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Coral Reefs (1997) 16, Suppl.: S67—S76 The ecology and evolution of seaweed-herbivore interactions on coral reefs M. E. Hay University of North Carolina at Chapel Hill, Institute of Marine Sciences, Morehead City, NC 28557, USA Phone: 919—726—6841 ext. 138 FAX: 919—726—2426 E-mail: [email protected] Accepted: 18 November 1996 Abstract. Because seaweeds grow rapidly and are easy to manipulate, they have provided a wealth of information on how consumers affect coral reef community organization. Herbivory is the dominant force affecting the distribution and abundance of reef seaweeds, with seaweed morphology, structure, chemistry, and competitive ability often being a function of herbivory by fishes and larger invertebrates. Seaweeds that deter these herbivores become the favored living sites and foods of smaller, less mobile mesograzers that derive protection from consumers by associating with defended hosts. Host specialization reduces mesograzer susceptibility to predation through crypsis, sequestration of chemical defenses, and reduction of encounters with consumers. Mesograzers can serve as either pests or mutualists, depending on their feeding behavior and how it affects the host. Some mesograzers protect hosts from competitors while others attack hosts, causing induction of chemical defenses. More limited studies of corals and sponges parallel findings for seaweeds. Introduction Seaweeds are rarely studied by coral reef ecologists. Of the nearly 400 papers that have been published in Coral Reefs since the journal’s inception, 46% focus on corals, 22% on other invertebrates, 9% on fishes, 7% on seaweeds, and 16% deal with other topics such as physical processes, biogeochemical cycling, and methodology. Most of the papers dealing with seaweeds were published in a special issue devoted to Halimeda, leaving only about 3% of the regular publications devoted to seaweeds. The minimal focus on seaweeds appears appropriate if one looks at their abundance on many reefs. However, this view misses the point that, if they are not removed by herbivores, they are the competitively dominant organisms on coral reefs and are capable of destroying reefs as we know them (Hughes 1994). Although studying macrophytes on reefs often borders on the study of what is not there, the small size and robustness of reef seaweeds make experimental transplantation remarkably easy, and the high productivity of reef seaweeds allows growth rate responses to be measured in days rather than months or years (Hay 1981a, 1985; Hay et al. 1983; Lewis 1986; Carpenter 1988). Seaweeds are, therefore, exceptional tools for studying the basic processes affecting population and community organization on coral reefs. Below, I provide an overview of general ecological and evolutionary insights that have been provided by the study of reef seaweeds. Because recent investigations of sponges (Dunlap and Pawlik 1996) and corals (Littler et al. 1989) both found patterns and processes mirroring those known for seaweeds, seaweed investigations may provide a template for understanding the ecology and evolution of coral reefs in general. Herbivory on coral reefs Although seaweed distribution and abundance are determined by the interactive effects of herbivory, competition, and physical disturbances or stresses (Littler and Littler 1984; Steneck and Dethier 1994), repeated experiments on coral reefs have documented the overwhelming importance of herbivory in most situations (Randall 1965; Hay 1985, 1991a; Lewis 1986; Carpenter 1986; Lessios 1988; Morrison 1988; Hughes 1994; Hixon and Brostoff 1996). Herbivores commonly remove almost all seaweed biomass on shallow fore reefs, leaving primarily encrusting corallines, which are resistant to herbivore removal, and small rapidly growing filamentous algae that tolerate herbivory by rapidly replacing lost tissues (Steneck 1988; Duffy and Hay 1990). On topographically complex portions of coral reefs, herbivorous fishes bite the bottom at rates of 20 000 to 156 000 bites/m2/day, and either fishes alone or, in some locations, sea urchins alone can remove nearly 100% of algal production (Hatcher and Larkum 1983; Carpenter 1986, 1988; Klumpp and Poulunin 1989). Rates of herbivory on coral reefs exceed rates measured in any other habitats, either terrestrial or marine (Carpenter 1986). S68 These high rates are generated by the high density and diversity of reef herbivores, the high metabolic rates of some species (e.g., fishes) and high densities of others (e.g., sea urchins), and by the need for herbivores to consume large masses of low protein algae in order to acquire adequate nitrogen for growth and reproduction (Mattson 1980; Horn 1989). As an example, in their quest for adequate protein, herbivorous fishes on the Great Barrier Reef have been estimated to consume 10 times as much carbon as is needed to meet their energetic needs (Hatcher 1981). The high productivity of reefs combined with the tight coupling between production and consumption result in plant-herbivore interactions being one of the dominant forces affecting community structure as a whole. The studies cited provide a wealth of experimental demonstrations of the strong effects that herbivores have on seaweeds and the strong effects that seaweeds can have on other reef organisms (Hughes 1994). Grazing scars left in fossilized coralline algae demonstrate a long evolutionary history of herbivory on coral reefs (Steneck 1983). To persist on reefs, seaweeds must escape, tolerate, or deter herbivory (Lubchenco and Gaines 1981). In this work I concentrate on determining (1) which types of herbivores have the greatest impact on reef seaweeds, (2) seaweed traits that deter these herbivores, and (3) the indirect effects of these defensive traits on non-target organisms and on reef communities in general. Herbivores and their effects on reef seaweeds Reefs may be populated by diverse groups of herbivores including fishes, sea urchins, turtles, manatees, dugongs, crabs, amphipods, polychaetes, and other invertebrates. The diversity of herbivore life histories, sizes, mouth parts, and digestive physiologies makes it difficult, if not impossible, for reef seaweeds to escape or deter all herbivores. However, if seaweeds are to persist on reefs, they have to decrease herbivory to levels that allow production to exceed removal. Many experimental studies have documented the large and direct effects of fishes and sea urchins on coral reef seaweeds (see reviews by Birkeland 1989; Hay 1991a). As an example, when Lewis (1986) excluded fishes from shallow reef areas in Belize for 10 weeks, abundance of palatable macroalgae increased dramatically, overgrowing and killing corals and several less palatable seaweeds. When fishes were allowed to re-enter this area, virtually all of this increased algal mass was consumed within 48 hours. Equally dramatic results occur when sea urchins are excluded from reefs where they are abundant (Carpenter 1986; Morrison 1988; Lessios 1988). In many instances, palatable seaweeds persist in tropical communities only because they grow in mangroves, seagrass beds, reef flats, or topographically simple areas that serve as spatial refuges from reef herbivores (Hay 1981a, 1984b, 1985, 1991a), apparently because herbivores are at greater risk of predation in these habitats. Several studies suggest that overharvesting of fishes on coral reefs may allow sea urchin populations to expand because of fewer predatory and competing fishes (Hay 1984a; Hay and Taylor 1985; Carpenter 1986, 1990; McClanahan and Shafir 1990). When Carpenter (1986) evaluated grazing by fishes versus sea urchins on a reef in St. Croix, he found that the groups had different effects on algal standing stock, but that either fishes or sea urchins alone could remove virtually all algal production. This suggests that removal of sea urchins