II

OIKOS <>9:-l7~9X. Copcnhagen 1994

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A functional group an svroach to the structure of algal-dominated

cornmunities

Robert S. Steneck 'and Megan N. Dethier

Steneck, R. S. and Dethier. M. N. 19Y~. A functional group approach to the ,tructure ofalgal-dominated communties. - Oiko" 69: 476-498.

R. S. Sreneck. Depr of Oceallograplr.'" am/ Cerzrer/or Marille SllIdit's. Dar/in? Mari,,!.'Cemer. Univ. (Jj .'v!aine. lI-'alpo/e.. \fE 04573. USA. - M. IV. DelÍli"r. Insr. .•.or EIl\'i-l'(}Illllell/a/ SllIdies and Fridav Harbor Labf}r(l(ories. U"i\'. oj \\ilshi"!!!l";. Frie/a\'H'lrbor. WA 98250. USA.

Natura communities shauld be described in rerms simple6~~ R " ",\f1;'óO~ .e_:n_lu a be rs 000 and deraded enough to convéyuseful information about their structure and functionalcomponents. There exists a bread spectrum 01' ways todescribe panems. At one end 01'this specrrum. species arethe fundamental unit 01' measure. Because many factorscontribute to the distribution and abllndance of a givenspecies, it is often impossible to predict its behaviorconsistently. At the other end of rhe spectrum are func-tional groups which categorize species according to fea-tures such as body plan. behavior 01' rife history strategy.In this paper, we argue that analyzing cOIlununity pat-tems for marine algae via groupings based on functionalaspects of their morphology and anatomy provides sub-

Accepted 17 September 1993

Cop}right © OIKOS 1994ISSN 0030-1299Printed in Denmark - aH rights reservecl

476

stantial insight into communiry strucrure. A functionalgroup analysis can be applied more broadly in 'pace fol'making biogeographical comparisons. :md in time forreconstrucríng paleocommllnities, than is possible at rhelevel of spec:.::s 01' among relared higher taxa.

O\'er the past three decades mosr community ecol-ogis(s. followin" the lead of Hutchinson and ~[;:¡c.-\rthur.

..... (.) ;C.O¡.dlO. .

stressed the l/l1lqut!ness of specles. That no (\\'0 specle~can occupy (he same ecological niche has been a drivingaxiom stimulating interest in a variety oi topics includingcompetiríon. niche compression. ~haracrer displa~emenl.resource panitioning and species diversificatian. Ho\\'-ever. many af these cancepts have been qLles[ion~d andrecently criticized (e.g., see Sale 1977. Peters 1991. Bond

011-;05 n~:.1 (1'1~'¡)

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MORPHOLOGY

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;':~. cm

-1lO

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lO _ lO

IÓI

THALLUS S1ZE (•• 1

4 CORTtCATEDMACl'.OPHYTI:S

(ta'e~)

Clt.ondnu and Gi,artUia

nJNCTIONAL CROUPS COMPARATIVE ANATOMY

1 MlCROALGAE (sin,l ••• U)Cyanoboc1eria and di.""",

2 FILa.MENTOIJS ALGAE(uniseriato)

C1DdoploDr4 aN1B ••• , ••

3 roUOSE ALGAE (.inSk Uyer)MOftOStTOII't4 ar multiIayered

VI••••P"'T'."a

5 LEATHERYMACROPHYTES

Kelp andFucus

6 ARnC'.Jt.ATED CALCAREOUSALGAE

C""alJiNJ andHtJi~d4

7 CRUSTOSE ALGAELilholluvnnion,

PIJ$1DNV/i4and

"Ralfsi."

CORnCA TED FOUOSE3.5 ALGAE

Djc1yo1a and Padind

Fil!. l. Diagrammaticrepresentation ol" algalfunctional groups.Anatomical components arenot drawn to scale. butillustrate tissuedifferentiation such asbetween the cortex andmedullary regions of thethallus 01' a macroalga. Thespecific form of eachfunctional group illustratedis indicated in parentheses.A few representati ve gener;¡are given as examples foreach group. Numbers at len,algal group ("AG") numbers,are for quick reference(rankings are described inResults). Note that groups ofa given morphology withincceased anaromicJicomplexity (e.g .. they arecorticatcd) are designated byhigher AG numbers. Thus.thinly corticated orpolysiphonous filamentsbecome AG 2.5 andsimilarly corticated foliosefonns becorne AG 1.5.

et al. 1992). A funcrional group approach, in contrast,stresses similarities among unrelated species that sharecritical organismal fearures. We discuss the overridingimportance of a small number of species attributes to thestructure of benthic marine algal communities, and notethat these attributes may be shared polyphyletically.

The functional group approach, although having re-ceived little attention among community ecologists, mayhave been foreseen by MacArthur (1972) when he pre-dicted that "the future principIes of the ecology of coexis-tence will... be of the form 'for organisms of type A inenvironment of structure B, such and such relationshipwill hold'" (boldface ours). We will consider the types ofmarine algae that live under specitic marine environ-ments (defined below). We offer data and examplcs insupport of this approach as an altemative to other meansof studying communities. rather than as éL strict test of ourhypothesis. Our objective is to examine pattems 01" algalfunctional group abundance, diversity and dominance

relative 10 extrinsic charucteristics of their environmenl.To demonstrate rhe broad applicability of the functionalgroup approach. we examined three biogeographicallydi'stinct regions: the westem North Atlantic, the eastemNorth Pacifico and the Caribbean as exemplified by sitesin Maine, Washington and St. Croix (U.S. Virgin Is-lands), respectively.

Definition of terms and rationale

We explore the hypothesis that observed pattems in thedistribution and abundance of life forms of algae (func-tional groups) result largely from two environmental pa-rameters: 1) productivity potential (factors that contribmeto the maximum possible rute of biomass production) and2) disturbance potential (factors responsible for the maxi-mum possible rute of biomass lost). It is important lO note

OtKOS 69:3 (1994) 477

Q «;&Y:¡iLUtnm .....su ,-' ., _C

Bi = R¡ + Pn, - Di' where

Fig. 2. The relati0nship between disturbance imensity and fre-qency. LOW, MEO and HIGH refer to disturbance levels.

Si = Biomass of an algal speeies 01' functionaJ group (i)that accumulates over sorne period of time. i = the

spccilic algal functional group(s) conccmed i.e .. 1-7(sce Fig. 1). The numeric designalion in Fig. I is basedon Ihe ranking of mass-specitic productivity (see Re-sults).

R, = Rate of recruitment. which is a function of:1) lntrinsic properties of the algal species or funetional

group (i) such as the numbt:r and viability of propa-gules .2) Extrinsie properties of the environment or therecruitment potentinl of the environment (such asavailability of free space for gerrnination).

Pni = Rate of o~t plj,wary productivü)'. whieh is a fune-tion of:1) lntrinsic properties of the algal speeies or functional

group (i) or the "Mass-speeitie rate of production".2) Extrinsic properties of the environment or the"Productivity potemial of Ihe environmem".

Di = Rate of herbivore-induced disturbance. which. as-suming no refuge, is a funclion of:1) lntrinsic properties of the oiga! species 01' fünctic.'Oal

group (i), which involves:Resistance to disturbam.:e (e.g .. due 10 mechanicalproperties sueh as roughness and morphology). anddeterrence of disturbance (e.g .. ehemistry of preyspecies affecting herbivore choice).

2) Ex{nnsic properties of the environmem which werefer to as the: "Distllrbance potential oi the envi-ronmem". This can be measured as:Rate of disturbance (e.g., from herbimres). involv-ing:Disturbance intensity (amount of biomass lost per

event).Disturbance frequency (events per unir rime).

We define the "productivity potemial of an en\ironmem"as being detennined by the extrinsie factors that ser anupper limir to the net primary producrivity possible inthat environment. A reduction in productivity potemial ofthe environment by this definiríon equals an increase instress (sensu Grime 1981). In rhe marine realm. factorsintlueneing rhe productivity potential include lighr. nutrí-ems, desiccation. freezing, and water motion (\\hich con-trols both nutrient and gas exchange: e.g., Blinks 1955.Leigh et al. 1987). Thus the productivity potential on hardsubstrata decreases in a logarithmic fashion from maxi-mum levels in lhe lower intenidal and shallo\\ subtidallOne toward minimal levels in the upper reaches of theintertidal lOne and the lower limits of the photic lOne.Evidence for these gradients have been published from avariety of locations (Nicotri 1977, Raffnelli 1979. Round1981, K"eser and Larson 1984, Underwood 1984a, b.Hardwick-Wirman 1985, Bosman et al. 1986. illustratedin Hawkins and Hartnoll 1983, Steneck et al. 1991).

Grime (1981: 39) defines disturbanee to be ··the mech-anisms which limit plant biomass by cnusing its partial 01'

total destruetion·'. Disturbance has two componems: fre-quency and intensity (Reichle er al. 1975, Steneck 1988.Steneck et al. 1991). High Icvels of disturbance result

UNES OF EQUALDISTURBANCE(EQUAL BIOMASSREMOVED)

NO VIABLE STRATEGYFOR PERSISTENCE

LOW

•DISTURBANCE FREQUENCY

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that the productivity and disturbaricé potemials of theenvironment are theoretically independem of residentplam assembiages and tllus may not directly reflect theobserved level of productivity 01' disturbnnce in the sys-temo Independence of structuring environmemal compo-nems from organisms comprising the eommunity is es-sential (e.g., Van del' Steen and Scholten 1985, South-wood 1988) and thus we will earefully detail the imrinsicand extrinsic components of the community and theirenvironment below. At this point we will uevelop thisidea exclusively for herbivore-induced disturbanees. al-though most aspeets apply equallY well ro abiotic disturb-ances.

