227 Chemical Mediation of Macroalgal–Herbivore Interactions: Ecological and Evolutionary Perspectives Valerie J. Paul,* Edwin Cruz-Rivera, and Robert W. Thacker CONTENTS I. Diversity and Natural Products Chemistry of Marine Macroalgae 227 II. Marine Herbivores 232 A. Marine Benthic Herbivory and Herbivore Nutrition 232 B. Herbivore Diversity 234 C. Herbivore Size and Guilds 234 III. Chemically Mediated Interactions between Marine Macroalgae and Herbivores 236 A. Feeding-Deterrent Effects of Algal Secondary Metabolites 236 B. Physiological Effects of Algal Chemical Defenses 241 C. Intraspecific Variation in Secondary Metabolite Production 243 IV. Indirect Effects of Algal Chemistry: Associational Defenses, Mutualisms, and Shared Doom 246 V. Algal Chemical Defenses and Benthic Community Structure 247 VI. Conclusions 248 Acknowledgments 249 References 250 I. DIVERSITY AND NATURAL PRODUCTS CHEMISTRY OF MARINE MACROALGAE This chapter considers interactions between herbivores and benthic marine algae and seagrasses. It also discusses benthic cyanobacteria because many species are large, conspicuous, and common components of tropical communities, and recent studies suggest that their role is similar to that of true algae in coral reefs. The term “seaweeds” traditionally includes the macroscopic, multi- cellular, marine green, brown, and red algae; the benthic, filamentous blue-green algae are also sometimes considered. All seaweeds are unicellular at some stage of their life cycle (usually as spores or zygotes), and they are viewed as “primitive” photosynthetic organisms because of their simple construction and reproduction. There is a wide variation in algal classification among systematists, but the traditional divisions for algae are the Cyanobacteria (prokaryotic blue-green algae, sometimes termed Cyanophyta), Chlorophyta (green algae), Phaeophyta (brown algae), and * Corresponding author. 6 9064_ch06/fm Page 227 Tuesday, April 24, 2001 5:18 AM © 2001 by CRC Press LLC 228 Marine Chemical Ecology Rhodophyta (red algae). 1–3 The seagrasses are the only truly submerged angiosperms in the marine environment. Benthic algae are influenced by diverse biological and environmental factors such as herbivory, competition, light, temperature, salinity, water motion, and nutrient availability. 1,2 Variations in these parameters directly influence algal distribution and growth 1,2 and can indirectly affect algal susceptibility to herbivores by altering the nutrient or defensive chemical content of algae. 4 Fur- thermore, algae acquire nutrients from the water column rather than from roots, and they rely on the buoyancy of water, rather than stiff structural material or woody tissues, to float toward the surface and light. Thus, virtually all of the algal thallus is exposed to fouling by epiphytic micro- organisms, algae, and sessile invertebrates, and consumption by herbivores and other consumers (including humans). 1 Seaweeds have several mechanisms for tolerating or resisting herbivory, and these defensive strategies have been discussed previously. 4,5 Many seaweeds can deter herbivores by morphological, structural, and chemical defenses 6–9 or by associating with deterrent seaweeds or other benthic organisms that reduce herbivore foraging. 10–15 Structural defenses such as calcification and tough- ness are common in certain groups of green and red seaweeds and have been previously dis- cussed. 6,7,16–19 Chemical defenses of seaweeds have been recently reviewed 8,9,20–24 and will be discussed more thoroughly in this chapter. Often, several defensive mechanisms may be functioning simultaneously, 16,23, 25–31 and the importance of multiple defenses may be very significant in herbi- vore-rich tropical waters. The common co-occurrence of CaCO 3 and secondary metabolites in tropical seaweeds has been suggested to be adaptive because the high diversity of tropical herbivores limits the effectiveness of any single defense. 