alone or fishes alone might not significantly decrease herbivory on seaweeds in this habitat; however, recent events have shown that removal of both groups allows seaweeds to escape control by herbivores, sometimes killing entire reef systems. Hughes (1994) provides impressive documentation of how overfishing of reefs in Jamaica did not appear to have dramatic effects on the reefs until the sea urchin Diadema antillarum, which occurred there in very high densities, experienced a mass mortality due to disease (Lessios 1988). Once neither herbivore group was common on Jamaican reefs, seaweed cover increased from 4% to 92% and coral cover declined from 52% to 3% on the 9 reefs Hughes studied along 300 km of coastline. The increased cover of seaweeds prevented coral recruitment, killed many adult corals, and effectively destroyed Jamaican reefs. Although other herbivores, such as crabs (Coen 1988; Stachowicz and Hay 1996), chitons (Littler et al. 1995), or limpets (Steneck 1997) can have important effects on a limited spatial scale, fishes and larger invertebrates like sea urchins appear to be responsible for most herbivory on coral reefs (Carpenter 1986; Klumpp and Pulfrich 1989; Hay and Steinberg 1992). That these groups exert stronger effects on tropical coral reefs than on temperate rocky reefs is also indicated by the recent findings that both temperate and tropical sea urchins prefer temperate over tropical seaweeds and that most of those preferences can be explained by the greater deterrency of chemical extracts from the tropical seaweeds (Bolser and Hay 1996). Thus, greater herbivory on tropical reefs appears to have resulted in more potent chemical defenses among tropical, as opposed to temperate, seaweeds. All of these considerations suggest that selection for traits that deter reef herbivores will be greater in tropical than in temperate areas and will be generated by a diverse assemblage of generalist fishes and invertebrates that differ in mobilities, habitat requirements, feeding modes, and digestive physiologies. In the face of this type of diffuse herbivore pressure (Fox 1981), selection should favor seaweeds with traits that are broadly active against numerous types of herbivores. Because single groups of herbivores such as fishes alone or sea urchins alone are capable of consuming all algal production in some habitats (Carpenter 1986), the evolution of species-specific or even groupspecific herbivore deterrents may be of limited value unless they are coupled with additional defenses that deter other herbivores. This may be why seaweeds on herbivore-rich coral reefs so commonly employ combinations of structural, morphological, and chemical defenses and, in some cases, coordinate these defenses with patterns of temporal and microhabitat escape (Hay 1984b; Paul and Hay 1986; Lewis et al. 1987; Paul and Van Alstyne 1988a; Hay and Fenical 1988; Hay 1996). Some secondary metabolites that have been demonstrated to be broadly deterrent against a wide variety of reef herbivores can also function to deter fouling or possibly microbial pathogens (Schmitt et al. 1995). These multiple roles for single S69 metabolites further limit the importance of individual herbivore species in selecting for particular plant traits. Seaweed defenses against herbivores Tropical seaweeds possess morphological, structural, mineral ("CaCO ), and chemical traits that deter reef herbi3 vores (Hay and Fenical 1988, 1996; Duffy and Hay 1990; Hay and Steinberg 1992; Paul 1992; Hay 1996). Many seaweeds combine several of these defensive traits and, in some instances, these act additively or synergistically to reduce losses to herbivores (Hay et al. 1994; Schupp and Paul 1994; Meyer and Paul 1995; Hay 1996; Pennings et al. 1996). Morphological and structural deterrents Seaweeds vary tremendously in their size, shape, toughness, degree of calcification, and thus susceptibility to being bitten or damaged by herbivores. Herbivore mouth parts, biting force, and digestive physiology also vary considerably, affecting how seaweeds may interact with different herbivores. Littler, Steneck, and their co-workers have developed general models of how seaweed productivity and susceptibility to being eaten change as a function of seaweed morphology (Littler and Littler 1980; Steneck and Watling 1982; Littler et al. 1983a,b; Steneck 1983; Steneck and Dethier 1994). They predict that microalgae are most susceptible to herbivores and that resistance to herbivores increases in the following order: filamentous algae, sheet-like algae, coarsely branched algae, leathery or rubbery algae, jointed calcareous algae, and crustose corallines (see Fig. 1 in Steneck and Watling 1982 or Table 1 in Littler et al. 1983a). This hierarchy is based in part on the decreasing food value that should occur as seaweeds devote more of their mass to indigestible structural materials that make them tougher and more difficult to bite. Feeding patterns of molluscs (Steneck and Watling 1982) and sea urchins (Littler et al. 1983a, b) are somewhat supportive of this hypothesis. Assays with reef fishes have been more variable (Hay 1991a). Littler et al. (1983b) found patterns supporting the model. However, using a larger data set from multiple reefs, Hay (1984b) found that only the extreme ends of the morphological spectrum differed significantly in their susceptibility to herbivores. The model had limited predictive value in the central portion of the morphology-susceptibility spectrum (also see Lewis 1985). Both Hay (1984b) and Paul and Hay (1986) also found that many of the tougher or calcified seaweeds produced unusual secondary metabolites that could act as chemical defenses, thus potentially confounding the effects of chemical and morphological traits. A few studies have addressed directly the effects of algal morphology on susceptibility to herbivores. Steneck and Adey (1976) demonstrated that the encrusting coralline ¸ithophyllum congestum grew as a smooth crust on subtidal reef slopes where feeding by fishes was intense but produced upright branches when it grew on the edges of reef flats where herbivory by fishes was reduced. Production of upright branches allowed enhanced growth and reproduction but also increased susceptibility to parrotfishes, which precluded the upright morphology from the reef slope. Hay (1981b) found that clonal seaweeds like Halimeda, Dictyota, and ¸aurencia could occur as loose aggregations that grew rapidly but had increased susceptibility to herbivorous fishes and sea urchins, or they could occur as densely packed colonies of uprights that had lowered susceptibility to herbivores but also lower rates of growth due to increased self-shading and diffusion gradients. On reef areas most affected by herbivores, these species occurred as tightly packed colonies. On reef areas minimally affected by herbivores, they occurred as loosely arranged uprights that could grow more rapidly. One of the more dramatic examples of morphological shifts in response to herbivory was investigated by Lewis et al. (1987). They documented a striking morphological dichotomy for the brown seaweed Padina jamaicensis and demonstrated that the different forms were a direct result of spatial patterns in grazing by herbivorous fishes. In heavily grazed areas, Padina grew as an uncalcified turf of small, irregularly branched and prostrate axes that were tightly attached to the substratum by rhizoids produced on ventral portions of the thallus. Branches on this form of the alga terminated in a single apical meristem. On areas of the reef where herbivory was slight, Padina grew as a calcified, upright, and foliose blade with the entire margin of the blade being composed of meristematic cells (see Fig. 1 in Lewis et al. 1987). These two forms are so dissimilar that taxonomists initially placed the two forms in different genera (the turf form being designated as Dictyerpa, »aughniella, or