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Marine Plant-Herbivore Interactions: The Ecology of Chemical Defense

Author(s): Mark E. Hay and William FenicalReviewed work(s):Source: Annual Review of Ecology and Systematics, Vol. 19 (1988), pp. 111-145Published by: Annual ReviewsStable URL: http://www.jstor.org/stable/2097150 .

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Ann. Rev. Ecol. Syst. 1988. 19:111-45Copyright? 1988 by Annual Reviews Inc. All rights reserved

MARINE PLANT-HERBIVOREINTERACTIONS:The Ecology ofChemical DefenseMark E. HayUniversityof North Carolinaat Chapel Hill, Instituteof MarineSciences, MoreheadCity, North Carolina28557WilliamFenicalInstitute of Marine Resources, Scripps Institution of Oceanography, University ofCaliforniaat San Diego, La Jolla, California92093-0228

INTRODUCTIONHerbivoryhas a profound effect on seaweeds in both temperateand tropicalcommunities 11, 17, 21, 33, 43, 47, 80, 124). This is especiallytrueon coralreefswhere 60-97% (11, 42) of the total seaweed productionmay be removedby herbivores. To persist in marine communities, seaweeds must escape,deter, or tolerate herbivory. The ecological and evolutionary importanceofspatialand temporal escapes has been extensively studied for seaweeds andadequatelyreviewed in the recent literature(33, 45, 47, 71, 80).The ability of seaweeds to tolerateherbivoryhas receivedlimited attention.On coralreefs, rapidly growing filamentousalgae areheavily grazed,butthealgae quickly replacethese losses andappear o be dependentuponherbivoresto preventtheir habitatfrom being overgrown by largerbut less herbivore-tolerant species (11, 71). Additionally, several seaweeds have spores orvegetative portions that can withstandgut passage;in some cases this signifi-cantly increases the growth ratesof the newly settled spores (6, 122). Thesetypes of seaweeds may be considered herbivoretolerant.

Althoughnumerousseaweed characteristics an deter some herbivores, theeffects of morphologyandchemistryhave been studied mostthoroughly.The1110066-4162/88/1120-011 1$02.00


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112 HAY & FENICALgeneral hypotheses and data supportingthe importanceof morphologicaldeterrentshave been outlined previously (74, 75, 136, 137), as have someexceptions to the predictedpatterns 45, 70, 90). We do not review morpho-logical defenses but do discuss how they interact with chemical defenses.Seaweeds may also deter herbivores by associating with other plants thatinterferewith herbivore oraging or feeding. These associationaldefenses arejust beginning to be investigated in marine systems (18, 47, 48, 76, 112).There is an implied chemical natureto these interactions,but it has not beenrigorously investigated. In this paper we concentrate on the ecology ofseaweed chemical defenses since this is a new and rapidly advancing area inwhich even recent reviews (45, 93) are outdated.

Approximately500-600 secondary compounds have been isolated frommarinealgae (23, 24, 123). Manyof these compoundspossess strongbiologi-cal activities in laboratoryassays (3, 23, 24, 27, 45, 52, 93, 104); however,theirecological functions under naturalconditionshave been addressedonlyrecently. Seaweed secondary metabolites may function as herbivore de-terrents(see below) or as allelopathicand antifouling agents (57, 85, 128).Recent investigations (52, 116) suggest that the primaryfunction of manyof these compoundsis to deter herbivory. However, secondarymetabolitesalso may have multiple or alternatefunctions. Below we review the avail-able informationon chemically mediated seaweed-herbivoreinteractions,compare their effects in marine vs terrestrial ommunities, and interpret herobustnessof present plant-herbivore heory in light of the emerging mar-ine patterns.

SECONDARY METABOLITESOF MARINE ALGAESeaweeds are similarto terrestrialvegetation in that they produce terpenes,aromatic compounds, acetogenins, amino acid-derived substances, andpolyphenolics as secondary metabolites. They differ from terrestrialplantsbecausethey incorporatehalogensintotheirsecondarymetabolitesand do notproducethe nitrogen containingalkaloidscommon in some terrestrialplants(primarily legumes). Selected families and genera of all four divisions ofseaweeds produce secondarymetabolites.Withingeneraand families, somecompounds are products of consistent biosyntheses, i.e. are produced byterpenoidor acetate-derivedbiosyntheses. The compounds areoften species-or genus-specific, and they have been used as taxonomiccriteriato separatemorphologicallysimilar species within a single habitat(29). A summaryofthe generastudiedandthecompoundtypesobservedare listed in Table 1. Theprimary iteratureon this topic consists of 600 to 800 publications;most ofthese are accessible throughrecent reviews (23, 24, 104).


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SEAWEEDCHEMICALDEFENSES 113

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SEAWEEDCHEMICALDEFENSES 1150 >

