Seaweed Adaptations to Herbivory Author(s): J. Emmett Duffy and Mark E. Hay Source: BioScience, Vol. 40, No. 5 (May, 1990), pp. 368-375 Published by: American Institute of Biological Sciences Stable URL: http://www.jstor.org/stable/1311214 Accessed: 06/01/2010 15:17 Your use of the JSTOR archive indicates your acceptance of JSTOR's Terms and Conditions of Use, available at http://www.jstor.org/page/info/about/policies/terms.jsp. JSTOR's Terms and Conditions of Use provides, in part, that unless you have obtained prior permission, you may not download an entire issue of a journal or multiple copies of articles, and you may use content in the JSTOR archive only for your personal, non-commercial use. Please contact the publisher regarding any further use of this work. Publisher contact information may be obtained at http://www.jstor.org/action/showPublisher?publisherCode=aibs. Each copy of any part of a JSTOR transmission must contain the same copyright notice that appears on the screen or printed page of such transmission. JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact [email protected]. American Institute of Biological Sciences is collaborating with JSTOR to digitize, preserve and extend access to BioScience. http://www.jstor.org Seaweed Adaptations to Herbivory Chemical,structural, and morphologicaldefenses are often adjustedto spatial or temporalpatterns of attack J. EmmettDuffy and Mark E. Hay erbivoryon seaweedscan be kelp beds along several kilometersof intense,with nearly100% of and coastline (Tegnerand Dayton 1987), production being consumed Fish, urchins, these events are rare. Mesograzer in some habitats (Carpenter1986). gastropods can each populationsare usuallymaintained at Seaweedsminimize damage from her- low densities by predation, and they bivores by any of three strategies strongly affect seaweed commonly have little obvious effect (Lubchencoand Gaines 1981). They communities on most seaweeds (Duffy in press, can escapein space or time so they do Hay et al. 1988c). However, meso- not co-occur with important herbi- . grazerscan have subtle but important vores or are not detected when they effects on some seaweeds, and the do co-occur. They can deter feeding ture; in temperate communities, ur- types of effectscan differdramatically by herbivoresthat encounterand rec- chins and gastropods tend to be most among mesograzer species (Brawley ognize the plant. And they can mini- important (Carpenter 1986, Gaines and Adey 1981, Duffy in press). mize the decrease in fitness that re- and Lubchenco 1982, Hawkins and Fish may have been especially im- sults from herbivoreattack. Hartnoll 1983, Hay 1984a, in press a, portant in selecting for antiherbivore Herbivory'sprofound effects on the Lubchenco and Gaines 1981). Al- traits in seaweeds (Hay in press a, organizationof seaweedcommunities though mesograzers such as amphi- Steneck1983) becauseof their mobil- has been extensively reviewed (Car- pods can dramatically affect seaweed ity, abundance,high metabolic rate, penter 1986, Dayton 1975, Hay communities by destroying entire and, for some abundanttropical spe- 1985, Lewis 1986, Lubchenco and Gaines 1981). In this article, we de- scribeseaweed characteristicsthat di- minish losses to herbivores. Seaweeds are consumed by a di- verse assemblage of herbivores that includes fishes, urchins, gastropods, crabs, and numerous smaller herbi- vores such as amphipods, isopods, and polychaetes (collectivelytermed mesograzers). In tropical habitats, fish and urchins have the greatest effect on seaweed community struc- J. EmmettDuffy is a postdoctoralfellow in the Departmentof InvertebrateZool- ogy, NationalMuseum of NaturalHis- tory, SmithsonianInstitution, Washing- ton, DC 20560.Mark Hay is an associate professorof marinesciences, biology, and ecology at the Universityof North Caro- lina at Chapel Hill, Institute of Marine Sciences, Morehead City, NC 28557. ? 1990 AmericanInstitute of Biological Sciences. A dense school of parrotfishgraze algae on a coral reef. Photo: M. Hay. 368 BioScienceVol. 40 No. 5 cies, fused teeth (Figure 1), which Hypnea musciformis was quickly allow them to feed on tough or calci- eaten by fish when growing alone, but fied seaweeds. Urchins and gastro- it grew more rapidlythan it was con- pods can also be importantin habi- sumedwhen placedin contactwith its tats where they reach high densities unpalatable competitor, the brown (Carpenter1986, Hawkins and Hart- alga Sargassum filipendula (Hay noll 1983). 