Marine Plant Herbivore Interactions PDF

Marine Plant-Herbivore Interactions: The Ecology of Chemical Defense Author(s): Mark E.
Hay and William Fenical Reviewed work(s): Source: Annual Review of Ecology and Systematics, Vol. 19 (1988), pp. 111-145 Published by: Annual Reviews Stable URL: http://www.jstor.org/stable/2097150 . Accessed: 31/03/2012 05:02
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Ann. Rev. Ecol. Syst. 1988. 19:111-45 Copyright ? 1988 by Annual Reviews Inc. All rights reserved
MARINE PLANT-HERBIVORE INTERACTIONS:The Ecology of Chemical Defense

Mark E. Hay
University of North Carolina at Chapel Hill, Instituteof Marine Sciences, Morehead City, North Carolina 28557
WilliamFenical
Institute of Marine Resources, Scripps Institution of Oceanography, University of California at San Diego, La Jolla, California 92093-0228
INTRODUCTION
Herbivoryhas a profound effect on seaweeds in both temperateand tropical communities(11, 17, 21, 33, 43, 47, 80, 124). This is especially trueon coral reefs where 60-97% (11, 42) of the total seaweed productionmay be removed by herbivores. To persist in marine communities, seaweeds must escape, deter, or tolerate herbivory. The ecological and evolutionary importanceof spatial and temporal escapes has been extensively studied for seaweeds and adequatelyreviewed in the recent literature(33, 45, 47, 71, 80). The ability of seaweeds to tolerateherbivoryhas received limited attention. On coral reefs, rapidly growing filamentousalgae are heavily grazed, but the algae quickly replace these losses and appearto be dependentupon herbivores to prevent their habitat from being overgrown by larger but less herbivoretolerant species (11, 71). Additionally, several seaweeds have spores or vegetative portionsthat can withstandgut passage; in some cases this significantly increases the growth rates of the newly settled spores (6, 122). These types of seaweeds may be considered herbivore tolerant. can deter some herbivores,the Although numerousseaweed characteristics effects of morphologyand chemistryhave been studied most thoroughly.The 111 0066-4162/88/1120-011 1$02.00
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general hypotheses and data supporting the importance of morphological deterrentshave been outlined previously (74, 75, 136, 137), as have some exceptions to the predictedpatterns(45, 70, 90). We do not review morphological defenses but do discuss how they interact with chemical defenses. Seaweeds may also deter herbivores by associating with other plants that interferewith herbivoreforaging or feeding. These associationaldefenses are just beginning to be investigated in marine systems (18, 47, 48, 76, 112). There is an implied chemical natureto these interactions,but it has not been rigorously investigated. In this paper we concentrate on the ecology of seaweed chemical defenses since this is a new and rapidly advancing area in which even recent reviews (45, 93) are outdated. Approximately 500-600 secondary compounds have been isolated from marinealgae (23, 24, 123). Many of these compoundspossess strongbiological activities in laboratoryassays (3, 23, 24, 27, 45, 52, 93, 104); however, their ecological functions under naturalconditions have been addressedonly recently. Seaweed secondary metabolites may function as herbivore deterrents(see below) or as allelopathic and antifouling agents (57, 85, 128). Recent investigations (52, 116) suggest that the primary function of many of these compounds is to deter herbivory. However, secondary metabolites also may have multiple or alternatefunctions. Below we review the available information on chemically mediated seaweed-herbivore interactions, compare their effects in marine vs terrestrialcommunities, and interpretthe robustness of present plant-herbivoretheory in light of the emerging marine patterns.
SECONDARY METABOLITESOF MARINE ALGAE

Seaweeds are similar to terrestrialvegetation in that they produce terpenes, aromatic compounds, acetogenins, amino acid-derived substances, and polyphenolics as secondary metabolites. They differ from terrestrialplants because they incorporatehalogens into their secondarymetabolitesand do not produce the nitrogen containing alkaloids common in some terrestrialplants (primarily legumes). Selected families and genera of all four divisions of seaweeds produce secondary metabolites. Within genera and families, some compounds are products of consistent biosyntheses, i.e. are produced by terpenoidor acetate-derivedbiosyntheses. The compounds are often speciesor genus-specific, and they have been used as taxonomic criteriato separate morphologically similar species within a single habitat(29). A summaryof the genera studiedand the compoundtypes observedare listed in Table 1. The primaryliteratureon this topic consists of 600 to 800 publications;most of these are accessible through recent reviews (23, 24, 104).
SEAWEED CHEMICALDEFENSES
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Red Algae (Rhodophyta)

The families Bonnemaisoniaceae, Plocamiaceae, Rhizophyllidaceae, and Rhodomelaceaetend to be particularly rich in biologically active compounds ranging in structurefrom simple aliphatichalo-ketonesand brominatedphenols to more complex monoterpenes, sesquiterpenes, and diterpenes (C1O, C15, and C20compounds) (23, 27, 28). Yields of these compounds (mass of compoundextractedper mass of plant) range from trace amountsto as much as 3-5% of the plant's dry mass (27, 28, 52). Genera that have been extensively studied include Laurencia, Plocamium, Asparagopsis, Bonnemaisonia, Ochtodes, Chondrococcus, and Sphaerococcus. However, many reportsof secondarycompoundproductionare less well documented(21, 23, 27). Most of the well-studied genera produce several related compounds (Table 1) with strong biological activity. The extreme example is the genus Laurencia, various species of which produce terpenoids and acetogenins of very complex types. Within the terpenes, over 400 different compounds representat least 26 differentstructuralclasses. At least 16 structural groups are novel and found only in Laurencia species (21, 24). One of the better known Laurencia metabolites is elatol (Figure 1), a chamigrene-classsesquiterpenoidthat is cytotoxic, ichthyotoxic, insecticidal, and deters feeding by reef fishes (52).
Green Algae (Chlorophyta)

The order Caulerpaleshas been studied extensively (53, 99-104, 107, 139). Families in this order are the Caulerpaceae, containing the single genus Caulerpa, and the Udoteaceae and Halimedaceae, containing the genera Halimeda, Tydemania, Penicillus, Udotea, Avrainvillea, Chlorodesmis, Pseudochlorodesmis, and others. Species in these genera produce a closely related group of sesquiterpenoid and diterpenoid compounds that exhibit broadbioactivity in pharmacologicalassays and deterherbivoresin both field and laboratoryassays (53, 103, 104). Approximately70 secondarymetabolites have been isolated from these seaweeds. Many are relatively unstable once isolated and purified, making it difficult to quantify their naturalconcentrations.Reportedyields range from trace amountsto 2% of whole plant dry mass, with most determinationsfalling between 0.2% and 1.5% (101, 103). However, the compounds are not uniformlydistributedthroughoutthe plant, and concentrationsin some plant portions may be 5%, or greater(53, 107). The diterpene trialdehyde, halimedatrial (Figure 1), produced by numerousspecies of Halimeda, is one of the betterstudiedand most bioactive compounds from this group. It is structurallyrelated to the powerful insect antifeedant,warburganal (102), and inhibits feeding by reef fishes (53, 107). Halimedatrialalso shows strong biological activities against bacteria, fungi, fishes, and the sperm, fertilized eggs, and larvae of sea urchins (103).
117
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Other families of green seaweeds are less well studied. The green alga Cymopolia barbata (Dasycladaceae) produces a series of terpene-hydroquinones (56; see Figure 1 for an example), as well as a water-solublephenolic compoundof the coumarinclass (86). This lattercompoundwas also isolated from the related alga Dasycladus vermicularus. Cladophora fascicularis (Cladophoraceae)produces a brominateddiphenyl ether of a structureclass not found in any other algal source (104).
Brown Algae (Phaeophyta)

