENTS

          Many thanks to the 'U.C. Irvine Committee on Faculty Travel (especially
    Peter Dixon) for funding my participation in the workshop; to the discussion
    participants for providing' written summaries of their contributions (my sincere
    apologies for any misquotes); to Marjorie Reaka and John Ebersole for constructive
    comments on my manuscripts; and, especially, to Marjorie Reaka for bringing us
    all together.

                                           31

                                   LITERATURE CITED

    Connell, J. H. 1974. Field Experiments in Marine Ecology," pp. 21-54. In:
       R. N. Mariscal (ed.), Experimental Marine Biology.  Academic Press, N.Y.

    Fitz, H. C., M. L. Reaka, E. B. Bermingham, and N. G. Wolf. 1983. "Coral
       Recruitment at Moderate Depths: the Influence of Grazing," pp. 89-96. In:
       M. L. Reaka (ed.), The Ecology of Deep and Shallow Coral Reefs, Symp. SeTr.
       Undersea Res., Vol. 1T1). NOAA Undersea Res. Progr., Rockville, Md.

    Hay, M. E. 1984. "Patterns of Fish and Urchin Grazing on Caribbean Coral
       Reefs: Are Previous Results Typical?" Ecology 65:446-454.

    Hixon, M. A., and W. N. Brostoff. 1983. "Damselfish as Keystone Species in
       Reverse:  Intermediate Disturbance and Diversity of Reef Algae."  Science
       220:511-513.

    Lessios, H. A., P. W. Glynn, and D. R. Robertson. 1983. "Mass Mortalities of
       Coral Reef Organisms." Science 222:215.

    Likens, G. E. 1983. "A Priority for Ecological Research." Bull. Ecol. Soc.
       Amer. 64:234-243.

    Ogden, J. C., R. A. Brown, and N. Salesky. 1973. "Grazing by the Echinoid
       Diadema antillarum Philippi: Formation of Halos Around West Indian Patch
       Reefs."  Science 182:715-717.

    Sammarco, P. W. 1980. "Diadema and Its Relationship to Coral Spat Mortality:
       Grazing, Competition, and Biological Disturbance." J. Exp. Mar. Biol. Ecol.
       45:245-272.

    Shulman, M. J., J. C. Ogden, J. P. Ebersole, W. N. McFarland, S. L. Miller, and
       N. G. Wolf.  1983.  "Priority Effects in the Recruitment of Juvenile Coral
       Reef Fish."  Ecology 64:1508-1513.

    Steneck, R. S.  1983.  "Quantifying Herbivory on Coral Reefs:  Just Scratching
       the Surface and Biting Off More Than We Can Chew," pp. 103-112. In: M. L.
       Reaka (ed.), The Ecology of Deep and Shallow Coral Reefs, Symp. Ser. Undersea
       Res., Vol. 1( 1.  NOAA Undersea Res. Progr., Rockville, Md.

    Wolf, N. G., E. B. Bermingham, and M. L. Reaka.  1983.  "Relationships Between
       Fishes and Mobile Benthic Invertebrates on Coral Reefs." pp. 69-78. In:
       M. L. Reaka (ed.), The Ecologqy of Deep and Shallow Coral Reefs, Symp. Ser.
       Undersea Res., Vol.-T1l).  NOAAndersea-es. Progr., Tockville, Md.

    Note added in proof: A recent update on the mass mortality of urchins can be
    found in:

    Lessios, H. A., D. R. Robertson, and J. D. Cubit.  1984.  "Spread of Diadema
       Mass Mortality Through the Caribbean."  Science 226:335-337.

                                            32

                     SOME THOUGHTS ON THE PAST, PRESENT, AND FUTURE OF STUDIES
                                 ON CORAL REEF COMMUNITY METABOLISM

                                            S. V. Smith
                                 Hawaii Institute of Marine Biology
                                       Kaneohe, Hawaii 96744

                Marjorie Reaka, as editor of these two volumes on The Ecology of Deep
          and Shallow Coral Reefs, has kindly offered me the opportunit  tocment on
          where I see studies orreef community metabolism to be coming from--and going
          to. The following thoughts arise as I consider, in particular, the seven
          papers loosely grouped in "The Organization of Reef Ecosystems" in these
          proceedi ngs.

                These papers have some aspect of the metabolic performance of coral reef
          communities or systems as a broad common theme. Within the context of that
          theme, all of the papers can trace their ancestry back to the "foundation
          studies" by Sargent and Austin (1949) at Rongelap Atoll and Odum and Odum (1955)
          at Enewetak Atoll. Earlier papers in the field of reef community metabolism
          can, of course, be identified. They have tended to remain lost in obscurity
          compared to the two I have cited. Over the intervening years, the field has
          matured and expanded sufficiently that citation of these important papers is
          beginning to drop off. Instead, I recognize increasing proportions of second
          (or third) generation citations, both in the papers on reef metabolism in these
    *     ~volumes and in the general literature.

                These early papers dealt primarily with oxygen and carbon flux of reef-
          flat communities. Several of the papers in the present volumes and a survey
          of the literature suggest that we can move beyond a direct concern with average
          rates of oxygen and carbon fluxes in studies of reef metabolism. We now can
          speak with some confidence about the typical oxygen and carbon metabolic
          performance of reef-flat communities. It is, however, worth noting that we
          remain without a comparable large data base for other parts of coral-reef
          ecosystems.

                We are beginning to gain an appreciation for the relationships between
          variation in reef metabolism and the controlling roles of external physical,
          chemical, and biological variables. Many casual observations about reef
          metabolic response to external controls have led to erroneous or trivial
          conclusions. Clearly, controlled experiments and carefully designed field
           surveys need to be conducted in order to test hypotheses about metabolic
           responses to controlling variables.

                 The study of nutrient fluxes in relation to community metabolism has,
           perhaps, been more extensive than other aspects of controls on community
           metabolism. This work became prominent during the Symbios Expedition to Enewetak
           Atoll (Johannes, et al., 1972). Studies of nutrient flux continue, and most of
           the papers on ree~f m tbolism in these volumes at least touch on this subject.
           in particular, there is an interest in the effects of both quantity and quality
    *     ~of nutrient supply on reef metabolism and in the interactive roles of various
           communities (especially macrofauna/meiofauna/microfauna in interreef soft-

                                                   33

    sediment communities) in nutrient processing of the total system. From my own 1
    bias, I perceive the need to "balance the books" of nutrient fluxes in entireW
    reef systems as a recurrent--and important--theme.

          Solar radiation is clearly fundamental to the community metabolism of
    reefs, yet our understanding of metabolic responses to light remains poor.
    Traditionally, most studies of coral reef metabolism have not adequately
    considered either the quantity or the quality of incident solar radiation,
    light attenuation through the water column, or loss of radiant energy through
    back-scattering. This situation is beginning to change. We see among the
    papers in these volumes several attempts to evaluate the metabolic response of
    reefs to light. More work is needed.

          Finally, I observe that students of coral reefs tend to emphasize the
    unique characteristics which make reefs such pleasurable places to work. I
    suggest that we have a great deal more to learn, as ecologists, by considering
    coral reefs within the spectrum of other ecosystems than we will ever learn by
    treating reefs as unique.

                                    LITERATURE CITED

    Johannes, R. E., and the Project Symbios Team. 1972. "The Metabolism of Some
       Coral Reef Communities: A Team Study of Nutrient and Energy Flux at Eniwetok."
       BioScience 22:541-543.

    Odum, H. T., and E. P. Odum. 1955. "Trophic Structure and Productivity of a
       Windward Coral Reef Community on Eniwetok Atoll." Ecol. Monogr. 25:291-320.

    Sargent, M. C., and T. S. Austin. 1949. "Organic Productivity of an Atoll."
       Trans. A~mer. Geophys. Union 30:245-249.

                                           34

                          CHAPTER III. CONTRIBUTED PAPERS

                                       Figure 1

         Further studies of deep coral reefs and sea mounts have been possible
    through the use of submersibles such as NOAA's MAKALI'I, which is shown while
    in transit on its launch, retrieval, and transport (LRT) vehicle (fig. 1).
    During launch, the LRT is submerged with the submersible; at 50 feet the
    submersible is released to continue its descent for research (fig. 2).

                                       Figure 2

                                        35

          Figure 3

                                                            Figure 4

         NOAA also supports research on the biology of deep water communities in
    various localities through the deep diving bell facilities operated off the
    R/V SEAHAWK (figs. 3, 4) which is based at the University of North Carolina
    at Wilmington. An additional habitat is being constructed for use in research
    on marine communities off the southern California coast (fig. 5).

                                       Figure 5

                                       36

                RECRUITMENT OF YOUNG CORAL REEF FISHES FROM THE PLANKTON

                                  William N. McFarland
                           Section of Ecology and Systematics
                                   Cornell University
                                Ithaca, New York 14853

                                     John C. Ogden
                                 West Indies Laboratory
                             Fairleigh Dickinson University
                                       Teague Bay
                         St. Croix, U.S. Virgin Islands 00820

                                        ABSTRACT

         This paper examines the widely held view that the planktonic eggs and/or
    larvae of most coral reef fishes represent mechanisms that reduce predation
    and/or serve for dispersal of the young. Data on spawning, the pelagic phase,
    and recruitment of coral reef fishes are examined. Recruitment represents the
    successful end product of a complex suite of adult and larval behaviors and
    physical conditions that directly affect survival of offspring. Although
    considerable data are available, in no single species has the cycle from spawning
    to recruitment been clearly documented. As a result, assessing the various
    hypotheses that attempt to explain the almost universal presence of a pelagic
    larval phase in coral reef fishes remains tenuous.

         Predation on young and ultimate dispersal are both potent selective factors.
    The high degree of variation in reproduction, larval characteristics, and
    recruitment amongst coral reef species implies, however, that these two selective
    factors undoubtedly vary in importance among species.

                                      INTRODUCTION

         Virtually all coral reef fishes produce numerous offspring and release
    either their eggs or larvae into the offshore plankton (Breder and Rosen, 1966;
    Ehrlich, 1975; Goldman and Talbot, 1976; Sale, 1977, 1978a; Johannes, 1978;
    Barlow, 1981). There is one known exception, the pomacen-trid Acanthochromis
    polyacanthus; members of this species brood their young and disperse them
    directly onto the reef (Robertson, 1973). Also, some apogonids (mouth brooders)
    and some brotulids (live bearers) have completely eliminated the planktonic
    larval phase.

         Considering the high diversity of reef fishes (Connell, 1978; Sale, 1980)
    and their numerous ecological roles (Hobson, 1974; Sale, 1978b; Smith, 1978),
    it is astonishing that so many species use the same reproductive strategy.
    Indeed, the central position of a larval pelagic existence in coral reef fishes
    led Helfman (1978) to wonder whether answers to the high species diversity of
    coral reef fish assemblages "lie in the plankton." One major hypothesis favors
    the view that community composition is dependent on the chance recruitment of
    each species from the plankton when space becomes available (Russell, et al.,

                                          37

    1974; Sale and Dybdahi , 1975, 1978; Sale, 1977, 1978a). Thus, species compositI
    on a reef should change through time, but over years as opposed to centuriesV
    or longer. A contrasting hypothesis suggests that species composition is more
    deterministic and dependent on competition between adults for resources (Smith,
    1973, 1978; Smith and Tyler, 1973). Recruitment from the plankton, therefore,
    would not primarily affect diversity but the abundance of each species over
    time. No doubt there is truth in each view, but the controversy continues with
    additional participants (Gladfelter and Gladfelter, 1978; Holles, 1978; Talbot,
    et al., 1978; Gladfelter, et al., 1980; Ogden and Ebersole, 1981; Shulman,
    l98TV-Abrams , 1984).

         Given the virtually universal use of a pelagic egg and/or larval phase and
    its potential significance to explanations of the high diversity amongst
    assemblages of coral reef fishes, investigations of the reproductive activities
    of adults, the disposition of their eggs and larvae at sea, and the effect(s)
    of currents on the dispersal of these propagules are, therefore, not inconsequen-
    tial. If, for example, the recruitment of each species is not consistent over
    a reasonable time scale, then the high diversity of coral reef fishes could not
    be maintained.

         In general, data about recruitment processes in coral reef fishes are
    sparse and must often be gleaned from literature that primarily deals with
    other aspects of coral reef fish biology. Over the last few years, however,
    efforts have been directed toward recruitment in particular species. Given the
    central importance of recruitment to coral reef fish community structure, we
    expect that larval biology at sea will be explored in great detail over the          __
    coming decade. Here we summarize what is presently known about recruitment andV
    closely related processes in coral reef fishes.

                                       REPRODUCT ION

         Spawning- activities in coral reef fishes vary considerably. Only over the
    last 10 years have sufficient direct observations accumulated to provide a
    basis for understanding how the spawning act might be adaptive. Many reef
    species spawn over long periods of each year, but they usually show maximum
    reproduction in either spring and/or fall (Munro, et al.,, 1973). In Munro's
    study, which examined the state of the gonad as annde~x of reproductive
    potential, over half of the species were active for longer than 6 months.
     Labrids (Warner, et al., 1975) and somne haemulids (McFarland, 1980, 1982) spawn
    over the entire y`iar-,-ut many species have highly restricted spawning seasons.
     Between these extremes, however, some species produce all of their eggs in a
     single or in very few reproductive acts, while others rely on a more consistent
     release which involves the release of fewer eggs during each reproductive
     bout. It is difficult to generalize with certainty how these highly varied
     spawning tactics relate to dispersal and recruitment. This is further complicated
     by the fact that virtually every assemblage of coral reef fishes contains
     species that utilize each reproductive tactic.

          Many species tend to show periodicity of spawning over a season or even
     longer.  In a survey of reproduction in 52 tropical fishes, ,Johannes (1978)         1

                                            38

    found that 20 tended to spawn near or at new moon, 8 at full moon, 13 at times
    of both new and full moon, and the remaining 11 during quarter moons.

         Several direct observations have related the timing of spawning to specific
    phases of the moon (e.g., quarter moons, Polydactylus sexfilis, May, et al.,
    1979; Centropyge potteri, Lobel, 1978).  The periodicity in spawning has been
    interpreted as an adaptation to enhance the chance that the eggs will be flushed
    by tidal currents away from the reef, and therefore reduce mortality by egg
    predators, which is commonly observed (Randall and Randall, 1963; Moyer, 1974;
    Meyer, 1977; Robertson and Hoffman, 1979; Colin, 1978; Robertson, 1983).

        Mortality among the pelagic eggs and larvae is high when compared to the
    adults (Sale, 1980). Very likely as a response to this high mortality (but
    perhaps also to increase the probability that some propagules will be dispersed)
    the fecundity of reef fishes is high, usually in excess of 50,000 eggs per year
    per female in pelagic spawners (Randall, 1961; Bryan, et al., 1975; Thompson
    and Munro, 1978), and greater than 8,000 eggs in demersal spawners (Warner, et
    al., 1975; Bell, 1976).

         In addition to varied lunar periodicities, many reef fishes migrate to the
    deeper areas of the reefs and/or to pinnacles and reef extensions to spawn, and
    there usually invoke discrete behaviors when spawning (e.g., a rush to the
    surface to spawn the eggs as far from the reef as possible; Lobel, 1978; Colin,
    1982). In addition, spawning often shows a daily cycle (e.g., occurring at
    dusk; Lobel, 1978). These behaviors have been interpreted as acts to reduce
    egg predation and may be particularly effective because eggs are small,
    transparent, and therefore difficult to detect, especially at dusk (Hobson and
    Chess, 1976). Many species, however, spawn during midday or the afternoon
    (Colin, 1982; Robertson, 1983).

         Although the observations on spawning behavior suggest tactics that can
    reduce mortality of eggs and improve dispersal away from the reef, few observations
    are supported by direct measurements of prevailing tides, currents, and other
    conditions to verify that this is what actually happens. A recent paper by
    Robertson (1983) combines careful field observations of spawning in seven
    species of surgeonfishes at four differen' localities in the Pacific and Indian
    Oceans. Readers are referred to the original for the wealth of observations
    detailed by Robertson. Several general conclusions, however, are important.
    (1) The various species spawned over different intervals of the day (a few in
    the morning; most from midday until dusk). (2) Both paired spawnings and group
    spawnings occurred in several of the species. (3) Except where territorial
    harems were established, most individuals migrated toward outer and deeper
    portions of the reefs to spawn. (4) In. almost all instances, spawning fishes
    rose toward the surface to spawn. (5) The most common feature among the seven
    species was a strong tendency to spawn during ebb tides, as water was flushed
    off the reef. All of these-behaviors would minimize the chance that freshly
    fertilized eggs would be exposed to planktivorous reef fishes. Spawning as
    tides flush water off reefs also was indicated by Randall (1961), Robertson and
    Choat (1974), Lobel (1978), and Thresher (1979). In contrast, Robertson (1983)
    found no distinct tidal rhythms in surgeonfish spawnings at Lizard Island where
    the currents flow parallel to the reef rather than on and off the reef.  This

                                             39

    finding suggests that spawning in a species is strongly influenced by local        __
    conditions. Thus, behaviors that in one location may reduce egg mortality U
    might increase egg mortality if repeated precisely at another site.

         In summary, reproductive efforts in a species often can be shown to diminish
    predation on spawned eggs and enhance the chance of their dispersal. But, many
    species show variable spawning behavior. It is therefore uncertain that all
    reproductive behaviors are selected to reduce egg predation and/or assure
    dispersal.

                             DISPERSAL -- THE PELAGIC PHASE

                     Hypotheses to Explain the Pelagic Larval Phase

         Why should almost all coral reef fishes cast their eggs and/or larvae
    offshore? Three primary hypotheses have been suggested: (1) the antipredator
    hypothesis, (2) the food hypothesis, and (3) the dispersal hypothesis (see
    Johannes, 1978, for review). Jdhannes, who favors the antipredation hypothesis,
    argues that if the eggs and larvae were left on the reef unprotected, they
    would be subject to an excessive mortality by reef predators (see also Smith,
    1978). Although it is certain that predation on eggs and larvae is very high
    by reef planktivorous fishes (Hobson and Chess, 1978) and by sessile filter
    feeders (Johannes, 1978), it is not clear how much predation is reduced when
    eggs and larvae are offshore (Barlow, 1981). Egg mortality offshore can approach
    30% per day (Jones and Hall, 1974; Ware, 1975). Considering the relative merit~
    of these factors and others led Barlow (1981) to postulate that the reduction U
    in predation achieved from a pelagic phase was of less significance to survival
    than the advantages that are derived from dispersal (over both short and long
    distances). Barlow sees dispersal as a means to ensure survival of a species
    by reducing inbreeding (Bengtsson, 1978), and, particularly, as an adaptation
    to the instability of reef communities (Connell, 1978; Sale, 1978a). He argues
    that the lor~ger an egg or larvae travels, the less its chance of survival
    (Thorson, 1946; Gadgil, 1971). For long-range dispersal to succeed, reef fishes
    must produce numerous offspring, which they do, and larvae must be adapted for
    a lengthened pelagic life, which in many species is true (e.g., in surgeonfishes,
    butterflyfishes, wrasses, and in eels; Barlow, 1981). The possibility exists,
    nevertheless, that cohorts fromi a single spawning may remain together as eggs
    and larvae in the plankton, and thus maintain genetic relatedness among recruits
    (see Shapiro, 1983). This interesting possibility, which would increase inbreeding
    success, remains to be documented.

         The food hypothesis is dismissed by both Johannes (1978) and Barlow (1981)
    because in general planktonic food is less available offshore than inshore;
    thus, the advantage of offshore disperal must find another explanation, such as
    a reduction in predation or enhanced dispersal.

         Although Johannes and Barlow are aware that both recolonization and long-
    range dispersal occur, their respective arguments favor different views of the
    role of dispersal in larval recruitment from the plankton. Barlow (1981) views
    the long-range transport of larvae to other localities than the parent reef
     (island, etc.) as the essential selective force that has operated. In contras*

                                            40

    Johannes (1978) emphasizes avoiding predation and invokes data (largely
    anecdotal) to suggest that eggs are cast into local current gyres that often
    return to the same island or, at least, to the same general locality and not
    necessarily to far distant shores. There were some data to suggest that this
    was so when Johannes (1978) postulated the role of local currents in recolonization
    (Jones, 1968; Sale, 1970; Watson and Leis, 1974; Lobel and Reaka, 1977; and
    since then Leis, 1982). More convincing data have now been provided by Lobel
    and Robinson (1983) that current gyres do develop off the big island of Hawaii
    twice each year and, importantly, coincide with the two major seasonal spawning
    peaks for many of the coral reef fishes in Hawaii (Jones, 1968; Sale, 1970).
    Lobel and Robinson, using radio-tracked drogues, found circulation times of 7-
    14 days (offshore and return inshore) and evidence for at least two cycles.
    Thus, there would be time for eggs and larvae to develop to a sufficient size
    to settle onto the reef after initially being advected away from the reef.
    However, it should be emphasized that in multiple releases of drogues, some
    returned close to the inshore release site, but others drifted off and even
    headed toward the island of Molokai. Furthermore, as Barlow (1981) emphasizes,
    even if major seasonal spawnings at Hawaii do coincide with the weakest offshore
    currents and the presence of local gyres (Watson and Leis, 1974) which might
    favor recolonization, spawning nevertheless continues in many species at other
    times of the year when currents would not favor recolonization, but rather long-
    range dispersal.

                                Duration of Larval Life

         Certainly if long-range dispersal is to be invoked, as for example Barlow
    (1981) suggests occurs for those coral reef species that have managed to cross
    the Indo-Pacific barrier (see Rosenblatt and Walker, 1963), then the length of
    larval life must be long. An alternative tactic for long-range dispersal would
    invoke rafting of juveniles or adults, a requirement if the larval phase is of
    short duration (< 20-30 days). How long, then, are larvae advected at sea?

         By comparing spawning dates with recruitment dates, larval duration has
    been estimated to vary among coral reef species from a week to several months
     (Randall, 1961; Moran and Sale, 1977; Johannes, 1980). Over the last few years,
    the otolith daily aging technique has allowed direct estimation of the age of
     individual larvae (Brothers and McFarland, 1981). The results to date indicate
    that larval duration does vary from weeks to months in different species
     (Ralston, 1976; Brothers, et al., 1983; Victor, 1983a; and Brothers and Thresher,
     1985).  The duration withina species is often variable, as it is in marine
     invertebrates (Scheltema, 1968, 1971), but some species have very restricted
     lengths of larval life, the cause of which is unknown (Brothers and McFarland,
     1981). For the 115 species of Pacific coral reef fishes studied, Brothers and
     Thresher (1985) obtained otolith ages for settlement (the so-called settlement
     check mark; see Brothers and McFarland, 1981; Brothers, et al., 1983; Victor,
     1983b) that range from 15 to 82 days.  In some labrids, it can be a week (Victor,
     1983b), and in grunts settlement always occurs at about 15 days (McFarland,
     1982T. These pelagic periods favor only short-range dispersal. But, some
     labrids can have larval durations up to 50 days (Brothers, et al., 1983), which
     would allow for long-range dispersal.

                                             41

                                    Larval Behavior

         Another factor that can affect larval mortality and dispersal is the
    behavior of fish larvae at sea. It is generally conceded (although with little
    direct evidence) that fish larvae disperse passively in offshore currents (Sale,
    1970; Leis and Miller, 1976) and, therefore, that their final destinations are
    subject to hydrographic conditions. Alternatively, it has been argued that
    larval drift is not passive (Sale, 1980). In Hawaii, larvae from species with
    pelagic eggs (labrids, chaetodontids, acanthurids) are more common offshore
    than species with demersal eggs (pomacentrids and gobies), which are more common
    inshore (Miller, 1974; Leis and Miller, 1976; Watson and Leis, 1974). This is
    explained by invoking active larval mechanisms. However, it may also be
    explained merely by initial passive drift of pelagic eggs. Nevertheless, once
    fish larvae begin to swim, vertical movements could place them in currents that
    would hold them inshore or advect them away. Unfortunately very little is
    known about larval behaviors. Several investigations have established that
    many pelagic invertebrates undertake marked diel vertical migrations, ascending
    toward the surface at night and to deeper depths during the daytime (see Segal,
    1970, for overview). Recent investigations also have revealed that reef
    meroplankton emerge high into the water column at night, especially during the
    dark phase of the moon (Porter, et al., 1977; Porter and Porter, 1977; Alldredge
    and King, 1977, 1980; Hobson and-Chess, 1979; Robichaux, et al., 1981; Ohlhorst,
    1982, 1985).  These vertical movements take place over a T-i -meters.  Similar
    vertical distributions seem to occur in coral reef fish larvae, at least nearshore
    (Hobson and McFarland, preliminary unpubl. data).  It is known, however, that
    reverse tidal currents can occur over shallow depths, as they do at St. Croix
    (Lee, et al., 1977), and it is possible, even likely, that fish and invertebrate
    larvae'-si-hese currents, in combination with vertical migratory behavior, in
    their dispersal.

         Certainly broad parallels occur between benthic marine invertebrates and
    fishes. In tropical regions, 80-85% of the invertebrates produce long lived,
    planktotrophic larvae that will hatch, as in fishes, from relatively small eggs
    (Thorson, 1950). In general, larval pelagic existence is longer in tropical
    invertebrates than in species from higher latitudes (see Thorson, 1950;
    Mileikovsky, 1971; and Jablonski and Lutz, 1983, for review). Extended larval
    periods appear to enhance dispersion and are associated with broad geographic
    distributions in tropical invertebrates (Scheltema, 1968, 1971), and this
    pattern seems, at least tentatively, to also hold for coral reef fishes (Brothers
    and Thresher, 1985).

         In summation, there is no simple explanation in terms of dispersal versus
    antipredatory mechanisms that resolves what major selective processes have
    caused virtually all coral reef fishes to produce pelagic propagules. In fact
    the data cited show such-wide variation that it is likely that in some species
    dispersal was the preeminent selective factor, while in other species antipreda-
    tion was the most important. In any case, dispersal and antipredation are not
    mutually exclusive selective factors, and certainly both act to increase
    survival. Nevertheless, it is difficult not to wonder, as Barlow (1981) has,
    why more coral reef fishes do not invest in postzygotic activities to reduce
    the duration of the larval pelagic phase, or even eliminate it. i

                                            42

         Barlow suggests that postzygotic activity leads to a reduction in lifetime
    fecundity in part because of the parental investment required. Most coral reef
    fishes that spawn demersal eggs tend to be small, a circumstance that in itself
    limits egg production. In addition, most coral reef species are strongly site-
    attached and spend their adult lives in a relatively small local area (Sale,
    1980). Pelagic dispersal thus can be considered a necessary consequence of
    their restricted mobility. If, for example, specific reef habitats tend to be
    unstable over time, a circumstance that recent events document (e.g., severe
    hurricane damage of reef habitat at Jamaica, Woodley, et al., 1981; Kaufman,
    1983; storm effects at Lizard Island, Lassig, 1983; coral-Tight in the Caribbean
    and Pacific, Lessios, et al., 1983), then dispersal to colonize adjacent or
    distant habitats is an essential element in each species' survival.

                      RECRUITMENT--HOW DO FISHES SETTLE ON REEFS?

         In a review of coral reef fish ecology, -Sale (1980) stated, "The mechanisms
    whereby larval fishes make their return to the reef are totally unknown."  In
    addition, it is only over the last few years that more systematic observations
    of recruitment in reef fish larvae have begun to appear in the literature.  For
    most of the observations, maximum recruitment occurs over a single season and
    often is episodic; it may follow a lunar periodicity (Johannes, 1978); it may
    be monthly but not coupled to a particular phase of the moon (mixed guilds of
    pomacentrids; Williams, 1983), or a rhythm may not be conspicuous (Thalassoma
    bifasciatum; Victor, 1982, 1983a).

         Larval French grunts (Haemulon flavolineatum) settle from the offshore
    plankton following a semi-lunar timetable.  This periodicity is most closely
    correlated with the quarter moons and/or daily intermediate tidal excursions
    that fall between the spring and neap tides (McFarland, et al., 1985; also see
    McFarland, 1982).  Furthermore, although seasonal, some recruitment continues
    throughout the year.  Larval life is short (ca. 15 days; Brothers and McFarland,
    1981), which implies that spawning also must occur throughout the year; also
    ripe eggs are present in adult French grunts at all times of the year (Munro,
    et al., 1973).

         The extreme variations seen in the spawning periodicities of reef fishes
    (see earlier section) are reflected in the variable periodicity in recruitment.
    What do larvae select when they settle from the plankton to the reef? Here we
    are almost totally in ignorance. Most larval (or postlarval) recruits are
    first observed on substrate (coral patches, seagrass beds, sand, etc.). Usually,
    it is not possible to state that they have just settled. In a study of recruiting
    pomacentrids, Williams and Sale (1981) found that different species tended to
    prefer different species of corals. Earlier Sale (1969) found that young
    surgeonfish preferred reefs with shaded overhangs. It is generally understood
    that each species has certain needs for settlement, but determination of these
    needs has barely been initiated. In addition, settlement to a specific site
    can be dramatically influenced by resident competitors (Shulman, et al., 1983).

         Actual settlement has seldom been observed. During observations of the
    acronurus larvae of Acanthurus triostegus in Hawaii, Randall (1961) concluded

                                            43

    that they settle at night. We have observed the same nocturnal timing for
    acronurus larvae on settlement reefs at St. Croix. Recruiting young
    pomacentrids also seem to appear overnight (Doherty, 1981). But daytime
    settlement is not precluded. Given the present status of our knowledge of
    larval fish behaviors, it is difficult to envision how a larval fish avoids
    settling if by chance it is carried across suitable substrate during the daytime;
    but, in contrast, how does a larval fish "know" that it should settle at night?
    Are cues visible, olfactory, or, perhaps, sonic? Certainly, planktivorous reef
    fishes are less active at night (Hobson, 1974; Hobson, et al., 1981-, Gladfelter
    and Johnson, 1983), but filter-feeding sessile invertebrate~s are most active at
    night (Sebens and DeReimer, 1977). Obviously, more precise studies are required
    to evaluate just how important nocturnal settlement is to survival.

         It should be emphasized that recruitment of larvae varies considerably
    from year to year (Williams and Sale, 1981; Williams, 1983). As Williams
    states, "One large pulse alone is sufficient to make total recruitment in a
    year unusually successful." He reminds us as well that a large recruitment of
    one species does not mean the same for another species, even in the same guild.

         Finally, it has been implicit in the various arguments of recent fish
    biologists interested in explaining the diversity in coral reef fish assemblages
    that the offshore plankton provides a huge, although variable, reservoir of
    potential recruits which is drawn upon when appropriate space opens on the reef
    (Dale, 1978; Sale, 1978a; Smith, 1978). Perhaps this is so, but Doherty (1981)
    suggests that at least at certain times the larval pool may not be endless and
    can be limiting to the maintenance of reef populations. His theoretical model
    assumes that larval existence for most species is "precarious" at best (see           Is
    also Johannes, 1978), and this limiting function introduces a high degree of
    chance into the recruitment process.

                                      CONCLUSIONS

         From what is currently known about the recruitment of coral reef fishes
    from the plankton, it seems likely that strong interactions between local
    currents and the times of spawning exist. The functions) of this interaction
    is best explained as a mechanism to both remove eggs and larvae from the vicinity
    of the reef to reduce predation and to disperse the young to other localities.
    The possibility of seasonally developed recirculating eddies could lead to
    local recolonization. Even totally isolated islands could sustain their fish
    populations by holding larvae in downstream eddies (Emery, 1972), especially if
    discrete larval behaviors are used to remain in the eddies. What is missing is
    an unambiguous case that this routinely occurs.

                                    ACKNOWLEDGMENTS

         Our research as reported in this paper was supported by NSF Research Grant
    OCE-79-18569. This paper is Contribution Number 128 of the West Indies
    Laboratory, St. Croix, U.S.V.. We thank Drs. John Ebersole and Marjorie Reaka
    for their many critical and constructive comments during the preparation of the
    manuscri pt.

                                            44

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                                            51

                 PELAGIC DURATION, DISPERSAL, AND THE DISTRIBUTION OF
                            INDO-PACIFIC CORAL-REEF FISHES

                                  Edward B. Brothers
                                     3 Sunset West
                                Ithaca, New York 14850

                                   Ronald E. Thresher
                             Division of Fisheries Research
                             C.S.I.R.O. Marine Laboratories
                            Cronulla, N.S.W., 2230 Australia

                                        ABSTRACT

         The breadth of distribution of most Indo-Pacific coral-reef fishes does
    not clearly correlate with the duration of their pelagic developmental stages.
    Rather, there is a threshold effect at approximately 45 days, above which
    species tend to be broadly distributed, butbelow which pelagic duration and
    distribution appear unrelated. Long larval durations also characterize species
    that have colonized geographically isolated areas, such as the Hawaiian Islands
    and the Eastern Pacific. Comparison of larval durations with estimates of time
    required to cross the "East Pacific Barrier" further suggests colonization of
    the New World to be an infrequent event, most likely associated with unusually
    strong development of the Equatorial Countercurrent.

                                      INTRODUCTION

         The pelagic larval stage characteristic of many invertebrates and fishes
    is widely assumed to serve as a dispersal mechanism (Scheltema, 1971, 1978;
    Crisp, 1976; Barlow, 1981; Smith, 1982). A logical corollary of this assumption,
    also widely accepted, is that long larval duration correlates with broad
    dispersal and consequent broad distribution (Shuto, 1974; Strathmann, 1974;
    Zinsmeister and Emerson, 1979; Reaka, 1980; Ayal and Safriel, 1982; Jablonski
    and Lutz, 1983). We tested this hypothesis by comparing the distributions
    of 115 species of Indo-Pacific coral-reef fishes, in 22 families, with the
    duration of their pelagic developmental stages, determined by examination of
    otolith microstructure. The data suggest a threshold effect, with long pelagic
    durations correlating with broad distributions only above a species mean value
    of approximately 45 days. Only 20% of the species we examined have pelagic
    durations this long, a value in surprisingly close agreement with independent
    estimates of the frequency of "true long-distance" pelagic larvae of marine
     invertebrates (Thorson, 1961). We also examine the question of whether long
    pelagic durations are typical of those species that have colonized geographically
     isolated areas, such as the Hawaiian Islands, and, particularly, the Eastern
     Pacific.

                                         METHODS

          Duration of the pelagic larval stages was determined either by aging of
     individuals newly recruited to the reef (Brothers, et al., 1983) or by examination

                                             53

    of otolith "settlement marks" in juveniles and adults, the latter involving
    techniques similar to those used in other studies (Brothers and McFarland,
    1981; Victor, 1982; Thresher and Brothers, in press). Total duration of the
    pelagic stages was assumed to be equal to calculated otolith ages for most
    demnersal spawning fishes. This assumption is based on limited data (Brothers,
    unpublished data) which suggests that daily growth increments in most demersal
    spawning fishes begin forming shortly after hatching. The only demersal spawning
    families for which this is not likely to be true are Balistidae and Siganidae,
    both of which hatch as relatively undeveloped prolarvae (see review in Thresher,
    1984). For these two families, 2 days were added to calculated pelagic durations
    to account for the likely duration of pelagic pre-feeding stages. For pelagic
    spawning fishes, total duration of the pelagic stages was estimated by adding 3
    days to otolith ages. This was based on a mean incubation time of 43.1 hours
    for pelagic eggs of such fishes (Thresher, 1984), plus limited data suggesting
    that another 24 hours may pass before the first growth increment forms (Brothers,
    unpublished data).

         Species distributions were based on taxonomic reviews and comparison of
    faunal lists for different areas. The extent of distribution was quantified by
    dividing the tropical Indo-Pacific into 29 "bio-geographical areas" and counting
    the number of areas inhabited by each species. Division of the Indo-Pacific
    follows Allen (1979). The rationale behind this approach is discussed in
    Thresher and Brothers (in press).

         Data were obtained for 115 species (see table 1) in 22 families, essentially
    all those we had available to us. The taxonomic distribution is not intended
    to be qualitatively or quantitatively representative of typical reef
    ichthyofaunas, although effort was made to include representatives of as many
    families as possible. The only fishes specifically excluded from the analysis
    were Hawaiian endemics and a few families, such as kyphosids and carangids,
    that are known or strongly suspected to raft as juveniles or adults under
    floating objects. The few Hawaiian endemics we had available were excluded
    because of difficulty in discerning a single or discrete "settlement mark" (see
    Thresher and Brothers, in press, for further discussion of this problem). Some'
    material was obtained for us directly in the field (the Philippines, Japan, the
    Marshall Islands, and Australia), but the majority were obtained as juveniles
    and small adults from the aquarium. As such, most were probably collected in
    the Philippines, the Hawaiian Islands, or off the Australian Great Barrier
    Reef. Specimens maintained in captivity for a variable period were suitable
    for our study since they were initially captured as settled juveniles or adults
    (rather than being reared in captivity) and because there are no indications,
    nor expectations, that conditions in captivity affect structures already laid
    down in the otoliths.

         Specific samples sizes were typically small (range I - 15, Y = 2.62, mode
     =1), but intraspecific variation in most species examined was also small (see
    results; also Thresher and Brothers, in press).  Calculated durations, therefore,
    are likely to be robust for most species examined.  Results of our analysis are
    also sufficiently broadly based that minor adjustments of a few species are likely
    to have little or no impact on the conclusions drawn.

                                            54

                                        RESULTS

         Table 1 summarizes our data for mean pelagic duration and geographic
    distribution for the 115 species examined. Intraspecific variation appears to
    be low for most species. Of 57 species with N > 2, this variation ranged from
    O to 25 days, with a mode of 3 days, a mean of 5.0 days, and a standard deviation
    of 4.97 days. Only seven species (5 broadly distributed) varied intraspecifically
    by more than 10 days, and only three, Coris gamaird and Gomphosus varius
    (Labridae) and Rhinomuraena amboinensis (Muraenidae), varied by more than 20
    days.  Based on observations of specimens collected in other areas, la;ge
    intraspecific variation appears to be more common in these families and also the
    Gobiidae and Scaridae (Brothers, et al., 1983; and Brothers, unpublished data)
    than in the remaining families.  <i yet, we have no data on geographical or
    environmental effects on intraspecific variability in larval duration, if any.

         Based on species mean values, there is a conspicuous threshold effect in
    the relationship between pelagic duration and species distribution at approximately
    45 days total pelagic duration (fig. 1). Below this threshold, duration of the
    pelagic stage does not correlate with breadth of distribution (Spearman Rank
    Correlation = 0.12, N = 92, p > 0.2), suggesting that for most Indo-Pacific
    coral-reef fishes (79.3% of species examined, and all representatives in 14 of
    the families), the length of time that pelagic eggs and/or larvae disperse is
    not the principal determinant of the extent of species distributions. In
    contrast, of the 23 species that have mean pelagic durations longer than 45
    days, all but three are broadly distributed in the Indo-Pacific, with more than
    half (14 of 23) inhabiting 25 or more biogeographic areas (as compared with 3
    out of 92 subthreshold species; this difference is significant at p < 0.001;  x2
    = 53.7, df = 2). The exceptions to the above are Chaetodon collare (total
    duration 46 days), Neocirrhites armatus (51 days), and Rhinomuraena amboinesis
     (74 days). Of these, the first two are close to the threshold value. We are
    unable, however, to account for the limited distribution of the muraenid, R.
    amboinesis.  The two specimens examined differed markedly in apparent larval
    duration (63 and 85 days), but both are well above the threshold and are con-
    sistent with our data for other muraenid species.

          The data also suggest that unusually long pelagic durations are critical
     for colonization of geographically isolated areas. The average pelagic duration
     for Central Pacific species that also are found in the Hawaiian Islands, widely
     considered an isolated out-lier of the Indo-Pacific faunal province (Ekman,
     1953; Briggs, 1974), is 68.4% longer than those that are not found in Hawaii
     (Central Pacific only, X = 49.1 days, S.D. = 9.5, N = 91; species also in
     Hawaii, k = 49.1 days, S.D. = 10.3; N = 15; difference significant at p < 0.001,
     Kolmolgorov-Smirnov test for unequal sample sizes; fig. 2). The minimum observed
     duration of Hawaiian-inclusive species, 35 days, is longer than the mean
     durations of 59.5% of the species examined, suggesting that most Central Pacific
     species may be incapable of colonizing Hawaiian reefs under normal circumstances.
     The pattern for colonizing Eastern Pacific reefs by Indo-West Pacific species
     is similar (fig. 2). Trans-Pacific species examined have a mean pelagic duration
     25.6% longer than even Hawaiian-inclusive species, and a minimum duration (48
     days) that is longer than mean durations of 81.0% of the species we examined.

