Skip to main content
SpringerLink
Log in

Plant defense associations in the marine environment

  • Published:
Coral Reefs Aims and scope Submit manuscript

Abstract

In contrast to terrestrial systems, few positive plant-plant associations have been recorded in tropical reef environments. This study, conducted at Carrie Bow Cay, Belize during 28 March–10 April 1984, provides the first documentation of herbivore escapes for natural combinations of palatable and unpalatable marine plants. For example, there was a highly significant association of several macrophyte taxa (Laurencia poitei, Dictyota spp., Amphiroa fragilissima, Cladophoropsis macromeres, Galaxaura cylindrica, rhodophycean turf) within a 2.0-cm radius of the herbivore-resistant brown alga Stypopodium zonale. Almost twice as many taxa occurred within 10 cm of S. zonale as within 10 cm of an equal number of random Stypopodium-free points, and there were no algal species negatively associated with S. zonale. The association of A. tribulus, L. poitei, Digenia simplex, rhodophycean turf, and Jania adherens with S. zonale provided them a fourfold greater survivorship per 48 h in the presence of grazing activity by fishes (mainly Acanthuridae and Scaridae). Reduced herbivory by fishes on macroalgae associated with S. zonale was not solely a consequence of its structural aspect. Losses of the palatable alga Acanthophora spicifera were significantly greater for thalli spatially remote (30 and 60 cm) from either a real or simulated Stypopodium; however, losses of A. spicifera adjacent to actual Stypopodium plants were significantly less than the losses next to models. The inter-relationships studied here, where an abundant and well-defended plant provides a significant refuge habitat for at least five relatively edible macroalgae, clearly facilitates the survival of certain taxa in the reef system and concomitantly enhances the within habitat diversity. Our findings also suggest an interaction counter to the process of competitive exclusion, since the single predominant plant has a positive rather than negative net effect on the abundances of other species that utilize the same general resources (e.g., light, space, nutrients).

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Adey WH, Vassar JM (1975) Colonization, succession and growth rates of tropical crustose coralline algae (Rhodophyta, Cryptonemiales). Phycologia 14:55–69

    Google Scholar 

  • Atsatt PR, O'Dowd DJ (1976) Plant defense guilds. Science 193:24–29

    Google Scholar 

  • Bakus GJ (1969) Energetics and feeding in shallow marine waters. Int Rev Gen Exp Zool 4:275–369

    Google Scholar 

  • Black R (1976) The effects of grazing by the limpet, Acmaea insessa, on the kelp, Egregia laevigata, in the intertidal zone. Ecology 57:265–277

    Google Scholar 

  • Borowitzka MA (1981) Algae and grazing in coral reef ecosystems. Endeavour 5:99–106

    Google Scholar 

  • Brawley SH, Adey WH (1977) Territorial behavior of threespot damselfish (Eupomacentrus planifrons) increases reef algal biomass and productivity. Environ Biol Fishes 2:45–51

    Google Scholar 

  • Brawley SH, Adey WH (1981) The effect of micrograzers on algal community structure in a coral reef microcosm. Mar Biol 61:167–177

    Google Scholar 

  • Brock RE (1979) An experimental study on the effects of grazing by parotfishes and role of refuges in benthic community structure. Mar Biol 51:381–388

    Google Scholar 

  • Carpenter RC (1985) Sea urchin mass-mortality: effects on reef algal abundance, species composition, and metabolism and other coral reef herbivores. Proc 5th Int Coral Reef Symp 2:66

    Google Scholar 

  • Choat JH (1982) Fish feeding and the structure of benthic communities in temperate waters. Annu Rev Ecol Syst 13:423–449

    Google Scholar 

  • Coley PD (1983) Herbivory and defensive characteristics of tree species in a lowland tropical forest. Ecol Monogr 53:209–233

    Google Scholar 

  • Connell JH, Slatyer RO (1977) Mechanisms of succession in natural communities and their role in community stability and organization. Am Nat 111:1119–1144

    Google Scholar 

  • Dahl AL (1972) Ecology and community structure of some tropical reef algae in Samoa. In: Nisizawa K (ed) Proceedings of the 7th International Seaweed Symposium. University of Tokyo Press, Tokyo, pp 36–39

    Google Scholar 

  • Dethier MN, Duggins DO (1984) An “indirect commensalism” between marine herbivores and the importance of competitive hierarchies. Am Nat 124:205–219

