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Associational plant refuges: convergent patterns in marine and terrestrial communities result from differing mechanisms

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An associational plant refuge occurs when a plant that is susceptible to herbivory gains protection from herbivory when it is associated with another plant. In coastal North Carolina, the abundance of the palatable red alga Gracilaria tikvahiae is positively correlated with the abundance of the unpalatable brown alga Sargassum filipendula during times of increased herbivore activity. To see if grazing by the sea urchin Arbacia punctulata could generate this pattern, controlled experiments were conducted in out-door microcosms and in the laboratory. Gracilaria beneath a canopy of Sargassum was eaten significantly less than Gracilaria alone. When Arbacia were excluded, Gracilaria alone grew significantly more than Gracilaria beneath Sargassum, demonstrating that Sargassum is a competitor of Gracilaria. Experiments investigating Sargassum's deterrent role indicated that Sargassum decreased the foraging range of Arbacia and the rate at which it fed on Gracilaria. Additional experiments with plastic Sargassum mimics indicated that the decreased grazing on Gracilaria was not a result of Sargassum morphology, but was probably attributable to some chemical characteristic of Sargassum. The pattern of increased grazing in monocultures (only Gracilaria present) versus polycultures (both Gracilaria and Sargassum present) demonstrated in this study also has been demonstrated for plant-insect interactions in terrestrial communities. In these communities, insect density is higher in monocultures than in polycultures because insects find and immigrate to monocultures more rapidly, and once in a monoculture, they emigrate from them less often than from polycultures. In this study, urchins did not find and immigrate to monocultures more rapidly, nor did they tend to stay in them once they were found; in fact, they emigrated from monocultures of Gracilaria more rapidly than from Gracilaria and Sargassum polycultures. Increased grazing in Gracilaria monocultures resulted from increased rates of movement and feeding of individual herbivores, not from increased herbivore density as has been reported for terrestrial systems.

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References

  • Adams SM (1976) The ecology of eelgrass Zostera marina (L.), fish communities. I. Structural analysis. J Exp Mar Biol Ecol 22:269–291

    Google Scholar 

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

    Google Scholar 

  • Bach CE (1980) Effects of plant diversity and time of colonization on an herbivore-plant interaction. Oecologia 44:319–326

    Google Scholar 

  • Bertness ME, Yund PO, Brown AF (1983) Snail grazing and the abundance of algal crusts on a sheltered New England rocky beach. J Exp Mar Biol Ecol 71:147–164

    Google Scholar 

  • Bock RD (1975) Multivariate Statistical Methods in Behavioral Research. McGraw-Hill, New York

    Google Scholar 

  • Bonsdorff E, Vahl O (1982) Food preferences of the sea urchins Echinus acutus and E. esculentus. Mar Behav Physiol 8:243–248

    Google Scholar 

  • Brown BJ, Ewel JJ (1987) Herbivory in complex and simple tropical successional ecosystems. Ecology 68(1):108–116

    Google Scholar 

  • Buss LW (1978) Habitat selection, directional growth and spatial refuges: why colonial animals have more hiding places. In: Larwood G, Rosen BR (eds) Biology and systematics of colonial organisms. Academic Press, London, pp 459–497

    Google Scholar 

  • Carpenter RC (1981) Grazing by Diadema antillarum (Philippi) and its effects on the benthic algal community. J Mar Res 39(4):749–765

    Google Scholar 

  • Connell JH (1978) Diversity in tropical rain forests and coral reefs. Science 199:1302–1310

    Google Scholar 

  • Connell JH, Orias E (1964) The ecological regulation of species diversity. Am Nat 98:399–414

    Google Scholar 

  • Cromartie WJ (1975) The effect of stand size and vegetational background on the colonization of cruciferous plants by herbivorous insects. J Appl Ecol 12:517–533

    Google Scholar 

  • Darcy GH (1985a) Synopsis of biological data on the spottail pinfish, Diplodus holbrooki (Pisces: Sparidae). NOAA Technical Report NMFS 19, 11 pp

  • Darcy GH (1985b) Synopsis of biological data on the pinfish, Lagadon rhomboides (Pisces: Sparidae). NOAA Technical Report NMFS 23, 32 pp

  • Dayton PK (1971) Competition, disturbance, and community organization: the provision and subsequent utilization of space in a rocky intertidal community. Ecol Monogr 41:351–389

    Google Scholar 

  • Dayton PK (1975) Experimental evaluation of ecological dominance in a rocky intertidal algal community. Ecol Monogr 45:137–159