4,23–31 Multiple defenses could act additively or synergistically to reduce the ability of herbivores to adapt to seaweed defenses. For example, combinations of CaCO 3 and secondary metabolites have been tested as feeding deterrents, and both additive 28–31 and synergistic 27 effects of these combined defenses have been observed. Over 2400 natural products have been isolated from marine red, brown, and green algae, and the majority of these have come from tropical algae. 32 In general, these compounds occur in relatively low concentrations, ranging from 0.2% to 2% of algal dry mass, although compounds such as the polyphenolics in brown algae can occur at concentrations as high as 15% of algal dry mass. 8,33 Except for metabolites from phytoplankton and cyanobacteria (blue-green algae), very few nitrogenous compounds have been isolated from algae. 32,34 Some red algae, blue-green algae, and a few green algae incorporate halides from seawater into the organic compounds they pro- duce. 8,35,36 Bromine and chlorine are the most common halides found in marine algae. Halogenating enzymes such as bromoperoxidases and chloroperoxidases function in the biosynthesis of these halogenated compounds. 37 The majority of macroalgal compounds are terpenoids, especially sesqui- and diterpenoids. Acetogenins (acetate-derived metabolites) including unusual fatty acids constitute another common class of algal secondary metabolites. 34 Most of the remaining metabolites result from mixed biosynthesis and are often composed of terpenoid and aromatic portions. Blue-green algae (cyanobacteria) occur in a variety of marine benthic habitats, including rocky shores, sandy shores, and salt marshes. 38–40 Cyanobacteria are important in marine environments because they play a major role in nitrogen fixation, and they are important primary producers. 2 Their ability to fix nitrogen may explain their production of many nitrogen-containing secondary metabolites including peptides and lipopeptides. 41–43 In general, the ecological roles for cyanobac- terial compounds are poorly known; most studies have focused on their biomedical potential. 41–43 High abundances of Lyngbya spp. and Oscillatoria spp. have been observed on coral reefs, where benthic mats of these blue-green algae can cover thousands of square meters. 38,40,44 These benthic, filamentous cyanobacteria produce a wide variety of secondary metabolites, many of which are toxic or pharmacologically active. 41–45 Cyclic peptides and depsipeptides isolated from blue- green algae have recently been reviewed. 43 Members of the Oscillatoriaceae, especially strains of Lyngbya majuscula , have proven to be rich sources of natural products. Metabolites isolated from L. majuscula include (see Figure 6.1) malyngolide, a lipid metabolite with antibiotic activity; 46 9064_ch06/fm Page 228 Tuesday, April 24, 2001 5:18 AM © 2001 by CRC Press LLC Chemical Mediation of Macroalgal–Herbivore Interactions 229 FIGURE 6.1 Examples of secondary metabolites from marine cyanobacteria. O O OH Malyngolide NH N NH OH O CH 3 Lyngbyatoxin A N O NH OH NH O NHO NH O O OH NH NH NH NH NH NH O O O O O O Hormothamnin A NH O OOOCH 3 Malyngamide H N O OH O OCH 3 O CH 3 Cl Malyngamide I OCH 3 N S HH Curacin A N CH 3 CH 3 NH O H H N O CH 3 H NNH S N H O CH 3 O H O CH 3 O H Dolastatin 10 OH 9064_ch06/fm Page 229 Tuesday, April 24, 2001 5:18 AM © 2001 by CRC Press LLC 230 Marine Chemical Ecology lyngbyatoxin A, a cyclic depsipeptide that is a potent phorbol-ester-type tumor promoter; 47–49 curacin A, an antimitotic agent with potent brine shrimp toxicity; 50 and the lipopeptides malynga- mide H, 51 I, 52 J, K, and L, 53 which are toxic to brine shrimp and goldfish. Other species of marine blue-green algae also produce unusual secondary metabolites. Hor- mothamnin A, a cyclic peptide isolated from Hormothamnion enteromorphoides , (Nostocaceae) has both antibiotic and cytotoxic activity. 54,55 Several dolastatins and dolastatin analogs have recently been isolated from the marine cyanobacteria Symploca hydnoides , 56,57 Lyngbya majuscula , 58–60 and mixed cyanobacterial assemblages. 61 Dolastatins and dolastatin analogs are potent cytotoxins, three of which are currently in clinical evaluation as potential anticancer drugs. 62 Dolastatins were originally isolated from collections of the herbivorous sea hare Dolabella auricularia. 