Dilophus). When herbivorous fishes were excluded from heavily grazed portions of the reef, the uncalcified turf form started growing as the calcified upright form within 96 h. After a few weeks of herbivore exclusion, the upright form began overgrowing and killing reef corals. A series of transplant and caging experiments demonstrated that the upright form of Padina grew rapidly, reproduced, and was a superior competitor; however, it was highly susceptible to removal by herbivorous fishes. In contrast, the turf form could persist in areas of high herbivore impact, but it did not outcompete other reef species and was never observed to reproduce. These examples indicate that morphological plasticity helps seaweeds persist in areas that are heavily grazed but that the morphologies that resist herbivory entail a significant cost in terms of growth and reproduction. Calcification as a deterrent Calcification of seaweeds has generally been viewed as deterring herbivory by making seaweeds harder and more difficult to bite or by diminishing their nutritional value due to the addition of indigestible structuring materials (Littler and Littler 1980; Steneck 1983, 1986; Hay 1984b; Duffy and Hay 1990; Targett and Targett 1990; Duffy and Paul 1992; Pennings and Paul 1992; Pitlik and Paul 1997). These assumptions are consistent with the fact that CaCO -containing seaweeds are often relatively low 3 S70 preference foods for reef herbivores (Littler et al. 1983a,b; Hay 1984b; Paul and Hay 1986; Steneck 1988). However, although the increased hardness of the thallus undoubtedly prevents some herbivores from feeding on heavily calcified seaweeds (Steneck and Watling 1982), many reef herbivores (e.g., parrotfishes, sea urchins) can easily bite into calcified seaweeds, and several recent investigations indicate that the CaCO in seaweed thalli may actually 3 serve as a chemical, as well as a structural, deterrent (Hay et al. 1994; Schupp and Paul 1994, Meyer and Paul 1995; Pennings et al. 1996). Pennings and Paul (1992) developed methods for adding CaCO to artificial foods to test its effects on 3 herbivore feeding preferences. This method mimics the presence of CaCO in an algal food but does not increase 3 hardness. This methodology was modified by Hay et al. (1994) so that algal-based foods could be created that differed only in the presence of CaCO , not in food value 3 or toughness. Assays with gastropods, fishes, sea urchins, and amphipods indicated that CaCO could significantly 3 affect the feeding of some species of these herbivores, even when the CaCO was added in a way that had no effect on 3 the nutritional value or toughness of the food (Pennings and Paul 1992; Hay et al. 1994; Schupp and Paul 1994). The study by Schupp and Paul (1994) gave the clearest indication of what mechanisms might be operating to produce this effect. Adding CaCO to foods significantly 3 decreased the feeding rates of fishes with acidic digestive tracts, but stimulated, or did not affect, feeding by fishes with neutral or more basic guts (also see Hay et al. 1994; Meyer and Paul 1995; Pennings et al. 1996). These patterns suggest that CaCO may deter feeding for some 3 species because of the neutralizing effect that it would have in a low pH gut and possibly because of the large amount of CO that would be released. These findings do 2 not diminish the potential importance of CaCO in defend3 ing seaweeds by increasing their hardness (Pitlik and Paul 1997), but they do indicate that CaCO can also deter 3 herbivory in other ways, possibly by functioning as a chemical defense. Schupp and Paul (1994) suggested using the term mineral defense to distinguish this chemical effect from that of CaCO serving as a hardening agent or from 3 the chemical effects of bioactive secondary metabolites. Recent work also has demonstrated that the CaCO 3 contained in seaweeds need not lower their nutritional value as foods and that, in fact, the heavily calcified corallines may provide as much, or more, metabolizable plant mass per bite than most other macrophytes on the reef (ME Hay and QE Kappel in preparation). Most reef herbivores consume and process food on a volumetric basis (i.e., how much nutrition does a seaweed yield per bite, per mouthful or per gut full?). Viewing seaweed cross sections in a basic phycology text shows that many seaweeds are largely water rather than nutritious plant cytoplasm (e.g., the internal volume of many fleshy seaweeds largely comprises of water-filled medulary cells that have minimal nutritional content). In the calcified seaweeds, CaCO can simply replace water and thus need 3 not dilute the nutritional value of the plant per bite. Additionally, many calcified red seaweeds are composed of densely packed cells that are filled with organelles and storage products rather than water. We recently measured the ash-free-dry mass (AFDM) per volume of 40 species of seaweeds and found that heavily calcified seaweeds like Halimeda, Penicillus, Amphiroa, and Neogoniolithon could contain 0.6 to 5.6 times as much AFDM per volume as fleshy seaweeds like ¸aurencia, Acanthophora, Gracilaria, or Dictyota. Most investigators might have assumed that the fleshy species would have been more nutritious because of the absence of calcification. For the 40 species investigated, there was no significant difference in AFDM/volume between calcified and noncalcified seaweeds. Thus, incorporation of CaCO into algal thalli may not lower 3 the alga’s nutritional value to an herbivore, and ‘‘structural’’ traits like calcification can also be acting as chemical defenses. Given that both defensive metabolites and the digestive processes of consumers are sensitive to changes in gut pH, there is considerable potential for CaCO 3 to change gut pH in ways that alter digestive efficiency and affect the activities of algal secondary metabolites (Hay et al. 1994). Secondary metabolites as deterrents Investigations of how secondary metabolites produce among-species differences in susceptibility to consumers have provided insights into factors (a) driving ecological specialization (Hay 1992), (b) affecting population and community organization (Hay 1984b, 1991a; Morrison 1988; Hay and Fenical 1996), (c) determining herbivore feeding patterns and digestive efficiencies (Horn 1989; Hay 1991a; Pennings and Paul 1992; Targett et al. 1995; Lindquist and Hay 1995; Paul 1997), and (d) producing parallels and contrasts between marine and terrestrial communities (Hay 1991b; Hay and Steinberg 1992). An increased understanding of seaweed chemical defenses thus provides insights into a wide range of ecological and evolutionary topics. Because herbivory in tropical marine systems is so intense and because these systems are often more experimentally tractable and less disturbed than terrestrial systems, it has been possible to identify the most ecologically important herbivores that should be used in laboratory bioassays or to test compounds in the field to determine their effectiveness against the diverse assemblage of herbivores that occur there (reviewed by Hay and Steinberg 1992). Thus, marine investigators can apply pure metabolites at natural concentrations to otherwise palatable organisms or can imbed the metabolites in experimental foods placed on natural reefs and determine in a very short period of time whether or not the compounds decrease herbivory under natural field conditions (Hay et al. 1987b; Hay 1991a; Hay and Steinberg 1992; Paul 1992). This ability to assay secondary metabolites under field conditions on remote reefs where the densities and diversities of herbivores have been minimally affected by humans is relatively unique to marine systems. In this respect, marine investigators have some advantage over terrestrial ecologists. Field bioassays of plant chemical defenses have rarely been conducted in terrestrial communities. Additionally, the tremendous