Only brown seaweeds producepolyphenolics. Althoughthese compoundsare hypothesizedto function like tertestrialtannins(35, 116, 132, 134, 142), we emphasize that the polyphenolics in seaweeds differ chemically from those in terrestrial plants. In contrastto the complex biochemical origins of phenolics in terrestrial plants, algal phenolics are derivedfrom the simple C6 precursor, phloroglucinol(1,3,5-trihydroxybenzene)(Figure 1). Because of these chem(116) to ical differences, some authorshave used the term "phlorotannins" refer to the polyphenolicsproducedby brown algae. This term is appropriate since it emphasizes the differences between terrestrial"tannins"and their
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show antibiotIn laboratoryassays, some phlorotannins marinecounterparts. ic, antifungal, antialgal, and antilarvalactivities. Some also deter feeding by marine herbivores (35, 134). Phlorotanninsoccur in high concentrations (commonly 1-15% of dry mass) in manytemperatebrown seaweeds (22, 116, 132) but appearto be absent, or presentonly in low concentrations(less than 2% of dry mass), in tropical habitats (133, 143). seas, brown algae in the orderDictyotales In tropical and warm-temperate (Dictyota, Pachydictyon, Glossophora, Dictyopteris, Zonaria, and others) producecomplex mixturesof terpenoids,acetogenins, and terpenoid-aromatic (mixed biosynthetic origin) compounds (23, 84). The bicyclic diterpene alcohol pachydictyol-A (Figure 1) is a well-studied example of a diterpenoid from this group. This simple diterpenoidalcohol shows no inhibitoryeffects against fungi, bacteria, diatoms, or fertilized sea urchin eggs (36), yet it effectively deters feeding by tropical (52) and temperateherbivores(51, 54). Reported yields of the secondary compounds from dictyotacean algae are similar to those from red and green algae (52, 93). Brown algae in the genus Desmarestia concentratesulfuricacid up to 18% of plant dry mass (1). The acid does not appearto be released from healthy plants; however, dislodged plants washed onto rocky shores dissolve barnacles from the rocks (M. Hay, personal observation)and will sterilize rocks covered by blue-green algae, leaving a whitened imprintof the plant on the otherwise darkenedsurface (1). In Chilean kelp beds heavily grazed by sea urchins, the palatablekelp Macrocystis cannot successfully colonize unless it invades an area encircled by Desmarestia plants which appearto act as "acid brooms"that prohibiturchinsfrom enteringthe area (18). Although we know of no controlled experiments clearly demonstratingthat this acid content deters herbivores, the calcified teeth and tests of sea urchinswould probably suffer significantly from consuming this alga.
Blue-Green Algae (Cyanophyta)

These organisms are now consideredcyanobacteriainstead of seaweeds. We include them here because they are ecologically similar to many seaweeds. Although several blue-green algae are known to produce toxic secondary metabolitesthat often containhalogen substituents,this tendencyis especially noticeable in the family Oscillatoriaceae (88, 89). Unlike other seaweeds, cyanobacteria produce compounds containing nitrogen in amide or indole constellations. These nitrogen-containingcompounds are often inhibitory towardfungi, bacteria,and cancercells (92). Theireffects on herbivoreshave not been evaluated. Examples of the compounds produced by blue-greens include aplysiatoxin and the majusculamidesfrom Lyngbya majuscula (12, 64) and lyngbyatoxinA (Figure 1), an indole-basedamide found to produce potent inflammatoryand carcinogenic effects (8). LyngbyatoxinA was sug-
SEAWEED CHEMICAL DEFENSES
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gested as a major cause of "swimmer'sitch," a contact dermatitiscontracted by swimmers in Hawaii who apparentlyencounteredblooms of a unique strain of Lyngbya majuscula.
Chemical and Ecological Methodology

The general methods for extraction,purification,bioassay, and identification of secondary metabolites have been reviewed for small organic molecules and (94) and for phlorotannins (116). With the exception of the phlorotannins coumarins, almost all of the secondary compoundsknown for marine algae are lipid soluble (23, 24). This is also true for the majority of terrestrially derived compounds, and this characteristicyields significant experimental advantages. Known quantities of lipid metabolites can be dissolved in a volatile organic solvent like diethyl ether and coated at desiredconcentrations onto the exteriorof palatableseaweeds that have been blotted dry. After the solvent evaporates,these hydrophobiccompoundsadhereto the surfaceof the seaweed and remain there when it is placed back into seawater (52, 53, 83, versus controlplants 100, 107). Comparisonsof grazingon compound-treated (coated only with the solvent) allow a determinationof the effects of the compound alone. When nonpolar, lipid-soluble compounds or extracts from the green alga Caulerpaor the red alga Gracilaria were coated onto seaweeds that were then placed in seawater, 100%of the Gracilaria extractsand 88% of the Caulerpa extractsremainedon the coated plants 2-3 hr later (83). Similarexperiments with the diterpenealcohol pachydictyol-Ashowed that 93% of the compound remainedon the coated plants after24 hr in seawater(M. E. Hay, W. Fenical, unpublisheddata). Plants coated with compoundsand placed onto coral reefs for several hours retain the compounds, but the total amountremaininghas not been assessed (52, 53, 100, 107). Given the excellent retentionof the few of compoundsor extractsevaluated, and the similar solubility characteristics most of the known seaweed secondarymetabolites, this method can probably be used successfully with most of the small organic compounds. One of the most significantecological problemsinvolved in these assays is of the compound.The actualconcentradeterminingthe naturalconcentration tion of secondarymetaboliteshas not been well documentedsince most of the literaturehas been generatedby chemists interestedprimarilyin describing new compounds, rather than in carefully documenting their natural concentrations. These chemists rarely list the yield of the compound. When yields are given, they are conservative since (a) extractionis rarely, if ever, complete, (b) most isolation and purification techniques entail the loss of significantquantitiesof the metabolites, and (c) handlingof plantsbefore and duringextractionmay result in compounddegradationif the compounds are relatively unstable (104). Maximum yield of single terpenoid metabolites
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from seaweeds usually rangesfrom 0.5% to 1.5%of plantdry mass (52, 103), with rare reportsof metaboliteyield in the 2-5% range (28, 93, 101). Given the problems of extraction and purificationlisted above, it is possible that many of the listed yields are only half or less of the true concentrations.This is trueespecially for compoundsgiving low yields since a largerproportion of the compound is lost in the purificationprocess. are large molecules that occur in complex mixtures Because phlorotannins and are water-soluble, they are relatively difficult to work with from both a chemical and an ecological perspective. The most common method of estimating phlorotanninconcentrationis the Folin-Denis procedurewhich has been discussed by numerous authors (116, 140). This method does not directly measurephlorotanninsbut rathermeasuresreactive phenol residues. determinations Thus, phlorotannin may be confoundedby ascorbicacid, urea, polypeptides, diethyl ether, detergents, and nontannic phenols. When not subject to significant interference,this methodprovides a general measureof total phenolics but does not differentiatebetween the many different types. Given the uncertaintiesof the Folin-Denis procedure,most authorsalso use the Bate-Smith hemanalysis method (116) to estimate the protein binding ability (relative as-tringency) of the phenolics in their samples. In this assay, the extractedphlorotannins are reactedwith the proteinof freshly hemolyzed blood, and the hemoglobin remainingin solution is determinedspectrophotometrically(116). In general, there is good agreementbetween the results of the astringencyand total phenolics assays when these are run on a numberof different algal species (1, 132). However, some problematicspecies are clear exceptions to the general trend. Examples of these include: (a) Analipus japonicus which appearsto be high in phenolics but low in tanning ability (132); (b) Ecklonia maxima which has a tanning ability that would imply a phenolic content some seven times that measured by the Folin-Denis procedure (1); and (c) Sargassumpolycystum,S. cristaefolium,Turbinariaornawhich give Folin-Denis reactions indicating0.8 to ta, and Alaria margintata 1.6% phenols by dry mass but which show no phloroglucinol derivatives when subjected to more specific chemical assays (143). These commonly used assays thus give a reasonably good general devalue must terminationof phenolic contentand astringency,but any particular be viewed as uncertain. These chemical difficulties have hindered rapid advances in research on the ecological roles of phlorotanninseven though phlorotanninswere used in some of the first experimentsdemonstratingthe deterrenteffects of seaweed secondary metabolites (35). Since these compounds are water-soluble, tests of their effects against herbivores usually involve mixing phlorotanninsin an agar matrix which contains an alga that stimulatesfeeding. Grazingon phlorotannin-containing agaris comparedwith grazing on similar agar preparationsthat lack the phlorotannins.Agar pre-
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vents excessive loss of many but not all phlorotannins (35, 134). Additionally, if phlorotanninsact against herbivoresby complexing proteins and thus reducing digestibility (116, 132, 142), then mixing phlorotanninsinto agar may result in prebindingof proteins. This could produce a bias in favor of detecting an effect of phlorotanninssince many herbivoresappearto use gut pH, surfactants,or other means to prevent tannins from binding proteins in their guts (4, 81, 82).
SECONDARY METABOLITESAS HERBIVORE DETERRENTS