63–65 The discovery of dolastatins in blue-green algae suggests that their occurrence in sea hares is a result of dietary consumption. Recent investigations have also demonstrated that Dolabella auricularia readily consumes certain species of cyanobacteria and is capable of growing on a strictly cyano- bacterial diet. 66 The marine green algae (Chlorophyta) range from cold temperate to tropical waters; several families are exclusively tropical. 2 Most of the compounds isolated from the green algae (229 compounds) 32 are terpenes; sesquiterpenes and diterpenes are particularly common (see Figure 6.2). 8 Tropical green algae of the order Caulerpales have been especially well studied; members of this group, including species of Caulerpa and Halimeda , contain acyclic or monocyclic sesqui- and diterpenoids. 67,68 Triterpenes, which are not very common in marine algae, have been reported from Tydemania expeditionis. 69,70 Only a few green algae produce halogenated compounds. Neomeris annulata (Dasycladaceae) produces brominated sesquiterpenes, 71,72 Cymopolia barbata (Dasycla- daceae) produces brominated prenylquinones of mixed terpenoid and aromatic biosynthesis, 73 and Avrainvillea spp. produce brominated aromatic compounds. 74,75 The brown algae are almost exclusively marine and primarily dominant in temperate waters. They range in size from small filamentous forms to subtidal kelps, which are the largest and most abundant benthic marine algae in temperate seas. 2,76 Brown algae are the only seaweeds that produce polyphenolic compounds. Although these compounds may function like terrestrial tannins by binding proteins or other macromolecules, they are structurally different compounds that are complex polymers derived from a simple aromatic precursor, phloroglucinol (1,3,5-trihydroxyben- zene). 33,77,78 These metabolites are often termed phlorotannins to distinguish them from the terrestrial tannins. Tannins found in higher plants are divided into two classes: condensed tannins (including lignins) and hydrolyzable tannins. Tannins are polymeric, consisting of multiple structural units containing phenolic groups. Lignins are large phenolic polymers bound to polysaccharides in plant cell walls. Hydrolyzable tannins are formed from polymerization of esters of glucose with gallic acid or related compounds. 79,80 None of these types of tannins occur in marine algae. Polyphenolics in brown algae may function as defenses against herbivores, 33,78 as antifoulants 81,82 83 ), as chelators of metal ions, 77 and in UV absorption. 84 Over 980 secondary metabolites have been isolated from the brown algae. 32 In addition to polyphenolics, brown algae in the order Dictyotales produce nonpolar metabolites such as terpe- noids, acetogenins, and compounds of mixed terpenoid-aromatic biosynthesis (see Figure 6.3). For example, over 230 compounds have been isolated from Dictyota spp. 32 Sargassum species also produce acetogenins and compounds of mixed terpenoid-aromatic biosynthesis. Brown algae of the genus Desmarestia are also known to concentrate high amounts of sulfuric acid, which may be used in defense. 1,8,85,86 The greatest variety of secondary metabolites is probably found among the red algae, where all classes of compounds except phlorotannins are represented and many metabolites are haloge- nated. 35,87 Over 1240 compounds have been reported from the red algae. 32 Red seaweeds from the families Bonnemaisoniaceae, Rhizophyllidaceae, and Rhodomelaceae are rich in halogenated com- pounds that range from halogenated methanes, haloketones, and phenolics to more complex terpenes 9064_ch06/fm Page 230 Tuesday, April 24, 2001 5:18 AM © 2001 by CRC Press LLC (but see Jennings and Steinberg Chemical Mediation of Macroalgal–Herbivore Interactions 231 (see Figure 6.4). 35,36,87,88 The red algal genus Laurencia , the subject of extensive investigations, produces over 570 compounds, 32 many of which are halogenated and of unique structural types. 32,87,89 Seagrasses are known to produce phenolic acids, 90 phenolic acid sulfate esters, 91 and sulfated flavonoids. 