Functional groupings of algae are based on anatomicaland morphologieal characteristics (Stcneck and Watling1982, Steneek 1988, Fig. 1) that often eorrespond toecological charaeteristies (identified below). Thus theydiffer from guilds (sensu Roar 1973). whieh are basedstrictly on sim!larities in resource utilization. We consideran algal-dominated eornmunity as an assemblage of fune-tional groups. with the abundance of cach group mea-sured by its somatic biomass. Biomass is maintained by adynamic balance between the rates of constructive forcesof recruitment and net primary 01' biomass production andthe destructive force of disturbance. The measurable re-sult of these processes depends on.both imrinsic proper-ties of the organisms and extrinsic properties of the envi-ronment. This relationship can be expressed in biomassunits for any given area as:

478 0110;05 09:.1 119'M)

fmm condilions ranging fmm high frcqucncy. low in-lensilY dislurbances lo low frequency. high intensilY di s-llIrbances (Fig. 2). [1'dislurbance frequency and intensilYare both high. organisms are unlikely lO persist. Ourconcept of dislurbance elaborates on Grime' s (1981) byrecognizing lhal there are agents of disturbance such assea urchins or severe Slorms with lhe pOlentiallo destroyplant biomass. bul which certain planls such as structur-ally robusl, lough or highly elastic ones, can resisl (dis-cussed below). Thus. we speak of lhe "dislurbance pOlen-tial of an environment" as extrinsic to and indeP.endent oflhe residen! algae, and nOle that lhe ••clual amount ofbiomass removed (i.e., lhe "dislurbance") is in part afunclion of intrinsic properties of the plants.

We focus on herbivory as a source of disturbancebecause in m••ny marine systems it is lhe most importanlcause for lhe loss of biomass (e.g .. Lubchenco and Gaines1981). This includes ccnsumption and consequent los sesdue 10 dislodgement (e.g .. Padilla 1987). Herbivory is byno means lhe only fonn of disturbance, bUl it is suffi-cienlly ubiquilouS and important ro be the focal point ofour research. We suggest that physical disturbances (orsenescence) having a frequency ard intensily similar ro.lhose caused by herbivores will have the same impacl onlhe slruclure of algal communities (e.g .. see Kendrick·1991 ).

Study sites and general methodsStudy sites

We studied lhree biogeographically dislinct locations.each of which had preselecled largel habitats which \Verelocated al different siles. Each habital or lOne was quanti-lalively sampled along lransecl Iines where we quantifiedalgal productivilY and lhe biomass of herbivore and algalspecies.

Maine

Subarctic coastal research in lhe \Vestem North Atlanticwas conducled on an exposed rock-Iedge habitat nearPemaquid Point, Maine (44°30' N. 69°32' W) (see Sle-neck 1982 for detailed site description) and a prolecledintertidal habilat near the Darling Marine Center in Wal-pole (43°57'N, 69°35'W). Sampling transects were estab-lished along a depth gradient at seven discrete lOnes (i.e.,high intertidal. + 1.6 m: low intertidal - 0.2 m; and sub-tidal deplhs of 1, 3, lO, 20 and 30 m). Multiple lateraltransects were eSlablished al each deplh lOne. Offshoredeep waler research was conducted at Ammen RockPinnacle (42°52'N, 68°58'W) which is localed 112 kmsouthwest of Boothbay Harbor. Maine (see Yadas andSteneck 1988 for delailed sile descriplion). Sampling allhis sile used small manned submersibles. Scuba divingfor biomass ard productivity sampling al lhe 30 m deplhslation used mixed-gas NITRO X lechniques.

OIKOS 69:3 (1994)

..•••••••••••••• ¡

~¡'ílShillgll'"

Boreal inlertidal research in lhe eastern Norlh Pacilic wasconducled al relalively prOlected siles on San Juan Island(,¡s030'N, 123"IO'W) and at exposed siles on Tatoosh(sland (48°25'N, 124°35'W) in Washington state. On SanJuan Island transects were eSlablished at four lOnesaround lhe island, sampling at very high, high. mid, low,and ver)' low intertidal lOnes (ca> 2, 1.3,0.6, O, and - 0.6m. respectively). Delailed descriptions of loé San JuanIsland sites appear in Dayton (1971): Taloosh Island lran-seClS \Vere established al very high, high. mid and lowintertidal ?011eS (ca > 3~·z.:-1. and O m respectively; seeLeigh et al. 1987 for sile details).

C[/ribbean

Tropical subtidal research \Vas conducted on lhe Carib-bean islands of SI. Croix (Teague Bay reef; 17°46'N,64°3TW and Salt River Canyon 17°48'N, 64°45'W) andJamaica (18°28'N. 77° lTW). Productivity. herbivory andalgal communilY structure were measured al three sitesand nine depth zones dislribuled along the north shore of51. Croix (0-40 m deplhs. site delails in Sleneck 1983a).Seasonal comparisons in the slructure of algal communi-ties were made at a site on the soulh shore of SI. Croix(site delails in Adey and Sleneck 1985). Lón'g-te~ re-search lransects in J••maica \Vere eslablished on the west-em reef of Discovery Bay (site details in Wood!ey et al.1981 l. Replicaled transects \Vere surveyed in 1978. 1982and 1987 al target sites situated in lhe backreef (1 m), andshallow (3 m) and deep (lO m) fol'ereef lOnes.

General methodsPalterns of distribution Glld abll/ldance

.-\t each largel habilat along subtidal sampling lransects,haphazardly lossed quadrats (25 cm x 25 cm) were sam-pled for algal percent cover. canopy height and biomass.Intertidal sampling used 10 x 10 cm quadrals which werealso haphazardly lossed. Herbivores in each quadrat wereidentified. counted. and measured (Iength or tesl diame-ter). Algal biomass was eSlimated using a relatively non-destructive lechnique developed al our study sites in\;laine. The heights of lhe algal cano pies in quadrals weremeasured by repeatedly inserting a ruler or calibratedtloating line 10 lhe substrarurn and measuring the longestfronds. Algal percent cover was visualIy delermined. Allalgae were colIecled wilhin randomly chosen quadrats for10lal biomass and canopy height determinations. The re-gression of algal biomass and algal canopy height issignificant (F ralio = 59.1. 'p' < 0.00 1) for quadrats havinga 100o/c algal cover: y= 13'¡.8+7.76x. Rl=0.53, n=53,where y = dry rnass of algae (g) per meter square andx = canopy height (mm). This relalionship applies acrossspecies so thal only the canopy heighl of algal mass andpercenl cover data were recorded fol' lhe majorily of theintertidal zone biomass estimates al the Maine and Wash-ington sites.

Biomass was measured directly for alI sites in SI. Croix

479

and Jamaica by harvcsting all macroalgac within quad-mts. Algac wcrc lhcn lixcd. drieu and wcighed. Whcrconly diminutive algae were found. substratum samplesapproximately 25 cm x 10 cm in size were taken to thelaboratory. scraped. tixed, and decalcified for both algalcommunity structure and biomass sampling (see Adeyand Steneck 1985 for sampling details). The decalcifiedbiomass samples were filtered onto preweighed milliporefilters. dried and weighed. Ten control filters were han-dled identically except without algal samples to assesshandling effects. Algal community composition was de-termined using the subsampling and point COU!lt tech-nigue of Adey et al. (1981).

Quantifying productivity potential of the

environment

To assay the productivity potential at each target habitat,we lIleasured the rate of dry mass production on hardsubstrata growing under herbivore free conditions. Whenpossible, we recorded light levels and examined the cor-respondence between the two. Commensurability prob-lems among differf'nt biogeographic regions were mini-mized by ranking target habitats from lowest to higheslproductivity pott~ntial within each region.

Maine

Dry mass production wasdetermined from monthly algalbiomass accumulation rates on epoxy putty substrata setin herbivore-free conditions for over ayear. For this.rocks embedded in epoxy putty 'Vere surrounded by I cmlong, 3 mm diameter pegs protruding every 1-2 cm2 toexclude urchin grazing. The subtidal epoxy islands wereplaced on copper sheets to exclude limpels. Monthlyinspection of lhe substrata for urchin and limpet bitemarks indicated that the experiments rem;¡ined herbivorefree for the duration of the experimenr. After monthlybiomass estimates for percem cover and canopy heights.the epoxy putty substrata were scrubbed to a negligiblelevel of remaining biomass from which would sproutnext month's biomass. Sublidal lighl levels for targethabitats were measured using a Licor underwater pho-tometer (model Li 188b, integrating gua~tum meter) witha spherical sensor (Li 905B) during luly at mid-day underclear calm conditions (from Vadas and Steneck 1988) todetermine relative light availability.

Washington

Dry mass production was measured on San Juan Island.based on algal biomass accumulation over two weeks inAugust on epoxy putty under herbivore-free conditions inAugusr. Herbivores were excluded by clearing a striparound each epoxy putty island and paillling it with cop-per based antifouling paint (see Paine 198.+). Biomasswas estimated from canopy heights and percent covers(see aboye). The outer-coast site (Tatoosh Island) wasassumed to have higher productivity pOlential per lOne

480

bccausc uf lhc slrongcr wavc aCliun tLeigh el al. 1987)and the decrcascd desiccalion slress lhere (due to fog.spray. and lhe timing of low lides: Dayton 1971 l.

Sto Croix

Dry mass production was based on lhe rate of change inalgal biol11ass growing on coral plales under herbivorefree conditions (Steneck 1983a). For this, six scraped andsix unscraped plates were suspended al each target depthin lhe waler column away from the reef; after six days,new alga1 biomass was rescraped and taken as an in-dicalion 01' dry l11¡\.SsprodJJcti&lt. A r/¡alassia bioassay(Hay 1981 a) and visual 5-min watch~s revealed no signsof grazing (Steneck 1983a). Producti\·ity rales \Vere alsodetermined in situ using a portable respirom~ter for peri-ods of 24 h at each sile. Each 24-h run simullaneouslyrecorded changes in oxygen concenlration among lhreereplicale unscraped coral plate samples. The chambertops \Vere composed of optically pure quartz glass. Whilerecording oxygen concentrations, Iighl intensilY measure-mems \Vere taken with a Licor light meler and ~very t\Vohours lhe respiromeler was tlushed (see Porter 1980/.