As chemical informationon seaweed secondary metabolites became available, ecologists began correlatinglow susceptibility to herbivores with the presence of biologically active secondarycompoundsin many species (1, 44, 45, 49, 63, 70, 71, 75, 78, 93, 95, 96, 105, 131, 132, 142). These correlations suggested that (a) many chemically rich seaweeds or seaweed partswere relatively resistant to herbivory, (b) a few chemically rich species were surprisinglysusceptible to herbivores, and (c) most heavily calcified species (an obvious morphological defense) also contained biologically active secondary metabolites. The first direct tests of algal chemical defenses were conducted against single species of herbivores. Such assays provide ecologically and evolutionarily interesting informationon the herbivore-specificeffects of compounds but do not assess the overall effectiveness of compounds against the diverse types of herbivores that consume plants in the field (52). Field assays determine the ability of compounds to provide a selective advantage under naturalconditions, but with rareexceptions (53), they provideno information on species-specific effects. These distinctions are obvious but often go unmentioned in studies of both types.
Phlorotannins
The snail Littorina littorea decreased its feeding by 50% or more when phlorotanninsfrom the temperateseaweeds Fucus vesiculosus and Ascophyllum nodosum were incorporatedat natural concentrations (about 1% dry mass) into the agar discs upon which it fed (35). The terrestrialtannins gallotannin and phloroglucinol dihydratealso decreased grazing during this same study; gallotannin was more effective than phloroglucinol dihydrate. This study was poorly replicated and not statistically analyzed, but the repeatabledecreases in feeding and the patternsof decreased consumption with increasing phenolic concentrationwere convincing. Laterstudies showed that feeding by a differentgastropod,Tegulafunebralis, was also deterredwhen the palatableseaweed Macrocystis was "tanned"
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by soaking it in a solution of tannic acid (a tannin that does not occur in plants) until it acquireda phenolic contentsimilarto several phenolic-richand more herbivoreresistant seaweeds with which it co-occurred(132). A more recent study (134) has tested specific types of phlorotanninsagainst two herbivoroussnails and a sea urchin. The phlorotannins assayed included:the monomer phloroglucinol (of which brown algal phenolics are composed); a mixture of high molecular weight (hundredsof phloroglucinolunits) phlorotannins from Fucus vesiculosus, low molecularweight (six or fewer phloroglucinol units) phlorotanninsfrom Eisenia arborea, and phlorotanninsfrom Halidrys siliquosa composed of a mixtureof high and low molecularweight molecules. These compounds were all tested against the gastropod Tegula funebralis. A few were also tested against the gastropodT. brunnea and the sea urchin Strongylocentrotus purpuratus. Test concentrationswere 0.0%, 0.2%, 0.5%, or 2.2% of the wet mass of the agarand food used in the grazing would be on a dry mass basis; assays. It is not clear what these concentrations however, given the high wet mass to dry mass ratio of most agar mixes, concentrationscould be high relative to those found in most seaweeds. The monomer phloroglucinol at 2.2% of wet mass had no effect on grazing by Tegulafunebralis but inhibitedgrazingby the sea urchin. Otherphlorotannins were generally significant deterrentsto T. funebralis feeding. In six cases a phlorotanninwas tested against more than one herbivore. In two of these cases a compound that deterred feeding by one species had no effect on another.This supportsthe contentionthattanninsmay have specific activities and be less generalized than is often assumed (146). Early investigationssuggested thatplantphenolics acted againstherbivores by complexing proteins and decreasing digestive efficiency; this effect was originally assumedto be broad, generalized,and difficult if not impossible for herbivoresto avoid (26, 119). The variance in response of different marine herbivoresto the same polyphenolic compoundsand the differences in effect of different polyphenolics on the same herbivore suggest that herbivores and that similarpolyphenolics possess differentialtolerancesto phlorotannins can differ markedlyin theirdeterrent effect. This is in generalagreementwith recent terrestrialstudies suggesting that (a) tannins may have more specific activities than is generally assumed (146), (b) they are not impervious to counteradaptation by herbivoressince many insects are not affected by high tannin content in their foods (4, 30, 81, 82), and (c) tannins may not act as digestibility reducers but, like some terpenes, appear to act by inhibiting feeding or causing cell damage (4, 81, 82). interactions Despite the uncertaintiessurroundingpolyphenolic-herbivore in both terrestrialand marine communities, the above experiments demonstrate that feeding by sea urchins and gastropods can be significantly suppressed by phlorotannins.Additionally, there are negative correlationsbe-
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tween phenolic content or relative astringencyand (a) the partsof kelps eaten by snails (63, 131), (b) the species of seaweeds preferredby the sea urchin Parechinus (1), (c) the marshplants eaten by herbivorousgeese (5), and (d) the general feeding preferences reported for 17 species of herbivorous invertebratesin the temperateNorth Pacific (132). A recentexperimentdemonstratinginduction of increased phlorotanninsynthesis after simulatedherbivore attack also corroboratesthe effectiveness of some phlorotanninsas feeding deterrents(142).
Small Organic Molecules