                                              55

       Table 1.--Duration of pelagic larval stage (in days, as number of pre-transition otolith increments,
         age of new recruits, or both) and extent of geographical distribution (number of biogeographic areas
         occupied) for 115 species of Indo-Pacific coral reef fish.  Location:  AT = Aquarium Trade, AUS =
         Australia, JA = Japan, MI = Marshall Islands, OT = One Tree Island, PH = Philippines.

    Family and species                        No. bf      Source          X Otolith increments          Larval        Size of
                                           specimens                                   Total for   duration       geographic
                                                                   Pre-transition  new recruits    (Range)   distribution

        ACANTHURIDAE

           Acanthurus glaucopareius                3         AT             59.7                         56-62          18
           A. lineatus                             2         AT             39.5                         38-41          21
           A. triostegus                           1         AT             51                             -            28
           Naso lituratus                          1         AT             69                             -            27
           Paracanthurus hepatus                   1         AT             37                             -            17
           Zebrasoma veliferum                     1         AT             36                             -            26

        APOGONIDAE

           Apogon cyanosoma                        5         OTI                             18.2        18-19         20
           A. doderleini                           5         OTI                             22.6        16-27          8
           Cheilodipterus quinquelineata           4         OTI            18.8                         17-20         24
                                                  25         OTI                            23.1        17-21
           Siphamia orbicularis                    1         AT             17                            -            13

        BALISTIDAE

           Balistoides conspiculatum               3         AT            36.0                         35-38          18
           Rhineacanthus rectangulatus             6         AT            43.5                         39-46          24
           R. aculeatus                            1         AT            48                             -            25
           Palaluteres prionurus                   1         OTI                            28                         21

    gable l.--Continued

    Family and species                         No. of       Source           X Otolith increments           Larval         Size of
                                             specimens                                     Total for   duration        geographic
                                                                       Pre-transition  new recruits    (Range)   distribution

       BLENNIIDAE

           Petroscirtes mitratus                     2          OTI            24.5                          24-25          19

        CALLIONYMIDAE

           Synchiropus splendens                     2          AT             36                            33-39            4

        CHAETODONTIDAE

           Forcipiger flavissimus                    3          AT             50.7                          41-57          28
           Heniochus diphreutes                      2          AT             32.0                          30-34           8
           Chelmon rostratus                         2          AT             27.0                          26-28          11
                                                     2         OTI                              25.5        25-26
           Chaetodon lineolatus                      1          AT             54                              -            22
           C. kleini                                 1         AT              56                                           22
           C. speculum                               1          AT             26                              -            10
           C. trifascialis                           2         AT             32                             30-34          24
           C. baronessa                              2         AT             38                              38             8
           C. auriga                                 2         AT             46.5                          40-53           26
           C. unimaculatus                           2         AT             35.0                            35            24
           C. collare                                1         AT             43                                             6
           C. rainfordi                              1         OTI                              35                           3
           C. plebius                                1         OTI                              39                          13

        CIRRHITIDAE

           Cirrhitichthys oxycephalus                1         AT             51                                            27

       Table I.--Continued

    Family and species                       No. of       Source         X Otolith increments           Larval        Size of
                                           specimens                                   Total for   duration    geographic
                                                                   Pre-transition  new recruits    (Range)   distribution
       CIRRHITIDAE (continued)

          Neocirrhites armatus          I                   AT             48                             -            10
          Oxyeirrhites Upus                       3         AT             69.0                         62-73         20

       EPHIPPIDAE

          Platax pifinatus            I                      AT            25                             -21

       GOBIIDAE

          Amblygobius rainfordi                   4         OTI                            40.3         40-41          4
          Paragobiodon echinocephala       I                OTI                            36             -           19
          P. mnelanosoma                          3         OTI                            42.3         39-47         11

       LABRIDAE

          Anampses coeruleopunctatus        I               AT             25                            -20
          Consl aygula              I                       AT             51                             -           26
           C.gamnaird              I                        AT            51.3                         35-60          26
           C.variegata                            3         OTI                            29.7        28-30           5
          Cirrhilabrus temminkii         I                  OTI           24                             -            23

                                                  1        OTI                            30
                    C. cyanopleura                1 ~ ~~~ AT              30                             -            10
          GompRhosus Varius                       5         AT            52.8                         42-75          26
          Halichoeres biocellatus        I                  OTI           21                                          10t

                                                 I OTI                                   27
          Hemipteronotus taeniurus                2         AT            45.0                         43-48          27

       Table l.--Continued

    Family and species                        No. of       Source          X Otolith increments           Larval         Size of
                                             specimens                                    Total for   duration        geographic
                                                                     Pre-transition  new recruits    (Range)   distribution

       LABRIDAE (continued)

          Labroides dimidiatus                     6          AT, OTI       23.2                          22-24          23
          L. bicolor                               1         AT             24                              -            23
          Lierdenella fasciata                     2          AT            20.0                          19-21          16
           Macropharygodon meleagris                1         AT             30                              -            24
          Stethosulis axilaris                     1          PH            35                                           24
          Thalassoma hardwicki                     6          PH            45.7                          44-47          16
           T. lunare                                4         AT, OTI        47.0                          42-50          26

       LETHRINIDAE

           Lethrinus nebulosus                      1         OTI            37                                           20

        LUTJANIDAE

           Lutjanus sebae                           1         AT             40                                           17

        MALCANTHIDAE

           Hoplolatilus purpureus                   3         AT             34.0                         33-36           4

        MURAENIDAE

           Echidna nebulosus                        1         AT             80                             -            27
           Rhinomuraena amboinensis                 2         AT             71                           60-82           9

        OSTRACIIDAE

           Ostracion meleagris                      2         AT             69.0                         68-70         25

       Table 1.--Continued

    Family and species                        No. of       Source          X Otolith increments           Larval         Size of
                                             specimens                                    Total for   duration        geographic
                                                                      Pre-transition  new recruits    (Range)   distribution

       POMACA NTHIDAE

           Apolemichthys trimaculatus               3         AT             24.2                          22-26          17
           Centropyge acanthops                     1         AT             34                              -             3
           C. bicolor                               3         AT             32.0                          29-34          11
           C. bispinosus                            3          AT            32.0                          31-33          17
           C. eibli                                 6         AT             25.3                          24-27           7
           C. ferrugatus                            1         AT             38                              -             3
           C. flavissimus                           3         MI, AT         30.3                          28-32           7
           C. heraldi                               4         AT             32.0                           32             7
           C. interruptus                           2         JA             31.5                          29-34           2
           C. loriculus                             1         AT             38                              -             6
           C. multifasciatus                        3         AT             26.2                          25-28           7
           C. nox                                   2         AT             31.5                          28-33           5
           C. tibicen                               3         AT             30.0                          27-34          10
           C. vroliki                               1         AT             29                              -            10
           Chaetodontoplus melanosoma               3         AT             22.2                          20-23           6
           C. mesoleucas                            5         AT             19.9                          18-22           7
           C. personifer                            4         AT, AUS        23.25                        23-24           3
           C. septemtrionalis                       1         AT             23                             -             5
           Genicanthus bellus                       1         AT             25                             -             9
           G. melanospilos                          1         AT             25                             -             6
            Holacanthus venustus                     1         AT             25                             -             3
           Pomacanthus annularis                    2         AT             21.0                         20-22           6

           Table l.--Continued

        Family and species                         No. of      Source          X Otolith increments           Larval         Size of
                                                 specimens                                    Total for   duration       geographic
                                                                          Pre-transition  new recruits    (Range)   distribution

           POMACANTHIDAE (continued)

              P. imperator                             2          AT            22                              22           25
              P. navarchus                             3         AT             22.8                          22-24           3
               P. semicirculatus                        4         AT             19.5                          19-20          21
               P. sexstriatus                           2         AT, AUS        18.0                          17-19           8
               P. xanthometopon                         4         AT             20.4                          19-22           5
               Pygoplites diacanthus                    2         AT             24.5                          23-26          25

           POMACENTRIDAE
    cn
               Chrornis caeruleus                       5         PH             25.0                          23-26         21
               C. atripectoralis (probably)             1         AT             19                             -            11
                                                        2         OTI                            23.0         20-26
               Dascyllus aruanus                        5         AT             22.4                         20-26          25
                                                        4         OTI                            22.0         20-23
               D. melanurus                             3         AT             23.3                         22-24           5
               D. reticulatus                           1         AT             23                             -            23
               D. trimaculatus                          5         AT             24.2                         21-25          23
               Abudefduf saxatilis                      1         OTI            23                             -            22
               Glyphidodontops cyaneus                  6         AT             19.5                         17-21           7
               G. biocellatus                           1         AT             19                             -             8
               G. hemicyaneus                           5         AT             19.25                        18-21           4
               G. rex                                   3         AT             22.0                         19-25           8
                                                        3         OTI           19.7                          19-20

         Table I.--Continued

      Family and species                       No. of      Source         XOtolith increments          Larval         Size of
                                             specimens                                  Total for   duration    geographic
                                                                     Pre-transition  new recruits   (Range)   distribution

        POMACENTRIDAE (continued)

           G. rollandi                             3        OTI                            23.0          23           2
           G. talbot i             I                        OTI                            22
           Dischistodus pseudochrysopoecilus    I           OTI                            23            -            3
           Neopomnacentrus azysron        I                 OTI                            24            -            3
           Paraglyphidodon behni                   4        AT            17.75                        15-21          6
           Pomacentrus amboinensis                 8        OTI           19.6                         19-20          6
                                                  is OTI                                   22.5        18-26
    N3  ~P. australis                               4        OTI           25.0                         23-26          1
                                                   2        OTI           85.0                          85
           P. coelestis             I                       AT            20                            -            13
                     P ~~~~~~~10                            OTI            19.1                        18-21          8
                                                   4        OTI                            24.0        23-25
           P. wardi                               7         OTI           20.0                          20            1
                                                   4        OTI                            24.25       23-25
            P. vaiuli                              6         OTI           24.2                         23-26         10
            P. Sp.                                15         OTI                           22.9        20-24           4

        SCARIDAE

            Bulbometopon muricatum         I                 AT            31                             -21

         SCOLOPSIDAE

            Scolosis dubiosus                      3         OTI                           19.0        15-23           8

       Table l.--Concluded

    Family and species                       No. of      Source          X Otolith increments         Larval         Size of
                                           specimens                                   Total for   duration      geographic
                                                                  Pre-transition  new recruits   (Range)   distribution

      SERRANIDAE

         Anthias pascalus                        1         AT            26                                          7
          Cromileptis altivelis                   1         AT            24                            -             9

      SIGANIDAE

          Siganus (Lo) vulpinus                   2         AT            23.5                         23-24          8

      ZANCLIDAE

          Zanclus cornuta                         1         AT            57                            -            28

             30

                                       A               AM
             25-       o�                              �
                     o        A�  �
                        c lo
                      0   O 0 0   0                    U
           w 20.         0       0 �
                      0          o
                         o    o  o   o

           1- oo

            0   0 08                     0
                     oo          o
                         00                             0

             000 o  o    00 0

              ~0
                      *_/  oo o    o

           '~10 '  o  P   ooo

                               o

              �10    io0   30    40    50    60    70    80
                        X  PRE-TRANSITION  OTOLITH  INCREMENTS

    Figure 1.--The relationship between species mean pelagic larval duration, as
      indicated by the number of pre-transition daily growth increments, and the
     breadth of distribution of 115 species of Indo-Pacific coral-reef fishes.
     Total pelagic durations are 0-3 days longer than increment counts, depending t
     on the family.

                                         64

    -

                    .~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~

                              25'-
                                   2    ~ ~5     -Western and Central Pacific Only
                                                                X 29.4   S.D.=9.5
                                                                      N 91

                           wK
                                      0 .                      ,         ,  J   '  .~~~~~~~~.I
                           Zr 0
                           L      Hawaiian

                               Ot                                 L
                           X  50 X= 49.1  S.D.       = 160.3
                           _  a, L     N= 15

                              ' 5  X=62.2   S.D.= 11.4
                            Z           N x 9

                                 10    20    30    40    50    60    70    80
                                       DURATION   OF  PELAGIC   STAGE  (DAYS)

                 Figure 2.--Comparison of the duration of the pelagic stages for species showing
                   different zoogeographic distributional patterns. Values on the abscissa are
                   adjusted (see text) to convert pre-transition increment counts to pelagic
                   duration. Open circles = means for species occurring in the Western and
                   Central Pacific only; solid triangles = species whose range includes the
                   Hawaiian Islands; solid squares = species distributed trans-Pacifically.  All
                   but one trans-Pacific species are found also in the Hawaiian Islands.

                                                           65

                                                                  ~~~~~~~~I

    The mean duration for trans-Pacific species is 62.2 days (S.D. = 11.4, N = 9).
    The difference between these and the Hawaiian-inclusive species is not significantW
    (p = 0.13; Kolmolgorov-Smirnov test, two-tailed), although the trend in the
    data is both evident and consistent with predictions made elsewhere in the
    literature (e.g., Rosenblatt and Walker, 1963). All but one trans-Pacific
    species also is found in Hawaii.

                                       DISCUSSION

         Our results suggest that a general correlation between long pelagic larval
    durations and broad geographic distributions is a valid assumption only when
    applied to a relatively few species with exceptionally long-lived pelagic stages
    (see also Thresher and Brothers, in press). In this respect, our conclusions
    are strikingly similar to those of Thorson (1961), who surveyed the pelagf
    durations and distributions of marine invertebrates. Thorson concluded
    only 20% of all bottom invertebrates with pelagic larvae have "true long-t~tance
    larvae." These he defined as those with a planktonic life longer than 6 weeks.
    Both of these figures are strikingly close to those we calculate for Indo-
    Pacific coral-reef fishes, i.e., a threshold value of about 45 days, with 20.7%
    of the species examined exceeding this value. The latter figure obviously
    could be manipulated by adding species with high or low pelagic durations. We
    strongly suspect, however, that this threshold value will remain robust as more
    data are added. It is premature to draw strong conclusions without additional,
    detailed work for other families of fishes and other phyla, but the surprisingly
    close quantitative agreement between the current study and Thorson (1961)
    suggests that some fundamental principle that applies across phyla may be
    involved.

         Our data are also in substantial agreement with suggestions that geographically
    isolated regions of the Indo-Pacific are colonized primarily by species with
    longer than average pelagic developmental stages. This point has previously
    been raised, particularly with respect to colonization of the Eastern Pacific
    Faunal Province by Indo-West Pacific species, both for marine invertebrates
    (e.g., Thorson, 1961; Dana, 1975; Zinsmeister and Emerson, 1979; Reaka, 1980)
    and coral-reef fishes (Briggs, 1961, 1974; Rosenblatt and Walker, 1963;
    Rosenblatt, 1967). Comparison of the minimum observed pelagic durations of
    species that occur in Hawaiian waters and in the Eastern Pacific with the large
    majority of species found only in the Central Pacific suggests that, although
    an element of chance certainly is involved, under normal circumstances the
    majority of Central Pacific species may not be capable of colonizing these
    outlying areas. Moreover, even for those species that have colonized the
    Eastern Pacific, such colonization may well be intermittent rather than
    continuous, and dependent on the occurrence of unusual oceanographic conditions.
    The minimum time required to cross, the "Eastern Pacific Faunal Barrier" (see
    Ekman, 1953) can be estimated from the distance between the likely source of
    colonists, the Line Islands, and the westernmost point of the Eastern Pacific
    faunal province, Clipperton Island, and peak reported values for the Equatorial
    Countercurrent, the presumed route of colonization (e.g., Leis, 1983; Reaka and
    Manning, 1980). The distance involved is approximately 5250 kin, and normal
    peak current velocities are in the range of 0.46 to 0.7 in sec-1 (Wyrtki, 1965;
    Tsuchiya, 1974). Consequently, normal transit time of the Eastern Pacific

                                           66

    Barrier by a passively drifting object will be at least 87 days; given that
    currents vary temporally and also decline as the near-shore environment is
    reached, a minimum estimate of 100 days is probably more realistic. Yet,
    apparent pelagic durations of nine trans-Pacific species examined range from 48
    to only 83 days, averaging 24.8 days less than a reasonable minimum. None of
    the 302 specimens we examined had a larval duration longer than 87 days,
    suggesting that, even if one includes individual variation in larval competance,
    few if any species are likely to cross the barrier under normal circumstances.
    Our tentative conclusion, therefore, is that such colonization takes place only
    during periods when the countercurrent is unusually strong, i.e., during El
    Nifo-type events (Wyrtki, 1965). If so, then we would predict that, following
    the recent very strong El Nino event in 1982-83 (see Gill and Rasmussen, 1983;
    Philander, 1983), unusually large numbers of new recruits of Indo-West Pacific
    species should be present on Eastern Pacific reefs.

                                    ACKNOWLEDGMENTS

         We thank A. Gronell and N. Wolf for discussions of this work as it
    progressed, W. N. McFarland for providing unpublished material for our examination,
    L. Bell, 0. Bellwood, P. L. Colon, G. Dingerkus, R. Greenfield, A. Gronell, J.
    T. Moyer, P. F. Sale, and D. Williams for providing specimens, and S. Blaber
    and J. Stevens for comments on an earlier version of this paper.

                                    LITERATURE CITED

    Allen, G. R. 1979. Butterfly and Angelfishes of the World, Vol. 2. Wiley,
       New York. 352 pp.

    Ayal, Y., and U. N. Safriel.  1982.  "R-curves and the Cost of the Planktonic
       Stage." Amer. Nat. 119:391-401.

    Barlow, G. W. 1981. "Patterns of Parental Investment, Dispersal and Size
       Among Coral-Reef Fishes." Environ. Biol. Fish. 6:65-85.

    Briggs, J. C. 1961. "The East Pacific Barrier and the Distribution of Shore
       Fishes." Evolution 15:545-554.

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                    DIURNAL PERIODICITY OF SPAWNING ACTIVITY BY
                THE HAMLET FISH, HYPOPLECTRUS GUTTAVARIUS (SERRANIDAE)

                                  Phillip S. Lobell
                        Center for Earth and Planetary Physics
                                  Harvard University
                               Cambridge, Massachusetts 02138

                                         and

                                   Steve Neudecker
                                   1301 Union Drive
                               Davis, California 95616

                                       ABSTRACT

         Many coral reef fishes spawn during the afternoon crepuscular period, a
    time of increased predatory activity by piscivores. We document the diel
    timing and spawning behavior of the hamlet fish, Hypoplectrus guttavarius, at
    St. Croix, U.S.V.I. This fish spawns daily during dusk in the water column
    above specific reef sites.

         The time of spawning relative to sunset was quantified at two sites at
    different depths. Spawning commenced earlier at the deep reef site and
    continued later at the shallow reef site. A field manipulation evaluated how
    this species responded to disburbances during reproduction. When scuba divers
    attempted to alter the fish's behavior by swimming vigorously toward mating
    pairs, the hamlets did not abort spawning. The pair responded (1) by continuing
    to spawn later into the night than those not disturbed and (2) by spawning
    progressively nearer the substratum.

                                     INTRODUCTION

         Until the 1970s, the reproductive behavior of most tropical coastal
    marine fishes eluded observation. This has changed recently with the discovery
    that many species spawn during restricted times of ebb tide, off-reef current
    flow, or crepuscular periods. A majority of coral reef fishes spawn eggs
    that are bouyant and are advected by ocean currents. Having planktonic
    propagules is thought to facilitate both rapid advection/dispersal in currents
    and reduced predation by other reef fishes (Johannes, 1978; Lobel, 1978;
    Barlow, 1981). In general, fishes seek out specific reef localities and/or
    pinnacles over which they ascend and spawn. This behavior is particularly
    interesting for fishes spawning shortly before and during dusk because
    crepuscular periods are generally believed to be times of increased predator
    activity and success (e.g., Hobson, 1968, 1972, 1974). Also, to witness

         1 Present affiliation: Woods Hole Oceanographic Institution, Woods Hole,
    Massachusetts 02543.

                                            71

    natural predation an spawning fishes or their eggs is not rare (Randall and
    Randall, 1963; Hobson, 1965; Moyer, 1974, 1975; Meyer, 1977; Colin, 1976,
    1978; Robertson and Hoffman, 1977; Jones, 1981; Robertson, 1983).  Some
    species gather in spawning aggregations and apparently are oblivious to human
    or natural piscivore predators even when disturbed or attacked (Johannes,
    1978, 1981; Robertson, 1983). In contrast, the mere presence of a diver-
    observer will interrupt the mating of some smaller species unless the fish
    are approached and observed with stealth (Johannes, 1978; Lobel, 1978).

         To date, studies on the reproductive behavior of tropical coastal marine
    fishes in the field have been primarily observational. The emphasis has been
    on documenting where, when, and how various species spawn. Herein we report
    the spawning behavior, diel timing, and a manipulation that attempted to
    disturb the behavior of a fish during reproduction. Our goal was to see
    whether and how the spawning behavior of the Caribbean hamlet, Hypoplectrus
    tuttavarius, might be altered. Because hamlets and many other fishes spawn
     uring the evening crepuscular period when predation by piscivores is most
    likely, we wanted to determine whether fish that were disturbed by scuba
    divers during the spawning act would cease all activity, move sites, depart
    and seek other mates, or merely continue despite the disturbance.

         The Caribbean hamlet, Hypoplectrus guttavarius (fig. 1) was selected for
    study because it maintained stable, identifiable pairs which spawned almost
    every evening at specific sites during February 1980, at St. Croix. It was
    common, easily observed, and the spawning act was unmistakable and easily
    quantified. The diel timing of spawning is compared with that of H. chlorurus,0
    H. nigricans, H. puella, and H. unicolor.

         The reproductive ecology of hamlets is somewhat enigmatic. It has been
    suggested that Hypoplectrus nigricans and other hamlets are simultaneous
    hermaphrodites, and that individuals alternate sexual roles between spawning
    clasps (Barlow, 1975; Fischer, 1980a, 1980b, 1981). It is also controversial
    whether different morphological varTants oT hamlets represent aggressive-
    mimetic morphs of the single species, Hypoplectrus unicolor, or are reproductively
    isolated incipient species (Thresher, 1978; Graves and Rosenblatt, 1980;
    Fischer, 1980b). Hamlets usually mate assortatively by color patterns,
    although mixed pairs have been observed, and individuals which exhibit color
    markings characteristic of two or more color forms are known (Barlow, 1975;
    Thresher, 1978; Graves and Rosenblatt, 1980; Fischer, 1980a). Thus, the
    reproductive behavior of hamlets is interesting from several perspectives.
    To maintain simplicity and clarity, we refer to the various hamlets by their
    established species names (cf. Randall, 1968).

                                     STUDY SITES

         Fish were examined at two locations on St. Croix, U.S. Virgin Islands
    (64035'W, 17045'N). The first site was the east slope of Salt River canyon
    within the excursion limits of the NOAA National Undersea Laboratory System
    habitat (HYDROLAB). Since we were saturated, we spent approximately 53 hours
    per person observing fish at 20-30 m depths from February 11 to 15, 1980.
    The second site was located on several patch reefs at about 10 m depths in

                                             72

       Figure 1.--Adult Hypoplectrus guttavarius (the shy hamlet) approximately
                                   11 cm in length.

    the Buck Island Channel outside Teague Bay Reef on the northeast coast of St.
    Croix. Observations were made from February 20 to March 3, 1980. Further
    site descriptions are given by Neudecker and Lobel, 1982.

                                       METHODS

         Specific pairs of H. guttavarius were identified and details of their
    spawninq nehavior were recorded before, during, and after the manipulation.
    Observers selected one pair each evening and positioned themselves unobtrusively
    on site at least 15 min before the fish initiated courtship. The baseline
    spawning behavior of each pair was determined during one or two evenings
    prior to the disturbance manipulation (3 of 7 pairs were observed for 2
    consecutive days before the manipulations; the other 4 pairs were observed
    the day before the manipulations). In cases where sites lacked distinguishing
    natural features, the specific site at which each pair spawned was marked
    with small floats. We spent several days diving at all hours, including
    sunrise, and saw hamlets spawn only during dusk (total observation 158.7 man-
    hours during the 7 days in HYDROLAB). Data recorded each time a pair spawned
    included the time, height in the water relative to the bottom and the
    coral/gorgonian structure over which spawning took place, approximate distance
    moved between spawning sites, and general notes on the pair's response to
    observers and other species.

                                            73

       Figure 2.--A pair of Hypoplectrus guttavarius engaged in courtship at a
         typical spawning site (Deep Reef at East Wall of Salt River Canyon,
         HYDROLAB site).

         The disturbance manipulations were conducted the day after baseline
    spawning behavior was determined.  The manipulation was to disrupt the spawning
    act each time the fish attempted it. As the pair began to enter the spawning
    clasp, the observer swam rapidly toward the pair (in an attempt to mimic a
    predator's behavior). The pair was harassed repeatedly this way for as long
    as spawning was attempted. When mates parted, close watch was maintained
    unt~' it was certain that spawning had ceased for the night. Occasionally, a
    pair qould separate, swim several meters apart, return several minutes later,
    reloin and attempt to spawn again. Follow-up observations were made on the
    sarme pair the day after the manipulation. Data analysis of treatments used
    tne nonparametric Mann-Whitney U test statistic.

         On any given day, at least three diver/observers were engaged in various
    phases of the manipulation. To provide control observations, a diver watched
    a spawning pair without interfering while other divers were either harassing
    a spawning pair or conducting follow-up observations.

                                           74

      Figure 3.--Hypoplectrus guttavarius embraced in the spawning clasp. The
                  individual facing head-down has bent body in an S-shape.

                                      RESULTS

    Typical Spawning Behavior

        Our observations provided the following general picture of spawning in
    H. guttavarius. Hamlets mate only in pairs. Fertilization is external and
    zygotes are planktonic. During the daytime, mates appear loosely associated
    in adjacent or nearby home ranges. They begin to interact within 2 hr
    of sunset. They first rendezvous, remain close together, and engage in
    occasional short chases. The spawning act begins when one fish presents a
    late-al display while flicking its pelvic fins (fig. 2). The displaying
    ind`iicual slowly rises while continuing its display.  The bright blue flank
    of this individual fades to a pastel shade. The other fish follows. The two
    then rise together about I m above some towering reef structure. At St.
    Croix, tnese structures were vertical colonies of the gorgonian, Pseudoplexaura
    sp., or the coral, Acropora cervicornis.

         Once the proper height (about 1-2 m) is attained over a tall reef
    structure, the following fish folds around the pale colored leader, who poses
    head down in an S-shaped position (fig. 3). Release of eggs and sperm occurs

                                           75

    Figure 4.--Hypoplectrus guttavarius embraced in the spawning clasp.  The
               individual folded around the other one facing head-down opens its
              mouth while quivering and spawning.

    as both fish quiver. Quivering lasts for 2-3 sec. The individual folded
    around the other often opens its mouth while quivering (fig. 4). Following
    consummation, the fish cease embracing and quickly descend to the bottom.
    The embracing behavior of hamlets when spawning has been termed the spawning
    clasp (Fischer, 1980a) and occurs many times throughout an evening. Infrequently,
    fish would embrace but not quiver, and the release of gametes was not evident.
    Cisc-e-  1980a) has described the similar spawning behavior and sexual role of
    ~. -2ricans.

         :ach pair of hamlets initiated spawning at a specific reef location each
    -enen5.  Pairs showed strong spawning site specificity.  They moved between
    aew f'from 1 to 4) particular sites each evening, and frequently a pair
    -eor-ed to their original site.  When some pairs moved between spawning
    sies, other individuals occasionally interfered and attempted to steal a
    -ate.  These 'floater' individuals were seldom successful.  Out of all namlet
    spawnings observed (N = 314 of 5 spp.), only once was a floater successful in
    stealing a mate by breaking up an existing pair (the pair and floater species
    was H. unicolor).

                                            76

        25-  SHALLOW REEF  Full Moon
        20-    (approx. lO m depth)
    a.

            25DEEP REEF NAew Moor)
        20"  (pprox. 25m depth)
    'C

     ._ 10'-CS
    z

    {

        iU            0 3       3 25   20   15   10    5  5  5Moon                     20

                                                     SUNSET
                 TIME BEFORE AND AFTER SUNSET(minutes)

    Figure s.--oiel reproductive timing of Hypoplectrus guttavarius at two depths.
       "The sha llow site (10 m depth)            was occupied during the full moon

              phase (Feb. 24-27, 1980), while the deep site (22-30 m depth) was
              occupied during the new moon (Feb. 11-13, 1980). The shallow
              group consisted of 4 pairs observed over 4 days for a total of 67
              spawning clasps. The deep group consisted of 7 pairs observed
       i0-

              over 4 days for a total of 210 spawning clasps. Time is in minutes
                  45   4    35 $0   25   20   15   10    5   �        5    10   15   20
                                                     SUNSET
                 TIME BEFORE AND AFTER SUNSET(minutes)

      beFigure 5.--and after sunset. Seive timing of Hypoplectr discuusi at two depths.

                                        77
              The shallow site (10 m depth) was occupied during the full moon
              phase (Feb. 24-27, 1980), while the deep site (22-30 m depth) was
              occupied during the new moon (Feb. 11-13, 1980). The shallow
              group consisted of 4 pairs observed over 4 days for a total of 67
              spawning clasps. The deep group consisted of 7 pairs observed
              over 4 days for a total of 210 spawning clasps. Time is in minutes
              before and after sunset. See text for discussion.

                                        77

    2"el ~eproductive 'imin
         Hypoplectrus guttavarius spawned almost every evening during the study
    eriod.Fish were studied at two sites which differed in depth. The deep eef
    site (20-30 m depth) was occupied by us February 11-15, and the shallow site
    tI0 m depth) from February 20-March 3.  We did not see hamlets spawn on two
    evenings, February 21-22. Observations at the deep site corresponded to the
    presence of a new moon (February 15). We were at the shallow site during the
    full moon (March 1). The dates on which hamlets were not seen spawning
    coincided with the last quarter moon phase (February 22).

         The diel timing of reproduction, relative to sunset, differed for H.
    guttavarius at the two sites (depths) and lunar phases. The first spawnengs
    at the deep reef site began 50 min before sunset (with a mean, X, and stancard
    deviation, S.D., of 33 + 1 min) and the last spawnings ended 10 min (X + S.. =
    2 + 9 min) after sunset; most spawnings occurred just prior to sunset.  Spawning
    at the shallow reef site commenced later, 25 min (X + S.D. = 16 + 7 min) oefore
    sunset, and ended later, 20 min (X + S.D.-= 3 + 6 min) after sunset; here most
    spawnings occurred just past sunset (fig. 5). Reproduction by fish at tne
    two sites did not differ in any other aspect.

         We did not observe any strong lunar periodicity in the daily spawning
    behavior of H. guttavarius. However, our data do not allow distinguishing
    between the possible effects of 1) different phases of the moon during the
    times that each group was observed vs. 2) the difference in depth and
    corresponding changes in light levels during dusk.

    Effects of Disturbance on Spawning Behavior

         All H. guttavarius persisted in spawning in spite of overt and constant
    harassment. Harassed pairs attempted twice as many spawning clasps and
    continued for about 25 min later than nonharassed (day before and day after)
    pairs (tables 1, 2). However, the frequency of spawning clasps attempted per
    5 min remained the same (about 2 + 1 clasps; tables lb, 2b). The number of
    times a pair changed spawning sites relative to the number of spawning clasps
    also did not vary significantly (tables lc, 2c). One particularly striking
    effect of disturbance on these spawning fish was that, as spawning was
    continuously disrupted, a pair attempted to spawn progressively nearer the
    substratum (based on our qualitative observations). At the end of the
    disturbance period, several pairs were trying to spawn next to the bottom
    while hidden among coral/gorgonian branches. This result simply may indicate
     tnat once ovulation has begun, the fish must spawn.

          Overall, the fish persisted in spawning despite the aggressive behavior
     of the scuba divers. However, we have no estimate of the fate of zygotes
     when released next to the bottom and in between coral/gorgonian branches as
     compared to those normally dispersed about a meter above reef structures.
     The experience of the disturbance had no apparent lasting effects on the
     fish. The fish's behavior did not differ markedly on the day after compared
     to the day before the disturbance (tables 1, 2).

                                              78

    Table l.--Effect of disturbance on the spawning behavior of Hypoplectrus guttavarius.  Data for shallow anid deep
      water groups were pooled except when related to sunset time.  In addition to the above changes, whorl Fish were
      disturbed, they would attempt to spawn closer to the substrate until they were on the bottom. Notations in last
      rows (e, f) indicate before (-) or after (+) sunset.

                                       Baseline before disturbed            During disturbance            Day after disturbed
                                       (7 pairs;  10 observations)      (6 pairs; 6 observations)    (5 pairs; 5 observations)

    a. X + S.D. (range) no. spawning
        clasps per pair                        12 + 3 (7 to 16)              25 t 9 (10 to 33)               12 t 2 (9 to 15)

    b. X � S.D. (range) no. spawning
        clasps per 5 min                        2 � 1(0.6 to 3.6)             2 + 1 (1.5 to 3.1)              2 � 1 (1.5 to 3.2)

    c.  X + S.D. (range) ratio of
        no. moves pair made between
        spawning sites to total no.
        spawning clasps                     0.23 � 0.16 (0 to 0.5)        0.48 � 0.30 (0.06 to 0.86)  0.26 t 0.19 (0 to 0.46)

    d. X t S.D. min. (range) duration
        of spawning period per day             31 + 8 (11 to 91)             57 + 21 (33 to 69)             28 + 8 (21 to 38)

    e.  Time (X, range) relative to sunset that spawning commenced (min)

        shallow group (full moon)          -16 (-22 to  -6) (N = 4)   -24 (-44 to  -8) (N = 3)    -11 (-19 to  -2) (N = 3)
        deep group (new moon)              -33 (-50 to -19) (N = 6)   -50 (-71 to -35) (N = 3)    -40 (-44 to -35) (N = 2)

    f.  Time (X, range) relative to sunset that spawning ceased (min)

        shallow group (full moon)          +13 (+ 5 to +18) (N = 4)   +30 (+20 to +38) (N = 3)    t12 (f 2 to +24) (N = 3)
        deep group (new moon)              - 2 (-19 to + 5) (N = 6)   +10 (- 2 to +21) (N = 3)    -   (- 6 to - 1) (N = 2)

      Table 2.--Statistical comparison of data from table 1. Values listed are
        calculated values of Z using the Mann-Whitney U test.  Values marked by *
        are statistically different at p = 0.05 (critical value for Z   1.960.)

                                           Before vs.       After vs.       Before vs.
                                             During          During            After
                                           Disturbance    Disturbance       Disturbance

    a.  No. spawning clasps per pair            *2.490          *2.008            0.245

    b.  No. spawning clasps per pair
          per 5 min.                             1.844          0.548             1.347

    c.  No. moves pair made between
          spawning sites per total
          no. sPawning clasps                    1.627           1.278            0.367

    d.  Duration of spawning period             *2.169          *2.373            0.857

    Spawning of Other Hamlets

         Four other hamlets also were observed spawning at the shallow reef site:
    H. puella, H. unicolor, H. chlorurus, and H. nigricans.  We did not see mixed _
    mating among hamlets.  Data contrasting aspects of reproduction in these            W
    fishes and of H. guttavarius are presented in table 3. However, the data set
    lacks sufficient detail to allow more than a general indication of how the
    pattern and timing of reproduction might vary among congeners of hamlets.

                                      DISCUSSION

         Many diurnal tropical marine fishes that remain active during the evening
    crepuscular period may risk being eated by piscivores, whose feeding activities
    generally are believed to increase at this time (Hobson, 1968, 1972, 1974;
    Domm and Domm, 1973; Major, 1977). This increased threat of predation is
    reflected in the potential prey's behavior, and most species retreat to
    shelter, aggregate, or forage closer to the reef (Hobson, 19783, 1978;
    Robertson and Sheldon, 1979). However, many species also periodically spawn
    during dusk (e.g., Randall, 1961; Lobel, 1978; Moyer and Nakazano, 1978;
    Moyer, 1979; Moyer and Zaiser, 1981; Zaiser and Moyer, 1981; Neudecker and
    Lobel, 1982; Moyer, et al., 1983). Spawning during the evening crepuscular
    period is thought to reduce the likelihood of predation on planktonic eggs,
    since most planktivorous fishes that select such small prey are inactive by
    this time. It is noteworthy that the eggs of nestbuilding, demersal-spawning
    balistid and pomacentrid fishes hatch after dark, whereupon the larvae become
    planktonic (Allen, 1972; Moyer and Bell, 1976; Ross, 1978; Fricke, 1980;
    Lobel and Johannes, 1980; Doherty, 1983). Diurnal planktivores consume
    smaller prey, including eggs, than nocturnal planktivores which infrequently

                                            80

    Table 3.--Reproductive behavior by other hamlets (Hypoplectrus spp.).  These fish were observed at 25-30 ft.
      depth, February 25-March 2, 1980.  For H. nigricans (*), see Fischer, 1980, for comprehensive spawning data.

                                                H. puella         H. unicolor         H. chlorurus          H. nigricans*
                                               (N  - 2 pairs)     (N = 2 pairs)       (N = 2 pairs)          TN = 1 pair)

    X (range) no. spawning clasps per day        10 (8-12)           12 (6-17)          17 (16-18)                 27

    X (range) no. spawning clasps per 5 min.    3 (3-4)               2 (2-2)            2 (-2-2)                   1

    X (range) no. moves pair made between
      spawning sites per 10 spawns                5 (4-6)             7 (7-7)            7 (7-7)                    7

    X (range) min. duration of spawning
      per day                                    15 (14-16)         27 (16-38)          42 (38-45)                101

    Minutes before sunset that spawning
      commenced                                   5 + 6               13 + 16            28 + 39                  87

    Minutes after sunset that spawning
       ceased                                      8 + 11              1 + 24              8 + 11                   14

    eat eggs (Hobson and Chess, 1978). Most egg-eating fishes cease foraging as *
    light levels diminish, since low light levels make visual orientation difficultW
    and also predation by piscine predators generally increases at this time
    (Hobson, 1972, 1974: Hobson and Chess, 1978). Additionally, any planktivores
    still actively feeding through dusk may be quickly satiated by the simultaneous
    spawning of many fishes.

         Spawning during dusk may reduce mortality of fish eggs by predation, but
    it also may increase the potential risk of predation for adult fishes. Hobson
    (1968, 1972, 1974, 1978; Hobson, et al., 1981) has documented extensive
    evidence suggesting increased predation by fish predators on tropical reef
    fishes exposed or otherwise vulnerable during the crepuscular periods. Fishes
    also are thought to be more vulnerable to predation when preoccupied with
    mating (Johannes, 1978, 1981; Robertson, 1983). Furthermore, it must be
    noted that there are many fishes, particularly labrids and scarids, which
    spawn throughout the day, appearing more in phase with tidal currents than
    crepuscular periods (Barlow, 1981; Kuwamura, 1981; Robertson, 1983).

         In this study, we wanted to evaluate how a fish would alter its mating
    pattern when disturbed or attacked. The results might then provide some insight
    into the selective pressures molding the reproductive tactics of coastal marine
    species in the tropics. At the time, the best arrangement we could devise to
    test the possible effect of predation was by simulating predator behavior using
    scuba divers. Other studies also have considered a fish's response to a human
    diver as indicative of reaction to a piscine predator (e.g., Coates, 1980).
    Nevertheless, results of this manipulation should be related only tenuously to
    how the hamlet might respond to a fish predator. A fish predator probably
    would not continue to attack the same prey throughout dusk.

