Marine Chemical Ecology - Chapter 9 pptx

Resource Allocation in Seaweeds and Marine Invertebrates: Chemical Defense Patterns in Relation to Defense Theories Greg Cronin CONTENTS I.. Both groups areanchored in place, must grow i

Trang 1

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

Trang 2

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 includinggrowth, reproduction, maintenance, defense, and further resource acquisition It is often assumedthat 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, withinevolutionary and ecological constraints

While organisms must allocate resources to the above-mentioned processes, resources varyqualitatively and quantitatively among species For example, autotrophs and heterotrophs havefundamentally different modes of resource acquisition; the former acquires energy from solarradiation or reduced minerals (i.e., abiotic sources), and the latter acquires energy from reducedcarbon molecules (i.e., biotic sources) This chapter attempts to address how differences amongautotrophs, heterotrophs, and mixitrophs affect resource allocation Mixitrophic sessile invertebratesshare several biological and ecological similarities with autotrophic seaweeds Both groups areanchored in place, must grow in an open manner to acquire resources (light for both groups andplankton among filter feeding invertebrates), have modular body plans,9 can regenerate from basalportions following a dormant period,10 and can regenerate tissue lost to disturbance or partialpredation.11,12 These similar biological traits result in similar ecological strategies; both groups aretolerant 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 andthen 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 generalterm 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 greaterproportion 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 defensessubtracts 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 conditionswith little predation pressure, as organisms that allocate heavily towards further resource acquisitionand growth would likely be superior competitors Of course, the context in which these interactionstake 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 haveallelopathic effects on competitors as well as defensive properties against predators, then thedefended organism may compete well regardless of the abundance of predators Under physicallystressful conditions, an allocation pattern that favors maintenance may be most adaptive sinceorganisms 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

Trang 3

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 algaehave some of the highest growth rates, doubling in size every few days, while some crust-formingcoralline algae have very slow growth rates, taking months to double in size.14 Ecologists havedetected 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., resourceacquisition) 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 surfacearea to volume ratio, a large amount of structural material, or compressed mats or turfs have reducedphotosynthesis due to self-shading or limited nutrient uptake, but are typically less susceptible andless 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., matesearching, 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.

Trang 4

B D EALING WITH N ATURAL E NEMIES

All organisms are composed of fixed carbon, biomolecules, and mineral nutrients, and thereforerepresent 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 Forexample, induction of chemical defenses can be viewed as using an avoidance strategy until beingdetected by a predator, tolerating a small amount of consumption that serves as the cue to makethe 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 lowdensities of predators, such as reef flats, sand plains, sea grass beds, and mangroves,20–23 ortemporally, 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 StressResource Acquisition Maintenance Defense

Trang 5

Tolerating consumption involves having rates of regeneration that can keep up with losses toconsumers Generally, organisms with a modular body plan such as plants and colonial invertebrateshave 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 portionsprotected in crevices of the reef (i.e., the basal portions avoid consumption here), but the tops ofthe filaments are quickly consumed by herbivores shortly after growing above the protectivecrevice 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 thegrasses, which have their meristems protected close to the ground or below ground, simply replacethe lost portion.13

Defending tissue against consumption involves making it less attractive to or shielding it frompotential consumers Defense is a common strategy among sessile or sluggish organisms, especiallyones 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 defensesused 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, sharpspines 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 internaltissues 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 asspicules and sclerites are distributed throughout the soft tissues of some sponges, cnidarians, andascidians Calcareous or siliceous spicules of sponges are arranged in specific configurations by alattice of spongin fibers, creating a tough skeleton that provides support and possible defense forthe organism The effectiveness of these structures as antifeedants is unclear as the sclerites fromgorgonians and soft corals deterred fishes,27,28 but the spicules from several sponges30 and anascidian31 did not deter fishes in bioassays

Calcium carbonate makes up as much as 90% of the dry mass14,32 of the hard thallus of seaweeds.This calcium carbonate does not form structures like spicules, but rather precipitates as smallspheres that would not likely pierce an herbivore that bit into it It was long believed that thiscalcium carbonate served like concrete to make the overall thallus harder to bite (i.e., a structuraldefense), 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 byherbivores even when it does not influence the hardness or nutritional value of food Under theseconditions, CaCO3 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 chemicaldefenses (see below), alternative uses of these defenses may help defray their costs Hard chitonouscoverings 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 Theprecipitation of calcium carbonate from seawater is a consequence of photosynthesis altering pHand CO2–3 concentrations,14,37 hence the cost of producing this defense may be considered low.However, CaCO3 is an opaque powder that could shade chloroplasts, costing the seaweed ormixitrophic invertebrates photosynthetic potential Calcareous coralline algae are among the slowestgrowing seaweeds.16