Quantifying disturbance potential of the

environment

The dislurbance pOlential of lhe environmeTJl invol\'esbOlh the intensity and [reguency of disturbance. Herb-ivore-induced disturbance freguency \Vas estimated cif-feremly for invertebrates than for fishes. A\·erage in-ver.:ebrate herbivore biomass per unil ;lrca for eJ.<:h largelhabilal \Vas estimated from guadrat data by applyingindividual body size to biomass regressions C\¡leng~1972) and relating lhat to populalion densily dala. Dis-turbance fr~quency for herbivorous fishes was deter-mined cinematically by recording bile rales (Sleneck1983a). Grazing imensilY was eslÍmated by cat~gorizingherbivores by feeding abilily from published studiesbased on impact per bite (i.e .. excavaling pOlentials) ofgastropods. molluscs, urchins and grazing fish groups(methods 01'Sleneck 1982, 1983a, b, 1988, 1990. Steneckel al. 1991 l. Grazing intensilÍes by invertebral~ groupsare comparable among biogeographic lOnes (Steneck1983b. 1990). Most estimates of frequency (i.e .. herb-ivore biomass) and imensilY (feeding capability) are cor-relaled among lOnes for each region. facililating lhe rank-ing of dislurbance potentials of targel habitals (see R~-sults ).

Al Maine and Washinglon, three leveis of in\·ertebraleherbivore-i'nauced disturbance intensity were id~ntif¡edbased on impact per bite. They were 1) shallow-grazingmolluscs such as litlorinids, creating the 10west-intensilYdisturbances, 2) deep-grazing molluscs such as limpels.and 3) lhe intense-grazing urchins. Based on body sizcand population density, invertebrate herbivore biomasse,< 10 g {drYI/m2, ID lO 100 g (dry)/m' and > 100 g (dry)/m:\Vere ranked as low, mid, and high dislurbance potemial

OIKOS 6q:~ 119'i~1

A eMass-specific Productivity Canopy Height

12A o

10 o E so.s 40-" 8 +~~ + +

6 II +o lJ 30¡¡¡

~ 6 lE ---6-..° J:20'tl o a >-

"" + A c.."- 4 0~ --".-- c- z 10E I o + é <:

2 8~+

uo 0_o 2 3 4

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oi i

o 2 3 4 5 6 7 E 300

ALGAL RJNcnONAL GROUPS .s Washingtonf- 32 SpeciesJ: 200lJ

B ¡¡¡

Thallus longevityJ:>- 100c..

100 ..• oa z<:

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'"e 10 8 60wlJ " " Caribbean<: 5 50

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O 2 3 4 5 6 7u

O O 2 3 4 5 6 7ALGAL RJNCTIONAL GROUPSALGAL FUNCTIONAL GROUPS

Fig. 3A. Mass-specific productivity of algae from southem California (O Linier and Arnold 1982 l. the Caribbean (j. Littler et al.1983b, X Carpenter 1986). and Hawaii ( + Doty 1971). Average productivity values for well studied functional groups arerepresented by horizontal lines. Numbers for algal functional groups correspond to the numbers in Fig. l. :-.iote that AG :2 (turt)production may be low due to inadequate agitation (see Carpenter 1985). B. Thallus longevity. Poims represe m thallus longevity of27 species based on 25 published studies (AppendixJ. Average longevity values for well studied functional groups are represented byhorizomallines. C. Canopy heights measured in the field for dominant species in Maine. Washington. and the Caribbean (DiscoveryBay, Jamaica). Lines envelop the maximum canopy heights recorded for each algal functional group and poims represent averagecanopy heights per species. Error bars represem standard deviation per species.

respeclively. Only habitats with significanl urchin abun-dance (the invertebrate herbivore that grazes with thehighest intensity) were scored as having a high disturb-ance potentia1.

Our quadrat data for SI. Croix were taken in 1982.before the Diadema antillarum mass mortality in 1983.and thus urchins were still a significant herbivore. Due tothe addition of grazing fishes at tropical sites. the rankingof herbivore-induced disturbance in SI. Croix differedfrom that of Washington or Maine. Just as ¡nvertebrareswere separated according to their intrinsic differences ingrazing intensity, so too were fish groups subdivided.Based on inlensity and impact, herbivorous fishes weresubdivided imo: 1) non-denuding (no net removal ofa1gae from the substratum, Hixon and Brostoff [983). 2)denuding and 3) excavating (Hatcher 1983. Steneck1983a, 1988). For our ranking, only bites from denudingand excavating fishes were used since they are unequiv-

ocally agents of disturbance to algae. Fish grazing fre-quency was measured as bite rates and was determinedfroro visual observations and lime-lapse movies taken in198 i and 1982 (see Steneck 1983a for methods). In-vertebrate herbivores at tropical sites were measuredidemically to those of non-tropical sites but zones thatincluded bite-rates from tishes in addition to significantinvertebrate grazing achieve the disturbance potentialranking of "very high".

ResultsIntrinsic properties oC organisms:characteristics oC Cunctional groups

Algal morphology and anatomy (e.g., Fig. 1) correspondto intrinsic properties such as mass-specitic productivity

OIKOS 69:3 (1994) 481

~,. SWh19t-$42 ••.. $(,4 . ti

Tabk 1. Potcnlial impact 01 herbivore laxa on funclillnal groupsof algae (number rcfcrenccs to fUl1ctional groups identilied inFig. I l. COllllnunily Slructure is most affected by the groups thalcomrnol1ly denude algae. X = Commonly denudes group. X =COOlmol1ly consumes group, - = Occasionally consumes group.Blan!.: = Rarely or never consumes group.

Herbi"llre talla Algal functional groups

2 3 4 5 6 7

Poi ychaela I X X XMalacostraca~ X X XGastropoda

RhipidoglossaJ X X X'Taenioglossa" X X XDoco!!lossa; X X X X

Polyplacophora6 X X X X X X XEchinoida1 X X X X X X XPercifonnes

Low intensity' X X XHigh intensity· X X X X X X X

% groups <.:ommonly 100 67 33 22 22 11 11denuding

I Dav 1967. Fauchald and Jumars 1979*, Hartman 1968. Woo-din' 1977. Kohn and White 1977. Steneck 1983b

~ Brawley and Adey 1981. Carpenter 1986. Howard 1982. Zim-merman et al. 1979. Hicks 1986, Steneck 1983a.b. Brawlevand Fei 1987 '

J Graharn 1955"'. Steneck and Watling 1982*, Steneck 1983a.b,Ward 1966. Ankel 1936

• Lubchenco 1978, Steneck and Wat1ing 1982*. Sleneck1983a.b. Graham 1955

; Niculri 1977. Slen~ck and Walling 1982. Sleneck 1932.Branch and Branch 1980. Walker 1972. Fletcher 1987

6 Sleneck and Watlin!! 1982*. Sleneck 1983a.b. Graham 1955.Delhier and Duggins 1984

1 Carpenter 1981. 1986. Steneck 1983a.b. Lawrence 1975*.Flelcher 1987

& (c.g .. Pomacentridae. Acanlhuridae) Jones 1968, Hillon andBroslOtT 1983. Vine 1974. Russ 1987. Monlgomery 1980.Brawlev and Adev 1977. Sleneck 1983a.b. Lewis 1985

9 (e.!! .. S'caridae) Hatcher 1981. Russ 1984. Steneck 1983a.b.Le~vis 1985

*Review articles.

(Fig. 3A), thallus longevity (Fig. 3B, Appendix) andcanopy height (Fig. 3C). Canopy height increases withthallus complexity (i.e .. tissue differenti'ation into cortexand medulla. Fig. 1) which al so correlates with planebiomass (see Melhods aboye). In general, me thalli oflarger erect algae are longer-lived and slower-growingthan thalli of small filamentous and microalgal forms.The progressively enlarged cortex with thick cell walls(algal groups "AG" 4-5) and calcification (AG 6 andsorne AG 7) appear to make macroalgae more resistant 10physical and biological disturbances (Steneck and Wat-ling 1982, Linier et al. 1983a. Pennings and Paul 1992).As a result of the size. growth and longevity character-istics. larger forms (see Fig. 3 for AG 4-6) are bener atmonopolizing light resources than smaller or low-canopyforms (AG 1,2 and 7: reviewed in Carpenter 1990). Evi-dence for mis is seen in studies of algal succession (e.g.

482

Paine IlJ77. Elm:rson anJ Zedlcr IlJ7S. Murray and Lil-tlcr 1978. and Sousa el al. 198 1). and in cxperirnentswhere lhe rernoval of largcr macrophYles allows lhegrowth of smaller canopy-forming algal groups (e.g ..Dayton 1975. Sousa 1979, Lubchcnco 1980, So usa et al.1981, Ojeda and Santclices 1984. ano Duggins and Deth-ier 1985) or wherc removal of herbi,w~s results in dom-inance of larger forms (Paine and Vadas 1969a, Sam-marco et al. 1974, Lewis 1986). The close correspond-ence between functional groupings and ecologicalcharacterislics is explored further below."" Fuat:tionally- different herbivore groups can differen-tiany affect algal groups. [ntrinsic properties of herb-ivores such as bite penetration deplhs into calcareouscrustose algJe have been measured JS indicating herb-ivore-induced disturbance intensity (e.g .. Steneck 1983b.1990. Sleneck et al. 1991). Table I shows herbivore taxain terms of lheir capacity 10 consume andlar denudevarious JIgal funcl!onal groups. Many grazers entirelyremove microulgae. filame:ltous. Jnd foliose fonns, bUlfewer can denude larger macroalgae and even fewer re-move crusts (particularly coralline cruslS). Larger expan-sive and calcified algal forms also appear to suffer lesssecondary lissue 10S5 (e.g .. 10 wave": Jction followinghemivory) crian do simpler ••forms (Padilla 1987) and thusareless likely to.bé denuded. Comll1unity-level impact ofdifferent herbivore groups appears la fol!ow denudingcapacity. For example. scarids (parrolfishcs), which havethe deepest bite-depm penetration into calcareous algae.can remove al! funcuonal groups of algae. Among lhe¡nvertebrates. grazing intensity ranges from echinoids. todeep grazing gastropods and finally tI) shallow grazinggastropods and olher low intensity grazers such as poly-chaeles (Steneck 1983b), and their reported impact fol-lows this panero (Table 1).

