Allelopathy and Spatial Competition Among Coral Reef Invertebrates (Species Interactions/Community Structure) J
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Proc. Nat. Acad. Sci. USA Vol. 72, No. 12, pp. 5160-5163, December 1975 Zoology Allelopathy and spatial competition among coral reef invertebrates (species interactions/community structure) J. B. C. JACKSON AND LEO Buss Department of Earth and Planetary Sciences, The Johns Hopkins University, Baltimore, Maryland 21218; and Discovery Bay Marine Laboratory, Box 35, Discovery Bay, Jamaica, West Indies Communicated by Hans P. Eugster, August 5,1975 ABSTRACT Species of ectoprocts and solitary encrusting METHODS animals were subjected in aquaria to homogenates of 11 sympatric species of sponges and colonial ascidians. Five of The Natural System. The undersurfaces of foliaceous reef the nine sponge species and one of the two ascidian species corals (e.g., Agaricia and Montastrea spp.) support a highly exhibited species-specific allelochemical effects. Evidence diverse encrusting fauna of sponges, ectoprocts, colonial as- suggests that allelochemical interactions provide a wide- cidians, serpulids, brachiopods, and bivalves (5). Free space spread, specific, and complex mechanism for interference is almost entirely lacking (maximum 1-5%) and competition competition for space among natural populations of coral reef organisms. The existence of such species-specific mecha- for space is intense. Predators or signs of predation (tooth nisms may provide a basis for maintenance of diversity in marks, drill holes, bare zooids, etc.) and physical distur- space-limited systems in the absence of high levels of preda- bances are rare in cryptic environments. Sponges, some ecto- tion and physical disturbance. procts, and colonial ascidians are the important competitors, occupying the largest proportion of the available substrate Space on which to live is often the most important limiting (J. B. C. Jackson, unpublished data). resource in marine hard-substrate environments. Mainte- Experimental Procedures. Colonies of foliaceous corals nance of a given level of diversity in these environments has were collected during January 1975 from depths of -15 to been attributed to the interacting roles of competition, -60 m at Discovery Bay and Rio Bueno along the north predation, and disturbance (1, 2). Evidence from manipula- coast of Jamaica, West Indies. The morphology and zonation tive experiments on the rocky intertidal shore reveals a situa- of these reefs has been described in detail (22-25). All exper- tion where, in the absence of predation and disturbance, a imental animals except serpulids were obtained from these single competitive dominant monopolizes all available space corals. Serpulids were collected from Transite (asbestos-ce- (1-3). In this system preservation of high diversity requires ment) panels placed at -40 m on the Discovery Bay reef 6 the presence of either a predator or a disturbance agent. Yet, months previously. Small pieces of corals or Transite sub- in some systems predation and disturbance effects appear strate supporting potential victims were broken off, cleaned unimportant [e.g., cryptic coral reef communities (4, 5)]. of all surrounding organisms with a scalpel and toothbrush, Here, though no clear competitive dominant exists, high di- examined for possible damage, and maintained in running versity is, nonetheless, maintained. Interpretation of the seawater aquaria for 1-2 days before use. manner in which high diversity is preserved in situations of Homogenates were prepared of sponges and colonial asci- low disturbance rates is of fundamental significance and re- dians suspected of possessing allelochemicals. Depending on quires an understanding of the various competitive mecha- the growth form of the potential aggressor, volumes of tissue nisms utilized by space-limited organisms. ranging from 2.5 to 20 ml were scraped from the coral un- Sessile marine organisms exhibit numerous mechanisms dersurfaces with a scalpel, ground with a mortar and pestle, important in interference competition for space. These in- homogenized in 0.45 ,um Millipore-filtered seawater in a clude structures and growth patterns that lower or hinder glass homogenizer, and diluted to 100 ml. Homogenates overgrowth, low susceptibility to epizooic recruitment were used immediately or stored under refrigeration for up ("fouling"), aggressive behavior (e.g., coral feeding re- to 2 days. Homogenates stored under refrigeration displayed sponses), escape in size, and differential susceptibility to dis- the same allelochemical effects as homogenates of the same turbance. Terrestrial plants exhibit many parallel mecha- species used immediately after preparation. nisms for space competition (6-12). One potentially impor- At the start of the experiments single colonies