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116 HAY & FENICALRed Algae (Rhodophyta)The families Bonnemaisoniaceae, Plocamiaceae, Rhizophyllidaceae, andRhodomelaceae end to be particularly ich in biologically active compoundsrangingin structure rom simple aliphatic halo-ketones andbrominatedphe-nols to more complex monoterpenes, sesquiterpenes, and diterpenes(C1O,C15,andC20compounds) (23, 27, 28). Yields of these compounds(mass ofcompoundextractedper mass of plant) rangefromtrace amountsto as muchas 3-5% of the plant's dry mass (27, 28, 52). Genera that have beenextensively studied include Laurencia, Plocamium, Asparagopsis, Bonne-maisonia, Ochtodes, Chondrococcus,and Sphaerococcus. However, manyreportsof secondarycompoundproductionare less well documented 21, 23,27). Most of the well-studied genera produce several related compounds(Table 1) with strong biological activity. The extremeexample is the genusLaurencia, various species of which produce terpenoids and acetogenins ofvery complex types. Within the terpenes, over 400 different compoundsrepresentat least 26 different structural lasses. At least 16 structural roupsare novel and found only in Laurencia species (21, 24). One of the betterknown Laurencia metabolites is elatol (Figure 1), a chamigrene-class ses-quiterpenoid hat is cytotoxic, ichthyotoxic, insecticidal, and deters feedingby reef fishes (52).Green Algae (Chlorophyta)The orderCaulerpaleshas been studiedextensively (53, 99-104, 107, 139).Families in this order are the Caulerpaceae,containing the single genusCaulerpa, and the Udoteaceae and Halimedaceae, containing the generaHalimeda, Tydemania, Penicillus, Udotea, Avrainvillea, Chlorodesmis,Pseudochlorodesmis,and others. Species in these genera producea closelyrelated group of sesquiterpenoidand diterpenoid compounds that exhibitbroadbioactivityin pharmacologicalassays and deterherbivores n bothfieldand laboratoryassays (53, 103, 104). Approximately70 secondarymetabo-lites have been isolated from these seaweeds. Many are relatively unstableonce isolated and purified, making it difficult to quantifytheir naturalcon-centrations.Reportedyields rangefromtrace amountsto 2% of whole plantdry mass, with most determinations alling between 0.2% and 1.5% (101,103). However, the compoundsare not uniformlydistributed hroughout heplant, and concentrationsn some plant portions may be 5%, or greater(53,107). The diterpene trialdehyde, halimedatrial(Figure 1), produced bynumerousspecies of Halimeda, is one of the betterstudiedandmostbioactivecompoundsfrom this group. It is structurally elated to the powerful insectantifeedant,warburganal 102), and inhibitsfeeding by reef fishes (53, 107).Halimedatrialalso shows strong biological activities againstbacteria, fungi,fishes, and the sperm, fertilized eggs, and larvae of sea urchins (103).


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SEAWEED CHEMICALDEFENSES 117

BrV~KA"'i'C CHOCHOr tCJX H OH" /CHO

Elatol Halimedatrial

OHHO OH Br>

OH OH

Phloroglucinol Cymopol

CH3HNJ N OH

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Pachydictyol A LyngbyatoxinFigure I Secondarymetabolitesfrom marine algae

Other families of green seaweeds are less well studied. The green algaCymopoliabarbata (Dasycladaceae)producesa series of terpene-hydroqui-nones (56; see Figure 1 for an example), as well as a water-solublephenoliccompoundof the coumarinclass (86). This lattercompoundwas also isolatedfrom the related alga Dasycladus vermicularus. Cladophorafascicularis(Cladophoraceae)producesa brominateddiphenyl ether of a structureclassnot found in any other algal source (104).Brown Algae (Phaeophyta)Onlybrown seaweeds producepolyphenolics.Althoughthese compoundsarehypothesizedto functionlike tertestrial annins(35, 116, 132, 134, 142), weemphasizethat the polyphenolicsin seaweeds differ chemically from those interrestrialplants. In contrast o the complex biochemicaloriginsof phenolicsin terrestrialplants, algal phenolicsare derived from the simpleC6 precursor,phloroglucinol 1,3,5-trihydroxybenzene) Figure 1). Becauseof these chem-ical differences, some authorshave used the term "phlorotannins"116) toreferto the polyphenolics producedby brown algae. This termis appropriatesince it emphasizes the differences between terrestrial"tannins"and their


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118 HAY& FENICALmarinecounterparts. n laboratoryassays, some phlorotannins how antibiot-ic, antifungal,antialgal, and antilarvalactivities. Some also deter feeding bymarine herbivores (35, 134). Phlorotanninsoccur in high concentrations(commonly 1-15% of dry mass) in many temperatebrown seaweeds (22, 116,132) but appear o be absent, or presentonly in low concentrations less than2% of dry mass), in tropical habitats (133, 143).In tropical andwarm-temperate eas, brown algae in the order Dictyotales(Dictyota, Pachydictyon, Glossophora, Dictyopteris, Zonaria, and others)producecomplex mixturesof terpenoids,acetogenins,and terpenoid-aromatic(mixed biosynthetic origin) compounds (23, 84). The bicyclic diterpenealcohol pachydictyol-A (Figure 1) is a well-studied example of a diterpenoidfrom this group. This simple diterpenoidalcohol shows no inhibitoryeffectsagainst fungi, bacteria, diatoms, or fertilized sea urchin eggs (36), yet iteffectively detersfeeding by tropical(52) andtemperateherbivores(51, 54).Reported yields of the secondary compounds from dictyotacean algae aresimilar to those from red and green algae (52, 93).Brown algae in the genusDesmarestia concentrate ulfuricacid up to 18%of plant dry mass (1). The acid does not appearto be released from healthyplants; however, dislodged plantswashed onto rocky shores dissolve barna-cles from the rocks (M. Hay, personalobservation)and will sterilize rockscovered by blue-green algae, leaving a whitenedimprintof the planton theotherwise darkenedsurface (1). In Chileankelp beds heavily grazedby seaurchins,the palatablekelpMacrocystiscannotsuccessfullycolonize unless itinvades an area encircledby Desmarestiaplantswhich appear o act as "acidbrooms" hatprohibiturchinsfromenteringthe area(18). Althoughwe knowof no controlled experiments clearly demonstrating hat this acid contentdetersherbivores,the calcified teeth and tests of sea urchins would probablysuffer significantlyfrom consumingthis alga.Blue-Green Algae (Cyanophyta)These organismsare now considered cyanobacterianstead of seaweeds. Weinclude them here because they are ecologically similarto many seaweeds.Although several blue-green algae are known to produce toxic secondarymetabolites hat often containhalogen substituents, his tendency s especiallynoticeable in the family Oscillatoriaceae(88, 89). Unlike other seaweeds,cyanobacteriaproduce compounds containing nitrogen in amide or indoleconstellations. These nitrogen-containingcompounds are often inhibitorytowardfungi, bacteria,and cancercells (92). Their effects on herbivoreshavenot been evaluated. Examples of the compounds produced by blue-greensinclude aplysiatoxinand the majusculamides rom Lyngbya majuscula(12,64) and lyngbyatoxinA (Figure 1), an indole-basedamide found to producepotent inflammatoryand carcinogeniceffects (8). LyngbyatoxinA was sug-