1986). During the yearlypeak in her- Fish, urchins, and gastropods can bivore abundance,Hypnea and other each strongly affect present-daysea- palatableseaweeds were found exclu- weed communities (Carpenter1986, sively in associationwith unpalatable Hawkins and Hartnoll 1983, Hay plants; at times of year when herbi- 1985, Lewis 1986, Lubchenco and vores were less active, palatable Gaines 1981), and the fossil record plants were not strongly associated suggests they have played a major with unpalatablespecies. role throughout evolutionary time In communities where associa- (Steneck 1983). In this article, we tional refuges are important, species discuss how seaweeds escape, deter, richnesscan increase rather than de- or tolerate herbivory. The depth in crease as the community becomes which we cover each of these topics dominatedby a few unpalatablesea- reflects the availability of rigorous weeds (Hay 1986). In these cases, experimentalstudies; we know little palatablealgae that would have been of the relative importance of these eliminatedby grazerscan persistonly differenttraits. in association with their unpalatable competitors.Similarly, on coral reefs, Figure1. The beak-liketeeth (top) and twice as taxa occur from herbivores mill and in nearly many Escaping pharyngeal (middle bottom) within 10 cm of the chemically de- Seaweeds can avoid theback of thethroat from two speciesof fended brown zo- Spatial refuges. Caribbeanparrotfishes. The fusedteeth alga Stypopodium herbivoresby growing in habitats, in enablethe fishto bite into hardcalcified nale as in similar-sized areas away from et al. microhabitats,or at times of year in surfacesto extractalgal tissues. The pha- Stypopodium (Littler which herbivoresare not active. For ryngealmill functionslike a mortarand 1986). As a final example, brown example, on tropical coral reefs pestle,grinding the seaweedsalong with algae in the genus Desmarestia con- whereherbivores are abundant,many sedimentsand coralrock. Because these centrate sulfuric acid up to 18% of seaweeds that are physiologicallyca- fish have no cellulases,they use their plant dry mass (Andersonand Velim- pable of growing on topographically mouthpartsto physicallyrupture the algal irov 1982). In Chilean kelp beds complex reef slopes occur only where cells.Photo: S. M. Lewis. heavily grazed by sea urchins, the herbivoredensities are low-on topo- palatable kelp Macrocystis cannot graphically simple sand plains and successfullycolonize unless it invades reef flats (Hay 1981a, 1984b, 1985, spatial refuges for seaweeds. Reef an area encircled by Desmarestia Lewis 1986). Similarly, Caribbean damselfishare small, aggressiveher- plants, which appear to act as "acid patch reefs are often surroundedby bivoresthat establishgardens of pal- brooms"that sweep the substrateand halos of bare sand that are kept free atablealgae by removingunpalatable prohibit urchins from entering the of seagrassesby grazing fish and ur- species and by vigorously defending area (Dayton 1985). chins (Ogden et al. 1973, Randall their gardens against other herbi- Associational refuges can thus be 1965). Because many reef-associated vores. Though the damselfishfeed in effectivein a variety of marine habi- grazersare reluctantto venturemore the gardens, these plots experience tats and against different kinds of than approximately 10 m from the reduced herbivory relative to areas herbivores. Interestingly, although shelter of the reef, seagrassesthrive not defended by damselfish.A few the patternsand processesof associa- beyond this radius. seaweedsdepend on these herbivore- tional resistancein marineand terres- On a smaller spatial scale, sea- created refuges, and algal diversity trial systems are similar, the mecha- weeds may live in cracks and holes can be higherin damselfishterritories nisms producing them can be inaccessibleto herbivores. On inter- than in eithercaged or uncagedareas strikingly different. In the best- tidal rock surfaces along Pacific Pa- outside territories(Hixon and Brost- studied marine example (Pfisterand nama, where herbivoryis particularly off 1983). Hay 1988), the palatable seaweed intense, herbivore-resistant algal Gracilariawas grazed more by sea crusts dominate exposed surfaces, Associational refuges. Herbivore- urchinswhen it occurredas a mono- whereas less-resistantleafy algae oc- influenced communities are often culture than when it occurred in a cur primarilyor exclusively in holes dominated by unpalatableseaweeds polyculturewith the unpalatablealga or cracks(Menge et al. 1985). Spatial that may createrefuges for more pal- Sargassum. The greatest grazing in escapes have been discussedin detail atablespecies (Hay 1986, Littleret al. monoculturesoccurred because indi- by Lubchencoand Gaines (1981) and 1986, Pfister and Hay 1988). For