         The hamlet, Hypoplectrus guttavarius, altered its normal mating behavior
    when harassed by 1) attempting more clasps longer into the night and 2) spawning
    progressively nearer to the bottom in and among shelter. In no case was spawning
    terminated early; in fact, the opposite occurred, and fish prolonged spawning
    attempts. This result simply may indicate that once ovulation has begun, the
    fish must spawn. The spawning sites were all reef structures (gorgonian and
    coral) taller than the surrounding terrain. Only after a pair had shifted
    sites repeatedly did they commence spawning nearer the bottom or in shelter.
    Difference in survivorship of the free-floating zygotes when released high
    above the reef vs. near the bottom was not determinable. Fish which were
    attacked and harassed one day showed no indication of lasting behavioral affects
    the next day.

         The importance attributed to spawning above a tall reef structure is that
    it provides a degree of safety for the adults. It allows the fish to mate
    relatively high in the water column while remaining as close as possible to
    shelter. Spawning high in the water places the free-floating eggs beyond the
    grasp of benthic planktivores and in a position most favorable to advection by
    currents.

         Hobson (1972, 1974) has suggested that the well defined twilight activities
    of tropical reef fishes have been shaped by the threat of crepuscular predators
     (Hobson, et al., 1981).  If this hypothesis is correct, then it would seem that

                                             82

    fishes spawning during evening crepuscular periods have not been overtly deterred
    by the potential threat of predation. Alternatively, the adaptive pressures
    favoring zygote survival may have been more influential in molding the diel
    timing of reproduction than factors affecting survival of the parents (e.g.,
    predation) while spawning during the evening crepuscular period.

                                    ACKNOWLEDGMENTS

         We are grateful for the stimulating conversation and help received from
    our fellow aquanaut, William Hamilton III, both underwater and topside. The
    study was made possible by the tireless support of the HYDROLAB personnel, Bill
    and Joan Schane, Barry Walden, Rod Catanach, and Joe Langersdorf, and support
    divers, Scott Grace and Don Morris. Valerie Paul, Stacy Tighe, and Nancy Wolf
    greatly aided in the field observations. We also received generous support
    from the West Indies Laboratory, for which we are grateful. We thank Marjorie
    Reaka and William McFarland for their thoughtful reviews of this paper. This
    research was funded by a NOAA HYDROLAB (NULS 80-1) grant to S. Neudecker and by
    an OPER grant from the Institute of Ecology, University of California at Davis,
    to William Hamilton, S. Neudecker, and P. Ward.

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    Barlow, G. W.  1981.  "Patterns of Parental Investment, Dispersal and Size
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    Kuwamura, T.  1981.  "Diurnal Periodicity of Spawning Activity in Free-Spawning
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    Lobel, P. S.  1978.  "Diel, Lunar and Seasonal Periodicity in the Reproductive
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                                             85

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                                            86

                       PATTERNS OF REPRODUCTION IN SMALL JAMAICAN
                    BRITTLE STARS: FISSION AND BROODING PREDOMINATE

                                    Roland H. Emson1
                                 Department of Zoology
                          King's College, University of London
                            London, WC2R 2LS United Kingdom

                                   Philip V. Mladenov
                                   Biology Department
                                Mount Allison University
                       Sackville, New Brunswick, EOA 3C0 Canada

                                     lain C. Wilkie
                           Department of Biological Sciences
                             Glasgow College of Technology
                            Glasgow, G4 OBA United Kingdom

                                        ABSTRACT

         Brittle stars were collected from coralline algae and from an adjacent
    turtle grass bed in the back reef lagoon at Discovery Bay, Jamaica.  Fissiparous
    species are numerically predominant in both habitats. These species, although
    systematically diverse, share strikingly similar life history characteristics,
    including small adult size (< 4.5 mm disc diameter), low fecundity, yet probable
    planktotrophic development and asexual propagation. Brooding species are also
    well represented. They too are small in adult size (< 4.0 mm disc diameter)
    but are hermaphroditic direct developers, brooding small numbers of young in the
    bursae. There appears to be selection for small adult size in brittle stars in
    the habitats studied here. Small size in turn is correlated with modified
    reproductive patterns like fissiparity and brooding. The relative importance
    of these patterns in reef habitats is considered and the frequency and geographic
    distribution of fissiparity and brooding in brittle stars briefly discussed.

                                      INTRODUCTION

         Coral reefs present many microhabitats which may provide refuges from the
    pressures of predation generally considered to exist on open surfaces in such
    areas. Coralline algae, sponges, and coral boulder scree all offer cryptic
    spaces exploitable by certain species. Such crevices potentially provide both
    a refuge for juveniles of large species and a habitat in which small species
    can complete their entire life history.

         During studies on the reproductive biology of the small fissiparous brittle
    star Ophiocomella ophiactoides (H. L. Clark) at Discovery Bay, Jamaica, W.I.
    (Mladenov, et al., 1983; Mladenov and Emson, 1984), we became aware that in the

         1 Contribution number 343 of the Discovery Bay Marine Laboratory of the
    University of the West Indies.

                                             87

    coralline algal habitat occupied by 0. ophiactoides and adjacent turtle grass,
    a number of other small brittle stars were present, some in abundance. Of
    these species, some showed evidence of fissiparity; others, however, were
    nonfissiparous brooding species which nevertheless shared certain characteristics
    with the fissiparous forms. In this paper, we present data on the relative
    abundance of brittle stars in these microhabitats, briefly review some of the
    life history characteristics of these brittle stars, discuss the similarities
    and differences between them, speculate on the reasons for the abundance of
    small brittle stars in these habitats, and comment on the association of small
    size with fissiparity and brooding in brittle stars.

                                STUDY SITES AND METHODS

         The study sites consisted of (1) a shallow, sheltered cove (known locally
    as Maze Cove or the Blue Maze) located in a part of the back reef just west of
    the dive locker of the Discovery Bay.Marine Laboratory, Jamaica, and (2) a
    closely adjacent bed of turtle grass.

         The rocky walls of the cove are covered with a deep carpet of coralline
    and other red algae in which Amphiroa rigida and A. fragillisima are most
    prominent.  These algae are a l   Cdoark     incolor and,-except at the bases of the
    fronds, relatively free of detritus. During August 1981 and July 1984, clumps
    of algae were carefully transferred to polythene bags underwater, removed to
    the laboratory, and searched for brittle stars and other fauna. The brittle
    stars were identified, examined for evidence of cross-disc division (three long
    arms and three shorter regenerating arms on the disc), counted, and measured
    (the parameters noted were the greatest dimension of the disc and, in the case
    of the fissiparous species, the length of the arms). The sexual condition of
    the animals was later examined by dissection. In the case of Ophiocomella
    ophiactoides, egg size was obtained by measuring the diameter of spawned,
    fertilized eggs. For the other species studied, the diameter of the largest
    oocytes present in histological sections of ripe females was measured. For
    estimation of total egg number, the ovaries were removed, blotted free of excess
    moisture, and weighed. A small fraction was then separated, weighed, and the
    number of eggs counted. Total egg number was obtained by multiplication.

         The site adjacent to the cove has a sand and silt substratum that supports
    an abundance of turtle grass, Thalassia testudinum, as well as a variety of
    algae.  The bases of the Thalassia are uniformly pale, due to attached detritus
    and the presence of dead decaying leaf bases on the outsides of the plants.
    Detritus is abundant around and between the plants. Thalassia shoots were
    pulled from the substratum and placed in polythene bags underwater along with
    samples of the surface of the substratum from immediately around the base of
    the plants. This material subsequently was treated similarly to that obtained
    from the algal clumps.

                                        RESULTS

    The Species and Their General Characteristics

         The brittle stars found in the algal turf are listed in table 1A.. This
    table also shows their relative abundances in these microhabitats and gives

                                             88

         Table 1.--Characteristics of the brittle stars from two adjacent habitats at Discovery Bay, Jamaica, in 1981.
           A.  Coralline algal turf (N = 195); B.  Thalassia bed (N = 75).  Algal volume 1.5 1.  Thalassia volume approxi-
           mately 6 1.
                                                   Relative           Maximum                              Mode of
        Species                  Family            Abundance          disc size    Appearance             Reproduction
                                               (% of specimens         (mm)
                                                 in sample)

    A.  Ophiocomella        Ophiocomidae              69                 4.5        Dark green,      Fissiparous and broadcasts
        o-phi-actoides                                                              arms banded      planktotrophic larvae
                                                                                                   (Mladenov, et al., 1983;
                                                                                                  Mladenov an-Em-son, 1984)

        Amphipholis        Amphiuridae                21                 3.0       Brown disc,       Brooder (Fell, 1946)
    o   squamata                                                                    arms paler
                                                                                  and often
                                                                                  banded

        Ophiactis          Ophiactidae                 9                 3.0       Brown or         Fissiparous and broadcasts
        savignyi                                                                   mottled disc,   larvae; probably plankto-
                                                                                  banded brown    trophic (Mortensen, 1931)
                                                                                  and white arms

        Ophiostigma        Amphiuridae                 1                 4.0       Sand colored    Fissiparous; mode of sexual
        isacanthum                                                                                  reproduction unknown

    Table 1.--Continued

                                                    Relative           Maximum                               Mode of
        Species                  Family             Abundance          disc size    Appearance              Reproduction
                                                (% of specimens         (mm)
                                                  in sample)

    B.  Ophiostigma          Amphiuridae               52                  4.0        As in A above   As in A above
        isacanthum

        Ophiolepis          Ophiolepidae               21                 4.0        Sand colored    Brooder (Hendler, 1979)
        pauci spina

        Amphipholis         Amphiuridae                15                  3.0        As in A above   As in A above
        squamata

        Ophiocomella        Ophiocomidae                5                  4.5       As in A above   As in A above
        ophiactoides

        Ophioderma          Ophiodermatidae             4                 4.5        Sand colored    Only juveniles in this habi-
        cinereum                                                                                       tat.  Mode of reproduction
                                                                                                     unknown.

        Ophiactis           Ophiactidae                 1                 3.0        As in A above   As in A above
        savignyi

        Ophiothrix          Ophiothricidae              1                                  -           Only juveniles in this habi-
        oerstedi                                                                                       tat.  Adults broadcast
                                                                                                    lecithotrophic larvae
                                                                                                     (Mladenov, 1979)

     Table 2.--Relative abundance (% of specimens) in samples from the coralline
               algal turf habitat in 1984.  * = all juveniles with disc diameter
               less than 5 cm.

                                        A               B            C            D

    Total number recovered             N = 115        N = 164        N = 50       N = 183

    Algal volume (ml)                   1,505           1,390           345        1,260

    Ophiocomella ophiactoides           76.5            61.0             58        75.4

    Amphipholis squamata                10.4            12.2             34        14.2

    Amphiura stimpsoni                   5.2            16.4              2         9.9

    Ophiactis savignyi                   3.4             3.0             0           0

    Ophiostigma isacanthum               0.9             5.5            4.4          0

    Ophiactis algicola                    -              0.6              2         0.5

    Ophiocoma pumila*                    0.9

    Ophiothrix oerstedi*                 0.9

    Ophioderma appressum*                1.8             0.6

    Ophiolepis paucispina                 -              0.6

    details of their sizes, appearances, and reproductive modes. Of the four
    species present in 1981, Ophiocomella ophiactoides was the most abundant and
    Ophiostigma isacanthum, the least. Further samples from this habitat in 1984
    (table 2) show that the pattern is consistent over time, although in these
    later samples rather more occasional species were taken and Amphiura stimpsoni
    was moderately abundant. Four of the six most common species (0. ophiactoides,
    Ophiactis savignyi, Ophiactis algicola, and 0. isacanthum) in the latter
    collections are fissiparous, able to reproduce asexually by cross-disc division,
    and two (Amphipholis squamata and A. stimpsoni) are brooders. The fissiparous
    species are members of three different families (Ophiocomidae, Ophiactidae,
    Amphiuridae). The species represented as juveniles may be found in abundance
    as adults elsewhere in Discovery Bay.

         A rather similar group of species of brittle stars was found in the samples
    taken (in 1981 only) from the detritus surrounding the Thalassia testudinum
    shoots and, to a small extent, the axils of Thalassia leaves (table IB). Of
    the seven species found, all except Ophioderma cinereum were also in the algal
    turf. However, the relative abundances of these species are very different in

                                             91

    the two habitats, since 0. isacanthum, Ophiolepis paucispina, and A. squamata
    are the prominent species in this habitat.  Only A. squamata achieves a similar
    abundance in both habitats, and fissiparous species are numerically predominant
    in both habitats.

         Two features were common to all the species in these habitats. One is
    small body size.  No species exceeds 4.5 mm maximum disc di-ameter, and most
    species are smaller than this. All species except 0. cinereum and Ophiothrix
    oerstedi included reproductively active adult indivTiuals.  The second feature
    common to these species is the color pattern of the brittle stars. All are
    very difficult to see in the natural habitat because of their size and because
    the coloration of the animals renders them cryptic; the banded arms of several
    species are particularly concealing. Even when the algae were dissected in the
    laboratory, many brittle stars were detected only when they moved. Furthermore,
    for those residing in coralline algae, the arms were similar in diameter to the
    algal strands. It was noticeable that other fauna found within the algal
    clumps, notably the small (2-5 cm) holothuroid Synaptula hydriformis and some
    unidentified amphipods, also were cryptically patterned. A dark green with
    paler blotches, S. hydriformis is very similar to 0. ophiactoides in color.

    Asexual Reproduction in the Fissiparous Species

         The overall percentage of individuals showing evidence of fission in each
    of the three common fissiparous species is very high (table 3) and is clearly
    an important means of population increase in all three. This similarity is
    only one of several that can be discerned. For instance, the range of disc
    size was very similar (table 3), and the size frequency histograms (fig. 1)
    were virtually identical in pattern, each population being dominated by
    individuals with disc diameters of 1.0-2.5 mm. Few animals of larger disc size
    were evident, and very small animals also were missing. Data were available
    only for August 1981 and July 1984 for 0. savignyi and 0. isacanthum, but for
    0. ophiactoides data were also available-for June, July,-and December of 1981
    TMladenov, et al., 1983) and July of 1984; the size frequency patterns were
    identical at all times. No evidence of larval recruitment was apparent in that
    species at any time. While it remains possible that larval recruitment occurred
    in intervening months, we suspect that the populations of all three species
    are, at these sites, maintained almost solely by asexual reproduction.

         Another similarity between the species is in the relationship between disc
    size and evidence of recent fission. Table 4 shows the proportion of animals
    with different disc sizes found in each of four regeneration categories. In
    all three species, there is a clear trend: most small animals show evidence of
    recent splitting (i.e., a low ratio for length of short/long arms), while a
    high proportion of large animals do not.

    Sexual Reproduction in the Fissiparous Species

         Larger individuals in all three fissiparous species may contain mature
    functional gonads (table 3 and below). Mladenov and Emson (1984) already have
    reported that 0. ophiactoides with disc diameters greater than 2.2 mm can

                                             92

    Table 3.--Some features of fissiparous brittle stars from Discovery Bay, Jamaica. 1 = Diameter of spawned
                              fertilized eggs; 2 = largest oocytes present in mature females.

                                          % fission                                                   Egg number
                           Range of     apparent in      Minimum disc size                            of largest
    Species                 disc size    population       of mature females       Egg diameter      specimen sampled
                              (mm)

    Ophiocomella             1.0-4.5          90                2.2 mm               0.08 mmI             7,400
    ophiactoides
      (N = 359)

    Ophiostigma              1.0-4.0          80                3.3 mm               0.12 mm2             5,000
    isacanthum
      (N = 56)

    Ophiactis                1.0-3.0          67          None of the specimens
    savignyi-                                             contained gonads
      (N = 65)

      60.

      SO.

          ~40        ~Ophlocomella                 Ophiostigma                Ophiactis
      40.
                         n=359                       n=56                     n=65
       30

      20

      10

           .6    1.6   2-6   36          6    1'6   2.6   3'6      .6    16    2.6  3-6

                                              SIZE(mm)

    Figure 1.--Size frequency distributions of discs of the three fissiparous
                    brittle stars at Discovery Bay (August 1981).

    contain ripe gonads, and of 246 animals with disc diameters greater than 2.0
    mm, 57 were female (23%). Of the 56 specimens of 0. isacanthum examined during
    this study, 11 with disc diameters greater than 2.7-mm had recognizable
    gonads. Of the 11, 2 with disc diameters of 3.6 and 3.3 mm were mature
    females, 3 with disc diameters of 3.5 and 2.8 mm were mature males, and the
    remaining 6 were unsexable. None of the 0. savignyi examined from the
    Discovery Bay sites contained gonads (table 3), but Emson and Wilkie (1984)
    have shown that at the Bogue Islands in Montego Bay on the Jamaican north
    coast, 0. savignyi achieved a larger size (up to 5.5 mm) and specimens with
    disc diameters greater than 4.0 mm may contain ripe ova and achieve successful
    sexual reproduction. The largest oocytes in these specimens measured 0.10 mm
    in diameter, and the largest individual (5.5 mm disc diameter) contained
    roughly 10,000 eggs.

         The three fissiparous species are similar in producing small eggs within
    the size range (0.07-0.20 mm) regarded as resulting in planktotrophic larvae
    (Hendler, 1975; Mladenov, 1979).

         Since disc size and egg size are similar in the three species, it is not
    surprising that reproductive output, as measured by maximum number of eggs
    produced, is roughly equivalent (table 3). The maximum egg number for these
    species is two to three orders of magnitude lower than that recorded for nonfis-
    siparous brittle stars with planktotrophic development (Hendler, 1975; Mladenov,
    1979; Mladenov and Emson, 1984). Compared to their nonfissiparous planktotrophic

                                            94

        Table 4.--Comparison of the regeneration patterns of the three fissiparous brittle stars found at Discovery Bay,
            Jamaica. Regeneration category refers to the ratio of length of short arms to length of long arms. Data are
            given as percent of all individuals with a given disc diameter.

                                      Ophiocomella
         Species                       ophiactoides                     Ophiactis savignyi              Ophiostigma isacanthum
                                         (N = 359)                           (N = 65)                          (N= 56)
         Regeneration
    to   category (%)            0-25   26-50   51-75   75+          0-25   26-50   51-75   75+        0-25   26-50   51-75   75+

                        0-0.5     0        0        0     0            0       0        0      0         0       0        0      0
           Disc      0.6-1.0    63        37        0      0         42       12       21    25         75       0        0    25
         Diameter    1.1-1.5    55         28      14      3          21       35      13    31         53       18      19    10
           (mm)      1.6-2.0    51        28       17     4           0        0       33    67        20       20       27    33
                      2.1-2.5    45       16       26    13            0       0        0   100         40       0       20    40
                      2.6-3.0    14       42       15    29                                              0       0        0      0
                      3.1-3.5     0       28       14    58                                             0        0        0   100
                      3.6-4.0      0       0        0   100                                              0       0        0     0
                      4.1-4.5      0       0        0   100

    counterparts, therefore, these fissiparous brittle stars broadcast exceedingly
    small numbers of larvae at each spawning, with important potential consequences
    for recruitment. Even if these species spawned 10 times a year, their output
    would be low. As only a small proportion of the population is sexually
    mature, the output of larvae must be very small.

         The three nonfissiparous species present as adults (A. squamata, A.
    stimpsoni, and 0. paucispina) share similar reproductive methods. They are
    hermaphroditic s-pecies which produce a small number of relatively large yolky
    eggs. These are brooded within the genital bursae and released, quite possibly
    throughout the year, as competent juveniles (although Hendler, 1975, and
    Emson, unpub. obs., have noted that release is reduced at some seasons).

    Observations of Potential Predators

         Many species of fishes live in the water adjacent to the algal carpets.
    During our collections, fish were observed picking at the surface of the
    algae on several occasions. Blue Tangs (Acanthurus coeruleus), Surgeon Fish
    (Acanthurus chirurgus), and, in particular, Slippery Dicks (Halichoeres
    bivittatus) were observed darting at and pushing into the algal clumps. The
    latter species is known to eat invertebrates (Randall, 1967).

                                      DISCUSSION

         Throughout the Discovery Bay area, brittle stars are an abundant and
    obvious component of the benthic macrofauna. In most areas, large species
    predominate, although crevices and algae such as Halimeda sp. harbor both
    juveniles of large species and individuals of small species. The algal turf
    and turtle grass habitats studied here, however, were unusual in having a
    large number of very small, inconspicuous species of brittle stars occurring
    in abundance. Large species were extremely rare at these sites and, when
    present, were represented only by small juvenile forms. It appears that
    these microhabitats are particularly favorable for small species and not
    suitable for large species. Brittle stars are considered to be subject to
    considerable predation pressure in Discovery Bay (Sides, 1982) and our obser-
    vations suggest that fish may pose a threat to brittle stars easily visible
    in the algal clumps. It seems possible that a similar situation exists
    around the bases of Thalassia.

         Larger brittle stars survive by concealment beneath rocks, within rubble,
    or in crevices, and by burying within the sediment; many also are nocturnal
    in activity. They are probably absent from algal turf because it would be
    difficult for them to move through, would offer inadequate concealment, and
    perhaps would not provide suitable feeding opportunities. Conversely, the
    stiff, narrowly spaced strands of the algal turf provide an ideal microhabitat
    for the small species which dominate it, a microhabitat that allows movement,
    provides concealment, and, if abundance is a guide, offers good feeding
    conditions. The juveniles of large species that settle in this microhabitat
    presumably emigrate when they "outgrow" it or become victims of predation.

                                             96

         The axils and detrital layer around the bases of Thalassia are also
    inaccessible to large brittle stars. There appears, however, to be no reason
    why the equally cryptically colored adults of, for example, the species
    of Ophioderma should not be successful in the sandy areas between Thalassia
    plants.

         It seems reasonable to suppose that similar sized crevices elsewhere on
    the reef would also be populated by small species, providing that food is
    available, and evidence for this has recently been obtained by Hotchkiss
    (1982, who found many of the species considered here living in empty conch
    shells), Hendler (in press), and the present authors.

         The two microhabitats considered in this study, coralline algal turf and
    Thalassia beds, are sufficiently different that no single species is predominant
    inFbth7. This has several potential causes. Feeding opportunities will
    likely be different in the algal turf and around Thalassia beds. Apparent
    detritus feeders such as 0. isacanthum are favored in Thalassia, whereas the
    scavenging and apparently predatory 0. ophiactoides (Emson and Mladenov, in
    prep.) is favored in algal turf. It is interesting that the highly adaptable
    onmivorous detritivore A. squamata achieves moderate abundance in both
    habitats. Perhaps reflecting predation pressures, body coloration is also
    probably important, since the algal turf generally hosts dark colored species
    and the Thalassia paler species.

         Small size in brittle stars clearly has resulted in reproductive
    constraints. Small size inevitably means that small numbers of eggs can be
    produced. Thus the production of long lived, planktotrophic larvae is unlikely
    to be a successful mode of reproduction for small species, unless perhaps
    gametes are shed several times a year. Several alternatives appear to be
    open to small species. Two are alternative means of sexual reproduction.
    One is abbreviated development (Hendler, 1975) in which rapid development
    results in a post larva. The other involves direct development, often with
    associated viviparity or brooding. A third alternative is to supplement
    sexual reproduction with asexual multiplication.

         All the brittle stars in this sample of small adult size either reproduce
    asexually or brood the young. The similarity in life history traits among
    the three abundant fissiparous species is remarkable. Despite the fact that
    they are from three different families, they are small in size, they reproduce
    asexually by fission, and they can produce only a very small number of small
    eggs which apparently develop into planktotrophic larvae. Rearing experiments
    already have demonstrated that fertilized eggs of 0. ophiactoides develop
    into typical planktotrophic ophioplutei (Mladenov and Emson, 1984), and the
    egg sizes suggest that this is probably the case for the other species as
    well.

         Asexual reproduction appears to be the dominant mode of propagation in
    all three fissiparous species. It is probably responsible for reliable local
    recruitment, whereas sexual reproduction may result in dispersal of small
    numbers of larvae which, on occasion, found new populations or recruit into
    existing populations maintained mainly by asexual reproduction.

                                             97

         Brooding is the other reproductive pattern exhibited by the small adult
    brittle stars of this study. This reproductive mode appears to be a clear
    adaptation to low fecundity resulting from small size. Hendler (1979) noted
    an association between size and brooding in ophiolepid brittle stars and
    suggested that there was selective pressure for brooding because of low
    fecundity. Also, Menge (1975) and Emson and Crump (1979) found similar
    associations between size and brooding in the sea stars and suggested the
    same cause.

         A general relationship between small adult size and brooding has been
    documented for many groups of invertebrates including echinoderms, and
    hypotheses explaining the association have been advanced by Strathmann and
    Strathmann (1982). However, brooding is rare among brittle stars, although
    it is obvious in the present study. Hendler (1979) noted that only 57 of all
    known brittle stars brood, and of these only 7 are tropical. It seems that,
    although the particular conditions of the habitats sampled here favor this
    life history pattern, elsewhere other methods are selected.

         The alternative to brooding, abbreviated development (Hendler, 1975), is
    also characteristic of species with relatively small disks that are capable
    of producing eggs in numbers of the same order of magnitude as fissiparous
    species (e.g., Amphiura chiajei; Hendler, 1975). Species with this reproductive
    pattern are present on coral reefs but were not found in our study.

         Fission is also uncommon in brittle stars. Emson and Wilkie (1980)
    reported that only 34 species possess this habitat, although they failed to
    record 0. isacanthum as fissiparous (Hotchkiss, 1982). By contrast with
    brooding, however, fissiparity is largely a warm water phenomenon.  Emson and
    Wilkie (1980) recorded that 24 of the 34 fissiparous species were tropical in
    distribution. The reasons for these patterns are unknown and would bear
    further investigation.

         The similarity of these results to the situation described by Boffi
    (1972) for Brazil is considerable. Not only are the fissiparous ophiactids
    Ophiactis lymani and Amphipholis squamata the predominant species in the
    algal turfs examined by Boffi, but the other species in which adults were
    present were Amphipholis januarii and Ophiactis savignyi. The remaining four
    species were represented by juveniles and uncommon.

         It thus seems possible that these reproductive patterns may prevail
    among small brittle stars inhabiting algae throughout the tropical and
    subtropical Atlantic, since the present authors have established that similar
    reproductive patterns are characteristic of small brittle stars from Bermuda
    and Carrie Bow Cay, Belize. Hotchkiss (1982) observed many of the same
    species in discarded conch shells, demonstrating that these reproductive
    patterns probably are adaptive for many cryptic habitats in sheltered areas
    of coral reefs.

         Evolution to a small size is infrequent in brittle stars, but those
    species which achieve it may become very successful. The brooding Amphipholis
    squamata and the fissiparous Ophiactis saviqnyi are among the most abundant
    brittle stars. Their size apparently allows them access to an underexploited

                                            98

    microhabitat, and their biological characteristics, particularly their
    reproductive patterns, enable them to achieve remarkable success in this
    environment.  Much of contemporary life history theory is concerned with
    trade-offs between dispersal ability, fecundity, reproductive effort, and
    body size (e.g., Stearns, 1984; Olive, et al., 1984). The situation briefly
    examined here illustrates two examples of successful trading and probably
    deserves more detailed study.

                                   LITERATURE CITED

    Boffi, E. 1972. "Ecological Aspects of Ophiuroids From the Phytal of S.W.
      Atlantic Ocean Warm Waters." Mar. Biol. 15:316-328.

    Emson, R. H., and R. G. Crump. 1979. "Description of a New Species of
      Asterina (Asteroidea) With an Account of Its Ecology." J. Mar. Biol. Assn.
      U.K. 54:77-94.

    Emson, R. H., and I. C. Wilkie. 1980. "Fission and Autotomy in Echinoderms."
      Oceanogr. Mar. Biol. Ann. Rev. 18:155-250.

    Emson, R. H., and I. C. Wilkie. 1984. "An Apparent Instance of Recruitment
      Following Sexual Reproduction in the Fissiparous Brittlestar Ophiactis
      savignyi." J. Exp. Mar. Biol. Ecol. 77:23-28.

    Fell, H. B.  1946.  "The Embryology of the Viviparous Ophiuroid Amphipholis
         squamata Delle Chiaje." Trans. Roy. Soc. New Zeal. 75:419-464.

    Hendler, G. 1975. "Adaptational Significance of the Patterns of Ophiuroid
      Development." Amer. Zool. 15:691-715.

    Hendler, G. 1979. "Sex-Reversal and Viviparity in Ophiolepis kieri, n.sp.,
      With Notes on Viviparous Brittlestars from the Caribbean (Echinodermata:
      Ophiuroidea)." Proc. Biol. Soc. Wash. 92:783-795.

    Hendler, G. 1985. "A Study of Ophiuroid Size, Abundance and Reproductive
      Mode in Relation to Coral Reef Zones and Substrata." In: B. F. Keegan
       (ed.), Proc. 5th Int. Echinoderm Conference, Galway, Ireland.  A. A. Balkema
       Press, Rotterdam.

     Hotchkiss, F. H. C.  1982.  "Ophiuroidea (Echinodermata) from Carrie Bow Cay,
       Belize."  In:  K. Rutzler and I. G. Macintyre (eds.), The Atlantic Barrier
       Reef Ecosystem at Carrie Bow Cay, Belize.  Smith. Contr. Mar. Sci., Vol. 12:
       387-4 12.

     Menge, B. L.  1975.  "Brood or Broadcast?  The Adaptive Significance of
       Different Reproductive Strategies in the Two Intertidal Seastars, Leptasterias
       hexactis and Pisaster ochraceus." Mar. Biol. 31:87-100.

     Mladenov, P. V.  1979.  "Unusual Lecithotrophic Development of the Caribbean
       Brittle Star Ophiothrix oerstedi." Mar. Biol. 55:55-62.

                                             99

    Mladenov, P. V., R. H. Emson, L. V. Colpitts, and I. C. Wilkie.  1983.
      "Asexual Reproduction in the West Indian Brittle Star Ophiocomella ophiactoideW
      (H. L. Clark) (Echinodermata: Ophiuroidea)." J. Exp. Mar. Biol. Ecol. 72:1-
      23.

    Mladenov, P. V., and R. H. Emson. 1984. "Divide and Broadcast: Sexual
      Reproduction in the West Indian Brittle Star Ophiocomella ophiactoides and
      Its Relationship to Fissiparity." Mar. Biol. 81:273-282.

    Mortensen, T. 1931. "Contributions to the Study of the Development and
      Larval Forms of Echinoderms. I. The Development and Larval Forms of Some
      Tropical Echinoderms; II. Observations on Some Scandinavian Echinoderm
      Larvae." K. Danske Vidensk. Selsk. Skr. (Naturv. Math. Afd.), Series 9,
      Vol. 4, No. 1, pp. 1-39.

    Olive, P. J. W., P. J. Morgan, N. H. Wright, and S. L. Zhang. 1984.
      "Variable Reproductive Output in Polychaeta: Options and Design Constraints."
      In: W. Engels, W. H. Clark, Jr., A. Fischer, P. J. W. Olive, and D. F. Went
     Teds.), Adv. Invert. Reprod. 3:399-408. Elsevier, Amsterdam.

    Randall, J. E. 1967. "Food Habits of Reef Fishes of the West Indies."
      Stud. Trop. Oceanogr. 5:665-847.

    Sides, E. M. 1982. "Estimates of Partial Mortality for Eight Species of
      Brittlestars," p. 327 (abstract). In: J. M. Lawrence (ed.), Proc. Int.
      Echinoderm Conference, Tampa Bay, Florida.  A. A. Balkema, Rotterdam.                i

    Stearns, S. C. 1984. "The Tension Between Adaptation and Constraint in the
      Evolution of Reproductive Patterns." In: W. Engels, W. H. Clark, Jr., A.
      Fischer, P. J. W. Olive, and D. F. Went(eds.), Adv. Invert. Reprod. 3:387-398.
      Elsevier, Amsterdam.

    Strathmann, R. R., and M. F. Strathmann. 1982. "The Relationship'Between
      Adult Size and Brooding in Marine Invertebrates." Amer. Nat. 119:91-101.

                                                     100

                                           100

                   REEF ZOOPLANKTON COLLECTED ALONG A DEPTH GRADIENT
                               AT DISCOVERY BAY, JAMAICA

                                   Sharon L. Ohlhorst
                           Fisheries and Wildlife Department
                                 Utah State University
                                   Logan, Utah 84322

                                        ABSTRACT

         Reef zooplankton from three sites in the vicinity of Discovery Bay, Jamaica,
    were sampled on 29 nights during 1976-77 to determine their abundance and
    species composition. DeRth was inversely correlated with zooplankton volume;
    10.2 ml of zooplankton/mz/night were collected at 6 m, 5.3 ml at 15 m, and 3.2
    ml at 24 m. No seasonality in volume of zooplankton was observed. Variability
    in volume both within and between nights at any one site was high, but never
    were enough zooplankton collected to meet more than an estimated 12% of the
    metabolic requirements of the sessile reef dwellers.

         Volume of zooplankton was positively correlated with the number of
    individuals in the sample. The unpredictability of zooplankton abundance is at
    least partially explained by the swarming behavior of the dominant (usually >
    95% of individuals) copepod, the holoplanktonic Oithona colcarva Bowman.
    Because of this variability, it is unlikely that local zooplankton abundance
    and distribution has any causal effect upon reef species diversity. In addition
    to many groups of holoplanktonic copepods, ostracods, isopods, and decapods
    were among the most numerous taxa represented. The 6 m site differed from the
    sites at 15 m and 24 m in the relative abundance of noncopepod groups.

                                      INTRODUCTION

         Zooplankton are an important component of food webs in coral reef
    communities. They provide nutrients to corals (Goreau, et al., 1971; Johannes,
    et al., 1970; Porter, 1974) and to other benthic suspension _Teders such as
    zoanthids (Sebens, 1977), crinoids (Liddell, 1980; 1982) and ophiuroids (Macurda,
    1976), and they form a major part of the diet of many reef fish (Hobson, 1974;
    Gerber and Marshall, 1974; Hobson and Chess, 1978). Emery (1968) first reported
    that many zooplankton reside within coral reefs and, more recently, researchers
    using light (Sale, et al., 1976) and emergence traps (e.g., Alldredge and King,
    1977, 1980; Hobson Wand c-less, 1979; McWilliam, et al., 1981; Porter and Porter,
    1977; Porter, et al., 1977; Walter, et al., 1982T have characterized certain
    aspects of the resident zooplankton o       1f hllow reefs and lagoons in the Pacific.
    Few studies have examined reef-associated zooplankton in the Caribbean; Robichaux,
    et al. (1981) and Youngbluth (1982) placed traps over sand and/or seagrass
    beds, while Ohlhorst (1982) reported on diel patterns over reef substrata at
    one depth. Only one study (McWilliam, et al., 1981) has addressed the question
    of seasonality in zooplankton (from the Pacific), and none have sampled along a
    depth gradient on a reef. Further information on the abundance and behavioral
    patterns of these zooplankton, especially in the Caribbean, is necessary to the

                                            101

                         MONTEGO DISCOVERY SAY
                          BAY

                            to JAMAICA       I ;

                                     KINGSTON
                      - -  -  -  -  -  -  -  -  - -  -  -  -  -/
                                            A/ ,*24M/
                         somr                     EFR

                               WFR        / /E F
                        Crest     .        /.

    Figure 1.--Map of Discovery Bay, Jamaica, and adjacent fore reef showing the
      three sites sampled in this study.  EFR = East Fore Reef; WFR = West Fore
      Reef.

    development of realistic models of reef energetics and an understanding of the
    behavioral and feeding strategies of many reef organisms.

         This study was undertaken to examine patterns of abundance and distribution
    among reef zooplankton at three depths on a Caribbean reef. In this study,
    reef zooplankton are those zooplankton [holoplanktonic, meroplanktonic, and
    demersal forms (Robichaux, et al., 1981)] which reside for some period in or
    near the reef substratum and at some time migrate at least 1 m into the water
    column. Most planktivory by the sessile reef community should be upon this
    group of zooplankton during their vertical migration. Zooplankton were collected
    with emergence traps in a collection program designed to answer the following
    questions about the quantity and predictability of zooplankton available as a
    potential food source for reef organisms: (1) What quantity of zooplankton is
    available to the reef community, especially to sessile reef-dwelling organisms?
    (2) How variable is the amount of zooplankton on different nights? (3) Do reef
    sites at different depths differ in a predictable way with respect to abundance
    of zooplankton? (4) Do reef sites at different depths differ in species
    composition of zooplankton? (5) Is there any predictable cycling of zooplankton
    abundance?

                                 MATERIALS AND METHODS

         A total of 392 zooplankton samples were collected over 29 new and full
    moon nights during 1976-77 using a modified version (Ohlhorst, 1980, 1982) of
    the demersal trap described by Porter and Porter (1977). Traps were placed
    prior to sunset, and collection bottles were removed the following morning.

                                             102

                    52*
                                                *

                    32

                   28--
               E
                    24-
               w
                                            2
                     20--
               0

                    16-- *
                       18-. �

                          632 2L 0 * 2 2 * '
                    12--   2   2              2 0

                         224  00  2         3
                         23  2 *2  2          22 2        4
                                              �

                     4-..  2 2. 2 3 2   .  2
                       2     4  24*  4 2   * 2 2              2 ~  *
                           1t  **0 3          0t   +              *s~
                               I  I*          * ! , , !,,I
                          >0 s  p  to  go  >a  z  <    �   �   �  a a a a a a a
                         _ C _ _ _ _     u w  4   - c  - X  U W 3  N  ao  - X 0 m M  4 � -

    Figure 2.--Volumes of zooplankton (ml/m2) from the 15 m site are plotted for
      the 29 nights sampled.  Stars indicate full moon nights, and circles indicate
      new moon nights.

    Samples were preserved in 5-10% formalin immediately upon return to the surface.
    Each sample was concentrated over a 90 m mesh sieve, resuspended in formalin
    solution and allowed to settle in graduated centrifuge tubes until a constant
    volume was reached (usually after 48 hr) (Porter, et al., 1978).

         Zooplankton were collected from three reef sites at Discovery Bay, Jamaica
    (fig. 1): a shallow site (6 m) immediately behind the reef crest to the east
    of the Discovery Bay ship channel; a 15 m site on a broad, shallow sloping fore
    reef plain to the east of the boat channel; and a 24 m site on this same plain
    (see Ohlhorst, 1980, and Liddell, et al., 1984, for site descriptions). Because
    of the variability in abundance of-zoopankton from different locations at any
    one reef site on a single night (fig. 2), traps were placed over the same
    permanently marked reef locations at each sampling to eliminate substrata
    induced variation when comparing one night with the next.

                                            103

                   80000 -

                   70000 -
                                                               .

                   60000-

                 -J                                          .
                   50000-

                 - 40000-

                 a:                         �
                  30000-               .               N
                 Z                                     N=48
                   20000-                             r2: .75
                               � |1                  S.R.= P<.O0
                   10000-    1

                     0     I    I                   I  I ,        I
                           0    X   2    3    4    5    6    7    8
                                        SETTLING VOLUME (ML)

    Figure 3.--Correlation of zooplankton settling volume with the number of
      individuals counted in the sample. Results are given for regression analysis
      (r2) and Spearman Rank Correlation (S.R.).

         Caloric determinations were made on six freeze-dried (10.5-15.5 mg) samples
    of zooplankton (all dominated by copepods) using a microbomb calorimeter (Tinkle
    and Hadley, 1973). Samples of known volume were ashed at 450�C for 5 hr for
    ash weight determination. Samples of known settling volume were freeze dried,
    weighed, and the weight/individual calculated using the mean value of 1.6 x 10-4-
    individuals/ml settling volume determined from a count of individuals from 30
    samples of known settling volume. Samples consisting of 20-30 individuals were
    removed and weighed on a Cahn Electro-balance for an independent estimate of
    individual weight.

         In addition to volumetric determinations on all 392 samples, 56 of the
    zooplankton samples from 7 nights at the 3 reef sites were enumerated.

                                         RESULTS

         Differences in the "packability" of species may result in difficulties in
    interpreting settling volume data. However, the dominance of a single species
    and the general similarity in morphology, size, and composition of species in
    these samples made volume determinations a relatively easy method by which to
    compare sites. As illustrated in figure 3, the number of zooplankton is
    positively correlated (Spearman Rank Correlation, p < 0.01) with the settling
    volume of zooplankton.