Extrinsic properties oCthe environment

The ranking of productivily potential of the en\'ironmentin the well mixed. subtidal environments of Maine andSI. Croix corresponded directly to recorded light levels(Table 2). [n Maine. lhe monthly rale of algal biomassproduclion was highly correlated wilh light intensity (Ta-ble 2A: r = 0.98, n = 7 stations). A similar panero wasfound on a wave-exposed forereef lransect in SI. Croix.grading from mean low water to a deplh of nearly 40 m(Table 2B. Steneck 1983a. Carpemer 1985a). Dry massproductivity under herbivore free conditions at four ca-nyon wal! habilats correlared wim light (r = 0.89. n = 4)and oxygen production recorded using a respirometer(r = 0.94). Oxygen productivity correlated (r = 0.86, n = 8)with light over the entire oepth transect from mean lowwater to 40 m (Table 2B).

[ntertidal environments (in Maine and Washington)from mean lower low water to lhe upper reaches of lheinterridal zone encompass another gradient of progressiv-ely reduced annual produclivity pOlential (Tables lA and

OIKOS 6'1:3 (19941

Tabk 2A. Ranking producti"ily pOlenrial nI' lhe cnvironmcnl at target habilats in Maine. Habitals are arranged from highcsl lOne lO

grealesl depth. Productivity "ariance expressed as slandard error.

Maine

Targel habitals Production Number Light Productivity(sub- and intertidal) g (dry )f1n~/yr 01' salnpks (1L1n01/m~/s) polential

High intertidal zone (+1.6 In) 0.98 (±O.9) 6 ND LOWLow intertidal zonc (-0.2 m) 5.1 (±1.6) 9 ND MIOCoastal -1 In depth 152.3 (±17.5) 6 900 HIGHCoastal -3 In deplh 56.0 (±28.6) 6 450 HIGHCoastal -10 In depth 1.2 (±O.03) 6 90 MIOCoaslal -20 In deplh 0.2 (±O.2) 6 9 LOWCoaslal -30 m deplh 0.7 (±O.OI) 6 ~""'" I LOWOffshore -30 m deplh 14.0 (±O.9) ~ 20 MIOOffshore -45 m deplh O (±O) ~ 7 LOW

Table 28. Ranking producti"ity polentia1 01' the environment at target habilats in SI. Croix. Dry mas s productívily variance isexpressed as standard error (n = 6).

SI. Croix

Targel habilals(sub- and intertidall

Algal ridge at ML\VA(ga! ridge 0.5 InBaclaeef 1 mForereef 1.5 mForereef 5 InForereef 10mCanvon wall 10 InCanvon waH 20 mCanyon \Vall 30 mCanyon \VaH 40 m

Productiong (dry )/m~/d

NDNDND-

NDNDND

3.0 (±0.28)1.35 (±0.25)093 (+1.1)0.79 (±1.8)

ProduclionILgO)cm~1h

2215 (±6OO)1255 (±502)553 (±393.)940 (±269)756 (±159)536 (±79)ND

561 (±39)387 (±86)213 (±42)

Lighl(moITm~/d)

43ND28282317

ND1163

No. 01' Produclivilysamples' pOlential

3 HIGH3 HIGH3 MIO3 HIGH3 MIO3 MIO

ND MIO3 MIO3 LOW:3 LOW

1 Number 01' coral plales useJ in res¡Jirometer.

Table 2C. Ranking producli"ily pOlenrial of the environmenr al largel habílats in Washinglon State bascd on height in the intertidalzone (e.g .. "very high" to ""ery 10w") and degree 01' exposure (see lext). AH productivity measuremenrs \Vere done underherbi vore-free condilions. Producli"¡ry variance expressed as slandard deviatíon.

Washington

Targel habilars(intertidal)

SJI' Verv highTI Very -highSJI HighTI HighSJI \<IidTI MidSJI Low (few herblTI Low (herb removed)SJI Low (Wilh herb)TI Low (with molluscs)TI Low (Wilh urchins)SJI Very low (few herb)SJI Very low (\Vilh herb)

Productiong (dry)/In~/mo

7.2 (±15.6)

97.8 (:!:92.4)

464.0 (:!:227.O)

Number01' samples

10

20

10

ProductivitypOlenlial

V. LOWV. LOW

LOWLOWMIOMIOHIGHHIGHHIGHHIGHHIGHHIGHHIGH

*SJI = San Juan Island. TI = Tatoosh [sland.

OIKOS 69:3 (I'1'l4) 483

__ o

Tabk ~A. Ranking oisturbance potemial in Mainc baseo on gra/.ing frc4ucncy (as intlicated by hcrbivore biomass. sce tcxtlhcrbivorc hiomass and grazing inten~ity Iincreasing left to right from shalll1w gral.ing molluscs to un:hins).

Maine

Target habitats Shalluw Oeep Urchins.1 Total No. uf Oisturbancegrazing grazing herbivore samples potential

molluscs' molluscs! biomass

+ 1.6 In Intertidal 1.2 (±6.I)· O O 1.2 T2~ LOWO m Intertidal 56.9 (± 17.8) O O 56.9 83 MIOCoastal I In oepth O 0.02 (±O.02) O" 0.02 34 LOWCoastal 3 m depth O 0.2 (±0.2) 229.2 (±36) 229.4 39 HIGHCoastal 10 m depth O 0.2 (±0.02) 1890 (±13.73\ .- 189.2 ... 76 HIGHCoastal 20 m depth O 0.9 (±0.4) 9.5 (=5.3) 10.4 30 MIOCoastal 30 m depth O O O O 33 LOWOffshore 30 m depth' O O' O O >30 dives· LOWOffshore 45 m depth O O O O > 10 dives'o LOW

, Biomass (g(dry)/m!) ofherbivores used throughoul. Shallow grazing molluscs = Li[(orina lirtorea.! TecllIra lesllIdinalis. TOllicellaI'lIber. T. marmorea.·\ Srrongy/ocelllroflls droebachiensis. • Except for this value (standard deviation\ all variances are expressed asstandard error because they are average s 01' a population 01' means. ; n = number 01' m! quadrats. • Urchins having a biomass of56.3(±8.75) (g(dry)/m1) were found in crevices only. This analysis involves plants growing on the upper surfaces 01' rhe boulderswhere the •.e are no urchins. ' The offshore site is Ammen Rock Pinnacle (104 km east 01' Boothb3y H3rbor. ME. ~ee Vadas andSteneck 1988).' Arare « 1/l0 m!) limpet species is the sol e herbivore. • Number 01' scuba dives. 'o Number 01' submersible dives byseveral observers.

Tab1e 3B. Ranking disturbance potemial in Washington state (identical rnethod 10 Table 3A)~' Tar~e1 habttats are arranged fromhighest to lowest elevations in the intertidal zone for our stations on San Juan (SJI) and TatOosh (TI) Islands in Washington state.

Washington

Target habitats Shallow Oeep Urchins' Total No. Oisturoancegrazing grazing herbivore samples pOtemial

molluscs' mollucs! biomass

SJI Very high 2.9 \:!:~.O) 3.4 (±5.~) O 6.3 10 lO\\'TI Very high 8.0 1=~.9) O O 8.0 5 LOWSJI High 2.71:=2.8) 4.3 (±8.3) O 7.0 18 LOWTI High 3.9 (:=3..+) 7.1 (±II.4) O 11.0 14 lO\\'S1I Mid 0.5,=0.1) 4.4 (±6.4) O 4.9 23 LOWSJI Low (few herb) 0.1 1=0.2) l.l O 1.2 24 LO\\'SJI Very Iow (few herb) O 1.2 O 1.2 16 LO\VTI Mid 0.51:=0.1) 42.1 (±4l.l) O 42.6 13 MIOTI Low (herb removed) O 0.4 O 0.4 5 LO\~'S1I Low (with herb) O 42. 1 (±~8.6) O 42.1 7 :VilOS1I Very low (with herb) O 76.8 (±86.3) O 768 11 :VIlOTI Low (with molluscs) 0.2 1=0.9) 40.3 (±56.6) O 40.5 13 \110TI Low (with urchins) O 3.7· (±7.3) 2340 (± 1605); 2344 8 HIGH

, Summed biomass (g(dry)/m2) 01' Litrorilla spp .. Onchidella sp., Siphonaria sp.: ! Lotria pella. TeCIUra SClllUm. TOllicella lineara.Kar/J(Irilla rllllicara; 3 Srrongy/ocenrrotlls pll}pllrarus; • Tonicella lilleara; ; Urchin biomass estimations were based on test diameterto dry mass regression (calculated for S. droebachiensis) of: y = 0.2827 ·x!·O). r = 0.94, n = 30).

C respectively); here, however, the factor most limitingalgal productivity is probably desiccation rather thanlight or wave action (Castenholz 1961. Dayton 1971,Seapy and linier 1982, Horn et al. 1983. Cubit 1984).Measured productivity rates under herbivore-free envi-ronments in Washington (Table 2C) show !he expectedinverse relationship between rates of productivity andelevational height in the intertidal zane.