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SEAWEEDCHEMICAL EFENSES 119gested as a major cause of "swimmer's tch," a contact dermatitiscontractedby swimmers in Hawaii who apparentlyencountered blooms of a uniquestrain of Lyngbya majuscula.Chemical and Ecological MethodologyThe general methods for extraction, purification,bioassay, and identificationof secondary metabolites have been reviewed for small organic molecules(94) and forphlorotannins 116). With the exceptionof the phlorotannins ndcoumarins, almost all of the secondary compounds known for marine algaeare lipid soluble (23, 24). This is also true for the majority of terrestriallyderived compounds, and this characteristicyields significant experimentaladvantages. Known quantities of lipid metabolites can be dissolved in avolatile organicsolvent like diethylether and coatedatdesired concentrationsonto the exterior of palatableseaweeds that have been blotted dry. After thesolvent evaporates, hese hydrophobic ompoundsadhere o the surfaceof theseaweed and remainthere when it is placed back into seawater(52, 53, 83,100, 107). Comparisonsof grazingon compound-treatedersus controlplants(coated only with the solvent) allow a determinationof the effects of thecompoundalone.When nonpolar, lipid-soluble compoundsor extracts from the green algaCaulerpaor the redalgaGracilaria were coated onto seaweedsthatwere thenplaced in seawater, 100%of the Gracilariaextractsand 88%of the Caulerpaextractsremainedon the coatedplants2-3 hrlater(83). Similarexperimentswith the diterpenealcoholpachydictyol-Ashowed that93%of the compoundremainedon the coated plantsafter24 hr in seawater M. E. Hay, W. Fenical,unpublisheddata). Plantscoated with compoundsandplacedonto coral reefsfor several hours retain the compounds,but the total amountremaininghasnot been assessed (52, 53, 100, 107). Given the excellent retentionof the fewcompoundsor extractsevaluated,and the similarsolubilitycharacteristics fmost of the known seaweed secondarymetabolites,this method can probablybe used successfully with most of the small organic compounds.One of the most significant ecological problems nvolved in these assays isdetermining he natural oncentration f thecompound.The actualconcentra-tion of secondarymetaboliteshas not been well documented ince most of theliteraturehas been generated by chemists interestedprimarily n describingnew compounds, rather than in carefully documenting their naturalcon-centrations. These chemists rarely list the yield of the compound. Whenyields are given, they are conservativesince (a) extraction s rarely, if ever,complete, (b) most isolation and purification techniques entail the loss ofsignificantquantitiesof the metabolites,and(c) handlingof plantsbefore andduringextractionmay result in compound degradation f the compoundsarerelatively unstable (104). Maximum yield of single terpenoid metabolites


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120 HAY & FENICALfrom seaweeds usually ranges from 0.5% to 1.5% of plantdry mass (52, 103),with rare reportsof metaboliteyield in the 2-5% range (28, 93, 101). Giventhe problems of extraction and purification isted above, it is possible thatmany of the listed yields are only half or less of the true concentrations.Thisis true especially for compoundsgiving low yields since a largerproportion fthe compoundis lost in the purificationprocess.Because phlorotannins re largemolecules that occur in complex mixturesand are water-soluble, they are relativelydifficult to work with from both achemical and an ecological perspective. The most common method of es-timating phlorotanninconcentration s the Folin-Denis procedurewhich hasbeen discussed by numerous authors (116, 140). This method does notdirectly measure phlorotanninsbut rathermeasuresreactive phenol residues.Thus, phlorotannindeterminationsmaybe confoundedby ascorbicacid, urea,polypeptides, diethyl ether, detergents, and nontannic phenols. When notsubjectto significant interference,this method providesa general measureoftotal phenolics but does not differentiatebetween the many differenttypes.Given the uncertaintiesof the Folin-Denisprocedure,most authorsalso usethe Bate-Smith hemanalysis method (116) to estimate the protein bindingability (relative as-tringency) f the phenolics in their samples. In this assay,the extractedphlorotannins re reacted with the proteinof freshly hemolyzedblood, and the hemoglobin remaining n solution is determinedspectropho-tometrically(116). In general, thereis good agreementbetweenthe resultsofthe astringencyand totalphenolics assays when these arerunon a numberofdifferentalgal species (1, 132). However, some problematic pecies are clearexceptions to the general trend. Examples of these include: (a) Analipusjaponicus which appearsto be high in phenolics but low in tanning ability(132); (b) Ecklonia maxima which has a tanningability that would imply aphenolic content some seven times that measured by the Folin-Denis pro-cedure(1); and(c) Sargassumpolycystum,S. cristaefolium,Turbinariaorna-ta, and Alaria margintatawhich give Folin-Denisreactions indicating 0.8 to1.6% phenols by dry mass but which show no phloroglucinolderivativeswhen subjectedto more specific chemical assays (143).These commonly used assays thus give a reasonably good general de-terminationof phenoliccontent andastringency,but any particular alue mustbe viewed as uncertain. These chemical difficulties have hindered rapidadvances in researchon the ecological roles of phlorotannins ven thoughphlorotanninswere used in some of the first experimentsdemonstrating hedeterrenteffects of seaweed secondarymetabolites (35). Since these com-pounds are water-soluble, tests of their effects against herbivores usuallyinvolve mixing phlorotannins n an agar matrix which contains an alga thatstimulatesfeeding. Grazingon phlorotannin-containinggar s comparedwithgrazing on similar agar preparations hat lack the phlorotannins.Agar pre-


