Section II Organismal Patterns in Marine Chemical Ecology 9064_Section II Div/fm Page 155 Tuesday, April 24, 2001 5:13 AM © 2001 by CRC Press LLC 157 Chemical Ecology of Mobile Benthic Invertebrates: Predators and Prey, Allies and Competitors John J. Stachowicz CONTENTS I. Introduction 157 II. Chemical Mediation of Predator–Prey Interactions 158 A. Prey Defenses against Predators 158 1. De Novo Production 158 2. Sequestration of Diet-Derived Defensive Compounds 161 3. Predator Detection and Avoidance 163 B. Consequences of Feeding Deterrents for Predators 165 1. Susceptibility of Consumers to Defensive Chemicals 165 2. Consequences of Consuming Defensive Metabolites 167 C. Chemically Aided Predation 169 1. Foraging and Prey Detection 169 2. Toxin-Mediated Prey Capture 171 3. Feeding Stimulants 172 III. Chemical Mediation of Competition Among Mobile Invertebrates 173 A. Antifoulants 173 B. Allelopathy and Community Structure 174 IV. Chemical Mediation of Mutualistic and Commensal Associations 175 A. Host Location 176 B. Associational Refuges 178 C. Local Specialization and Population Subdivision 180 V. Chemical Mediation of Reproductive Processes 181 A. Sex Pheromones 181 B. Synchronization of Reproduction 182 C. Timing of Larval Release 183 VI. Conclusion 183 Acknowledgments 184 References 184 I. INTRODUCTION The diversity of topics addressed in this volume attests to the fact that marine chemical ecology is more than just animals and plants producing chemicals that deter predation. Chemicals are involved 4 9064_ch04/fm Page 157 Tuesday, April 24, 2001 5:17 AM © 2001 by CRC Press LLC 158 Marine Chemical Ecology in mediating a diverse array of inter- and intraspecific interactions including predation, competition, mutualism, and reproductive processes, as well as interactions between organisms and their physical environment. This diversity is best exemplified in the mobile invertebrates. Mobile invertebrates are the dominant predators and herbivores in many marine systems and serve as “keystone” species in several of these systems. Thus, factors (including chemistry) that determine their distribution, abundance, and impact on communities and ecosystems should be of broad interest to marine biologists and ecologists. Straightforward production of predator-deterrent chemicals is rare in this group as compared to sessile invertebrates and seaweeds, and this has led the ecologists and chemists studying these organisms to diversify in terms of the types of interactions they study. Waterborne chemicals help mobile invertebrates locate food, mates, and appropriate habitats or symbiotic partners; they also help regulate and synchronize reproductive cycles and alert organisms to the danger of nearby predators. Nevertheless, the bulk of research on chemically mediated interactions has focused on predator–prey interactions, so much of the chapter is necessarily devoted to these interactions. In areas where rigorous studies involving mobile benthic invertebrates are rare (e.g., antifouling and allelopathy), examples from other groups (plants, sessile invertebrates, or verte- brates) or habitats (open water marine, freshwater, or terrestrial) are provided to identify areas deserving increased attention. More detailed treatments of particular types of interactions or habitats can be found in the other chapters of this volume. Several excellent reviews currently exist on particular aspects of marine chemical ecology, 1–6 so this chapter does not attempt to provide a comprehensive or historic overview, but rather tries to provide a sound conceptual discussion of the diversity and importance of chemically mediated interactions involving mobile invertebrates. Due to space constraints, not all relevant studies can be included, and recent studies are sometimes cited in favor of more classical work, as these provide similar conceptual information but often use more advanced methodologies and provide greater access to other literature on the topic. Where possible, this chapter highlights studies that assess the importance of chemically mediated interactions within the broader context of ecology and evolutionary biology. II. CHEMICAL MEDIATION OF PREDATOR–PREY INTERACTIONS Both primary and secondary metabolites from marine organisms play an important role in mediating all phases of predator–prey interactions, from defending prey against detection and attack to helping predators locate prey from a distance and subdue it once it is captured. A. P REY D EFENSES AGAINST P REDATORS Although relatively few mobile invertebrates produce their own defensive compounds, many more use the defensive compounds produced by other organisms, either by physiologically sequestering them from their prey, or by developing commensal or mutualistic associations with other chem- ically unpalatable organisms (see Section IV.B). Additionally, some animals use waterborne cues to detect the presence of predators and adjust their behavior and use of refuges to minimize the risk of detection. 