Abstract
The potential for spatial associations between palatable and unpalatable plant species to reduce herbivore pressure on the palatable species has been described as associational resistance, associational refuge or associational defense for numerous terrestrial and marine communities. One of the closest associations between species-epibiosis-has not been thoroughly investigated in this regard. In this study we evaluated how different associations between host seaweeds and epibiotic plants and animals influenced the movement of an omnivorous sea urchin (Arbacia punctulata) to the host and subsequent feeding on the host. A. punctulata showed clear preferences when given pairwise choices between 12 prey species (3 animals, 9 algae). These preferences were consistent and allowed us to rank the six epibiont species and six host species linearly from least to most preferred by A. punculata. Most host-epibiont associations dramatically changed urchin preference, increasing or decreasing urchin grazing on fouled hosts as compared to clean conspecifics. Herbivory on the host increased when the epibiont was more preferred, and decreased when it was less preferred than the unfouled host alga. Taking the host species as a point of reference, we classified epibiosis-caused decrease in herbivory as associational resistance, while epibiont-caused increases in herbivory were defined as shared doom. These epibiont-host-herbivore interactions could select for hosts that facilitate the growth of certain low preference epibionts on their surfaces in situations where the resulting decreases in herbivory would offset the various negative effects of being fouled. In contrast, in situations where herbivores are common, the negative effects of being fouled by palatable epibionts may be much greater than is generally assumed. In our assays, unpalatable hosts fouled by palatable epibionts became much more attractive to urchins and rose several ranks on the urchins' preference hierarchy.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Andrew NL (1993) Spatial heterogeneity, sea urchin grazing, and habitat structure on reefs in temperate Australia. Ecology 74:292–302
Atsatt PR, O'Dowd DJ (1976) Plant defense guilds. Science 193:24–29
Bach CE (1980) Effects of plant diversity and time of colonization on an herbivore-plant interaction. Oecologia 44:319–326
Barkai A, McQuaid C (1988) Predator-prey role reversal in a marine benthic ecosystem. Science 242:62–64
Bernstein BB, Jung N (1979) Selective pressure and coevolution in a kelp canopy community in Southern California. Ecol Monogr 493:335–355
Brawley SH (1992) Mesoherbivores. In: John DM, Hawkins SJ, Price JH (eds) Plant-animal interactions in the marine benthos. (Systematics Association, special vol 46). Clarendon Press, Oxford, pp 235–263
Davis AR, Targett NM, McConnell OJ, Young CM (1989) Epibiosis of marine algae and benthic invertebrates: natural products chemistry and other mechanisms inhibiting settlement and overgrowth. In: Scheuer PJ (ed) BioOrganic marine chemistry, vol 3. Springer, Berlin Heidelberg New York, pp 86–114
Dean TA, Schroeter SC, Dixon JD (1984) Effects of grazing by two species of sea urchins (Strongylocentrotus franciscanus and Lytechinus anamesus) on recruitment and survival of two species of kelp (Macrocystis pyrifera and Pterygophora californica). Mar Biol 78:301–313
Denno RF, McClure MS (1983) Variable plants and herbivores in natural and managed systems. Academic Press, New York
Duffy JE (1990) Amphipods on seaweeds: partners or pests? Oecologia 83:267–276
Duffy JE, Hay ME (1994) Herbivore resistance to seaweed chemical defense: the roles of mobility and predation risk. Ecology 75:1304–1319
Elner RW, Vadas RL (1990) Inference in ecology: the sea urchin phenomenon in the northwestern Atlantic. Am Nat 136:108–125
Feifarek BP (1987) Spines and epibionts as antipredator defenses in the thorny oyster Spondylus americanus Hermann. J Exp Mar Biol Ecol 105:39–56
Fletcher WJ (1987) Interactions between subtidal Australian sea urchins, gastropods, and algae: effects of experimental removals. Ecol Monogr 57:89–109
Gil-Turnes MS, Hay ME, Fenical W (1989) Symbiotic marine bacteria chemically defend crustacean embryos from a pathogenic fungus. Science 246:116–118
Harrold C, Reed DC (1985) Food availability, sea urchin grazing, and kelp forest community structure. Ecology 66:1160–1169