    Google Scholar 

  • Dean TA, Shroeter 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

    Google Scholar 

  • Dethier MN (1981) Heteromorphic algal life histories: the seasonal pattern and response to herbivory of the brown crust, Ralfsia californica. Oecologia 49:333–339

    Google Scholar 

  • Dethier MN (1984) Disturbance and recovery in intertidal pools: maintenance of mosaic patterns. Ecol Monogr 54(1):99–118

    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 

  • Egloff DA (1986) Effects of Olisthodiscus luteus on the feeding and reproduction of the marine rotifer Synchaeta cecilia. J Plank Res 8(2):263–274

    Google Scholar 

  • Foster MS (1975) Regulation of algal community development in a Macrocystis pyrifera forest. Mar Biol 32:331–342

    Google Scholar 

  • Fuentes ER, Hoffman AJ, Poiani A, Alliende MC (1986) Vegetation change in large clearings: patterns in the Chilean mattoral. Oecologia 68:358–366

    Google Scholar 

  • Gaines SD (1985) Herbivory and between habitat diversity: the differential effectiveness of defenses in a marine plant. Ecology 66(2):473–485

    Google Scholar 

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

    Google Scholar 

  • Garnick E (1978) Behavioral ecology of Strongylocentrotus droebachiensis (Muller) (Echinodermata: Echinoidea). Oecologia 37:77–84

    Google Scholar 

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

    Google Scholar 

  • Grubb PJ (1986) Problems posed by sparse and patchily distributed species in species-rich plant communities. In: Diamond J, Case T (eds) Community Ecology. Harper and Row, New York, pp 207–225

    Google Scholar 

  • Gurevitch J, Chester ST Jr (1986) Analysis of repeated measures experiments. Ecology 67(1):251–255

    Google Scholar 

  • Hay ME (1981 a) Herbivory, algal distribution, and the maintenance of between-habitat diversity on a tropical fringing reef. Am Nat 118(4):520–540

    Google Scholar 

  • Hay ME (1981 b) The functional morphology of turf-forming sea-weeds: persistence in stressful marine habitats. Ecology 62(3):739–750

    Google Scholar 

  • Hay ME (1984) 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 paterns of herbivore impact and their importance in maintaining algal species richness. Proc Fifth Int Coral Reef Cong, Tahiti, 4:29–34

    Google Scholar 

  • Hay ME (1986) Associational defenses and the maintenance of species diversity: turning competitors into accomplices. Am Nat 128:617–641

    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 

  • Hay ME, Duffy JE, Pfister CA, Fenical W (1987 a) Chemical defense against different marine herbivores: are amphipods insect equivalents? Ecology 68:1567–1580

    Google Scholar 

  • Hay ME, Fenical W, Gustafson (1987 b) Chemical defense against diverse coral-reef herbivores. Ecology 68:1581–1591

    Google Scholar 

  • Hay ME, Lee RR Jr, Guieb RA, Bennett MM (1986) Food preference and chemotaxis in the sea urchin Arbacia punctulata (Lamarck) Philippi. J Exp Mar Biol Ecol 96:147–153

    Google Scholar 

  • Himmelman JH, Steele DH (1971) Food and predators of the green sea urchin Strongylocentrotus droebachiensis in Newfoundland waters. Mar Biol 9:315–322

    Google Scholar 

  • Hixon MA, Brostoff WM (1983) Damselfish as keystone species in reverse: intermediate disturbance and diversity of reef algae. Science 220:511–513

    Google Scholar 

  • Hutchinson GE (1959) Homage to Santa Rosalia or why are there so many kinds of animals? Am Nat 93:145–159

    Google Scholar 

  • Karieva P (1982) Experimental and mathematical analyses of herbivore movement: quantifying the influence of plant spacing and quality on foraging discrimination. Ecol Monogr 52(3):261–282

    Google Scholar 

  • Karlson R (1978) Predation and space utilization patterns in a marine epifaunal community. J Exp Mar Biol Ecol 31:225–239

    Google Scholar 

  • Klinger TS, Lawrence JS (1985) Distance perception of food and the effect of food quantity on feeding behavior of Lytechinus varigatus (Lamarck) (Echinodermata: Echinoidea). Mar Behav Physiol 11:327–344

    Google Scholar 

  • Larson BR, Vadas RL, Keser M (1980) Feeding and nutritional ecology of the sea urchin Strongylocentrotus drobachiensis in Maine, USA. Mar Biol 59:49–62