The greaterease with which terpenes and other small organic molecules can be purified, identified, and tested against various herbivores has allowed ecologists to investigate more thoroughlythe chemical ecology of seaweeds with these types of defenses. As one example, calcified seaweeds in the tropical genus Halimeda are among the best studied of the chemically defended algae (45, 53, 99, 100, 102-105, 107, 139). These seaweeds produce several relatedbioactive terpenoids;halimedatrial(a diterpenoidtrialdehyde) and halimedatetraacetate (a diterpenoid tetraacetate)are usually the major metabolites (53, 102-104, 107). Palatable seaweeds treated with natural and placed on herbivore-diverse areasof coral concentrationsof halimedatrial reefs in both the Pacific and Caribbeanexperience significantly less loss to grazing fishes than do adjacent control plants (53, 107). Assays with halimedatetraacetate give similar although more variable results (100) and is significantlymore deterrentthan halimedatetraaceshow that halimedatrial tate (107). In additionto these tests against coral-reeffishes in general, field tests show that halimedatrialdeters feeding by both Caribbeanparrotfishes and surgeonfishes (53); laboratory assays show that halimedatetraacetate deters feeding by the tropicalgrassbedparrotfish Sparisomaradians (139) but does not affect feeding by the Pacific rabbitfishSiganus spinus (104). In addition to their chemical defenses, Halimeda spp. reduce losses to coral-reef herbivores by capitalizing on diel patterns of herbivore activity (53). These seaweeds produce new growth almost exclusively at night when herbivorousreef fishes are inactive. These youngest plant portions represent 3-4.5 times the food value (nitrogenor organic content)of older portionsbut in field assays are only moderatelymore susceptible(53) or no more susceptiof chemical defenses. ble (107) to herbivores,due to theirhigh concentrations In the 48 hours aftertheirinitial production,structural defenses (calcification) increase, the tissues become less valuable as a food for herbivores, and chemical defenses decrease. Levels of chemical defenses in mature plant portions are less than 10% of those in the youngest portions (53, 107). Additionally, new growthof Halimeda remainsunpigmenteduntiljust before sunrise. Thus, the valuable, nitrogen-containingmolecules associated with
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photosynthesis are not placed in the new and more herbivore susceptible growth until light is available and they can start producing income for the plant (53). In addition, crude extractsof these young white tips deter grazing by coral-reef fishes significantly more than do crude extracts from more maturegreen tips (107). Extractsfrom some populationsof Halimeda in areas of high herbivoreactivity also deter herbivorousfishes more than do extracts from populations of the same species in habitats subject to lower rates of herbivory (107). Seaweeds in the tropical genera Udotea, Cymopolia, Tydemania, Chlorodesmis, and Pseudochlorodesmisalso producecompoundsthat reduce feeding by coral-reefherbivores.The diterpenoidschlorodesminand an epoxylactone, from Chlorodesmisfastigiata and Pseudochlorodesmisfurcellata respectively, deterredfeeding by reef fishes in field assays and by the rabbitfish Siganus spinus in laboratory tests (100, 101, 104). A diterpenoid from Tydemania expeditionis also reduced feeding by the rabbitfish S. spinus (104). However, the effectiveness of chemical defenses may vary among locations or times; the diterpenoiddialdehyde acetate, udoteal, from several Udotea species significantly reduced losses to reef fishes in only one of the three field assays in which it was used (100). The chemistry and ecology of Caulerpa species have recently been reviewed (104). Although a large numberof unusualterpenoidcompounds are producedby the genus, some of the early reportsregardingthe chemistry of Caulerpa appearto have been in error. The pigment caulerpinwas initially reported to be biologically active, but recent studies indicate that it lacks substantive effects (104). Additionally, the toxin caulerpicin, reportedas a minor metaboliteof several species, is not a purecompoundbut representsan undefined mixture of metabolites. Caulerpenyne, a unique acetylenic sesdescribedin the quiterpenoidsynthesizedby several species, is appropriately literature.It deters feeding in laboratoryassays with the Caribbeanparrotfish Sparisomaradians (139), decreases survivorshipwhen fed to juvenile gastropods (103), and appearsto deter feeding in the tropicalsea urchinLytechinus variegatus (83). It does not affect feeding by the Pacific rabbitfishSiganus spinus (104). Few studies have assessed the herbivore-deterrent propertiesof different secondary metabolites under field conditions (52, 100, 107). In one such study (52), five compounds from different tropical marine algae and one related compound from an herbivoroussea hare (Aplysidae) were coated at approximatelynaturalconcentrationsonto the palatable seagrass Thalassia testudinumand placed on Caribbeancoral reefs where they could be eaten by the diverse group of herbivorousfishes that occur there. Laboratoryassays with the sea urchin Diadema antillarum were also conducted. When comparedto appropriate controls, the following terpenoidcompoundssignificant-
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ly reducedThalassia consumptionby both fishes and urchins:stypotriolfrom the brown seaweed Stypopodium zonale; pachydictyol-A, which is produced by several genera of tropical (Dictyota and Dilophus) and warm-temperate (Pachydictyon and GlQssophora)brown seaweeds; elatol, from the red alga Laurencia obtusa; and isolaurinterol,which is producedby several tropical and warm-temperate species of Laurencia. Under very mild acid cQnditions, isolaurinterolis convertedto a structurally similar compound, aplysin, found in high concentrations in sea hares that feed on isolaurinterol-containing Laurencia species. Aplysin did not deter feeding by either type of herbivore. Cymopol (Figure 1), a terpenoid bromohydroquinone from the green alga Cymopolia barbata, significantly reduced feeding by reef fishes but significantly stimulatedfeeding by Diadema. In contrast,cymopol appearsto deter feeding by the tropical sea urchin Lytechinus variegatus (83). Pharmacologicaland crude bioactivity assays suggest that several of the above compoundsshould function as generalizedtoxins (52). However, these laboratory assays are not necessarily good predictors of how compounds affect feeding by herbivores. As one example, pachydictyol-Aand stypotriol are equally effective at deterringfishes and Diadema even though pachydictyol-A shows almost no bioactivity in laboratoryassays while stypotrioland its oxidation product, stypoldione, are broadly bioactive cytotoxins (52). Other algal compounds have also been shown to deter herbivoresin controlled and ecologically realisticexperiments.However, because these studies focus primarilyon the effectiveness of chemical defenses againstlarge mobile versus small sedentaryherbivores, they are discussed in a later section. For completeness, the compounds, seaweeds producing them, and herbivores they deter are listed below: ochtodene from the red alga Ochtodes secundiramea deters feeding by Caribbeanand Pacific reef fishes, and an unidentified from this same alga deters feeding by a mixed mixtureof halo-monoterpenes species group of Caribbeanamphipods(106); dictyopterenesA & B from the reef fishes (50); pachydicbrown alga Dictyopterisdelicatula deterCaribbean tyol-A from the brown alga Dictyota dichotomadetersfeeding by the temperate herbivorous fishes Lagodon rhomboides and Diplodus holbrooki; and dictyol-E from Dictyota dichotoma deters the temperatesea urchinArbacia punctulata as well as the two temperatefishes listed above (51, 54).
Physiological Effects on Herbivores

Although many seaweed metaboliteshave been investigatedin pharmacology assays (23), their physiological effects on herbivores are largely unknown. When the omnivoroustemperatefish Diplodus holbrookiwas fed for approximately three weeks on a diet with pachydictyol-A as 1% of food dry mass, treatmentfish grew only half as rapidly as control fish even though both groups consumed the same quantity of food (51). In a similar although
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pseudoreplicatedexperiment,juvenile gastropods(Strombuscostatus) fed on control, halimedatrial, udoteal, or caulerpenyne laced diets showed the following survivorshipover a two week period: control diet 100%, udoteal diet laced diet 55%, caulerpenyne-laceddiet 33%, and halimedatrial-laced 0% (103).
Relationships Structure-Function
Structurallysimilar compounds can differ dramaticallyin their effects on herbivorefood choice, and compoundsthatdeterone herbivorecan have very different effects on another (50-52, 54, 104, 106, 134). As examples, isolaurinterol and aplysin (52), pachydictyol-A and dictyol-E (51), and similar terpenes ochtodene and chondrocole-C(106) are pairs of structurally in which one compoundsignificantlyaffects feeding while the otherdoes not. Ecologists often classify the activities of secondary metabolites in very general ways, such as, "terpenes are toxins" or "terpenes are qualitative given that comdefenses." These generalizations are clearly inappropriate pounds differing by only one hydroxyl substitution(51) or only stereochemically (104) can show great variancein their activities. If furtherprogressis to of chemical defenses, ecologists will have to be made in our understanding increase their appreciationof the chemical complexities involved and refrain from lumpingcompoundsand their activities into convenientbut ecologically unsubstantiated groups.
Spatial and TemporalDistribution of Compounds