Trang 6

2 Associational Defenses

Associational defenses occur when a species gains protection from a natural enemy by associatingwith 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, beunaffected, 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 defensesinto one of these catagories because the impact of the interaction on the defending species istypically 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 ofmany 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 protectingthe basibiont with an unpalatable covering Such interactions include associations betweenwhelk–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 thereare examples of palatable epibionts increasing the susceptibility of the basibiont to predators Thissituation was termed “shared doom”41 as both species in the association are consumed together.Nonepibiotic defensive mutualisms include clown fish–anemone, amphipod–hydroid,46 andsome seaweed–herbivore interactions.47–49 For example, the coralline alga Neogoniolithon strictum

gains protection from fouling organisms (which could interfere with resource acquisition viaexploitative competition) from the crab Mithrax sculptus, even though Neogoniolithon does notdirectly provide the crab with significant food.49Neogoniolithon is a very hard, calcified seaweedthat is defended structurally, and perhaps chemically, against herbivores, including Mithrax, byCaCO3 The crab benefits by consuming epiphytes that it clears from Neogoniolithon and by usingthe hard seaweed as shelter from predators Branches of the hard seaweed provide a shelter for thecrabs: 20% of crabs tethered near the seaweed were consumed within 30 min, while 100% of crabstethered 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., thehost provides both food and habitat to the protected host) Small relatively immobile invertebratesreduce predation by associating with noxious hosts: these associations can be specialized50–54 orgeneralized.33,55–59 Predatory associational defenses are often chemically mediated, includingsequestration of host chemical defenses by the defended species Sequestration is most commonamong specialists50–54 but there are examples of larger generalists being able to sequester chemicaldefenses from their diet.33,59

3 Nutritional Defenses

An organism that is of low nutritive value may be protected from consumption because it is notworth eating.35,60 Optimal foraging theory would dictate that any would-be predator should foragefor more valuable prey This strategy is available to seaweeds and gelatinous animals, but is generallyunavailable to most animals, as their tissue is more nutritious.61 It is difficult to envision how anorganism allocates resources to nutritional defenses However, one can envision costs that may beassociated with this strategy; by maintaining itself at a low nutritional value, such an organism mayconstrain its ability to store nutrients and energy for lean periods or its ability for rapid growth

Trang 7

structures,62 but can also include more generic compounds such as sulfuric acid63,64 or CaCO3.33–36

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 therelated allocation costs of secondary metabolites, it is important to recognize that there are otherpotential costs of chemical defense that are unrelated to allocation These nonallocation costs includeecological, autotoxicity, and genetic costs Ecological costs occur when a secondary metabolitethat defends against one consumer makes the prey more susceptible to a second consumer Forexample, 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 byinterfering 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 theyare 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 marineorganism, 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 thanits costs reduce fitness, on average A growing literature on the evolution of chemical defensessuggests that decreased susceptibility to consumers can be achieved only by diverting materialsand energy from other functions.7,19,65–68 While there are several theoretical reasons to believe thatdefenses are costly in terms of trade-offs, this common assumption is supported by little directevidence.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 appropriatecurrency 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 differentbiological functions,70 (3) the amount of limiting resource allocated to different processes, (4) thecompetitive ability of organisms with different allocation patterns, and (5) some measure of fitnesstrade-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 secondarymetabolites with cost of chemical defenses because it is the defensive roles of these compoundsthat have been most studied However, it is important to recognize that the benefits of secondarymetabolites 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 multiplefunctions, the total cost of secondary metabolite production could be less than that of theseindividual functions summed together

The synthesis of secondary metabolites requires materials in the form of atoms that composethe secondary metabolites, energy to form covalent bonds between the atoms, the enzymes thatcarry out the formation reactions, the genetic material that codes and synthesizes the enzymes, andthe cellular machinery that maintains pH, ionic strength, and redox potentials within a range thatallow enzymes to function properly.85 Some materials such as hydrogen and oxygen are readilyavailable and cheap, and contribute little to the material cost of synthesis Other materials such asphosphorus and nitrogen are of limited supply in many marine habitats.86 The use of these rarematerials 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