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122 HAY & FENICALby soaking it in a solution of tannic acid (a tannin that does not occur inplants) until it acquireda phenolic content similar o several phenolic-richandmore herbivore resistant seaweeds with which it co-occurred(132). A morerecent study (134) has tested specific types of phlorotanninsagainst twoherbivoroussnails and a sea urchin. The phlorotannins ssayed included: themonomer phloroglucinol (of which brown algal phenolics are composed); amixtureof high molecularweight (hundredsof phloroglucinolunits) phloro-tannins from Fucus vesiculosus, low molecular weight (six or fewer phloro-glucinol units) phlorotannins rom Eisenia arborea, and phlorotannins romHalidrys siliquosa composedof a mixtureof high andlow molecular weightmolecules. These compoundswere all tested against the gastropod Tegulafunebralis. A few were also tested againstthe gastropodT. brunnea and thesea urchin Strongylocentrotuspurpuratus. Test concentrationswere 0.0%,0.2%, 0.5%, or 2.2% of the wet massof the agarandfood used in the grazingassays. It is not clear whattheseconcentrationswouldbe on a drymassbasis;however, given the high wet mass to dry mass ratio of most agar mixes,concentrationscould be high relativeto those found in most seaweeds. Themonomer phloroglucinol at 2.2% of wet mass had no effect on grazing byTegulafunebralisbut inhibitedgrazingby the sea urchin.Otherphlorotanninswere generally significantdeterrents o T. funebralis feeding. In six cases aphlorotanninwas tested against more than one herbivore. In two of thesecases a compound that deterredfeeding by one species had no effect onanother.This supports he contention hattanninsmayhave specific activitiesand be less generalizedthan is often assumed (146).Early investigationssuggestedthatplant phenolicsactedagainstherbivoresby complexing proteinsand decreasing digestive efficiency; this effect wasoriginally assumedto be broad, generalized,and difficultif not impossibleforherbivoresto avoid (26, 119). The variancein responseof differentmarineherbivores o the samepolyphenolic compoundsand the differencesin effectof different polyphenolics on the same herbivore suggest that herbivorespossess differential olerancesto phlorotannins ndthat similarpolyphenolicscan differmarkedly n their deterrent ffect. This is in general agreementwithrecent terrestrial tudies suggesting that (a) tanninsmay have more specificactivities than is generally assumed (146), (b) they are not impervious tocounteradaptation y herbivores since many insects are not affectedby hightannin content in their foods (4, 30, 81, 82), and (c) tanninsmay not act asdigestibility reducersbut, like some terpenes, appearto act by inhibitingfeeding or causing cell damage (4, 81, 82).Despite the uncertaintiessurroundingpolyphenolic-herbivorenteractionsin both terrestrialand marinecommunities, the above experimentsdemon-strate that feeding by sea urchins and gastropodscan be significantly sup-pressed by phlorotannins. Additionally, there are negative correlationsbe-


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124 HAY & FENICALphotosynthesis are not placed in the new and more herbivore susceptiblegrowth until light is available and they can start producingincome for theplant (53). In addition, crude extractsof these young white tips deter grazingby coral-reef fishes significantly more than do crude extracts from morematuregreen tips (107). Extracts rom some populationsof Halimedain areasof high herbivoreactivityalso deter herbivorous ishes more than do extractsfrom populations of the same species in habitats subject to lower rates ofherbivory (107).Seaweeds in the tropical genera Udotea, Cymopolia, Tydemania, Chlor-odesmis, andPseudochlorodesmisalso producecompoundsthat reduce feed-ing by coral-reefherbivores.The diterpenoids hlorodesminand an epoxylac-tone, from Chlorodesmis astigiata and Pseudochlorodesmis urcellata re-spectively, deterred eeding by reef fishes in field assaysand by the rabbitfishSiganus spinus in laboratorytests (100, 101, 104). A diterpenoidfromTydemania expeditionis also reduced feeding by the rabbitfish S. spinus(104). However, the effectiveness of chemical defenses may vary amonglocations or times; the diterpenoiddialdehyde acetate, udoteal, from severalUdotea species significantlyreduced losses to reef fishes in only one of thethree field assays in which it was used (100).The chemistry and ecology of Caulerpa species have recently been re-viewed (104). Although a largenumberof unusualterpenoidcompounds areproduced by the genus, some of the early reportsregarding he chemistryofCaulerpa appearto have been in error.The pigment caulerpinwas initiallyreported to be biologically active, but recent studies indicate that it lackssubstantive effects (104). Additionally, the toxin caulerpicin,reportedas aminor metaboliteof severalspecies, is not apure compoundbutrepresentsanundefined mixture of metabolites. Caulerpenyne,a unique acetylenic ses-quiterpenoid ynthesized by severalspecies, is appropriately escribed n theliterature.It deters feeding in laboratoryassayswith the CaribbeanparrotfishSparisomaradians(139), decreasessurvivorshipwhen fed to juvenile gastro-pods (103), andappears o deterfeeding in the tropicalsea urchinLytechinusvariegatus (83). It does not affect feeding by the Pacific rabbitfishSiganusspinus (104).Few studies have assessed the herbivore-deterrent ropertiesof differentsecondary metabolites under field conditions (52, 100, 107). In one suchstudy (52), five compounds from different tropical marine algae and onerelatedcompoundfrom an herbivoroussea hare (Aplysidae) were coated atapproximatelynatural concentrationsonto the palatableseagrass Thalassiatestudinumand placedon Caribbean oral reefs wherethey couldbe eatenbythe diverse group of herbivorous ishes that occur there. Laboratoryassayswith the sea urchin Diadema antillarumwere also conducted. When com-paredto appropriate ontrols, the following terpenoidcompoundssignificant-


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SEAWEEDCHEMICAL EFENSES 125ly reducedThalassia consumptionby both fishes and urchins:stypotriol romthe brown seaweed Stypopodium onale; pachydictyol-A, which is producedby several genera of tropical (Dictyota and Dilophus) and warm-temperate(Pachydictyonand GlQssophora)brown seaweeds; elatol, from the red algaLaurencia obtusa; and isolaurinterol,which is producedby several tropicaland warm-temperate pecies of Laurencia. Undervery mild acid cQnditions,isolaurinterol s convertedto a structurally imilar compound, aplysin, foundin high concentrations in sea hares that feed on isolaurinterol-containingLaurencia species. Aplysin did not deter feeding by either type of herbivore.Cymopol (Figure 1), a terpenoid bromohydroquinone rom the green algaCymopolia barbata, significantlyreducedfeeding by reef fishes but signifi-cantly stimulated eeding by Diadema. In contrast, cymopol appears o deterfeeding by the tropical sea urchinLytechinusvariegatus (83).Pharmacologicaland crude bioactivity assays suggest that several of theabovecompoundsshould function as generalized oxins (52). However, theselaboratory assays are not necessarily good predictors of how compoundsaffect feeding by herbivores.As one example, pachydictyol-Aandstypotriolare equally effective at deterring ishes andDiadema even though pachydic-tyol-A shows almost no bioactivityin laboratoryassays while stypotriol andits oxidation product, stypoldione, are broadlybioactive cytotoxins (52).