1. De Novo Production As with sessile animals and plants (see other chapters, this volume), the chemical deterrence of mobile invertebrates is best assessed using an approach in which ecologically relevant consumers are offered palatable food items with chemical extracts coated on, or embedded within, them. 7 Assays in which the toxicity of compounds is assessed by dissolving them in the water containing the assay organisms have been repeatedly shown to bear no relation to the effects of compounds when ingested with prey. 1,8,9 Most feeding deterrents of mobile invertebrates appear to be lipid-soluble, thus these 9064_ch04/fm Page 158 Tuesday, April 24, 2001 5:17 AM © 2001 by CRC Press LLC Chemical Ecology of Mobile Benthic Invertebrates 159 assays should not encounter problems with compounds dissolving or leaching into the water, and extract or compound concentration can be carefully controlled. Several investigators have found minimal loss of lipophilic extracts from test foods during the duration of a bioassay. 1,10 Given the long retention time of the few compounds or extracts that have been evaluated and the similar solubility characteristics of many marine secondary metabolites, this general methodology can probably be used with most nonpolar, lipid-soluble metabolites. Methods for assaying the feeding deterrent properties of marine organisms have recently been critically reviewed, 7 and interested readers should consult that paper. Using these methodologies, chemical defenses against predation have been reported from sea spiders, echinoderms, and molluscs. However, compared to sessile invertebrates 4 and seaweeds (see Chapter 6 in this volume), relatively few mobile invertebrates appear to produce their own chemical feeding deterrents. Although this may be due in part to phylogenetic constraints, mobile invertebrates also have a broader array of behavioral defenses, including flight, aggression, and avoidance of predators by restricting activity to periods when predators are less active. Not surprisingly, then, chemical defenses among the mobile invertebrates appear most common among groups that lack obvious morphological or behavioral mechanisms of defenses. For example, shell- less gastropods, including nudibranchs, sea hares, and ascoglossans (sacoglossans), are often supposed to elaborate some form of chemical defense. 4,11 Although many of these animals obtain dorid nudibranchs and sacoglossans are known to produce the deterrent chemicals de novo. 12–18 In the first example of de novo synthesis of chemical defenses by a dorid nudibranch, Cimino et al. 12 noted that polygodial (Structure 4.1), a defensive compound isolated from the dorid nudibranch Dendrodoris limbata , was not present in the sponges on which the animal fed. Using radiolabeling techniques, the authors demonstrated that the nudibranch produces deterrent chemicals not directly derived from its diet. Several other dorid nudibranchs appear to be capable of synthesizing sesquiterpenoids, diterpenoids, and sesterterpenoids that are effective feeding deterrents, but only a few have been demonstrated to employ both sequestration and de novo synthesis. 16,19 Species with de novo synthesis are freed from the constraints of specialization on a chemically defended food in order to obtain defensive compounds and are thus able to exploit a broader taxonomic range of food items. 18 Cimino and Ghiselin 18 have suggested that in some cases, de novo synthesis may evolve retrospectively from sequestration rather than independently, as enzymes and biochemical pathways originally employed in detoxification and sequestration are modified to synthesize compounds originally derived from the diet. The exciting possibility of unraveling the evolutionary history of chemical defenses in this group (and other groups) may benefit from collaborations with the emerging field of molecular phylogenetics. Some shelled gastropods do produce chemical defenses, although this is far less common. One South African limpet, Siphonaria capensis , occurs at very high densities on rocky shores, appar- ently protected from predators by chemical feeding deterrents. These animals are rarely consumed relative to Patella granularis (a similar limpet that lacks defensive chemistry) and exude a repellent mucus onto the surface of their shell when attacked. Nonpolar extracts from Siphonaria confer resistance from predation to Patella when they are coated on its shell. 