    Google Scholar 

  • Denno RF, McClure MS (eds) (1983) Variable plants and herbivores in natural and managed systems. Academic, New York

    Google Scholar 

  • Duggins DO (1980) Kelp beds and sea otters: an experimental approach. Ecology 61:447–453

    Google Scholar 

  • Earle SA (1972) The influence of herbivores on the marine plants of Great Lameshur Bay. Los Angeles County Nat Hist Mus Sci Bull 14:17–44

    Google Scholar 

  • Fenical W (1980) Distributional and taxonomic features of toxin-producing marine algae. In: Abbott IA, Foster MS, Eklund LF (eds) Pacific seaweed aquaculture. California Sea Grant College Program, Institute of Marine Resources, University of California, La Jolla, Calif, pp 144–151

    Google Scholar 

  • Fox LR (1981) Defense and dynamics in plant-herbivore systems. Am Zool 21:853–864

    Google Scholar 

  • Futuyma DJ (1983) Evolutionary interactions among herbivorous insects and plants. In: Futuyma DJ, Slatkin M (eds) Coevolution. Sinauer, Sunderland, Mass, pp 207–231

    Google Scholar 

  • Gaines SD (1985) Herbivory and between-habitat diversity: the differential effectiveness of defenses in a marine plant. Ecology 66:473–485

    Google Scholar 

  • Gaines SD, Lubchenco J (1982) A unified approach to marine plant-herbivore interactions. II. Biogeography. Annu Rev Ecol Syst 13:111–138

    Google Scholar 

  • Gallagher ED, Jumars PA, Trueblood DD (1983) Facilitation of soft-bottom benthic succession by tube builders. Ecology 64:1200–1216

    Google Scholar 

  • Geiselman JA, McConnell OJ (1981) Polyphenols in brown algae Fucus vesiculosus and Ascophyllum nodosum: chemical defenses against the marine herbivorous snail, Littorina littorea. J Chem Ecol 7:1115–1133

    Google Scholar 

  • Gerwick WH (1981) The natural products chemistry of the Dictyotaceae. PhD dissertation, University of California, San Diego, Calif

  • Gerwick WH, Fenical W (1981) Ichthyotoxic and cytotoxic metabolites of the brown alga, Stypopodium zonale. J Org Chem 46:22–27

    Google Scholar 

  • Gerwick WH, Fenical W, Fritsch N, Clardy J (1979) Stypotriol and stypoldione; ichthyotoxins of mixed biogenesis from the marine alga Stypopodium zonale. Tetrahedron Lett 1979:145–148

    Google Scholar 

  • Harper JL, Clatworthy JN, McNaughton IH, Sagar GR (1961) The evolution and ecology of closely related species living in the same area. Evolution 15:209–227

    Google Scholar 

  • Harris LG, Ebeling AW, Laur DR, Rowley RJ (1984) Community recovery after storm damage: a case of facilitation in primary succession. Science 224:1336–1338

    Google Scholar 

  • Hay ME (1981a) Spatial patterns of grazing intensity on a Caribbean barrier reef: herbivory and algal distribution. Aqua Bot 11:97–109

    Google Scholar 

  • Hay ME (1981b) Herbivory, algal distribution, and the maintenance of between-habitat diversity on a tropical fringing reef. Am Nat 118:520–540

    Google Scholar 

  • Hay ME (1981a) Patterns of fish and urchin grazing on Caribbean barrier reefs: are previous results typical? Ecology 65:446–454

    Google Scholar 

  • Hay ME (1984b) Predictable spatial escapes from herbivory: how do these affect the evolution of herbivore resistance in tropical marine communities? Oecologia 64:396–407

    Google Scholar 

  • Hay ME (1985) Spatial patterns of herbivore impact and their importance in maintaining algal species richness. Proc 5th Int Coral Reef Symp 4:29–34

    Google Scholar 

  • Hay ME, Taylor PR (1985) Competition between herbivorous fishes and urchins on Caribbean reefs. Oecologia 65:591–598

    Google Scholar 

  • Hay ME, Colburn T, Downing D (1983) Spatial and temporal patterns in herbivory on a Caribbean fringing reef: the effects on plant distribution. Oecologia 58:299–308

    Google Scholar 

  • Hedin PA (ed) (1983) Plant resistance to insects. American Chemical Society Symposium Series 208, American Chemical Society, Washington, DC