92 While the natural functions of most of these compounds are not known, some of the phenolic acids and the sulfate esters inhibit growth of microorganisms and fouling organisms such as barnacles 91,93 and deter grazing by amphipods. 93 Herbivory on seagrasses may be important for the structuring of seagrass communities in nearshore environments, 94 but very little is known about the role of chemical defenses in the ecology of seagrasses. Many possible defensive functions for algal secondary metabolites have been proposed includ- ing antimicrobial, antifouling, and antifeedant activities. To date, the role of these compounds as FIGURE 6.2 Examples of secondary metabolites from marine green algae. AcO OAc OAc Caulerpenyne OAc AcO Chlorodesmin Taxifolial OHC OAc AcO OAc OAc CHO AcO OAc OAc Halimedatetraacetate CHO H CHO H CHO Halimedatrial CHO AcO AcO Oxytoxin OAc OAc CHO Udoteal OAc AcO Flexilin Avrainvilleol Br OHOH OH Br OH O H Br HO Debromoisocymobarbatol 9064_ch06/fm Page 231 Tuesday, April 24, 2001 5:18 AM © 2001 by CRC Press LLC 232 Marine Chemical Ecology defenses against herbivores has been studied most. Recent studies have clearly shown that many seaweed natural products function as feeding deterrents toward herbivores. 8,21–24 However, many compounds may also have other roles or may function simultaneously as defenses against pathogens, fouling organisms, and herbivores, thereby increasing the adaptive value of these metabolites. 67,95 A consideration of multiple functions for secondary metabolites is important, because even though algal secondary metabolites may function as defenses against herbivores, they may have evolved for other reasons such as resistance to pathogens or competitors. Some algal secondary metabolites do show antimicrobial 96–98 or antifouling 81,95,99–101 effects. Chapters 10 and 17 in this volume cover the topic of natural antifoulants in more detail. II. MARINE HERBIVORES A. M ARINE B ENTHIC H ERBIVORY AND H ERBIVORE N UTRITION Herbivory in benthic marine systems is intense. For example, on coral reefs, herbivores can remove almost 100% of the biomass produced daily by marine macroalgae, whereas in the most intensely grazed terrestrial systems — African grasslands — herbivores only consume about 66% of the above-ground plant biomass. 9,21,102 While terrestrial plants produce subterranean structures such as roots, bulbs, and tubers that are generally inaccessible to most animals, most marine algae do not FIGURE 6.3 Examples of secondary metabolites from marine brown algae. Sporochnol A H HO OH Zonarol HO H HO H Pachydictyol A O HO H O O Stypoldione O HO H HO OH Stypotriol OH OH H H Dictyol E Dictyopterene B Dictyopterene A O H H OAc Acutilol A Acetate 9064_ch06/fm Page 232 Tuesday, April 24, 2001 5:18 AM © 2001 by CRC Press LLC Chemical Mediation of Macroalgal–Herbivore Interactions 233 produce equivalent underground parts (although at least one species of Caulerpa is known to absorb nutrients through its underground rhizomes 103 ). Therefore, virtually all algal biomass in the ocean is potentially exposed to consumers, epibionts, and pathogens. 104 The feeding activities of herbivores constitute an important ecological force controlling the structure and dynamics of plant communities; however, from an herbivore’s point of view, feeding is only a means of gaining adequate nutrition for survival, growth, and reproduction. Herbivores make a living consuming food that is much lower in nutritional value and much higher in indigestible structural material than their own tissues. 105–107 As a result, herbivores must process large quantities of food 108–110 or rely on alternative strategies that enhance nutrient uptake per unit of food. 105,106 Although marine algae do not have the large quantities of nondigestible structural material that terrestrial plants have, 9,104 nutrient uptake can nevertheless be constrained for marine herbivores. For example, coral reef fishes may eat many times their required energetic needs in order to gain enough nitrogen from seaweeds. 108 The nutritional component of marine plant–herbivore interactions has often been overlooked by many workers, particularly chemical ecologists. 