                                             104

     *^      Variability in Volume of Zooplankton Within Reef Sites

                  Volumes of zooplankton from the 15 m site ranged from 0.4-50.8 ml/m2 (  =
             5.3 ml/m2) (figs. 2, 4) and, on any one night, differed among sites by 0.4-49.2
             ml/m2 (X difference in volume/night = 8.0 ml/m2).  The variability occurring
             between consecutive nights was as great as that between randomly paired nights
             (Mann Whitney U Test, p > 0.05). This wide range in volumes was found for all
             three sites, with samples from 24 m showing the least variation (fig. 4).

             Differences in Abundance of Zooplankton Between Reef Sites

                  The results of the zooplankton sampling from all three sites are presented
             in figure 4. Volume of zooplankton is inversely correlated with depth (Spearman
             Rank Correlation, p < 0.01). The shallow (6 m) site yielded the greatest volume
             ( = 10.2 ml/m2), while the 24 m site yielded the least (X = 3.2 ml/m2).
             Pairwise comparison of volumes from all nights shows that volumes from 6 m vs.
             24 m and 15 m vs. 24 m are significantly different (Mann-Whitney U Test, p <
             0.01), but not 6 m vs. 15 m. However, these relationships do not hold for every
             night considered separately. When the sites are paired night by night, the
             volume at 6 m is greater than at 24 m only 45% of the nights (N = 11), and the
             volume at 15 m is greater than at 24 m only 57% of the nights (N = 14). While
             overall the volumes from 6 m and 15 m do not differ significantly, volumes from
             6 m are greater than those from 15 m on 45% of the nights.

                  When the total numbers of individuals captured at each site (table 1) are
             compared, similar patterns are observed as for volume.  More individuals occurred
             at 6 m than at 24 m (Mann Whitney U Test, p < 0.0006) and more at 15 m than at
              24 m (Mann Whitney U Test, p < 0.002), but there was no difference between 6 m
             and 15 m. However, the pattern changes when the dominant copepod is removed
             from calculations. With Oithona colcarva Bowman removed, the site at 6 m does
              not have significantly more individuals than 15 m or 24 m (Mann Whitney U Test,
              p > 0.05), and, curiously, the 24 m site has significantly more than the 15 m
              site (Mann Whitney U Test, p < 0.002).

              The Effect of Lunar Phase on Abundance of Zooplankton

                   The phase of the moon appears to influence volumes of zooplankton, although
              the results from different depths are conflicting.  The 6 m site yielded a
              significantly greater volume on nights of the new moon than full moon, while
              the 15 m site yielded a greater volume on nights of the full moon than new moon
              (Mann Whitney U Tests, p < 0.01).

                   The lunar effect on numbers of zooplankton was significant only at the 6 m
              site, where significantly greater numbers (Mann Whitney U Test, p < 0.03) were
              captured on nights of the new moon than full moon, both for total plankton and
              for plankton without 0. colcarva. However, with only 7 nights (2 full moon, 5
              new moon) sampled, this deserves further investigation.

                   When numbers of zooplankton captured in different phases of the moon are
    0          compared among sites, collections at 6 m did not differ from those at 15 m or

                                                        105

      25 -

      20 -

                             MEAN      950/  cl    MEDIAN    N(SAMPLES)    N(NIGHT)
            is-        ~~~ 10.24          �3.12         1.5      es                  11

      70-

      60 -             15

    40                             5.28     �0.74          0.9           214            29

    :0 z

    z20-~

      70-

         Yo  24 M

      50-

            40-                 ~~~3 21   �0.77         0.5           112            14

      40-

      30-

            20-~ ~ ~~~V7

                        PLANKTON  VOLUME  (ML) >2

                                                I 0 6

    Table 1.--Zooplankton collected over 1 m2 of reef substrata at three depths.
       Mean, standard deviation and percent of samples containing each organism
       are given for the common categories of organisms. Samples from 6 m included
       8 samples from 3 nights; those from 15 m included 27 samples from 7 nights;
       and those from 24 m included 21 samples from 7 nights.

                                                 6 M                                        15 M                                       24 M

     ZooDlankton                     Mean number    (St.Oev.)                    Mean nu                                    Meannumber         (St.Dev.)        %

     Oithona  colcarva                  124396           (83206)        100          79307           (51392)       100          54381          (118901)        100
     Cyclopoid #1                                                         0              32              (64)       27             492             (617)        71
     Cyclopoid #2                            27              (50)        88              55            (100)        54              87             (116)        52
     Cyclopoid #3                            26              (74)        38              47              (85)       63              41              (85)        43
     Corycaeus  sp.                        1832            (2215)       100             690            (771)        85             876             (839)       100
     Misc.  cyclopoids                      136             (277)        38             130             (199)       59             243             (346)        81
     Harpacticoid #1                         26              (74)        63            281             (333)        93             226             (265)        90
     Harpacticoid  #2                                                     0              15              (40)       52              32              (70)        48
     Misc.  harpacticoids                    68             (148)        38             501            (336)        93             760             (512)      100
     Calanoid #1                           3046            (5877)        63             177            (319)        52              47              (76)        33
     Misc.  calanoids                     12649           (17242)        88             477            (539)        89           1820            (2280)        100
     Copepod nauplii                         21              (58)        13              35              (79)       22             110             (140)        52
     Barnacle  nauplii                        74             (85)        75              42              (88)       56              65             (105)        52
     Ostracods                                                             0             87             (196)       89             404             (929)        95
     Amphipod   #1                                                         0             53              (84)       63              21              (37)        43
     Amphipod   #2                                                         0              8              (29)       30              20              (46)        29
     Misc.  amphipods                         78            (156)        38              62            (107)        89              61              (66)        86
     Isopod #1                              322             (430)        75            154             (218)        52            324             (376)         71
     Isopod #2                               84             (162)        75            243             (264)        89            148             (222)         71
     Tanaids                                 53             (107)        38             112            (165)        89              93             (125)        95
     Cumaceans                                93            (151)        88              23              (60)       70               9              (22)        57
     Mysids                                   53            (148)        88              85            (131)        74              80              (78)        90
     Lucifer sp.                           1560            (2413)        75                                           0                                          0
     Misc.  decapods                        132             (226)       100              88            (381)        70              43              (55)        81
     Polychaetes                            148             (161)       100              98            (125)        93             126             (142)        86
    Appendicularians                                                      0             15              (49)        15             87             (138)        52
     Chaetognaths                                                          0            172            (178)        93             105             (113)        95
     Gastropods                               77            (106)        50              83            (144)        56              94              (90)        38

     Total (includes
     uncommon  species not              146056          (102924)                     83244           (51216)                    60904          (118592)
     included above)

    Figure 4 (opposite page).--Volume frequency histogram for the three reef sites.
       The number of samples of differing volumes (converted to volume/m2) is plotted.
       Volume is plotted in 2 ml increments with the midpoint volume indicated for
       each.

                                                                           107

    24 m on new moon nights (Mann Whitney U Test, p > 0.05) but did have greater
    numbers than samples from 15 m or 24 m on new moon nights.  This holds for
    counts both with and without 0. colcarva, except that samples from 6 m have
    more individuals than those from 24 m on full moon nights when O. colcarva is
    included.

    Composition of Zooplankton

         The mean, standard deviation, and percent occurrence for 29 categories of
    organisms are presented in table 1. No statistically significant differences
    between sites in occurrence of taxa were noted across all nights, with the
    exception of the absence of several organisms and the exceptional abundance of
    a holoplanktonic decapod, Lucifer sp., at 6 m. The relative abundance of
    copepod groups was similar (Spearman Rank Correlation, p < 0.01) at all sites,
    but the ranking of noncopepod groups differed between 6 m and both 15 m and 24 m
    (Spearman Rank Correlations, p > 0.05). The 24 m site possessed a significantly
    greater number of organism categories [17.9 + 6.2 (S.D.)] than did the sites at
    either 6 m (10 + 3.2) or 15 m (12.5 + 5.9). Evenness and species diversity
    were consistentTy higher at 15 m and-24 m than at 6 m (X H' at 6 m = 1.35,
    15 m = 2.11, 24 m = 2.46).

    Bomb Calorimetry and Biomass Determination

         The results of caloric and biomass determinations are presented in table
    2.  Bomb calorimetry produced caloric values of 5.6 [+ 0.05(S.D.)] calories/mg
    dry weight, a figure which agrees well with published values (Cummins and
    Wuycheck, 1971). Only 6% of the freeze dried weight was inorganic ash material.
    The weighing of a known number of Oithona colcarva individuals (the dominant
    organism; Ohlhorst, 1980, 1982) produced weights averaging 2.5 pg/individual,
    while the weighing of a known volume with a calculated number of individuals
    produced weights averaging 1.6 pg/individual.

                                       DISCUSSION

         The highly three-dimensional nature of the reefs in this study made it
    impossible to place traps completely flush with the reef floor, and thus some
    zooplankton movement undoubtedly occurred both into and out of the traps. A
    number of workers have addressed the problems related to demersal trap design
    (Robichaux, et al., 1981; Youngbluth, 1982), and their results should be taken
    into account when evaluating the results of work based on demersal emergence
    traps. Caution is necessary in interpreting the origin of the zooplankton
    ["demersal traps" catch more than demersal plankton (Robichaux, et al., 1981)]
    and their relative abundances due to differing plankton behavior- Robichaux, et
    al., 1981; Youngbluth, 1982). Nonetheless, studies such as this, with one
    method used throughout, provide data by which different sites can be compared.
    The volumes of zooplankton obtained in this study give an indication of the
    amount and types of zooplankton available for capture by the sessile inhabitants
    of the reef, and serve as a useful basis for comparison of different reef sites..

                                            108

    Table 2.--Biomass and caloric value determinations of zooplankton samples (mean + standard deviation).
      a: The value of 5.584 calories/mg dry weight agrees well with similar determinations by other workers
      (Cummins and Wuycheck, 1971). b: The mean values from weight determinations by two independent
      methods (see text). c: Values calculated by Johannes, et al. (1970) for 1 m2 living coral.

                                                    Dry Weight         Ash Free             Calories
                                                      (mg)            Dry Weight
                                                                        (mg)

                 1 ml settling volume                31.5 (�8.1)        29.6 (�+7.5)           175.9 (+45)a
                 1 Oithona colcarva (0.5 onm)b       0.002 (�+4 x 10-4)   0.0019 (�+4 X 10-4)  0.012 (+3 x 10 3)
                 Zooplankton over 1 m2 reef
                 at 15 m                             167 (�35)          157 (i33)              928 (�176)
                 Metabolic requirements of
                 1 m2 of reefC                      6000                                      33,600

    Abundance of Zooplankton

         The average volume of 5.3 ml of zooplankton per i m2 reef substratum at 15 m
    depth on the East Fore Reef indicates that only 3-4% of the reef energy needs,
    as determined by Johannes, et a]. (1970) for an area of high coral cover, could
    be met by the capture of alF-othe demersal zooplankton (table 2).  While the
    6 m site yielded more zooplankton, it was rarely more than 12% of the amount
    necessary to sustain the corals. Gut analyses of various reef planktivores,
    such as corals (Porter, 1974) and crinoids (Liddell, 1980, 1982), and observations
    of feeding by corals (Johannes and Tepley, 1974) confirm that inadequate numbers
    of zooplankton are caught to meet the estimated energy needs of these reef
    inhabitants.

         A comparison of results from this study with those of Alldredge and King
    (1977); Porter and Porter (1977); Porter, et al. (1977); McWilliam, et al.
    (1981); and Walter, et al. (1982) is presented in table 3. Volume and numbers
    of zooplankton collected over Jamaican reefs were larger than those of the
    other studies. This difference may reflect either real differences in the
    biology of the reefs studied or merely differences in the amount of swarming
    copepods captured because of imperfect fit of the traps to the substrata.
    Nonetheless, these studies together indicate the range of values for the amount
    of demersal zooplankton to be found over coral reefs. Further study using
    identical collection methods, including sealing efficiency and plankton mesh
    size, is necessary to determine the differences betwen the Caribbean reef
    studied in this work and the Pacific reefs studied by others.

    Variability in Abundance of Zooplankton

         The high degree of spatial and temporal heterogeneity in zooplankton volume
    (figs. 2, 4) is probably attributable to the swarming behavior of the dominant
    copepod, Oithona colcarva. Although swarms of this species were not observed
    by the author at Tamaica, other members of this genus are known to swarm in
    large numbers (Emery, 1968; Hamner and Carleton, 1979).

         One result of this variability was that patterns of differences in
    zooplankton volume between sites varied from night to night, although certain
    statistically significant trends were discernible when data from all nights
    were pooled. This illustrates how sampling frequency might influence conclusions
    about the presence or absence of differences between collection sites; depending
    on which nights were sampled, contrary conclusions could be drawn. McWilliam,
    et al. (1981) also reported on the variability of zooplankton abundance from
    consecutive nights.

    Factors Affecting Abundance of Zooplankton

         This study indicates that zooplankton volumes for fore reef sites are
    negatively correlated with depth within the range of 6-24 m. This is, therefore,
    a very important consideration when extrapolating from studies done over shallow
    reefs (all of the previous work) to those which may be deeper.

                                           110

    Table 3.--Comparative abundances of zooplankton over coral substrata on eight reefs.
      a:  This study.  b:  Samples collected as in this study, August 8-9, 1976; N =
      24. c: Samples collected as in this study, July 2-3, 1976; N = 12. d: Samples
      collected as in this study, July 26-27, 1976; N = 24.  e:  Alldredge and King
      (1977).  f:  Porter and Porter (1977) and Porter, et al. (1977).  g:  Walter,
      et al. (1982).  h:  McWilliam, et al. (1981).

      Reef location        Volume/m2/night (ml)  Number/m2/night  Ash free dry weight/
                                                                    m2/night (mg)

      Jamaicaa                    6m: 10            6m: 1.6x105            6m: 296
                                15m: 5.3          15m: 805x104           15m: 167
                                24m: 3.2          24m: 5.3x104          24m: 101

      Barbadosb                  20m: 3.5          20m: 103x104

      Colombiac                  15m: 3�4          15m: 1.9xlO4

      Curacaod                   15m: 4�8          15m: l14x104

      Lizard Island                                             4
      Lizard Island                                2-5m: l.lx104          2-5m: 95
      Lagoone

      Philippinesf               lOm: 905          lOn: 2O0x104

      Philippines9                                  3m: 5o4x104

      Great Barrier
      Reefh                                        4-5m: 3.7x103

          The apparent correlation between high zooplankton volume and full moon
     periods for collections at 15 m probably reflects the fact that a much higher
    proportion of the full moon nights were also "rain" nights (Fisher Exact
     Probability Test, p < 0.01). The correlation of volume with "rain" [volumes
     correlated only to rainfall (> 0.6 cm) within the 48 hr prior to collection]
     is found during both phases of the moon, and in this study it appears that
     lunar phase had no effect on the volume of vertically migrating zooplankton on
    the East Fore Reef (Ohlhorst, 1980). The implication of rain as a factor
     affecting zooplankton volume also has been reported for zooplankton collected
     over Puerto Rican reefs (Glynn, 1973) and in Kingston Harbor, Jamaica (Grahame,
     1973), where volumes of plankton from surface net samples correlated with
    monthly rainfall. It is not clear why rainfall should have the immediate effect
     found in this study, unless an increase in floculation of organic matter or
     land runoff occurred and produced an immediate increase in the foraging activity

                                              111

    of the zooplankton.  There was no measurable change in salinity at any site
    during rain periods (Ohlhorst, 1980).
         Interpretation is further complicated because no correlation between volume
    of zooplankton and lunar phase or rainfall was found at the 24 m site, and the
    6 m site yielded results opposite to those at 15 m, with more zooplankton
    captured on new moon (= "nonrain" in this study) than full moon nights. At the
    6 m site, there is an obvious advantage for zooplankton that do not enter the
    water column on full moon evenings, as visual predators should be more active
    on these nights. It is, therefore, surprising that yields of zooplankton at
    15 m were the reverse (highest on full moon evenings), since the reefs at 15 m
    were well illuminated on these nights also.

         Although Glynn's (1973) collections of plankton from the surface water in
    Puerto Rico sampled a different component of the reef zooplankton, his collections
    over a shallow reef (< 5 m) through one lunar cycle yielded a pattern consistent
    with that found for the shallow (6 m) site in this study; more zooplankton were
    collected on the new moon nights than on the full moon nights. In the study by
    Alldredge and King (1980) in the Pacific, abundance of zooplankton was not
    correlated with lunar phase.

         There was no seasonality observed in zooplankton volumes in this study,
    although some periods of the year were less intensively sampled (fig. 2).
    Periods of high zooplankton yields reflected the occurrence of rain within 48 hr
    of sampling; however, collections of very low volumes were interspersed with
    these high volumes, casting doubt on any real causative effect (such variation
    also is found in other reports of seasonality; Glynn, 1973).  It appears, there-
    fore, that zooplankton volumes are indicative of previous rainfall, but rainfall
    is not necessarily predictive of high zooplankton yields. Moore (1967) and
    Grahame (1976) found no patterns of seasonality in their collections of surface
    zooplankton from the south coast of Jamaica. In contrast, McWilliam, et al. (1981)
    did find seasonality on a Pacific reef, with more zooplankton in the siummer.

         With the exception of the trend for greater abundance of zooplankton on
    "rain" nights at the 15 m site and for lower yields on full moon ("rain") nights
    at the 6 m site, there was no indication that certain of the nights were more
    conducive than others for zooplankton migration. Neither the pairing of
    collections on the same night from the 15 m and 24 m sites nor the pairing of
    collections on the same night from the eight 15 m trap locations produced a
    significant correlation (Spearman Rank Correlation, p > 0.05). It appears,
    therefore, that abundance of zooplankton cannot be predicted on the basis of
    any environmental parameter which would be experienced throughout the reef.

    Composition of Zooplankton

         As reported earlier for Jamaican reefs (Ohlhorst, 1980, 1982), copepods are
    the dominant organism collected in demersal emergence traps placed over the
    reef. Because of the great variance, the sites rarely differed significantly
    and the ranks of abundances for copepod taxa were correlated between sites.

         Due to the absence from the 6 m site of a number of categories of organisms *
    and the presence of Lucifer sp. which was rare elsewhere, the rankings of

                                             112

    abundances for noncopepod categories differed at 6 m from those at either 15 m
    or 24 m. These data indicate differences between shallow and deeper reef sites
    which should be investigated further. They also indicate that caution should
    be used when extrapolating data from shallow reefs to other reef sites.

         Robichaux, et al. (1981) and Youngbluth (1982) discuss the effect of
    differing collection.methodology on zooplankton species composition. In light
    of the many confounding variables, comparisons between this study and others
    will be brief and restricted to shallow reef sites. The data from the 6 m site
    in this study compare most closely with those from 3 m in the Philippines
    (Walter, et al., 1982). The relative abundance of most plankton groups and the
    absolute abundance of certain groups are comparable.  Lucifer, for example, is
    an important component of the fauna in both shallow reef collections; however,
    amphipods are more important in their study than in this study. Although the
    abundant taxa from this study are not the same as those from the sealed traps
    of Hobson and Chess (1979) and Robichaux, et al. (1981), the values for certain
    of the taxa are comparable.  Robichaux, et1l. 71981), for example, collecting
    over a Thalassia bed (3 m), recovered an average of 56 tanaids and 54 amphipods/m2,
    while this study produced an average of 53 tanaids and 78 amphipods/m2 at the 6 m
    reef site.

                                      CONCLUSIONS

         This study indicates that reef-associated zooplankton can only be of minor
    caloric value to sessile reef organisms. While there is a negative correlation
    between abundance of zooplankton and depth of the reef site, local abundance is
    highly unpredictable. It would appear difficult for planktivores to choose
    areas of maximum food potential and unlikely that local zooplankton abundance
    has any causal effect upon patterns of species diversity. The polytrophic
    habit of many of the reef dwelling invertebrates (Trench, 1974) may reflect the
    unpredictability of this food source.

         It should be noted that the significance of zooplankton may lie not in
    their role as a major caloric source, but in their critical role in the cycling
    of nutrients in the reef environment. Zooplankton are able to feed on the very
    abundant mucus and organic particles in the water (Johannes, 1967; Gerber and
    Marshall, 1979; Richman, et al., 1975; Gerber and Gerber, 1979), much of which
    is generated by reef organisms themselves (Lewis, 1973; Coles and Strathmann,
    1973). Zooplankton also feed on the bacteria on these organic aggregates
    (Sorokin, 1973) and on the phytoplankton. Thus, the zooplankton prevent the
    nutrients from all of these sources from being lost from the reef ecosystem.
    Not only do these nutrients pass along the food chain through predation upon
    zooplankton, but the production of fecal pellets, often composed of only
    partially digested material, provides an important food source for certain
    benthic invertebrates (Frankenberg and Smith, 1967; Turner and Ferrante, 1979)
    and also serves to keep the important nutrients within the reef ecosystem.

                                    ACKNOWLEDGMENTS

         I would like to thank J. B. C. Jackson, N. Knowlton, W. D. Liddell., and M.
    Youngbluth for their very helpful criticism of this manuscript.  K. G. and J.

                                           113

    W. Porter provided suggestions concerning the design of the research, and W. D. _
    Liddell, V. Tunnicliffe, and B. Westrum provided invaluable diving assistance.
    This research was supported through funds provided by the International Women's
    Fishing Association, the Society of Sigma Xi, the Organization of American
    States, and the Women's Seamen's Friend Society of Connecticut.

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    Walter, C., L. Tulane, and J. N. Pasamonte. 1982. "A Preliminary Quantitative
       Study on the Emergence of Reef Associated Zooplankton From a Philippine
       Coral Reef." Proc. Fourth Int. Coral Reef Symp. 1:443-451.

    Youngbluth, M. J. 1982. "Sampling Demersal Zooplankton: A Comparison of
       Field Collections Using Three Different Emergence Traps." J. Exp. Mar.
       Biol. Ecol. 61:111-124.

                                            116

                       TEMPORAL PATTERNS OF ZOOPLANKTON MIGRATION

                                   Sharon L. Ohlhorst
                          Department of Fisheries and Wildlife
                                          and
                                    W. David Liddell
                                 Department of Geology
                                 Utah State University
                                   Logan, Utah 84322

                                        ABSTRACT

         The NOAA/NULS-1 underwater habitat facility at St. Croix was utilized
    during July 1982 for a study of the temporal patterns of migration into the
    water column by reef zooplankton. Samples were collected for 6 days at 9
    daily time intervals using mesh emergence traps, diver pushed plankton nets,
    and surface plankton net tows. This is the first study to sample such finely
    spaced time intervals. Preliminary analysis from 2 days indicated that there
    was migration throughout the night, with increased activity found prior to
    sunrise as well as following sunset. This is the first time a predawn rise of
    zooplankton has been documented.

         The cyclopoid copepod, Oithona colcarva, dominated most time intervals,
    although it was not nearly as abundant as in an earlier Caribbean reef zooplankton
    study. Most zooplankton taxa followed the same general pattern of activity, and
    the relative abundance of the common taxa generally remained the same throughout
    the 24 hours. The time intervals around sunset were an exception, however.
    For example, during the hour following sunset, calanoids, harpacticoids,
    polychaetes, and pagurid larvae were relatively more abundant than during the
    hour prior to sunset, while copepod nauplii and amphipods were less abundant
    during this postsunset time interval. Significantly more taxa were captured
    during the first hour of darkness than during any other time interval.

         The effects of different trap designs and types of reef substrata on
    zooplankton samples also were examined. There was no significant difference in
    the number of individuals collected between treatments using sealed and unsealed
    traps or between those using unsealed traps over coral and sand substrata.
    This is in contrast to other studies; two possible explanations for these
    discrepancies relate to the types of substrata over which sealed and unsealed
    traps are compared and to differences in trap sealing efficiency when different
    substrata types are being compared.

                                      INTRODUCTION

         The zooplankton that reside within or near coral reef ecosystems have only
    recently begun to receive the attention of researchers. Zooplankton have been
    studied from various wcific reef communities primarily by using various
    modifications of emergence traps (Alldredge and King, 1977, 1980; Porter and
    Porter, 1977; Porter, et al., 1977; Hobson and Chess, 1979; Birkeland and

                                            117

    Smalley, 1981; McWilliam, et al., 1981; and Walter, et al., 1982).  Fewer
    studies of reef zooplankton from the Caribbean have been conducted (Ohlhorst,
    1980, 1982, 1985; Robichaux, et al., 1981; and Youngbluth, 1982). While the
    diel migration patterns of these zooplankton have been shown to influence the
    behavior of nocturnal planktivorous fish (Hobson, 1974; Hobson and Chess, 1978;
    Robertson and Howard, 1978) and might affect the behavior of other reef
    planktivores (Porter, 1974; Sebens, 1977; Liddell, 1982), few studies have
    investigated the diel migration patterns of reef zooplankton in detail (Alldredge
    and King, 1980; Ohlhorst, 1982; Walter, et al., 1982). The only study of
    migration by Caribbean reef zooplankton T onducted at Jamaica by Ohlhorst,
    1982) suggests that there is no single pulse of migratory activity; rather
    zooplankton rise into the water column at variable rates throughout the night
    with a peak of activity during the second hour after sunset. Also, different
    taxa were shown to exhibit differing migratory patterns. While these observations
    are consistent with those from the Pacific, it is important to determine whether
    or not such patterns occur elsewhere in the Caribbean. Additionally, more
    frequent sampling than previously conducted would be of value in refining the
    patterns of zooplankton migration.

         One of the reasons for the paucity of detailed studies addressing this
    question is the physiological limitation placed upon safely conducting the
    repeated sampling dives which are necessary for such studies. Previous studies
    which have addressed the question of migratory patterns of reef zooplankton
    have been restricted to sampling widely spaced time intervals or sampling very
    shallow (< 5 m) sites. Data from Ohlhorst (1985) suggests that caution should
    be used when extrapolating data from shallow sites to greater depths.  The
    present study examines the migratory patterns of reef zooplankton at an
    intermediate (15 m) depth at St. Croix through repeated sampling of finely
    spaced time intervals. This sampling was made possible by saturation diving
    from the NOAA/NULS-1 Underwater Habitat, HYDROLAB.

                                        METHODS

         Sampling of reef zooplankton was conducted from the NOAA/NULS-1 HYDROLAB
    located at 15 m depth in the Salt River submarine canyon on the north coast of
    St. Croix, U.S. Virgin Islands (17045' N, 64�45' W) during July 1982. Samples
    were collected from both reef and sand areas located approximately 15 m east
    of the Habitat. To eliminate biases caused by the proximity of the study sites
    to the Habitat, all of the external lights of the HyDROLAB remained off for the
    duration of the study. Saturation diving from the HYDROLAB enabled two teams
    of divers to collect plankton samples at closely spaced intervals over a 6-day
    period.

         Zooplankton were sampled by three methods: (1) Emergence traps, which
    covered 0.5 m2, were placed over various types of reef substrata to capture
    zooplankton moving from the reef site into the water column. Certain of these
    traps were sealed over their substrata by a skirt (Robichaux, et al., 1981),
    while others were affixed more loosely over their substrata.  7) Diver pushed

                                                      118

        Table I.  Number of zooplankton captured/m2/hour, beginning with 0030 on July 16 and
        continuing through 2300 on July 17, 1982. ST= Students' T test at pgO.05, 0 = no
        significant difference between this and the previous time interval, + = a significant
        increase, - = a significant decrease; MWU = Mann Whitney U test at psO.05, symbols are
        the same as for ST.

        Time Interval       #Samples       Mean (Std. Dev.)      Median      ST       MWU

            0030               8            139.2  (78.0)         136.6
            0230               8            109.4  (52.0)         100.0        0        0
            0500               8            176.0  (97.8)         168.0        0        0
            0600               4             26.6  (20.2)          20.0        -        -
            1200               8             10.6   (9.0)           8.0        0        0
            1830               8             40.0  (21.8)          39.0        +        +
            1930               8            246.8 (103.8)         256.0        +        +
            2230               8             99.6  (60.0)          92.0        -        -
            0030               8            348.0 (376.0)         202.0        0        0
            0230               8            702.0 (662.0)          54.6        0        0
            0500               8            306.0 (364.0)         140.8        0        0
            0600               8             55.8  (22.2)          60.0        0        0
            1200               8              6.2   (2.0)           6.0        -        -
            1800               4             92.6  (24.2)          90 0        +        +
            1930               4            399.2 (199.0)         341.4        +        0
            2030               4            189.6 (144.2)         133.0        0        0

            2300               4             51.0  (26.0)          40.4        -        0

    zooplankton net samples were collected 1 m and 5 m above the reef. (3) A
    plankton net was towed at the surface from a boat to sample zooplankton just
    below the surface, and vertical net hauls from 15 m to the surface also were
    made from the boat. The emergence traps and zooplankton nets were made with 90
    micron meshes. Two additional emergence traps were constructed with clear
    polyvinyl. The traps were modified (Ohlhorst, 1980, 1982) from those used by
    Porter and Porter (1977).

          Five hundred and eighty samples were collected over 6 days and 9 time
    intervals each day (table 1). Samples were preserved in 5-10% buffered formalin
    immediately after collection and counted as in Ohlhorst (1982). Preliminary

                                                   119

                   TEMPORAL PATTERNS OF ZOOPLANKTON MIGRATnON                             0

              800 -

              700 -

             '400-

            Z300-

              200 -

              ,oo- Legend
                                                                  A TOTAL
                    * -.' ".                 -.                      *  LESS  4Ao"  -
               0         -

                                      liME

    Figure I.--The number of individuals captured per hour during the different
      time intervals are plotted, both with and without the copepod Oithona colcarva.
       Samples from 2030 on July 16 have not been counted.  Refer to table 1 for the
      means, medians, and standard deviations.  Note that units of time along the x
       axis are unequal.

    results from 148 samples from mesh emergence traps from 2 days (July 16-17)
    will be presented herein. During the collection period sunrise was at 0600,
    sunset at 1800, and the lunar phase was new moon.

                                       RESULTS

    Effects of Traps and Substrata

         No significant differences Cp < 0.05; Mann Whitney U (MWU), Students' T
    (ST) tests] in the number of individuals captured per hour were observed between
    mesh traps with sealed vs. unsealed bottoms over coral substrata. Additionally,
    no significant differences (p < 0.05) in the number of individuals captured per
    hour occurred between traps positioned over sand vs. those positioned over coral
    or rubble. For all subsequent tests, data from sealed and unsealed traps and
    traps located over sand and over coral or rubble were pooled. The polyvinyl
    traps tended to capture more zooplankton than mesh traps. Although the difference
    between types of trap was not significant, most of the data presented herein
    are from mesh traps only.

                                          120

     Table 2. Percent occurrence of phyla in demersal traps. Samples were collected on
     July 16-17, 1982 and are from both mesh and polyvinyl traps.  The taxonomy is
     according to Barnes (1980).

               time:  0030   0230   0500   0600   1200   1830   1930   2030   2230
            # traps : (20)   (20)   (20)   (14)   (20)   (16)   (16)   ( 6)   (16)
     Phyla

     ANNELIDA         30    65    35    21    20          6    100    67    56
     ARTHROPODA       100   100   100   100   100   100   100   100   100
     CHAETOGNATHA      25    30    15    14        5     19    13       0     25
     CHORDATA          15    15    25       7     20    19    25    33    31
     COELENTERATA       0     25    25    21    25    38    56    67    44
     ECHINODERMATA      0     0      0      0      5      0      0      0      0
     MOLLUSCA          40    35    35    29    60    94    81    50    38
     NEMATODA           0     0      0      0      5      0     13      0      0
     PLATYHELMINTHES    0      5     0      0      5      0     19      0      0
     SARCODINA         35    80    45    29    80    94    81    67    31
     SIPUNCULIDA       25    15    10    21    40    25    63    67    25

    Temporal Patterns

         The number of zooplankters migrating per hour for the various sampling
    intervals is presented in table 1 and figure 1. Data from July 16-17 displayed
    significant decreases (p < 0.05; MWU, ST tests) in the total number of individuals
    captured per hour between 0500 or 0600 and 1200 hours, and significant (p <
    0.05) increases between 1200 and 1800/1830 hours and between 1800/1830 and 1930
    hours, followed by a significant (p < 0.05) decrease after 1930 hours. The
    pattern differed somewhat when the cyclopoid copepod Oithona colcarva (Bowman)
    was removed from analysis (fig. 1).

         There was no significant (p < 0.05; MWU, ST tests) difference between the
    2 days in the number of individuaTs migrating per hour for most time intervals
    (fig. 1, table 1). Significantly more individuals (p < 0.05; MWU, ST tests)
    were captured on July 17 than on July 16 in both the intervals from 0030-0230
    and 1200-1800/1830. When the samples were considered without 0. colcarva,
    numbers of zooplankters differed between days both in the intervals mentioned
    above and at 0500-0600.

         Crustaceans made up the majority of the zooplankters captured by the traps,
    although representatives of 11 phyla, including foraminifera, echinoderm larvae,
    sipunculids, Amphioxus, and appendicularians also were collected (table 2).  A

                                             121

                      MEAN NUMBER OF TAXA PER TIME INTERVAL
               25-

                                                 t
               20 -

               is-

               10-

                                      ~t
                5-

                    0o 0 023o 050os  0600 1200 1830 1930 2030 2300
                                       TIME

    Figure 2.--The mean number of taxa captured during the various time intervals
      (days combined) is plotted. Vertical bars represent 95% confidence intervals.
      Units of time along the x axis are unequal.

    total of 73 taxa were identified from these samples. Many were rarely encountered,
    and 27 taxa was the maximum found in a single sample (July 17, 1982). Figure 2
    shows the pattern for the mean number of taxa captured during each time interval
    for the 2 days pooled. The only significant differences (p < 0.05, MWU, ST
    tests) between the 2 days in the number of taxa captured occurred at 0030 and
    0600, when significantly fewer were captured on July 16. When the days were
    pooled, there were significant increases (p < 0-.05; MWU, ST tests) in number of
    taxa in samples collected at 0030 vs. 0230 and in those collected at 1830 vs.
    1930; in addition, significant decreases in number of taxa were observed between
    0500 and 0600, 1930 and 2030, and 2030 and 2300. In general, the fewest taxa
    were captured during the day, the most during the first hour after sunset, and
    intermediate numbers during the rest of the night.

         The mean and standard deviation for the abundance of the more common taxa
    are presented for the different time intervals in table 3. The cyclopoid
    copepod Oithona colcarva (Bowman) was the most abundant of the organisms captured
    at all time intervals except those between 1200-2030, although there was some
    variation in this pattern when the days were considered separately (fig. 1).
    During the morning interval (0600-1200), O. colcarva, foraminifera, and certain
    calanoid and harpacticoid species were themost abundant organisms; however,
    all occurred in relatively low numbers. In the afternoon (1200-1830), foraminifera_

                                           122

        Tab~le  3.   Organismus  captured  at  vdrious   time  intervals   (x- = mean,  SO                                    standard  deviation,   *           present   in  50-75,, of  samlples,
                present   in  75-100'.  of  samples).    Only   the  29  most  common  of  the  73  taxa  recorded  are  presented  here.

                                    Time:        00 30               0230                0500                   0600                  1200                1830                 1930                    2030                   2230
                               #SamplIes:          16                  16                  16                     12                   16                  12                    12                       4                     12
                Taxa                          x      (S)                 )Sri~                    ) i                (S)            K    (SD)           2      (SO)            i     (SD)             i      (SO)                   (so)

        Dithona colvarva                     200   (272)-*         354 (538)-'         186  (260)""         20.2  (18.2)1*         2.8  (6.6)**        3.7    (3.1)**        33.0  (3)NP)""         24.0  (3    )*        46.8  (47.4)**

        Corycaeus spp.                       0.5   (0.61*          0.9  (1.0)*         1.9   (3.5)*          3.8   (4.3)**         0.1  (0.2)          0.7   (0.7)*           1.8   (2.61*              0                   0.1   (0.3)

        Calanoid  "A"                        5.8   (9.8)-*         4.1  (4.3)**       9.8  (21.4)**          2.5   (2.3)*          0.7  (0.61**        0.5   (0.5)-          12.5   (9.9)*-          4.5   (7.7)*           4.1   (5.W)*

        Calanoid  "B"                        5.6   (9.11*          4.5  (6.31*         9.0  (21.8)**         0.5   (0.9)           0.1  (0.2)          0.1   (0.1)            8.8   (9.?)**          7.5   (3J*             0.8   (1.6)

        Microsetella  spp.                   2.3   (2.71*          8.2  (7.2)**        2.5   (3.5)           5.8  (11.21*          0.4  (0.7)          5.0  (13.31*          22.4  (37.2)          43.6  (50.2)*"           0.2   (0.4)

        Hlarpacticoid  "A"                   1.4   (2.41*          2 .7  (2.8)*       5.1   (5.4)*           2.2   (2.31*          0.7  (0.91*         1.3   (3.7)           42.8  (52.4)**        22.6  (25..2)**          5.8   (8.1)**

        Ilarpacticoid  "8"                   0.2   (0.7)          0.4  (1.0)          2.0   (2.8)               0                  0.3  (0.41*         1.2   (1.53*           4.5   (6.51"             0                   2.8   (5.3)*

        liarpacticoid  'C'                   0.4   (0.9)           1.2  (2.2)          0.3   (1.0)           0.5   (1.2)              0                   0                   0.1   (0.4)            3.0   (3.5)--            0

        Copepod  "A"                         0.6   (0.8)           1.2  (1.3)*        0.8   (1.0)            0.7   (1.3)           0.1  (0.1)          0.1   (0.3)            5.7   (7.0)*           7.5   (4.4)**         0.4   (0.6)

         Copepod  nauplii                     0.2   (0.4)          0.5  (0.9)           3.1   (6.91*          0.7   (1.0)           0.1 (0.2)           0.8   (1.7)            9.1  (16.1)           5.0   (7.61*           0.3   (0.7)

         Barnacle nauplii                        0                 0.6  (1.0)          0.2   (0.6)               0                 0.1  (0.1)          0.1   (0.2)             1.3   (1.31*             0                   0.1   (0.3)

         Ostracods                            0.4   (0.8)          0.3  (0.6)          0.5   (1.0)            0.3   (1.2)          0.1  (0.3)          0.1   (0.2)             3.6   (3.6)**           0                    0.4   (0.8)

    "3   Amphipod  "A"                        4.2   (4.0)**         4.2  (4.8)**        2.9   (4.9)"          3.0   (7.9)           0.1  (0.2)             0                   6.9   (6.7)""         3.0   h1.1""           1.9   (2.0)**

         Amphipod  "B"                        0.1   (0.2)          1.3  (1.3)**        0.2   (0.5)            0.7   (1.8)          0.3  (0.4)          0.7   (1.41            8.0  (13.11*           7.0  110.1)-*            0

         Isopods                             0.3   (0.6)           0.2  (0.4)          0.5   (0.7)              0                  0.1  (0.1)          0.2   (0.2 )           2.4   (1.4)""         1.0   (1.2)*           1.4   (1.9)*

         Cumarean "A"                         4.8   (4.31**        4.8  (4.0)**        4.9   (4.7)*-            0                  0.1  (0.1)          0.1   (0.5)           10.6  (16.2)**        24.6  (33.2)**          4.1   (4.8)""

         Cumacean  "8"                        0.7   (1.0)          0.2  (0.5)          0.2   (0.4)              0                     0                   0                   1.4   (2.8)           1.0   (2.0)           0.1   (0.3)

         Tanaids                              0.3   (0.6)          0.4  (0.8)          0.8   (1.11*          0.2   (0.6)              0                   0                   1.3-  (2.?)           0.5   (1.0)           0.3   10.6)

         Mysids                               0.1   (0.5)          0.6  (0.9)          0.7   (1.2)            0.2   (0.6)             0                0.1   (0.1)            1.6   (2.4)       a                         2.4   (4.4)**

         Shrimp                               0.7   (1.0)          1.1 (1.21*          0.3   (0.7)              0                  0.1  (0.2)          0.1   (0.1)            0.7   (1.6)           3.0   (2.6)""         2.0   (2.61*

         Shrimp  larvae                       0.5   (1.2)          0.1 (0.3)           0.4   (0.9)              0                    0                   0                    7.9   (6.9)**           0                   0.5   (0.9)

         Pagurid  larvae                      7.0  (15.0)**        2.4  (4.11*         1.8   (2.71*          0.3   (0.8)           0.1  (0.1)          0.1   (0.1)          19.4  (33.2)           5.0   (5.0)**          2.5   (4.21*

         Decapod zoea                         0.1   (0.3)          1.2  (1.51*         1.8   (3.2)           0.2   (0.6)             0                 0.1   (0.1)           0.7   (1.4)           0.5   (1.0)            0.1   (0.3)

         Miscellaneous  crustaceans    0.7   (1.3)                 3.2  (3.5)""        0.4   (1.2)            0.2   (0.6)          0.1  (0.2)          0.6   (0.81*         15.1  (18.3)**         6.6   (4,l)**           0.7   (0.81*

         Chaetognaths                         0.5   (1.7)          0.4  (0.7)          0.1   (0.4)           0.3   (0.8)             0                 0.1   (0.1)           0.2   (0.6)              00.6   tl.4)

         Polyctiaetes                         0.2   (0.4)          0.7  (0.81*         0.3   (0.6)           0.3   (0.8)           0.1 (0.1)           0.1   (0.1)          17.7  (1.5)""           7.0   (6.6)**         0.8   (0.71*

         Gastropods                           0.4   (0.6)          0.4  (0.7)          0.6   (1.0)           0.3   (1.0)           0.5  (03*         18.8  (23.2)""         30.2  (27.8)**          3.0   (3.81*          0.6   (0.7)

         Sipuncul ids                         0.3   (0.6)          0.1  (0.3)          0.2   (0.6)           0.3   (0.8)           0.2  (0.5)          0.1   (0.2)            4.8  (11.21*         2.5   (2.5)""          0.2   (0.4)

         Fordminiferd                         1.2   (2.0)          2.2  (2.4)**        1.9   (3.2)"          0.8   (1.6)           1.1  (1.2)*"      22.8  (14.7)**           8.5   (8.1)**         3.0   (2.6)**         1.2   )2.1)

    and gastropods dominated the samples.  Samples collected in the hour following
    sunset were dominated by harpacticoids, with a variety of other organisms
    (including 0. colcarva and gastropods) occurring abundantly. Samples taken
    during the second hour after sunset again were dominated by harpacticoids,
    although the relative abundance of the different harpacticoid species switched
    (table 3). Oithona colcarva and a species of cumacean were the other most
    abundant taxa during this second hour.  Oithona colcarva dominated the other
    night time intervals from 2030-0500.