or individu- tant mechanism of plants is the use of allelochemicals (6, 13, als of potential victim species were placed upright in aerat- 14) which may also function to reduce herbivory (13-15). ed, one liter polyethylene aquaria. Depending on the quan- Although animal toxins apparently serve in defense against tity available, sponge or ascidian volumes of 2-5 ml were predation (13, 16-18), their possible importance in competi- added to the aquaria and the animals were observed at daily tion has received little attention (19-21). The suggested intervals for 5-8 days. Similar volumes of filtered seawater plant parallel, in addition to known antipredatory toxic were added to the controls. properties of sponges (16, 17), and our observation that ecto- Nine species of sponges and two of colonial ascidians were proct colonies being overgrown by sponges may exhibit a tested for possible toxic effects on three species of ectoprocts, band of dead zooids a few millimeters wide paralleling the two as yet unidentified serpulids, the brachiopod Argyrothe- growing edge of the sponge suggested to us that allelochemi- ca johnsoni, and the bivalve Basilomya goreaui (Table 1). cal interactions are important in spatial competition on coral Identifications of many of the sponges and colonial ascidians reefs. Here we (1) present field observations and prelimi- are tentative and await further work by specialists. Some of nary experiments suggesting that allelochemicals may serve the sponges are probably undescribed. Sponge 1 possesses as an important, specific mechanism in interference compe- abundant large strongyles and tiny raphids and sponge 2 tition for space among coral reef animals and (2) propose a very few spicules and abundant unicellular algae (? endo- model for maintaining diversity in space-limited systems in symbionts). Specimens of each species tested were deposited the absence of high levels of predation and disturbance. at the Yale Peabody Museum. Five replicate colonies or in- 5160 Downloaded by guest on September 25, 2021 Zoology: Jackson and Buss Proc. Nat. Acad. Sci. USA 72 (1975) 5161 Table 1. Results from addition of sponge and colonial ascidian homogenates to aquaria containing ectoprocts and solitary invertebrates Species exposed to homogenates Ectoprocts Solitary animals Stylo- Stegano- Stylopoma poma Repta- Argyro- porella spongites spongites deonella theca Basilomya magnilibris (Pallas) (Pallas) violacea Serpulid Serpulid johnsoni goreaui Homogenates (Busk) type 1 type 2 (Johnston) 1 2 (Cooper) (Bayer) Sponges Mycale laeuis (Carter) D' NTE - NTE NTE NTE NTE ?Tenaciella sp. NTE NTE NTE NTE NTE NTE ?Toxemna sp. NTE D - NTE NTE NTE NTE ?Halisarca sp. NTE NTE - NTE NTE NTE Sponge 1 NTE NTE - NTE NTE NTE NTE Plakortis ?sp. Dl? NTE DI - Sponge 2 NTE NTE - Agelas ?sceptrum (Lamarck) MF NTE Ectyoplasia ferox (Duchassaing and Michelotti) NTE D D D- Colonial ascidians Didemnum sp. NTE NTE NTE NTE NTE Ascidian 2 MF D - NTE NTE NTE No. species tested 11 11 1 3 7 7 7 3 No. species showing toxic effect 4 3 1 2 0 0 0 0 NTE, no apparent toxic effect; normal movement and feeding of ectoproct zooids; MF, no movement or feeding; ectoproct zooids intact; D, ectoproct colonies dead; zooids deteriorating; D', brown body formation in deteriorating zooids;,-, no experiment run. Results were the same for all five replicates. dividuals of potential victim species were used for each cals in nature. For example, toxins might be stored within sponge or ascidian species and for controls. the organisms and not released into the surrounding water. Solitary animals were observed macroscopically for signs Bare zones might result from predation by small inverte- of allelochemical effects. Both controls and animals of these brates living within sponges, although these appear to be species subjected to homogenates usually remained closed quite rare on thin, encrusting species [e.g., for terrestrial within their valves or tubes but all species exhibited sporadic plants (26, 27)]. However, the results do demonstrate the po- degrees of opening and feeding. Ectoproct colonies were ob- tential significance of allelochemicals in competition for served under a dissecting microscope for periods up to 10 space between ectoprocts, sponges, and ascidians. Of course, min for movement of opercula, lophophores, and avicularia sponge or ascidian allelochemical substances may act in and for ciliary feeding. Ten minutes was always adequate to more subtle ways than direct mortality, perhaps by inhibi- observe movement and feeding by controls. tion of feeding as observed for Steganoporella magnilibris subject to homogenates of Agelas ?sceptrum and the un- identified ascidian, or by inhibition of growth and reproduc- RESULTS tion. Further support for such effects comes from the re- Results are summarized in Table 1. Five of the nine sponge