22,111,112 Chemical defenses, in essence, keep herbivores from effectively exploiting potential nutrient sources and, therefore, may affect herbivore nutrition both directly and indirectly. 27,112–115 For example, prey nutritional value can alter the effectiveness of marine chemical defenses against diverse consumers, 27,113,115 and interactions between nutritional value and algal chemistry can affect consumer fitness. 112 Prey quality can affect the perception of a chemical defense 27,113,115 and the consumer’s ability to digest or detoxify the compound, 116,117 114 FIGURE 6.4 Examples of secondary metabolites from marine red algae. OO H O H Br Aplysistatin O Cl Br O Chlorofucin Debromolaurinterol Isolaurinterol OO Br H Palisadin A O OH Cl Br Br Pacifenol Cl Br HO Elatol Br Br Cl O Prepacifenol Br Cl BrBr 2-chloro-1,6,8-tribromo- OH OH Br O Br Br OH HO Lanosol ochtodene 9064_ch06/fm Page 233 Tuesday, April 24, 2001 5:18 AM © 2001 by CRC Press LLC or may indirectly alter digestive associations with gut symbionts (see Slansky 234 Marine Chemical Ecology for terrestrial examples). Although digestive associations with microbes are known for a number of herbivorous fishes, 111,118,119 the effects of algal defenses on gut microbes and consequences for the host have not been demonstrated. B. HERBIVORE DIVERSITY Herbivores in the sea are phylogenetically more diverse than on land. Seaweeds are eaten by diverse vertebrate ectotherms and an array of invertebrate consumers that vary both in their selectivity and in their impact on algae. Vertebrate herbivores are comprised of various fish families and species, as well as some turtles. 24,111,120–125 Invertebrate herbivores span at least four different phyla and include an array of gastropods (such as snails, limpets, sacoglossans, sea hares, cephalaspideans, and chitons), urchins, crabs, amphipods, isopods, shrimps, polychaete worms, copepods, and a few insect species that feed on algae living in the upper littoral zone. 24,110,123,126–135 The importance of different herbivore groups varies geographically, and herbivore species diversity increases towards the tropics in most groups. 111,122,136 This contrasts with the patterns of speciation in algae (and in some particular invertebrate groups) for which the number of species increases with latitude. 137,138 However, differences in the latitudinal effects of herbivorous fishes could arise from higher fish abundances, rather than species diversity, in the tropics. 139 Nonetheless, herbivore radiation in the tropics likely has had important consequences for the evolution of seaweeds, as evidenced by the increased diversity of defenses and higher chemical deterrence of tropical algae when compared to their temperate counterparts. 24,140–144 The biogeography of herbivorous fishes has been reviewed elsewhere. 111,122,139,145 For invertebrate grazers, information is available for some gastropods 146 and urchins. 147 Although there are obvious limitations in our understanding of herbivore biogeography, some patterns do emerge. Latitudinally, herbivory by gastropods is more important in temperate systems than in the tropics, fish herbivory shows the opposite pattern, and urchin herbivory appears to be intense in both temperate and tropical zones. 136 Although amphipod diversity increases with latitude, 137 little is known about the feeding habits of most species, precluding biogeographical comparisons in herbivory. Despite latitudinal variation in the importance of particular groups of consumers, herbivory and predation increase in intensity and more developed prey defenses occur in the tropics than in temperate regions. 140,141, 148–154 Likewise, studies of seaweed–herbivore interactions have sug- gested that a higher diversity and higher tissue concentrations of small, lipophilic secondary metabolites are found in tropical seaweeds than in temperate seaweeds. 8,32 However, few studies have rigorously tested this hypothesis. 143,144 In contrast, larger water-soluble phlorotannins, namely, the polyphenolic compounds produced by brown seaweeds, have been hypothesized to be more abundant in temperate species than in tropical species. 