Trang 8

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 HCO3) 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 molluscs50,54,59,86–88 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 carryconstruct-ing 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 vesicles92 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

Trang 9

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 larvae6,31,50,104–106 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

Trang 10

independent system support a model, that model is more robust Observations from another systemthat 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 thesemodels apply to seaweeds and marine invertebrates is addressed

A O PTIMAL D EFENSE T HEORY

The optimal defense theory (ODT) asserts that organisms allocate defenses in a way that maximizesfitness, and that defenses are costly (in terms of fitness) when enemies are absent However, in thepresence of enemies, defensive secondary metabolites can become beneficial when their costs areoutweighed by benefits gained with protection.7 This theory encompasses both evolutionary andecological 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 whenthe probability of attack is high In tropical latitudes where herbivory is generally more intensethan 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 Hay120 foundthat temperate seaweeds were eaten about twice as much as closely related tropical species, andthat secondary chemistry accounted for most of the observed variation in palatability Within aregion, seaweeds from areas of coral reefs where herbivory is intense often produce more potentand higher concentrations of chemical defenses than plants from habitats where herbivory is lessintense26,121 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 notheld when tested in additional locations in the Caribbean.126,127 The paucity of phlorotannins insome tropical seaweeds was attributed to their ineffectiveness against tropical herbivores,128–130

although phlorotannins from temperate seaweeds can deter some tropical herbivores.125 Becausegeographic patterns of phlorotannins and their impacts on herbivores are unclear, it is difficult todetermine 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 thefitness 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 valuabletissue by allocating fewer defenses to it Based on tissue value, seaweeds might be expected topreferentially defend meristems that are responsible for the production of new cells, holdfasts thatanchor the entire thallus to the substrate, reproductive tissues that are responsible for passing geneticmaterial to the next generation, and young vegetative tissue that represents a greater productivepotential 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 morevulnerable to small predators (i.e., pathogens) Therefore, surfaces that are greatly exposed toconsumers 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 mantleand digestive gland than in its foot, a pattern consistent with the ODT The digestive gland beingcombined with the gonad confounds the interpretation, given the fact that the nudibranch provisionsits eggs with high concentrations of defensive metabolites.50 Similarly, the dictyoceratid sponge

(see Pawlik et al and Wright et al

Trang 11

Dysidea herbacea, which sequesters brominated biphenyl ethers synthesized by symbiotic bacteria,

concentrates these secondary metabolites in their ectosomal area.89

Besides the location of the tissue, other characteristics that affect its risk of attack include itsnutritive value and its tenderness (i.e., lack of nutritional or physical defenses) In plants, youngtissues are usually more nutritious and more delicate than older tissues,131–133 placing them at higherrisk of being attacked, when all other factors are equal The ODT predicts that these high-risktissues should be heavily defended with chemicals

Patterns of within-individual defenses predicted by the ODT are borne out in many terrestrialplants.66,131,132 Exposed external tissues are usually better defended than internal tissues in roots,stems, leaves, seeds, bulbs, and tubers.66,131 Because young leaves are often more productive,nutritious, and delicate than older leaves, they are often endowed with higher concentrations ofsecondary metabolites than older leaves.66,131,134,135 Even though young foliage is more chemicallydefended than mature foliage, most herbivore damage occurs to young leaves135 because insectsusually perform better on young nutritious tissue than old tissue.134 However, most herbivorousinsects are feeding specialists that may have adapted to circumvent host allelochemicals.136

Although less is known about the within-plant distribution of secondary metabolites in weeds, it might be expected that the degree of within-plant variation in seaweeds would be lessthan in terrestrial plants because seaweeds have fewer differentiated parts than terrestrial plants.111,133

sea-Terrestrial plants exhibit a greater division of labor among plant parts than seaweeds; roots uptakewater and nutrients, leaves capture light energy to nourish themselves and the rest of the plant, andstems and trunks extend the leaves toward the sun, support the weight of leaves, and transportwater, nutrient, and photosynthate from sources to sinks In contrast, the cells or parts of mostseaweeds are more independent; they absorb the majority of their own nutrients and make theirown photosynthate because most seaweeds lack structures for efficient translocation.137 However,exceptions occur among siphonous green seaweeds with coenocytic cellular structure and amongsome kelps with sieve elements, hyphal cells, and sieve tubes that allow photosynthate and othermaterials to be rapidly (10 to 70 cm h–1) translocated.138 Most support of seaweed parts comes fromseawater and not stiff structural tissue Although some seaweeds fit this description well, the degree

of differentiation varies considerably among species Kelps provide an example of a high degree

of tissue differentiation in seaweeds; they have strong holdfasts that anchor the huge seaweeds,large floats that raise the photosynthetic fronds toward the sunlight, stipes that attach the frondsand floats to the holdfast, and vascular tissue that transports materials from sources to sinks Similar

to terrestrial plants, kelps can display considerable within-plant variation in chemical defenses.139,140

