Allelopathy and Spatial Competition Among Coral Reef Invertebrates (Species Interactions/Community Structure) J

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proportion of the available substrate Space on which to live is often the most important limiting (J. B. C. Jackson, unpublished data).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 ported inhibition of ciliary movement and developmental species and one of the two colonial ascidian species tested processes in sea urchins by numerous Jamaican sponge displayed some allelochemical effects. All ectoproct species species (18). The potential inhibition of ectoproct growth, tested suffered some mortality. In cases of adverse effects, reproduction, and recruitment by adjacent living sponges in mortality or cessation of movement and feeding occurred situ remains to be investigated. for all replicates. Controls suffered no mortality or apparent Field observations provide strong circumstantial evidence abnormal behavior. Allelochemical effects appear quite spe- that sponge allelochemical interactions may be important in cific among ectoprocts, as no sponge or ascidian caused mor- spatial competition with groups other than ectoprocts. In tality or cessation of feeding in all ectoproct species tested. open reef environments scleractinian corals may occupy Solitary animals suffered no apparent effects. At the end of most of the available hard substrate of Jamaican reefs, espe- the experiments, living serpulids swam away when their cially on the fore-reef slope where foliaceous corals predom- tubes were chipped away at the origin and living brachio- inate (refs. 22, 23, and Fig. 3 in ref. 28). However, massive pods and bivalves resisted prying open and then rapidly sponges are also common in this environment, attaining per- closed their valves. haps their greatest biomass/unit surface area of anywhere on the reefs (29). Preliminary qualitative observations of The evidence for allelopathy coral-sponge interactions on the fore-reef slope revealed Mortality of ectoprocts subjected to whole-organism homog- that sponges overgrow corals much more commonly than enates and the presence of bare zones around sponges do not the reverse. Rare observations on the overgrowth of sponges establish the importance of sponge or ascidian allelochemi- by corals revealed no signs of damage to sponge tissues adja- Downloaded by guest on September 25, 2021 5162 Zoology: Jackson and Buss Proc. Nat. Acad. Sci. USA 72 (1975)

.~~~-A A

FIG. 1. Interactions between colony of the coral Montastrea cavernosa and three chimneys of the excavating sponge Siphonodictyon co- ralliphagum Ritzler. Note the bare zone (B) of dead coral skeleton and mucous strands between the lowermost sponge and the surrounding coral and the lag in growth (C) of the coral growing edge (A) and resulting wide bare zone around the sponge on the left. Sponges about 10-15 cm diameter, depth -30 m.

cent to overgrowing corals. The reverse was true in many strate and decreases the probability of overgrowth by adja- cases, but clear examples of bare zones of dead coral skele- cent organisms. Stylopoma also exhibits raised colony bor- ton adjacent to sponges were commonly observed (Fig. 1). In ders which inhibit overgrowth by other organisms and/or al- such cases, an area of dead coral as wide as 1-3 cm parallels lows overgrowth by Stylopoma. Stylopoma and Steganopo- the advancing or stationary edge of the sponge. The exis- rella are thus potentially important space competitors tence of these bare zones provides strong circumstantial evi- against the normally dominant encrusting sponges in cryptic dence for the presence of allelochemical mechanisms for reef environments. The possible use of allelochemicals space competition by massive reef sponges. Secretion of mu- against these ectoprocts could be an important mechanism cous by many such sponges, as by Siphonodictyon (30), may in preventing their dominance of the cryptic reef habitat. provide a mechanism for concentration of allelochemicals in The specific effects of the homogenates probably reflect the the immediate vicinity of the sponges without excessive inability of certain sponges and ascidians to physically over- dilution by currents. Although the importance of alleloche- grow one or the other of these species. mical interactions among reef animals in nature is as yet un- Second, the same arguments may explain the apparent proven, allelopathy appears to be a widespread, complex absence of toxic effects upon any of the solitary animals test- and quite specific mechanism for spatial competition among ed. Colonial animals in the cryptic reef habitat commonly these organisms. overgrow the unprotected calcareous tubes and shells of ser- pulids, bivalves, and some brachiopods. Initially these soli- Allelopathy and competition tary animals survive such overgrowth of their skeleton by To emphasize the potential importance of allelopathy in spa- maintaining open space at their feeding apertures. Eventu- tial competition, we discuss here two cases of how possession ally even their apertures are often overgrown. Evidence for of allelochemicals may relate to competitive mechanisms this pattern comes from the common observation that soli- displayed by the organisms tested. First, animals used in the tary animals at the center (oldest and often thickest portion) experiments comprise many of the most abundant (by num- of colonies of sponges, colonial ascidians, and ectoprocts are ber of individuals and/or space occupied) species in the nat- completely overgrown more frequently than solitary ani- ural cryptic reef environment. Stylopona spongites and mals at colony peripheries. With regard to competition for Steganoporella magniibris are the most successful ecto- space, however, the area occupied by solitary animal feed- procts in the under-coral habitat, occasionally occupying al- ing apertures is always much less than 0.1% of the total most the entire undersurfaces of foliaceous corals. Both space available. Thus it is not surprising that no toxic effects species were observed to overgrow thin encrusting sponges, were noted between sponges, ascidians, and solitary animals, although not as frequently as they themselves are over- for there seems to be little selective advantage for evolution grown. They also exhibit growth patterns that aid in their of specific allelochemicals for elimination of such trivial resistance to overgrowth. Among Steganoporella colonies, space occupiers. peripheral zooids are occasionally raised away from the sub- stratum, allowing the colony to grow over adjacent organ- Diversity and competition isms. Stylopoma commonly exhibits frontal budding which Experimental studies on the rocky intertidal shore have raises the feeding surface of the colony away from the sub- demonstrated that, in the absence of disturbance, substrates Downloaded by guest on September 25, 2021 Zoology: Jackson and Buss Proc. Nat. Acad. Sci. USA 72 (1975) 5163