  • Hixon MA, Brostoff WN (1982) Differential fish grazing and benthic community structure on Hawaiian reefs In: Cailliet GM, Simenstad CA (eds) Fish food habit studies. Proceedings of the 3rd Pacific Workshop. Washington Sea Grant Program, University of Washington, Seattle, Wash, pp 249–257

    Google Scholar 

  • Inouye DW (1982) The consequences of herbivory: a mixed blessing for Jurinea mollis (Asteraceae). Oikos 39:269–272

    Google Scholar 

  • Jensen KR (1980) A review of sacoglossan diets, with comparative notes on radular and buccal anatomy. Malacol Rev 13:55–77

    Google Scholar 

  • Kraft GT (1972) Preliminary studies of Phillippine Eucheuma species (Rhodophyta). Part 1, taxonomy and ecology of Eucheuma arnoldii Weber-van Bosse. Pac Sci 26:318–334

    Google Scholar 

  • Kroh GC, Beaver DL (1978) Insect response to mixture and monoculture patches of Michigan old-field annual herbs. Oecologia 31:269–275

    Google Scholar 

  • Lawrence JM (1975) On the relationships between marine plants and sea urchins. Oceanogr Mar Biol Annu Rev 13:213–286

    Google Scholar 

  • Lessios HA, Robertson DR, Cubit JD (1984) Spread of Diadema mass mortality through the Caribbean. Science 226:335–337

    Google Scholar 

  • Levin DA (1973) The role of trichomes in plant defense. Q Rev Biol 48:3–15

    Google Scholar 

  • Levings SC, Garrity SD (1983) Diel and tidal movement of two co-occurring neritid snails; differences in grazing patterns on a tropical rocky shore. J Exp Mar Biol Ecol 67:261–278

    Google Scholar 

  • Lewis SM (1985) Herbivory on coral reefs: algal susceptibility to herbivorous fishes. Oecologia 65:370–375

    Google Scholar 

  • Lewis SM, Wainwright P (1985) Herbivore abundance and grazing intensity on a Caribbean coral reef. J Exp Mar Biol Ecol 87:215–228

    Google Scholar 

  • Littler MM, Littler DS (1980) The evolution of thallus form and survival strategies in benthic marine macroalgae: field and laboratory tests of a functional form model. Am Nat 116:25–44

    Google Scholar 

  • Littler MM, Littler DS (1984) Models of tropical reef biogenesis: the contribution of macroalgae. In: Round FE, Chapman DJ (eds) Progress in phycological research, vol 3. Biopress, Bristol, England, pp 232–364

    Google Scholar 

  • Littler MM, Littler DS, Taylor PR (1983a) Evolutionary strategies in a tropical barrier reef system: functional-form groups of marine macroalgae. J Phycol 19:229–237

    Google Scholar 

  • Littler MM, Taylor PR, Littler DS (1983b) Algal resistance to herbivory on a Caribbean barrier reef. Coral Reefs 2:111–118

    Google Scholar 

  • Lubchenco J (1983) Littorina and Fucus: effects of herbivores, substratum heterogeneity, and plant escapes during succession. Ecology 64:1116–1123

    Google Scholar 

  • Lubchenco J, Cubit J (1980) Heteromorphic life histories of certain marine algae as adaptations to variations in herbivory. Ecology 61:676–687

    Google Scholar 

  • Lubchenco J, Gaines SD (1981) A unified approach to marine plant-herbivore interactions. I. Populations and communities. Am Rev Ecol Syst 12:405–437

    Google Scholar 

  • Lubchenco J, Menge BA (1978) Community development and persistence in a low rocky intertidal zone. Ecol Monogr 48:67–94

    Google Scholar 

  • McConnell OJ, Hughes PA, Targett NM, Daley J (1982) Effects of secondary metabolites from marine algae on feeding by the sea urchin, Lytechinus variegatus. J Chem Ecol 8:1437–1453

    Google Scholar 

  • Menge BA, Lubchenco J (1981) Community organization in temperate and tropical rocky intertidal habitats: prey refuges in relation to consumer pressure gradients. Ecol Monogr 51:429–450

    Google Scholar 

  • Montgomery WL (1980) Comparative feeding ecology of two herbivorous damselfishes (Pomacentridae: Teleostei) from the Gulf of California, Mexico. J Exp Biol Ecol 47:9–24