Although rarely studied in an ecologically context, many seaweed secondarymetabolitesappearto be potent appropriate toxins whose effects are not specific to certainorganisms(23, 52, 93, 104). If that is true, then these compounds may be as toxic to the seaweeds that contain them as they are to the herbivores. Little is known about the sites of synthesis and storage of secondary metaboliteswithin algal cells. However, several studies suggest that the sites are partitioned from other cellular vesicles close products and processes and are contained in membrane-bound to the plant surface. For example, the halogenatedsesquiterpenesin Laurencia snyderae are concentrated in cytoplasmic vesicles, labeled "corps en cerise," which lie within cells of the outer cortex (145); these would be the first cells brokenopen by herbivores.These vesicles are presentin the cortical cells of all Laurencia species that produce haloterpenoidcompounds. They are absent in Laurencia species that do not produce these compounds, and also from the inner cortical cells of all Laurencia species. The halogenated terpenes appear not to be released to the environment (58); they are held vesicles. within the membrane-bound In brown algae, most if not all of the phlorotanninsare contained in
LOCATION WITHIN THE CELL
DEFENSES SEAWEED CHEMICAL
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vesicles, vacuoles, and similar structurescalled physodes (116). Unlike the Laurencia metabolites, phlorotanninsdo tend to be released into the environmentbut the rate undernaturalconditions may be much lower than some older estimates indicated (10). In addition to their role as antifeedants, many secondary metabolites may function as antifouling agents (57, 85, 128). This is possible for the phlorotanninsand some other algal products, such as stypotriol and stypoldione from Stypopodiumzonale (37) and lanosol from Neorhodomela (Rhodomela) larix (114), which appear to be released from the alga, perhaps under stress. This could not be the function of metabolites such as those of Laurencia, which are not released at the alga's surface.
WITHIN-PLANT VARIATION Numerous studies suggest that herbivore defenses are costly to the plants that deploy them and must therefore be differentially allocated to plant portions depending on the value of each portion and that portion's relative risk of herbivoreattack (26, 45, 80, 118, variation 119). If this is the case, then we might expect considerableintraplant in the concentrationor type of defensive compounds. Few rigorousstudies of within-plant variation have been conducted; however, compounds clearly tend to be most abundantin young, actively growing, and thus most productive seaweed portions. Species with apical growth tend to have highest concentrationsin the upper portions of their branches (53, 107, 113); those with intercalarymeristems have the highest concentrationof compounds in the meristematicregion (63). The sulfuricacid producingalga Desmarestia is at variance with this trend since the acid appearsto be equally distributedin the different plant portions (1). Reproductive tissues may also be differentially defended. In the kelp Alaria, phlorotannincontent of the sporophyllsis 5-6-fold greaterthan that of the vegetative portions, and sporophyllsare significantly less palatableto grazing snails (131). However, in most brown seaweeds, receptacles are not enriched in phlorotannins(116). The tropical green seaweed Halimeda has relative to gametangiathat are considerablyenriched in halimedatetraacetate mature vegetative portions (103). The red alga Neorhodomelalarix producesthe bromophenollanosol, which varies seasonally between 1.2% and 3% of plant dry mass; winter concentrationsare about three times those of summer (113). A similar pattern occurs in the brown algae Ascophyllum and Fucus with winter maxima in phlorotannincontent that are 40-100% higher than summer minima (117). For both of these temperatespecies, herbivoryshouldbe higherin the warmer summermonths;therefore,the temporalpatternin compoundproductiondoes not appear to correlate with increased herbivore activity. Additionally, for Fucus and Ascophyllumthe seasonal minima in phlorotanninconcentrations
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are at or near the time of maximal fruit body shedding (117). The seasonal highs are, thus, not being used to defend reproductivetissues. Within-plant patterns in allocation of defensive metabolites are best documented for calcifying seaweeds in the genus Halimeda. Since these seaweeds are siphonous, they probably have translocationmechanisms that are unavailableto seaweeds outside the order Caulerpales.Newly produced portions of Halimeda are initially defended by very high concentrationsof (53), the more deterrentof the two majorHalimeda metabolites halimedatrial (107). As new sections become less valuable foods due to increasing calcification and decreasing nitrogen and metabolizable organic content, (53). The chemical defense shifts to the less potent halimedatetraacetate of even this compounddecreasein more mature,less valuable, concentrations and less vulnerableportionsof the plant. Newest plant portionsare thus both qualitatively and quantitativelybetter defended than older portions. As an indication of this, the crude lipid-soluble extractsof very young plants or of 30%of the newest, unpigmentedsegmentsof matureplantsare approximately plant dry mass; the crude extract of matureplant portions is only 5-6% dry mass (107). When each of these crude extracts was applied to palatable seaweeds at a concentrationof 5-6% dry mass and these were transplanted onto tropical reefs, the extracts from the younger plants or portions were to naturalpopulationsof grazingfishes thanwere significantlymore deterrent those from the older portions. Mature portions of Halimeda plants (tops, stipe, and holdfast) do not differ in metabolite concentration(103).
BETWEEN-PLANT VARIATION Chemical variation between individual plants has been reportedfor the red alga Plocamium cartilagineum(91) and zonale (38). Tropicalgreen seaweeds in the for the brown algae Stypopodium family Udoteaceae can show considerablebetween-plantvariationin both the of those metabospecific metabolitesbeing producedand in the concentration lites. These differences occur among individualsgrowing only a few meters apart(104, 107) or between populationsgrowing in differenttypes of habitats (103, 104, 107). In some cases, the differences in concentrationsand compound types appear to be adaptive; populations from reef-slope habitats, where herbivory is intense (45-47), often produce higher concentrationsof deterrents,more potent and more diverse deterrentsthando populationsfrom habitats where herbivory is often much lower (103, 104, 107). concentrationin brown seaweeds can be alteredby salinity or Phlorotannin tidal exposure (116), thus creating among-plantdifferences along salinity or exposuregradients.Lanosol levels in populationsof Neorhodomelalarix have also been reported to be twice as high in tide-pool plants as they are in intertidal plants (113). The ecological consequences of these patterns are unexplored.
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Ecologically relevant experiments have been conducted on changes in phlorotannin levels in the brown seaweed Fucus distichus(142). These plants elevated phlorotannin levels by 20% within two weeks of simulatedherbivore attack and decreasedtheir losses to herbivoroussnails by about 50% relative to control plants that had not been induced. The between-plantdifferences in phlorotannin levels detectedin the field (about20%) were similarto the levels caused by induction. The majorityof seaweed secondary metabolites appearto be producedby generathatarepredominately tropicalor subtropical in distribution(Table 1; also see 23, 93). In the few cases in which species from these genera also occur in temperateseas, the temperaterepresentatives appearto contain less defensive compoundthan do theirtropicalcounterparts (98). Brown seaweeds that producephlorotanninsare a strikingexception to this general trend. In temperate seas, brown algae in the family Fucales in high concentrations (rockweeds)tend to producephlorotannins while those in the family Laminariales (kelps) usually have low concentrations (132, 143). Fucales and other brown seaweeds in tropicalhabitatsall appearto be low in phlorotannins(133, 143). This lack of phlorotanninproductionby tropical seaweeds does not appear to occur because phlorotanninsare ineffective against tropicalherbivores.When tested on naturalcommunitiesof reef fishes in Guam, extracts from phlorotannin-rich temperate species all significantly decreased fish grazing, while extracts from phlorotannin-poor temperate species had no deterrenteffects (143).
GEOGRAPHIC VARIATION
The Cost of Chemical Defenses

A growing literatureon herbivory and the evolution of herbivore defenses suggests that decreased susceptibilityto herbivorescan be achieved only by divertingenergy and nutrientsfrom otherplant needs (15, 26, 80, 118, 119). Thus, defenses are hypothesizedto be costly, and in the absence of herbivory, less defended individuals or species will have higher fitness than do more heavily defended individualsor species. Several terrestrialexamples fit this pattern(15, 118). If this reasoningapplies to seaweeds, then habitatsthatserve as predictable escapes from herbivory should be populated primarily by species or individuals that are highly susceptibleto herbivoredamage. Low susceptibility of those species or individualsthat occur to herbivoryshould be characteristic in habitats where herbivory is predictably high. This pattern occurs in a number of marine communities (22, 44, 45, 49, 80, 103, 104, 107), and experimentaldecreases in herbivoryresult in the more herbivore-susceptible forms (71, 80). seaweeds dominatingthe more herbivore-resistant There are no direct experimental assessments of the cost of chemical
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defenses in seaweeds. Additionally, since seaweeds are often nitrogenlimited (19) but seldom carbonlimited (66), it is unclearthatallocationof energy (i.e. carbon bonds) to defenses will entail any direct costs. However, substantial costs could be involved in synthesis, storage, and possibly degradationof these often toxic compounds. Producing and maintaining the unusual enzymes requiredfor the synthesis and safe managementof these compounds could be much more costly than the energy invested in the compounds themselves. It is interestingto note thatseaweeds do not producethe nitrogenplants. With containingalkaloidsthatare commondefenses in some terrestrial metabolites that contain seaweed secondary a few rare exceptions, the only which are 88, 89), (23, the algae blue-green by nitrogen are produced fixers. nitrogen The differentialallocationof chemical defenses to differentplants andplant parts (53, 103, 107), the induction of chemical defense following attack (142), the concentrationof chemically defended seaweeds in habitats most affected by herbivores and their relative scarcity in habitats with minimal between chemically defended herbivory(45), and the competitiveinteractions of herbivores in the absence (22, 47, 71) all suggest undefended and plants assessment of cost are defenses any rigorous However, chemical costly. that would have to include the cost of synthesis, storage, translocation, breakdown, and turnover as well as alternative or additional functions of the compounds, and the way all of these interactwith the various environmental stresses the plant experiences.
Herbivore Diversity and Chemical Defenses

The probabilityof any single plant defense being ineffective against some herbivoreshould increase with increasingdiversity of herbivoretypes in the coral reefs so community(80). This may be why seaweeds on herbivore-rich commonly employ combinationsof structural,morphological, and chemical defenses and, in some cases, coordinatethese with patternsof temporaland microhabitatescapes (45, 53, 73, 105, 107). Most terrestrial studies of chemical defenses have tested compoundsagainstone or a very few herbivore in different species. However, correlativestudies of compoundconcentrations individualsor species vs naturalratesof herbivoryhave been conductedin the field; in general, compoundconcentrationhas explained surprisinglylittle of the variationin herbivory(14, 31, 79, 90). More of the variationis usually explained by nitrogenor water content of the foliage. Few, if any, terrestrial chemical defenses alone and assayed studies have experimentallymanipulated them againstnaturalcommunitiesof herbivoresin the field. The high rates of herbivoryon tropicalreefs have facilitatedsuch studies in marinehabitats(50, 52, 53, 100, 101, 104, 106-108), and these clearly show that some algal metabolites confer significant resistance even against the diverse array of herbivores that occur on coral reefs.