33 Recent investigations by Targett and co- workers 78,155,156 have challenged this view, finding that tropical brown seaweeds can have high concentrations of phlorotannins. However, these phlorotannins appear to have little effect on common tropical herbivores. 156 C. HERBIVORE SIZE AND GUILDS Marine herbivores span a smaller size range than their terrestrial counterparts. 102 For algal consum- ers, marine equivalents of terrestrial megaherbivores (such as elephants, rhinoceri, hippopotami, and a variety of large extinct grazers) 102,157–159 are not known, nor is there fossil evidence that they have existed. Although seagrasses are consumed by large mammals such as manatees and dugongs, 94 algae are consumed by these animals only under severe food limitation, 160 and, thus, the largest grazers on algae are fishes, 111,122 turtles, 121 and the larger sea hares (e.g., Aplysia vaccaria can reach more than 15 kg and are the largest gastropods in the world). 161 Because size can impose constraints on mobility, predation risk, and per capita impact on food plants, it is often useful to divide marine herbivores into functional groups or guilds sharing certain 9064_ch06/fm Page 234 Tuesday, April 24, 2001 5:18 AM © 2001 by CRC Press LLC Chemical Mediation of Macroalgal–Herbivore Interactions 235 general characteristics. Although such categories are useful for describing patterns and processes of plant–herbivore interaction, they should be used with caution; closely related consumers can sometimes exploit quite different food sources, and broad categorization may potentially overlook important complexities in the interaction of animals with plants. 110,111,135,162–164 In terms of size, marine herbivores can be roughly divided into macro-, meso-, and micrograzers. Macrograzers or macroherbivores include larger, more mobile herbivores that can cover considerable areas while foraging, whose feeding activities often have strong impact on seaweeds, and that generally do not 165 for an exception). Most herbivorous fishes, turtles, sea urchins, and large gastropods (e.g., the sea hare Dolabella auricularia) 30,129 qualify as macro- grazers, and tend to have broad, generalized diets. Mesograzers, in contrast, often feed and live on plants larger than themselves. In terms of size, mesograzers include herbivores between 0.2 and 20 mm, of potentially limited mobility, that live on the plants they eat but generally cause limited damage, and for which predation risk is often large. 134,166–168 Aside from smaller consumers, many larger animals may spend part of their lives as functional mesograzers. A number of mesoherbivores are trophic specialists that consume one or a few algal spe- cies, 9,167,169–177 often chemically defended ones. 9,167,175,176 Other, more generalized feeders may also have strong preferences for, and form close associations with, chemically defended algae. 135,166,178–180 However, in comparison with terrestrial environments, 181,182 feeding specialization among marine herbivores is rare. 9,104,167 Mesograzers find shelter in the seaweeds they consume and are often more resistant to algal chemical defenses than larger herbivores. 131,133,167 Because predation on mesograzers can be intense, associating with noxious or unpalatable hosts can have clear selective advantages. 9,22,167 Association with particular seaweeds can reduce predation risk of these smaller herbivores either via crypsis, reduced mobility coupled with selection of unpalatable algae as habitats, adaptations that reduce the risk of being removed from their host plants, behavioral or physiological sequestration of chemical defenses from the algae they eat, or a combination of these 9,167 (also reviewed in Chapter 4 in this volume). Metabolites that are toxic or deterrent toward generalist herbivores such as fishes and sea urchins are often ineffective against mesograzers and may even function as feeding stimulants. Specialist herbivorous molluscs such as sea hares and sacoglossans (ascoglossans) selectively consume chem- ically rich seaweeds and often concentrate seaweed secondary metabolites 8,9,183 as defenses against their own natural enemies. These metabolites can be concentrated on the skin or actively exuded when the molluscs are attacked. 