325 Resource Allocation in Seaweeds and Marine Invertebrates: Chemical Defense Patterns in Relation to Defense Theories Greg Cronin CONTENTS I. Overview 325 II. Allocation of Finite Resources 326 A. The Model 326 B. Dealing with Natural Enemies 328 1. Structural Defenses 329 2. Associational Defenses 330 3. Nutritional Defenses 330 4. Chemical Defenses 330 III. Allocation of Resources to Secondary Metabolites 331 IV. Allocation Models for Chemical Defense 333 A. Optimal Defense Theory 334 1. Inducible Defenses 335 B. Growth–Differentiation Balance Hypothesis 337 C. Carbon–Nutrient Balance Hypothesis 340 D. Environmental Stress Theory 341 E. Resource Availability Model 342 F. Plant Apparency Model 342 G. Spatial-Variation-in-Consumers Model 343 V. Final Remarks 344 Acknowledgments 345 References 345 I. OVERVIEW To be successful, all organisms must acquire resources. They must also tolerate, avoid, or defend against becoming a resource for consumers, at least until after reproduction. The majority of this volume deals with how organisms use chemicals to defend themselves from consumers, though secondary metabolites affect their interactions with competitors, parasites, commensals, conspecifics, 9 9064_ch09/fm Page 325 Tuesday, April 24, 2001 5:22 AM © 2001 by CRC Press LLC 326 Marine Chemical Ecology and the abiotic environment. 1–6 This chapter discusses how organisms allocate acquired resources to various life processes, including the production of secondary metabolites. The finite resources available to organisms must be allocated to several life processes including growth, reproduction, maintenance, defense, and further resource acquisition. It is often assumed that a resource allocated to one process incurs a cost to the remaining processes because the resource is diverted away from them. 7,8 It is also assumed that natural selection acts to optimize the allocation of resources to best suit the life history and environment for a particular organism, of course, within evolutionary and ecological constraints. While organisms must allocate resources to the above-mentioned processes, resources vary qualitatively and quantitatively among species. For example, autotrophs and heterotrophs have fundamentally different modes of resource acquisition; the former acquires energy from solar radiation or reduced minerals (i.e., abiotic sources), and the latter acquires energy from reduced carbon molecules (i.e., biotic sources). This chapter attempts to address how differences among autotrophs, heterotrophs, and mixitrophs affect resource allocation. Mixitrophic sessile invertebrates share several biological and ecological similarities with autotrophic seaweeds. Both groups are anchored in place, must grow in an open manner to acquire resources (light for both groups and plankton among filter feeding invertebrates), have modular body plans, 9 can regenerate from basal portions following a dormant period, 10 and can regenerate tissue lost to disturbance or partial predation. 11,12 These similar biological traits result in similar ecological strategies; both groups are tolerant of some consumption and are often defended by structural or chemical defenses. 1–6 This chapter briefly discusses the various processes to which organisms allocate resources and then concentrates on allocation to secondary metabolites, the focus of this volume as a whole. Throughout this chapter, the term predator refers to any consumer of seaweeds or invertebrates. Therefore, herbivores, parasites, and consumers of animal prey are all covered under the general term predators. II. ALLOCATION OF FINITE RESOURCES A. T HE M ODEL Pie charts are used to represent the total amount of resources (i.e., materials and energy) acquired by an organism, and the size of each pie slice represents the proportion of total resources allocated to a particular process (Figure 9.1). The size of the pie is larger for organisms that allocate a greater proportion of resources to further resource acquisition. The reason chemical defenses are assumed, though rarely determined, to be costly is because the pie slice that represents allocation to defenses subtracts from the amount of resources available to the remaining processes. The relative success of each allocation pattern is dependent on the biotic and abiotic conditions in which the organism finds itself (Figure 9.2). Allocating resources heavily towards defense may be adaptive under conditions of intense predation pressure, but may be maladaptive under conditions with little predation pressure, as organisms that allocate heavily towards further resource acquisition and growth would likely be superior competitors. Of course, the context in which these interactions take place is far too complicated to address every possible caveat of allocation patterns. For example, in the case just given, if the secondary metabolites produced by the heavily defended species have allelopathic effects on competitors as well as defensive properties against predators, then the defended organism may compete well regardless of the abundance of predators. Under physically stressful conditions, an allocation pattern that favors maintenance may be most adaptive since organisms will be better equipped to maintain life processes under adverse physical conditions. 