Ranking disturbance potential ::ttnong target habitatswithin each biogeographic location involved only theabundance and feeding capability of herbivore groups,not their preferences. In most cases. tOlal biomass and

484

abundance of most intense herbivores correspond (Tables3A-C). In Maine, the 3 and 10 m depth zones had boththe greatest tOlal herbivore biomass and dominance byurchins, which are capable of the most intensive grazing(i.e .. they are capable of taking large and relatively deepbites into the most resistan! algae) and thus were rankedas having a high disturbance potential. At the O m in-tertidal habita!. the dominant herbivore is Littorirlll litro-

rea which is a low-intensity agent of disturbance (i.e ..does not graze deeply, Steneck 1990) but is found in highnumbers. This habitat is ranked identically to the 20 mhabitat where herbivore biomass is lower but feeding

OIKOS 69:3 (19941

Table 3C. Ranking dislurbanee potemial in S!. Croix ba,ed on invenebrale herbivores (identieal to Tahles 3A and B) and tish grazing(bite rate) arranged by illl:reasíng grazing imensily fmm lefl \O righl (no shallow gra/.ing molluscs \Vere found) in larget habitatsarranged from shallowesl 10 deepesl (se:: test).

SI. Croix

Targel Deep grazing Urehins' Bile rale Number Sample Dislurbaneehabítals molluscsl tishes" quadrats" size5 polential

Algal ridge O" m O O 20 3 LOWAlgal ridge 0.5 m O 3R.3 (±3. 7 ¡' 313 (±311) 10 3 MIOBaekreef" ! m O 144.4 (± 11.6) 896 (±896) 31 3 HIGHForereef 1.5 m 0.03 (±D.O 1) 137.6 (±7,,-+) 2823 (±85()) 13 3 V. HIGHForereef 5 m 0.02 (±D.O:!) • 12 L:r (±4.5) l.563 (± 1381) 20 3 V. HIGHForereef 10m O st (±5.-+) 409 (±371) 21 3 MIOCanyon wall· 10 m O 4.2 (± l.:!) 109 (±51)'0 19 ~ MIOI

Canyon wall 20 m O 20.5 (± 1.68) 294 (±975) 30 11 MIOCanyon wall 30 m O 1.01±0.32) 235 (±621) 20 7 MIOCanyon wall 40 m O O O 20 8 LOWCanyon wall" 1O m O O O O 3 LOWCanyon wall 20 m O O O O 3 LOWCanyon wall 30 m O O O O 3 LOWCanyon wall -+0 m O O O O 3 LOW

I Biomass (g(dry)/m') of Acmaeú /eueop/el/ra. ' Biomass igtdry)/m') af Diadema anrillartll/1 (data from 1982), Eehillometra/ueumer (primarily reslricleJ to burrows) ..• Bite rates (biles/m:/h) for denuding fishes (Microspat/lOdoll elrl}·sunls. OphiobJelllliusat/anrieus. Aeall1lrlirus blllriallus. Aealll/lllrus coeru/eus) and exeavaling fishes (Scams croieellsis. Sparisoma clrrysopterum.Sparisoma viride) (Steneek 1983a. bl. Only forereef at 1.5 m had measurable searid grazing. ' For urchins and molluses only .

. ' Visual 5-min eounts 1981. 1982, lime lapse movies 1982 I\'isual eoums 1982 anly Ca!\'yOSl wall statíons), 6 MLW = Mean LowWaler for spring tides, 7 Variance cxpressed as standard error of rhe mean. g Reef si tes artTeague Bay Reef. • Can yo n sites are SaltRiver Canyon . 10Varianee as standard Je\ iatíon because lh'is value is nOl derived from a populatíon of means. " Plales weresuspended from raeks away from ean~un wall al identieal deplhs as Canyon Wall stalÍons. Herbivory \Vas never observed at any ofthese racks. They are lisled as "0 HERB." in Fig. 4C.

IOGH

,...J--<¡:Z[..IJ¡-

><JOOp..,

>-¡-

:>¡:U:Jel LOW

O¡::,::p..,

A. MAINE

,1m·'mSUanOAl

COASTAL SUlTlDAlCOASTAL

':"m LOW -1O",

SUITIDAL u-.lF.R.TIOAi. SU1noALOF'PSHORE COASTAL

':10m ·"mCOASTAL COASTAl

HICHfN'iU.nOAL

·<SmOFPSHORE

KlCH

lOW

V.LOW

B. WASHINGTON

<XJ'TiA CeA:) ¡

1~=AL ~;~~~ALlOWf:'.."'TD.m .••:.NO n:aarvORES Q\Il y MOlLUSCS URCHIN lONEmLowJ-Wt.~'Pd)1 rn Low04olluIOII :n lowll!rdI",""

PRO:'ECTID ro",,!, nort:crm OOASTVF:RYlOW ~ "'i'U.TtDAL vay l.QlN' tsTERTIDAl

HE.RSfVottES RA.U Q\IlY MOUUSCi

(SIl \'.LowcF-i-iont:lLll 1$ V.LOW CMolbaaII

PROT:c:m CDASi P1lOTEl."7EDCOASILOW 1~i'D.r.:oAl. lOW t~1DT1DALHERBl\'~ lAJlE ONLY MOlLUSCS(SfILow\f~Iicr.-s.1 ISI1l.ow~l/

~c:mroAST WTDCOASTMIO ~1DTtI>Al MIO DntltT1DALHER.8['l:O:u.s R.A.U 0Nt y MOU.U!lCSts¡1'M.d1 m ••••1

C'llJl"EJ::COAST

tDCH l"lT'EJ:nDALHERal\'OR~ JAUmH..pl

PIOTECTED COA5i"HlGH 1.""'T!llltDALHERBI"'ORIS JAlEISIIHi~1

OUTD co.~!''"BYHJCH 1:'IoiD.nDAlmV.HI!-.,1

rROITC!1D COASI'VERY HlCH 1:\~r.nAl ..tsI1 V.HJpl -

HICH

MIO

LOW

C. SToCRO¡X

ALeA!. ALCAL SK.",UOwiUOCE RlOCE lOlWlE.EI'~lW O.im I.'m

10M FOWtOEf SACXiEEf lOlWlE.EI'OHaR. 10m 1m lm"'CX

CANYON

WAlL10m

"" CANYOSO H'ERI. WALL

"'CX 31m

.,~ CANYONO I-GRI. WALL"'CX lOm

CAI'o"YO,WALL<1m...•

•DISTURBANCE POTENTIAL

•DISTURBANCE POTENTIAL

LOW HICH LO'"

•D1STURBANCE POTENTIAL

lOW MIO HlCH V. HJGH

Fig. -+.Target habitals arranged aeeording 10 produelivilY and dislUrbanee potemials (based un data in Tables 1 and 2, respeetively).A) Maine. Nole thal offshore sites are more produelive al ;J gi\'en depth than eoastal siles beeause of grealer water elarity (Vadas andSteneek (988). B) Washinglon Slare. Abbn!viarions used in Tables lB and 2B are in braekets. Outer euast siles were assumed lO havehigher productivily potential per zone because of lhe slronger ",ave aClion and lhe deereased desiecation stress there (due to fog.spray. and lhe timing of low tides). C) SI. Croix.

" '

OIKOS 69:3 (1994) 485

.-----.-

MAINE

DISTURBAl'KE POTENTIAL

Hí.h•

Mid

WASHINGTON

Low

B)

o

1500

Low Mid '1iShD1STURBANCE POTENTIAL

o

A)

Hígh•

D1STURBANCE POTENTIAL

D) GENERAL MODEL

v:v:«¿e¡;;

A~~o~A~=~I:~;=S/AG 6 ~ AllTIClJL<rw CAl.C1F1ED

AG ~ CJ CORTICAnD MA'.:ROPHYrES

AG J alIIJ FOLXlSE ALGAE

AG 1 e::zJ Fu.M.ENrOUS A1.GAE.

AJ:j I c:J Mk.:'RtJALGA5

AG 7 _ CRUSTOSE ALGAS

Hígh V-':,gh

DISTURBANCE POTENTIAL

STo CROIX

o

C)

Fig. 5. Model of algal community struclure at a functional group level based on environmenlal structuring parameters of disturbanceand productivity potentials. Biomass data werc collected for A) Maine. B) S!. Croix. C) Washington in large[ habilJtS (Fig. 4). AIIbiomass data were galhered at the species level and pooled imo functional groups (see lexll. D) Represems an ideal.ized modelderived from patterns in A-e. Algal groups are arranged according to increasing canopy height with the largesl forms comprising theupper segmems of the stacked histograms. "ND" indicates no data.

capabilities are greater (i.e .. urchins vs molluscan coun-terpart; Steneck 1990). Similar analysis in Washington(Table 38) of shallow and deep grazing mOlluscs clearlyseparates the low herbivore biomass habilats dominatedby low intensity grazers from thos~ .paving a higherbiomass of more intense grazers. Th~ highest disturbancepotential of the habitats w~ studied in Washington is inthe zone dominated by sea urchins on Tatoosh {sland.There, urchins are highly abundant, large. and capable ofgrazing deeply into al! algal groups.

At our tropical sites, integrating the dislurbance poten-tial from vertebrate and invertebrate herbivores is rela-tively easy because urchin abundance and bite rates fromfishes are directly correlated over the target habitats (Ta-ble 3C, r=0.84.n= 10, P=0.003). The lowest leveIs ofherbivory were at the O m algal ridge site and the 40 mcanyon wall sile. whereas both were ma.ximal at the twoshallow forereef sites at 1.5 and 5 m water depth. Allhabitats with un abundance of urchins (i.e .. biomass > 100g/m2) were categorized as ~ilher high or very high in

disturbance potential depending upon the herbivore dis-turbance attribUlable 10 fishes. The sites ha\"ing intemle-diate invertebrate herbivore biomass al so had intermedi-ate le veIs of fish grazing (0.5 m algal ridge, 10-30 mcanyon wall) and lhus were categorized as having anintermediate ("mid

OO

) disturbance potentia!.Fig. 4 (A-C) summarizes the extrinsic components of

the environment as ranked aboye for each ol' the surveyedhabitats at each of [he geographic regions. Productivitypotemial is summarized from Tables :2A-C. and disturboance potential from Tables 3A-C.