8,87,170,173,184–186 Some mesograzers do not obtain secondary metab- olites from their algal diets but appear to biosynthesize their own metabolites. 187 Sacoglossans feed suctorially and some can retain photosynthetically functional chloroplasts from their host algae. 177 Thus, certain sacoglossans may be capable of synthesizing their chemical defenses from primary metabolites derived from photosynthesis. 188 Other small mesograzers such as amphipods, crabs, and polychaetes may also preferentially consume seaweeds that are chemically defended. 8,9,166,167,189 Amphipods, crabs, and polychaetes do not appear to sequester algal secondary metabolites. These small marine herbivores sometimes feed selectively or exclusively on seaweeds that are chemically defended from fish. Hay and coworkers 9,22,132,167 have shown that the association between mesograzers and chemically defended seaweeds reduces predation on the herbivores. They have hypothesized that escape from predation may be a dominant factor selecting for dietary specialization among these herbivores (see also Chapter 4 in this volume). However, Poore and Steinberg 134 showed that the nest-building amphipod Peramphithoe parmerong seemed to rely primarily on intrinsic host plant qualities in determining its seaweed diet, rather than on extrinsic properties, such as predation, in determining food choice. Although the role of micrograzers (e.g., copepods, cladocerans, ostracods, etc.) in pelagic communities is well studied, extremely little is known about micrograzers on the marine benthos. This is probably due to the assumption that such small consumers are constrained by size to 9064_ch06/fm Page 235 Tuesday, April 24, 2001 5:18 AM © 2001 by CRC Press LLC live on the algae they consume (see Steinberg 236 Marine Chemical Ecology feeding on microalgae. At least some species of harpacticoid copepods are known to consume macroalgae, and one species can become a pest for seaweed aquaculture. 190–193 In Israel, a copepod tentatively identified as Amphiascus minutus 193 infests ponds containing Gracilaria conferta and tunnels through the alga. During their summer reproductive peak, copepod infestations can become severe and lead to the collapse of algal cultivation ponds. 192,193 Other benthic copepods form associations with algae 194 and cyanobacterial mats, 195 but their feeding habits have not been addressed. However, copepods of the genus Diarthrodes are known to bore into algae in a fashion similar to the example described above. 190 More information on the ecology of benthic marine micrograzers is clearly needed. Marine herbivores are a diverse group, and strict compartmentalization into guilds should not be interpreted as an all-encompassing scheme. In particular, the relation between size and mobility of mesograzers has been criticized by some authors and has led to debate. 162,163,168 Larger consumers such as urchins may have reduced mobility and live closely associated with their food plants, essentially acting as “large” mesograzers, 165 while small consumers may perform diel migrations of several meters. 168,196 It is also clear now that related mesograzers can vary in their relative mobility. 110,135,164,168,180 In the case of amphipods 110 and crabs, 164 lower mobility appears to be associated with a higher ability for compensatory feeding, and, therefore, an increased ability to exploit lower quality algal foods. Given their large impact on algal communities, macroherbivores appear to be more important selective agents for the evolution of chemical defenses than meso- or microherbivores. 9,21,167 Although mesograzers can have strong effects on algal communities, 197–202 they are rarely acknowl- edged as definitive forces shaping the evolution of seaweed defensive chemistry. The grazing pressure of meso- and micrograzers could be more important for early algal stages and gametes. 