changes in abundance of terrestrial herbivores resulting from the Pleistocene extinctions, agricultural practices, deforestation, and other S71 anthropogenic alterations to terrestrial communities make it difficult to determine which types of herbivores would have been most likely to have affected the evolution of defenses in present-day plants. It is possible that the tremendous focus on chemical-mediation of plant-insect interactions in terrestrial systems is actually the study of how compounds that evolved in response to 50 million years of feeding by megaherbivores serendipitously affect herbivorous insects now that the larger herbivores are absent (Crawley 1989; Hay and Steinberg 1992). Coral reefs provide a less disturbed evolutionary setting in which to place chemically mediated plant-herbivore interactions. In the last decade, a large number of investigations have demonstrated that many seaweed secondary metabolites strongly deter feeding by reef herbivores under both field and laboratory conditions (for reviews, see Paul and Fenical 1987; Hay and Fenical 1988, 1992, 1996; Van Alstyne and Paul 1988; Duffy and Hay 1990; Hay 1991a, 1996; Hay and Steinberg 1992; Paul 1992). Most of the common macrophytes on coral reefs (i.e., Halimeda, Penicillus, ºdotea, Caulerpa, Chlorodesmis, ¸aurencia, Ochtoides, Dictyota, Stypopodium, etc.) produce lipid-soluble chemical defenses that deter feeding by reef herbivores. Thus, a large number of diverse seaweed secondary metabolites deter herbivores; however, there can be considerable variability in the effects of a given compound on different herbivores or of related compounds on a single species of herbivore (see Hay and Steinberg 1992; Schupp and Paul 1994). Reviews on the particulars of seaweed chemical defenses have become a growth industry. Rather than repeat this information I will focus on the general ecological patterns emerging from studies of seaweed chemical defenses. Chemical structure and ecological function The biological effects of different chemical defenses are often generalized on the basis of structural class alone. As an example, tannins have been called nontoxic digestibility reducers whereas alkaloids and other small organic molecules have been called toxins (Feeny 1976). Presumably because similar types of compounds function in similar ways, investigators often measured ‘‘total’’ plant defenses (e.g., total phenolics) without establishing which specific compounds were present and often without demonstrating that any particular compound, or even the crude chemical extract, had any deterrent effect on herbivores (see Hay and Steinberg 1992; Hay 1996 for a discussion of problems associated with this approach). These types of generalizations are invalid because effects of seaweed secondary metabolites are unique to specific metabolites and herbivores (Hay and Fenical 1988; Hay and Steinberg 1992; Hay 1996; Paul 1997). Although many seaweed secondary metabolites are broad-spectrum feeding deterrents, several have no known effects against herbivores, and few, if any, deter all herbivores. Because minute changes in chemical structure may drastically modify the deterrent properties of compounds, generalizations about compound functions are misleading. As an example, brown algae in the order Dictyotales produce a family of structurally similar diterpenes called dictyols. Pachydictyol-A, dictyol-E, and dictyol-B are three examples. Pachydictyol-A differs from the others by the replacement of an OH by hydrogen; dictyol-E and dictyol-B differ only in the position of the additional OH. Although these compounds are very similar structurally, dictyol-E either stimulates or does not affect feeding by Caribbean and Pacific reef fishes, whereas the other compounds are significant deterrents (Hay and Steinberg 1992). Similar patterns are also apparent in tests against other types of herbivores. Variation in the effects of particular compounds on different herbivores and of structurally similar compounds on particular herbivores appears to be the rule rather than the exception (Hay 1991b; Paul 1992; Hay and Steinberg 1992; Paul 1997). However, compounds produced by many reef seaweeds significantly suppress feeding when they are tested in the field against the diverse groups of herbivores on coral reefs (Hay et al. 1987b; Hay 1991a; Paul 1992). These compounds clearly increase survivorship for the seaweeds. Integrated pest management Although seaweed secondary metabolites have strong demonstrable effects on herbivore feeding preferences, they do not act in isolation from other plant traits or from the environmental context in which seaweed-herbivore interactions occur (Cronin and Hay 1996b; Hay 1996). The role of seaweed chemical defenses will not be adequately understood until we appreciate the full range of defenses that seaweeds use and how these defenses are integrated and altered under different circumstances. Few investigators have simultaneously manipulated multiple defenses or varied defensive traits along with prey nutritional quality to assess how multiple defenses may work in concert to affect algal susceptibility to consumers. When Duffy and Paul (1992) evaluated how marine secondary metabolites affected feeding by reef fishes using foods that differed in their ratios of protein to carbohydrate, they found that some compounds were effective at defending low protein foods but ineffective at defending higher protein foods. Hay et al. (1994) noted a similar pattern when they varied algal concentrations in agarbased foods being consumed by a sea urchin. Paul and coworkers have also documented numerous instances in which seaweeds with both chemical and CaCO defenses 3 deterred a broad spectrum of reef fishes. Parrotfishes generally were deterred by the chemical but not the CaCO , defenses, while surgeonfishes were deterred by the 3 CaCO but not the chemicals (Schupp and Paul 1994; 3 Meyer and Paul 1995; Pennings et al. 1996; Paul 1997). The combination of traits provides protection against a broader range of herbivores than would be provided by either trait in isolation. The defensive value of secondary metabolites in seaweeds of variable nutritional quality should change as a function of how compounds affect herbivores. If a compound strongly suppresses survivorship or reproduction, then consumers should avoid the compound regardless of the nutritional value of the seaweed producing it. However, if a compound lowers growth rate or digestive S72 efficiency rather than survivorship or fecundity, then an herbivore might choose a defended but high quality alga over an undefended but lower quality alga because the herbivore’s net income from the defended but nutritionally rich alga could be higher. These possibilities have rarely been assessed, but the demonstrations that deterrent secondary metabolites have variable effects when applied to foods of differing nutritional quality (Duffy and Paul 1992; Hay at al. 1994) suggest that this interaction should be evaluated more closely. Chemically defended seaweeds commonly produce multiple secondary metabolites that could interact to produce synergistic or additive effects. Investigations are needed on the interactive effects of multiple metabolites; however, the very limited studies done to date have rarely found synergistic interactions among secondary metabolites. As an example, when Lumbang and Paul (1996) tested multiple brominated sesquiterpenes produced by the green alga Neomeris annulata against two reef fishes and a sea urchin, they found that each compound was significantly deterrent at or below its natural concentration and that all of the compounds together were not more deterrent than each alone. More studies like this will be needed before the potential effects of interacting metabolites can be evaluated. Several studies have indicated that chemical and mineral defenses (i.e., CaCO ) commonly co-occur