EFFECTS OF HERBIVORE SIZE AND MOBILITY
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Despite the proven general effectiveness of some compounds, severalrecent studies show that feeding by small, relatively sedentary, and commonly overlooked marine herbivores (mesograzers) like amphipods, polychaetes, and ascoglossans is often unaffected, or occasionally stimulated, by compoundsthat deter larger, highly mobile, and more commonly studiedherbivoressuch as fishes and sea urchins (50, 51, 54, 106, 108). In several respects, marine mesograzers may be ecological equivalents of terrestrial insects since dispersal to plants that provide adequatefood and protectionfrom predatorsmay be one of the major difficulties these herbivores face (50, 51, 54). Mesograzerscan consume a wide variety of algae, but they appear in many cases to prefer feeding on seaweeds that are chemically deterrentto other herbivores, especially fishes (50, 51, 54, 106, 108). They commonly live on the seaweeds they consume and thus may often be incapable of separating food choice from habitat choice. Since they are subject to intense predation from predatory, omnivorous, and herbivorousfishes, mesograzersthat live on and eat seaweeds that are rarelyvisited by fishes should have a higher fitness than those living on seaweeds commonly eaten by fishes. To accomplishthis they would need to be resistant to seaweed chemical defenses. Similar argumentshave been advancedconcerningthe evolution of insect feeding patternsand the need for "enemy-free-space"(59, 115). Although only five studies have investigated how seaweed secondary metabolites affect feeding by mesograzers as opposed to larger herbivores (50, 51, 54, 106, 108), all show that compounds significantly deterring herbivorous fishes either stimulate or do not affect feeding by common mesograzers. Since these studies were conducted in both temperate and tropical habitats and involved different fishes, mesograzers, seaweeds, and defensive chemicals, this pattern may prove to be general. Additionally, several naturalhistory observationssupportthis hypothesis. The sulfuricacid containing kelp Desmarestia is avoided by sea urchins in both South Africa and Chile (1, 18), but the amphipod Amphithoehumeralisforms nesting tubes in the kelp and grazes its surface (1). On Caribbeanreefs, the amphipod Pseudamphithoidesincurvariaeats, lives in, and makes an unusualbivalved domicile from the brown seaweed Dictyota bartayresii;the amphipodwill not eat or make domiciles from several other seaweeds common in its habitat (72). D. bartayresii produces pachydictyol-A (93), which has been demonstratedto deter feeding by Caribbeanreef fishes (52). In the eastern North Pacific, the amphipodAmpithoe tea excavates chambers in the brown alga Pelvetia (41) which produces high concentrationsof phlorotannins(132).
HERBIVORES Adequately documentingand comparingfeeding specialization among herbivores is difficult (32), especially for marine mesograzersthat have rarely been carefully studied. However, the informaSPECIALIZED
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tion presently available suggests that specialist herbivoresmay be less comcommunities(51, 80, 135). The few specialmon in marinethat in terrestrial ized marine herbivores known tend to be relatively small, to have limited mobility, and to live on and consume plants that provide them with some protectionfrom their predators(51, 54, 108, 135). The best studied of the gastropods. Many lineages specialized marine feeders are the opisthobranch within this subclass have evolved from shelled snails into sea slugs as they developed the ability to feed on defendedprey and to sequestertheir defenses (25). As examples, the eolid nudibranchssequester stinging capsules from sequestertoxins from sponges; their coelenterateprey; the dorid nudibranchs and sea hares (Anaspidea)and ascoglossans (Ascoglossa) sequesterdefensive compounds from seaweeds. Ascoglossans are small (some mm to a few cm long) sea slugs that feed by sucking algal sap (60). They sequester both secondarymetabolites(62, 108) and algal chloroplasts;the undamagedchloroplasts are retained intracellularlyand show sustainedphotosynthesis, with the photosyntheticproductsbecoming availableto the animal(141). Sea hares are largerthan ascoglossans (some reachinga mass of 6800 g); they consume large quantities of seaweeds which they chew instead of suck; and they sequester algal secondary metabolites but not chloroplasts (2, 129). Both ascoglossans and sea hares are usually cryptic when in their naturalhabitat (25, 62). Ascoglossans feed primarilyon Caulerpaspp. and generain the chemically rich families Halimedaceaeand Udoteaceae (Halimeda, Penicillus, Udotea, Cymopolia, Chlorodesmis,Avrainvillea and others);however, some species have radiatedonto otherfoods (60, 61). Few studies have rigorouslyassessed feeding by ascoglossans, but most species are reportedto feed on one or a small numberof relatedspecies (60). Althoughit is widely assumedthat they are defended by sequestered algal metabolites contained in the mucus and autotomized cerata that they release when disturbed, investigations of this phenomenon are rare. Elysia halimedae, on Guam, is reportedto occur exclusively on Halimeda species, with animals grazing most heavily on the gametangia and lightly calcified new segments (108), which are the plant regions with the highest concentrations of chemical defenses (53, 103, 107). They convert the Halimeda compounds to a related diterpene alcohol that they sequester as approximately7% of theirdry mass; the compoundis also sequesteredin their egg masses which they tend to place on Halimedatips (108). In field assays, a concentrationof 3% dry mass of this compoundsignificantlydeterredfeeding by both herbivorousand carnivorousreef fishes (108). Studies of Mourgona germaineae in Florida suggest a similar pattern, although the chemical aspects of the interactionsare less well documented. This ascoglossan feeds exclusively on Cymopolia barbata (62), which pro-
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(56). Comduces a number of bioactive terpenoid-bromohydroquinones pounds appearedto be sequesteredand released in mucus and autotomized cerata. Small invertebratesconfined with these secretions died within a few hours (62). Naturalhistory observationssuggest that other ascoglossans may also sequester chemical defenses from their seaweed diet (13, 69). Since many ascoglossans appearto feed on one or a very few species (60), morphologiesthat have foot widths and radulartooth (the feeding apparatus) are tightly coupled with the structureof their algal hosts (61), and sequester the defensive chemicals produced by their hosts (62, 108), ascoglossans appear to be very specialized feeders relative to most known marine herbivores. In at least one case (16), an ascoglossan, Elysia chlorotica, has been shown to containcompoundsthatcould not be tracedto an algal source. Some ascoglossans may thereforebe capable of synthesizing their own defensive chemicals. Like the ascoglossans, sea hares also sequesterdefenses from the chemically rich seaweeds upon which they preferentiallyfeed. They sequestersecondary metabolites from the brown algae Dictyota, Dictyopteris, and Glossophora (23, 40, 87), the blue-greenalga Lyngbyamajuscula(23, 120), and the red algae Plocamium, Laurencia, and Asparagopsis (23, 40, 110, 111, 125, 126, 129, 130, 144). They prefer the seaweeds above; however, they also consume a wide variety of seaweeds that do not produce secondary metabolites (9, 68). Their large size and rapid growth rate (2) probably preclude restrictive specialization to a single prey species. An adult would consume many plants per day, rapidly exhausting its local food supply and mandatingcontinualmigrationsto otherprey patches. Given the patchinessof many seaweeds and the limited mobility of sea hares, locating other prey patches could be difficult and unpredictable.However, juveniles do show evidence of specialization. Species in the genus Aplysia selectively settle on and consume species of Laurencia and Plocamium, which produce toxic and apparentsecondarymetabolitesthatare sequesteredby the opisthobranch ly used in its own defense (67, 68, 93, 109, 129). Since Aplysia appearto be able to grow and reproduceequally well on eitherPlocamium or Enteromorpha (9) (a genus without chemical defenses), the preferencefor chemically rich seaweeds appearsto reflect the need for predatordefense as opposed to some unique dietaryrequirement.The juveniles are also very cryptic on both Laurencia and Plocamium (2). WhenAplysia consume chemically rich seaweeds, the seaweed compounds are sequesteredin the "digestive gland," which does not digest but stores the compounds(65, 129, 144). In A. californica, the algal-derivedpolyhalogenated terpenes and sesquiterpenesstored in this gland comprise 0.7% of the animal's wet mass and have a turnovertime of less than 3 months (129). Compounds in the digestive gland are slowly moved to the skin (65, 144)
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where they may function as predatordeterrents. When disturbed, Aplysia producea purpleink thatis not toxic but may interferewith the chemosensory apparatusof predators;if the disturbancecontinues, they produce a milky fluid that containstoxic oils reportedto cause muscularparalysisand deathof marine organisms (129). Although the direct role of the algal metabolites in Aplysia's defense againstpredatorsseems obvious, there are no ecologically realistic and rigorouslyconductedtests of this. Severalchemists have reported fragmentarybioassays suggesting that the compounds function as predator deterrents(65, 129, 130). Additionally, a juvenile fish has been suggested to be a Batesian mimic of an Aplysia with which it co-occurs (55). If this interpretation is correct, it argues stronglyfor the predictableeffectiveness of Aplysia defenses. AlthoughAplysia and ascoglossans sequestertoxic metabolites from their algal prey, most of these animals are very cryptic. Few show the warningcolorationsthatcommonly occur in terrestrial insects thatsequester plant toxins or in dorid nudibranchsthat sequester sponge toxins. Given the tremendous effects that herbivorous fishes, sea urchins, and gastropods have on seaweeds (11, 43, 47, 71, 80), most seaweed chemical defenses probably evolved in response to diffuse herbivory (30) from these diverse types of herbivores, and not in response to the few more specialized herbivores discussed above.
EVOLUTIONARYOVERVIEW AND COMPARISON WITH TERRESTRIALCOMMUNITIES