Otheralgal compoundshave also been shown to deter herbivores n con-trolled andecologically realisticexperiments.However,because these studiesfocus primarilyon the effectivenessof chemicaldefensesagainst arge mobileversus small sedentaryherbivores, they are discussed in a later section. Forcompleteness, the compounds, seaweeds producing them, and herbivoresthey deter are listed below: ochtodene from the red alga Ochtodes secundir-amea detersfeeding by Caribbeanand Pacific reef fishes, andan unidentifiedmixtureof halo-monoterpenesrom this same alga detersfeeding by a mixedspecies groupof Caribbeanamphipods 106); dictyopterenesA & B from thebrownalgaDictyopterisdelicatula deterCaribbean eef fishes (50); pachydic-tyol-A from thebrownalga Dictyotadichotomadetersfeeding by the temper-ate herbivorous fishes Lagodon rhomboides and Diplodus holbrooki; anddictyol-E from Dictyota dichotomadeters the temperatesea urchin Arbaciapunctulata as well as the two temperatefishes listed above (51, 54).Physiological Effects on HerbivoresAlthough manyseaweed metaboliteshave been investigated n pharmacologyassays (23), their physiological effects on herbivores are largely unknown.Whenthe omnivoroustemperate ish Diplodusholbrookiwas fed for approx-imatelythree weeks on a diet with pachydictyol-Aas 1%of food dry mass,treatmentfish grew only half as rapidly as control fish even though bothgroups consumed the same quantity of food (51). In a similar although


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SEAWEEDCHEMICAL EFENSES 127vesicles, vacuoles, and similar structurescalled physodes (116). Unlike theLaurencia metabolites, phlorotanninsdo tend to be released into the envi-ronmentbut the rate undernaturalconditions may be much lower than someolder 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 lan-osol from Neorhodomela (Rhodomela)larix (114), which appearto be re-leased from the alga, perhaps under stress. This could not be the functionof metabolites such as those of Laurencia, which are not released at thealga's surface.WITHIN-PLANT VARIATION Numerous studies suggest that herbivorede-fenses are costly to the plants that deploy them and must therefore bedifferentially allocated to plant portions depending on the value of eachportionand that portion'srelativerisk of herbivoreattack(26, 45, 80, 118,119). If this is the case, thenwe mightexpectconsiderable ntraplant ariationin the concentrationor type of defensive compounds.Few rigorousstudies ofwithin-plant variation have been conducted; however, compounds clearlytend to be most abundant n young, actively growing, and thus most pro-ductive seaweed portions. Species with apical growth tend to have highestconcentrations n the upper portionsof their branches(53, 107, 113); thosewith intercalarymeristemshave the highest concentrationof compoundsinthe meristematic egion(63). The sulfuricacid producingalgaDesmarestiaisat variancewith this trendsince the acid appears o be equallydistributed nthe differentplant portions (1).Reproductive tissues may also be differentially defended. In the kelpAlaria, phlorotannin ontent of the sporophylls s 5-6-fold greater hanthatof the vegetative portions, and sporophyllsare significantlyless palatabletograzingsnails (131). However, in most brownseaweeds, receptaclesare notenriched in phlorotannins 116). The tropical green seaweed Halimeda hasgametangiathatareconsiderablyenrichedin halimedatetraacetateelative tomaturevegetative portions (103).The redalgaNeorhodomela arixproduces hebromophenolanosol, whichvaries seasonally between 1.2% and 3% of plant dry mass; winter con-centrationsare about three times those of summer(113). A similarpatternoccurs in the brown algae Ascophyllumand Fucus with winter maxima inphlorotannincontent that are 40-100% higher than summer minima (117).For bothof these temperate pecies, herbivoryshouldbe higher n the warmersummermonths; herefore,thetemporalpatternn compoundproductiondoesnot appear to correlatewith increased herbivoreactivity. Additionally, forFucus andAscophyllum he seasonal minimain phlorotannin oncentrations


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SEAWEEDCHEMICAL EFENSES 129Ecologically relevant experiments have been conducted on changes inphlorotanninevels in the brown seaweed Fucus distichus (142). These plants

elevated phlorotannin evels by 20% within two weeks of simulatedherbivoreattack anddecreased their losses to herbivorous nails by about 50%relativeto controlplants thathadnot been induced. Thebetween-plantdifferencesinphlorotannin evels detected n the field (about20%)were similar o the levelscaused by induction.GEOGRAPHIC VARIATION The majorityof seaweed secondary metabolitesappear o be producedby generathat arepredominately ropicalor subtropicalin distribution Table 1; also see 23, 93). In the few cases in which speciesfrom these genera also occur in temperate eas, the temperaterepresentativesappear o containless defensive compound hando theirtropicalcounterparts(98). Brown seaweeds thatproduce phlorotanninsare a strikingexceptiontothis general trend. In temperate seas, brown algae in the family Fucales(rockweeds)tend to producephlorotanninsn high concentrationswhile thosein the family Laminariales(kelps) usually have low concentrations(132,143). Fucales and other brownseaweeds in tropicalhabitatsall appear o below in phlorotannins 133, 143). This lack of phlorotanninproductionbytropical seaweeds does not appearto occur because phlorotanninsare in-effective againsttropicalherbivores. When tested on naturalcommunitiesofreef fishes in Guam, extracts from phlorotannin-rich emperate species allsignificantly decreased fish grazing, while extracts from phlorotannin-poortemperate species had no deterrenteffects (143).The Cost of ChemicalDefensesA growing literatureon herbivoryand the evolution of herbivoredefensessuggests thatdecreased susceptibilityto herbivorescan be achieved only bydivertingenergy andnutrients rom otherplantneeds (15, 26, 80, 118, 119).Thus, defenses arehypothesized o be costly, and in the absence of herbivory,less defended individualsor species will have higher fitness than do moreheavily defended individualsor species. Several terrestrial xamples fit thispattern (15, 118).If this reasoningappliesto seaweeds, thenhabitats hat serve as predictableescapes from herbivory should be populated primarily by species or in-dividuals that arehighly susceptibleto herbivoredamage. Low susceptibilityto herbivoryshouldbe characteristic f those species or individuals hat occurin habitats where herbivory is predictably high. This pattern occurs in anumberof marine communities (22, 44, 45, 49, 80, 103, 104, 107), andexperimentaldecreasesin herbivoryresult in the more herbivore-susceptibleseaweeds dominatingthe more herbivore-resistantorms (71, 80).There are no direct experimentalassessments of the cost of chemical