13 Important life processes that require energy and material resources include growth, maintenance, reproduction, further resource acquisition, and dealing with natural enemies. It is important to 9064_ch09/fm Page 326 Tuesday, April 24, 2001 5:22 AM © 2001 by CRC Press LLC Resource Allocation in Seaweeds and Marine Invertebrates 327 recognize that these various processes occur simultaneously within organisms and are interrelated in complex ways. Growth rates vary tremendously among marine organisms. Among seaweeds, filamentous algae have some of the highest growth rates, doubling in size every few days, while some crust-forming coralline algae have very slow growth rates, taking months to double in size. 14 Ecologists have detected correlations among growth form, growth rates, and strategies to deal with herbivores. 15,16 Forms with high surface area to volume ratio have high levels of photosynthesis (i.e., resource acquisition) but are generally susceptible to herbivores. However, rapid growth allows these species to replace tissue rapidly (i.e., they can tolerate consumers). In contrast, seaweeds with a low surface area to volume ratio, a large amount of structural material, or compressed mats or turfs have reduced photosynthesis due to self-shading or limited nutrient uptake, but are typically less susceptible and less tolerant to herbivores. 14,17,18 Once tissue is grown, it does not stop requiring resources. Material and energy are needed (1) to maintain tissue, whether or not it is actively growing, (2) for reproductive effort (e.g., mate searching, gamete production, and parental care), (3) for the acquisition of additional resources, and (4) for dealing with natural enemies. The allocation of resources to dealing with natural enemies, especially predators, is the focus of this chapter. FIGURE 9.1 Conceptual model of allocation of resources among various life processes. The defense pie could be further divided into slices for defense against predator 1, defense against predator 2, defense against parasite 1, secondary metabolite 1, secondary metabolite 2, or secondary metabolite 3, since many organisms produce multiple secondary metabolites that are differentially effective against different natural enemies. The top pie is larger (i.e., has more total resources) than the bottom pie because a greater proportion of resources is allocated to resource acquisition in the former situation. Maintenance Synthesis Transport Reproduction Storage Defense Acquisition Growth Acquisition Growth Storage Defense Transport Maintenance Reproduction Synthesis 9064_ch09/fm Page 327 Tuesday, April 24, 2001 5:22 AM © 2001 by CRC Press LLC 328 Marine Chemical Ecology B. D EALING WITH N ATURAL E NEMIES All organisms are composed of fixed carbon, biomolecules, and mineral nutrients, and therefore represent energy and nutrient resources for consumers. To be successful (i.e., grow, maintain self, and reproduce), organisms must avoid, tolerate, or defend against natural enemies. 19 Of course, these strategies are not mutually exclusive, and many species use more than one strategy. For example, induction of chemical defenses can be viewed as using an avoidance strategy until being detected by a predator, tolerating a small amount of consumption that serves as the cue to make the switch to the defensive strategy. Avoiding consumption involves being where and/or when consumers are rare or inactive. Seaweeds and sessile invertebrates can avoid predators spatially, by growing in habitats with low densities of predators, such as reef flats, sand plains, sea grass beds, and mangroves, 20–23 or temporally, by growing when predation pressures are low. 24–26 FIGURE 9.2 Different allocation patterns predicted to be adaptive along environmental gradients of abiotic stresses, competition, and predation pressures, which should select for high resource allocation to maintenance, resource acquisition, and defense, respectively. This model predicts allocation patterns for Grime’s plant strategies 13 and draws predictions from various chemical defense theories. Allocation to reproduction and growth are not shown for clarity. Competition Predation Abiotic Stress Resource Acquisition Maintenance Defense 9064_ch09/fm Page 328 Tuesday, April 24, 2001 5:22 AM © 2001 by CRC Press LLC Resource Allocation in Seaweeds and Marine Invertebrates 329 Tolerating consumption involves having rates of regeneration that can keep up with losses to consumers. Generally, organisms with a modular body plan such as plants and colonial invertebrates have a greater power of regeneration than organisms with determinant growth such as verte- brates. 