20 Because the metabolites responsible for the chemical defense have not been fully isolated and characterized, it is still unclear whether the compounds that confer resistance to predation in Siphonaria are diet derived or synthesized de novo . Chemical defenses are less commonly reported in other groups of mobile marine invertebrates, but they may exist. Heine et al. 21 showed that a common Antarctic nemertean worm is rejected as prey by co-occurring fishes despite the lack of obvious structural defenses. The unpalatability has been attributed to a highly acidic mucus coating (pH 3.5), although toxic peptides were also present 22 CHO CHO 4.1 9064_ch04/fm Page 159 Tuesday, April 24, 2001 5:17 AM © 2001 by CRC Press LLC their chemical defense from their prey either directly or in an altered form (Section II.B.2), a few 160 Marine Chemical Ecology and are thought to serve a defensive function in other nemertean worms. 23 However, rigorous experimental data in support of a defensive function for these peptides are generally lacking. Despite their diversity, and in contrast to their terrestrial counterparts, examples of the presence of either diet-derived or de novo production of defensive chemicals among marine arthropods are rare. However, several studies provide evidence that suggests no chemical defense in this group. A pinnotherid pea crab has been shown to be unpalatable to mummichogs that consumed similar- sized blue crabs, although it is unclear whether this defense is chemical or structural in nature. 24 Several marine amphipods have bright coloration that has been thought to function as warning coloration, 25 but rigorous bioassays to determine whether these species are chemically unpalatable have yet to be reported. In the one example where chemical components of a marine arthropod have been shown to deter predation by ecologically realistic predators at natural concentrations, ecdysteroids (Structures 4.2 and 4.3) protected a pycnogonid sea spider from predation by green crabs. 26 These compounds serve a normal function as a molting hormone, 27 but were present in all developmental stages, including nonmolting stages. Additionally, concentrations were much higher than normally required for the induction of molting, suggesting their alternative function of predator deterrence. In general, secondary metabolites isolated from marine arthropods have not been shown to deter feeding by ecologically relevant predators. A survey of the frequency of chemical defense in echinoderms from the Gulf of Mexico found that a number of asteroids (10/12 species examined) and ophiuroids (3/3 species) echinoderms contained deterrent chemicals within their body walls. 28 Although the specific chemicals responsible for deterrence among the echinoderms have only rarely been isolated and characterized, crude chemical extracts varied in their effectiveness against different predators. Many extracts deterred feeding by the pinfish ( Lagodon rhomboides ), while fewer extracts were effective against predation by a majid crab ( Stenorhynchus seticornis ), mirroring the differences in susceptibility to algal chemical defenses observed in large, mobile (fishes) vs. small, sedentary (amphipods, crabs) 29,30 OH OH HO HO OH O O O 4.3 OH OH HO HO OH OH O 4.2 9064_ch04/fm Page 160 Tuesday, April 24, 2001 5:17 AM © 2001 by CRC Press LLC herbivores (Section II.B.1). Chemical Ecology of Mobile Benthic Invertebrates 161 2. Sequestration of Diet-Derived Defensive Compounds Although relatively few mobile invertebrates produce their own defensive chemicals, many more are able to physiologically sequester defensive compounds from their prey. The opisthobranch molluscs, in particular, offer a diversity of examples in which species with highly specialized diets obtain chemical defenses directly from their prey; for example, dorid nudibranchs from sponges and sea hares and sacoglossans from red algae. The evolutionary progression of shell loss in this group has been hypothesized to be the result of the deployment of diet-derived defensive com- pounds that rendered a hard shell obsolete for defense. 31 Several reviews 4,11,17,18,32 describe the mechanisms behind physiological sequestration. Described here are several taxonomically diverse examples in which both the ecological and chemical aspects of the interaction have been partic- ularly well characterized. Dorid nudibranchs feed almost exclusively on sponges and commonly sequester sponge-pro- duced defensive compounds. For example, the Spanish dancer nudibranch, Hexabranchus san- guineus , feeds on sponges in the genus Halichondria which produce oxazole-containing macrolides that deter feeding by fishes. 