in marine 3 plants and can function either additively or synergistically to reduce susceptibility to consumers (Hay et al. 1994; Schupp and Paul 1994; Meyer and Paul 1995). As an example, the green alga Halimeda goreauii contains both an unusual secondary metabolite and a heavily calcified thallus. When sea urchins and a nutritionally valuable food were used to test the effects of the metabolite alone or of CaCO alone, neither trait had any deterrent effect; 3 when these traits were combined, they interacted synergistically to strongly suppress feeding (Hay et al. 1994). This interaction changed when the experiment was repeated using a food of lower quality, indicating that food value, CaCO , and secondary metabolites were interacting to 3 affect sea urchin food choice. Several species of Halimeda also appear to substitute mineral for chemical defenses as plant segments mature and change their nutritional value and thus attractiveness to herbivores. Halimeda produces its new segments at night while herbivorous fishes are inactive. The new segments are uncalcified and more nutritious than older segments, but they are also defended by higher concentrations of more potent feeding deterrents (Hay et al. 1988a; Paul and Van Alstyne 1988a). As the new segments calcify during the first day following their production, they become more heavily invested with CaCO , less nutritious, 3 and the concentration of chemical defenses decrease. These examples demonstrate that seaweed defenses will not be adequately understood unless they are viewed as suites of interacting characteristics. Induction of chemical defenses The production of chemical defenses is hypothesized to be costly because defenses utilize resources that could have been allocated to growth or reproduction (Herms and Mattson 1992). Constitutive defenses require expenditure of resources even when herbivores are absent and the benefits of protection are not realized. In contrast, inducible defenses allow costs to be delayed until herbivores have been detected. Induced resistance may therefore minimize costs by keeping defenses low until they are needed (Harvell 1990; Baldwin 1994). For some seaweeds, the pattern of variation in secondary metabolites suggests that herbivore-induced increases of chemical defenses may be responsible for some intraspecific variation in concentrations of secondary metabolites. For example, seaweeds from areas of coral reefs where herbivory is intense often produce more potent and higher concentrations of chemical defenses than plants from habitats where herbivory is less intense (Paul and Fenical 1986; Paul and Van Alstyne 1988a). However, in the green seaweeds Halimeda, ºdotea, and Caulerpa that show this pattern, clipping experiments failed to induce increased terpenoid chemical defenses (Paul and Van Alstyne 1992). Clipping or sea urchin grazing of temperate seaweeds also failed to induce higher levels of phlorotannins in the kelps Ecklonia and Alaria or in the rockweed Sargassum (Pfister 1992; Steinberg 1994, 1995). Thus, the higher levels of constitutive chemical defenses from sites with many herbivores could have been generated by preferential grazing that removed the more susceptible individuals, founder effects, local selection, or among-habitat differences in other variables. Additionally, for some of the siphonous green seaweeds studied by Paul and Van Alstyne (1992), weakly deterrent metabolites stored in the alga were immediately converted to more strongly deterrent metabolites if the alga was damaged by crushing or cutting it. To distinguish this rapid enzymatic conversion of available metabolites from the classic notion of induction, Paul and Van Alstyne termed this process, ‘‘activation.’’ There are two documented examples of herbivores inducing chemical defenses in seaweeds (Van Alstyne 1988; Cronin and Hay 1996c). In contrast, there are many examples of inducible chemical defenses in the terrestrial literature (Baldwin 1994 and references therein). This discrepancy between marine and terrestrial systems could be due to the construction of vascular terrestrial plants versus non-vascular seaweeds (e.g., the induction stimulus from localized damage may not be efficiently translocated in seaweeds, see Cronin and Hay 1996a); but lack of research on seaweeds relative to terrestrial plants may also explain the disparity. Furthermore, most terrestrial investigations of induction have focused on insect grazing, while most marine investigations have focused on larger herbivores such as fishes and sea urchins rather than on mesograzers such as amphipods that may be more ecologically similar to insects (Hay et al. 1987a; Hay and Steinberg 1992). Mesograzers have been considered to be less important than larger herbivores because of the perception that they remove little seaweed biomass relative to the larger herbivores (see the debate among Bell 1991; Duffy and Hay 1991b; Brawley 1992). Ignoring mesograzers as potential inducers of seaweed chemical defenses is inappropriate. The two clear S73 examples of induction in seaweeds (Van Alstyne 1988; Cronin and Hay 1996c) both involve mesograzers (a snail and an amphipod), each of which could graze for long periods on a plant without killing it and could thus be affected by a defense that took days, or weeks, to induce. In contrast, fishes and sea urchins are large relative to many seaweeds and are often capable of rapidly killing a plant that they find palatable. Thus, to avoid being killed by these larger more mobile herbivores, plants may need to be constantly defended rather than inducing defenses following attack. For many chemically defended seaweeds and invertebrates, low concentrations of chemical defenses are generally effective deterrents against fishes and sea urchins but are less effective or may even stimulate feeding by mesograzers (Hay et al. 1987a, 1988b, 1989, 1990a,b; Hay 1991b, 1992, 1996; Van Alstyne and Paul 1992; Duffy and Hay 1991a, 1994). I suggest that it is the smaller, less mobile mesograzers that will cue induction of chemical defenses in seaweeds. These types of herbivores feed over temporal and spatial scales that would allow induced responses to be beneficial to seaweeds, and it is the mesograzers that often are not deterred by chemical defenses until the metabolites are induced to higher levels (Cronin and Hay 1996c; Hay 1996). It is therefore possible that induction in seaweeds has appeared uncommon, because it rarely occurs in response to clipping or grazing by larger herbivores but occurs more often in response to mesograzer feeding. There are too few studies of chemical induction to adequately evaluate the relative importance of large mobile versus small sedentary herbivores in inducing seaweed chemical defenses. However, the results of Cronin and Hay (1996c) illustrate that mesograzer feeding can cause induction. These authors noted spatial and temporal patterns of amphipod abundance, algal defensive chemistry, and algal palatability that suggested that the brown seaweed Dictyota menstrualis was inducing terpenoid chemical defenses in response to amphipod feeding. When Dictyota plants were split and grown in the field for 2—3 weeks with one half of each plant periodically subjected to amphipod grazing and the other half not grazed, plant halves attacked by amphipods produced higher levels of defensive compounds and became less susceptible to amphipod grazing. This lowered susceptibility to amphipods resulted from induction of defensive compounds in attacked plants rather than from alterations in plant nutritional content or from previous grazers selectively removing the least defended tissues and thus leaving more chemically rich tissues. The among-site differences in palatability and concentrations of chemical defenses occurred in years when amphipods were abundant but not in years when they were rare. Thus, both spatial and temporal variance