become dominated by one species (1-3). Higher diversity re- sions with N. Knowlton, B. A. and J. L. Menge, S. M. Stanley, and S. sults from the introduction of a disturbance, either in;the A. Woodin. Research support came from the National Science Institutes of form of predation or physical processes, which makes free Foundation (DES72-01559 A01) and the National Health (3505-RR07041-0851). To all we are grateful. space available for inferior competitors (1, 2). This model for maintenance of a given level of diversity is dependent on 1. Dayton, P. K. (1971) Ecol. Monogr. 41,351-389. a ranked hierarchy of competitive ability (Species A > 2. Paine, R. T. (1974) Oecologia 15,93-120. Species B > Species C > Species D) coupled with the maxi- 3. Connell, J. H. (1961) Ecology 42,710-723. mum effects of disturbance operating upon the competitive 4. Hartman, W. B. & Goreau, T. F. (1970) Symp. Zool. Soc. Lon- dominant (Species A). don 25,205-243. In some systems, for example, the cryptic coral reef com- 5. Jackson, J. B. C., Goreau, T. F. & Hartman, W. D. (1971) munity discussed here, no obvious disturbance agent, either Science 173, 623-235. 1-24. in the form of predation or physical processes, is apparent, 6. Baker, H. G. (1974) Annu. Rev. Ecol. Syst. 5, 7. Harper, J. L. (1961) Symp. Soc. Exp. Biol. 15, 1-39. a 300 encrusting animal yet high diversity (more than 8. Horn, H. S. (1971) The Adaptive Geometry of Trees (Prince- species) is maintained. We suggest an alternative but com- ton Univ. Press, Princeton, N.J.). plementary model for maintenance of diversity in space- 9. Patwain, P. D. & Harper, J. L. (1970) J. Ecol. 58,251-264. limited systems in the absence of high levels of predation or 10. Ross, M. A. & Harper, J. L. (1972) J. Ecol. 60,77-88. physical disturbance. The model requires that overall com- 11. Tripathi, R. S. & Harper, J. L. (1973) J. Ecol. 61, 353-368. petitive ability of space-occupying organisms does not follow 12. White, J. & Harper, J. L. (1970) J. Ecol. 58, 467-485. a simple linear ranked hierarchy. We propose that such sys- 13. Whittaker, R. H. & Feeny, P. P. (1971) Science 171, 757-770. tems may be structured by competitive networks (Species A 14. Levin, D. A. (1971) Am. Nat. 105, 157-182. > Species B > Species C > Species D, but Species D wins 15. Freeland, W. J. & Janzen, D. H. (1974) Am. Natur. 108, 269-289. over Species A or Species B) as opposed to competitive 16. Bakus, G. J. (1973) The Biology and Geology of Coral Reefs hierarchies. For example, the ?Tenaciella sp. might over- 2, eds. Jones, 0. A. & Endean, R. (Academic Press, New grow the ?Toxemna sp. in all interactions. ?Toxemna is York), pp. 326-368. toxic to Stylopoma spongites. But, if Stylopoma could over- 17. Bakus, G. J. & Green, G. (1974) Science 185, 951-953. grow ?Tenaciella, no species would immediately appear the 18. Burkholder, P. R. (1973) The Biology and Geology of Coral clear dominant in this 3-species system. Each of these inter- Reefs 2, eds. Jones, 0. A. & Endean, R. (Academic Press, New actions has been observed in cryptic reef environments but York), pp. 117-182. we do not yet know if they are of general occurrence. There 19. Goodbody, I. (1961) Nature 190,282-283. is also evidence of such a situation for scleractinian corals 20. Chiba, Y. & Kat6, M. (1966) Sci. Rep. Tbhoku Univ. Ser. 4 32, and sponges. The more species and the more numerous and 201-206. 21. Cameron, A. M. (1974) Proc. 2nd Int. Symp. Coral Reefs 1, the competitive networks of any such system, the complex 513-518. slower will space tend to be occupied by a single competitive 22. Lang, J. (1974) Am. Sci. 62,272-281. dominant, and the less the amount of external disturbance 23. Goreau, T. F. & Goreau, N. I. (1973) Bull. Mar. Sci. 23, 399- necessary to maintain a given level of diversity within the 464. system. Such a situation is made more likely, or perhaps in- 24. Goreau, T. F. & Land, L. (1974) Soc. Econ. Paleontol. Miner- evitable, by the existence among a group of organisms of al. Spec. Publ. many competitive mechanisms, especially allelochemical. 25. Kinzie, R. A., III (1973) Bull. Mar. Sci. 23,93-115. 26. Bartholomew, B. (1970) Science 170, 1210-1212. C. Arneson, P. L. Colin, P. Gilman, M. J. Lindley, and B. D. Kel- 27. Christensen, N. L. & Muller, C. H. (1975) Am. Midl. Nat. 93, ler assisted in the collection and preparation of animals and setting 71-78. up of the experiments. A. H. Cheetham identified the ectoprocts 28. Barnes, D. J. (1973) Bull. Mar. Sci. 23,280-298. and W. D. Hartman identified the sponges. C. Arneson provided 29. Reiswig, H. M. (1973) Bull. Mar. Sci. 23, 191-226. the photograph. Development of this paper benefitted from discus- 30. Rfitzler, K. (1971) Smithson. Contrib. Zool. 77, 1-37. Downloaded by guest on September 25, 2021