33 The nudibranch sequesters halichondramide (Structure 4.4), alters it slightly (Structure 4.5), and concentrates these compounds in its dorsal mantle and egg masses where they serve as a potent defense against consumers. Concentrations of the defensive compounds are lowest in the sponge, higher in the nudibranch, and highest in the nudibranch egg masses, but even the lowest natural concentrations strongly deter feeding by fishes. As mentioned previously, compounds are often not sequestered uniformly throughout the body tissue. For example, many dorid nudibranchs accumulate sequestered compounds along the mantle border. 33–35 In some cases, to avoid autotoxicity, inactive precursor compounds are stored in the digestive gland and are converted to the toxic form and transferred to the mantle border where they may be more effective deterrents. 34 Although it has been hypothesized that such localization of compounds is important for chemical defense, there is little experimental evidence in support of this. On Guam, the nudibranch Glossodoris pallida sequesters defensive compounds from its sponge prey, localizing them in mantle dermal formations (MDF) on the surface of the animal. 35 In the most direct test available to date, removal of these tissues of locally high concentration of defensive compounds increased the palatability of these animals to predation by fishes and crabs, but assays with artificial foods showed no difference in palatability of foods with localized vs. uniform concentrations of metabolities. 35 Thus, a high, localized concentration of chemicals in the MDFs was no more effective at reducing predation than lower, uniform levels. However, localization of compounds in the surface tissues of the mantle may facilitate excretion of compounds into mucus on the surface of the animal, enhancing the effectiveness of the defense. Alternatively, such localization may serve nondefensive functions such as sequestration of noxious compounds away from vital internal organs and avoidance of autotoxicity. 35 The causes and consequences of within- individual variation in the concentration of defensive compounds should provide an area of research worthy of further consideration. Ascoglossan sea slugs (Sacoglossa) feed suctorially on marine algae and sequester functional chloroplasts from their prey in the tissues of their mantle. 14,36 Additionally, these animals often OHC N Me O N O N O N O OMe OMe O O O OH OMe O 4.4 4.5 9064_ch04/fm Page 161 Tuesday, April 24, 2001 5:17 AM © 2001 by CRC Press LLC 162 Marine Chemical Ecology store sequester seaweed secondary metabolites for defense against predation. 37–39 In some instances, precursors to defensive compounds that are obtained from prey and converted to more deterrent compounds prior to deployment. For example, Elysia halimedae obtains halimedatet- raacetate (Structure 4.6) from Halimeda macroloba , reduces the aldehyde group on this com- pound into the corresponding alcohol (Structure 4.7), and uses this compound in its own defense. 37 Some ascoglossans use fixed carbon from sequestered chloroplasts to produce their own defensive compounds. 14,15,17 Sea hares (order Anaspidea) have been repeatedly shown to sequester metabolites that defend seaweeds from generalist herbivores 11,40–43 and may use a combination of diet-derived and de-novo - produced compounds for defense. 44 In contrast to the strategic location of compounds in the mantle border by nudibranchs and sacoglossans, sequestered compounds appear most concentrated inter- nally, in the digestive gland of sea hares. This suggests that the accumulation of these compounds in sea hares may be a simple consequence of the detoxification of ingested metabolites rather than an adaptation to reduce predation. 42 In Dolabella auricularia , for example, whole body extracts deter predators, but this pattern is due almost entirely to the unpalatability of the digestive gland, as feeding assays with other body tissues and their extracts showed no effect on palatability. 42 However, some sea hares do contain sequestered algal metabolites in the skin and surface tissues at concentrations that are deterrent to predators. 43 Many opisthobranchs also secrete copious amounts of diet-derived compounds into their egg masses, which is often thought to render them unpalatable to generalist predators, although rigorous evidence for this is rare. For example, egg masses from the sea hare Aplysia juliana are chemically unpalatable to reef fishes, but diet-derived metabolites do not appear to be the cause of this unpalatability. 