         The relative abundance of nine common taxa (0. colcarva, calanoid copepods,
    harpacticoid copepods, copepod nauplii, amphipods, cumaceans, pagurid larvae,
    polychaetes and gastropods; table 3) were compared using Spearman Rank Corre-
    lations (SRC). Although the abundances were greater at night, the relative
    abundances (% total sample) of these taxa were correlated (p < 0.05) between
    pooled day samples and pooled night samples.  When samples from consecutive
    time intervals were compared, the relative abundances of taxa in all such pairs
    were correlated (p < 0.05) except those from 1800/1830 vs. 1930, and 1930 vs.
    2030. For example, harpacticoids, pagurid larvae, calanoids, and polychaetes
    were relatively more important, while copepod nauplii, amphipods, and gastropods
    were relatively less abundant, at 1930 than at 1800/1830. Cumaceans and
    amphipods increased in relative abundance between 1930 and 2030, while gastropods
    and pagurid larvae decreased in relative numbers over this interval. Therefore,
    the hours around dusk were the only ones where the relative abundance of captured
    organisms differed.

         Differences in the relative abundances of certain taxa reflect their
    different temporal behavior patterns.  Sixty-two percent of the 29 common taxa
    (table 3) were captured in greatest numbers during the first hour after sunset
    (1830-1930), while 17% were captured in greatest abundance during the second
    hour after sunset. The only taxon showing peak abundance during the day was
    foraminifera. Many of the taxa exhibit sustained vertical migration throughout
    the night following the post-sunset pulse (e.g., calanoid "A," amphipod "A,"
    cumacean "A," pagurid larvae in table 3). A few taxa (calanoid "B," decapod
    zoea) were captured most frequently during the last interval of night (0230-0500),
    and many (28%) exhibited a pulse of migration at this time. Only the cyclopoid
    Corycaeus spp. peaked in abundance during the hour prior to sunrise (0500-0600);
    the harpacticoid Microsetella spp. also exhibited a pulse of vertical migration
    at this time. The behavior of 0. colcarva was variable throughout the various
    time intervals (fig. 1).  The mean number of this species captured for both
    nights combined was greatest at 0230; however, that peak reflects an especially
    high number captured on July 17 (I = 638) and a similar pattern was not observed
    on July 16 (fig. 1). Migration rates for this species were high during all
    night hours.

                                       DISCUSSION

         The zooplankton captured by emergence traps in this study do not solely
    represent, either in numbers or composition, the demersal zooplankton (Hobson
    and Chess, 1979; Robichaux, et al., 1981) living within the reef substrata over
    which the traps are placed.  These data do, however, provide information on the
    temporal patterns of migration by the total reef zooplankton which is of value    _
    to studies of reef energetics and the behavior of reef planktivores.

                                           124

         Both Robichaux, et al. (1981) and Youngbluth (1982) addressed the question
    of trap design and both found differences in number and composition of zooplankton
    between sealed and unsealed traps.  Both of these studies, however, were
    conducted over sandy bottoms where a complete seal was possible and zooplankton
    movement through the underlying substrata unlikely.  In this study, both sealed
    and unsealed traps were placed over reef substrata; the former were sealed as
    well as possible through the use of sand and rubble placed over the trap skirts.
    No differences were observed in the numbers of zooplankton captured between the
    two treatments, possibly suggesting that there is more movement by zooplankton
    through interstices of the reef than previously thought. Analysis of differences
    in species composition between the two treatments is currently underway.

         While Alldredge and King (1977) and Porter and Porter (1977) found the
    most zooplankton over structurally complex coral substrata, this was not found
    by Ohlhorst (1980) or Birkeland and Smalley (1981). In the present study,
    there also was no difference in the number of individuals captured over different
    substrata. One contributing factor may be the differential ability to seal
    traps over sand and coral substrata. Robichaux, et al. (1981) and Youngbluth
    (1982) both found that more zooplankton were captured by unsealed traps than by
    sealed traps when both were placed over sand substrata. Youngbluth (1982)
    observed that a gap of 1 cm between trap and substratum resulted in capture of
    significantly greater numbers of zooplankton than a total seal, while there was
    no difference between samples from traps with gaps of 1 and 10 cm. Therefore,
    differences in number of zooplankton collected over different types of substrata
    might be expected when certain treatments are well sealed and others not. If
    the sand traps of Alldredge and King (1977) and Porter and Porter (1977)
    were well sealed in contrast to those over coral substrata, it may be difficult
    for these researchers to compare their substratum treatments.  Birkeland and
    Smalley (1981) compared coral substrata to algal turf pavement and probably
    were able to sample both treatments similarly, since in either habitat a total
    seal is unlikely. Ohlhorst (1980) and this study used unsealed traps to sample
    both coral and sand substrata. These traps captured the zooplankton moving
    along the reef bottom over both types of substrata, and the data indicated that
    the numbers of zooplankton available to planktivores were comparable in both
    habitats. Analysis of the species composition of zooplankton over various reef
    substrata is in progress.

         Fewer zooplankton were captured per hour in this study than in previous
    Caribbean studies by one of the authors (Ohlhorst, 1980, 1982, 1985). The most
    probable explanation lies in the sole use of polyvinyl traps in the previous
    studies. In this study, two polyvinyl traps were used in addition to mesh
    traps (details will be discussed elsewhere); and, while no statistically
    significant differences were found in abundance of plankton between these
    treatments (due to high variance and small sample size of polyvinyl traps), the
    polyvinyl traps usually captured considerably more zooplankton. Both this
     study and the earlier work by Ohlhorst (1980, 1982, 1985) found considerable
     variability between nights sampled.

          The bimodal emergence pattern (post-sunset, pre-sunrise) suggested by
     Glynn's (1973) data from plankton tow nets appears to be supported by this
     study (fig. 1), although more complete information will be available when all
     the samples have been analyzed.  The present study provides the first documentation

                                             125

    of a presunrise emergence of zooplankton and has considerable implications for
    reef bioenergetics and planktivore feeding behavior.

         As in the previous work where plankton were collected over Caribbean reef
    substrata at different time intervals (Ohlhorst 1982), Oithona colcarva, various
    calanoids and harpacticoids, copepod nauplii, amphipods, and polychaetes were
    important components of the fauna. The relative abundances of these organisms
    from the two studies are correlated (p < 0.05, SRC). There are, however,
    differences in the behavior of certain taxa between these studies. In Jamaica,
    for example, the harpacticoid Microsetella spp. migrated in greater numbers
    during the day than at night, while at St. Croix the peak migration was during
    the first and second hour after sunset. Also, isopods were an important
    component of the Jamaican fauna but were relatively rare at St. Croix. Oithona
    colcarva was less abundant at St. Croix than in Jamaica, and its activity
    pattern differed. At Jamaica 0. colcarva was captured in the greatest numbers
    during the second hour after sunset, while at St. Croix the capture rate of
    this copepod was highest from midnight to just prior to sunrise. The sample
    size needs to be increased at both reef locations to determine if these
    differences are real.

         The differences between this study and those over primarily sand substrata
    in the Caribbean (Robichaux, et al., 1981; Youngbluth, 1982) may be related to
    habitat differences and/or trap idesign.  The relative abundance of nine common
    taxa from this study and the unskirted traps of Robichaux, et al. (1981) were
    positively correlated (p < 0.05, SRC). There was no correlation, however,
    between the relative abundance of taxa in this study and that from any of  the
    treatments of Youngbluth (1982).  While harpacticoids were a very important
    component of the reef zooplankton in St. Croix, they did not dominate to
    the degree reported by Robichaux, et al. (1981) and Youngbluth (1982) in the
    Bahama Islands.  The St. Croix sampTes usually were dominated by the cyclopoid
    Oithona colcarva. This is a swarming meroplanktonic species unlikely to be
    captured in traps sealed over sand. Cumaceans and calanoids were important
    over St. Croix reefs, as was found with certain trap designs over sand by
    Youngbluth (1982) but not by Robichaux, et al. (1981).

         This preliminary analysis of data collected from St. Croix is consistent
    with earlier diel studies (Walter, et al., 1981; Ohlhorst 1982) which indicated
    that zooplankton move up into the water column throughout the night with a pulse
    in activity following sunset. Although zooplankton are therefore available to
    planktivores throughout the night, the indication that there are predawn (this
    study) and postdusk peaks of migration is consistent with the hypothesis that
    fish predation is an important selective factor upon zooplankton behavior since
    these dawn and dusk peaks of emergence coincide with periods when there are few
    fish predators (Hobson, 1975).

                                    ACKNOWLEDGMENTS

         This study was made possible by logistical support and a grant (NA 82-AAA-
    01345) provided by NOAA. Additional support and funding were provided by the
    West Indies Marine Laboratory of Fairleigh Dickinson University, St. Croix; the t
    Ecology Center of Utah State University; and the Lerner-Gray Fund for Marine

                                           126

    Research of the American Museum of Natural History, New York. We wish to
    express our appreciation to fellow aquanauts Bonnie K. Schwann and Lee H.
    Somers, who aided in the sampling program; to Stephen K. Boss, who was responsible
    for collecting surface samples and preserving all samples collected; and to
    Lloyd Bennett and Mark T. Segars, who assisted in counting the zooplankton
    samples.

                                   LITERATURE CITED

    Alldredge, A. L., and J. M. King.  1977.  "Distribution, Abundance, and Substrat.
      Preferences of Demersal Reef Zooplankton at Lizard Island Lagoon, Great Barrier
      Reef." Mar. Biol. 41:317-333.

    Alldredge, A., and J. M. King. 1980. "Effects of Moonlight on the Vertical
      Migration Patterns of Demersal Zooplankton." J. Exp. Mar. Biol. Ecol.
      44:135-156.

    Barnes, R. D. 1980. Invertebrate Zoology. 4th Edition. Saunders, Philadelphia.
      1089 pp.

    Birkeland, C., and T. L. Smalley. 1981. "Comparison of Demersal Plankton From
      Comparable Substrata From a High Island and an Atoll." Proc. 4th Int. Coral
      Reef Symp. 1:437-442.

    Glynn, P. M.  1973.  "Ecology of a Caribbean Coral Reef.  The Porites Reef Flat
      Biotope: Part 2. Plankton Community With Evidence for Depletion." Mar.
      Biol. 22:1-21.

    Hobson, E. S. 1974. "Feeding Relationships of Teleostean Fishes on Coral
      Reefs in Kona, Hawaii." Fish. Bull. 72:915-1031.

    Hobson, E. S. 1975. "Feeding Patterns Among Tropical Reef Fishes." Amer.
      Sci. 63:382-293.

    Hobson, E. S., and J. R. Chess. 1978. "Trophic Relationships Among Fishes and
      Plankton in the Lagoon at Enewetak Atoll, Marshall Islands." Fish. Bull. 76:
      133-153.

    Hobson, E. S., and J. R. Chess. 1979. "Zooplankters That Emerge From the
      Lagoon Floor at Night at Kure and Midway Atolls, Hawaii." Fish. Bull. 77:275-
      280.

    Liddell, W. D. 1982. "Suspension Feeding by Caribbean Comatulid Crinoids,"
      pp. 173-182. In: J. M. Lawrence (ed.), Echinoderms: Proceedings of the
      International Conference, Tampa Bay.  A. A. Balkema, Rotterdam.

    McWilliam, P. S., P. F. Sale, and D. T. Anderson. 1981. "Seasonal Changes
      in Resident Zooplankton Sampled by Emergence Traps in One Tree Lagoon, Great
      Barrier Reef."  J. Exp. Mar. Biol. Ecol. 52:185-203.

                                            127

    Ohlhorst, S. L. 1980. "Jamaican Coral Reefs: Important Biological and Physicala
      Parameters."  Ph.D. thesis, Yale University.  147 pp.

    Ohlhorst, S. L. 1982. "Diel Migration Patterns of Demersal Reef Zooplankton."
      J. Exp. Mar. Biol. Ecol. 60:1-15.

    Ohlhorst, S. L. 1985. "Reef Zooplankton Collected Along A Depth Gradient at
     Discovery Bay, Jamaica," pp. 101-116.  In:  M. L. Reaka (ed.), The Ecology of
      Coral Reefs, Symp. Ser. Undersea Res., Vol. 3(1). NOAA Undersea Res. Progr.,
     Rockville, Md.

    Porter, J. W. 1974. "Zooplankton Feeding by the Caribbean Reef-Building Coral
     Montastrea cavernosa." Proc. 2nd Int. Reef Symp. 1:111-125.

    Porter, J. W., and K. G. Porter. 1977. "Quantitative Sampling of Demersal
      Plankton Migrating From Different Coral Reef Substrates." Limnol. Oceanogr.
      22:553-556.

    Porter, J. W., K. G. Porter, and Z. Batac-Catalan. 1977. "Quantitative Sampling
      of Indo-Pacific Demersal Reef Plankton." Proc. 3rd Int. Coral Reef Symp.
      1:105-112.

    Robertson, A. I., and R. K. Howard. 1978. "Diel Trophic Interactions Between
      Vertically-Migrating Zooplankton and Their Fish Predators in an Eelgrass
      Community." Mar. Biol. 48:207-213.

    Robichaux, D. M., A. C. Cohen, M. L. Reaka, and D. Allen.  1981.  "Experiments
      With Zooplankton on Coral Reefs, or, Will the Real Demersal Plankton Please
      Come Up?" Mar. Ecol. 2:77-94.

    Sebens, K. P. 1977. "Autotrophic and Heterotrophic Nutrition of Coral Reef
      Zoanthids." Proc. 3rd Int. Coral Reef Symp. 1:397-404.

    Walter, C., L. Tulane, and J. N. Pasamonte. 1982. "A Preliminary Quantitative
      Study on Emergence of Reef Associated Zooplankton From a Philippine Coral
      Reef." Proc. 4th Int. Coral Reef Symp., 1:443-451.

    Youngbluth, M. J. 1982. "Sampling Demersal Zooplankton: A Comparison of
      Field Collections Using Three Different Emergence Traps." J. Exp. Mar. Biol.
      Ecol. 61:111-124.

                                           128

                      FIELD ANALYSIS OF THE DOMINANCE HIERARCHY
                              OF THE BICOLOR DAMSELFISH
                  STEGASTES PARTITUS (POEY) (PISCES: POMACENTRIDAE)

                                     Yvonne Sadovy1
                                Department of Zoology
                               University of Manchester
                             Manchester, M13 9PL England

                                        ABSTRACT

        The dominance relations of the damselfish Stegastes partitus were examined
    in the field. The dominance hierarchy, based on aggressive interactions, was
    linear and size-dependent, with most aggression between individuals most similar
    in size and least between those most dissimilar in size. These results show
    both similarities to and differences from results obtained in a very similar
    earlier study on the same species but conducted entirely in the laboratory.
    The importance of field studies in assessing the degree of reliability of
    results obtained under artificial conditions is emphasized.

                                      INTRODUCTION

         Many species of animals display a dominance hierarchy among members of
    social units.  A group of animals may be said to have a dominance hierarchy if
    the interactions between individuals allow some to have priority over others
    under certain circumstances. The most simple hierarchy is defined as follows:
    individual A dominates all members of a group; another animal B dominates all
    members except A, and so on to the last member, omega, which dominates no other
    individuals. If this relationship holds, then the hierarchy is said to be
    linear (Chase,'1974).

         Considerable research has examined the dominance relations of a wide
    variety of animal species. However, the majority of studies have been conducted
    in the laboratory or under other artificial conditions.  In studies carried out
    both in the field and in the laboratory on the same species, there often have
    been discrepancies in the conclusions. Thompson (1960) found that laboratory
    populations of house finches had a hierarchy dominated by females, but that
    field populations did not show this pattern. In some primates, a different
    form of social structure was evident between captive animals and the same
    species in the field (Rowell, 1967; Hinde, 1974). In the baboon, Papio anubis,
    interactions were about four times as frequent among captive animals as among
    individuals observed in the field (Rowell, 1967). Among the fishes, Myrberg
    (1972a) conducted a field and laboratory study of territoriality and social
    hierarchy in the bicolor oamselfish (Pomacentridae), Stegastes (= Eupomacentrus)

          1 Present address: Department of Marine Sciences, University of Puerto
    Rico, Mayaguez, Puerto Rico 00708.

                                            129

    partitus. However, limitations of resolution in the underwater camera used for
    field observations precluded analyses as detailed as those obtained during the
    laboratory section of the work. Therefore, the two parts of the study were not
    strictly comparable.

         Many damselfish are territorial, and the bicolor, like several other
    closely related species, defends a territory which it infrequently leaves. in
    the field, several or many such territories may be found in close proximity,
    forming colonies on suitable substrate. Reproduction usually occurs within
    colonies, which consist of both males and females. Colony members frequently
    interact with each other close to territory borders. In small colonies, all
    colony members may interact with one another, whereas in very large colonies
    many individuals rarely come into contact. Small colonies are, therefore,
    particularly useful for studies on intracolony social relationships.

         The aims of the present study were: (a) to examine in detail the aggressive
    social interactions of small colonies of the bicolor damselfish in the field
    and (b) to compare the dominance system of these colonies with hierarchies
    found in the laboratory (Myrberg, 1972a).

                                        METHODS

         The study was conducted from October 9-16, 1980, from the NOAA underwater
    facility, HYDROLAB, situated in 50 feet of water off the north coast of St.
    Croix in the U.S. Virgin Islands.

         Seven small damselfish colonies, each confined to a patch of coral rubbleW
    and separated from each other by clear areas of sand, were selected. The
    colonies were small enough to permit interactions between all colony members.
    Aggressive social interactions ("chases") were recorded between all individuals
    in each colony, where both the giver and receiver of each "chase" were noted.
    A chase is defined as a rapid swim towards a fish that is moving away or that
    starts to move away from the chaser (Myrberg, 1972b).

         Each colony contained six to eight individuals, most of which were
    distinguishable on the basis of size. However, very small fish ("tinies") were
    difficult to identify individually. Consequently, in the colonies containing
    more than one "tiny," i.e., in colonies larger than six fish, the number of
    interactions per tiny was determined by dividing the sum of chases given or
    received by all tinies of a particular colony by the number of tinies in that
    colony. Therefore, in each colony larger than six individuals, the rank (see
    below) of six consisted of an average interaction rate per tiny.

         Data were taken during both the morning and afternoon over a period of
    3-6 days and until at l'east 65 interactions had been noted for each colony
    (average observation time per col~ony = 131 minutes; range = 85-240 minutes).
    Since colonies were monitored for varying lengths of time, the observations
    were standardized to give the number of chases per 100 minutes per colony so
    that the colonies could be compared directly.

         Matrices were constructed for the chase data from each colony by ass ignin*
    dominance ranks to every colony member. For example, rank I chased each other*

                                            130

    colony member more than any member chased it; rank 2 chased each colony member
    more than any other member chased it, except for rank 1.

         For analysis, data on chases were ordered by rank, and all data for each
    rank were summed across all 7 groups. The data were then divided into three
    categories: (a) the number of chases received by each rank; (b) the number of
    chases given by each rank; and (c) the number of chases given by each rank to
    each other rank. Each of these categories was analyzed using the Kruskal-Wallis
    one-way ANOVA to determine whether or not there was a significant difference
    among ranks, i.e., an H-value giving p < 0.05. If so, then the data were
    subjected to a nonparametric version of the Newman-Keuls Multiple Range test
    (Zar, 1974) to determine how the distribution of chases varied among ranks
    (significance level, p < 0.05).

                                        RESULTS

         For each colony, a distinct size-dependent social hierarchy was apparent;
    it was highly linear with proportionally very few reversals (4.5%). A reversal
    is a chase directed at an individual higher in the hierarchy than the chaser.

         Figure I shows the distribution of chases received by each rank (category
    a). This distribution is not homogeneous (Kruskal-Wallis, p < 0.001). The
    nonparametric Multiple Range test showed that ranks 3 and 4 received the most
    chases; ranks 2, 5, and 6 received less than 3 and 4 but more than rank I (p <
    0.05 in each case).

         Figure 2 shows the distribution of chases given by each rank (category b).
    This distribution is not homogeneous (Kruskal-Wallis, p < 0.001). The
    nonparametric Multiple Range test showed that ranks 1, 2, and 3 gave the most
    chases; rank 4 gave fewer chases but more than ranks 5 and 6 (p < 0.05 in each
    case).

         Figure 3 shows the distribution of chases from each rank to each rank
    below it in the hierarchy (category c). The distribution is not homogeneous
    for ranks 1 to 4 (Kruskal-Wallis, p < 0.01). In most cases, each rank directed
    most chases to its closest ranking subordinate and least to the individual
    ranked farthest from itself. See figure 3 for the significant differences
    shown by the nonparametric Multiple Range test (p < 0.05 in each case).

                                      CONCLUSIONS

         The analyses of the distribution of chases given and received show that
    there is a distinct pattern to intracolony aggression:

          (a) there is a strong size-dependent social hierarchy which is linear
    with few reversals;

          (b) individuals chase those closest to and just below themselves in rank
     most frequently and those furthest in rank least frequently;

          (c) the highest ranking individuals (1, 2, and 3) chase more than other
     ranks.  Lower ranking individuals chase progressively less the lower their rank;

                                             131

            40

            32-
                 H~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~
                 H~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~

      > I

                              / I                    I         I
                                     I              ~~~~~~~~~~~~~~I
                                     I              ~~~~~~~~~~~~I

                                          '-                  11
           16 I
                                          II

                        1         2       3          4         5          6
                                       FISH  RANK

    Figure 1.--Chases received by each rank plotted as medians and interquartile
      ranges. The asterisks denote significant differences between adjacent
     points (p < 0.05); e.g., rank 2 received more chases than rank 1.
                                         132

                          T
              40
                                    T
                          l          l

                          l          l
                          I          I

              32         4

             >~~~~~~~~~~~~~~~
        H

                 C~~~~~~~~~~~
          o                X      6    II

                                         I~~~~~
                 $   ~~~~24  6              \ I
        4                  I           l     \  I
             H F    IS  IN
                          I                   i
        0

             X           ~~~I  Ix
                          I          I

           (p < 0.05); e~~~~~~~~g., rak4gvsfwrchsstaak3
              1.6  II '               ''1

                          I.

                                 I   I       J~~~~~~~~~~.

                          1         2        3         4          5         6
                                       FISH RANK
    Figure 2.--Chases given by each rank plotted as medians and interquartile
      ranges. The asterisks denote significant differences between adjacent points
      (p <~ 0.05); e.g., rank 4 gives fewer chases than rank 3.
                                          133

     120
                                      RANK 2
                                      x

     100

      so  80RANK 3

      60

                                                    x
                                                                       RANK 4

      20

                       2            3                4             56

                                   FISH RANK

    Figure 3.--Chases given by each rank to each rank below it.  Data from all seven
     groups are summed. Each line represents the chases given by a particular rank
     to all ranks below it; e.g., rank I chased rank 2 a total of 96 times. The
     asterisks denote significant differences (p < 0.05) between adjacent points;
     e.g., rank I chased rank 2 significantly more than it did rank 3.

        (d) ranks 2, 3, and 4 receive most chases and ranks 1, 5, and 6, the least.

        It is clear that in'the bicolor damselfish, size plays an important role
    in intraspecific aggression. As in many other species, dominance relations are
    strongly correlated with body size (beetles, Beebe, 1947; lobsters, Fielder,
    1965; voles and deerniice, Grant, 1970). Aggression is most intense between
    individuals of similar size and least intense between individuals most dissimilar
    in size (Noble, 1939; Collias, 1944; Miller, 1964; Coates, 1977).

        The importance of size in the dominance relations of damselfish may result i
    from size-dependent competition for certain resources. Individuals of different

                                       134

    sizes may have different food or shelter requirements (Rasa, 1969; Emery, 1973).
    Several studies have reported that in pomacentrids, small individuals often
    share the territory of an adult conspecific (Clarke, 1970; Emery, 1973; Sale,
    et al., 1980), either because the adult tolerates them or because of "topological
    -ce--Tion" (Sale, et al., 1980) whereby they can avoid the adult by using space
    in which they cannot t~pursued. The low number of chases given and received
    by these small individuals implies that they are not attempting to compete
    aggressively with the larger fish for the space they share. Large size in male
    bicolors appears to be one of the factors associated with high reproductive
    success (Schmale, 1980). In order to establish the significance of size and
    how it relates to aggression in this species, detailed studies on the feeding,
    reproduction, and use of space and shelter are necessary. Account should be
    taken of fish size, stage of maturation (juvenile, adult; reproductive,
    nonreproductive), and sex.

         The present study demonstrates both similarities and differences between
    field and laboratory results on the dominance relations of the bicolor damselfish.
    Previous work on this species (Myrberg, 1972a) focused on two distinct time
    periods: reproductive and nonreproductive. The distribution of aggression
    between colony members was found to differ markedly between these two periods
    in the laboratory phase of the study. The field phase of the study covered
    only the reproductive period and was much less detailed than the laboratory
    phase because of the inability of the underwater camera to record all aggressive
    interactions between colony members, especially those involving very small
    fish. The present study is considered equivalent to the nonreproductive period
    of the Myrberg study, since little courtship activity and no egg-guarding
    behavior by males were observed.

         The present field analysis and Myrberg's laboratory results for the
    nonreproductive period show the following similarities: There is a strong size-
    dependent linear dominance hierarchy with a very low percentage of reversals;
    the highest ranking individuals did the most chasing and the lowest ranks the
    least; the middle ranks received the most chases and rank 1 and the lowest
    ranks the least.

         However, there were two differences between the two studies. First, the
    rate of interactions was markedly higher in the laboratory study, in which a
    rate of 10 chases per individual per hour was recorded as opposed to the 1.5
    chases per individual per hour in the present study. This is a common difference
    between field and laboratory studies and may be due to: (a) the inability of
    small individuals to escape those chasing them in an aquarium, (b) the lack of
    interspecific interactions in the laboratory, and/or (c) the lack of space
    available per individual in an aquarium, although both the present study and
    Myrberg's laboratory study had similar fish densities of 0.2 m2 (Myrberg) and
    0.1-0.2 m2 (this study).

          Second, the relative distribution of chases given by each rank to each
    other rank below it in the hierarchy differs between the two studies. In the
     laboratory (Myrberg, 1972a), the distribution of chases among individuals showed
     no clear pattern, except -or one fish, YB, which directed successively fewer
     chases at individuals ranked progressively further away from itself.  This 'YB'
     pattern of chasing was seen very clearly and consistently in all colony members
     of the present study.

                                             135

         It is of considerable interest that during the reproductive period of
    Myrberg's study, the pattern of intracolony aggression in the laboratory and
    possibly in the field differed from that recorded during the nonreproductive
    period, with more aggression being directed towards the lowest ranking individuals
    than towards those closest in rank. Field work similar to that of the present
    study needs to be conducted during the reproductive period to establish if this
    difference is significant and related to the phase of the reproductive cycle.

         In conclusion, the dominance relations in the bicolor damselfish during
    the nonreproductive period show both similarities and differences when laboratory
    and field studies on colonies of similar size are compared. The nature of
    these differences implies that the laboratory may be used for detailed work
    impossible to carry out in the field, but that laboratory results must be
    interpreted with caution and should not be used as the sole source of information
    on the ecological significance of dominance relations. The importance of
    parallel field and laboratory studies is emphasized, since it is evident that
    many factors may influence intracolony aggression.

                                    ACKNOWLEDGMENTS

         I wish to thank Kimberly Leighton-Boulon for her invaluable help during
    the field study and Ileana ClaviJo, who did the organizational work prior to
    the HYDROLAB mission. I also wish to thank the HYDROLAB staff in St. Croix for
    making the mission so successful. For suggestions and comments on the manuscript,
    I am very grateful to D. Y. Shapiro and G. R. Mitcheson.

         The study was carried out with the financial assistance of NOAA and of the
    SERC of Great Britain Grant No. 78307917.

                                    LITERATURE CITED

    Beebe, W.  1947.  "Notes on the Hercules Beetle, Dynastes hercules (Linn.) at
       Rancho Grande, Venezuela, With Special Reference to Combat Behavior."
       Zoologica, New York 32:109-116, .

    Chase, I. 0. 1974. "Models of Hierarchy Formation in Animal Societies."
       Behav. Sci. 19:374-382.

    Clarke, T. A. 1970. "Territorial Behavior and Population Dynamics of a
       Pomacentrid Fish, the Garibaldi Hypsypops rubicunda." Ecol. Monogr. 40:189-
       212.

    Coates, D. 1977. "The Social Behaviour of the Humbug Damselfish Dascyllus
       aruanus (Pieces: Polacentridae), With Notes on Two Other Species (D.
       reticulatus and D. trimaculatus)." M. Sc. Thesis, Univ. Newcastle Upon
       Tyne, England. 750 pp.

    Collias, N. E. 1944. "Aggressive Behavior Among Invertebrate Animals."
       Physiol. Zool. 17:83-123.

                                            136

    Emery, A. R. 1973. "Comparative Ecology and Functional Osteology of 14 Species
       of Damselfish (Pisces: Pomacentridae) at Alligator Reef, Florida Keys."
      Bull. Mar. Sci. 74:649-770.

    Fielder, D. R. 1965. "A Dominance Order for Shelter in the Spiny Lobster
      Jasus lalandei (H. Milne-Edwards)." Behaviour 24:236-245.

    Grant, P. R. 1970. "Experimental Studies of Competitive Interactions in a Two-
       Species System: II. The Behaviour of Microtus, Peromyscus and Clethrionomys
       species."  Anim. Behav. 18:411-426.

    Hinde, R. A. 1974. Biological Bases of Human Social Behaviour. McGraw-Hill
       Book Co., Inc., New York. xvi + 462 pp.

    Miller, R. S. 1964. "Ecology and Distribution of Pocket Gophers (Geomyiidae)
       in Colorado." Ecology 45:256-272.

    Myrberg, A. A., Jr. 1972a. "Social Dominance and Territoriality in the Bicolor
       Damselfish Eupomacentrus partitus (Poey) (Pisces: Pomacentridae)." Behaviour
       41:207-231.

    Myrberg, A. A., Jr. 1972b. "Ethology of the Bicolor Damselfish Eupomacentrus
       partitus (Pisces: Pomacentridae): a Comparative Analysis of Laboratory and
       Field Behavior." Anim. Behav. Monogr. 5:199-283.

    Noble, G. K. 1939. "The Role of Dominance in the Social Life of Birds." Auk
       56:263-273.

    Rasa, O. A. E. 1969. "Territoriality and the Establishment of Dominance by
       Means of Visual Cues in Pomacentrus jenkinsi (Pisces: Pomacentridae)."  Z.
       Tierpsychol. 26:825-845.

    Rowell, T. E. 1967. "A Quantitative Comparison of the Behaviour of a Wild and
       a Caged Baboon Troup." Anim. Behav. 15(4):499-509.

    Sale, P. F., P. J. Doherty, and W. A. Douglas. 1980. "Juvenile Recruitment
       Strategies and the Coexistence of Territorial Pomacentrid Fishes."  Bull.
       Mar. Sci. 30:147-158.

    Schmale, M. C. 1980. "A Preliminary Report on Sexual Selection in the Bicolor
       Damselfish, Eupomacentrus partitus." Bull. Mar. Sci. 30:328 (abstract).

    Thompson, W. L. 1960. "Agonistic Behavior in the House Finch: II. Factors
       in Aggressiveness and Sociality." Condor 62:378-402.

    Zar, J. H. 1974. Biostatistical Analysis. Prentice-Hall, Inc., Englewood
       Cliffs, N.J. xic + 620 pp.

                                           137

    I 0

     0

     0

    A COMPARISON OF FORE AND BACK REEF POPULATIONS OF DIADEMA ANTILLARUM PHILIPPI
        AND EUPOMACENTRUS PLANIFRONS CUVIER AT ST. CROIX, U.S. VIRGIN ISLANDS1

                     C. Lance Robinson2 and Ann Houston Williams

                           Department of Zoology-Entomology
                       Alabama Agricultural Experiment Station
                                  Auburn University
                                Auburn, Alabama 36849

                                        ABSTRACT

         The community structure of populations of threespot damselfish (Eupomacentrus
    planifrons) and the black sea urchin (Diadema antillarum) in fore reef and back
    reef habitats of Teague Bay reef off the West Indies Laboratory, St. Croix,
    U.S. Virgin Islands, was examined during July and August 1981. All populations
    studied occupied patches of Acropora palmata at depths of 3-5 m and were observed
    with SCUBA.

         Field observations indicated that populations of Diadema within back and
    fore reef habitats differed in the following ways: 1) mean urchin test diameter
    was significantly larger on the back reef (X = 74.48 mm) than on the fore reef
    (7 = 47.94 mm), 2) mean urchin density, sampled during daylight hours was lower on
    the back reef (X = 2.3 urchins m'3) than on the fore reef (X = 5.04 urchins m'3),
    and 3) on the back reef 60.8% of the urchins were found on coral branches more
    than 60 cm above the substrate, whereas on the fore reef 74.5% of the urchins
    were found below that level. Damselfish densities were significantly lower on
    the back reef (X = 0.18 m-3 vs. 0.31 m-3) and algal lawns were significantly smaller
    (X = 146.1 cm2 vs. 349.1 cm2) than on the fore reef. Back reef damselfish were
    more aggressive (7 bites min'1 = 27.6) than those on the fore reef (X bites
    min-1 = 6.6).

         These differences in community structure may indicate differing levels of
    competitive interaction between threespot damselfish and Diadema. The higher
    energy environment of the shallow fore reef may effectively reduce the size of
    Diadema by reducing urchin grazing. Thus, competitive interactions between
    threespots and Diadema may be lower on the fore reef than on the back reef.

                                      INTRODUCTION

         The community structure and competitive interactions between threespot
    damselfish (Eupomacentrus planifrons Cuvier) and the herbivorous sea urchin
     (Diadema antillarum Philippi) have been documented in the East Back Reef of

    1 Contribution No. 130 from the West Indies Laboratory, Fairleigh Dickinson
        University.
    2 Present address: 41 Wagon Wheel Drive, Semmes, Alabama 36575.

                                             139

    Discovery Bay, Jamaica, West Indies (Williams, 1978, 1979, 1980, 1981).  The
    damselfish maintains algal lawn territories on dead branches of staghorn coral
    (Acropora cervicornis Lamarck) and actively excludes herbivores, such as Diadema,
    from these territories (Myrberg and Thresher, 1974; Williams, 1979). Through
    these competitive interactions, habitat partitioning occurs which affects the
    distribution and abundance of Diadema on the reef (Williams, 1979, 1981).
    Because of its influence on the distribution of grazing sea urchins, the
    damselfish is considered to be a keystone species (Williams, 1980). Sammarco
    and Williams (1982) also have suggested that E. planifrons indirectly affects
    shallow reef coral community structure by infuencing the differential success
    of coral recruitment and algal growth both within and outside damselfish
    territories.

         This preliminary study examines the structure of two similar communities
    and the interactions of these species on the reefs of St. Croix, U.S. Virgin
    Islands, to determine whether or not damselfish occupy a similar role in reef
    communities other than Jamaica. Both fore and back reef communities were
    examined for comparison with each other and with previous observations from
    Jamaica.

                                 MATERIALS AND METHODS

         Field studies were conducted on the bank barrier reef (Adey, 1978) located
    north of West Indies Laboratory on the northeast coast of St. Croix, U.S.V.I.
    (17�45.5'N, 64�35.5'W). The reef studied was representative of the area, with
    the back reef composed of elkhorn coral (Acropora palmata) in the shallower
    areas and various head corals (Montastrea annularis, Diploria spp., etc.) found
    in deeper water. Millepora complanata and A. palmata were found in the high
    energy areas of the crest, while A. palmata, A. cervicornis, and several species
    of head corals prevailed on the fore reef (Ogden, 1974).  A study site was
    established west of the WIL pier at the site of solar panels on both fore and
    back reefs in comparable water depths. This area was chosen because of
    accessibility of the fore reef through a swim cut in the reef crest. All
    observations and experiments were carried out between 1030 and 1545 hr using
    SCUBA.

         Study of the interactions between threespot damselfish and Diadema was
    restricted to those which took place among branches of A. palmata, an apparent
    preferential substrate for threespots in the absence of-. cervicornis (Williams,
    pers. obs.; Itzkowitz, 1974). Individual stands of A. paTmata were selected for
    observation by the following criteria: at least twothreespot damselfish per
    coral stand; coral stand boundaries easily discernible; and coral stands located
    in -3 to -5 m of water. Aluminum tags were used to identify the A. palmata
    stands. Length, width, and height of each stand were recorded and used in
    calculating densities of damselfish and urchins (number of individuals m'3).
    Wilcoxon rank sum tests were used to compare densities and coral stand measure-
    ments between fore and back reefs. Correlation analysis (Sokal and Rohlf,
    1969) was utilized to examine relationships between the species' densities.

         Vertical distributions of urchins within coral stands were recorded by
    suspending a leaded line, calibrated in centimeters, among the branches of             0

                                            140

    coral and counting individuals located within 5 cm intervals above the substrate.
    A G-test of independence (Sokal and Rohif, 1969) was used to compare distribu-
    tions of urchins above and below 60 cm coral height on both sides of the reef.

         A comparison of urchin populations located in the two habitats was made by
    examining the size class structure of Diadema. Haphazard samples of individuals
    from each population were collected by hand from several areas east and west of
    the study sites. Greatest test diameter was measured (to the closest 0.01 cm)
    across the ventral surface using vernier calipers for 106 individuals from both
    fore and back reefs. Mean test diameters were compared using a Student's t-
    test, and size class structures were determined by the method of Harding (1949).

         A measure of the relative aggression of threespots toward Diadema in both
    habitats was recorded.  These data were obtained by placing an urchin representa-
    tive of the mean size in the algal lawn of a haphazardly chosen damselfish and
    counting the number of bites on urchin spines made by the damselfish in 1 min
    or until the urchin was outside the algal lawn. Relative levels of aggression
    were compared using a Student's t test. All statistical computations were
    completed by using the Statistical Analysis System (SAS).