in palatability may have been generated by induced defenses following attack by amphipods. Preliminary experiments suggest that induction in response to mesograzer feeding also occurs in other seaweeds (discussed in Hay 1996). These examples indicate that seaweed chemical defenses can be allocated in complex ways that may vary with time, other defenses, nutritional state of the alga, and history of previous attack. Marine chemical ecologists have recently focused more attention on trying to understand seaweed defenses within these broader, more ecologically realistic, and more holistic contexts. These efforts are well founded and need to continue. Cascading effects of seaweed chemical defenses The tremendous feeding activity of reef herbivores makes seaweed chemical defenses especially important on tropical coral reefs (Bolser and Hay 1996). In areas where generalist consumers feed intensively, small mesograzers like amphipods and polychaetes that use plants as both food and habitat could be consumed incidentally if they lived on plants that were preferred by fishes. Therefore, it has been hypothesized that selection should favor sedentary mesograzers that can live on and eat seaweeds that are chemically defended from fishes because these seaweeds can provide mesograzers with safe sites from both direct and incidental consumption (Hay et al. 1987a, 1988b; Hay 1992). Initial tests of this hypothesis in the temperate Atlantic found that the tube-building amphipod Amphithoe longimana and the tube-building polychaete Platynereis dumerilii both minimized contact with fishes by selectively living on and consuming the brown alga Dictyota menstrualis, which produced diterpene alcohols that deterred fish feeding but that had little effect on feeding by the amphipod or polychaete (Hay et al. 1987a, 1988b; Duffy and Hay 1991a, 1994). In seasons when fishes were common, amphipod species that could not tolerate algal chemical defenses became locally extinct while the amphipod Amphithoe longimana remained abundant because it used a defended alga as a safe site from fish predation (Duffy and Hay 1991a, 1994). The hypothesis that small sedentary consumers could minimize predation by associating with, or specializing on, toxic hosts was tested more broadly using amphipods, crabs, and molluscs that live on chemically defended seaweeds in the Caribbean or tropical Pacific (Hay et al. 1989, 1990a,b). In all of these cases, mesoconsumers were undeterred, or sometimes stimulated, by host compounds that deterred fish feeding. Additionally, mesograzers escaped or deterred predation through their association with these chemically rich hosts (Hay 1992). As one example (Hay et al. 1990a), the Caribbean amphipod Pseudamphithoides incurvaria lives in a mobile, bivalved domicile that it constructs from the chemically defended seaweed Dictyota bartayresii. The diterpene alcohol that causes fishes to reject the alga as food is the compound that cues domicile building by the amphipod. Amphipods in domiciles built from this alga are rejected as food by predatory fishes but are rapidly eaten if they are removed from their domiciles or if they are in domiciles that they have been forced to build from a seaweed that is not chemically defended. Although the amphipod cannot physiologically sequester its host’s chemical defenses, it achieves sequestration behaviorally by building its domicile from this defended alga. Herbivorous ascoglossans that feed selectively on chemically rich seaweeds, sequester the seaweed toxins, and use these in their own defense provide welldocumented examples of physiological sequestration of S74 host chemical defenses by mesoherbivores (Paul and Van Alstyne 1988b; Hay et al. 1989, 1990b; Hay 1992). These animals generally feed on noxious seaweeds in the order Caulerpales (e.g., Caulerpa, Halimeda, Avrainvillea, Chlorodesmis) and concentrate the algae’s chemical defenses until they comprise as much as 3—8% of the gastropod’s dry mass (Paul and Van Alstyne 1988b; Hay et al. 1990b). Concentrations of these compounds in the seaweeds rarely exceed about 1% of plant dry mass. Sequestered compounds serve to defend both the adult animal and its egg masses, which are placed on the surface of its host plant. A taxonomically diverse assemblage of specialized mesograzers escape or deter their consumers by living on, feeding from, and, in some cases, morphologically mimicking or sequestering defensive compounds from their toxic hosts (see Hay 1992; Hay and Steinberg 1992; Paul 1992; Hay 1996). These compounds are known to be deployed in defense of ascoglossan egg masses (Paul and Van Alstyne 1988b). They might also be passed on to larvae, as occurs for other groups of chemically defended invertebrates (Lindquist and Hay 1996). In most instances, mesograzers showing strong preferences for particular plant species appear to be functioning simply as herbivores. However, a few of the mesograzers on encrusting corallines play a mutualistic role, sometimes despite their direct feeding on the host. Littler et al. (1995) demonstrated that about 50% of the diet of the herbivorous chiton Choneplax lata consisted of its preferred host coralline, Porolithon pachydermum. However, if this herbivore was removed from its host, the host became fouled by other algae, and these algae attracted parrotfishes that fed on both the palatable epiphytes and the coralline host (termed ‘‘shared doom’’ by Wahl and Hay 1995). The deep bites of the parrotfish caused more damage to the coralline host than had been done by the chiton. Thus, removal of the herbivorous chiton increased, rather than decreased, grazing on the coralline. Stachowicz and Hay (1996) found a somewhat similar mutualistic association between an herbivorous crab and the branched coralline Neogoniolithon. When the crab was removed from this structurally complex coralline, the crab was quickly eaten by fishes. Without the grazing activity of the crab, the coralline was rapidly overgrown by other seaweeds. As with mesograzers, palatable seaweeds that are usually driven to local extinction by herbivores can sometimes persist in herbivore-rich communities if they grow on or beneath their herbivore resistant competitors (Hay 1986; Littler et al. 1986; Wahl and Hay 1995). As an example, numerous species of palatable seaweeds are significantly more common near the base of the chemically defended seaweed Stypopodium zonale than several centimeters away; if the deterrent plant is removed, these more palatable species are rapidly eaten (Littler et al. 1986). When plastic mimics of Stypopodium are placed in the field, they also provide a partial refuge for palatable species, but they are less effective than the real plants, suggesting that associational refuges are generated in part by the physical presence of a non-food plant, but that the plant’s chemical repugnance makes the associational refuge more effective. These associational refuges can significantly increase the numbers of species co-existing in a community, and under some circumstances, a seaweed can be completely dependent on its major competitor to keep it from being driven to local extinction by consumers (Hay 1986; Hay and Fenical 1996). In addition juvenile stages of many reef invertebrates and some fishes escape predators by using well defended seaweeds as protective nursery habitats (reviewed by Hay 1997). Conclusions Although seaweeds are not commonly studied by coral reef ecologists, they are exceptionally productive experimental tools. Manipulations using seaweeds have provided a wealth of information on processes affecting population and community structure on coral reefs. Studies on corals and sponges parallel those for seaweeds, suggesting that seaweed studies may provide a template for understanding processes affecting a broad variety of reef organisms. Herbivorous fishes and sea urchins have a profound effect on the