42 Sea hares not only sequester compounds from their algal prey into their body tissues, but also produce copious amounts of “ink” that has (largely through anecdotal evidence) been postulated to serve a defensive function. 44 These animals are generally too slow moving to use the ink cloud as a “smoke screen” to escape all but the most sedentary predators (e.g., anemones), but noxious chemicals in the ink cloud could stun or repel more mobile predators. These hypotheses have been tested by manipulating ink production by the sea hare Aplysia californica by altering the diet; Aplysia fed red algae ( Gracilaria sp.) produce copious amounts of ink, whereas individuals fed green algae ( Ulva sp.) do not. 45 When ensnared in the tentacles of sea anemones ( Anthopleura xanthogrammica , a natural predator of Aplysia in Pacific coast tide pools), red-algal fed sea hares released ink, causing the anemone to release it unharmed; green-algal fed individuals did not release ink and were readily consumed. Similar amounts of ink applied to inkless (green-algal fed) Aplysia when trapped by sea anemones caused these otherwise palatable animals to be rejected as prey. 45 CH 2 OH OAc OAc AcO OAc 4.7 CHO OAc OAc AcO OAc 4.6 9064_ch04/fm Page 162 Tuesday, April 24, 2001 5:17 AM © 2001 by CRC Press LLC Chemical Ecology of Mobile Benthic Invertebrates 163 Aplysia with chemical defenses in their tissues but without ink were consumed at a similar rate to those without toxins (20% vs. 12%), whereas those without toxins in their tissues, but with ink exhibited much greater survival (71%), suggesting that the excretion of ink may be the primary defense of these sea hares when being consumed by slow-moving predators like sea anemones. 45 Pennings 42 also found that ink from some (but not all) sea hares could deter predators, however he found no evidence that the metabolites responsible for defense were diet derived. Sea hares also secrete opaline when attacked by predators, although the function of this secretion has yet to be unambiguously determined. 44 As a final example of the physiological sequestration of defensive chemicals from prey items, some authors have argued that the enhanced concentration of toxins from marine phytoplankton that accumulate in filter feeding bivalves should be considered a form of sequestration of chemical defenses. However, many, if not most, filter feeders are harmed by the ingestion of these toxins, 46 so any benefit of reduced predation levels may be outweighed by costs. Yet some bivalves are particularly resistant to phytoplankton toxins like those that cause paralytic shellfish poisoning (PSP). For example, some species of butter clam ( Saxidomus ) are 1 to 2 orders of magnitude more resistant to the effects of saxitoxin (Structure 4.8) produced by red-tide forming dinoflagellates than other co-occurring bivalves. 47 These clams sequester the toxins for up to two years in their siphon, the most exposed part of the animal and thus the most vulnerable tissue to predation, and use these sequestered toxins as a chemical defense against predation by siphon-nipping fishes. 48 Because they were less susceptible to siphon nipping, clams containing saxitoxin consistently extended their siphons further into the water column, presumably increasing their access to food. These sequestered toxins were effective deterrents against a range of potential clam predators, including sea otters. 49 Otters are historically rare in areas where toxic phytoplankton blooms are common, but are present where these blooms have been rare, so the sequestration of phytoplankton defenses by bivalves may limit the distribution of this important predator. Otters are also voracious predators of sea urchins, which can reach high numbers in the absence of otters, and devastate kelp beds through their grazing activities. 50,51 Thus, in the absence of otters, ecosystem structure and function are altered dramatically, so the sequestration of toxins from phytoplankton may dramati- cally alter nearshore communities like kelp beds through indirect effects on keystone species such as sea otters. 49 However, because areas prone to blooms of toxic phytoplankton may also be more subject to degradation by humans, including loading of nutrients and pollutants, a causal link between red tides and kelp forest health may be difficult to conclusively demonstrate. 