                                        RESULTS

         Stands of elkhorn coral were significantly smaller in total volume on the
    fore reef than on the back reef due to significantly smaller width dimensions
    (table 1).  Densities of Eupomacentrus planifrons associated with the fore reef
    stands were significantly higher than those of the back reef. Algal lawns were
    significantly larger on the fore reef than on the back reef (table 1). Although
    more coral substratum apparently was available in the back reef, fewer fish
    maintained smaller territories in this region.

         The density of Diadema was higher on the fore reef than on the back reef
    (table 1). Additionally, mean test diameter was significantly smaller (t =
    18.64; df = 191; p < 0.0001) on the fore reef (: = 47.94 mm) than on the back
    reef (: = 74.48 mm). Population size class structure exhibited no apparent
    differences between habitats (fig. 1). When all urchins from both habitats are
    considered, a probable negative relationship may exist between the size and
    density of Diadema. However, because of the limited data available on mean
    test diameter and mean density of Diadema in each habitat (N = 2), correlation
    analysis could not be completed.

          Although significance was not testable due to small sample sizes (N = 3),
    an apparent negative correlation was demonstrated between the density of Diadema
    and the density of E. planifrons on the back reef, but this was not the case on
     the fore reef (fig. 2).  Thus, in the back reef habitat where densities of E.
     planifrons were low and algal lawns were small, small numbers of large Diadema
     were found.

          Relative aggression levels of E. planifrons toward Diadema were found to
     be much higher (t = 5.25, df = 13,   <0.0002) on the back reef (X bites
     min-1 = 27.6) than those exhibited by threespots on the fore reef (X bites
     min-1 = 6.6) (fig. 3). Thus, intensity of the behavioral interaction between

                                            141

    Table 1.--Comparison of communities on fore and back reefs at St. Croix,
       U.S.V.I.  Data are means (+ SE) and were tested with Wilcoxon rank sum tests
       (Z statistic) for all tests except for algal lawn, where a t test was used.

                             Fore Reef          Back Reef      Test Statistic        P

     A. palmata (m3)

     Volume                     9.5(1.3)         16.79(2.52)        Z = 1.75       0.04

          N                     3                 3

     A. palmata (m)

     Height                     1.42(.03)         1.5(.05)          Z = 1.03       n.s.

          N                    3                  3

     A. palmata (m)

     Width                      1.87(.19)        2.63(.28)          Z = 1.75       0.04

          N                     3                  3

     Threespot Density

     No. ind.m                  0.31(.04)        0.18(.01)          Z = 1.75       0.04

          N                    3                  3

     Diadema Density

     No. ind.m 3                5.04(1.86)        2.30(.47)        Z = -1.75       0.04

          N                    3                  3

     Algal lawn

      (cm2)                   349.11(44.57)      146.11(12.89)      t = -4.38   < 0.002

           N                    9                  9

                                                142

      12    Fore Reef
       11
      10
       9
       8
       7
       6
       5
    < 4
       4 -   - -
    U 3
    <: 2
      a ,      I-
    LA.I
    0
     = 8     Back Reef
    .Z 7

        5
        4
        3
        2                           [i

                           n mnM    n nd  l                                        fn
               25   30   35   40   45   50   55   60   65   70   75   80   85

                               TEST DIAMETER [mml

    Figure 1.--Frequency distribution of size classes (mm) for Diadema occurring
       on the fore reef (top) and back reef (bottom) of St. Croix; N = 106 for
       each site.

    threespots and Diadema was strongest, and Diadema density varied inversely with
    damselfish density on the back reef.
         Although the volume of A. palmata per stand differed in the two habitats,
    the heights of A. palmata stands were not significantly different (table 1).
    However, within T. palmata stands on the fore and back reefs, the vertical
    distribution of Dadema was found to differ significantly (table 2).  A large

                                             143

                                              o                                             �
          8

    E

    zoo4                                                                                     o
    a    \

    a                     a
         31

         0-
          0.C1            0.20            0. 2             0.30             0.35            0.40

          DAMSELFISH  DENSITY (no. ind. 3)
    Figure 2.--Relationship between density of Diadema (no. inds. m-3) and threespot
       damselfish (no. inds. m-3). Closed circles ='back reef populations; open
       circles -= fore reef populations.           144

             30                   S.E.=2.68

             28                          X  27.6

             26

             24

          " 22

             20
          ,I)
          I- 18

            16

          Z  14
          0
          12
          AdI 10
            10 8S.E.=1.57

                                                      I        X =6.6
              6
                                                      I
              4

              2

              0
                              B                         F

    Figure 3.--Mean relative aggression level (bites min-1) of threespot damselfish
      toward urchins on the fore reef (F) and back reef (B) of St. Croix. Fore
      reef N = 5, back reef N = 10.

    proportion of the Diadema (60.8%) tended to occupy the upper branches of coral
    ( > 65 cm in height) on the back reef, while 74.5% of the urchins on the fore
    reef were located on coral branches less than 60 cm above the substrate.
    Differences in sampling times cannot account for these differences, since all
    observations but one were made between 1545 and 1830 hr. One back reef

                                         145

    Table 2.--Comparison of proportional  (%) vertical distributions of Diadema
      within stands of A. palmata on fore and back reefs. A G-test compared
       individuals found at heights of < 60 cm or > 65 cm (G = 10.76, p < 0.005,
       df = 1).

       Ht.                      Fore Reef                  Back Reef
       (cm)

      15-30                        13.9                        19.6

      35-60                        50.6                        19.6

      65-90                        21.5                        12.2

      95-135                       13.9                        48.6

        N                          79                         107

                                                                                     m

    observation was made at 1030 hr; however, it did not differ from samples taken
    later in the same area. Thus, differences in vertical distribution must have
    been due to differing urchin behavior.

                                       DISCUSSION

         Although the damselfish-Diadema assemblages in the fore and back reef
    environments at St. Croix appear similar in population composition, the structures
    of these two assemblages differ in population abundances, distributions, and
    mean size. These differences may be the result of differing physical factors
    and/or biological interactions.

         Colonies of Acropora palmata were similar in height but significantly
    smaller in volume on the fore reef (table 1).  The difference in volume was
    attributable to differences in width of coral stands. This structural difference
    in the corals may be related to the higher wave energy on the fore reef.  Waves
    can cause considerable damage to fore reef corals, as evidenced by abundant
    coral rubble found on the fore reef substratum (Robinson, pers. obs.; Van den
    Hoek, et al., 1978). Rogers, et al. (1982) documented that storm damage on the
    reefs of St. Croix was due to fractures of the distal ends of A. palmata
    branches.

         Mean test diameters of Diadema from the fore reef are smaller and those
    from the back reef are larger in the present study than those reported by Ogden,

                                            146

    et al. (1973) on patch reefs at St. Croix (7 = 59 mm).  They also are slightly
    larger than mean diameters measured by Bauer (1980) on the back reef at St.
    Croix (7 = 52.3 mm). Such differences may indicate differences in the availability
    of food, mortality, or adaptations to energy levels in the three different
    habitats.

         The differences between fore and back reef observed in this study also may
    reflect differences in the availability of food, mortality, and/or adaptations
    to differing wave energy levels. Preliminary data indicate that smaller urchins,
    such as those found on the fore reef, may feed at a faster rate than the larger
    urchins of the back reef (Robinson, unpub. data). However, the larger algal
    lawns also found on the fore reef indicate a reduced grazing pressure by urchins
    (table 1). Van den Hoek, et al. (1975, 1978) attributed a higher biomass of
    algal turf to lower grazing pressure from Diadema in similar high energy regimes.
    Thus, the smaller body size of urchin populations found on the fore reef may be
    due to food limitation (Carpenter, 1981) even though abundant food is present
    (i.e., larger damselfish lawns, table 1). High wave energy may force urchins
    to remain lower in the coral matrix, preventing them from reaching this potential
    food source (table 2). High energy regimes either may select for individuals
    with smaller test diameters (i.e., smaller surface area for exposure to wave
    energy) or may result in smaller urchins by reducing their effective feeding
    periods. Lissner (1980) reported an inverse relationship between turbulence
    and activity of the urchin Centrostephanus coronatus.

         Williams (1981) demonstrated that Diadema and threespot damselfish in
    Jamaica were actively involved in competition for either food or space in the
    back reef. This competition affected the amount of algae accumulating outside
    of algal lawns. The relative level of competition in differing environmental
    conditions was not measured in that study. We believe that the lower levels of
    aggression in damselfish (fig. 3) and their larger lawns on the fore reef
    provide evidence of reduced competitive interactions in this environment as
    compared to the back reef. Additionally, larger lawns and a greater food
    supply may be necessary for damselfish to maintain themselves in this high
    energy regime. Reduced competition may be the result of environmental mediation,
    whereby high wave energy reduces urchin grazing and thus increases the size of
    damselfish territories.

         Sammarco, et al. (1974) and Sammarco (1980) indicated that, at high
    densities of Diadema, successful settlement of corals was inhibited; in contrast,
    maximum diversity of successfully settled coral spat was achieved at lower
    densities of Diadema. Sammarco and Williams (1982) also indicated that settlement
    success varied within and outside of damselfish algal lawns due to alterations
    in urchin grazing levels. Similar factors affecting the settlement success of
    corals will vary between fore and back reef habitats at St. Croix and may
    account for differences in adult coral diversities in these two environments.

                                    ACKNOWLEDGMENTS

         We wish to thank the staff and researchers of the West Indies Laboratory
    of Fairleigh Dickinson University. Special thanks go to Drs. J. C. Ogden, J.
    Ebersole, and J. Morin for their advice and helpful comments. We thank R.

                                            147

    Carpenter, J. Sutherland, R. Lishak, W. Mason, and two anonymous reviewers                B
    for critical reviews of the manuscript.  We especially appreciate the assistance
    of J. Ebersole and J. Sobel in diving. Financial support was provided for one
    of us (AHW) by the Department of Zoology-Entomology, Auburn University, especially
    through the generosity of Dr. George Folkerts.

                                   LITERATURE CITED

    Adey, W. H. 1978. "Coral Reef Morphogenesis: A Multi-Dimensional Model."
       Science 202:831-837.

    Bauer, J. C. 1980. "Observations on Geographic Variations in Population
       Density of the Echinoid Diadema antillarum Within the Western North Atlantic."
       Bull. Mar. Sci. 30:509-515.

    Carpenter, R. C. 1981. "Grazing by Diadema antillarum (Philippi) and Its
       Effects on the Benthic Algal Community.'  J. Mar. Res. 39:749-765.

    Harding, J. P. 1949. "The Use of Probability Paper for the Graphical Analysis
       of Polymodal Frequency Distributions." J. Mar. Biol. Assn. U.K. 28:141-153.

    Itzkowitz, M. 1974. "A Behavioral Reconnaissance of Some Jamaican Reef Fishes."
       Zool. J. Linn. Soc. 55:87-118.

    Lissner, A. L.  1980.  "Some Effects of Turbulence on the Activity of the Sea
       Urchin Centrostephanus coronatus Verrill." J. Exp. Mar. Biol. Ecol. 48:185-
       191.

    Myrberg, A. A., and R. E. Thresher. 1974. "Interspecific Aggression and Its
       Relevance to the Concept of Territoriality in Reef Fishes." Amer. Zool.
       14:81-96.

    Ogden, J. C. 1974. "The Major Marine Environments of St. Croix." In: H. G.
       Multer and L. C. Gerhard (eds.), Guidebook to the Geology and EcoT2gy of
       Some Marine and Terrestrial Environments. West Indies Laboratory, Fairleigh
       Dickinson University, Spec. Pub. 5:5-19.

    Ogden, J. C., D. P. Abbott, and I. Abbott. 1973. The Population of Diadema
       antillarum on Patch Reef #3. Studies on the Activit and Food of the Echinoid
       Diadema antT'larum PRiippi on a West Indian Patch Reef-' West Indies
       Laboratory, Fairleigh Dickinson-Un-i versity,Spec. Pu7 -2:24-28.

    Rogers, C. S., T. H. Suchanek, and F. A. Pecora. 1982. "Effects of Hurricanes
       David and Frederic (1979) on Shallow Acropora palmata Reef Communities:
       St. Croix, U.S. Virgin Islands." Bull. Mar. Sci. 32:532-548.

    Sammarco, P. W. 1980. "Diadema and Its Relationship to Coral Spat Mortality:
       Grazing, Competition, and Biological Disturbance." J. Exp. Mar. Biol. Ecol.
       45:245-272.

                                            148

    Sammarco, P. W., J. S. Levinton, and J. C. Ogden. 1974. "Grazing and Control
       of Coral Reef Community Structure by Diadema antillarum Philippi
       (Echinodermata: Echinoidea): A Preliminary Study." J. Mar. Res. 32:47-51.

    Sammarco, P. W., and A. H. Williams. 1982. "Damselfish Territoriality:
       Influence on Diadema Distribution and Implications for Coral Community
       Structure." Mar. Ecol. Pros. Ser. 8:53-59.

    SAS Institute, Inc. 1982. SAS User's Guide: Statistics. Cary, North Carolina.
       584 pp.

    Sokal, R. R., and F. J. Rohif. 1969. Biometry: The Principles and Practice
       of Statistics in Biological Research.  W. H. Frean, San Francisco.  776 pp.

    Van den Hoek, C., and A. M. Breeman. 1978. "The Distribution of Algae, Corals
       and Gorgonians in Relation to Depth, Light Attenuation, Water Movement, and
       Grazing Pressure in the Fringing Coral Reef of Curacao, Netherlands Antilles."
       Aquat. Bot. 5:1-46.

    Van den Hoek, C., A. M. Cortel-Breeman, and J. B. W. Wanders. 1975. "Algal
       Zonation in the Fringing Coral Reef of Curacao, Netherlands Antilles, in
       Relation to Zonation of Corals and Gorgonians." Aquat. Bot. 1:269-308.

    Williams, A. H. 1978. "Ecology of Threespot Damselfish: Social Organization,
       Age Structure, and Population Stability." J. Exp. Mar. Biol. Ecol. 34:197-
       213.

    Williams, A. H.  1979.  "Interference Behavior and Ecology of Threespot
       Damselfish." Oecologia 38:223-230.

    Williams, A. H.  1980.  "The Threespot Oamselfish:  A Non-Carnivorous Keystone
       Species." Amer. Nat. 116:138-142.

    Williams, A. H. 1981. "An Analysis of Competitive Interactions in a Patchy
       Back-Reef Environment." Ecology 62:1107-1120.

                                            149

                       CARBONATE SEDIMENT PRODUCTION BY THE ROCK-BORING URCHIN
                        ECHINOMETRA LUCUNTER AND ASSOCIATED ENDOLITHIC INFAUNA
                                  AT BLACK ROCK, LITTLE BAHAMA BANK

                                  Charles M. Hoskin and John K. Reed
                                      Marine Geology Department
                                    Harbor Branch Foundation, Inc.
                                     Fort Pierce, Florida 33450

                                               ABSTRACT

                Bioerosion studies were conducted during four cruises in 1982-83 to Black
           Rock, a 405 m long island of carbonate eolianite on Little Bahama Bank. The
           urchin population (X = 37 adults m'2, 92 x 103 total) bores in a 6 m wide zone
           at depths of 0.5-3 m. SCUBA divers using chisels collected rocks with urchins
           in their bore holes and similarly sized rocks without urchins and placed them
           separately in 20 1 buckets with 0.0625 mm screen-walls for 2 days (13 usable
           measurements). Urchins produced spherical to elliptical pellets 1-2 mm in
           diameter. Disaggregated pellets contained no particles > 1.00 mm. The pellets
           were 46% (wt) unimodal sand, with a modal grain size between 0.125-0.177 mm,
           and 54% mud. Urchins produced an average of 242 mg sediment urchin-1 day-1
           (dry wt), which is equivalent to 8.9 g m-2 day-1, or 9 tons yr-1 for the entire
           population. Volume of individual urchin bore holes averaged 72 cm3. Calculating
           from boring rates, the bore holes were excavated in an average of 2.9 years.

                Rocks without urchins (controls) produced an average of 0.5 mg organic-
           free sediment cm-2 day-1 (dry wt). These particles were produced by bioerosion
           of the infauna, which included eunicid and sipunculid worms, sponges, Lithotrya
           barnacles, pelecypods, and microborers. Inorganic sediment weight was correlated
           (r = 0.968, p < 0.05) with surface area of the control rocks. Infauna from
           control rocks produced 5.0 g m-2 day-1, equivalent to 6.5 tons yr-1, for Black
           Rock.

                                             INTRODUCTION

                Bioerosion has a two-fold role in coral reefs; hard substrate is removed,
           creating cavities, and some of the former substrate becomes sedimentary particles
           that may be transported to new environments (Hopley, 1982). We have been
           studying the area surrounding Black Rock, a small Pleistocene eolianite island
           on the southwestern Little Bahama Bank, in order to identify and measure sources
           of sediment, to follow dispersal pathways, and to measure the rate at which the
           sediments accumulate.

                Bioerosion by the urchin Echinometra lucunter (Linnaeus) has been studied
           previously in Barbados (McLean, 1967), Bermuda (Hunt, 1969), and the Virgin
           Islands (Ogden, 1977). Another species, E. mathaei, has been studied in Persian
           Gulf reefs by Shinn (p. 39, in Hughes Clar-e and Keij, 1973) and Enewetak
    *s    ~(Russo, 1980).  The purposes of this study are to determine the rate of sediment
    isw     production and cavity formation by E. lucunter using a new method, to characterize

                                                   151

    p M~~~~~~~~~~~pw -~~~~~~~~~

    the size distribution of the particles produced, and to compare these data with
    the rate of production and size of particles produced by the rock-boring infauna
    closely associated with the urchin bore holes.

                                        METHODS

    Urchin Population

         The distribution and abundance of E. lucunter adults (about 3 cm test
    diameter) was determined by SCUBA divers off western Black Rock. Most of the
    eastern side is sand, without urchins. Using a 0.25 m2 PVC frame, the divers
    counted the adult urchins within each frame (total of 35 frames) on three
    separate transects that were continuous from the intertidal zone seaward until
    no more urchins were found. The number of adult urchins was calculated for
    each linear meter in a seaward direction. These numbers were extrapolated for
    the lateral extent of the island to yield the total number of urchins.

    Sediment Yield

         Using chisels, SCUBA divers collected rocks, each containing one urchin in
    its intact bore hole, from 2-3 m depths off western Black Rock. Similarly
    sized rocks without urchins were collected for controls. Each rock was brushed
    underwater to remove loose particles. The rocks were placed separately, without
    exposure to air, in 20 1 plastic buckets.  Each rock was placed on a styrofoam
    pad and secured to the bottom of the bucket by criss-crossed rubber bands
    latched onto plastic hooks attached inside the buckets. The buckets were
    ventilated with 1150 cm2 of 0.0625 mm nylon screen on the side and 72 cm2 of
    0.5 mm nylon screen at the top. Using an oxygen electrode, measurements made
    at the start and end of an experimental run showed only a small decrease (maximum
    decrease of 0.4 mg 1-1) in dissolved oxygen within the bucket. Buckets were
    secured to the seafloor at the collection site in various ways, all designed to
    minimize movement of the rock within the bucket, which otherwise might have
    produced sediment particles by abrasion (fig. 1A). Buckets were deployed for
    43-50 hr during four separate cruises. Five control and eight experimental
    buckets yielded thirteen usable measurements out of the twenty-four buckets
    deployed. Some buckets were lost in squalls and others had rips in the nylon
    mesh and therefore were not included.

    Figure 1 (opposite page).--(A) Buckets (20 1)' in situ at 2.5 m depth used for
      urchin study; (B) SEM of limestone (eolianiteT wall in Echinometra lucunter
      bore hole. Upper right - encrusted with lithothamnoid algae. Lower left -
      algae-free area eroded by urchin and showing spherical grains in the limestone;
      (C) Fecal pellets from alimentary tract of E. lucunter. Bar = 0.5 mm;
      (D) Broken and partially regrown spine of E.7lucunter; (E) Abraded end of
      tooth from Aristotle's lantern of E. lucunter; (F) SEM close-up of fig. 1E
      (arrow), showing laminated microstructure of tooth tip visible from abrasion.
      Tip pointing to right.

                                            153

         The particles produced were recovered by gently washing the rock (and
    urchin) while inside the bucket, siphoning off the water, and then washing the
    particles into polyethylene bags. Particles, rocks, and urchins were labelled
    and then preserved in 70% ETOH. Particles were washed free of salt, oven dried
    at 950C, and weighed to 0.01 mg. Twelve free-living urchins were collected and
    their alimentary tracts removed by dissection, measured, and the length of
    tract containing sediment estimated. The gut contents were removed, washed,
    dried, and weighed. The organic content of sediment from the urchin alimentary
    tracts, experimental buckets, and control buckets was determined by weight loss
    following H202 digestion. Subsequently, inorganic sediment from each sample was
    wet sieved (0.0625 mm stainless steel screen) to separate mud. Gravel and sand
    size particles (> 0.0625 mm) were oven dried at 95�C and dry sieved at 0.5 Phi
    intervals for 5 min using agitation by Vibrapad. Weight of each sieve fraction
    was recorded to 0.01 mg. Particle size distributions were generated by the
    Cal-Comp plotter from these weights.

         Attached organisms (mostly algae) were removed from each rock, washed,
    dried, and weighed. Each rock was then oven dried, and the exposed surface
    area was measured by the aluminum foil method (Reed, et al., 1982). The volume
    of each urchin bore hole was measured by determining t-levolume of water
    contained in a latex sheath placed inside the bore hole. Each rock was dissolved
    in acid (HCl + HN03) to recover the infauna, which was washed, dried, and
    weighed. Urchins were dried and weighed, and test dimensions and volume were
    determi ned.

                                        RESULTS

    Urchin Population

         The total urchin population at Black Rock was 92.4 x 103 adults within an
    area of 2521 m2. Average urchin density was 37 adults m-2 (maximum was 100
    m-2). Urchins were present between the intertidal zone and 7 m depth. Urchins
    never were observed to leave their bore holes; during the day they remained
    stationary at the bottom of the hole, but at night they moved within their
    individual bore holes. The urchins fed upon both endolithic algae and pieces
    of algae that apparently drifted into the bore holes.

    Sediment Yield

         For control rocks (without urchins), a significant correlation (r = 0.968,
    p < 0.05) was found between the total inorganic weight of sediment recovered
    from buckets and the total surface area of the rocks. Linear regression gave
    the formula for this relationship:

                                  Y = 1.133X - 119.71,

    where Y = inorganic sediment weight and X = total rock surface area. The
    average organic content of sedimentary particles recovered was 23.74% (range :
    14.99 - 41.98%).  The mean weight of attached macro-organisms on control rocks

                                           154

    was 4.6 g dry weight (range = 1.3 - 13.9). The average yield of inorganic
    particles produced by infauna of the control rocks was 0.50 + 0.07 mg cm-2 day-1
    (X + 1 SD; table 1). This rate of sediment production was equivalent to 5.0 g
    m-2-day-1, and for the area of 2521 m2 in which these rocks occurred, the yield
    was 12.6 kg day-1. The average dry weight of infauna recovered by acid dissolu-
    tion of each control rock was 8.6 g (range = 4.5 - 13.8).. Dominant infauna
    included eunicid polychaetes, sipunculids, boring sponges, Lithotrya barnacles,
    pelecypods, and other microborers.

         For experimental buckets (rock + urchin), the sediment recovered was a
    mixture of particles produced by the rock infauna and by the urchin inside its
    bore hole. We assumed that the amount of sediment passing through the mesh
    from outside sources was the same for control and experimental buckets. Because
    our underwater observations showed that visibility was 12-18 m, we further
    assumed that the possibility of mud contaminating the buckets was insignificant.
    The average organic content of particles recovered was 15.83% (range = 11.75 -
    20.30%). The average weight of attached macro-organisms was 6.7 g dry weight
    (range = 1.0 - 13.1). To calculate the weight of sediment produced solely by
    the urchin, we used the regression formula (above) and subtracted the weight of
    sediment made by the infauna of the experimental rock from the total inorganic
    weight of sediment recovered. The calculation for each experimental bucket was
    made as follows:

                         [total organic-free wt] - [1.133 x area of experimental
                                                    rock - 119.71]
    mg urchin-1 day' 1 =                                                               x 24.
                                        duration of experiment in hours

    These calculations indicated that the average weight of inorganic sediment
    produced by adult urchins was 242.2 + 146.0 mg urchin-1 day-  (X + 1 SD, table
    1).  The total urchin population produced 22.4 kg day-1 or an average of 8.9 g
    m12 day-1 within the 2521 m2 area containing urchins. Urchin bioerosion was
    64% of the total 13.9 g m'2 day-1 measured by our bucket experiments. In
    nature, physical processes of abrasion and other bioeroders (fish) would
    contribute additional particles.

         Particle size analysis showed that the percentages of sand (2.00 - 0.0625
    mm) and mud (< 0.0625 mm) were similar for sediment from alimentary tracts of
    uncaged urchins and from control and experimental rocks. The alimentary tracts
     of the urchins contained mostly pellets (fig. 1C) which readily disintegrated
     into sand and mud. No gravel (> 2.00 mm) was found in alimentary tracts of
     urchins. Sediment from control and experimental buckets contained 0 - 28.5%
     gravel. Sand fractions from alimentary tracts of uncaged urchins contained
     particles most abundantly between 0.125 - 0.177 mm (fig. 2, top) and particles
     of this size were also the most abundant in sediment recovered from experimental
     buckets which contained eolianite and a living urchin (fig. 2, middle). As
     determined with a low-power microscope, the grain size of sand particles in the
     eolianite is the same as the modal grain size of sand from urchin alimentary
     tracts (0.125 - 0.177 mm).  However, sediment from urchin alimentary tracts was
     50% mud, which greatly exceeds the mud content of the eolianite. These
     observations suggest that urchins cause erosion at Black Rock by breaking
     individual eolianite grains away from the substrate, yielding sand, and also by

                                             155

    Table 1.--Comparison of sediment production rates of infauna (control rocks)
                             and urchins (experimental rocks)

                                          Control (rock, no urchin)

    Date and             Total Organic-free        Rock Surface       Sediment Production
    Duration             Sediment Recovered         Area (cm2)          Rate by Infauna
                            (dry wt, mg)                                (mg cm-2 day-1)

    25-27 August 1982          442.13                  428.1                  0.57
        43.5 hr
                               286.63                 396.5                  0.40

                               500.19                 591.6                  0.47

    13-15 April 1983           689.78                  722.6                  0.50
        45.5 hr
                               814.86                 802.4                  0.54

                                                                       X = 0.50 + 0.07

                                         Experimental (rock + urchin)

    25-27 August 1982         1507.63                  640.2                 497.65
        43.5 hr
                              1031.92                 774.5                 169.99

                              1044.32                 621.0                 254.03

    13-15 April 1983          1146.83                  902.4                 128.77
        45.5 hr

    21-23 June 1983            1278.27                1119.5                  62.83
        49.5 hr
                              1270.90                 795.5                 237.24

                              1588.92                 756.0                413.13

                              1355.85                 985.9                 173.84

                                                                        X = 242.2 + 146.0

    abrading more tightly cemented eolianite grains, yielding mud (fig. iB).
    Infaunal bioeroders produced a much broader spectrum of particle sizes (fig. 2,
    bottom), perhaps due to the many species of bioeroders active within these
    rocks.

    Evacuation of Bore Holes

         Inspection of eolianite at the bottom of urchin bore holes by low-power
    microsr pe and SEM revealed no scratches on the substrate (fig. 1B).  Individual

                                              156

                                  URCHINS

                                      *1~~~~~~~~~~~~~~~~~~~~'
                                 URCHINS   \
                                    AND
                                  ROCKS

                                      t~~~~l,.u
                                                            N
                                                         em   &

                                  CONTROL ROCKS

                               .0  1.0  0.5  0125 0.125 0.0625 mm
                  4- GRAVEL I                 SAND             I MUD -4
    Figure 2.--Size-frequency curves for the sand fraction of sediment from alimentary
     tracts of uncaged urchins (upper), from urchins and rocks in bucket enclosures
      (middle), and from rocks without urchins in bucket enclosures (bottom). Data
      for the gravel and mud fractions are not given; scale of the y-axis is identical
      for all sediments.                          157

                     Table 2.--Bioerosion by Echinometra lucunter.

    Method                Substrate            Rate of Erosion          Author
                                           (g urchin-1 yr-1)

    Gut contents          Beachrock                 18.6                McLean, 1967

    Gut contents          Algal ridge on            44.0                Ogden, 1977
                           coral reef

    Gut contents          Eolianite                128.0                Hunt, 1969

    Bucket enclosure      Eolianite                 88.0                This paper

    teeth from the Aristotle's lantern of the urchin had abraded tips; most spines
    were sharply pointed, but a few had broken and re-grown tips (fig. 1D, E, F).
    It is possible that E. lucunter may use its spines in addition to teeth in
    substrate erosion (MZTean, 1967; Hunt, 1969).  The rate of spine re-growth may
    be so rapid, averaging 0.3 mm day-1 at 20�C (Davies, et al., 1972, fig. 1, p.
    874), that damage to spine tips is not ordinarily obseFvir-Te.

         Volume of bore holes for individual urchins averaged 72 cm3 (range = 17 -
    126).  Using a measured density of 2.13 g cm-3 for the eolianite and the average
    rate of substrate erosion by the urchins, we estimated that an average of 2.9 yr
    was required to excavate a bore hole (range = 0.7 - 10.3 y).

                                        DISCUSSION

         Previous studies (McLean, 1967; Hunt, 1969; Ogden, 1977) measured only the
    amount of sediment within urchin alimentary tracts and assumed that frequency
    of gut turnover was once each day.  Disadvantages of the gut contents method
    are that 1) gut turnover frequency is not verified, 2) the material in the gut
    is not necessarily produced by urchin activity and may have been ingested after
    transport to the urchin bore hole from an allochthonous source, and 3) not all
    particles produced by urchin tooth and spine movements may be ingested.

         The advantages of the bucket enclosure method are that 1) all sediment
    produced by the urchin is captured, 2) rates of infaunal sediment production
    and the grain size of their product can be determined, and 3) contamination by
    sediment from outside sources is minimized.  There is, however, the possibility
    of loss of some mud-sized particles through screen windows in the buckets, the
    exclusion of drifting algal bits, and reduced water flow inside the buckets.

          Measurements of bioerosion by E. lucunter from various places are summarized
     in table 2; there are too many variiales to resolve the different rates reported.
     To place our measurements in perspective, a comparison with other erosion

                                             158

            Table 3.--Comparison of erosion agents and rates for Black Rock
             (unpublished data of C. M. Hoskin, D. H. Mook, and J. K. Reed)

    Process             Agent                       Average Rate of Substrate Erosion
                                                           (mg cm-2 yr-1)

                       E. lucunter
                       5bucket enclosures)                         667

    Bioerosion          Rock infauna
                       (bucket enclosures)                         183

                       Intertidal microborers
                       (tethered limestone blocks)                  26

    Physical            Waves and currents
      abrasion          (tethered limestone blocks)                 5.5

    Chemical            Intertidal seawater
      solution          (filter-protected, suspended
                         limestone blocks)                         0-2

    processes at Black Rock (table 3) indicates that biological activities are more
    significant than physical and chemical processes in the degradation of reef
    substrates.

         In terms of paleoecological significance, we suggest that the most
    preservable part of the bioerosive activity of E. lucunter at Black Rock will
    be the band of bore holes.  However, with SEM we searched for and did not find
    appropriately sized scratch marks on the bottoms of bore holes which might be
    expected from urchin teeth.  The sediment produced by E. lucunter is initially
    pelleted, but the pellets quickly disintegrate.  Sand Tom the pellets is most
    abundant at sizes between 0.125 - 0.177 mm, but other processes may produce
    sand of the same size.  Approximately half (by weight) of the disintegrated
    pellets is mud with no distinctive properties.  Although the urchin population
    density was as high as 100 adults m-2, the total amount of echinoderm skeletal
    fragments in the sand fraction of nearby shallow water sediment was < 1%; Hine,
    et al.  (1981, table 1, p. 288) did not include echinoderm skeletons in their
    Tsting of carbonate constituents.

          Hine, et al. (1981, fig. 17-B, p. 278) have shown by seismic reflection
    profiling tFitte southwest margin of the Little Bahama Bank in the vicinity
    of Black Rock is a rocky surface, barren of sediment.  Our seismic reflection
     profiling confirms the seismic findings of Hine, et al. (1981), but from the
     JOHNSON-SEA-LINK submersibles we have seen sediments a few centimeters thick
     overlying hardgrounds on the western bank margin.  Using the geometry of sand
     bodies 3-12 km northeast of the bank margin as an indicator, Hine, et al. (1981,
     fig. 14, p. 275, and table 1, p. 268) suggested that sand is transported onto
     the Little Bahama Bank.  Sediment produced by E. lucunter and the associated

                                             159

    ror infauna is predominantly fine sand and mud. The amounts of this sediment
    art :onsiderable: 9 tons yr-1 for the urchins plus 6.5 tons yr-1 for the
    int una at Black Rock. This sediment probably does not accumulate in the
    shallow bank margin environment because currents are strong (Hine, et al.,
    1981, fig. 24, p. 287).

         From the JOHNSON-SEA-LINK submersibles we observed sediment-containing
    grooves passing through the bank-edge reefs and have counted 70 grooves in a
    400 m long segment of bank edge west of Black Rock. Hubbard, et al. (1981,
    fig. 17, p. 26) have illustrated similar sediment-containing grooves off Lucaya,
    Grand Bahama Island.  We made sediment trap measurements in the qrooves (32 m
    depth) west of Black Rock and found an average of 5.4 kg m-1 yrI of carbonate
    sediment moving westward. We suggest that this sediment, in part, represents the
    products of urchin and rock infauna bioerosion being transported over the bank
    edge and into deeper waters of the Northwest Providence Channel.

                                    ACKNOWLEDGMENTS

         We thank the officers and crews of R/V JOHNSON and JOHNSON-SEA-LINK I for
    their expert assistance at sea; Craig Caddigan, Chris Chulamanis, and Richard
    Morris who assisted with SCUBA diving in deployment and recovery of the bucket
    experiments; David Mook for Cal Comp plotting; and Marjorie Reaka and two
    anonymous reviewers for manuscript editing. This is Contribution No. 390 from
    Harbor Branch Foundation, Inc.

                                    LITERATURE CITED

    Davies, T. T., M. A. Crenshaw, and B. M. Heatfield.  1972.  "The Effect of
       Temperature on the Chemistry and Structure of Echinoid Spine Regeneration."
       J. Paleontol. 46:874-883.

    Hine, A. C., R. J. Wilber, and A. C. Neumann. 1981. "Carbonate Sand Bodies
       Along Contrasting Shallow Bank Margins Facing Open Seaways in Northern
       Bahamas." Bull. Amer. Assoc. Petrol. Geol. 65:261-290.

    Hopley, D.  1982.  The Geomorphology of the Great Barrier Reef:  Quaternary
       Development of Coral Reefs.  Wiley-Interscience, New York.  453 pp.

    Hubbard, D. K., L. G. Ward, D. M. Fitzgerald, and A. C. Hine. 1976. "Bank
       Margin Morphology and Sedimentation, Lucaya, Grand Bahama Island." Report
       No. 7-CRD, Coastal Res. Div., Univ. of South Carolina, Columbia, S.C. 36 pp.

    Hughes Clark, M. W., and A. J. Keij.  1973.  "Organisms as Producers of Carbonate
       Sediment and Indicators of Environment in the Southern Persian Gulf," pp. 33-
       56. In: B. Purser (ed.), The Persian Gulf. Springer-Verlag, New York.

    Hunt, M.  1969.  "A Preliminary Investigation of the Habits and Habitat of the
       Rock-Boring Urchin Echinometra lucunter near Devonshire Bay, Bermuda," pp.
        35-40.  In:  R. N. Ginsburg and P. Garrett (eds.), Seminar on Organism-
       Sediment-Tnterrelationships.  Spec. Publ. No. 2, Bermuda BioT. Sta., St.
        George's West, Bermuda.

                                            160

    McLean, R. F. 1967. "Erosion of Burrows in Beachrock by the Tropical Sea
       Urchin Echinometra lucunter."  Can. J. Zool. 45:586-588.

    Ogden, J. C. 1977. "Carbonate-Sediment Production by Parrot Fish and Sea
       Urchins on Caribbean Reefs," pp. 281-288. In: S. H. Frost, M. P. Weiss,
      and J. B. Saunders (eds.), Reefs and Relate4-Carbonates - Ecology and
       Sedimentology.  Stud. Geol. No. 4, amer. Assoc. Petrol. Geol., Tulsa,
      Oklahoma.

    Reed, J. K., R. H. Gore, L. E. Scotto, and K. A. Wilson. 1982. "Community
      Composition, Structure, Areal and Trophic Relationships of Decapods Associated
       With Shallow- and Deep-Water Oculina varicosa Coral Reefs." Bull. Mar. Sci.
       32:761-786.

    Russo, A. R. 1980. "Bioerosion by Two Rock Boring Echinoids (Echinometra
      mathaei and Echinostrephus aciculatus) on Enewetak Atoll, Marshall Islands."
       J. Mar. Res. 38:99-110.

                                           161

                   HIGHLY PRODUCTIVE EASTERN CARIBBEAN REEFS: SYNERGISTIC EFFECTS
                     OF BIOLOGICAL, CHEMICAL, PHYSICAL, AND GEOLOGICAL FACTORS

                                           Walter H. Adey
                                     Marine Systems Laboratory
                                      Smithsonian Institution
                                      Washington, D.C.  20560

                                                and

                                         Robert S. Steneck
                            Zoology Department and Oceanography Program
                                        University of Maine
                                  Darling Center Marine Laboratory
                                       Walpole, Maine 05473

                                              ABSTRACT

               Studies of reef productivity and community structure were conducted on
          three bank barrier reefs along the south shore of St. Croix, U.S. Virgin Islands.
          Primary productivity (rate of organic carbon fixation) was measured using
          upstream/downstream flow respirometry techniques. Mean annual gross primary
          productivity of the St. Croix reef ranged between 17-33 g C/m2/d. These are
    .     ~among the highest values reported for reefs or for any biological community.

               Reef productivity corresponds with the distribution and abundance of turf
          algae. These algae are minute filamentous forms which are highly diverse,
          productive, and abundant. Algal turf productivity is limited primarily by
          available solar energy and is influenced by wave surge and water flow (which
          enhance metabolite exchange). Turf cover is limited by the total surface area
          of standing dead coral. Nitrogen availability is increased by in situ nitrogen
          fixing blue-green algae, as evidenced by increased concentrations -577norganic
          nitrogen in water flowing over the most productive reef zones. Phosphorus
          availability is enhanced by wave surge and maintained by inflowing water from
          the open ocean.

                Over geological time, reefs grow toward sea level. The three reefs we
           studied represent three stages in reef development. Younger reefs to the east
          are deeper, with considerable live branching coral (Acropor  Ralmaa) and with
          a low abundance of turf algae.  The reverse is true  for  te ole reefs to the
          west, where live coral is minimal but the dominant algal turfs occupy a rather
           smooth pavement of limited surface area.  Intermediate between these tw o types
           of reefs, the abundance of live coral is low but biomass of algal turf is very
           high due to the large surface area left by the dead branching coral. The
           greatest reef productivity was measured under the latter conditions because of
           the synergistic effects of large surface area with abundant algal turf cover in
           shallow, strongly lighted, and turbulent water. It is clear that, given optimum
           conditions, coral reef algal turfs can develop primary productivities that
    .     ~reach and perhaps exceed the accepted theoretical maximum for primary production
    is ~in the sea.

                                                 163

                                      INTRODUCTION

         Coral reefs have attracted interest over the last 30 yr in part because
    they are among the most productive biological communities in the world. Early
    studies of reef productivity (Sargent and Austin, 1949; Odum and Odum, 1955)
    focused on determining the productivity of individual reefs. There is little
    agreement in these and subsequent studies as to how productive reefs can be,
    and there is even less agreement concerning why high levels of production are
    attained or why reefs differ from each other so much (Lewis, 1977; Sournia,
    1977; Mann, 1982). Smith (1981) considered some of these problems in an
    examination of the Houtman Abrolhos Islands off western Australia. We address
    these questions in some detail in our study of the reefs of St. Croix.