These large seaweeds allocate more polyphenolics to the thin outer meristoderm than to the innercortex and medullary tissue.140 The amphipod Allorchestes compressa will consume the inner tissues

of Ecklonia if the meristoderm is broken, but will not eat the meristoderm.141 Intercalary meristems

as well as holdfasts, stipes, and sporogenous tissue of kelps also have more polyphenolics thanmost other infertile, nongrowing tissue.139,140 Within-individual variation in secondary metabolitesalso occurs in other brown seaweeds,133,142–144 some green seaweeds,25,26,145,146 red seaweeds,92,147,148

bryozoans,149 sponges,89 and gorgonians.150

1 Inducible Defenses

Vulnerability of prey to attack is positively related to the abundance of predators.7 Constitutivedefenses require resources to synthesize, maintain, and store (plus other potential costs mentionedabove) even when consumers are absent and the benefits of protection are not realized Hence, theODT predicts that allocation to constitutive defenses should be kept low when predators are absent

as a means to reduce the costs of defenses when the benefits of protection are not being realized.However, once predators have been detected and tissues become vulnerable to attack, the allocation

to defenses should be increased The induction of higher levels of defenses is thought to be anadaptation to minimize the cost of defenses until costs can be offset by the benefits of protection.100,151

Trang 12

Induction may have advantages in addition to cost savings, such as creating intraspecific variation

in defenses and presenting predators with a moving target that may make it more difficult for theevolution of counter adaptations.152

Induction of defenses depends on a reliable cue that predicts the probability of future attacks.Attack by a predator is a reliable cue that predators are present and the probability of furtherattack is high This cue is useful to seaweeds and sessile invertebrates because these organismsare likely to survive initial attack since they can tolerate partial predation Using predator attack

as a cue to induce defenses is not a good strategy for organisms that suffer high mortality duringthe initial attack Organisms less tolerant to predation, such as zooplankton, mobile invertebrates,and vertebrates, often use visual cues to see predators, chemical cues to smell predators, or detectcompounds such as alarm pheromones or body contents that conspecifics release when attacked

by predators.153,154

For seaweeds and colonial invertebrates, the stimulus for induced defenses most likely originates

at the point of predator damage, but for other parts of the prey to become less susceptible to furtherpredation, induction of defenses should occur throughout the individual Therefore, the stimulusshould signal the rest of the individual that an attack has occurred The mobilization of defenses

or resources to areas that are under attack would also require an effective translocation system As

a result of these two important roles of translocation in inducible responses, it would seem thatnon-vascular seaweeds would be highly constrained to responding to a localized attack (i.e., singlebite), but perhaps not a diffuse attack.5 For vascular plants, an easily envisioned mechanism for asystemic response to localized damage is the vascular transport system

Results of induction experiments are far from consistent Induction of chemical defenses hasbeen detected in seaweeds that have rudimentary vascular systems such as kelps155 and rock-weeds.156,157 Despite the constraints of lacking effective vascular systems, inducible chemical

defenses have been demonstrated in the brown alga Dictyota menstrualis.158 This alga had highconcentrations of secondary metabolites and a greater number of grazing scars when collected fromsites with high densities of herbivorous amphipods, compared to conspecifics collected from a site

with few amphipods When Dictyota collected from the site with few amphipods was grazed by

artificially increasing the number of amphipods using cages in the field, the alga responded byincreasing the concentrations of secondary metabolites and by becoming less palatable to amphipods

in laboratory feeding assays.158

Other brown seaweeds also display induced resistance to herbivory in response to actual or

simulated grazing damage Padina gymnospora became less susceptible to grazing by the sea urchin

Arbacia punctulata within 0 to 5 days following actual or simulated urchin grazing, but this

resistance was lost 9 days after the damage occurred.159 The role of chemical defenses in the induced

resistance of P gymnospora is unknown, but a congener, Padina jamaicensis, becomes less

sus-ceptible to herbivores following attack by altering its growth form.160 P jamaicensis exists as a

resistant turf growth form when herbivore pressure is great but converts to a susceptible foliosegrowth form within 4 days of herbivore pressure being reduced