    Google Scholar 

  • Montgomery WL, Gerrodette T, Marshall LD (1980) Effects of grazing by the yellowtail surgeonfish, Prionurus nunctatus, on algal communities in the Gulf of California, Mexico. Bull Mar Sci 30:901–908

    Google Scholar 

  • Morris RF (ed) (1963) The dynamics of epidemic spruce budworm populations, no 31. Memoirs of the Entomological Society of Canada, Ottawa

  • Norris JN, Fenical W (1982) Chemical defense in tropical marine algae. In: Rützler K, Macintyre IG (eds) The Atlantic barrier reef ecosystem at Carrie Bow Cay, Belize, I. Structure and communities. Smithsonian Contrib Mar Sci 12:417–431

  • Odgen JC, Lobel PS (1978) The role of herbivorous fishes and urchins in coral reef communities. Environ Biol Fish 3:49–63

    Google Scholar 

  • Ogden JC, Brown RA, Salesky N (1973) Grazing by the echinoid Diadema antillarum Philippi: formation of halos around West Indian patch reefs. Science 182:715–717

    Google Scholar 

  • Osman RW, Haugsness JA (1981) Mutualism among sessile invertebrates: a mediator of competition and predation. Science 211:846–848

    Google Scholar 

  • Parrish JD, Zimmerman RJ (1977) Utilization by fishes of space and food resources on an offshore Puerto Rican coral reef and its surroundings. Proc 3rd Int Coral Reef Symp 1:297–303

    Google Scholar 

  • Paul VJ, Fenical W (1983) Isolation of halimedatrial: chemical defense adaptation in the calcarous reef-building alga Halimeda. Science 221:747–749

    Google Scholar 

  • Phillips JD, Pfeiffer RK (1960) An example of the relation between palatability of pastures and selective buttercup control. In: Proceedings of the 4th British Weed Control Conference. Society of Chemical Industry, London, pp 15–16

    Google Scholar 

  • Pimentel D (1961) Species diversity and insect population outbreaks. Ann Entomol Soc Am 54:76–86

    Google Scholar 

  • Randall JE (1961) Overgrazing of algae by herbivorous marine fishes. Ecology 42:812

    Google Scholar 

  • Randall JE (1965) Grazing effect on seagrasses by herbivorous reef fishes in the West Indies. Ecology 46:255–260

    Google Scholar 

  • Randall JE (1967) Food habits of reef fishes of the West Indies. Stud Trop Oceanogr Miami 5:665–847

    Google Scholar 

  • Rausher MD (1981) The effect of native vegetation on the susceptibility of Aristolochia reticulata (Aristolochiaceae) to herbivore attack. Ecology 62:1187–1195

    Google Scholar 

  • Rhoades DF (1979) Evolution of plant chemical defense against herbivores. In: Rosenthal GA, Janzen DH (eds) Herbivores: their interaction with secondary plant metabolites. Academic, New York, pp 3–54

    Google Scholar 

  • Risch SJ (1979) A comparison, by sweep sampling, of the insect fauna from corn and sweet potato monocultures and dicultures in Costa Rica. Oecologia 42:195–212

    Google Scholar 

  • Robinson T (1980) The organic constituents of higher plants: their chemistry and interrelationships. Burgess, Minneapolis, Minn

    Google Scholar 

  • Root RB (1973) Organization of a plant-arthropod association in simple and diverse habitats: the fauna of collards (Brassica oleraceae). Ecol Monogr 43:95–124

    Google Scholar 

  • Root RB (1974) Some consequences of ecosystem texture. In: Levin SA (ed) Ecosystem analysis and prediction. Proceedings of a Conference on Ecosystems, Alta, Utah, pp 83–97

  • Rosenthal GA, Janzen DH (1979) Herbivores: their interaction with secondary plant metabolites. Academic, New York

    Google Scholar 

  • Rützler K, Macintyre IG (eds) (1982) The Atlantic barrier reef ecosystem at Carrie Bow Cay, Belize, I. Structure and communities. Smithsonian Contrib Mar Sci 12:1–539

  • Sammarco PW (1983) Effects of fish grazing and damselfish territoriality on coral reef algae. I. Algal community structure. Mar Ecol Prog Ser 13:1–14