11–12 Algal species that tolerate herbivory well are responsible for the high levels of produc- tivity that occur on coral reefs. 14,16 These fast growing filamentous algae have basal portions protected in crevices of the reef (i.e., the basal portions avoid consumption here), but the tops of the filaments are quickly consumed by herbivores shortly after growing above the protective crevice. This consumption is nonlethal, and the alga simply regrows what was lost. This is similar to the strategies of turf grasses: grazers or lawnmowers frequently cut the tops of blades, and the grasses, which have their meristems protected close to the ground or below ground, simply replace the lost portion. 13 Defending tissue against consumption involves making it less attractive to or shielding it from potential consumers. Defense is a common strategy among sessile or sluggish organisms, especially ones that must grow in an exposed manner to acquire resources (e.g., photosynthetic or filter- feeding organisms). These life history traits place constraints on the ability to avoid consumption, because fleeing or hiding from consumers is difficult or impossible. Four categories of defenses used by marine species are structural, associational, nutritional, and chemical defenses. 1. Structural Defenses Structures that defend marine organisms from being consumed can act as external shields, sharp spines located externally or internally, or support material that make tissues too hard to easily bite, making them a good first line of defense. 16,27–29 External structures that protect vulnerable internal tissues include the chitonous exoskeleton of crustaceans, calcarious shells of molluscs and barnacles, tests of echinoderms, and the tough tunics of ascidians. 9 Needle-like internal structures such as spicules and sclerites are distributed throughout the soft tissues of some sponges, cnidarians, and ascidians. Calcareous or siliceous spicules of sponges are arranged in specific configurations by a lattice of spongin fibers, creating a tough skeleton that provides support and possible defense for the organism. The effectiveness of these structures as antifeedants is unclear as the sclerites from gorgonians and soft corals deterred fishes, 27,28 but the spicules from several sponges 30 and an ascidian 31 did not deter fishes in bioassays. Calcium carbonate makes up as much as 90% of the dry mass 14,32 of the hard thallus of seaweeds. This calcium carbonate does not form structures like spicules, but rather precipitates as small spheres that would not likely pierce an herbivore that bit into it. It was long believed that this calcium carbonate served like concrete to make the overall thallus harder to bite (i.e., a structural defense), or perhaps the calcium carbonate could dilute the nutritional value of the seaweed (i.e., a nutritional defense). Recent studies have shown that calcium carbonate reduced feeding by herbivores even when it does not influence the hardness or nutritional value of food. Under these conditions, CaCO 3 was likely acting as a chemical defense, perhaps by raising the pH of guts or by increasing the efficacy of secondary metabolites. 33–36 Defensive structures can represent considerable costs to organisms, but as with chemical defenses (see below), alternative uses of these defenses may help defray their costs. Hard chitonous coverings serve a protective role to arthropods, but these structures also serve as an exoskeleton (likely the main reason for this adaptive covering), which defrays some of the defensive costs. The precipitation of calcium carbonate from seawater is a consequence of photosynthesis altering pH and CO 3 2– concentrations, 14,37 hence the cost of producing this defense may be considered low. However, CaCO 3 is an opaque powder that could shade chloroplasts, costing the seaweed or mixitrophic invertebrates photosynthetic potential. Calcareous coralline algae are among the slowest growing seaweeds. 16 9064_ch09/fm Page 329 Tuesday, April 24, 2001 5:22 AM © 2001 by CRC Press LLC 330 Marine Chemical Ecology 2. Associational Defenses Associational defenses occur when a species gains protection from a natural enemy by associating with a protective host. Mechanisms of protection provided to the defended species can be chemical, structural, camouflage, or aggressive. 