Herbivore damage can cause the growth of adventitious branches in brown seaweeds.143,158 ODTpredicts that adventitious branches should have elevated levels of defenses given that they grow in

response to grazer damage Consistent with this hypothesis, Dictyota menstrualis collected from

sites with high densities of amphipods had a high incidence of adventitious branches Adventitious

branches of Dictyota had elevated levels of secondary metabolites, although these higher levels of

secondary metabolites did not afford the adventitious branches additional protection from

amphi-pods in laboratory feeding assays.158 Another brown seaweed, Fucus distichus, produced

adventi-tious branches at herbivore grazing scars, and these adventiadventi-tious branches had higher concentrations

of phlorotannins relative to apical meristems and were less susceptible to littorine snails.143

Many seaweeds apparently do not induce higher levels of secondary metabolites when grazed

Clipping experiments have failed to induce increased defenses in the brown alga Ascophyllum

nodosum,81 the green seaweeds Halimeda, Udotea, and Caulerpa,3,101 and the kelp Hedophyllum

Trang 13

sessile.155 Urchin grazing failed to induce defense in the kelp Ecklonia.124 The pattern of defended individuals being located in habitats with intense predation pressure could be generated

better-by preferential grazing, local selection, or among-habitat variation in other environmental variables,

in addition to inducible defenses

While there are only a few cases of induction of chemical defenses among seaweeds, thephenomenon is very common among terrestrial plants.99 This discrepancy in the prevalence ofinducible defenses in terrestrial vs marine plants could be due to the different biologies of vascularterrestrial plants vs nonvascular seaweeds (e.g., the induction stimulus from localized damage maynot be efficiently translocated in seaweeds133), complex interactions between grazing damage andenvironmental conditions,161 or herbivore taxa studied,5 but the lesser amount of research onseaweeds relative to terrestrial plants may also explain much of the disparity

Variation of defenses in invertebrates also suggests that defensive levels and probability ofattack are positively related Inducible structures, morphs, and behaviors have been noted for marineinvertebrates,151,162–169 suggesting allocation costs for these defenses However, induced resistance

in invertebrates has never been demonstrated to be chemically mediated,162 but inducible physicaldefenses have been observed In bivalves, the shell is composed of an outer periostracum coveringtwo to four CaCO3 layers.9 The periostracum is living tissue that secretes the shell, but it may alsoprotect the outer CaCO3 layer from dissolution and aid in forming a tight seal when the valves arebrought together tightly The CaCO3 crystals are deposited within an organic matrix Organicmaterial in the matrix and periostracum accounts for 12 to 72% of the shell’s dry mass.170 Thecosts of producing shells help explain why molluscs in the presence of crushing surf or predatorsproduce thicker shells than conspecifics in calm areas with fewer predators;169 when crushing surf

or predators are present, the costs of producing thick shells are offset by the benefit of protection

B G ROWTH –D IFFERENTIATION B ALANCE H YPOTHESIS

The growth–differentiation balance hypothesis (GDBH) states that resources are allocated betweengrowth processes (e.g., cell division and enlargement) and differentiation processes (e.g., cellularspecialization and production of defensive chemicals) and that differentiation tends to occur aftergrowth, although some overlap may occur.8,171 Treatment of the GDBH has largely dealt withevolutionary and ecological responses among species or whole plants,8 respectively, along environ-mental gradients, but the tenets of the GDBH can also be used to predict within-individual allocation

of differentiation products of both seaweeds and invertebrates, because cells of each of these groupsgrow and differentiate

The GDBH, like the ODT, assumes that a trade-off (i.e., reduced growth rates) is associatedwith the production of chemical defenses.8 When considering young, actively growing tissue, the

ODT and GDBH predict opposite patterns The ODT predicts that young, actively growing tissuesshould be preferentially defended relative to older tissue, all else being equal, because young tissuesare more valuable to the fitness of the plant (i.e., meristems make new cells and, thus, contributemuch to the future productivity of the plant) and are more vulnerable (i.e., often delicate andnutritious).66,131,132,135 In contrast, the GDBH predicts that actively growing tissue should be lessdefended than differentiated tissue because growth processes precede differentiation processes.There are numerous examples of the concentrations of secondary metabolites being higher inactively growing than in older tissue of terrestrial plants.66 Although these examples support theODT, they need not contradict the GDBH Because terrestrial plants can effectively translocatematerials among plant parts,172 secondary metabolites can be synthesized in differentiated tissuesand then be exported to actively growing regions (i.e., site of highest compound concentration neednot equal site of synthesis).8,131 The GDBH may be better tested in organisms with limited ability

to translocate secondary metabolites, like some chemically defended seaweeds

Cronin and Hay133 used the brown alga Dictyota ciliolata to test the GDBH because this alga

is defended from sympatric herbivores by diterpenoid secondary metabolites, grows at apical