    Google Scholar 

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

    Google Scholar 

  • Lewis S (1986) The role of herbivorous fish in the organization of a Caribbean reef community. Ecol Monogr 56(3):183–200

    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(1): 25–44

    Google Scholar 

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

    Google Scholar 

  • Littler MM, Taylor PR, Littler DS (1986) Plant defense associations in the marine environment. Coral Reefs 5:63–71

    Google Scholar 

  • Lubchenco J (1978) Plant species diversity in a marine intertidal community: importance of herbivore food preference and algal competitive abilities. Am Nat 112:23–39

    Google Scholar 

  • Lubchenco J (1983) Littorina and Fucus: effects of herbivores, substratum heterogeneity, and plant escapes during succession. Ecology 64(5)1116–1123

    Google Scholar 

  • Lubchenco J (1986) Relative importance of competition and predation: early colonization by seaweeds in New England. In: Diamond J, Case TJ (eds) Community ecology. Harper and Row, New York, pp 537–555

    Google Scholar 

  • Lubchenco J, Cubit J (1980) Heteromorphic life histories of certain marine algae as adaptations to variations in herbivory. Ecology 61(3):676–687

    Google Scholar 

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

    Google Scholar 

  • Mann KH, Wright JLC, Welsford BE, Hatfield E (1984) Responses of the sea urchin Strongylocentrotus droebachiensis (OF Muller) to water bourne stimuli from potential predators and potential food algae. J Exp Mar Biol Ecol 79:233–244

    Google Scholar 

  • McAuliffe JR (1986) Herbivore-limited establishment of Sonoran Desert tree, Cercidium microphyllum. Ecology 67(1):276–280

    Google Scholar 

  • McCall RB, Applebaum MI (1973) Bias in the analysis of repeated-measures designs: some alternative approaches. Child Development 44:401–415

    Google Scholar 

  • McNaughton SJ (1978) Serengeti ungulates: feeding selectivity influences the effectiveness of plant defense guilds. Science 199:806–807

    Google Scholar 

  • Menge BA, Sutherland JP (1976) Species diversity gradients: synthesis of the roles of predation, competition, and temporal heterogeneity. Am Nat 110:351–369

    Google Scholar 

  • Morin PJ (1983) Predation, competition, and the composition of larval anuran guilds. Ecol Monogr 53:119–138

    Google Scholar 

  • Morrison DF (1976) Multivariate statistical methods. McGraw-Hill, New York

    Google Scholar 

  • Norris JN, Fenical W (1982) Chemical defense in tropical marine algae. In: Rutzler K, MacIntyre I (eds) The Atlantic Barrier Reef Ecosystem at Carrie Bow Cay, Belize. I: Structure and communities. Smithsonian Contr Mar Sci 12:1–539

  • Norris JN, Fenical W (1986) Natural products chemistry in benthic marine algae: uses in ecology and systematics. In: Littler MM, Littler DS (eds) Handbook of phycological methods IV: Ecological field methods. Cambridge Univ Press, Cambridge, pp 126–146

    Google Scholar 

  • Ogden JC (1976) Some aspects of herbivore-plant relationships on Caribbean reefs and seagrass beds. Aquat Bot 2:103–116

    Google Scholar 

  • Padilla DK (1985) Structural resistance of algae to herbivores, a biomechanical approach. Mar Biol 90:103–109

    Google Scholar 

  • Paine RT (1966) Food web complexity and species diversity. Am Nat 100:65–75

    Google Scholar 

  • Paine RT (1984) Ecological determinism in the competition for space. Ecology 65:1339–1348

    Google Scholar 

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

    Google Scholar 

  • Paul VJ, Hay ME (1986) Seaweed susceptibility to herbivory: chemical and morphological correlates. Mar Ecol Prog Ser 33:255–264

    Google Scholar 

  • Peterson CH (1979) Predation, competitive exclusion, and diversity in the soft-sediment benthic communities of estuaries and lagoons. In: Livingston RJ (ed) Ecological processes in coastal and marine systems. Plenum Publishing, pp 233–264

  • Peterson CH (1982) The importance of predation and intra- and interspecific competition in the population biology of two infaunal suspension-feeding bivalves, Protothaca staminea and Chione undatella. Ecol Monogr 52:437–475

    Google Scholar 

  • Pianka ER (1966) Latitudinal gradients in species diversity: a review of concepts. Am Nat 100:33–45