5,38–42 The species providing protection can benefit, be unaffected, or be harmed by the association, resulting in the association being termed mutualistic, commensal, or parasitic/predatory, respectively. It is often difficult to place associational defenses into one of these catagories because the impact of the interaction on the defending species is typically not quantified. To add to this difficulty, the category of an interspecific interaction depends on the ecological context. For example, in the presence of light, zooxanthellae are mutualists of many sessile invertebrates, 43 but in darkness, they are commensal or parasitic. With defensive mutualisms protection from natural enemies is provided by the association with a protective host. Many suspected examples of defensive mutualisms are epibiotic associations, where an unpalatable epibiont benefits from the substrate provided by the basibiont while protecting the basibiont with an unpalatable covering. Such interactions include associations between whelk–bryozoan, 44 kelp–bryozoan, 40 clam–algae, 45 and mussels serving as the basibiont for hydro- zoans, sponges, barnacles, and algae. 41,42 Epibionts do not always protect the basibiont, and there are examples of palatable epibionts increasing the susceptibility of the basibiont to predators. This situation was termed “shared doom” 41 as both species in the association are consumed together. Nonepibiotic defensive mutualisms include clown fish–anemone, amphipod–hydroid, 46 and some seaweed–herbivore interactions. 47–49 For example, the coralline alga Neogoniolithon strictum gains protection from fouling organisms (which could interfere with resource acquisition via exploitative competition) from the crab Mithrax sculptus , even though Neogoniolithon does not directly provide the crab with significant food. 49 Neogoniolithon is a very hard, calcified seaweed that is defended structurally, and perhaps chemically, against herbivores, including Mithrax , by CaCO 3 . The crab benefits by consuming epiphytes that it clears from Neogoniolithon and by using the hard seaweed as shelter from predators. Branches of the hard seaweed provide a shelter for the crabs: 20% of crabs tethered near the seaweed were consumed within 30 min, while 100% of crabs tethered away from the seaweed were consumed during the same time period. 49 Predatory associational defenses are the most commonly reported type of associational defense. These involve situations where the protective host is consumed by the defended species (i.e., the host provides both food and habitat to the protected host). Small relatively immobile invertebrates reduce predation by associating with noxious hosts: these associations can be specialized 50–54 or generalized. 33,55–59 Predatory associational defenses are often chemically mediated, including sequestration of host chemical defenses by the defended species. Sequestration is most common among specialists 50–54 but there are examples of larger generalists being able to sequester chemical defenses from their diet. 33,59 3. Nutritional Defenses An organism that is of low nutritive value may be protected from consumption because it is not worth eating. 35,60 Optimal foraging theory would dictate that any would-be predator should forage for more valuable prey. This strategy is available to seaweeds and gelatinous animals, but is generally unavailable to most animals, as their tissue is more nutritious. 61 It is difficult to envision how an organism allocates resources to nutritional defenses. However, one can envision costs that may be associated with this strategy; by maintaining itself at a low nutritional value, such an organism may constrain its ability to store nutrients and energy for lean periods or its ability for rapid growth. 4. Chemical Defenses Organisms defend themselves chemically by using compounds that are distasteful, toxic, or other- wise repulsive to consumers. 1–6 Most defensive compounds are secondary metabolites of unique 9064_ch09/fm Page 330 Tuesday, April 24, 2001 5:22 AM © 2001 by CRC Press LLC Resource Allocation in Seaweeds and Marine Invertebrates 331 structures, 62 but can also include more generic compounds such as sulfuric acid 63,64 or CaCO 3 . 33–36 The production, transport, storage, and maintenance of defensive compounds require the allocation of resources, and, hence, are often assumed to incur a cost to the organism (Figure 9.1). While this chapter concentrates on the allocation of resources by marine organisms and the related allocation costs of secondary metabolites, it is important to recognize that there are other potential costs of chemical defense that are unrelated to allocation. These nonallocation costs include ecological, autotoxicity, and genetic costs. Ecological costs occur when a secondary metabolite that defends against one consumer makes the prey more susceptible to a second consumer. For example, secondary metabolites often defend against generalist consumers, but can actually stim- ulate feeding by specialist consumers that have adapted to using a specific noxious host. 56 Auto- toxicity, or self-poisoning, is problematic because secondary metabolites can be deterrent by interfering with basic biological processes (thereby making them effective against a large number of consumers), but the compounds can poison the same organism that they are defending if they are not properly handled. Finally, genetic costs occur when genes that confer chemical resistance to natural enemies have negative pleiotrophic effects on other processes (separate from the diversion of resources). 