Patterns oC algal cornrnunity structure

AIgal assemblages in each region were compared fortarget habitats (Figs 4A-C). Data on algal biomasseswere collected al the species leve!, then combined intofunctional groups and plotted on the appropriate coor-dinate of th~ dislurbance/productivity grid (Figs SA-C).

486 OIKOS 69:3 (1994)

4 Y. ti .C • e .;;a•..j.Si~ _+

Fi!.!.6. Seasonal stabilitv ofth~ 10 most abundant aí"als¡xcies (A) and function~lgroups (B) on a forereef 01'SI. Croi" (reanalysis 01' datain Adey el al. 1981).Differences in the lotalpercenl represented amongseasons for species (A) andfunclional groups (B)resulled from lhe differenlproponions 01' unidentifiablecomponenls when sampleswere analyzed al species vsfunclional group levels.

A

STo CROIX FOREREEF

WINTER SPRING SUMMER FALl.

SEASONS

SPEcrES

• PoIysiphonill SphUrDCllrpll

• Sphacslan. $p.• Hsrposiphonill SflCUndll~ Ostreobrium sp.O Po/ysiphonlll subtilissima

ID PeyssonMlia $p.

El Tlleniomll macrourum

!!l1 Gelidium pusiUum[4 Lophosiphonlll crlstata

O Ce'lImi!Jm niren,

Wl:-JTER SPRI:"C SUMMER FALL

SEASONS

FUNCTIONAL GROUPSANO ASSEMBLAGES

• AG7 CRUSTOSE ALGAE

iI AG 1 TURF ALGAEEl AG2

~ AG4 l'{.Aqq,ALGAEO AG6 .•

The combined biomass of aH species within each I"unc-tional group was plotted as stacked histograms startingwith plants having no canopy such as crustose algae (AG7) or minute canopies as among the micro· and til-amentous algal fonns (AG I and 2), to the largest canopyfonning groups such as the leathery macrophYles. whichinelude kelp (AG S).

In Maine (Fig. SAl, algal biomass and functional groupdiversity was lowest in habitats having the lowest pro-ductivity potentia! or híghest disturbance potential.Where productivity potential was highest and di,lUrb,lIlcepotentia! lowest, alga! biomass and functional group dí-versity were highest, and the community was dominatedby large leathery macrophytes (e.g., the kelp Luminaria

/ongicruris) and corticated macrophytes (e.g .. Chondrus

crispus and Mastocarpus ste//atus ). Crustose algae dOI11-inated zones having the highest disturbance potentialwhere productivity potential was also high. and zoneshaving the lowest productivity potential where dislUrb-ance potential was also low. The dominant cru,W,e algaewhere both environmental parameters were high ineludethe calcified coralline algal species: Lirhor/l(l/llIIiol/ g/lI'

cia/e. C/arhromorphum circumscripfUm ano Phm/lllO-

/ithan /aevigatum, whereas species dominating whcre

OIKOS 69:3 (19')4)

..•.R4'f;;i4lP@! 4

both were lo\\' \Vere the coralline Leptophyrum /aeve andlhe less abundant t1eshy red algal crust Peyssonne/ia

rosenl'ingii in subtidal and Verrucaria spp. in the higherint~rtidal zon~s" Due to obvious trophic limitations, nohabitat has been found in which the herbivore-induceddislurbance potential is high and produclivity potentiallo\\'.

In Washington (Fig. SB), biomass and functional groupdi,ersity agaín were greatest where disturbance potential\\as lowest ano productivity potential highest. There,karhery macroalgae (e.g., Hedúphy//um sessi/e, FuCl/S

gardneri and corticated macrophytes (e.g., Mastocarpus

¡JlIpi!larus. lridaea comucopiae and many other red al-gae) dominated the substrata. At target habitats havingthe highest proouctivity and disturbance potentials, crus-tose algae dominare (predominantly coralline crusts suchas Lit/1Or/wllinion phymarodeum and Pseudo/ilhophy/lum

\I"hidheyense). Wh~re both parameters were low. non-cakified ~ncrusting algae dorninate (e.g .• lichens and"P~trocelis"). Where the two proposed structuring param-elers were al il1lerrnediate levels. we found intennediate[e'"els 01" tOlal algal biomass and slightly reduced func-¡jonal group oi\'~rsity.

In SI. Croix (Fig. SC), algal bíomass and functional

487

.-----

Tahl<:~. Slabilily of n:ef-Jwelling algal communilies al Discovcry l3ay. Jalnai,':l fmm I97X to I':IX7. NOle small change follu",ingHurricane Alkn (1979) versus large chan!!e following mass mortalilv in IJi'id"IIICl u/ltil/unllII (I':IX3). A\!!ae are eombined inwfllnc¡jon:ti grollps and abundances ¡'¡"reexpre~,ed as ave'i-age decalcilicJbiuma;; Ig (dry)/m!). n = number Il(mcler square qlladrats.Cllmmllnily dominanl (i.e .. > 50% uf biomas~) in each zune al each timc i" printed in boldface.

Backreef (1 m) 1978 5.0. n 1982 5.0. n 1987 5.0. n

Herbi\'üreDiCldt!/I/{/ 1lI1til/arlll/l (no.lm!) 3.1 5.3 35 3A 0.03 22 0.4 1.2 37

Algal groupsAlgal [mf (AG 1-2) 9.8 4.9 27 7.0 ~ 14 25.7 13.1 21Macroalgae (AG 4-6) 233.4 10 27 259.0 3~A 14 265.1 66.7 21

CruslOse corallines (AG 7) O O 27 15.2 2.8 14 14.1 2.09 5Sum algal biomass 243.2 281.2 304.9

Shallow forereef (3 m) 1978 5.0. n 1982 5.0. n 1987 5.0. n

Herbí\'oreDiadellla llll/il/arum (no.lml) 8.1 0.7 33 9.1 1.6 25 0.4 0.9 6ó

Algal groupsAlgal [ur!' (AG 1-2) 10.5 l.3 33 25.6 ~.l 3 13.4 9.8 12Macroalgae (AG -l-6) O O 33 O O 3 46.3 20 12

CruslCse coral!ines (AG 7) 41.7 0.8 33 58.9 5.1 3 11.9 2 12Sum algal biomass 52.2 84.5 71.6

Deep forereef (10m) 1978 5.0. n 1982 SO n 1987 5.0. n

Herbi\'oreDiadpllia amil/arulll (no.lm!) \&.0 5.5 40 13.6 .SA 21 Q O 28

Algal groupsAlgal {ur!' \AG 1-2) 35.6 3.\ 10 49.9 280 3 11.3 2.4 30Macroalgae (AG 4-6) 2.-l 0.2 10 1.8 0.1 3 400.6 4.4 ."0

CruslOse corallínes (AG 7) 26.2 2.6 10 29A 5.1 3 0.2 0.2 30Sum algal bíomass 64.2 81.1 4\2.1

group diversity were greatest by far where disturbancepotemial was lowest and productivity potential highest.AIgal biomass was lowest where productivity potemialwas high and disturbance potential \Vas "very high".There. encrusting coralline species such as Porolithol1

pachydermum and Neogoniolithon spp. dominated. Theextinction depth of tropical marine algae far exceeded thedepths to which we could sample. and thus we did notsample where productivity potential was lowest. How-ever. at -+0 m on the Salt River Canyon \Vall in SI. Croix,algal biomass and functional group diversity were rela-tively low. We did not find an appreciable cover ofcrUSlOse algae as we did at other low productivity poten-tial habitats. This may have been beC:lUse of the abun-dance of sediment at our study site (Steneck pers. obs.).The tropical sites were dominated by diminutive turfalgae at all but the habitats having mid 10 low disturbancepotemial under the highest productivity potential.

Temporal changes in community structure

Sorting out species-Ievel ('noise" from significant chang-es in community structure is a goal 01' the functionalgroup Jpproach. The composition of Jlgal species chang-es significantly between seasons in tropical reef systems.

488

We reanalyzed data on algal species composition from astudy conducted in SI. Croix by Adey et al. (1981) inwhich almost none of the dominant species on foreree1'transects \\ere found from one season to the ne:\t (Fig.6A). Howe\er. by reassigning the species to their fune-tional groups (i.e., Fig. 1), a much higher degree ofstability was revealed (Fig. 6B). The only change ofsignificance was the addition of macroalgae during thewinter and spring. This seasonal shift was evidenl tothose working on this project (R. Steneck pers. obs.) bUIwas not ob\'ious with analyses conducted at the specieslevel (e.g .. Fig. 9A).

A long term study of algal abundance and herbi\'ory onlamaica's Discovery Bay reef was conducted period-ically from 1978 to 1987. During the study, two signif-icant natural events affected the reef: Hurricane Allen in1979 hit the reef (see Woodley et al. 1981) and the massmortality in 1983 of the predominant herbivore, Diadema

antillarllln (e.g., Hughes et al. 1987). Only following themass mortality of sea urchins did community structureshift; algal biomass increased, and dominance shiftedfrom corallines to macroalgae in the shallow forereef. andfrom minute algal turf to macroalgae in the deep forereef(Table -+). Similar changes were observed throughout theCaribbean following the mass mortality of sea urchins(e.g., in Curacao, Ruyter van Steveninck and Bak 1986:

OIKOS 69:3 (IYY4¡

~~.:ol"~.,...~i-----'-'-----"""'-~----~'---------------__4114._-'4!lws__ ·

in SI. John. L.:vilan 19XX: anu in SI. Croi\.. Carpc:nt.:r1985b, 1(90), This suggc:sts thal a reuuctiun in uisturh-Jnce potential under constantly high prouucti\ity poten-tial will shift community structure from one uf algal crustdominance, low biomass. and low functional group di-\'crsity to one 01' macrophyte dominancc. signil1cantlyhigher biomass. and high fur.ctional group di\crsity.