    Google Scholar 

  • Pianka ER (1967) On lizard species diversity: North American flatland deserts. Ecology 48:333–351

    Google Scholar 

  • Pianka ER (1969) Habitat specificity, speciation and species density in Australian desert lizards. Ecology 50(3):498–502

    Google Scholar 

  • Ricklefs RE (1987) Community diversity: relative roles of local and regional processes. Science 235:167–171

    Google Scholar 

  • Risch S (1980) The population dynamics of several herbivorous beetles in a tropical agroecosystem: the effects of intercropping corn, beans, and squash in Costa Rica. J Appl Ecol 17:593–612

    Google Scholar 

  • Root RB (1967) The niche exploitation pattern of the Blue-gray Gnatcatcher. Ecol Monogr 37:317–350

    Google Scholar 

  • Root RB (1973) Organization of a plant-arthropod association in simple and diverse habitats: the fauna of collards (Brassica oleracea). Ecol Monogr 43(1):95–124

    Google Scholar 

  • Root RB (1974) Some consequences of ecosystem texture. In: Levin SA (ed) Ecosystem analysis and prediction. Phila Soc Ind Appl Math, pp 83–97

  • Sharp D, Gray I (1962) Studies on factors affecting local distribution of two sea urchins, Arbacia punctulata and Lytechinus variegatus. Ecology 43:309–313

    Google Scholar 

  • Slocum CJ (1980) Differential susceptibility to grazers in two phases of an intertidal alga: advantages of heteromorphic generations. J Exp Mar Biol Ecol 46:99–110

    Google Scholar 

  • Sousa WP (1979) Disturbance in marine intertidal boulder fields: the nonequilibrium maintenance of species diversity. Ecology 60:1225–1239

    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 of marine brown algae. Ecol Monogr 55(3):333–349

    Google Scholar 

  • Steinberg PD (1986) Chemical defenses and the susceptibility of tropical marine brown algae to herbivores. Oecologia 69:628–630

    Google Scholar 

  • Steneck RS, Watling L (1982) Feeding capabilities and limitations of herbivorous molluscs: a functional group approach. Mar Biol 68:299–319

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Targett NM, Targett TE, Vrolijk NH, Ogden JC (1986) Effect of macrophyte secondary metabolites on feeding preferences on the herbivorous parrotfish Sparisoma radians. Mar Biol 92:141–148

    Google Scholar 

  • Taylor PR, Littler MM, Littler DS (1986) Escapes from herbivory in relation to the structure of mangrove island macroalgal communities. Oecologia 69:481–490

    Google Scholar 

  • Turchin PB (1986) Modelling the effect of host patch size on mexican bean beetle emigration. Ecology 67(1):124–132

    Google Scholar 

  • Underwood AJ (1980) The effects of grazing by gastropods and physical factors on the upper limits of distribution of intertidal macroalgae. Oecologia 46:201–213

    Google Scholar 

  • Underwood AJ (1981) Techniques of analysis of variance in experimental marine biology and ecology. Oceanogr Mar Biol Ann Rev 19:513–605

    Google Scholar 

  • Vadas RL (1977) Preferential feeding: an optimization strategy in sea urchins. Ecol Monogr 47:337–371

    Google Scholar 

  • Vadas RL (1985) Herbivory. In: Littler MM, Littler DS (eds) Handbook of Phycological Methods. Cambridge University Press, Cambridge, pp 531–572

    Google Scholar 

  • Vadas RL, Elner RW, Garwood PE, Babb IG (1986) Experimental evaluation of aggregation behavior in the sea urchin Strongylocentrotus droebachiensis, a reinterpretation. Mar Biol 90:433–448

    Google Scholar 

  • Winer BJ (1971) Statistical principles in experimental design. McGraw-Hill, New York

    Google Scholar 

  • Zar JH (1974) Biostatistical analysis. Prentice-Hall Inc, Englewood Cliffs, NJ

    Google Scholar 

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  1. Catherine A. Pfister

    Present address: Department of Zoology, University of Washington, 98195, Seattle, WA, USA

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  1. Institute of Marine Sciences, University of North Carolina at Chapel Hill, 3407 Arendell St., 28557, Morehead City, NC, USA

    Catherine A. Pfister & Mark E. Hay

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Pfister, C.A., Hay, M.E. Associational plant refuges: convergent patterns in marine and terrestrial communities result from differing mechanisms. Oecologia 77, 118–129 (1988). https://doi.org/10.1007/BF00380934

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