65 Genetic costs of secondary metabolites have not been determined for any marine organism, but there is limited information on ecological, autotoxicity, and allocation costs. III. ALLOCATION OF RESOURCES TO SECONDARY METABOLITES For a trait to be selected for, or not selected against, its benefits should increase fitness more than its costs reduce fitness, on average. A growing literature on the evolution of chemical defenses suggests that decreased susceptibility to consumers can be achieved only by diverting materials and energy from other functions. 7,19,65–68 While there are several theoretical reasons to believe that defenses are costly in terms of trade-offs, this common assumption is supported by little direct evidence. 65 However, there is much circumstantial evidence that supports the idea that the produc- tion, maintenance, transport, and storage of secondary metabolites have associated costs. One of the main obstacles for studying the allocation of resources is determining the appropriate currency to measure cost. The different currencies that have been used include (1) the energy stored in chemical bonds, 69 (2) biomass allocated to various tissues or materials responsible for different biological functions, 70 (3) the amount of limiting resource allocated to different processes, (4) the competitive ability of organisms with different allocation patterns, and (5) some measure of fitness trade-off. 71 Allocation costs of secondary metabolites are discussed below, even though no direct measures of these costs with marine organisms have been made. 69 We tend to equate cost of secondary metabolites with cost of chemical defenses because it is the defensive roles of these compounds that have been most studied. However, it is important to recognize that the benefits of secondary metabolites are not limited to defenses against predators; secondary metabolites can also be used as defenses against fouling organisms, 72–77 microbes, 78–80 competitors, 81 and the damaging effects of UV radiation, 82 as well as aggregation or gamete attractants. 83,84 As a result of serving multiple functions, the total cost of secondary metabolite production could be less than that of these individual functions summed together. The synthesis of secondary metabolites requires materials in the form of atoms that compose the secondary metabolites, energy to form covalent bonds between the atoms, the enzymes that carry out the formation reactions, the genetic material that codes and synthesizes the enzymes, and the cellular machinery that maintains pH, ionic strength, and redox potentials within a range that allow enzymes to function properly. 85 Some materials such as hydrogen and oxygen are readily available and cheap, and contribute little to the material cost of synthesis. Other materials such as phosphorus and nitrogen are of limited supply in many marine habitats. 86 The use of these rare materials in secondary metabolites is probably costly as they limit many primary metabolic path- ways, which helps explain the rarity of secondary metabolites that contain N or P. 2 Fixed carbon 9064_ch09/fm Page 331 Tuesday, April 24, 2001 5:22 AM © 2001 by CRC Press LLC 332 Marine Chemical Ecology can also be limiting under certain conditions (e.g., under shaded conditions for seaweeds). This limitation is not a materials limitation because inorganic carbon (i.e., in the form of HCO 3 – )is abundant in the ocean. Rather, it is an energy limitation, since reduced carbon compounds are the energy currency in living systems. The principal anabolic pathways for secondary metabolites originate from just a few interme- diates of primary metabolic pathways, such as acetyl CoA, shikimic acid, and melvonic acid. 86 Among the important cofactors are ATP, NADPH, and S-adenosylmethionine, which need to be continuously regenerated via primary metabolic pathways of respiration or photosynthesis. The fact that secondary metabolism shares chemical precursors with primary metabolism means that secondary and primary metabolic pathways may compete for substrates and cofactors, strongly suggesting that trade-offs occur at the biochemical level. Sequestration of chemical defenses synthesized by prey or symbionts is observed in several marine invertebrates. Sequestration is a common phenomenon among molluscs 50,54,59,86–88 but has only rarely been demonstrated among other invertebrate groups. 