distribution, abundance, and species richness of coral reef seaweeds, which are the potential competitive dominants on tropical reefs. When overfishing or natural disturbances remove too many of these herbivores, seaweeds can overgrow and kill other species, prevent recruitment of invertebrate larvae, and destroy coral reefs as we know them. To cope with the intense feeding of herbivores, reef seaweeds have developed complex suites of chemical, mineral, morphological, structural, and nutritional traits that diminish susceptibility to fishes and sea urchins. By their mere presence, seaweeds that deter these large herbivores create microsites of lowered consumer activity. Defended seaweeds thus become safe sites for small, less mobile mesograzers, for juveniles of several species of reef invertebrates and fishes, and for more palatable seaweeds that may be dependent upon their unpalatable competitors to prevent their local extinction due to herbivory. Seaweed defenses thus produce substantial cascading effects that alter reef community organization and species richness. Acknowledgements. This manuscript benefited from NSF grant OCE 95—29784 and from comments by P Hay, V Paul, and R Steneck. References Baldwin IT (1994) Chemical changes rapidly induced by folivory. In: Bernays EA (ed) Insect-plant interactions, vol 5. CRC Press, Boca Raton, pp 1—23 Bell SS (1991) Amphipods as insect equivalents? an alternative view. Ecology 72:350—354 Birkeland C (1989) The influence of echinoderms on coral reef communities. In: Jangoux M, Laurence JM (eds) Echinoderm studies, vol 3. Balkema, Rotterdam, pp 1—79 Bolser RC, Hay ME (1996) Are tropical plants better defended? palatability and defenses of temperate versus tropical seaweeds. Ecology 77:2269—2286 Brawley SH (1992) Mesoherbivores. In: John DM, Hawkins SS, Price JH (eds) Plant-animal interactions in the marine benthos. Systematics Association Special Volume, Clarendon Press, Oxford, pp 235—264 Carpenter RC (1986) Partitioning herbivory and its effects on coral reef algal communities. Ecol Monogr 56:345—36 S75 Carpenter RC (1988) Mass mortality of a Caribbean sea urchin: immediate effects on community metabolism and other herbivores. Proc Natl Acad Sci USA 85:511—514 Carpenter RC (1990) Mass mortality of Diadema antillarum II. Effects on population densities and grazing intensity of parrotfishes and surgeonfishes. Mar Biol 104:79—86 Coen LD (1988) Herbivory by crabs and the control of algal epibionts on Caribbean host corals. Oecologia 75:198—203 Crawley MJ (1989) The relative importance of vertebrate and invertebrate herbivores in plant population dynamics. In: Bernays EA (ed) Insect—plant interactions, vol 1. CRC Press, Boca Raton, pp 45—71 Cronin G, Hay ME (1996a) Within-plant variance in seaweed chemical defenses: Optimal defense theory versus the growth-differentiation balance hypothesis. Oecologia 105:361—368 Cronin G, Hay ME (1996b) Susceptibility to herbivores depends on recent history of both the plant and animal. Ecology 77:1531—1543 Cronin G, Hay ME (1996c) Amphipod grazing and induction of seaweed chemical defenses. Ecology 77:2287—2301 Duffy JE, Hay ME (1990) Seaweed adaptations to herbivory. BioScience 40:368—375 Duffy JE, Hay ME (1991a) Food and shelter as determinants of food choice in an herbivorous marine amphipod. Ecology 72:1286—1298 Duffy JE, Hay ME (1991b) Not all amphipods are created equal: a reply to Bell. Ecology 72:354—358 Duffy JE, Hay ME (1994) Herbivore resistance to seaweed chemical defense: the roles of herbivore mobility and predation risk. Ecology 75:1304—1319 Duffy JE, Paul VJ (1992) Prey nutritional quality and the effectiveness of chemical defenses against tropical reef fishes. Oecologia 90:333—339 Dunlap M, Pawlik JR (1996) Video-monitored predation by Caribbean reef fishes on an array of reef and mangrove sponges. Mar Biol 126:117—123 Feeny P (1976) Plant apparency and chemical defense. Recent Adv Phytochem 10: 1— 40 Fox LR (1981) Defense and dynamics in plant-herbivore systems. Am Zool 21:853—864 Harvell CD (1990) The ecology and evolution of inducible defenses. Rev Biol 65:323—340 Hatcher BG (1981) The interaction between grazing organisms and the epilithic algal community of a coral reef: a quantitative assessment. Proc 4th Int Coral Reef Congr 2:515—524 Hatcher BG, Larkum AWD (1983) An experimental analysis of factors controlling the standing crop of the epi-lithic algal community on a coral reef. J Exp Mar Biol Ecol 69:61—84 Hay ME (1981a) Herbivory, algal distribution, and the maintenance of between-habitat diversity on a tropical fringing reef. Am Nat 118:520—540 Hay ME (1981b) The functional morphology of turf forming seaweeds: persistence in stressful marine habitats. Ecology 62:739—750 Hay ME (1984a) Patterns of fish and urchin grazing on Caribbean coral reefs: are previous results typical? Ecology 65:446—454 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 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 (1991a) Fish-seaweed interactions on coral reefs: effects of herbivorous fishes and adaptations of their prey. In: Sale PF (ed) The ecology of coral reef fishes. Academic Press, New York, pp 96—119 Hay ME (1991b) Marine-terrestrial contrasts in the ecology of plant chemical defenses against herbivores. Trends Ecol Evolut 6:362—365 Hay ME (1992) Seaweed chemical defenses: their role in the evolution of feeding specialization and in mediating complex interactions. In: Paul VJ (ed) Ecological roles for marine secondary metabolites; explorations in chemical ecology series. Comstock Publishing Associates, Ithaca, pp 93—118 Hay ME (1996) Marine chemical ecology: what is known and what is next? J Exp Mar Biol Ecol 200:103—139 Hay ME (1997) Calcified seaweeds on coral reefs: complex defenses, trophic relationships, and value as habitat. Proc 8th Int Coral Reef Symp (in press) Hay ME, Fenical W (1988) Marine plant-herbivore interactions: the ecology of chemical defense. Annu Rev Ecol Syst 19:111—145 Hay ME, Fenical W (1992) Chemical mediation of seaweed-herbivore interactions. In: John DM, Hawkins SS, Price JH (eds) Plant-animal interactions in the marine benthos. Systematics Association Special Volume, Clarendon Press, Oxford, pp 319—337 Hay ME, Fenical W (1996) Chemical ecology and marine biodiversity: insights and products from the sea. Oceanography 9:10—20 Hay ME, Steinberg PD (1992) The chemical ecology of plantherbivore interactions in marine versus terrestrial communities. In: Rosenthal J, Berenbaum M (eds) Herbivores: their interaction with secondary metabolites, evolutionary and ecological processes. Academic Press, San Diego, pp 371—413 Hay ME, Taylor PR (1985) Competition between herbivorous fish and urchins on Caribbean reefs. Oecologia 65:591—598 Hay ME, Colburn T, Downing T (1983) Spatial and temporal patterns in herbivory on a Caribbean fringing reef: the effect on plant distribution. Oecologia 58:299 — 308 Hay ME, Duffy JE, Pfister C, Fenical W (1987a) Chemical defense against different marine herbivores: are amphipods insect equivalents? Ecology 68:1567—1580 Hay ME, Fenical W, Gustafson K (1987b) Chemical defense against diverse coral reef herbivores. Ecology 68:1581—1591 Hay ME, Paul VJ, Lewis SM, Gustafson K, Tucker J, Trindell RN (1988a) Can tropical seaweeds reduce herbivory by growing at night? Diel patterns of growth, nitrogen content, herbivory, and chemical versus morphological defenses. Oecologia 75:233—245 Hay ME, Renaud PE, Fenical W (1988b) Large mobile versus small sedentary herbivores and their resistance to seaweed chemical defenses. Oecologia 75:246—252 Hay ME, Pawlik JR, Duffy JE, Fenical W (1989) Seaweed-herbivore-predator interactions: host-plant specialization reduces predation on small herbivores. Oecologia 81:418—427 Hay ME, Duffy JE, Fenical W (1990a) Host-plant specialization decreases predation on a marine amphipod: an herbivore in plant’s clothing. Ecology 71:733—743 Hay ME, Duffy