3. Predator Detection and Avoidance There are three main types of chemical cues that prey use as warnings of the threat of predation: (1) those actively released by conspecifics that can serve as warning signals, (2) those released passively when prey tissue is damaged, and (3) odors released directly by predators. Much of this work has involved aquatic vertebrates (fishes, 52–56 amphibians, 57 and also freshwater algae 58 ), which often use chemical cues released by conspecifics injured by predators as an alarm signal and take appropriate predator avoidance measures such as hiding or reducing movement. However, a diverse array of mobile marine invertebrates appear to exhibit similar responses to the presence of injured or stressed conspecifics. 59–62 Chemicals released when organisms are attacked can serve to mark a location as dangerous to conspecifics. Many gastropods leave a slime trail behind them as they move, which can allow for easier location by conspecifics in search of mates. However, when sufficiently molested (as by a predator), Navanax inermis secretes a mixture of bright yellow chemicals (navenones A–C; Structures 4.9–4.11) into its slime trail, which causes an avoidance response in trail-following N N N N OH O H NH 2 H H OH NH 2 H H CNH 2 O 4.8 9064_ch04/fm Page 163 Tuesday, April 24, 2001 5:17 AM © 2001 by CRC Press LLC 164 Marine Chemical Ecology conspecifics. 60 Bioassay-guided fractionation of snail slime indicated that the navenones were responsible for the trail-breaking behavior and may be used as a warning cue by conspecifics. Other opisthobranchs can take advantage of species-specific chemicals in the slime trails and use them to track prey. The nudibranch Tambja abdere sequesters compounds (the tambjamines; see Structures 4.12–4.15) from its bryozoan prey that serve as deterrents against predation by fishes, and secretes these compounds in low amounts into the slime trail. 63 The predatory nudibranch Roboastra tigris preys on Tambja and uses the low concentrations of tambjamines in the slime trail to locate its prey. However, when attacked by Roboastra , Tambja secretes a mucus containing a higher concentration of tambjamines, causing Roboastra to break off the attack. This particular study highlights how the function of compounds can be altered not only by changes in structure, but also by changes in concentration: the tambjamines attracted predators at low concentrations, but repelled them at higher levels. 63 The slime trail examples of alarm pheromones offer systems that are relatively tractable experimentally, since chemical cues are bound to the substrate in the mucus. More frequently, chemicals involved in detection of danger are waterborne, posing significant challenges to inves- tigators, including accurate reproduction and characterization of the stimulus and the effects of moving water on the dispersal of chemical signals. 7,64,65 This is not a trivial point given that even moderate turbulence can have a substantial effect on chemical concentrations and the spatial distribution of an odor plume, 66 and thus an organism’s ability to locate an odor source. 65,67 Investigators in the lab have attempted to mimic natural field conditions using flumes (see Section II.C.1 for a more complete description of these methodological issues). As an example, an exper- iment with an intertidal marine gastropod used a flume with some vertical drop to mimic the organism’s intertidal habitat and tested the effects of the chemical scent of both predators and injured conspecifics on foraging behavior. 62 Gastropod activity was reduced by odors from crushed conspecifics or from crushed conspecifics and crabs (predators). Additionally, more snails sought refuge out of the water in the presence of these cues. However, when gastropods were starved, the predator and injured conspecific cues had no effect on snail behavior, suggesting that physiological state and diet history of the prey organisms may alter their willingness to take risks. In addition to their ecological importance, these findings also suggest that the common procedure of starving test organisms before use in bioassays may significantly alter results, as has been demonstrated in some feeding bioassays. 68 Specific chemical substances associated with flight responses have rarely been isolated, but this has apparently not been necessary for the adaptation of this phenomenon to applied problems. As one example, spider crabs in the genus Libinia are a nuisance for lobster fishermen in the north- eastern United States because they have little market value, consume bait, and increase the number N O 4.9 O HO 4.10 O 4.11 N H N OMe X Y NHR 4.12 X = H Y = H R = H 4.13 X = Br Y = H R = H 4.14 X = H Y = H R = i-Bu 4.15 X = H Y = Br R = i-Bu 9064_ch04/fm Page 164 Tuesday, April 24, 2001 5:17 AM © 2001 by CRC Press LLC Chemical Ecology of Mobile Benthic Invertebrates 165 of person-hours required to process traps. When crushed spider crabs were placed in lobster traps, catches of spider crabs decreased markedly, while catches of commercially valuable rock crabs and lobsters were unaffected. 