         In an examination of the "Potential Productivity of the Sea," Ryther
    (1959) concluded that (net) "primary productivity of organic matter of some
    10-20 g (dry)/m2/d may be expected," with a maximum of 25 g (dry)/m2/d under
    ideal conditions of maximum radiation and no nutrient limitation. Expected
    gross primary production (GPP) levels of up to 23-38 g (dry)/m2/d (50-80% higher
    than the net values) also were cited. Ryther suggested that, while planktonic
    open ocean production (particularly in tropical/subtropical areas) is limited
    by nutrients, such limitation in benthic communities is not likely because
    nutrients "are continually being replenished as the water moves over the plants
    [and] probably prevents their ever being [nutrient] limited."

         Recent reviews of coral reef primary productivity by Lewis (1977) and
    Sournia (1977), integrating 30 yr of research, reveal a range in GPP of nearly
    an order of magnitude (3.4 - 20 g C/m2/d). The mean of these cited reef values
    is about 10 g C/m2/d, but only a few points are above 13 g C/m2/d. The mode is
    7 g C/m2/d, which, using a typical conversion ratio, would convert to a net biomass
    production of about 15 g (dry)/m2/d. Overall, these values are much less than
    the theoretical maximum suggested by Ryther (1959). Significantly, all but one
    of the 17 coral 'reefs cited by these authors were located in the Indo-Pacific.

         Despite Ryther's (1959) suggestion to the contrary, nutrient limitation of
    reef productivity has been the focus of numerous studies. Many of these have
    focused on explanations of how highly productive reef ecosystems can thrive in
    nutrient deserts (Odum and Odum, 1955; Stoddart, 1969; Johannes, et al., 1972;
    D'Elia, et al., 1981; Andrews and Muller, 1983).  Recently, the roTe-o  major
    nutrients was questioned due to the finding that benthic algae have lower
    nutrient requirements than once thought (Atkinson and Smith, 1983). Also, some
    reefs are known to have a surplus of nitrogen (Webb, et al., 1975; Wiebe, et
    al., 1975) due to the in situ nitrogen fixation by cyanobacteria (blue-green
    algae) (Mague and Holm-Hansen, 1975; Capone, et al., 1977; Hatcher and Hatcher,
    1981; Wilkinson and Sammarco, 1983).  The benthic algal turf of reef communities
    usually is dominated by cyanobacteria (Sammarco, 1983; Van den Hoek, et al.,
    1975).

         Phosphorus concentrations over reefs generally have been thought to change
    little (Pilson and Betzer, 1973), and some authors have suggested that a "tight
    recycling" or retention of phosphorus occurs (Pomeroy, et al., 1974; Pomeroy
    and Kuenzler, 1969).  Atkinson (1982), on the other hand, ha-s shown reactive
    phosphate depletion over broad reef flats.

                                            164

         Our study examines the productivity of three reef environments in tropical,
    oligotrophic seas. Large-scale temporal and spatial variations in their primary
    productivity with respect to potentially important biological, chemical,
    physical, and geological differences between the reefs are explored.

                          MATERIALS, METHODS, AND STUDY SITES

         Our study was conducted on the southeastern bank barrier reef of St. Croix
    from October 1977 to November 1978. It extends 35 km along most of the windward
    shore of the island and is the most extensive reef system on the Puerto Rican-
    Virgin Island shelf. St. Croix is a small island which is unaffected by
    neighboring islands. Temperature, salinity, and wind direction and intensity
    are all remarkably constant.  The south shore is relatively unpopulated, and it
    has no natural rivers affecting salinity or ambient nutrients. The south shore
    of St. Croix is ideal for examining the factors that affect reef productivity.
    The two major factors that change from east-to west are water motion (decreasing)
    and geological reef development (increasing).

         The western reefs of St. Croix lie on a shallower limestone basement than
    do the eastern reefs; they were the first to grow to sea level (Adey, 1975;
    1978a), and they developed broader, more continuous reef flats.  Several of
    these reefs have become so shallow that the abundance of live coral is reduced
    due to the negative effects of intense sunlight (including ultraviolet), tempera-
    ture fluctuations, and desiccation during periods of extraordinarily low tides.

         We studied three reefs on the south shore of St. Croix intensely and
    several others to a lesser extent (fig. 1).  The following is a description of
    the morphology of the reefs from east to west.  Isaac Bay Reef is a "young"
    reef with a high coral cover, rapid reef growth rates, and a crest that is just
    reaching sea level today.  Mean depths are 6.3 m for the fore reef and 0.9 m for
    the back reef.  The reef structure is open (many channels and breaks in the reef
    crest), and there is no continuous reef flat.  Robin Bay Reef is more mature,
    with a nearly continuous crest and a moderately deep and broad reef flat.  Mean
    depths are 5.1 m for the fore reef and 0.7 m for the back reef.  Halfpenny Bay
    Reef is mature, with a continuous, broad, and shallow reef flat.  Mean depths
    are 5.1 m for the fore reef and 0.3 m for the back reef.  We selected these
    reefs because they fall along a gradient of reef maturity and because they are
    particularly well suited for the upstream/downstream method. All of these reefs
    have a continuous unidirection water flow inward across the reef to the lagoon.

         A profile of Robin Reef along a permanent transect line established at the
    beginning of our study is shown in figure 2. Comparisons with Isaacs and
    Halfpenny Reefs are give~n in the accompanying table. The transects were parallel
    to the predominant current flow and were established using drogues, to indicate
    the exact current flow. We omitted breaker zones due to logistic and scientific
    problems created by the turbulence (accelerated diffusion). The outer (seaward)
    limit to the fore reef was defined by the first appearance of the dominant reef-
    building coral, Acrpora pamaa   The inner fore reef and outer back reef zone
    were adjacent to te-F-are zoine.  The inner (landward) limit of the back reef
    was defined by the abrupt transition between the reef and sandy lagoon. Our fore
    and back reef zones are consistent with other published studies (Adey, 1975;
    Adey and Burke, 1976).

                                            165

                   nautical miles                                  1

                                       Airport                                      _   Holocene reef to
                                    ~~~~~~~~kilo~ 2meters                                       thick
                                                                                Island

                                                                                 Tague Bay

                              ST. CROIX
                                                                                                  ISAAC

                                                                                     ROBIN

                                                                 HALFPENNY
                                                 ChAioel                               LEGEND
                                         O#A irport                                      Holocene reef to
                                                                                         25 meters thick

    Figure I.--Locations of transects across bank barrier reefs studied on the south shore of St. Croix,
                                 U.S. Virgin Islands, northeastern Caribbean.

               BACK
            4  REEF  3    CREST    2               FORE REEF

       0-4-A.KAX

     4-x
       4-   REZONES
    _  -    SACREEF       14-313-2 1 2-1
       6-    ISAAC       |14811251287
    I         ROBIN       1471701203
    fi  8-    HALFPENNY 1621951138                 I&%

      10-        oI III

                            50 METER INCREMENTS

                      Figure 2.--Typical reef transects (Robin Reef).

         Diurnal measurements of changes in oxygen concentration and water flow
    were taken in all seasons of the year and were used to derive rates of community
    oxygen production (which reflect net or apparent productivity) and consumption
    (respiration). Accurate measurements of discharge rates (rate of water volume
    flow) are crucial to this upstream/downstream method. For this, we used a
    Marsh-McBirney model 527 electromagnetic, x-y current meter. .Water samples
    were taken at each transect every 2 hr over a 2- to 3-day period during each
    season. Particular care was taken to maximize the level of precision at every
    step of analysis (see Adey, et al., 1981). A plot of a typical diurnal cycle
    of oxygen concentration at the Robin Bay site is shown in figure 3.  Standard
    methods of calculating production in upstream-downstream methods were employed
    (Marsh and Smith, 1978). Computer plotting and integration of the area under
    the curve above the zero oxygen production level provided net daytime primary
    productivity values. The area below the zero line provided respiration values.

         The biotic composition (percent cover) and surface area of these reefs
    were determined with chain transects (methods detailed in Rogers, et al.,
    1982). We measured all surfaces along each transect that we could reach, except
    for truly cryptic habitats (nearly devoid of light). This method also gave a
    measure of surface area per projected square meter of bottom Cm /m , called a
    surface area ratio (SAR)].

         To examine community structure of algal covered surfaces, random Acropora
    p almata substrate samples were collected from both fore and back reef zones.
    Algal cover and distribution on the surface were mapped using grids with I cm
    squares placed over the top and bottom surfaces. Algal turfs were subsampled
    by scraping from 3-12 visually representative, but distinct, 1 cm2 microquadrats.
    Each sample included the upper millimeter of calcium carbonate in order to
    sample endolithic, crustose, and tightly adherent algae. Solutions of 5% HC1
    and 5% formalin were used to decalcify and fix the samples. A representative
    subsample of the scraped algal turf samples was spread in a monolayer over a
    microscope slide. Species composition of algal turf communities was quantified
    using a "point count" technique. This involved counting the number of times
    identifiable algae crossed points of intersection on an ocular grid placed
    within a compound microscope.

         At each of the reef study sites, water samples were collected and analyzed
    for nutrients at the beginning and end of each field session, between 1000 and
    1400 hr. Standard precision handling techniques were employed at every stage,
    and analyses for nitrate, nitrite, phosphate, and total dissolved phosphorus
    were accomplished with a Beckman DU spectrophotometer. Extensive descriptions
    of methods and data taken during the course of this study appear in Adey, et
    al. (1981).

                                 RESULTS AND DISCUSSION

    Reef Productivity

         The reefs studied were highly productive.  Community metabolism, as shown
    by mean diel oxygen production at each station, and seasonal metabolism at all
    stations is given in figures 4 and 5. Gross primary productivity (GPP), net

                                           168

           DISSOLVED OXYGEN

    8.6    . .*� backreef
    8.2                           0 forereef

                   -o                                ,
    7.8'O~.
    .4

    6.2.

    5.4
    o~~~ .,  \\                     . .          ,. .   .,                      ,. .            , .

    5.0
           1200               2400               1200               2400               1200               2400
                                                TIME OF DAY

          Figure 3.--Dissolved oxygen concentration across Robin Reef from 1/21/78 to 1/23/78.
                        Numbers on individual plots refer to standard reef sites.

      6-

                                             //       AAC ,

       4[

      2 -

    41
    s                                       /I

                0000          0400           0800           1200           1600           2000           2400

                                                  TIME OF DAY

                 Figure 4.--Mean yearly diurnal oxygen exchange for the reef transects.
                                                / / %~.  / / ~ ~ ~ ~ ~ ~ ~~~~~~~~~~~~~~�4

       8-

       6-                                          MAY '
                                                                   A- MAYUGUST

               ,>ru'~~~   OCTOBER
    E
    o                                                    .....

    z                       . .,_JANUARY

      -2-                                                   ---                                ---
               *                              �"/

    U'
                                          ,./...i/ //S"'JANUARY ' '....

      -2-
                                   S/                  .   ..                              ,.-..

                   0000           0400            0800             1200            1600           2000            2400

                                               TIME OF DAY

               Figure 5.--Mean seasonal diurnal oxygen exchange: summary of all transects.

                         Table 1.--Summaries of daily metabolism.

                      Gross Primary                Net Community
                       Productivity             Primary Productivity'   Respiration (-)

                       (9gO2/m2/day)                (g02/m2/day)            (gO2/m2/hr)

                   Fore    Back   Means    Fore  Means   Back   Means   Fore   Back

          Jan.   10.02    36.5               6.1            23.0             0.4    1.4

        e May    17.4       48.9             9.3            32.7              0.8    1.6
                                   46.7            8.4             27.5
       "Aug.    12.4       57.6              6.6            29.1             0.6    2.8

          Oct.    13.8     43.7             11.5            25.2             0.2    1.8

          Jan.    14.3     56.2              9.2            28.7             0.5    2.8

          May    15.2    109.0              10.6            72.4             0.5    3.7
       .~                          88.4            10.5             55.7
       - Aug.    18.3    115.3             15.0             78.9             0.3    3.6

          Oct.    14.6     72.9              7.2            41.0             0.7    3.2

          Jan.   17.3      40.2             10.9            22.0             0.6    1.8

       ' May    20.4       59.8             8.1            32.0              1.2    2.8
       tc                          50.9             7.9             26.3
       r Aug.   17.6       64.7              3.6            32.7             1.4    3.2

          Oct.   17.5      38.8              9.2            18.5             0.8    2.02

    daytime primary productivity (NPP), and respiration (R) for each reef at each
    season appear in table 1. Back reefs are more productive than fore reefs. A
    mean annual GPP of about 17.5 g C/m2/d is recorded at Isaac Reef, 19 g C/m2/d at
    Halfpenny Reef, and 33 g C/m2/d at Robin Reef (with a mean maximum value of 43.2
    g C/ml/d recorded in August and a mean all-reef productivity of 8500 g C/m2/yr).
    These values are based on a conversion ratio of 0.375 g C/g902 with a metabolic
    quotient for reefs of 1.1 (Marsh and Smith, 1978) applied to the means in table

                                              172

    1.  They are derived from the molecular weight difference and the ratio of
    oxygen to carbon dioxide exchange (the metabolic quotient) for reefs (Marsh and
    Smith, 1978). Higher GPP have been reported (Helfrich and Townsley, 1963;
    Connor and Adey, 1977), but such high levels of productivity have been subject
    to question. Because of this, great care was taken in data collection, and
    every potentially error-producing factor has been carefuly considered (see
    Adey, et al., 1981). The patterns we observed are not surprising once the
    processes affecting reef productivity are examined.

    Processes Affecting Reef Productivity

         Rates of carbon fixation on reefs reflect a complex interaction of
    environmental factors. Slight variations in some of these factors (water depth,
    biotic composition, substrate availability, or solar radiation) will affect
    these values. In the remaining sections of this paper, we will describe the
    results of our studies of biological, chemical, physical, and geological factors
    as they affect overall reef productivity.

    Biological Components: The Role of Algal Turfs

         Benthic algae, as both free-living forms and endosymbionts in coral and
    other invertebrates, are the primary producers on reefs. The focus of our
    study was on free-living benthic algae because it was the most abundant biological
    component of the reefs we studied (see table 2). Large-scale and small-scale
    data were integrated to determine community structure. Large-scale cover was
    based on chain transects and is presented as a measure of reef complexity (SAR)
    for the fore and back reef of each transect in table 2. Small-scale cover is
    based on point counts of prepared microscope slides (table 3).

         To test the hypothesis that algal turfs are the most important primary
    producers of the St. Croix reefs, we compared rates of turf biomass production
    with rates of flow respiratory production. To make such a comparison, several
    conversions are necessary to obtain common units of measure. All conversions
    involve values from either table 1 or 2, or from published literature for a
    similar environment. Values for each back reef will be reported in east to
    west order (i.e., Isaac, Robin, and Halfpenny Reefs, respectively). Algal NPP
    was calculated from community GPP values (table 1) by multiplying by 0.24,
    which is the mean NPP/GPP ratio derived from chamber studies of algae by Wanders
    and Wanders-Faber (1974) and Rogers and Salesky (1981). ~he resulting algal
    NPP values for back reefs are 11.2, 21.2, and 12.2 g 02/m /d.  To equate our
    projected m2 of a complex reef to a surface rather than a projected area, we
    divided by the SaR (table 2). This gave values of 4.1, 7.1, and 9.9
    g 02/(surface)/m /d. Assuming that all productivity was from algal turfs, we
    divided the surface production values by the proportion of turf in the back
    reef (table 2) (values of 15.8, 19.7, and 18.5 g 02/(planar) m /d. Oxygen
    production was converted to carbon production by multiplying by the difference
    in molecular weight (0.375) and dividing by the photosynthetic quotient for
    reefs (1.1) (Smith and Marsh, 1978), giving values of 5.4, 6.7, and 6.3
    g C/(surface) m2/d.  The conversion of carbon to organic matter involves the
    ratio of 2.2 dry wt/g C (Westlake, 1963, and confirmed by our carbon analysis of

                                            173

        Table 2.--Mean depth, major benthic components (% cover), and surface area
                                 ratio on chain transects.

                                                                                  Surface
              Mean   Acropora  Other                          Algal  Macro-        #    Area
              Depth  palmata   Corals  Millepora  Corallines  Turf   Algae  Sand  (m)  Ratio

    Fore Reefs

    Isaacs      6.3    18.9       7.2      5.1        8.4    40.1   10.1    8.2  16  1.87

    Robin       5.1    16.2       1.5       0          8.2    65.1      0      0    13  2.36

    Halfpenny   4.5    10.3       9.2     11.2        16.2      9.9    8.6   35.0   14  2.51

    Back Reefs

    Isaacs     0.9    65.9        0.8       0          1.9    25.9   5.7      0    6   2.70
    Robin       0.7    19.7        0       0.6         6.5     36.1   10.1  26.7   10  2.98
    Halfpenny   0.3      0        8.2       0           0      53.5    8.4   29.9  25   1.23

                                                                                        l
     St. Croix turfs). This means that the rates of organic matter production of
     10.0, 14.7, and 13.9 g (dry)/m2/d on actual reef surfaces (rather than projected
     area) are necessary to produce the rate of oxygen production we observed in the
     water flowing over reefs.

          Tests of these theoretical rates of biomass production were supported in a
     recent study in similar lagoon and back reef environments of Mayaguana in the
     Bahamas (Adey and Goertemiller, in ms.).  By harvesting algal turfs grown on
     screens, actual biomass production was found to be 6-18 g (dry)/m2/d.  A mean
     rate of 12 g (dry)/m2/d, under a nutrient regime of 0.10-0.13 microgram-at N/1
     (NO2 + NO3) (D'Elia, in prep.), was achieved.  A similar and more recent study
     at Grand Turk, Turk, and Caicos Islands (Peyton, et al., in prep.) gave rates
     of algal turf production of up to 31.8 g (dry)/m2d/d  tnutrient concentrations
     (as measured by NO2 + NO3 nitrogen) of less than 0.2 microgram-at N/1.  Steneck
     and Porter (in prep.) used a similar harvest technique for turfs growing on
     slabs of coral substrata at a depth of 10 m and found a production rate of 6.0
     g (dry)/m2/d.  These harvest production rates are minimal since they do not
     include losses to micro-herbivores, abrasion, leaking of dissolved organics, or
     the release of reproductive structures.  Thus, the values we obtained using
     upstream/downstream flow respirometry correspond well with measured rates of
     biomass produced by this "functional group" of algae (sensu Steneck and Watling,
     1982) in the Caribbean. This also supports the pattern of high rates of
     production (per unit biomass) for turf algae that have a high surface area to
     volume ratio (Odum, et al., 1958; Littler, et al., 1983) and, perhaps equally
     important, live in a strong wave surge environment.

                                            174

    Table 3.--Dominant algal turf genera and abundance as determined by point counts
      (% mean abundance top and bottom of samples). Data were generated at the
      species level and are in Adey, et al. (1981).

                                                    Mean   Isaac  Robin  Halfpenny
                 Non-Heterocysted Blue Greens        10.7    9.5    12.7       10.1

                 Heterocysted Blue Greens             7.3   14.6      5.1       2.2

                 Sphacelaria spp.                     7.2    7.3    11.8        2.7

            +-   Endolithic algae                     7.1    7.1      5.1       9.1

                 Polysiphonia spp.                    3.9    2.6      3.1       6.0

            �_  Taenioma sp.                          3.8    0.7      2.1       1.0

                 Herposiphonia spp.                   4.4    2.1      3.6       7.7

                 Lobophora sp.                        2.7    3.7      4.4       0

                 Jania spp.                           2.5    2.4      4.2       1.0

                 Non-Heterocysted Blue Greens        18.9   18.0    20.0       18.5

                 Jania spp.                          10.8    8.0    18.7        5.8

                 Amphiroa spp.                       10.3   13.4    14.5        3.2

                 Endolithic algae                     3.7    2.7      0         8.5

                 Gelidiopsis sp.                      2.1    3.8      2.0       0.4

                 Asparagopsis (Falkenbergia           1.6    0.6      3.9       0.2
                                     stage)
                 Heterocysted Blue Greens             1.5    3.7      0.3      0.5

                 Sphacelaria spp.                     0.8    2.2      0.4       0

         We found over 100 species of algae (mostly in turfs) in the course of this
    study. Of these, only 30-50 species were common throughout the year, and fewer
    than 10 were common at any site in a given season (table 3).  The most
    consistent elements on (and in) the upper surfaces of dead coral substrata were
    cyanobacteria, boring algae, and filamentous red and brown algae. A high

                                              175

    diversity of algae in low abundance was recorded on virtually every specimen
    regardless of season, reef, or zone.

         Cyanobacteria of 6-8 species formed a large part of the turf biomass on
    both fore and back reefs. Heterocysted species (particularly Calothrix spp.)
    are far more abundant in fore reefs than back reefs, but nonheterocysted species
    (e.g., Oscillatoria) were most abundant overall. Of eukaryotic filamentous
    algae, the brown (Sphacelaria spp.) and red (Polysiphonia spp., Herposiphonia
    spp., and Taenioma macrourum) species dominate fore reef substrates. Boring
    filaments (usually green algae, e.g., Ostreobium) were also ubiquitous.  The
    predominant macroalgae are calcareous, articulated red algae (e.g., Jania
    capillacea and Amphiroa fragilissima) which are found on bottom surfaces in the
    fore reef and on both top and bottom surfaces in back reefs. Crustose corallines
    (Porolithon pachydermum and Neogoniolithon megacarpum) were most abundant in
    the shallow fore reefs, particularly where grazing is intense.  Of the fleshy
    macroalgae, Lobophora variegata and Acanthophora spicifera were found but they
    were not abundant compared to the turf community. Minute macrophytes such as
    Gelidiella trinitatensis and Gelidium pusillum commonly were found in the turfs
    of the back reef.

         As shown in table 3, the differences between fore reef and back reef turf
    community structure along the St. Croix reef track are rather consistent.
    These numbers and the community structure of the turf species we found agree
    with that found on a reef in Curacao by Van den Hoek, et al. (1975).  With the
    exception of Lobophora variegata (which does not appear in Van den Hoek, et
    al., 1975, for Curacao) and Dictyota dichotoma (which was common in Curacao but
    not in St. Croix), the floras  for Curacao and St. Croix are quite similar.  There
    are also floristic similarities for the same reef zones between the Caribbean
    and Indo-Pacific at the genus level (Hatcher and Larkum, 1983; Sammarco, 1983).

         It is beyond the scope of this study to examine the myriad of factors
    maintaining turf algal community structure.  Most studies indicate that intensive
    herbivory in productive environments is important for maintaining a turf
    community (Borowitzka, 1981; Carpenter, 1981; Littler, et al., 1983; Sammarco,
    1983; Hatcher and Larkum, 1983).

    Primary Production: Not Nutrient Limited

         High primary productivity on reefs growing in nutrient poor water has
    received considerable scientific attention (reviewed by Mann, 1982). The
    resulting research has focused on the role of cyanobacteria as in situ nitrogen
    fixing organisms (Mague and Holm-Hansen, 1975; Capone, et al., IT77T.  Recently,
    Sammarco (1983) demonstrated that fish grazing on the Great--arrier Reef can
    cause a shift in the community structure of turf algae from filamentous reds
     (e.g., Polysiphonia) to minute filamentous cyanobacteria. Other studies have
    demonstrated that, as a result of this change in community structure, nitrogen
    fixation is significantly enhanced (Wilkinson and Sammarco, 1983). Our results
    support their conclusions.

         Heterocysted (nostocacean) and nonheterocysted (hormogonalean) cyanobacteria m
    are abundant in turfs growing on the upper surfaces of all reefs that we

                                             176

    Table 4.--Nutrient levels.  Each value is a mean of two replicates taken on
                   different days over approximately a 10-day period.

                       Nitrate + Nitrite (ug-at/1 - N as NO3 = NO2)

                                                                          Yearly
                                Jan       May        Aug        Oct       Mean

         Isaac       Fore      0.386        X       0.345        X        0.366
                      Back     0.980      0.302      0.391       .772     0.611

         Robin        Fore     0.294      0.175      0.549       .075     0.273
                      Back     1.016      0.328      0.589       .220     0.538

         Halfpenny   Fore      0.340        X        0.823       .107     0.423
                      Back     0.650      0.629      0.816       .099     0.549

         Channel      Fore                           0.457       .150
                      Back                           0.686       .130

         Airport      Fore     0.223      0.228        X         .050     0.167
                      Back     0.466      0.350        X         .130     0.315

                                                                      Grand Mean
         Means        Fore     0.311      0.,134      .572     0.096      0.283
                      Back     0.778      0.401       .599     0.270      0.512

                                     Phosphate (ug-at/l - P)

         Isaacs      Fore      0.024                0.118      0.032      0.058
                      Back     0.046                 0.020     0.038      0.035

         Robin       Fore      0.010                 0.055     0.187      0.084
                      Back     0.037                   X       0.047      0.042

         Halfpenny   Fore      0.010                 0.275     0.049      0.111
                      Back     0.034                 0.392     0.161      0.196

         Channel     Fore                                      0.080
                      Back                                     0.030

         Airport      Fore     0.010                 0.145     0.052      0.138
                      Back     0.017                 0.165     0.143      0.108

         Means        Fore     0.013                 0.148     0.080
                      Back     0.033                 0.192     0.084

                                             177

    studied, but particularly on fore reef and sand substratum habitats of Isaac
    Reef. Results of nutrient analyses for nitrate plus nitrite and phosphate are
    listed in table 4. The nitrite and nitrate concentration strongly increases in
    the water as it flows over the three reefs studied. Ten of the twelve sets of
    measurements showed a highly significant yearly increase of 0.35-0.57 microgram-
    at/1 across the reef. With a mean yearly flow rate of 6.83 m3/min/m for all
    three transects (discussed below), this translates to a net "fertilization
    rate" of 0.82 kg N/hectare/d (or 0.08 g N/m2/d).  While this is roughly half the
    rate estimated by Wieb, et al. (1975) for Eniwetak, the maximum rates we
    encountered on the south shore reef of St. Croix were three times the mean.

         We assume that this fertilization is due to nitrogen fixation by cyanobacteria
    (Wilkinson and Sammarco, 1983), but other possibilities exist. Regeneration of
    nutrients from the internal cavity of a reef was demonstrated by Andrews and
    Muller (1983). However, this is unlikely to occur on St. Croix reefs, since
    the coral of these reefs grows on a pavement, below which the reef structure is
    remarkably tight, with cavities usually sand filled (Adey, 1975; Adey and Burke,
    1976). Empty cavities for nutrient regeneration are rare in St. Croix, which
    is arid, devoid of rivers, and lacking in upwelling aquifers. Thus, nutrient
    enrichment from ground water, such as that described in Jamaica (D'Elia, et
    al., 1981) is unlikely. Nitrogen fixing algae may achieve a competitive iavan-
    tage in more oligotrophic waters, and thus nutrient availability probably has
    some significance in determining community structure. Nevertheless, the
    fact that this "excess" nitrogen escapes from the reef and flows over the highly
    productive back reef suggests that primary production on the reef proper is
    not nitrogen limited.

         Phosphorus is more problematic, since an atmospheric source is not possible.
    Reactive phosphorus as phosphate can be difficult to measure and, as briefly
    discussed above, older work did not generally show any consistent pattern of
    change in reef environments. A recent paper by Atkinson (1982) does show
    significant upstream-downstream depletion of phosphate across 1000 m of reef
    flat in Hawaii. However, in our St. Croix situation, with a mean incoming
    concentration of 0.084 microgram-at/I and a mean current flow of 6.83 m3/min/m,
    phosphorus as phosphate is delivered to a meter width transect of reef at a
    rate of about 25 g/d. Even if all net primary productivity were to be exported
    from these reefs, using a C/P of 430 (from Atkinson and Smith, 1983, for turfs),
    only about 6.4 g P/d/meter width would be removed.  Thus, phosphorus is present
    in large quantities, though at low concentrations, from the constantly inflowing
    waters of the North Equatorial Current as it impinges on St. Croix.

    Epibenthic Water Flow and Discharge Rates

         Nutrient availability, gas exchange, and metabolite release for aquatic
    primary producers is facilitated by water flow past algal thalli. Water flow
    over reef substrata (epibenthic water flow) is dependent upon the discharge
    rate (movement rate per volume of water), water depth, and on the wave surge or
    oscillation rate of the overflowing water. In St. Croix, water movement over
    the reefs results primarily from wind-driven wave energy. Thus, measured rates
    of epibenthic water flow have geologic (depth) and geographic (wind) components.

         Epibenthic flow rates over reefs are variable in space and time.  These
    variations can affect both the productivity of the reef and the measurements of

                                            178

    it. For these reasons, great care was taken in determining water flow and
    discharge rates (this information is provided in detail by Adey, et al., 1981).
    Our measurements of water motion demonstrate that water flowing over the reefs
    oscillates but has a net shoreward flow. Typically, we recorded a landward
    surge of 6-8 s duration (reaching speeds of about 0.3-0.6 m/s) and a reverse surge
    lasting 2-4 s (reaching 0.05-0.3 m/s). Net epibenthic water flow was determined
    from chart recordings of mean maximum currents in both directions (i.e., the
    peaks of spikes) integrated over 1 hr intervals from Marsh-McBirney current meter
    data. Reversing wave surges and accompanying turbulence produced by waves breaking
    over irregular reef surfaces mix the water flowing over the reef, particularly
    for back reef habitats where measured rates of production are the greatest. The
    turbulent effect of wave surges also significantly increases metabolite exchange
    and resulting photosynthesis and growth (Hackney, et al., in ms.).

         Epibenthic flow rates increase dramatically from fore to back reef. Means for
    all reef transects were 1.2 + 0.066 m/min for fore reefs and 11.0 + 3.5 m/min for
    back reefs. This increased Tlow rate results from the progressive-shallowing from
    fore reef (overall mean depth of 5.3 m) to back reef (overall mean depth of 0.6 m).
    With a constant discharge rate, flow rate varies with depth. Since depth changes
    daily with tidal changes, we recorded tidal heights during each sampling period.

         Discharge rates are not constant because wind-induced water movements change
    geographically along the south shore of St. Croix due to the island's effect of
    diminishing the strength of easterly trade winds. Specifically, in the fore
    reef environments, Isaacs Reef to the east has the highest discharge rate (mean
    8.1 m3/min/m, range 2.5-12.1 m3/min/m, N = 65 1 hr intervals). Robin Reef is
    intermediate (mean 6.2 m3/min/m, range 2.8-9.8 m3/min/m, N = 86 1 hr intervals),
    and Halfpenny Reef is the lowest (mean 5.3 m3/min/m, range 1.4-9.8 m3/min/m, N = 79
    1 hr intervals). These discharge rates created mean back reef epibenthic flow
    rates of 9.2, 8.8, and 15 m/min/m, respectively.  Although a geological pattern
    in exposure from east (most exposed) to west (least exposed) results in a
    similar pattern of decreased discharge rates, the magnitude is much less than
    the difference observed between back reef and fore reef at any one location.

         There is little support for the hypothesis that reef productivity is
    controlled by water motion even though differences in flow rates between fore
    and back reefs roughly correspond with differences in rates of production. If
    reef productivity was primarily dependent upon water flow, diurnal reef produc-
    tivity curves (figs. 4 and 5) would level off at the point where light saturation
    occurred rather than corresponding closely with variations in light intensity
    (discussed below). Also, for any given reef, productivity would correspond
    with data on water currents, which we did not observe. Water motion is an
    important factor, but the south shore of St. Croix is characterized by consis-
    tently high wind-induced wave energy year round (see Adey, 1978b); thus, water
    motion does not appear to limit productivity. Note that there Ts no relationship
    between reef productivity (table 1) and epibenthic flow rates.

    Light

         Primary production on the reefs we studied is most likely controlled by
    light. Evidence for this comes from the correspondence between diurnal and
    seasonal cycles in light intensity (fig. 6) and measured rates of primary

                                             179

                                MEAN SOLAR RADIATION-ST. CROIX

                                                X

          2  -

         500 -
      z
      0
      i-     -

                                            x~~~

                              X
         400 -
      z
           4~~~~~

                       x

                        /
                                x~~~~~~~~~~~~

         300   '          '           '      '      I '       '          X
                     Dec Jan  Feb  Mar  Apr May June Jul Aug Sept Oct Nov
                                             (1978)

                   Figure 6.--Monthly means of daily solar radiation.

    production (figs. 3, 4, and 5). If any other environmental factor was
    limiting, the rate of oxygen production would level off, indicating light
    saturation. In contrast to our field measurements, most studies using enclosures,
    even with stirring, commonly report light saturation. This is likely an artifact
    of insufficient water motion. In more recent work with chambers (e.g., Carpenter,
    in ms.), where efforts have been made to simulate surge motion, this lack of
    light saturation for algal turfs is repeatedly demonstrated.

         In this investigation, daily solar radiation levels were recorded with a
    pyroheliometer (see fig. 6 for monthly mean values). During our study we
    sampled two periods of high light intensity (May and August) and two periods of
    lower light intensity (January and October). Averaging hourly production rates

                                            180

              100

                 w~~~~~~

       I-
          ~' 60.

       =c7d
           so
       0  E
       L   mean IS

           0  20-
       0
                                                     ()annual mean- individual rest
                                                    a seasonal mean -all reefs

               0          200         400        600        800       1000

                          TOTAL ALGAL BIOMASS (AREA x SAR. x BIOM.1
                                      [gm dry/M2 projectedl

    Figure 7.--Back reef: Gross primary productivity as a function of total algal
                          biomass and monthly solar radiation

    for all reefs reveals a strong seasonal pattern in productivity corresponding
    to these seasonal differences in light intensity (fig. 5). Although the seasonal
    decrease in primary productivity roughly corresponds to a 40% reduction in
    light during that period, the relationship is not exact, since the GPP in October
    is reduced to only 30% of that value in May. A better correspondence exists
    between the seasonality of primary production and the combination of algal
    biomass and solar radiation. Loss of light in autumn is exacerbated on St.
    Croix by a higher frequency of rainfall and cloudiness. Thus, incoming light
    in October and November is considerably below that of December and January
    (fig. 6).

         The GPP data, when plotted directly against total algal biomass (per
    projected m2, fig. 7), suggests that a weak relationship between productivity
    and total biomass exists on these reefs (note that this is not surface biomass
    alone, but includes the effects of SAR and percent cover of algae). Also, the

                                            181

    plot of biomass as a function of seasonal productivity (line with closed circles,
    fig. 7) indicates a cyclic pattern. The sharp reduction in algal biomass
    recorded in the fall of 1978 (45% of that recorded in May) cannot be attributed
    to wave action, since that is generally a quiet season and no unusual conditions
    were experienced during the period of study. Data for nutrients (table 4) and
    suspended matter (Adey, et al., 1981) suggest very minimal effects of runoff on
    the reefs.  We observed, uETid not quantify, changes in the abundance of
    micrograzers (amphipods and worms). It is possible that during the spring and
    summer algal biomass and the resident micrograzers increase with higher levels
    of solar radiation. As light levels fall in autumn, grazing by the resident
    micrograzers exceeds rates of algal growth. Such overgrazing could result in a
    "crash" in both algal biomass and productivity.

    Geological Control of Reef Productivity: Synergy of Multiple Factors

         It is to be expected that those reefs which are less complex (lower SAR),
    deeper, with lower epibenthic water currents, and have a larger percentage of
    living stony coral (relative to algae)  will be less productive than the shallow,
    complex, algae-dominated reefs of the south shore of St. Croix.  All of these
    factors, however, are ultimately the result of the reef's geological history,
    and thus the relationship between reef morphogenesis and primary production
    should be considered.

         The south shore bank barrier reef system of St. Croix "matured" (i.e.,
    reached sea level) from west to east (see Adey, 1975; Adey and Burke, 1976, for
    a summary of the geological history of the reefs of St. Croix).  Isaac Reef is
    relatively young and is just reaching sea level today. Its live Acropora
    palmata cover is high (table 2), but its reef flats are narrow and the crest is
    broken (forming numerous channels).  Robin Reef is more mature, as evidenced by
    its nearly continuous crest and wide, relatively shallow back reef. While
    living Acropora palmata is still an important constituent, the percent cover of
    A. palmata on Robin back reef is less than a third of that found on Isaac back
    reef (table 2).  Halfpenny Reef is older and has a continuous crest and a very
    shallow reef flat with very few living acroporids.  The age difference between
    Isaacs and Halfpenny Reefs is about 500-1,000 yr.

         Productivity on the young Isaac Reef is low, even though its SAR is quite
    high. This is because coral is less productive than algae per unit of surface
    area (Rogers and Salesky, 1981).  At the other extreme, coral cover is low at
    Halfpenny Reef, and this shallow reef flat is dominated by turf algae. However,
    this reef is nearly planar (the SAR is half that of the other reefs), and thus
    the surface area available for turf photosynthesis is proportionately reduced.

         Because carnivorous predators are so abundant on reefs, herbivores do not
    stray far from their refuge in the spaces within the reef (e.g., Ogden, et al.,
    1973; Talbot and Goldman, 1972).  Thus, reefs with a high SAR are more h-eav-T
    grazed because they have more habitat space for reef-dwelling herbivores. In
    this way, geological events that contribute to a high SAR on reefs also maintain
    herbivore populations that intensely graze the dead coral substrate, thereby
    maintaining the turf communities.

                                            182

         Light levels, depth, current velocity, and abundance of live Acropora
    palmata all increase with geological time as a reef grows toward sea level.
    As it reaches the surface, several of these trends reverse (i.e., coral dies
    and water flow decreases). Aspects of this complex relationship between reef
    morphogenesis and primary productivity can be seen along the south shore of St.
    Croix. For example, productivity was greatest for the mature Robin Reef and
    lower on the younger Isaacs and older Halfpenny Reefs (fig. 7). On Robin Reef,
    the SAR of primarily dead Acropora palmata is very high and algal cover is
    about 80% greater than that of Halfpenny.  Thus, peak productivity probably
    occurs soon after the transition from a live, coral-dominated reef to one of
    equal surface area but dominated by algae. With time, productivity declines as
    destructive forces (e.g., bioeroding sea urchins or severe storms) reduce the
    standing dead coral to a pavement-like algal-dominated flat. This pattern of
    reef succession is characteristic of many reef systems. Adey, et al.
    (1977) described a similar history for the now largely planar aT-gaT dominated
    pavement in eastern Martinique. Over the past 500 yr the open Acropora palmata
    reef matured and lost its structure, possibly due to a catastrophi event suc
    as a hurricane. It has remained an algal pavement, devoid of coral, ever
    since. In the case of Martinique, excess sediment and nutrient runoff from
    the island following the introduction of intense sugar cane farming in the 17th
    century undoubtedly was a major factor in transforming these reefs into macroalgal
    pavements. After the completion of this study in 1978, a similar event occurred
    at the south shore of St. Croix when a hurricane passed off the coast in 1979.
    Rogers, et al. (1982) documented the event and showed a significant reduction
    in SAR and live coral following the hurricane.

         Differences in reef morphogenesis may be responsible for some of the
    reported differences in reef productivity. Holocene sea level characteristics
    for the Indo-Pacific differs from that of the Caribbean.  Sea level rise stopped
    over 5,000 yr ago in the Indo-Pacific (reviewed by Adey, 1978a), resulting in the
    characteristic old reefs of the region having emergent, broad reef flats (many
    km wide), often with no epibenthic water flow during low tide and with a low SAR.
    This extreme "old age" condition of Indo-Pacific reef flats, developed under
    stable or dropping sea levels, contrasts with conditions in the Caribbean, where
    sea level has been slowly rising until the past several centuries (e.g., Adey,
    et al., 1978a). This geological characteristic of reefs could be responsible
    for the loweF levels of primary production reported for the Indo-Pacific compared
    to results presented here for the St. Croix reefs.

                                      CONCLUSIONS

         Fundamentally, reef productivity is controlled by its geology (reef growth
    and morphogenesis). Coral reefs grow slowly towards sea level over time,
    thereby changing their physical, chemical, and biological environment. Primary
    productivity is maximal at the time when the reef surface is becoming too
    shallow to support a large cover of live coral but'still deep enough for contin-
    uous water flow. Dead branching coral (Acropora palmata) in standing position
     provides a complex and convoluted substratum on Which minute algal turfs can
     grow and herbivores can take refuge. The structurally complex reefs maintain a
     high biomass per projected area of reef, thereby increasing the total turf

                                             183

    biomass. The intense grazing maintains the algal community at the turf stage,
    wherein the productivity per unit biomass is very high.