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SEAWEEDCHEMICAL EFENSES 131EFFECTS OF HERBIVORE SIZE AND MOBILITY Despite the proven generaleffectiveness of some compounds, several recent studies show that feeding bysmall, relatively sedentary, and commonly overlooked marine herbivores(mesograzers) like amphipods, polychaetes, and ascoglossans is often un-affected, or occasionally stimulated, by compounds that deter larger, highlymobile, and more commonly studiedherbivores uch as fishes and sea urchins(50, 51, 54, 106, 108). In several respects, marine mesograzers may beecological equivalents of terrestrialinsects since dispersal to plants thatprovide adequate ood and protection rom predatorsmay be one of the majordifficulties these herbivores face (50, 51, 54). Mesograzers can consume awide variety of algae, but they appearin many cases to prefer feeding onseaweeds that arechemically deterrent o otherherbivores, especially fishes(50, 51, 54, 106, 108). They commonly live on the seaweeds they consumeand thus may often be incapable of separatingfood choice from habitatchoice. Since they are subject to intense predationfrom predatory, om-nivorous, andherbivorous ishes, mesograzers hat live on and eat seaweedsthat arerarelyvisited by fishes shouldhave a higherfitness than those livingon seaweeds commonlyeatenby fishes. To accomplishthis they would needto be resistantto seaweed chemical defenses. Similarargumentshave beenadvancedconcerningthe evolution of insect feeding patternsand the need for"enemy-free-space" 59, 115).

Although only five studies have investigated how seaweed secondarymetabolites affect feeding by mesograzersas opposed to largerherbivores(50, 51, 54, 106, 108), all show that compounds significantly deterringherbivorous fishes either stimulate or do not affect feeding by commonmesograzers. Since these studies were conducted in both temperate andtropicalhabitats and involved differentfishes, mesograzers, seaweeds, anddefensive chemicals, this pattern may prove to be general. Additionally,several naturalhistoryobservationssupport his hypothesis.The sulfuric acidcontaining kelp Desmarestia is avoidedby sea urchinsin both SouthAfricaand Chile (1, 18), buttheamphipodAmphithoehumeralis ormsnestingtubesin the kelp and grazes its surface (1). On Caribbeanreefs, the amphipodPseudamphithoides ncurvariaeats, lives in, and makes an unusualbivalveddomicile from thebrown seaweedDictyota bartayresii; he amphipodwill noteat or make domiciles from several other seaweeds common in its habitat(72). D. bartayresii produces pachydictyol-A (93), which has been demon-stratedto deter feeding by Caribbeanreef fishes (52). In the easternNorthPacific, the amphipodAmpithoetea excavates chambersin the brown algaPelvetia (41) which produces high concentrationsof phlorotannins 132).SPECIALIZED HERBIVORES Adequately documentingand comparingfeed-ing specialization among herbivoresis difficult (32), especially for marinemesograzersthathave rarelybeen carefullystudied. However, the informa-


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132 HAY & FENICALtion presently available suggests thatspecialistherbivoresmay be less com-mon in marine hatin terrestrial ommunities(51, 80, 135). The few special-ized marine herbivoresknown tend to be relatively small, to have limitedmobility, and to live on and consume plants that provide them with someprotectionfrom theirpredators(51, 54, 108, 135). The best studied of thespecialized marinefeeders are the opisthobranch astropods.Many lineageswithin this subclass have evolved from shelled snails into sea slugs as theydevelopedthe abilityto feed on defendedpreyand to sequester heir defenses(25). As examples, the eolid nudibranchs equester stinging capsules fromtheir coelenterateprey;the dorid nudibranchs equestertoxins fromsponges;and sea hares(Anaspidea)andascoglossans(Ascoglossa) sequesterdefensivecompoundsfrom seaweeds. Ascoglossans are small (some mm to a few cmlong) sea slugs that feed by sucking algal sap (60). They sequester bothsecondary metabolites(62, 108) and algal chloroplasts; he undamagedchlo-roplastsare retainedintracellularlyand show sustainedphotosynthesis,withthephotosyntheticproductsbecomingavailableto theanimal(141). Sea haresarelargerthanascoglossans (some reachinga mass of 6800 g); they consumelarge quantities of seaweeds which they chew instead of suck; and theysequester algal secondary metabolites but not chloroplasts(2, 129). Bothascoglossans and sea hares are usually cryptic when in their naturalhabitat(25, 62).Ascoglossansfeed primarilyon Caulerpa spp. andgenera n the chemicallyrich families Halimedaceaeand Udoteaceae (Halimeda, Penicillus, Udotea,Cymopolia, Chlorodesmis,Avrainvilleaand others); however, some specieshave radiatedonto otherfoods (60, 61). Few studieshave rigorouslyassessedfeeding by ascoglossans, but most species are reported o feed on one or asmall numberof relatedspecies (60). Although t is widely assumedthattheyare defended by sequestered algal metabolites contained in the mucus andautotomized cerata that they release when disturbed,investigationsof thisphenomenonare rare.Elysia halimedae, on Guam, is reported o occurexclusively on Halimedaspecies, with animals grazing most heavily on the gametangiaand lightlycalcified new segments (108), which are the plant regions with the highestconcentrations of chemical defenses (53, 103, 107). They convert theHalimeda compoundsto a related diterpenealcohol that they sequesterasapproximately7%of theirdry mass;thecompound s also sequestered n theiregg masses whichtheytend to place on Halimedatips (108). Infield assays, aconcentrationof 3%drymassof this compoundsignificantlydeterred eedingby both herbivorous and carnivorousreef fishes (108).Studies of Mourgona germaineae in Florida suggest a similar pattern,althoughthe chemical aspects of the interactionsare less well documented.This ascoglossan feeds exclusively on Cymopoliabarbata (62), which pro-