69 Spider crabs (Libinia dubia) also decrease feeding rate in response to predator odor. 70 Although the mechanistic details of a species-specific alarm cue are unresolved in this case, it seems unlikely that this would concern lobstermen who utilize this “technology” to increase their livelihood. Flight responses are unlikely to be effective when predators are more mobile than prey, and in these cases the presence of predators can induce morphological or chemical changes designed to reduce their susceptibility to predation. Not surprisingly, “inducible defenses” appear to be partic- ularly common among sessile marine organisms including seaweeds, 71,72 bryozoans, 73 and cnidar- ians, 74 phytoplankton, 75 and among terrestrial plants. 76 However, the phenomenon is by no means restricted to sessile organisms, as inducible defenses have been extensively studied in freshwater rotifers 77 and cladocerans. 78 Marine mobile invertebrates such as snails 79–81 and mussels 82 have also been shown to exhibit morphological shifts in the presence of highly mobile predators such as crabs. Three species of intertidal snail, Nucella lamellosa, Nucella lapillus, and Littorina obtusata, all produce thicker shells when subjected to water containing effluent from decapod crabs that commonly prey on snails. N. lamellosa exhibits even greater induction of shell thickness when exposed to water in which crabs were consuming conspecifics. 79 A combination of predator and killed prey appears to be the most effective stimulus for eliciting a range of antipredator behav- iors. 62,79 However, none of these studies demonstrate that the measured increase in the defensive trait results in a decrease in susceptibility to predation, although Leonard et al. 82 showed that the increased shell thickness of mussels exposed to green crabs and injured conspecifics increased the force required to break the shells. This type of correlative approach is widespread, as only a few marine studies involving inducible defenses (and none with mobile invertebrates) have directly demonstrated that the induc- tion results in a decrease in the susceptibility of the organism to predation. 71,72 Statistically signif- icant differences in shell thickness or concentrations of defensive chemicals may or may not meaningfully affect predator preferences in ecologically relevant field situations. For chemical defenses, compound dose–response relationships may be nonlinear, and threshold levels of defense could be sufficient to deter predators so that further induction has little additional benefit. Thus, future studies should focus on directly demonstrating whether an induced response reduces pre- dation on prey organisms. Implicit in any evolutionary argument for inducible defenses is the idea that defenses are costly to deploy, and, thus, in situations where attack is predictable, they can be selectively deployed during periods of maximum predator pressure. 83 However, unambiguous demonstrations of the fitness costs of inducible defenses for marine organisms are rare. Many advances in measuring the costs of induced defense have been made in those systems in which the organism induces defensive characteristics after being exposed to a chemical cue indicative of predator presence, as this allows quantification of the costs of induction without the confounding influence of tissue loss due to consumption. 73 The ability of waterborne cues from predators and damaged prey to induce a morphological change in gastropods and bivalves 79–82 suggests that these animals may be useful study organisms for addressing theoretical issues surrounding inducible defenses. B. CONSEQUENCES OF FEEDING DETERRENTS FOR PREDATORS 1. Susceptibility of Consumers to Defensive Chemicals An emerging generalization from studies of the susceptibility of consumers to prey chemical defense is that many small, low-mobility invertebrates such as amphipods, polychaetes, shell-less gastro- pods, and crabs readily consume seaweeds that produce chemicals that deter feeding by larger, mobile grazers like fishes and urchins. 30,38,39,84–87 From most of these studies it is unclear whether 9064_ch04/fm Page 165 Tuesday, April 24, 2001 5:17 AM © 2001 by CRC Press LLC [...]