         Facilitating this high productivity are nitrogen fixing cyanobacteria that
    fix more nitrogen than is required by even the most productive reef zones.
    Other nutrient requirements, particularly phosphorus, are met by the combination
    of continuous and strongly flowing equatorial currents as well as by constant
    wave-driven currents. This, with the lower phosphorus requirements of algal
    turfs, results in a highly productive community that is not limited by nutrient
    availability.

         Thus, synergy is attained by the interaction of factors that optimize reef
    productivity. If any factor is removed from this system (i.e., water depth,
    SAR, wave oscillation, water flow, or algal community structure), the primary
    productivity would be less than we found.

         The back reefs we studied are among the most productive biological
    communities in the world. Using standard conversions, our measurements of a
    mean annual gross production of about 23 g C/m2/d and a net production of about
    14 g C/m2/d exceed the theoretical maximum gross productivity hypothesized by
    Ryther (1959) of 17 g C/m2/d and the net productivity of 12.3 g C/m2/d. On the
    other hand, this is not unreasonable, since maximum experimental rates of net
    production of 22-31 g (dry)/m2/d (approximately 9-12 g C/m2/d) have now been
    found in both laboratory and field environments. Limitations to primary
    production due to desiccation, nutrient availability or gas exchange (Lieth and
    Whittaker, 1975) are nonexistent or of reduced importance on the reefs of St.           0
    Croix. Thus, productivity of these reefs seems to be limited by the ultimate
    limiting source: incoming solar radiation.

                                    ACKNOWLEDGMENTS

         This study was supported by the Smithsonian Institution, the Virgin Islands
    Government and the West Indies Laboratory of Fairleigh Dickinson University.
    We were assisted for much of the study by Caroline Rogers and Norman Salesky.
    Additional help came from Sara Armstrong, Susan Brawley, Robert Carpenter, and
    members of the West Indies Laboratory staff. Caroline Rogers, James Norris,
    Susan Brawley, Chris D'Elia, and John Ogden read early drafts of this manuscript
    and offered suggestions for its improvement. Steve Smith offered some valuable
    suggestions for improvement of the final manuscript.

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                                           187

    I

                                STUDIES ON THE BIO-OPTICS OF CORAL REEFS

                                             Phillip Dustan
                                         Department of Biology
                                         College of Charleston
                                  Charleston, South Carolina 29401

                                               ABSTRACT

                This paper examines the possibility of using underwater light measurements
           to study the primary productivity of coral reefs. This is a new technique that
           may have wide ranging uses as man begins to use remote sensing to study the
           processes taking place on the surface of the Earth.

                                              INTRODUCTION

                Sunlight is the primary source of energy for the coral reef ecosystem.
           Photosynthetic reef organisms utilize light to liberate oxygen from water, fix
           carbon, and enhance the rate of calcification. This paper will examine the
           concept of using bia-optical techniques (Smith and Baker, 1978a; Gordon, et
           al., 1980) to measure the input of light energy to coral reef 'Ecosystems. The
           simplicity of the technique, combined with nondestructive sampling, may enable
           reef ecologists to study the productivity and flow of energy into coral reefs
    .      ~~at a higher level of ecosystem organization than is presently possible.  In
           addition, it is of interest to understand the entrance of energy into these
           benthic ecosystems since many reef organisms may be termed polytrophic (Muscatine
           and Porter, 1977), and because the structure and dynamics of the primary
           production trophic level may have an influence on the structure and/or organization
            of subsequent higher trophic levels. Understanding the optics of coral reefs
           also holds the promise of one day being able to study these complex and remote
           ecosystems from orbiting spacecraft and other remote sensing platforms.

                 Investigators have long sought a technique that would quantify the primary
           productivity of coral reefs. For the most part, estimates have been made using
            respirometry and/or radiotracer experiments which have been extrapolated to the
           areal extent of the reef (see part III in Stoddart and Johannes, 1978, for
            review). While these techniques usually are precise, they are subject to errors
            in scale which arise from extrapolating data from an experimental specimen to
            the reef community. Another way to estimate primary production is to measure
            the input of light energy to the system over a relatively large area of substrate.
            Then, using known and theoretical estimates of the quantum efficiency for
            photosynthesis, it should be possible to estimate primary production on a scale
            commensurate with the scal-e of the reef ecosystem.

                 The initial step in primary production is the harvesting of light by the
            photosynthetic pigments of the primary producers (Rabinowich and Govingee,
            1969). This process is a function of the available light, both spectral quality
            and intensity, and the absorption characteristics of the algae. The absorption
    *      ~~and reflectance of light by phytoplankton also can be influenced by the
            nutritional state and age of the alga (Kiefer, 1973; Kiefer, et al., 1979;

                                                    189

    Wilson and Kiefer, 1979).  Present models that describe the light-limited growth
    rate of cultured phytoplankton have been formulated using the estimated quantum
    efficiency of photosynthesis and the cellular cross sectional area for light
    absorption (Laws and Bannister, 1980; Kiefer and Mitchell, 1983).  The formulation
    of similar models for coral reefs might provide estimates of primary production
    that would be applicable to different reef systems, habitats, or zones on a
    scale that is commensurate with the scale of these ecosystems. Formulation of
    such models requires the ability to make reliable estimates of light reflectance and
    absorption for the reef community.

         Morel (1978) defined a measure of light absorption termed Photosynthetically
    Useable Radiation (PUR). PUR defines the fraction of Photosynthetically
    Available Radiation (PAR) that a photosynthetic organism can absorb and have
    available for chemical work. PUR is the integrated product of normalized cellular
    spectral absorption and the spectral irradiance available to the organism
    (Morel, 1978). Measures of PUR are relative measures, though, and cannot be
    related to an absolute measure of the quantity of light being ~bsorbed. However,
    much can be learned by comparing the relative light absorption of photosynthetic
    organisms from different light environments.

         Calculations of PUR for isolated zooxanthellae from the reef-building coral
    Montastrea annularis (Ellis and Solander) have shown that the fraction of light
    absorbed varies at different depths, suggesting that the capture of light
    energy by these zooxanthellae varies as a function of the available light field
    (fig. 1; and Dustan, 1982).

                                        METHODS

         Optical oceanographers have developed precise terminology that describes
    the behavior and measurement of light in the underwater environment. Spectral
    irradiance is defined as the spectral components of the light field that impinge
    on a flat-plate, or cosine collector. Across each horizontal plane in the
    hydrosol are upward and downward flowing flux defined as upwelling and downwelling
    (Tyler and Preisendorfer, 1962; Gordon, et al., 1980). The ratio of upwelling
    to downwelling is termed spectral reflectance and is the basis for the measurement
    of remotely sensed optical signals (Gordon, et al., 1982; Smith and Baker,
    1978b). The difference between upwelling and downwelling at the surface of a
    substrate is the amount of light that is absorbed by the substrate. It is
    presently impossible to directly measure the upwelling irradiance close to the
    substrate because the shadow of the instrument alters the light field. However,
    the upwelling and downwelling irradiance at the reef substrate can be estimated
    by taking sets of upwelling and downwelling measurements above the substrate.
    From these data, the diffuse attenuation coefficient for spectral irradiance is
    calculated, and this quantity is used to calculate the light intensities at the
     surface of the substrate (Smith and Baker, 1978b). These derived data will
     vary with water depth, species absorption properties, and the ambient light
     field. Thus, measurements must be taken throughout the daytime period and at
     systematically varying depths to use these measurements as an index of light
     energy absorption and a community-specific spectral absorption signature. At
     this time, we do not fully understand the relationship between this derived measure
     and the actual amount of light absorbed by photosynthetic reef organisms, but,
     as a first approximation, the measure represents a maximum value which includes

                                            190

            1015            i

                                                    ALGAL DEPTH / LIGHT DEPTH -

     E

       c   1012_                              _
       6   '    _\                                             \31.5- 30 m
    X,                                                   \

    Figure  .--Photosynthetically Useable Radiation of zooanthell0ae isolated from

      spectroradiometer.  Note that the algae from different depths vary with
             109            l          l   191
               400        450        500         550        600         650        700

                                         WAVELENGTH rnm)

    Figure 1.--Photosynthetically Useable Radiation of zooxanthellae isolated from
      Montastrea annularis, Discovery Bay, Jamaica. Relative whole cell absorbance
      was measured at low temperature with a modified Cary 14 spectrophotometer.
      Measurements of underwater spectral irradience were made with a prototype
      spectroradiometer. Note that the algae from different depths vary with
      respect to their absorbance of light energy and its spectral quality (see
      Dustan, 1982, for experimental details).

    the absorption of light by both animals and plants. As such, the data will
    overestimate actual primary production until the measure is more fully understood
    and the model appropriately refined.

                                              191

    Table 1.--Preliminary calculations of light energy absorbed by a coral reef
      community.  Surface PAR light levels averaged 1.47 x 1017 quanta/cm2/s during
      the experiment. Measurements were carried out on Dancing Lady Reef, Discovery
      Bay, Jamaica, W.I.

                                  Calculated quanta          Percent of Incident
    Depth         Substrate         Absorbed (q/cm2/s)            Downwelling PAR
                                    (400-700 nm)                (400-700 nm)

    10 m            sand              2.679 x 1016                     87.0

                   coral             2.429 x 1016                     92.7

    30 m            sand              7.42 x 1015                      68.0

                   coral             1.08 x 1016                      957

                                     FIELD STUDIES

         In 1978 we developed a small submersible spectroradiometer to study the
    photobiology of zooxanthellae (Booth and Dustan, 1979).  I used the instrument
    to characterize the light field on Dancing Lady Reef, Discovery Bay, Jamaica,
    with special emphasis on the photobiology of Montastrea annularis, one of the
    principal reef-building corals on both the deep and shallow reefs of the region
    (Dustan, 1982).  As part of this study, I made systematic measurements of
    upwelling and downwelling irradiance and reasoned that it might be possible to
    measure the amount of light energy that the reef community "absorbs." In this
    experiment measurements were taken over sand, which was reasoned to be an
    almost perfect reflective surface, and over areas covered with living coral
    (see table 1).

         The calculations suggest that corals resemble black bodies in their
    absorption properties in both shallow and deep water environments. Reef sand
    is not a very good reflective surface, as I had first thought, but does absorb
    a smaller fraction of the incident light than corals. The difference in
    absorption between coral and sand is greater in deep than shallow water, possibly
    suggesting photoadaptive or geometric change in the members of the coral
    community.  The percentage of incident light absorbed by both substrates seems
    high, but since a reference of known standard reflectance was not used to
    "calibrate" the methodology, the degree to which light scattering and other
    possible nonlinear effects may distort the data is unknown. In addition, the
    sandy environment of coral reefs contains a variety of photosynthetic organisms,
    each with its own particular light absorption characteristics.

         A second set of spectroradlometer measurements was made in August 1982 on
    the Molasses Reef in the Key Largo National Marine Sanctuary, Florida. Spectral
    measurements were taken with a 15 channel spectroradiometer (Biospherical
    Instruments Mer-1015) during a research expedition in support of remote sensing
    of coral reefs (P. Dustan, C. R. Booth, and A. R. Hlbbs, unpub. data).  Data
    from a sandy zone on Molasses Reef gave a net absorbance of 1 x 1014 quanta/cm2/s
    which was 51% of the downwelling irradiance at the substrate surface (fig. 2).

                                             192

                              / OOWNWELLING

                E\

                C
                E

                C3 .   UP AND DOWNWELLING SPECTRAL IRRADIANCE      \
                  ^     ~~CALCULATED AT THE SUBSTRATE SURFACE  \ \
                  13    ~OVER A SAND BGTTOM ON MOLASSES REEF    \ \
                L        AT A DEPTH OF 7 METERS\ \
                L        MOLASSES REEF RUN 12  AUGUST 14. 1982\
                U

                 1
                cJ

                I0
                C
                  0     ~~UP AND DOWNWELLIING SPECTRAL IRRADIANCE
                  " ~~CALCULATED AT THE SUBSTRATE SURFACE
                         OVER A SAND BOTTOM ON MOLASSES REEF
                  L     ~~AT A DEPTH OF 7 METERS
                L-       MOLASSES REEF RUN 12  AUGUST 14. 1982
                         HER-1015 SPECTRORADIOMETER

                   0

                    400             soo              600             700
                                  Wave length  (nm.)

    Figure 2.--Calculated upwelling and downwelling spectral irradiance at the
      substrate surface of a sandy area 7 m deep on Molasses Reef, Key Largo. The
      difference between upwelling and downwelling irradiance equals the light
      absorbed by the substrate (1 x 1014 q/cm2/s).  Scans were calculated from
      sets of spectral irradiance data as described in the text.

    This fraction is somewhat higher than the earlier data from Jamaica but is
    within a range that could be considered acceptable, since the technique is in
    an early stage of development.

         Similar measurements made over a nearby grove of living coral on Molasses
    Reef revealed somewhat different and unexpected results.  The values for

                                             193

    upwelling spectral irradiance did not follow the expected pattern of exponential
    de ease with depth. As the instrument approached the coral, the spectral
    d- ribution of the upwelling irradiance showed a decrease in the blue and
    green regions of the spectrum but an increase at wavelengths greater than
    589 nm. Particularly striking was an increase in the far red at 694 nm (fig.
    3). The total integrated quanta in each scan follows the rule for conservation
    of energy and decreases with depth. The increase in the signal between 589 and
    671 nm results from reflectance of the yellow brown coral, which begins to
    "dominate" the spectral irradiance signature. The far red signal may be
    interpreted as an emission of red light due to algal fluorescence, as has been
    seen in oceanographic measurements of spectral irradiance (R. C. Smith, C. R.
    Booth, and P. Dustan, unpub. obs.). The intensity of the signal increases as
    the instrument approaches the coral (depth approx. 4.4 m), suggesting that the
    fluorescence may emanate from the zooxanthellae in the tissues of the coral.
    These findings complicate the calculation of an energy absorption budget for
    the coral, since the organism is simultaneously absorbing and emitting light
    and each process is functioning with its own wavelength dependency. However,
    the results suggest that we may have uncovered a measurable parameter that may
    one day be used to probe the photophysiology of corals and the bio-optics of
    coral reef ecosystems.

         Researchers are beginning to realize that the fluorescence signature of an
    alga contains information about the plant's photosynthetic apparatus, including
    information on its potential for primary productivity (Kiefer, 1973; Vincent,
    1979; Harris, 1980; Abbott, et al., 1982). The data on corals are particularly
    exciting, since they suggest that the spectral signals may contain information
    on the physiological state of corals and their zooanthellae in addition to
    possible estimates of primary production. This suggests that there is much to
    learn about the optics of corals and their associated zooxanthellae using the
    passive techniques of bio-optics.

                                     REMOTE SENSING

         Coral reefs cover areas of the ocean that are remote and difficult to work
    in for extended periods of time. They are also vast in their coverage of the
    world's tropical oceans and may play a significant role in the carbonate balance
    of the seas. If the optical signal emanating from the reef can be understood
    sufficiently to provide interpretation from an orbiting spacecraft, estimates
    of coral reef primary productivity and possibly calcification could be made on
    a global scale. The importance of this cannot be underestimated when one
    considers man's impact on the coral reef ecosystems that are presently in close
    proximity to centers of human habitation.

         Our research expedition to Florida in 1982 gathered data to test the
    hypothesis that coral reefs may be resolvable in spacecraft imagery (Landsat)
    (P. Dustan, C. R. Booth, and A. R. Hibbs, unpub. data). We obtained measurements
    of upwelling spectral irradiance from a variety of habitats in the shallow
    coral reef ecosystem of John Pennekamp Coral Reef State Park, including grass
    flats, coral colonies, and sand. We then simulated the spectral sensitivity of
    the Multispectral Scanner (MSS) onboard Landsat 3 so that the optical signal we
    recorded could be compared to the signal recorded by a Landsat MSS sensor.  The
    equation for the simulation then "converts" the spectroradiometer signal into

                                            194

                      I

                   E

                   E

                   4I) 0                                         \\\    4
                   � 0

                   D

                   03     UPWELLINC SPECTRAL IRRAOIANCE OVER Acroporo polmato
                   0o     MOLASSES REEF RUN 12  AUGUST 14. 1982
                   L      MER-lO15 SPECTRORADIOMETER

                          SCAN FILE DEPTH TOTAL QUANTA
                            #    n   (M)   (400-700nm)

                            1    40   1.8   1.9 x 1013
                            2    41   3.1   1.8 x 1013
                            3    43   3.6   1.7 x 103
                            4    42   3.9   1.5 x 1013
                            * OQ/cm2/suc
                      -1
                     10
                       400             500              600              700
                                      Wovelength  (nm.)

    Figure 3.--Upwelling spectral irradiance scans taken over a grove of elkhorn
      coral, Acropora palmata, at 4.4 m depth on Molasses Reef, Key Largo. Note
      that 589 nm is a relatively invariant wavelength. The increase in far red at
      694 nm is interpreted as in situ fluorescence by the symbiotic zooxanthellae
      of the coral.

    the bandwidths of the Landsat MSS sensor:

    Band 1 (green) = (.091x488nm + .76x507nm + .913x520nm + .98x540nm
                      + .97x570nm + .75x589nm + .05x625nm) / 4.514

                                              195

                          KEY LARGO. FLORIDA
                          UPWELLING SPECTRAL IRRADIANCE AT SURFACE
                          RUN 2 AUGUST 13. 1982 CLEAR SKY
                          MER-1O0S SPECTRORAOIOMETER

                 E

                 N

                 uJ

                 0
                 0 160

                     3:   4  4.    S    ass bed

                         eMER smulSS d MSS 1/Ha2 b iat
                         4  4.10 Sao gross ba d
                         30  4.a97 Swa  grace bar d                              t
                        109 13.39  Corals/sand

                          MER iemultatd MSS 1/2 ratio

                       surface  irrodionci(PAR)- 1. 39-l.41xo10 7/cms.

                   10
                     400            o500              6o00             700
                                   Wavelength  (nm.)

    Figure 4.--Upwelling spectral irradiances taken just beneath the sea surface
      over a variety of coral reef environments and the western edge of the Gulf
      Stream. The Mer simulated MSS ratio is the ratio of Band 1/Band 2 of Landsat,
      calculated from measurements taken with the Mer-1015 Biospherical Instruments
      spectroradiometer and wavelength weighting functions as described in the text.

    Band 2 (red) = (.036x589nm + .927x625nm + .960x656nm + .90x671nm
                     + .810x694nm) / 3.633

         We then calculated the ratio of the bands (Band 1/Band 2) to allow for
    differences in absolute intensity between the ground and spacecraft signals.

                                              196

    Figure 4 shows the spectral signals that upwell from different types of reef
    habitats in relation to the blue waters of the nearshore Gulf Stream. Different
    habitats are clearly distinguishable. The calculated MSS ratios for each habitat
    are also different, suggesting that reefs and their associated habitats may be
    distinguishable and quantitatively studied using multispectral spacecraft imagery.

                                      CONCLUSIONS
         While our work is by no means complete, we are beginning to show that an
    understanding of the bio-optics of the system can contribute to our understanding
    of the dynamics of coral reef ecosystems. The techniques that I have described
    suggest that optical measurements can be used to estimate the input of light energy
    into benthic ecosystems at various depths and habitats. Such data are necessary
    tounderstand and compare the energetics of coral reef communities and the degree
    to which the process of primary production varies and influences the organization
    of the ecosystem. The studies described in this communication are parallel to
    laboratory and field investigations on marine phytoplankton. The techniques
    are nondestructive, which means that the same environment can be repeatedly
    sampled. The measurements can be made over a variety of temporal and spatial
    scales, providing the potential to investigate large areas of coral reef ecosys-
    tems. The results are encouraging and suggest that with more research into the
    optics of coral reefs we may be able to use the techniques of remote sensing to
    routinely delineate, monitor, and, perhaps, manage these coral reef ecosystems.

                                    ACKNOWLEDGMENTS

         This work could not have been completed without the collaboration of
    Charles R. Booth, Biospherical Instruments Inc., and Albert R. Hibbs, Jet
    Propulsion Laboratory. Edmund Woloszyn and John Halas helped complete the
    field work in the Florida Keys. Special thanks go to Captain Mark Glisson,
    Florida Department of Natural Resources, for logistical support at John Pennekamp
    Coral Reef State Park. This research was funded by the National Science
    Foundation (NSF OCE 76-81071), National Oceanic and Atmospheric Administration
    (NA 82-AAA-02880), and the College of Charleston. This is Contribution Number
    66 from the Grice Marine Biological Laboratory.

                                    LITERATURE CITED

    Abbott, M. R., P. J. Richerson, and T. M. Powell. 1982. "In-Situ Response of
       Phytoplankton Fluorescence to Rapid Variations in Light." Limnol. Oceanogr.
       27:218-225.

    Booth, C. R., and P. Dustan. 1979. "Diver-Operable Multiwavelength Radiometer."
       Proc. Soc. Photo-Optical Instrumentation Engineers 196:33-39.

    Dustan, P. 1982. "Depth-Dependent Photoadaptation by Zooxanthellae of the
       Reef Coral Montastrea annularis." Mar. Biol. 68:253-264.

    Gordon, H. R., D. K. Clarke, J. L. Mueller, and W. A. Hovis.  1981.  "Phytoplankton
       Pigments From the Nimbus-7 Coastal Zone Color Scanner: Comparisons With
       Surface Measurements." Science 210:63-66.

                                           197

    Gordon, H. R.  R. Zannifeld, and R. C. Smith.  1980.  "Introduction to Ocean
       Optics."   -oc. Soc. Photo-Optical Instrumentation Engineers 208:14-54.

    Harris, G. P. 1980. "The Relationship Between Chl a Flourescence, Diffuse
      Attenuation Changes, and Photosynthesis in NaturaT Phytoplankton Populations."
      J. Plankton Res. 2:109-127.

    Kiefer, D. A. 1973. "Chlorophyll a Fluorescence in Marine Centric Diatoms:
       Responses of Chloroplasts to Light and Nutrient Stress."  Mar. Biol. 23:39-46.

    Kiefer, D. A., and B. G. Mitchell. 1983. "A Simple, Steady State Description
       of Phytoplankton Growth Based on Absorption Cross Section and Quantum
       Efficiency."  Limnol. Oceanog.r. 28:770-775.

    Kiefer, D. A., R. J. Olson, and W. Wilson. 1979. "Reflectance Spectroscopy of
       Marine Phytoplankton. Part 1. Optical Properties Related to Age and Growth
       Rate."  Limnol. Oceanogr. 24:664-672.

    Laws, E. A., and T. T. Bannister. 1980. "Nutrient- and Light-Limited Growth
       of Thalasiosira fluviatilis in Continuous Culture, With Implications for
       Phytoplankton Growth in the Sea." Limnol. Oceanogr. 25:457-473.

    Morel, A. 1978. "Available, Useable, and Stored Radiant Energy in Relation to
       Marine Phytoplankton."  Deep Sea Res. 25:673-688.

    Muscatine, L., and J. W. Porter.  1977.  "Reef Corals:  Mutualistic Symbioses
       Adapted to Nutrient-Poor Environments." Bioscience 27:454-460.

    Rabinowich, E., and Govingee. 1969. Photosynthesis. John Wiley and Sons, New
       York. 273 pp.

    Smith, R. C., and K. S. Baker.  1978a.  "The Bio-Optical State of Ocean Waters
       a"d Remote Sensing." Limnol. Oceanogr. 23:247-259.

    Smith, R. C., and K. S. Baker. 1978b. "Optical Classification of Natural
       Waters." Limnol. Oceanogr. 23:26U-267.

    Stoddart, D. R., and R. E. Johannes. 1978. Coral Reefs: Research Methods.
       UNESCO, Page Bros. Pub., Norwich, U.K. 581 pp.

    Tyler, J. E., and R. W. PreisEndorfer.  1962.  "Transmission of Energy Within the
       Sea," pp. 397-451. M. N. Hill (ed.), The Sea, Vol. 1. Interscience Pub., N.Y.

    Vincent, W. F.  1979.  "Mechanisms of Rapid Photosynthetic Adaptation in Natural
       Phytoplankton Communities: 1. Redistribution of Excitation Energy Between
       Photosystems I and II." J. Phycol. 15:429-434.

    Wilson, W. H., and D. A. Kiefer.  1979.  "Reflectance Spectroscopy of Marine
       Phytoplankton.  Part 2.  A Simple Model of Ocean Color."  Limnol. Oceanogr.
       24:673-682.

                                           198

                  PRELIMINARY STUDIES OF DENITRIFICATION ON A CORAL REEF

                                   Sybil P. Seitzinger
                                           and
                                  Christopher F. D'Elia1
                            Division of Environmental Research
                       Academy of Natural Sciences of Philadelphia
                            Philadelphia, Pennsylvania 19103

                                         ABSTRACT

          This preliminary study presents evidence that coral reefs may be the sites
     of potentially high rates of denitrification. Qualitative evidence for the
     existence of denitrification in dead coral heads and in sediments from a sea
     grass community were obtained using the acetylene blockage technique and by
     measuring the rate of nitrate reduction occurring in sediment slurries incubated
     under anaerobic conditions. The degree to which this denitrification offsets
     nitrogen fixation is unknown and awaits quantification with better techniques,
     but from rough approximation it appears to be considerable.

                                        INTRODUCTION

    *      Many studies on coral reefs have shown that while standing stocks for N
     species are low, rates of transformations of N species are rapid (Szmant
     Froelich, 1983). Coral reefs typically exhibit high rates of nitrogen fixation
      (Wiebe, et al., 1975; Mague and Holm-Hansen, 1975; Bunt, et al., 1970; Capone
     and TaylorjT77), the process by which atmospheric N2 gas is chemically
     transformed into "combined" nitrogen forms (e.g., ammonia) that can be utilized
     as nutrients by autotrophs. Indeed, some of the highest rates of N2 fixation
     for any ecosystem have been reported for coral reef areas.  However, denitrifi-
     cation, the process by which combined nitrogen is chemically transformed back
     to atmospheric N2 gas, has received much less attention in reef environments.
     Denitrification represents a potential removal mechanism for combined N both on
     the reef and in lagoons behind reefs.  Recent reports of substantial rates of
     nitrification (ammonia oxidation to NO2 and NO3) on coral reefs (Webb and Wiebe,
      1975; LIMER Expedition, 1977) indicate that a potential exists for denitrifica-
     tion to occur.

           This paper presents preliminary measurements of denitrification on a coral
      reef in Abrahams Bay, Mayaguana, Bahamas, and from sediments behind the reef
      in a lagoon with Thalassia  beds.  We used techniques suitable for qualitative
      determination of denitrification under field conditions.  This work was carried
      out on the R/V MARSYS RESOLUTE with the cooperation and support of Dr. Walter
      Adey of the Marine Systems Laboratory of the Smithsonian Institution. Additional
      support also was provided by the Ruth Patrick Foundation at the Academy of
      Natural Sciences of Philadelphia.

           1Present address: Chesapeake Biological Laboratory, Solomons, Maryland
      20688.

                                              199

               0    1   2   3   4   5   6

    Figure 1.--Mayaguana (Abrahams Bay) Coral Reef and Lagoon. Depths in fathoms;
                              x indicates the study area.

                                 MATERIALS AND METHODS

         This study was conducted during May 1983 in Abrahams Bay, Mayaguana, located
    in the southern Bahamas (fig. 1).

         Dead coral heads, each with a displacement volume of about 250-300 cm3,
    were collected by SCUBA divers from several areas behind the reef crest. The
    heads which were covered with algae and organic matter were brought back to the
    ship's laboratory and placed in gas tight glass incubation chambers (Seitzinger,
    et al., 1980) which were then filled to within 1 cm of the top with reef water
    '50oml). Denitrification rates were measured using acetylene to inhibit N20
    reduction to N2 (Balderston, et al., 1976). The gas phase (60 ml) was flushed
    with acetylene, and the water-Tntf-te chambers was stirred with floating magnetic
    stir bars to equilibrate the gas and water phases. Samples (30 ml) of seawater
    were then withdrawn at time intervals into stoppered 50 ml serum bottles and 1
    ml of saturated KOH solution added to each. After 3 hr a concentrated NO3 solution
    was added to two of the chambers to make the seawater concentration 40 pM N03.
    Time-series samples for N20 continued to be taken at 7, 9, and 17 hr.  The N20
    concentration in the gas phase of the serum bottles was measured by ECD gas
    chromatography within 1 week (Seitzinger, et al., 1980). The total amount of
    N20 in the samples was calculated using WeTls and Price's (1980) N20 solubility
    equation for the appropriate temperature and salinity.  The production of N20
    in the presence of acetylene by the coral heads then was calculated based on
    the change in concentration between sequential samples and equated to the
    denitrification rate.

         The potential for denitrification in the sediments from the reef lagoon was
    examined using measurements of pore water N02 and N03 concentrations, N03
    reduction rate measurements, and measurements of N20 production in the presence
    and absence of acetylene. Sed-ment cores (47 cm2 x 25 cm deep) were collected

                                           200

        Table 1.--Rate of denitrification by diad coral heads as measured by N20
          production (nmol N 0 h- coral head- ) in the presence of acetylene,
          but without added N03, except as indicated. Acetylene was added at
          time = 0 hr.  *   after 3 hr a concentrated N03 solution was added to
         make seawater 40 pM N03.

    Dead Coral Head          Incubation Period            Rate of N20 Producition
                                                              nmol N20 h-

           1                   2.5 - 5.5 hr                         1.3

           2                     2 - 5 hr                           2.1

           3                     0 - 3 hr                           1.6

                               *3 - 7 hr                          57

                                7 - 9 hr                          38

                                9 - 17 hr                         16

           4                     0 - 3 hr                           0.8

                               *3 - 7 hr                          51

                                 7 - 9 hr                          16

                                 9 - 17 hr                         6

    by SCUBA divers from the Thalassia beds in the reef lagoon.  One core was
    sectioned at 2.5 cm intervals and the pore water N02 and N03 concentrations
    determined using a Technicon AutoAnalyzer.

         N0O reduction rates were measured in a second core sectioned at intervals
    of 0-5 cm, 10-15 cm, and 20-25 cm.  Sediment slurries from these depths were
    placed in serum bottles with 20 uM NOj seawater solution and the change in N02
    + NO3 concentration with time measured. The incubations were done in the dark
    at 29�C.

         Denitrification rates in the lagoon sediments were measured, again using
    acetylene inhibition of N20 reduction. Sediments from three cores were sectioned
    at intervals of 0-5 cm, 10-15 cm, and 20-25 cm. Sediment slurries (14 cm3)
    from those depths were incubated aerobically in serum bottles with 15 ml of 20
    UM NO3 seawater solution and 0.3 atmospheres of acetylene. N20 production
     rates in the presence of acetylene then were measured at each depth after
     intervals up to 15.5 hr by injecting 2 ml of a saturated KOH solution into the
     serum bottles after approximately 0, 6, and 15.5 hr.  The production of N20 in

                                             201

                                      Concentration, .M
                          0   1  2  3  4  5  6   7  8  9  10
                         0
                             a  *~ ~ ~ ~ ~   ~ ~~~~~~~ I  I  I  It

                         1-

                         2-

                         3-

                         4-

                         5-

                       E 6-

                         8-

                         9-

                         10-

                         12-

                         13-

                         14

    Figure 2.--Depth profile of pore water nitrite (circles) and NO2 + N03 (triangles)
                                 in sediments of lagoon.

    the absence of acetylene was measured in a parallel set ofsamples incubated
    with 20 pM NO3 but without acetylene. The reduction of NO3 also was measured
    in another parallel set of samples with acetylene and 20 uM NO3.  N02 + N03
    concentrations were measured immediately after approximately 0, 6, and 15.5 hr
    (KOH was not added).

                                         RESULTS

         When coral heads were incubated in seawater that was not enriched with
    nitrate, the rate of denitrification (N20 production in the presence of acetylene)
    was approximately 1-2 nmol N20 per coral head per hour (table 1).  When the N03
    concentration in the surrounding seawater was increased to 40 pM, the rate of
    N20 production increased to approximately 50 nmol per hour per coral head and
    then decreased during the subsequent 14 hr.

                                             202

                      18 -

                      16 -

                      14 -

                      124-

                      22 -
                 8~   8-

                        0        4        8        12       16       20
                      24                                                  BB

                      20

                      16-

                       4-

                        0        4        8        12       16       20
                                           Elapsed Time, hrs

    Figure 3.--(A)  N03 depletion in lagoon sediments spiked to 20 uM NO3; (B) N20
      production by lagoon sediments incubated with a 20 pM N03 solution and in the
      presence of acetylene. Open circles = 0-5 cm depth; triangles = 10-15 cm
      depth; and closed circles = 20-25 cm depth.

         The concentrations of N02 + NO  in the sediments of the Thalassia bed were
    higher than the overlying seawater (0.5 4M NOj + NO3), ranging from 3.5 to 9 PM
    with a peak concentration at about 11 cm depth (fig. 2).

         When sediments were incubated in seawater enriched to a concentration of 20
    UM NO3, N03 concentrations decreased rapidly in sediments from all depths to
    below concentrations found in the pore waters (fig. 3A). Since this experiment

                                             203

    Table 2.--Rate of denitrification as measured by N20 production in lagoon
      sediments incubated with 0.3 atm acetylene and 20 OM NO3.  Rates are expressed
      per cm3 of sediment per hour.

      Depth Interval               Time Interval               N20 Producton
                  ~~(cm)               t~(hr)               (nmol N20 cm- h1)

            0- 5                        0- 7                      1.9 x 10--

                                      7 - 15.5                -0.3 x 10-1

           10 - 15                      0 - 6                     1.2 x 10-1

                                      6 - 15.5                -0.1 x 10-1

           20 - 25                      0 - 5.5                  2.8 x 10-1

                                    5.5 - 15.5               -0.02 x 10-1

    was performed in the presence of acetylene, no new nitrification was occurring,
    inasmuch as acetylene also blocks nitrification_(Bremner and Blackmer, 1979).
    During that same period of rapid decrease in NO3 concentration (0-6 hr), there
    was a rapid increase in N20 concentration in samples incubated with acetylene
    (fig. 3B).  The highest rates of N20 production during the first 6 hr was seen
    in the 20-25 cm depth interval (table 2). The concentration of N20 tended to
    decrease during the next 16 hr interval. The rate of NO3 reduction increased
    with increasing concentration of substrate (fig. 4).

         Concentrations of N20 in sediments incubated with NOT but without acetylene
    were negligible and tended to decrease slightly with time (not shown). Changes
    were small compared to changes measured in the presence of acetylene.

                                       DISCUSSION

         The preliminary measurements of denitrification reported here indicate that
    coral reefs and associated lagoon sediments are potentially active sites for
    denitrification. Nitrate concentrations inside dead coral heads have been
    reported by Webb and Wiebe (1975) and Risk and Muller (1983) to be higher than
    the surrounding seawater; this undoubtedly indicates that nitrification is
    occurring in dead coral heads. Low oxygen concentrations occur as organic
    matter decays in coral heads, thus providing the proper conditions for
    denitrification (Risk and Muller, 1983). Although nitrification and denitrification
    require different concentrations of oxygen to proceed, both can occur simultaneously
    in coral heads due to microdistributional variations in oxygen concentration
    that certainly must occur (Risk and Muller, 1983).

         Sediments in the lagoon behind the reef also appear to be active areas for
    denitrification as well.  This was demonstrated by both the N20 production

                                            204

                  60

                  5.0-

              c o
             a: 4.0
              2?
                 3.0-
              ccE

                 2.0-
                   Z~~~~~
                   1.0-

                    0       2A                            10 8l   12

             Figure 4.--Rate'of  NO reduction (nmo  N- 3 h-1) vs concentrateion ofM

         ~Figure 4.--Rate of NO   edcton(no3            h) vs. concentration of
                            NO3 (>M) in sediment experiment.

    rates measured in the presence of acetylene and the NO3 reduction rates. The
    source of N03 for denitrification must come from nitrification in the sediments
    as opposed to diffusion of N03 from the overlying water, since the N03 concentrations
    in the pore waters were much greater than in the overlying water. The N03
    concentrations we measured in the pore waters must be maintained by relatively
    high rates of nitrification. Two lines of evidence support this: (1) NO3 concen-
    trations were shown to decrease rapidly below concentrations measured in the
    pore waters when nitrification was inhibited by acetylene, and (2) denitrifi-
    cation rates were indicated to be high in the sediments and thus, to maintain
    NO3 concentrations in the pore waters with active denitrification occurring,
    nitrification must also be rapid.

         The rates of decrease of NO3 we observed in lagoon sediments were much
    greater than the rates of N20 production. One would expect them to be equal if
    all of the NO3 decrease was due to denitrification (see Taylor, 1983, for a
    review of the problems associated with these measurements). We can presently
    only speculate as to why the discrepancies occurred (figs. 3A and 3B). For
    example, acetylene blockage may not be complete or may not yield stoichiometric
    quantities of N20. Alternatively, NO3 could be reduced assimilatively, e.g.,
    by foraminiferans (Webb and Wiebe, 1978).

         We emphasize that the results presented here are preliminary for several
    reasons. First, we did only a limited number of experimental measurements and
    feel that a more detailed study is needed. Second, the techniques we used to
    measure denitrification are adequate for a preliminary survey in the field like
    this one but should be supplemented by the preferred, direct measurement of
    denitrification (Seitzinger, et al., 1980).  We consider the use of sediment

                                             205

    slurries that are enriched with nitrate and incubated under anaerobic conditions
    (Billen, 1978; Koike and Hattori, 1978, 1979; Oren and Blackburn, 1979; Iizumi,
    et al., 1980) to be good qualitative but not necessarily good quantitative
    tools--such experimental conditions destroy sediment microenvironmental structure
    (e.g., nitrate, oxygen, and organic matter concentrations) that cannot be
    simulated exactly in the laboratory. This is particularly problematic in the
    Thalassia bed sediments with their complex root structure.  The use of the
    acetylene blockage technique also incurs problems.  For example, acetylene blockage
    of N20 reduction may be inhibited by the presence of sulfide (Tam and Knowles,
    1979), and acetylene itself may be oxidized anaerobically (Culbertson, et al.,
    1981) or may inhibit nitrification (Bremner and Blackmer, 1979; Blackmer, et
    al., 1980), methanogenesis (Oremland and Taylor, 1975), methane oxidation
    (deBont and Mulder, 1976), and the growth of sulfate-respiring bacteria (Payne
    and Grant, 1982). Considering these limitations, it is likely that the
    denitrification rates reported here are underestimates of the field rates.

         The amount of fixed N being lost through denitrification in the lagoon
    behind the coral reef conceivably could be as high as that fixed by N2 fixation
    on the reef itself.  No measurements of N2 fixation are available for Mayaguana.
    However, measurements ofN2 fixation have been made on a number of other ~oral
    reefs.  Maximum rates found at Enewetak, for example, were 600 4mol N2 m   h'
    during daylight (Wiebe, et al., 1975; Webb, et al., 1975).  For an average rate
    over 24 hr, this rate should be decreased by approximately 50% to 300 ,mol m-2
    h-1, since such high rates only occur during daylight.  The above methodological
    limitations aside, we can make a rough approximation of denitrification in the
    lagoon.  The results from the acetylene inhibition experiments indicated that
    denitrification rates were approximately 0.2 nmol cm-  h-1 throughout the top
    25 cm of lagoon sediment. The integrated value for the top 25 cm is then
    50 umol m-2 h-1.  The area of the lagoon is estimated to be 10 times the area
    of the reef.  Therefore, in the reef-lagoon ecosystem, denitrification in the
    lagoon would more than balance the N2 fixation on the reef.  While these measure-
    ments and calculations are only preliminary, they do point to the probable
    importance of denitrification in reef ecosystems and to the need for further
    measurements.

                                    ACKNOWLEDGMENTS

         We thank Walter Adey and the crew of the R/V MARSYS RESOLUTE for giving us
    the opportunity to make these measurements. We also thank S. V. Smith and K.
    L. Webb for their critical comments and L. Woodbury, D. Engle, and G. Canaday
    for technical help.

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