52,89 By sequestering secondary metabolites, organisms are able to eliminate the costs of synthesis. There may be additional advantages of sequestration as well, such as providing chemical camouflage. 5,54,90 An interesting example of sequestration that can be interpreted as camouflage is the use of domiciles constructed of a chemically defended seaweed by the amphipod Pseudamp- hithoides incurvaria . 52 The amphipod does not physiologically incorporate its prey defensive compounds into its body, but rather behaviorally sequesters the compounds by remaining inside a bivalved domicile that the amphipod constructs out of the seaweed. The amphipod is palatable to fish once it is removed from the domicile, suggesting that the amphipod gains protection from predators by being camouflaged as seaweed. Such behavioral sequestration not only avoids the cost of synthesis (as does physiological sequestration), but also avoids many costs associated with storage, transport, maintenance, and autotoxicity; costs which physiological sequestration may not avoid. Potential costs associated with the domicile are the allocation of time and effort in construct- ing the domicile and the burden of carrying it around. For concentrations of secondary metabolites to be continuously maintained, production must keep up with growth (so increasing biomass does not dilute metabolites) and turnover. Turnover rates are probably species and compound specific. 69,91 Costs associated with maintaining secondary metabolites will depend on turnover rates and the degree at which breakdown products can be recycled by the organism. As with synthesis costs, organisms that sequester defenses may be able to avoid maintenance costs by simply eating another chemically laden meal. The storage of compounds can differ greatly between seaweeds and invertebrates. Compound storage in seaweeds is not well known, but it likely occurs at the subcellular level, in places such as cytoplasmic vesicles 92 and structures called physodes. 93 Animals can store secondary metabolites within cells as seaweeds do, 94 and they are also able to keep compounds in specialized organs or glands. For example, nudibranchs concentrate secondary metabolites in the dorsal mantle, 50 cer- rata, 96 digestive gland, 50,95–97 and in subepidermal structures called mantle dermal formations (MDF). 64,90,98 These structures, whether they are subcellular or storage organs, require materials to construct and energy to maintain. Related to costs of storage are costs of autotoxicity, or self-poisoning. Besides segregating secondary metabolites away from sensitive areas with storage structures, another way to reduce the cost of autotoxicity is to store defensive metabolites as inactive precursors and convert them to active compounds when they are needed for defense. 99,100 This process is termed activation in order to distinguish it from induction of defenses which refers to the longer term response in which the general defense mechanisms of an organism are increased above constitutive levels (induction is discussed below). Activation of chemical defenses is common among terrestrial plants, but has only been described for Halimeda spp. 101 and a sponge. 102 The major compound found in Halimeda is halimedatetraacetate, a compound that is not very deterrent against herbivores. Upon damage to the thallus, halimedatetraacetate is rapidly converted to halimedatrial, a much more deterrent 9064_ch09/fm Page 332 Tuesday, April 24, 2001 5:22 AM © 2001 by CRC Press LLC Resource Allocation in Seaweeds and Marine Invertebrates 333 compound. This activation of halimedatetraacetate is probably enzymatically mediated, though the enzyme has not been identified. It is also unknown how halimedatetraacetate is compartmentalized, but logic suggests that the compound is stored separately from the enzyme, and damage by an herbivore brings the two components of the reaction together. 101 Terrestrial ecologists suggested that autotoxicity might constrain the use of chemical defenses in developing organisms when they asked, “Why are embryos so tasty?” 103 It was hypothesized that chemical defenses might be fundamentally incompatible with development because bioactive compounds could have teratogenic effects on the embryo. However, chemical defenses are not completely incompatible with embryo development as many marine invertebrates produce chemi- cally defended eggs and larvae 6,31,50,104–106 as do some beetles and a few other terrestrial organisms. 