Trang 14

meristems, and does not contain structures associated with translocation.133,137 The actively growing

apices of Dictyota contained lower concentrations of secondary metabolites than older parts of the

thallus, were more delicate (i.e., had fewer structural defenses), and were highly preferred overolder tissues by herbivorous amphipods and urchins Assays using artificial diets indicated that thehigher palatability of apices was chemically mediated and was not due to differences in toughness

Similarly, the actively growing apices of Zonaria angustata contained fewer

phlorotannin-contain-ing physodes and were more palatable to an amphipod than older regions of the thallus, with theinteresting exception that the apical cell maintained a high concentration of physodes, apparently

by an uneven sharing of physodes during mitosis; the majority of physodes remained in the cellthat was to become the new apical cell, while the other daughter cell began its existence with littlechemical protection.93 In contrast, older tissues which are less involved with growth processes than

the apices, contained high concentrations of physodes Therefore, the apical cells of Zonaria did

not have to allocate a great proportion of resources to producing physodes (i.e., there was noapparent trade-off between growth and differentiation), but the young, physode-poor daughter cellsapparently had to divide, grow, and mature before attaining the level of physodes found in oldertissues (i.e., there is a trade-off between growth and differentiation in these cells) The level of

dissection of Dictyota did not allow comparison of the apical cell with the rest of the apex,133 but

the fact that apical tissue of Zonaria (with the exception of the apical cell) had lower concentrations

of secondary compounds and/or associated structures suggests that these seaweeds adhere to the

GDBH, though Zonaria has found a way to optimally defend the apical cell through uneven sharing

of physodes As another example, young apices of Fucus distichus were preferred over the older portion by the snail Littorina sitkana, and the concentration of phlorotannins in the apices was only

half that of the older sections.143 This example of lower phlorotannins in the meristems of F disticus

relative to older sections is contrary to the pattern seen during a broader survey of allocation patterns

in rockweeds.144 These patterns of chemical defenses and susceptibility to herbivores in Dictyota and Zonaria are contrary to the ODT and the patterns described for terrestrial plants They are

consistent, however, with allocation patterns of the GDBH which predicts that apices, which areactively involved in growth processes, would have low levels of defensive secondary metabolitesand would be less tough than older tissue because cell walls have not yet matured

Other seaweeds show within-thallus pattern of chemical defenses that are different from those

seen in Dictyota and Zonaria, but are more typical of patterns observed in terrestrial plants As

noted above, kelps allocate more secondary metabolites to their meristems and other young tissues

than to older tissues Why should Dictyota and Zonaria follow the pattern predicted by the GDBH while Halimeda,25–26 Neomeris,146 rockweeds173 143), kelps,173 and terrestrial plantsoften do not? One important distinction between the former and latter groups is that the formergroup does not have structures to effectively translocate materials All seaweeds probably sharesome resources among cells, but the ability to translocate materials far distances is most advanced

in coenocyctic green seaweeds and some brown seaweeds, including kelps and rockweeds.137,138

Green algae of the genus Halimeda show incredible control over allocation of resources to growth, defense, and resource acquistion For example, Halimeda spp acquire resources during the day,

grow at night,25 and contain both structural and chemical defenses that are differentially allocated

to different portions of the thallus.25,26,101 The alga initiates these new segments at night whileherbivorous fishes are inactive and defends the young, delicate, nutritious (i.e., vulnerable) segmentswith more potent and higher concentrations of feeding deterrents than older segments.25–26 Thesegreen seaweeds are even capable of translocating organelles; new, non-pigmented segments areproduced at night, and the plant waits to translocate chloroplasts into the new segments until daytimewhen they would be useful for photosynthesis.25 As the new segments calcify and become lessnutritious, the concentrations of chemical defenses diminish (i.e., nutritional and structural defensespartially replace chemical defenses) This tight control over resource allocation is made possible

(see Van Alstyne

Định dạng
Số trang	29
Dung lượng	602,54 KB