Discussion

Convergent patterns in algal community

structure at the functional group level<3-:> CO"

Similar pallems in algal community structure atthe func-tional group level emerged from aH three geographicareas. In each region, the highest biomass and functionalgroup diversity were found in habitats h,lVing the ll)westdisturbance and the highest productivity pOlcntials re-spectively (Figs 5A-C). The dominant aIgae (i,c .. thosewith the greatest biomass) under these conditions wp.respecies lhat e relatively large in size and long-lived.such as lea~hery or corticated macrophytes (AG 5 and 4respective!y in Fig, 1). Where disturbance and produc-tivity potentials were both high or both 10\\. cruslOseaigae usually dominated. In all cases, encru<;ting corallinealgae dominated where those factors were high. butfles'hy'c'rusts were found under sorne conditions whereboth were low. Fig. 50 summarizes a generalized (andidealized) model of algal biomass dominance and func-tional group uiversity relalIve 10 the producti\'ity anddisturbance potentials 01' the environmenl. Under greaterdisturbance or reduced productivity potemial. the bio-mas s and functional group diversity decrease. and dom-inance shifts toward groups with lower canopv heights.Cnder cOñditions 01' the highest levels 01' dist~rbance orlowest productivity pOlential, lhe dominant (and some-times only) algal form is crustose algae. We offer thisapproach and general model (Fig. 50) as a testable modelal' "templet" sensu Southwood (1977) against whichother systems can be examined.

Support for the generality 01' the model is found in theliterature. In productive environments. changes in dis-turbance significantly change the structure 01' algal com-munities. y[any studics have demonslrated that in pro-ductive environments with intense herbivore-induced dis-turbance (i.e., the upper right comer 01' Fig. 5D), algalcrusts dominate (e.g., Paine and Yadas 1969a, Branch1975, Lawrence 1975, Menge and Lubchenco 1981. Lev-ings and Garritv 1983. Hav and Gaines 1984, Paine 1984.D~ggins and Óethier 1985. Steneck 1986, Fletcher 1987,Fletcher and Underwood 1987. Lilller et al. 1991). Whenthe herbivores are removed (moving to the left along thedisturbancc axis in Fig. 5D), diversity increases and thecrusts are ~by larger. canopy-forming macroalgae(Paine and Yadas 1969a. Vine 1974, Da:, :vn 1975, Oug-gins 1980. Paine 1980. Slocum 1980. Ayling 1981. Sousaet al. 1981. Steneck 1982. Hertnes, 1984, Carpenter

32 OlKOS 09:3 t 1994)

..

19X5h. l 'J90. Harrold anu R~ed 1985. Hay ano Taylor1985. Lewis 1986, Meng~ et al. 1986. Fletcher 1987,Flctl:her and Underwood 1987. Morrison 1(88). Areaswher~ herbivores are restricted from foraging, such asreef tlats. isolated mangrove roots or heavily wavc-ex-posed sublittoral zones, are often i,lands 01' tleshy macro-algae within are as otherwise occupied by crusts, calcifiedalgac. or minute algal turfs (Adey et al. 1977, Hay et al.1983. Levings and Garrity 1983. Himmelman 1984,Ojeda and Santelices 1984,' Lewis 1986, Taylor et al.1986. Foster 1987). Changes in physically-induced di s-turbance potential such as an increase in sand scour canshift turf algal communitieS"-io (;oralline dominated com-munities (Kendrick 1~1). Under intermediate leve1s ofgrazing. or when grazin:; or physical disturbance occurintem1ittently. smaller, shoner-lived (ruderal-weedy) al-gal forms dominate (i.e., algal turfs AG 1-3: Littler andAmold 1982, Littier et al. 1983b. Carpenter 1986, Lewis1986).

Yarying produclivity potential can also affecl alg:JIconununity structure. [n tidepools. removing herbivoresfrom low-intenidal pools (high produclÍvity potential)resulted in dümination by leathery macrophytes (Paineand Yadas 1969a). whiie similar removals in mid-poolsled to foliose or corticated macrophytes. In high p.ools(i.e .. low productivity potential), the only change' \~asfrom one species 01' crust to another (Dethier 1981a, b).Cubit ([984) showed that in the high intertidal zone 01'

Oregon. a seasonal increase in productivity potential (dueto lowered desiccation stress) combined with little win-tertime change in grazing pressure shifts tht: cover on therock from largely bare al' covered with microalgae in thesummer to abundant filamemous and foliase algae in thewinter.

AIgal functional group dominance along productivitypotential gradients correspond to the left axis 01' Fig. 5D.In the absence 01' herbivory. there is a consistent. globaltr~n i'rf '&orphology among benthic marine algae alongsubtidal gradients in productivity potential (reviewed inYadas and Steneck 1988) with leathery macrophytesdominating the shallowest areas. corticated macrophytesand foliose algae somewhat deeper. and crustose algae atextinction depths (sensu Sears and Cooper 1978). Thus.

, cruslOse algae dominate under conditions where bOlhdisturbance and productivity potentials are low, such as atgreat depths or in cryptic environments (Sears andCooper 1978. Steneck 1978. 1986, Littler et al. 1985,1986,1991, Yadas and Steneck 1988). This helps explainwhy the mass mortality 01' urchins in the Caribbean hadrelatively linle impact on the dominance 01' crustose algaein deep cryptic habitats where both productivity and dis-turbance potentials were very low (i.e., > 30 m underplate corals, J ackson and Kaufman 1987, Morrison1988), but had a major effect in shallow water where bothwere high before the die off (e.g., Carpenter 1988, Morri-son 1988). Stands 01' large macroalgae require environ-ments with a high productivity potential because theysuppon proponionally more nonphotosynthetic tissue

489

".

y~.'", ,~ ... ': ;<¡é, ..

~. i;";O:' •

lhan uo minute turl' algae at lhe Olher end of Ihe l'unc-lional grour continuum (Lin!cr and Linier 1984). Thismay be why large leathery mat:rophytes apparenlly can-not grow in waler as deep as corticated macroalgae orartit:ulaled calcified forms (Vadas and Steneck 1988). Incontrast. Ihin (Iolally pigmented) cruslose forms havinglhalli normal lo Ihe direction of ineoming light can grow10 the greatest deplhs of the photic zone (Adey andMacintyre 1973, Littler et aL 1985, 1986, Vadas andSteneck 1988). In the Caribbean, Lobophora variegata, acortic:lted ereet mat:roalga in shallow water grows as aproslrate, almost crustose, plant at greater depths (Coenand Tanner 1989) .. This erecr ro crustose morphologicalplasticity may have eontributed to the increased abun-dance of this plant following the mass mortality of Dia-

dema alltillartll1l ir: deep water aboye extinction depths(RuYler van Steveninek and Bak 1986). At the eommu-nilY level, Littler et aL (1991) showed that comparisonsamong shallow habitats in the Indo-Pacific having highproduclivity potcmial (i.e., ele\'ated nutrient levels) withlow 10 high levels of habivore-induced disturbance po-tential (i.e., grazing activity) shifted to crustose cor::¡i-lines. Such diffcrences in morphology. biomass, diversityand dominance along a gradient in productivity potentialare readily visualized in Fig. 50. Thus. a small shift in thebalance betwet:n Ihe prod!l¡:tivity and the disturbancepotentials al' the· eñvironment can result in a. highly vis-ible and predietable shift in the algal assemblage.

Interactions between algal functional groupsand structuring processes

Feedback mechanisms between algae and herbivores con-tribute 10 the persistenee of patterns such as those in Fig.50. Sorne areas dominated by ¡arge. canopy formingerecl macroalgae (AG 4-6) resisl in\'asion from someinvertebrate herbivores by limiting suilable space onwhich Ihe herbivores can reside and grne (Hay 1981 b.Underwood and Jemakoff 1981. Sleneck and Watling1982). As a result. relatively few in\'ertebrate grazers canfeed on established macroalgae (Table 1). Such al~ae alsopersist because single ~ from herbi\'ores ar \u l' tvto remove them, and they can repair, themselves by re-forming meristematic tissues. When intense-grazingherbivores such as parroltishes capable of consuminglarge macroalgae feed. the loss of lhose algal groups(shift from left to right in Fig. 50) is often compensatedfor by an increase in mass-speéific productivity (Carpen-ter 1986). Turfs (AG 1-3) that coexisl under hig~ levelsof herbivory show rapid replacement. thereby maintain-ing high levels of local (e.g., limpeí-maintained gardens.Branch et al. 1992) or community produclivity (Adey andSteneck 1985, Carpenter 1986, Adey and Goertemiller1987. Williams and Carpenter 1990). and thus maintainor possibly increase the trophie carrying capacity of theirenvironmem. However if a further increase in herbivore-induced disturbance shifts the community 10 dominance

490

by t:ru~ts. then lhc lo\\' Ilutritional value (Paine and Vaua~1':I6':1b) ami rclatively high resislant:e to herbivory ol' thalgroup will luwcr the trophit: carrying capacilY 01' thalenvirollmenl for herbivores. This will limit furtÍler in-creases in herbivore populatiolls. Like c10nal terrestrialplants (Bazzaz et al. 1987). t:ruSIS are favored wherehorizolllal spread is advanlageous relative to verticalgrowth (i.e .. where inlense disturbance can remove anyvertical growth). Stable coralline-dominated communi-ties existing under cundilions óf most intense and frc-quent grazing have been reponed world-wide (reviewedby Lawrence 1975, Sleneck 1986).