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134 HAY& FENICALwhere they may function as predatordeterrents.When disturbed,Aplysiaproducea purple nkthat s not toxic but may interferewith the chemosensoryapparatusof predators; f the disturbancecontinues, they produce a milkyfluid that containstoxic oils reported o cause muscularparalysisanddeathofmarineorganisms(129). Althoughthe directrole of the algal metabolitesinAplysia's defense againstpredators eems obvious, there are no ecologicallyrealistic andrigorouslyconducted estsof this. Severalchemists have reportedfragmentarybioassays suggesting that the compoundsfunction as predatordeterrents 65, 129, 130). Additionally, a juvenile fish has been suggested tobe a Batesian mimic of an Aplysia with which it co-occurs (55). If thisinterpretations correct, it arguesstrongly for the predictableeffectiveness ofAplysia defenses. AlthoughAplysiaandascoglossanssequester oxic metabo-lites from theiralgal prey, most of these animals arevery cryptic. Few showthe warningcolorations hatcommonlyoccur in terrestrial nsects thatseques-ter plant toxins or in dorid nudibranchs hat sequestersponge toxins.Given the tremendous effects that herbivorousfishes, sea urchins, andgastropods have on seaweeds (11, 43, 47, 71, 80), most seaweed chemicaldefenses probably evolved in response to diffuse herbivory(30) from thesediverse types of herbivores, and not in response to the few more specializedherbivoresdiscussed above.

EVOLUTIONARYOVERVIEWAND COMPARISONWITH TERRESTRIALCOMMUNITIESPlant-herbivore nteractions n terrestrialcommunities have been studied ingreaterdetail and over a much longer period of time than have seaweed-herbivore nteractions.Muchof the terrestrial esearchhas focused on insectsas the herbivoresof primary mportance(20, 121). The availabilityof thisbackgroundnformationallowedecologists to startconstructinggeneraltheo-ries aboutplant defenses in the 1970s (26, 119). These theories were forwardlooking and made very broadpredictionsof generalizablepatternsbased onthe limited data thatwere thenavailable. Since theproposedmodelswere wellargued and reflected the patternsthat several authors were beginning todescribe, they were quickly accepted,rather thantested, by most ecologists.These theories of plant defense still serve as an influential framework forpresentday studies (15) even thoughsome of theirprimaryassumptionsandpredictions have been repeatedly questionedor demonstrated o need mod-ification (4, 14, 15, 30, 32, 81, 82, 146). Since an excellent summary ofdefensive theory is available (30), we discuss it only briefly here and thenevaluatethedegreeto whichthepredictions romterrestrialheorycoincide orconflict with patternsin the marineenvironment.


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136 HAY & FENICALturnoverratesandmay demandthatlarge amountsbe synthesizedin order tomaintaina 1%concentrationover the lifetime of the leaf. They suggest thattoxins could be more expensive than tanninsin some cases.In seaweeds, even the differencein turnoverrateis unclear.Some specieslike Laurenciaproducevery potenttoxins (27, 28, 52) thatare sequestered nmembrane-boundesicles (145) andapparentlynever releasedunless the cellis ruptured 58). Other seaweeds like the brown alga Stypopodiumproducepotent toxins that are released into the water (37) and must thereforebeconstantly synthesized. Brown seaweeds also releasephlorotannins116), sothe cost of turnoverand maintenancemaybe no different or plantsproducingphlorotanninsthan for those producing terpenes. Thus, species with lowconcentrationsof qualitativedefenses may incur either high or low costs, andit is not at all apparenthow these costs compare with those of supposedlyquantitativedefenses like phlorotannins.The indirectevidence that chemicaldefenses are somehow costly is persuasivefor both terrestrial 15, 30, 118)and marineplants (45, 80, 131, 142). There is, however, no evidence ofdifferentialcosts betweenwhat have traditionallybeen termedqualitativeandquantitativedefenses.DIFFERENCES BETWEEN QUALITATIVE AND QUANTITATIVE DEFENSESReevaluation s neededfor the widely held notion thattanninsand phlorotan-nins are dose-dependentdigestibilityreducers(26, 35, 119, 132, 134, 138,142) that are especially resistant to counteradaptation y herbivores andfundamentallydifferentfromother defensive compounds.First, the mode ofaction of phenolics may be no different from the mode of action of manyqualitativedefenses. Althoughtanninshave often been shownto decreasethegrowthandsurvivalof herbivores,recent studiessuggestthatthis resultsfromfeeding inhibitionand cell damage (as is the case with qualitativedefenses),not from interference with digestion and assimilation (4, 81, 82). Liketannins,phlorotanninsdecrease feeding by marine herbivores(35, 134), buttheir mode of actionorphysiologicaleffect on marineherbivoreshas notbeendetermined.Second, there is no evidence of fundamentaldifferencesbetween tanninsand qualitativedefenses in the probabilityof herbivoresevolving counter-adaptations. A wide variety of terrestrialherbivores feed primarily ontanniferous plants and are not negatively affected when grown on dietscontainingtannin(4, 30, 31, 81). For marineherbivores,feeding by somegrazers is not deterredby some phlorotannins,and many common herbi-vores in AustraliaandNew Zealandappear o be unaffectedby phlorotannincontent 2-3 times as high as those that commonly deter feeding by herbi-vores in coastal North America (22, 134; P. D. Steinberg personal com-munication).