Plant-herbivoreinteractionsin terrestrialcommunities have been studied in greater detail and over a much longer period of time than have seaweedherbivoreinteractions.Much of the terrestrial researchhas focused on insects as the herbivores of primaryimportance(20, 121). The availability of this backgroundinformationallowed ecologists to startconstructinggeneral theories aboutplant defenses in the 1970s (26, 119). These theories were forward looking and made very broad predictionsof generalizablepatternsbased on the limited datathatwere then available. Since the proposedmodels were well argued and reflected the patterns that several authors were beginning to describe, they were quickly accepted, rather than tested, by most ecologists. These theories of plant defense still serve as an influential framework for present day studies (15) even though some of their primaryassumptionsand predictions have been repeatedly questioned or demonstratedto need modification (4, 14, 15, 30, 32, 81, 82, 146). Since an excellent summary of defensive theory is available (30), we discuss it only briefly here and then evaluatethe degree to which the predictionsfrom terrestrial theorycoincide or conflict with patternsin the marine environment.
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The Plant ApparencyModel

One of the most influential models of plant-herbivore interactionshas been the plant apparencymodel (26, 119). This model contrastedtwo very different types of plants and sought to explain apparentdifferences in their defensive strategies. Plants that commonly dominatedclimax communities were termedapparentplants since they were "boundto be found"by herbivores.It was proposed that they would have to invest heavily in defenses that were very generalized and effective against a broad range of herbivores. Tannins were thought to fill this role by acting as digestibility reducersthat allowed on the part of herbivores. little, if any, possibility of counteradaptation Tannins were called quantitative defenses because they were thought to function in a dose-dependentmanner. In contrast, rapidly growing plants that were unpredictablein space and time were termed unapparent plants since many individualswith these characteristicswould escape detectionby herbivores.Because they allocatedmost of their resources to rapid growth, reproduction,and dispersal, unapparent plants were proposed to be defended primarilyby inexpensive toxins that were effective in low concentrationsagainst generalist herbivoresbut were easily circumventedby specialist herbivores that had evolved detoxication mechanisms. Because of their alleged effectiveness at low concentrations, these compoundswere called qualitativedefenses. Thus, apparent plantswere proposedto differ from unapparent plantsin threeimportant ways (30): (a) the amount of resources invested in defense, (b) the types of defenses employed (i.e. toxins vs digestibility reducers), and (c) the potential for co-evolution between plants and their specialized insect herbivores. A more recent model (15) explains most of the above patternsin termsof plantresourceavailability instead of plant apparencybut retains as its foundation many of the same distinctions regarding differences in costs and effects of qualitative versus defenses. Given the ecological and evolutionarygeneralitiesupon quantitative which the above models are based, there is no obvious reason for them to be habitat specific and they might apply equally well to-seaweeds.
COSTS One of the major assumptions in both models is that high con-
centrationsof tannins are more costly than low concentrationsof more toxic compoundssuch as terpenesor alkaloids. While more energy is storedin 20% dry mass of tanninsthan in 1%dry mass of terpenes, it is by no means clear that energy is the currencyin which costs should be measuredor that there is any significant difference in the total resources expended on each type of defense once the costs of synthesis, turnover,storage, and possible functions other than herbivoredeterrenceare considered. Swain (138), Fox (30), and others have pointed out that once tannins are producedthey appearto have minimal maintenancecosts, while many of the more active toxins have high
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turnoverrates and may demandthat large amountsbe synthesized in orderto maintaina 1% concentrationover the lifetime of the leaf. They suggest that toxins could be more expensive than tannins in some cases. In seaweeds, even the difference in turnoverrate is unclear. Some species like Laurencia producevery potent toxins (27, 28, 52) that are sequesteredin never released unless the cell vesicles (145) and apparently membrane-bound is ruptured(58). Other seaweeds like the brown alga Stypopodiumproduce potent toxins that are released into the water (37) and must therefore be (116), so constantlysynthesized. Brown seaweeds also release phlorotannins the cost of turnoverand maintenancemay be no differentfor plantsproducing phlorotanninsthan for those producing terpenes. Thus, species with low concentrationsof qualitativedefenses may incureither high or low costs, and it is not at all apparenthow these costs compare with those of supposedly quantitativedefenses like phlorotannins.The indirectevidence that chemical defenses are somehow costly is persuasive for both terrestrial(15, 30, 118) and marine plants (45, 80, 131, 142). There is, however, no evidence of been termedqualitativeand differentialcosts between what have traditionally quantitativedefenses.
DIFFERENCES BETWEEN QUALITATIVE AND QUANTITATIVE DEFENSES
Reevaluationis needed for the widely held notion that tanninsand phlorotannins are dose-dependentdigestibility reducers(26, 35, 119, 132, 134, 138, by herbivores and 142) that are especially resistant to counteradaptation fundamentallydifferent from other defensive compounds. First, the mode of action of phenolics may be no different from the mode of action of many qualitativedefenses. Althoughtanninshave often been shown to decreasethe growthand survivalof herbivores,recent studies suggest thatthis resultsfrom feeding inhibition and cell damage (as is the case with qualitativedefenses), not from interference with digestion and assimilation (4, 81, 82). Like tannins, phlorotanninsdecrease feeding by marineherbivores(35, 134), but their mode of action or physiologicaleffect on marineherbivoreshas not been determined. Second, there is no evidence of fundamentaldifferences between tannins and qualitative defenses in the probabilityof herbivores evolving counteradaptations. A wide variety of terrestrial herbivores feed primarily on tanniferous plants and are not negatively affected when grown on diets containing tannin (4, 30, 31, 81). For marine herbivores, feeding by some grazers is not deterred by some phlorotannins, and many common herbivores in Australiaand New Zealand appearto be unaffectedby phlorotannin content 2-3 times as high as those that commonly deter feeding by herbivores in coastal North America (22, 134; P. D. Steinberg personal communication).
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Third, the dose-dependentdifferences that define qualitativeversus quantitative defenses may be illusory. In a recent study (81) where adaptedand nonadaptedmoth larvae were fed diets with a wide range of tannin content, the adaptedmoth grew equally well on all diets, while the nonadaptedmoth showed equally decreased growth on all tannin-containingdiets, due to feeding inhibition.Therewere no dose-dependenteffects on eitherherbivore. In seaweeds, phlorotanninsdeter herbivore feeding in a dose-dependent manner(35, 134), but then so do terpenoids(51, 54). Additionally, the effect of phlorotannins on herbivore feeding shows significant variance among different herbivore species and different types of phlorotannins (134), suggesting that phlorotanninsare neither uniform in activity nor as broadly deterrentas has been assumed in most of the terrestrialmodels. Thus, in the respects discussed above, seaweeds and terrestrialplants seem reasonably similar; neither function as predicted by the models. If tannins are predictably found in apparentterrestrialplants, then this environments.In aspect of defense may differ between marineand terrestrial seaweeds, phlorotannin-richspecies are restricted almost exclusively to temperateand cold seas (132, 133, 143). Althoughphlorotannin-rich Fucales can be very abundantat some sites and tidal elevations, the most apparent plantsin cold andtemperateseas arekelps (17, 124), most of which arelow in phlorotannins(132, 143) and very susceptible to herbivoreattack(22, 124). As an explanation for the lack of defenses in temperate kelps, Estes & Steinberg (22) suggest that kelp beds have traditionallyattractedand maintained populationsof sea otters that preyed selectively on some of the major and negatingthe kelp grazers, thus precludingthese from becoming abundant need for chemical defenses. As sea otters were harvestedto near extinction, invertebrateherbivores escaped control and devastated kelp beds. Estes & Steinberg(22) develop a numberof paleontologicalargumentssuggestingthat the absence of sea otters in the southernhemisphereshould have selected for seaweeds with betterdeveloped chemical defenses and herbivoresbetter able to cope with these. On tropicalcoral reefs, where herbivoryis very intense and results from a diverse arrayof herbivores, phlorotanninsare rare or absent even within the Fucales (133, 143). Recent assays of extractsfrom phlorotannin-rich temperate seaweeds and their deterrenteffect on tropical reef fishes indicated that would be effective againstreef herbivores(143), so it is unclear phlorotannins why they do not occur there. Thereare few apparent uprightseaweeds in these communities, but those that are (Halimeda, Chlorodesmis, and sometimes other members of the Caulerpales and Dictyotales) all contain terpenoid compounds (qualitative defenses) instead of phlorotannins(quantitativedefenses). Many of the most common and herbivore-resistant species have both qualitativechemical defenses and calcification (45, 105). Since calcification