JE, Paul VJ, Renaud PE, Fenical W (1990b) Specialist herbivores reduce their susceptibility to predation by feeding on the chemically-defended seaweed Avrainvillea longicaulis. Limnol Oceanogr 35:1734—1743 Hay ME, Kappel QE, Fenical W (1994) Synergisms in plant defenses against herbivores: interactions of chemistry, calcification, and plant quality. Ecology 75:1714—1726 Herms DA, Mattson WJ (1992) The dilemma of plants: to grow or defend. Rev Biol 67:283—335 Hixon MA, Brostoff WN (1996) Succession and herbivory: effects of differential fish grazing on Hawaiian coral-reef algae. Ecology 66:67—90 Horn MH (1989) Biology of marine herbivorous fishes. Oceanogr Mar Biol Annu Rev 27:167—272 Hughes TP (1994) Catastrophes, phase shifts, and large-scale degradation of a coral reef. Science 256:1547—1551 Klumpp DW, Polunin NVC (1989) Partitioning among grazers of food resources within damselfish territories on a coral reef. J Exp Mar Biol Ecol 125:145—169 Klumpp DW, Pulfrich A (1989) Trophic significance of herbivorous macroinvertebrates on the central Great Barrier Reef. Coral Reefs 8:135—144 Lessios HA (1988) Mass mortality of Diadema antillarum in the Caribbean: what have we learned? Annu Rev Ecol Syst 19:371—393 S76 Lewis SM (1985) Herbivory on coral reefs: algal susceptibility to herbivorous fishes. Oecologia 65:370—375 Lewis SM (1986) The role of herbivorous fishes in the organization of a Caribbean reef community. Ecol Monogr 56:183—200 Lewis SM, Norris JN, Searles RB (1987) The regulation of morphological plasticity in tropical reef algae by herbivory. Ecology 68:636—641 Lindquist N, Hay ME (1995) Can small rare prey be chemically defended? The case for marine larvae. Ecology 76:1347—1358 Lindquist N, Hay ME (1996) Palatability and chemical defenses of marine invertebrate larvae. Ecol Monogr 66:431—450 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 Littler MM, Littler DS (1984) Models of tropical reef biogenesis: the contribution of algae. Progr Phycol Res 3:323—364 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 Littler MM, Taylor PR, Littler DS (1983b) Algal resistance to herbivory on a Caribbean barrier reef. Coral Reefs 2:111—118 Littler MM, Taylor PR, Littler DS (1986) Plant defense associations in the marine environment. Coral Reefs 5:63—71 Littler MM, Taylor PR, Littler DS (1989) Complex interactions in the control of coral zonation on a Caribbean reef flat. Oecologia 80:331—340 Littler MM, Littler DS, Taylor PR (1995) Selective herbivore increases biomass of its prey: a chiton-coralline reef-building association. Ecology 76:1666—1681 Lubchenco J, Gaines SD (1981) A unified approach to marine plant-herbivore interactions: I. Populations and communities. Annu Rev Ecol Syst 12:405—437 Lumbang WA, Paul VJ (1996) Chemical defense of the tropical green seaweed Neomeris annulata Dickie: effects of multiple compounds on feeding by herbivores. J Exp Mar Biol Ecol 201:185—195 Mattson WJ (1980) Herbivory in relation to plant nitrogen. Annu Rev Ecol Syst 11:119—161 McClanahan TR, Shafir SH (1990) Causes and consequences of sea urchin abundance and diversity in Kenyan coral reef lagoons. Oecologia 83:362—370 Meyer KD, Paul VJ (1995) Variation in secondary metabolite and aragonite concentrations in the tropical green seaweed Neomeris annulata: effects on herbivory by fishes. Mar Biol 122:537—545 Morrison D (1988) Comparing fish and urchin grazing in shallow and deeper coral reef algal communities. Ecology 69:1367—1382 Paul VJ (1992) Seaweed chemical defenses on coral reefs. In: Paul VJ (ed) Ecological roles of marine natural products. Comstock Publishing, Ithaca, New York, pp 24—50 Paul VJ (1997) Secondary metabolites and calcium carbonate as defenses of calcareous algae on coral reefs. Proc 8th Int Coral Reef Symp (in press) Paul VJ, Fenical W (1986) Chemical defense in tropical green algae, order Caulerpales. Mar Ecol Prog Ser 34:255—264 Paul VJ, Fenical W (1987) Natural products chemistry and chemical defense in tropical marine algae of the phylum Chlorophyta. Bioorg Mar Chem 1:1—29 Paul VJ, Hay ME (1986) Seaweed susceptibility to herbivory: chemical and morphological correlates. Mar Ecol Prog Ser 33:255—264 Paul VJ, Van Alstyne KL (1988a) Chemical defense and chemical variation in some tropical Pacific species of Halimeda (Halimedaceae; Chlorophyta). Coral Reefs 6:263—270 Paul VJ, Van Alstyne KL (1988b) The use of ingested algal diterpenoids by the ascoglossan opisthobranch Elysia halimedae Macnae as antipredator defenses. J Exp Mar Biol Ecol 119:15—29 Paul VJ, Van Alstyne KL (1992) Activation of chemical defenses in the tropical green algae Halimeda spp. J Exp Mar Biol Ecol 160:191—203 Pennings SC, Paul VJ (1992) Effect of plant toughness, calcification, and chemistry on herbivory by Dolabella auricularia. Ecology 3:1606—1619 Pennings SC, Puglisi MP, Pitlik TJ, Himaya AC, Paul VJ (1996) Effects of secondary metabolites and CaCO on feeding by 3 surgeonfishes and parrotfishes: within-plant comparisons. Mar Ecol Prog Ser 134:49—58 Pfister CA (1992) Costs of reproduction in an intertidal kelp: patterns of allocation and life history consequences. Ecology 73:1586—1596 Pitlik TJ, Paul VJ (1997) Effects of toughness, calcite level, and chemistry of crustose coralline algae (Rhodophyta:Corallineales) on grazing by the parrotfish Chlorurus sordidus. Proc 8th Int Coral Reef Symp (in press) Randall JE (1965) Grazing effect on seagrasses by herbivorous reef fishes in the West Indies. Ecology 46:255—260 Schmitt TM, Hay ME, Lindquist N (1995) Constraints on chemically-mediated coevolution: multiple functions for seaweed secondary metabolites. Ecology 76:107—123 Schupp PJ, Paul VJ (1994) Calcification and secondary metabolites in tropical seaweeds: variable effects on herbivorous fishes. Ecology 75:1172—1185 Stachowicz JJ, Hay ME (1996) Facultative mutualism between an herbivorous crab and a coralline alga: advantages of eating noxious seaweeds. Oecologia 105:377—387 Steinberg PD (1994) Lack of short-term induction of phlorotannins in the brown algae Ecklonia radiata and Sargassum vestitum. Mar Ecol Prog Ser 112:129—133 Steinberg PD (1995) Interaction between the canopy dwelling echinoid Holopneustes purpurescens and its host kelp Ecklonia radiata. Mar Ecol Prog Ser 127:169—181 Steneck RS (1983) Escalating herbivory and resulting adaptive trends in calcareous algal crusts. Paleobiology 9:44—61 Steneck RS (1986) The ecology of coralline algal crusts. Annu Rev Ecol Syst 17:273—303 Steneck RS (1988) Herbivory on coral reefs: a synthesis. Proc 6th Int Coral Reef Symp 1:37—49 Steneck RS (1997) Crustose corallines, other algal functional groups, and herbivores: complex interactions along reef productivity gradients. Proc 8th Int Coral Reef Symp (in press) Steneck RS, Adey WH (1976) The role of environment in control of morphology in ¸ithophyllum congestum, a Caribbean algal ridge builder. Bot Mar 19:197—215 Steneck RS, Dethier MN (1994) The structure of algal-dominated communities: a functional group approach. Oikos 69:476—498 Steneck RS, Watling L (1982) Feeding capabilities and limitations of herbivorous molluscs: a functional group approach. Mar Biol 68:299—319 Targett NM, Boettcher AA, Targett TE, Vrolijk NH (1995) Tropical marine herbivore assimilation of phenolic-rich plants. Oecologia 103:170—179 Targett TE, Targett NM (1990) Energetics of food selection by the herbivorous parrotfish Sparisoma radians: roles of assimilation efficiency, gut evacuation rate, and algal secondary metabolites. Mar Ecol Prog Ser 66:13—21 Van Alstyne KL (1988) Herbivore grazing increases polyphenolic defenses in the intertidal brown alga Fucus distichus. Ecology 69:655—663 Van Alstyne KL, Paul VJ (1988) The role of secondary metabolites in marine ecological interactions. Proc. 6th Int Coral Reef Symp 1:175—186 Wahl M, Hay ME (1995) Associational resistance and shared doom: effects of epibiosis on herbivory. Oecologia 102:329—340 .