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SEAWEEDCHEMICAL EFENSES 137Third, the dose-dependentdifferences that define qualitativeversus quan-titative defenses may be illusory. In a recent study (81) where adapted and

nonadaptedmoth larvae were fed diets with a wide range of tannin content,the adaptedmoth grew equally well on all diets, while the nonadaptedmothshowed equally decreased growth on all tannin-containingdiets, due tofeeding inhibition. There were no dose-dependent ffects on either herbivore.In seaweeds, phlorotanninsdeter herbivore feeding in a dose-dependentmanner 35, 134), but then so do terpenoids 51, 54). Additionally, the effectof phlorotannins on herbivore feeding shows significant variance amongdifferent herbivore species and different types of phlorotannins (134),suggesting that phlorotanninsare neither uniformin activity nor as broadlydeterrentas has been assumedin most of the terrestrialmodels. Thus, in therespects discussed above, seaweeds and terrestrialplants seem reasonablysimilar; neither function as predictedby the models.If tannins are predictablyfound in apparentterrestrialplants, then thisaspectof defense may differ between marineand terrestrial nvironments.Inseaweeds, phlorotannin-richspecies are restricted almost exclusively totemperateand cold seas (132, 133, 143). Although phlorotannin-rich ucalescan be very abundantat some sites and tidal elevations, the most apparentplantsin cold andtemperate eas arekelps (17, 124), most of which are low inphlorotannins 132, 143) and very susceptible to herbivore attack (22, 124).As an explanation for the lack of defenses in temperate kelps, Estes &Steinberg (22) suggest that kelp beds have traditionallyattractedand main-tainedpopulationsof sea otters thatpreyed selectively on some of the majorkelp grazers,thusprecluding hese frombecomingabundantandnegatingtheneed for chemical defenses. As sea otters were harvested o nearextinction,invertebrateherbivoresescaped control and devastatedkelp beds. Estes &Steinberg(22) develop a numberof paleontologicalarguments uggestingthatthe absenceof sea ottersin the southernhemisphereshould have selected forseaweeds with betterdevelopedchemicaldefenses and herbivoresbetter ableto cope with these.On tropicalcoralreefs, where herbivory s very intenseandresults from adiverse arrayof herbivores, phlorotanninsare rareor absent even withintheFucales (133, 143). Recent assays of extractsfromphlorotannin-richemper-ate seaweeds and their deterrenteffect on tropicalreef fishes indicatedthatphlorotanninswould be effective againstreef herbivores 143), so it is unclearwhy theydo not occur there. There arefew apparent pright eaweedsin thesecommunities, but those that are (Halimeda, Chlorodesmis, and sometimesother members of the Caulerpales and Dictyotales) all contain terpenoidcompounds (qualitative defenses) instead of phlorotannins quantitativede-fenses). Manyof the most common and herbivore-resistantpecies have bothqualitativechemical defenses andcalcification(45, 105). Since calcification


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SEAWEEDCHEMICAL EFENSES 139However, some marinemesograzersare partially, or restrictively, special-ized to certainhost plants (50, 51, 54, 60, 72, 108); these herbivores end tobe exceptions to the trendsin generationtimes and dispersalstrategies out-lined above. Amphipodsand some ascoglossansbrood theiryoung or undergodirectdevelopment, thus avoiding the planktonicdispersal stage. Many alsohave generation times similar to, or shorter than, their algal prey. Thesedifferences between mesograzersand largermarineherbivorescould facilitatelocal adaptation o host plants and explain, in part, why severalmesograzershave adapted to seaweed chemical defenses that are effective deterrentsoffishes and larger nvertebrates.Since young marineherbivoresarenot placedon appropriate ost plants by large, very mobile adults(as occurs in terrestrialhabitats), t should be difficult formarineherbivores o specialize on unappar-ent plants. Although data are limited and subject to interpretationalbias,marine herbivores appearto have specialized most often on apparentplantslike Dictyota (72), tropicalgreen seaweedsin the orderCaulerpales 60, 108),and seagrasses (60). In additionto being apparentwithin a habitat,most ofthese seaweeds are widely distributed among habitats. Young herbivoresshould thereforehave a higher probabilityof successfullydispersingto theseplants than to unapparentplants. Since these mesograzersappearto have alimited impact on plant fitness relative to the larger effects of fishes andurchins,thepotentialfor true coevolution betweenmesograzersand theirprey

is probablylimited (11, 47, 71).SUMMARYSeaweeds producea diversearrayof secondarymetabolites hat deterfeedingby commonmarineherbivores.However, the defensive value of a compoundis a specific functionof compoundstructureand the herbivorespecies attack-ing the plant. The functionof compoundscannotbe predictedby structuralclass alone so it is inappropriate,or example, to lump terpenesas toxins andphlorotanninsas digestibilityreducers.The spatialandtemporaldistributionof secondarymetaboliteswithincells, withinplants,andbetweenplantsoftenvary in ways that are adaptive.Individualplantsor plant portionsthat are atgreatestrisk are often best defended.Herbivore ize, mobility, andlife-historycharacteristics ppear o be corre-latedwith resistance o seaweedchemical defenses. Smallrelatively sedentaryherbivores ike some amphipods, polychaetes, and ascoglossans (mesograz-ers) often selectively consume seaweeds that are low preferencefoods forfishes and largerinvertebrates.Compounds romthese seaweeds deter feed-ing by largerherbivoresbut stimulate,or do not affect, feeding by severalmesograzers.Althougha few mesograzerssequesterchemicaldefenses fromtheiralgal hosts, most arenot highly specializedandappear o be advantaged


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140 HAY & FENICALindirectlyby their close associationwith seaweedsthat are not visited by theirpredators.A comparisonof chemical defense in marineversus terrestrial ommunitiessuggests that (a) the assumptionof a fundamentaldifferencein the cost andfunctionof qualitativevs quantitativedefenses needs to be reevaluated, (b)the degreeof feeding specialization n marinevs terrestrial ommunitiesmaydifferdue to fundamentallydifferentdispersalmodes of commonherbivores,and (c) truecoevolutionis unlikelybetween seaweeds andmarineherbivores.ACKNOWLEDGMENTS

Funding for our work on the chemical ecology of seaweeds has beenprovidedby NSF, CaliforniaSea GrantProgram,The National GeographicSociety, The CharlesA. LindberghFund, The AustralianMuseum, and theNorth CarolinaBiotechnologyCenter.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,andF. Wilson commentedon the manuscript,brought iteratureo ourattention,orhelpedin other ways.To all we are grateful.LiteratureCited

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