103 The constraint of producing chemically defended embryos seems to have more to do with adults being capable of producing chemical defenses and provisioning the eggs, and less to do with a physiological incompatibility, since examples of chemically defended eggs and larvae come from species where the adults are known to be chemically defended. 104,105 Questions about the source of secondary metabolites (whether they are autogenic or provisioned by the parent), where compounds are located within larvae, mechanisms that prevent secondary metabolites from poisoning devel- opment, or how chemical defenses change ontogenically are only beginning to be addressed in marine organisms. 6,31,50,104–107 There may also be costs associated with transporting secondary metabolites. The fact that secondary metabolites are compartmentalized or otherwise stored means that they must be actively transported against a concentration gradient into a vesicle, physode, or similar storage structure. To this author’s knowledge, the details of these processes have not been determined for marine organisms. However, such intracellular transport of polar metabolites may be similar to the current models of (1) active transport of amino acids, sugars, ions, and other cellular nutrients, (2) receptor mediated endocytosis, or (3) ion trapping. 108 The production of vesicles, carrier proteins, receptors, and ion pumps requires materials and energy, so such intracellular transport likely involves costs. Intercellular transport is advantageous because it allows the movement of defenses to areas that are under attack by natural enemies. However, such capability of efficient transport requires a vascular system, expenditure of energy, and subjects additional cells to risk of autotoxicity. The prevalence of chemical defenses among marine organisms suggests that the benefits of protection outweigh the various costs listed above. The benefit most often documented by marine ecologists is the decrease in losses to predators. 1–6,109–111 Empirical evidence abounds that secondary metabolites reduce consumption by predators, probably because of the availability of methods to test the antifeedant effects of secondary metabolites against consumers in ecologically realistic manners. It is likely that defensive secondary metabolites serve multiple roles such as allelochem- icals, 112,113 antifoulants, 73–76,114 antibiotics, 78,115,116 sex attractants, 82,83,117–119 or settlement cues, 72 but ecologically realistic assays for these functions are in their infancy. 5 As an example, for a secondary metabolite to be beneficial as an antifoulant, it should be located near the surface of the organism so any would-be fouling organism can contact and respond to it. A major drawback for studying such metabolite functions is our lack of knowledge about small-scale storage and deployment of defenses (see above). Such alternative roles of secondary metabolites help defray secondary metab- olite costs by receiving benefits from multiple functions. IV. ALLOCATION MODELS FOR CHEMICAL DEFENSE Most chemical defense theories were proposed by terrestrial ecologists to explain evolutionary and ecological patterns that were observed in interactions between terrestrial herbivores and vascular plants. There are basic biological differences between the organisms that these theories were proposed for (e.g., largely angiosperms and insects) and the organisms of this volume (e.g., seaweeds, sessile invertebrates, and their noninsect predators). 111 However, for an ecological theory to be a useful predictive tool, it should be applicable to different systems. If observations from an 9064_ch09/fm Page 333 Tuesday, April 24, 2001 5:22 AM © 2001 by CRC Press LLC 334 Marine Chemical Ecology independent system support a model, that model is more robust. Observations from another system that are contrary to the model can provide insights that can allow refinement of current models. An overview of the more prominent chemical defense theories is provided below, and how these models apply to seaweeds and marine invertebrates is addressed. A. OPTIMAL DEFENSE THEORY The optimal defense theory (ODT) asserts that organisms allocate defenses in a way that maximizes fitness, and that defenses are costly (in terms of fitness) when enemies are absent. However, in the presence of enemies, defensive secondary metabolites can become beneficial when their costs are outweighed by benefits gained with protection. 