    Google Scholar 

  • Sammarco PW, Levinton JS, Ogden JC (1974) Grazing and control of coral reef community structure by Diadema antillarum Philippi (Echinodermata: Echinoidea): a preliminary study. J Mar Res 32:47–53

    Google Scholar 

  • Shacklock PF, Doyle RW (1983) Control of epiphytes in seaweed cultures using grazers. Aquaculture 31:141–151

    Google Scholar 

  • Simberloff D, Brown BJ, Lowrie S (1978) Isopod and insect root borers may benefit Florida mangroves. Science 201:630–632

    Google Scholar 

  • Smith JG (1969) Some effects of crop background on populations of aphids and their natural enemies on Brussels sprouts. Ann Appl Biol 63:326–329

    Google Scholar 

  • Sokal RR, Rohlf FJ (1969) Biometry. Freeman, San Francisco, Calif

    Google Scholar 

  • Sousa WP, Schroeter SC, Gaines SD (1981) Latitudinal variation in intertidal algal community structure: the influence of grazing and vegetative propagation. Oecologia 48:297–307

    Google Scholar 

  • Steinberg PD (1984) Algal chemical defense against herbivores: allocation of phenolic compounds in the kelp Alaria marginata. Science 223:405–407

    Google Scholar 

  • Steinberg PD (1985) Feeding preferences of Tegula funebralis and chemical defenses in marine brown algae. Ecol Monogr 55:333–349

    Google Scholar 

  • Steneck RS (1982) A limpet-coralline alga association: adaptations and defenses between a selective herbivore and its prey. Ecology 63:507–522

    Google Scholar 

  • Steneck RS (1983) Quantifying herbivory on coral reefs: just scratching the surface or still biting off more than we can chew. In: Reaka ML (ed) The ecology of deep and shallow coral reefs. NOAA's Undersea Research Program, vol 1, no 1, National Oceanic and Atmospheric Administration, US Department of Commerce, Washington, DC, pp 103–111

    Google Scholar 

  • Stephenson W, Searles RB (1960) Experimental studies on the ecology of intertidal environments at Heron Island. Aust J Mar Freshwater Res 11:241–267

    Google Scholar 

  • Stimson J (1973) The role of the territory in the ecology of the intertidal limpet Lottia gigantea (Gray). Ecology 54:1020–1030

    Google Scholar 

  • Suchaneck TH (1978) The ecology of Mytilus edulis L. in exposed rocky intertidal communities. J Exp Mar Biol Ecol 31:105–120

    Google Scholar 

  • Sutherland JP (1974) Multiple stable points in natural communities. Am Nat 108:859–873

    Google Scholar 

  • Tahvanainen JO, Root RB (1972) The influence of vegetational diversity on the population ecology of specialized herbivore, Phyllotreta cruciferae (Coleoptera: Chrysomelidae). Oecologia 10:321–346

    Google Scholar 

  • Targett NM, McConnell OJ (1982) Detection of secondary metabolites in marine macrophytes using the marsh periwinkle, Littorina irrorata Sya, as an indicator organism. J Chem Ecol 8:115–124

    Google Scholar 

  • Turner T (1985) Stability of rocky intertidal surfgrass beds: persistence, preemption, and recovery. Ecology 66:83–92

    Google Scholar 

  • Vermeij GJ (1978) Biogeography and adaptation. Harvard University Press, Cambridge, England

    Google Scholar 

  • Vermeij GJ (1983) Intimate associations and coevolution in the sea. In: Futuyma DJ, Slatkin M (eds) Coevolution. Sinauer, Sunderland, Mass, pp 311–327

    Google Scholar 

  • Woodin SA (1978) Refuges, disturbance, and community structure: a marine soft-bottom example. Ecology 59:274–284

    Google Scholar 

Download references

Author information

Author notes

  1. Phillip R. Taylor

    Present address: Biological Oceanography Program, National Science Foundation, 20550, Washington, DC, USA

Authors and Affiliations

  1. Department of Botany, National Museum of Natural History, Smithsonian Institution, 20560, Washington, DC, USA

    Mark M. Littler, Phillip R. Taylor & Diane S. Littler

Authors
  1. Mark M. Littler
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Phillip R. Taylor
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Diane S. Littler
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Littler, M.M., Taylor, P.R. & Littler, D.S. Plant defense associations in the marine environment. Coral Reefs 5, 63–71 (1986). https://doi.org/10.1007/BF00270354

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00270354

Keywords

Search

Navigation