Hay ME (1985) Spatial patterns of herbivore impact and their importance in maintaining algal species richness. Proc 5th Int Coral Reef Congr 4:29–34
Hay ME (1986) Associational plant defenses and the maintenance of species diversity: turning competitors into accomplices. Am Nat 128:617–641
Hay ME (1992) The role of seaweed chemical defenses in the evolution of feeding specialization and in the mediation of complex interactions. In: Paul VJ (ed) Ecological roles for marine natural roducts. Comstock Press, Ithaca, NY, pp 93–118
Hay ME, Fenical W (1988) Marine plant-herbivore interactions: the ecology of chemical defense. Annu Rev Ecol Syst 19:111–145
Hay ME, Steinberg PD (1992) The chemical ecology of plant-herbivore interactions in marine versus terrestrial communities. In: Rosenthal J, Berenbaum M (eds) Herbivores: their interaction with secondary plant metabolites, vol II. Evolutionary and ecological processes. Academic Press, New York, pp 371–413
Hay ME, Lee RR, Guieb RA, Bennett MM (1986) Food preference and chemotaxis in the sea urchin Arbacia punctulata. J. Exp Mar Biol Ecol 96:147–153
Hay ME, Duffy JE, Pfister CA, Fenical W (1987) Chemical defense against different marine herbivores: are amphipods insect equivalents?. Ecology 68:1567–1580
Hay ME, Kappel QE, Fenical W (1994) Synergisms in plant defenses against herbivores: interactions of chemistry, calcification, and plant quality. Ecology 75:1714–1726
Karban R (1993) Costs and benefits of induced resistance and plant density for a native shrub, Gossypium thurberi. Ecology 741:9–19
Kearsley MJC, Whitham TG (1992) Guns and butter: a no-cost defense against predation for Chrysomela confluens. Oecologia 92:556–562
Lawrence JM (1975) On the relation between marine plants and sea urchins. Oceanogr Mar Biol Annu Rev 13:213–286
Littler MM, Taylor PR, Littler DS (1986) Plant defense associations in the marine environment. Coral Reefs 5:63–71
McNaughton SJ (1978) Serengeti ungulates: feeding selectivity influences the effectiveness of plant defense guilds. Science 199:806–807
Martin TE (1988) On the advantage of being different: nest predation and the coexistance of bird species. Proc Natl Acad Sci 85:2196–2199
Morris WF, Karieva PM (1991) How insect herbivores find suitable host plants: the interplay between random and non-random movement. In: Bernays EA (ed) Insect-plant interactions. CRC Press, Baton Rouge, pp 175–208
Pfister CA, Hay ME (1988) Associational plant refuges: convergent patterns in marine and terrestrial communities result from differing mechanisms. Oecologia 77:118–129
Renaud PE, Hay ME, Schmitt TM (1990) Interactions of plant stress and herbivory: intraspecific variation in the susceptibility of a palatable versus an unpalatable seaweed to sea urchin grazing. Oecologia 82:217–226
Root RB (1973) Organization of a plant-arthropod association in simple and diverse habitats: the fauna of collards (Brassica oleracea). Ecol Monogr 431:95–120
Schmitt TM, Hay ME, Lindquist N (in press) Constraints on chemically mediated coevolution: multiple functions for seaweed secondary metabolites. Ecology
Simms EL, Rausher MD (1987) Costs and benefits of plant resistance to herbivory. Am Nat 130:570–581
Sousa WP, Connell JH (1992) Grazing and succession in marine algae. In: John DM, Hawkins SJ, Price JH (eds) Plant-animal interactions in the marine benthos. (Systematics Association, special vol 46) Clarendon Press, Oxford, pp 425–441
Tahvanainen JO, Root RB (1972) The influence of vegetational diversity on the population ecology of a specialized herbivore, Phyllotreta crucifera (Coleoptera: Chrysomelidae). Oecologia 10:321–346
Vadas RL (1977) Preferential feeding: an optimization strategy in sea urchins. Ecol Monogr 47:337–371
Wahl M (1989) Marine epibiosis. I. Fouling and antifouling: some basic aspects. Mar Ecol Progr Ser 58:175–189
Williams GA, Seed R (1992) Interactions between macrofaunal epiphytes and their host algae. In: John DM, Hawkins SJ, Price JH (eds) Plant-animal interactions in the marine benthos. (Systematic Association, special vol 46) Clarendon Press, Oxford, pp 189–211
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Wahl, M., Hay, M.E. Associational resistance and shared doom: effects of epibiosis on herbivory. Oecologia 102, 329–340 (1995). https://doi.org/10.1007/BF00329800
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00329800