7 This theory encompasses both evolutionary and ecological time scales, providing explanations for between-species, within-species, and within- individual variation in defenses. Several observations suggest that seaweeds allocate more resources to chemical defenses when the probability of attack is high. In tropical latitudes where herbivory is generally more intense than at higher latitudes, a higher concentration and greater diversity of lipophilic secondary metab- olites are produced by seaweeds. This pattern is predicted in Figure 9.2. Bolser and Hay 120 found that temperate seaweeds were eaten about twice as much as closely related tropical species, and that secondary chemistry accounted for most of the observed variation in palatability. Within a region, 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 26,121 23 122 for invertebrate examples). In contrast to patterns for lipophilic secondary metabolites, water-soluble phlorotannins (i.e., polyphenolics produced by brown seaweeds) were initially reported to be more abundant in tem- perate than tropical Indo-Pacific seaweeds. 123–125 However, this apparent latitudinal pattern has not held when tested in additional locations in the Caribbean. 126,127 The paucity of phlorotannins in some tropical seaweeds was attributed to their ineffectiveness against tropical herbivores, 128–130 although phlorotannins from temperate seaweeds can deter some tropical herbivores. 125 Because geographic patterns of phlorotannins and their impacts on herbivores are unclear, it is difficult to determine how allocation patterns of phlorotannins relate to the ODT. One prediction of the ODT is that within an organism, costly defenses are allocated to tissues in direct proportion to the vulnerability and the value of the tissue, on a per mass basis, to the fitness of the organism. Most seaweeds and sessile invertebrates can recover from partial preda- tion, 11,12,14,19 so they are able to tolerate some predation and may be able to sacrifice less valuable tissue by allocating fewer defenses to it. Based on tissue value, seaweeds might be expected to preferentially defend meristems that are responsible for the production of new cells, holdfasts that anchor the entire thallus to the substrate, reproductive tissues that are responsible for passing genetic material to the next generation, and young vegetative tissue that represents a greater productive potential than an equivalent amount of older vegetative tissue. Valuable tissues for sessile inverte- brates include holdfasts and gonads for reasons similar to those given for seaweeds. For all organisms, the tissues most exposed to attack by predators are external tissues. Even if a predator seeks internal tissue, it must first penetrate outer tissues to gain access. Additionally, because animals must ingest materials to obtain nutrition, the lining of their gut is made more vulnerable to small predators (i.e., pathogens). Therefore, surfaces that are greatly exposed to consumers should be heavily defended based upon vulnerability. 50,89,95 The Spanish dancer nudi- branch is an example of a marine organism that allocates defenses based upon such vulnerability to predation. This nudibranch had higher concentrations of chemical defenses in its dorsal mantle and digestive gland than in its foot, a pattern consistent with the ODT. The digestive gland being combined with the gonad confounds the interpretation, given the fact that the nudibranch provisions its eggs with high concentrations of defensive metabolites. 50 Similarly, the dictyoceratid sponge 9064_ch09/fm Page 334 Tuesday, April 24, 2001 5:22 AM © 2001 by CRC Press LLC (see Pawlik et al. and Wright et al. [...]... Ecological Roles of Marine Natural Products, Paul, V.J., Ed., Comstock Publishing, Ithaca, NY, 199 2, 24 4 Pawlik, J.R., Marine invertebrate chemical defenses, Chem Rev., 93 , 191 1, 199 3 5 Hay, M.E., Marine chemical ecology: what’s known and what’s next?, J Exp Mar Biol Ecol., 200, 103, 199 6 6 McClintock, J.B and Baker, B.J., A review of the chemical ecology of shallow-water antarctic marine invertebrates,... interest in chemical ecology and for countless conversations about chemical strategies among seaweeds REFERENCES 1 Bakus, G.J., Targett, N.M., and Schulte, B., Chemical ecology of marine organisms: an overview, J Chem Ecol., 12, 95 1, 198 6 2 Hay, M.E and Fenical, W., Marine plant–herbivore interactions: the ecology of chemical defense, Ann Rev Ecol Syst., 19, 111, 198 8 3 Paul, V.J., Seaweed chemical defenses... 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SPATIAL-VARIATION-IN-CONSUMERS MODEL The spatial-variation-in-consumers model (SVICM) was proposed by marine ecologists to explain both interspecific and intraspecific patterns of chemical defenses. production of differentiation products such as 90 64_ch 09/ fm Page 3 39 Tuesday, April 24, 2001 5:22 AM © 2001 by CRC Press LLC 340 Marine Chemical Ecology chemical defenses. Thus, defenses do not use. are among the slowest growing seaweeds. 16 90 64_ch 09/ fm Page 3 29 Tuesday, April 24, 2001 5:22 AM © 2001 by CRC Press LLC 330 Marine Chemical Ecology 2. Associational Defenses Associational