... Prog Ser., 168, 187, 1998 92 Hay, M.E., The ecology of seaweed-herbivore interactions on coral reefs, Coral Reefs, 16, S67, 1997 © 2001 by CRC Press LLC 90 64_ ch 04/ fm Page 188 Tuesday, April 24, 2001 5:17 AM 188 Marine Chemical Ecology 93 Miller, M.W and Hay, M.E., Coral-seaweed-grazer-nutrient interactions on temperate reefs, Ecol Monogr., 66, 323, 1996 94 Duffy, J.E and Hay, M.E., Strong impacts of... Decho, A.W., Browne, K.A., and Zimmer-Faust, R.K., Chemical cues: why basic peptides are signal molecules in marine environments, Limnol Oceanogr., 43 , 141 0, 1998 140 Rittschof, D., Peptide-mediated behaviors in marine organisms, J Chem Ecol., 16, 261, 1990 141 Zimmer-Faust, R.K., Tyre, J.E., Michel, W.C., and Case, J.F., Chemical mediation of adaptive feeding in a marine decapod crustacean: the importance... Marine Natural Products, Comstock, Ithaca, NY, 1992 4 Pawlik, J.R., Marine invertebrate chemical defenses, Chem Rev., 93, 1911, 1993 5 Hay, M.E., Marine chemical ecology: what’s known and what’s next?, J Exp Mar Biol Ecol, 200, 103, 1996 6 McClintock, J.B and Baker, B.J., A review of the chemical ecology of Antarctic marine invertebrates, Am Zool., 37, 329, 1997 7 Hay, M.E., Stachowicz, J.J., Cruz-Rivera,... Oceanogr., 34, 1367, 1989 65 Weissburg, M.J and Zimmer-Faust, R.K., Life and death in moving fluids: hydrodynamic effects on chemosensory-mediated predation, Ecology, 74, 142 8, 1993 © 2001 by CRC Press LLC 90 64_ ch 04/ fm Page 187 Tuesday, April 24, 2001 5:17 AM Chemical Ecology of Mobile Benthic Invertebrates 187 66 Moore, P.A., Weissburg, M.J., Parrish, J.M., Zimmer-Faust, R.K., and Gerhardt, G.A., Spatial distribution... notably, chemical defenses produced by tropical seaweeds have been widely implicated in the persistence of these species in areas of intense herbivory like coral reefs1,3 (also see Chapter 6 in this volume) © 2001 by CRC Press LLC 90 64_ ch 04/ fm Page 167 Tuesday, April 24, 2001 5:17 AM Chemical Ecology of Mobile Benthic Invertebrates 167 AcO CHO CHO 4. 17 HO 4. 16 HO CHO CHO 4. 18 In contrast to the well-known... behavioral and ecological world within which chemicals act as signals The resulting blend of ecologically realistic bioassays and rigorous © 2001 by CRC Press LLC 90 64_ ch 04/ fm Page 1 84 Tuesday, April 24, 2001 5:17 AM 1 84 Marine Chemical Ecology chemical separation, quantification, and structural elucidation has yielded quantum leaps in our understanding of chemical mediation of interactions among organisms... 1161, 1989 © 2001 by CRC Press LLC 90 64_ ch 04/ fm Page 190 Tuesday, April 24, 2001 5:17 AM 190 Marine Chemical Ecology 146 Young, C.M., Tyler, P.A., Emson, R.H., and Gage, J.D., Perception and selection of macrophyte detrital falls by the bathyal echinoid Stylocidaris lineata, Deep Sea Res I, 40 , 147 5, 1993 147 Moore, P.A and Atema, J., Spatial information in the three-dimensional fine structure of an aquatic... 128, 48 9, 1997 119 Poore, A.G.B and Steinberg, P.D., Preference–performance relationships and effects of host plant choice in an herbivorous marine amphipod, Ecol Monogr., 69, 44 3, 1999 © 2001 by CRC Press LLC 90 64_ ch 04/ fm Page 189 Tuesday, April 24, 2001 5:17 AM Chemical Ecology of Mobile Benthic Invertebrates 189 120 Duffy, J.E and Paul, V.J., Prey nutritional quality and the effectiveness of chemical. .. M.R., Chemical attraction of newly hatched oyster drills, Biol Bull., 1 64, 49 3, 1983 129 Boyle, P.R., Responses to water-borne chemicals by the octopus Eledone cirrhosa (Lamarck 1798), J Exp Mar Biol Ecol., 1 04, 23, 1986 130 Glynn, P.W., An amphinomid worm predator of the crown-of-thorns sea star and general predation on asteroids in eastern and western Pacific coral reefs, Bull Mar Sci., 35, 54, 19 84 131... concentrated if the extract from a three-dimensional organism is applied to a twodimensional surface; here surface extraction techniques will be most relevant.169,1 74 Slow release of organic extracts from sessile invertebrates or seaweeds can be achieved by placing them into © 2001 by CRC Press LLC 90 64_ ch 04/ fm Page 1 74 Tuesday, April 24, 2001 5:17 AM 1 74 Marine Chemical Ecology Phytagel discs which can be . H 4. 13 X = Br Y = H R = H 4. 14 X = H Y = H R = i-Bu 4. 15 X = H Y = Br R = i-Bu 90 64_ ch 04/ fm Page 1 64 Tuesday, April 24, 2001 5:17 AM © 2001 by CRC Press LLC Chemical Ecology of Mobile Benthic. predation. Chemicals are involved 4 90 64_ ch 04/ fm Page 157 Tuesday, April 24, 2001 5:17 AM © 2001 by CRC Press LLC 158 Marine Chemical Ecology in mediating a diverse array of inter- and intraspecific. traits (e.g., protein, CHO HO CHO 4. 18 CHO AcO CHO 4. 17 HO 4. 16 90 64_ ch 04/ fm Page 167 Tuesday, April 24, 2001 5:17 AM © 2001 by CRC Press LLC 168 Marine Chemical Ecology caloric content, morphology)