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would reduce food quality and potentiallyadd to the processing and handling costs of herbivores, it might be considered to be -a quantitativedefense.
CO-EVOLUTION Two fundamentaldifferences between marine and terrestrial communities may vary the potential for co-evolution between these environments.First, insects arethe herbivoresof primaryimportancein many terrestrial communities, and they have generationtimes that are usually much shorterthan those of the plants on which they feed. This should allow insects to adapt to plant defenses faster than plants can respond to new feeding abilities of insects. In marinecommunitiesthis may not be the case. In coastal seaweed communities, fishes and sea urchinsare the primaryherbivores(1 1, 46, 71, 80), and their generationtimes are similarto or greaterthan many of the seaweeds on which they graze. This similarityin generationtimes might promote co-evolution, but this process is probablyprecludedby the dispersal phenomena discussed below. The second fundamentaldifference between marine and terrestrialherbivore communitiesis the mannerin whichjuveniles locate theirhost plants. In many specialized insects, highly mobile adults, which are often chemically defended and aposematicallycolored, are not tied to the food plant (i.e. flying butterflies,moths, and beetles); they searchlarge areas and carefullyoviposit hosts. The mobility, vision, and chemo-sensory their young on appropriate acuity of the adult allows the species to utilize even unapparentplants successfully (39). In contrastto this, herbivorousfishes and sea urchinshave planktoniclarval stages that are liberatedin coastal habitatsbut spend varying amounts of time developing in the plankton before returningto near-shore communities where they can settle, metamorphoseinto juveniles, and begin feeding on seaweeds. Although larvae have behaviors that promote their return to, or retention in, coastal habitats (127), their swimming ability is slight compared to currents, and they have only limited ability directly to affect their horizontaltransportand thus to choose particularmicrohabitats (7). They are thus taken into a large ocean that is unsuitablefor their adult existence and are faced with finding not only the small rim of the ocean on which they live as adultsbut also an appropriate portionof thatrim (say a reef instead of a grassbed, mud flat, or mangrove lined coast). Although some larvae settle selectively in response to general habitat cues (7), they are host plants since these would rarelybe unlikely to respondonly to unapparent encountered. Additionally, larvae approachingshore are subject to intense predationfrom fishes and benthic filter feeders (34, 96a), and thus they may be constrainedfrom approaching multipletimes in hopes of finding a rarehost plant. These factors should select for generalistfeeders that can use the wide variety of seaweeds they encounteras they entercoastal habitats.This may be why specialists seem and probablyare rare in marine as comparedto terrestrial communities.
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However, some marinemesograzersare partially, or restrictively, specialized to certainhost plants (50, 51, 54, 60, 72, 108); these herbivorestend to be exceptions to the trends in generationtimes and dispersal strategies outlined above. Amphipodsand some ascoglossansbroodtheiryoung or undergo direct development, thus avoiding the planktonicdispersal stage. Many also have generation times similar to, or shorter than, their algal prey. These differencesbetween mesograzersand largermarineherbivorescould facilitate local adaptationto host plants and explain, in part, why several mesograzers have adapted to seaweed chemical defenses that are effective deterrentsof fishes and largerinvertebrates.Since young marineherbivoresare not placed on appropriate host plantsby large, very mobile adults(as occurs in terrestrial habitats),it should be difficult for marineherbivoresto specialize on unapparbias, ent plants. Although data are limited and subject to interpretational marine herbivores appearto have specialized most often on apparentplants like Dictyota (72), tropicalgreen seaweeds in the orderCaulerpales(60, 108), and seagrasses (60). In addition to being apparentwithin a habitat, most of these seaweeds are widely distributed among habitats. Young herbivores should thereforehave a higher probabilityof successfully dispersingto these plants. Since these mesograzersappearto have a plants than to unapparent limited impact on plant fitness relative to the larger effects of fishes and urchins, the potentialfor truecoevolution between mesograzersandtheirprey is probably limited (11, 47, 71).
SUMMARY
Seaweeds producea diverse arrayof secondarymetabolitesthat deter feeding by common marineherbivores.However, the defensive value of a compound is a specific function of compoundstructureand the herbivorespecies attacking the plant. The function of compounds cannot be predictedby structural for example, to lump terpenesas toxins and class alone so it is inappropriate, phlorotanninsas digestibility reducers. The spatial and temporaldistribution of secondarymetaboliteswithin cells, within plants, andbetween plantsoften vary in ways that are adaptive. Individualplants or plant portions that are at greatest risk are often best defended. Herbivoresize, mobility, and life-historycharacteristics appearto be correlated with resistanceto seaweed chemical defenses. Small relativelysedentary herbivoreslike some amphipods, polychaetes, and ascoglossans (mesograzers) often selectively consume seaweeds that are low preference foods for fishes and larger invertebrates.Compoundsfrom these seaweeds deter feeding by larger herbivoresbut stimulate, or do not affect, feeding by several mesograzers.Although a few mesograzerssequesterchemical defenses from their algal hosts, most are not highly specialized and appearto be advantaged
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indirectlyby theirclose associationwith seaweeds that are not visited by their predators. communities A comparisonof chemical defense in marineversus terrestrial suggests that (a) the assumptionof a fundamentaldifference in the cost and function of qualitativevs quantitativedefenses needs to be reevaluated, (b) communitiesmay the degree of feeding specializationin marinevs terrestrial differ due to fundamentallydifferentdispersalmodes of common herbivores, and (c) truecoevolution is unlikely between seaweeds and marineherbivores.
ACKNOWLEDGMENTS
Funding for our work on the chemical ecology of seaweeds has been provided by NSF, California Sea GrantProgram,The National Geographic Society, The Charles A. LindberghFund, The AustralianMuseum, and the North CarolinaBiotechnology Center. T. Brunone, J. E. Duffy, J. Estes, G. Fuller, L. Fox, P. Hay, J. Lin, J. Lubchenco, S. Louda, V. Paul, J. Pawlik, C. Peterson, P. Renaud, A. Shanks, R. Trindell, and F. Wilson commented to our attention,or helped in otherways. on the manuscript,broughtliterature To all we are grateful. Literature Cited
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Marine Plant-Herbivore Interactions: The Ecology of Chemical Defense Author(s): Mark E.

MARINE PLANT-HERBIVORE INTERACTIONS:The Ecology of Chemical Defense

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SECONDARY METABOLITESOF MARINE ALGAE

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Red Algae (Rhodophyta)

Green Algae (Chlorophyta)

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Secondary metabolites from marine algae

Brown Algae (Phaeophyta)

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Blue-Green Algae (Cyanophyta)

SEAWEED CHEMICAL DEFENSES

Chemical and Ecological Methodology

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SEAWEED CHEMICAL DEFENSES

SECONDARY METABOLITESAS HERBIVORE DETERRENTS

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SEAWEED CHEMICAL DEFENSES

Small Organic Molecules

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SEAWEED CHEMICAL DEFENSES

Physiological Effects on Herbivores

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Spatial and TemporalDistribution of Compounds

DEFENSES SEAWEED CHEMICAL

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SEAWEED CHEMICAL DEFENSES

The Cost of Chemical Defenses

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Herbivore Diversity and Chemical Defenses

SEAWEED CHEMICAL DEFENSES

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DEFENSES SEAWEED CHEMICAL

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EVOLUTIONARYOVERVIEW AND COMPARISON WITH TERRESTRIALCOMMUNITIES

SEAWEED CHEMICAL DEFENSES

The Plant ApparencyModel

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SEAWEED CHEMICAL DEFENSES

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DEFENSES SEAWEED CHEMICAL

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