201–204 Although information on the chemical defense of early life stages is available for marine inverte- brates, 205,206 207 203 and Schnitzler et al. 204 ). Evaluating marine herbivore selective pressures at different scales needs more attention. Despite processes between seaweeds and their consumers 9,167 and should be refined rather than abandoned. III. CHEMICALLY MEDIATED INTERACTIONS BETWEEN MARINE MACROALGAE AND HERBIVORES A. F EEDING-DETERRENT EFFECTS OF ALGAL SECONDARY METABOLITES The common method of testing for feeding-deterrent effects against herbivores has been to incor- porate seaweed extracts or isolated metabolites at natural concentrations into a palatable diet, either a preferred seaweed or an artificial diet, and then to compare feeding rates of the grazers on treated foods with those on appropriate controls. 208 Deterrent effects observed in these assays appear to be based primarily on the taste of the treated food. If a compound is deterrent toward an herbivore, the degree of avoidance is often related to the concentration of the extract or metabolite in the diet. Higher concentrations often result in a more pronounced deterrent effect. 8,209–211 These methods do not assess toxicity or other physiological effects on the consumers or possible detoxification methods by herbivores. Compounds produced by marine cyanobacteria deterred feeding by several species of herbiv- orous fishes, 44,55,176,212–214 sea urchins, 55,214 and crabs. 55 In contrast, the opisthobranch sea hare Stylocheilus longicauda specializes on Lyngbya majuscula and prefers artificial diets containing compounds produced by blue-green algae; however, high concentrations of some of these metab- olites can still deter feeding by S. longicauda. 176,211 The sea hares S. longicauda and Dolabella auricularia sequester cyanobacterial compounds from their diets, gaining protection from fish and invertebrate predators. 66,176,212,215,216 9064_ch06/fm Page 236 Tuesday, April 24, 2001 5:18 AM © 2001 by CRC Press LLC its shortcomings, the use of guilds has proven useful in explaining ecological and evolutionary similar studies on algae are lacking (see Deal, Hay et al., [...]... radiata, Mar Ecol Prog Ser., 127, 169 , 1995 166 Hay, M E., Duffy J E., Pfister C A., and Fenical W., Chemical defense against different marine herbivores: are amphipods insect equivalents?, Ecology, 68 , 1 567 , 1987 167 Hay, M E., The role of seaweed chemical defenses in the evolution of feeding specialization and in the mediation of complex interactions, in Ecological Roles of Marine Natural Products, Paul,... broad-leaved forests, in Plant–Animal Interactions: Evolutionary Ecology in Tropical and Temperate Regions, Price, P W., Ed., John Wiley & Sons, Ithaca, NY, 1991 © 2001 by CRC Press LLC 9 064 _ch 06/ fm Page 2 56 Tuesday, April 24, 2001 5:18 AM 2 56 Marine Chemical Ecology 154 Pennings, S C., Siska, E L., and Bertness, M D., Latitudinal differences in plant palatability in Atlantic coast salt marshes, Ecology, ... Prod., 59, 812, 19 96 65 Pettit, G R Dolastatins, in Progress in the Chemistry of Organic Natural Products, Herz, W., Kirby, G W., Moore, R E., Steglich, W., and Tamm, C., Eds., Springer-Verlag, New York, 70, 1997, 1 66 Cruz-Rivera, E and Paul, V J., work in progress 67 Paul, V J and Fenical, W., Chemical defense in tropical green algae, order Caulerpales, Mar Ecol Prog Ser., 34, 157, 19 86 68 Paul, V J and... herbivory are often chemically defended species such as Halimeda and Dictyota spp.,353,3 56, 362 – 365 which are relatively unpalatable to herbivores Studies of phase shifts from coral-dominated to macroalgal-dominated communities have often overlooked filamentous blue-green algae (cyanobacteria), which generally have been grouped with turf algae in ecological research (e.g., Steneck and Dethier 366 ) Benthic cyanobacteria... 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A O OH Cl Br Br Pacifenol Cl Br HO Elatol Br Br Cl O Prepacifenol Br Cl BrBr 2-chloro-1 ,6, 8-tribromo- OH OH Br O Br Br OH HO Lanosol ochtodene 9 064 _ch 06/ fm Page 233 Tuesday, April 24, 2001 5:18 AM © 2001 by CRC. algal spe- cies, 9, 167 , 169 –177 often chemically defended ones. 9, 167 ,175,1 76 Other, more generalized feeders may also have strong preferences for, and form close associations with, chemically