The size, shape and material composilion of an algamay contrarloc abilit" f a graz~ 1 i ~the olap' ud

Q 1"\d~ Q..Sco .t u ~ 'lE:: "O~f'....:. 1\thu5 ~e p\\me ueter mant~ ot <; 101 It (e.\! .• Pe'lnIl121-and Paul 1992). In contrast, che ical ,ª'táren1S lOVO~'-ing palatability usually involve .&t~'l~- - ~ngestionland \ViII be important in mOdifying an herbivore's sub-sequent foraging behavior if the grazer is capable ofvisually or che;nic~lIy recognizing and biting the plaOl(i.e., il is apparent and edible). Accordingly. the majoril)'of chemical defenses are found among macroal:;ae (AG4-6: e.g .. Hay et JI. 1987, Hay and Fenical 1988. 1992).If an alga lVilh toxins ar digestion inhibilors (Tugwell andBranch 1992) is grazed. this constitutes a disturbance 10

the plant eveli if ¡he herbivore irnmediately li~?s"thetissue consumed (e.g .. Targetl et al. 1986). If these com-.pounds kili the grazer or result in a behavioral change toavoid the alga, then they are deterrent. Neither our sludy(Fig. 5) or others have faund chemitalIy defended algaedominating zones with high or very high dislurbancepotenlials. Thus there is little evidence thal chemicaldeterrcms determine lhe strueture of algal assemblagesalthough they probably control what species within afunclional group are found. Nutritional value of algaemay also affect the species consumed (Hom and :'-Jeigh-bors 198~. Steinberg 1985). but primarily at within-func-tional group levels.~J;¡ Wj.tN-ll -se~~t)~~ -funclional group processes may be useful distinclions instudying the structure and function of complex naluralcommunities.

Unifying concepts: marine and terrestrialcomparisons

The patlems we have described (Fig. 5D) indicate thatalgal functional groups exhibit similarities in their distri-bution and abundance corresponding to two strucruringparamelers in the environment. A functional group thuscomprises the intrinsic characteristics (e.g., morpholog-ical and anatomical) that conlribute to ilS ecologicaJ suc-cess at some point along the continua of environmentalproducli\'ilY and disturbance potemials (e.g., Fig. ~). Ter-restrial ecologists have long grouped ecologically ormorphologically similar plants (Raunkiaer 193~. Danse-reau 1957. Holdridge 1967) but no consistem schemeevolved from their efforts. Allhough rhere is general

OIKOS 6'1·3 (19941

Fig. 7. Gcncralized 1110del01"comrnunity dorninants (ha[ com·pares Grime', (1977) l11odel' (A) "ilh ours (Fig. 51 b~ usingGrirne' s (1977) lenninology and a comInon orientation of dis-turbance and prOdUCli\'ily potenlia!s uf [he environment (B. see(ext and Sou(h\Voou 1988 j. The syn(hesis (Cl incorporales di s-(urbance tulerance (O Grirne's (1977) model.

GRIME 1977A ..J

COMrETmVE PERENNlAL-<¡:

STRAnCY.C HERllSC·R Z~.~ .• In.'d ~.,,~ prtennt.ll.l UJ....•. 2c·s ,.e.g.. woody

NO VIABLE...

pl.ints :>STRATEGY 6STRESS ::>

TOLERANCE: S el".g .. Lid~ns O

'"~ "-DlSTURBANCE POTENTlAL

.'~"l'O - THIS sruOYB ;(

COMPETITlVE¡:Z

STRATECY:C '"e.g., ~lp rERENNIAl 2HERBS C·R

c·s,.¡-

e.g., .:"nic&t~ ~m.acropkytrs NO VIABLE tiSTRATEGY ::>STRESS elTOLERANCE, S Ú

e.g ..crusl. ouCTQ.i.lg;¡e ~~

DlSTt:RBANCE POTE.'1TlAL

conceptual agreement conceming the importance of di s-turbance and producti \'ity potenrial (often presented as itsinverse. "stress' or "adversity") as t\Vo of the most im-portanr environmenral componenrs. there is considerabledisagreement abollt how best lO apply these parameters(e.g .. see Greenslade 1983, Loehle 1988. Southwood1988. Taylor et al. 1990. Herms and Manson 1992).Many stlldie" choosc the t\Vo \"ariables of prú-'·;ctivityand disturbance to create rectangular plots (reviewed bySouthwood 19813). However. Grime (\974, 1977, 1981)added "competition" 10 form a. triangular model. Thisapproach has been criticized as tautological becausebiotic processes such as C'ornpetition and disturbance aremediated by intrinsic properties of the organisms andthus cannot be used lO predict organism dominance (Vander Steen and Scholten 1985). Despite other criticisms oftriangular reprcsentation of plant "strategies" (e.g .. Vander Steen ano Scholten 1985. Loehle 1988, Taylor et al.1990), many marine researchers have applied Grime'smodels lO the study of benthic mal;ne algae (e.g .. Shep-

Variations and Iimitations in approach

Russell (1986) notes that there are problems with anyclassificalion of strategies 01' marine algae (Fig. 7). Whilefunctional groups can be placed on such a diagram withsorne degree of certainty. individual species may be diffi·

hcro 19X1. Dayton el al. 19X~. Littlcr and Littkr \984). [nFig. 7A we mooified Grime', moJel taking into account,e\"eral of these criticisms into a rectangular madel basedon the productivity and disturbance potentials of the envi-ronment (i.c .. independent of ;llgae presentl a, \Ve havedefined those terms and in accordance with the habitattemplet model 01' Southwood t 1988).

The algal functiona\ groups presented here tFig. 1),and by Littler and Littler (1980. 1984) show some paral-lels wilh terrestrial plant strategies of Grime (Fig. 7A, B).Leathery macrophytes such as kelps correspond to the"Cl)mpeti~e Strategy" of Grime (198\) or the "Growth-D'ominated" plants of Herms and Mattson (1992) bybeing !:J.rge canopy-forming plants and thus often as-sllmed lO be good competilOrs for light. They are mostabundant in produclive. relati\"ely undisturbed environ-mems (Fig. 5) and have characteristics such as mediumlonge\·ity. often structural anci/ar chemical and anti-herb·i\"ore defen"es and low tolerar.ce to stress in comman"i¡h Southwood s (1983) habitat templet madel. Simi-larly. "Stress-Toleran!" (sensu Grime 1981) or "Differ-entiation-Dominated" (sensu Herms and Matlson 1992)algae in::lude sorne of the crusts and microalgae. both of'yhi.:h gro'" in les s productive environmen\s.: "Ruderal"alg"Je include microalgae. filamems, and foliese algaewhich. as in their terrestrial counterparts. are short-lived,but colonize and grow rapidly (Littler and Linier 1980,.-\dey and Goertemiller 1987). They may occupy habitatssuch :lS bOlllders that roll frcquently, causing repeated.se"ere dist~lrbances to the algal assemblage (Sousa 1979,Littler and Linier 198~).

H0"·e\·cr. marine algae ha ve a fourth distinct and com-mon strategy: Disturbance-Tolerance (Figs 7B. C: Daytonet al. 198~. Linier and Littler 1984, Russell 1986 l. Forexample. encrusting coralline algae tolerate disturbancesthm "ould se\"erely damage or remove other plants. Dis-turbance-tolerant plams either resist (by being structur-ally prolecled against injury, c.g .. Pennings and Paul1992) or rapidly recover from disturbances. Unlike theRuderai Strategy of Grime ( 1981 ) constam recruitment isnot necessary [O maintain their dominance. The terrestrialrealm also contains examplcs of genuinely disturbance-to~eram plants .. including plants that resist herbivory bybeing distasleful or inedible (Harper 1969), tolerate itwith regro"th (e.g., turf grasses. Ylack and Thompson1982) or thri\'e under frequem herbivore-induced disturb-ance (~1c;\allghton 1979). Other plams, such as those ofthe Fynbos of Southem Africa. routinely tolerate andeven require physical disturbance from fire (Bond et al.1992). ~

~...Z'"2,....:>

NO VIABLE BSTRATEGY ~

O

~

SYNTHESIS

OISTURBA..'1CE POTE1"llAL

c.

32' OIKOS ó<):.1(1'I'/41 491

-----

cult lo c1assify. He ciles examples ~uch a~ ulvoids whichare ckarly stress-tolerant and grazer-~usceptiblc. but un-del' some conditions. are good competitors (Lubchenco1978. Sousa 1979). Although no scheme is perfect, thegenerality al' the model can be seen in the volume 01'

literature (cited aboye) that it does explain. Some ob-jections can be answered by understanding intraspecificand intra-plant differences in functional characteristics.For example, algae pass through different functionalgroups as they grow (Stenc:ck and Watling 1982). The~e-fore macroalgae (AG 4-6) outcompeted by ulvoids (AG3) were in fact at a sporeJsporeling state, and thus moresimilar 10 microalgae or filaments in AG 1 and 2 at thetime 01' competition. Phcnotypic plasticity aiso allowsspecies to cross functional groups. Lewis et al. (1987)showed that ecotypic variation can be induced by herb-ivores: in the presence of freguent fish grazing, a corti-cated foliose alga (AG 3.5) can become a filamentousform (AG :n. Hanisak et al. (1988) showcd that genet-icaliy maintained morphological variants of the macro-alga Gracilaria sp. differ in mass-specifíc productivity.Similarly, the ploidy level of heteromorphic algae, bydefinition. determines functional differences related tomorphology (Slocum ~!)80, Oethier 1981 D. Steneck andWatling 1982, Liltler and Linier 1983. Linier e~al. 1987).

Sorne complex algae may be composed of severaldifferent functional modules (sensu Harper 1985). Forexample a SargassulIl plant (AG 5) may have a crustoseholdfast (- AG 7), a leathery stipe (AG 5) and thin-

. foliose "leaves" (-AG 3). Linier and Kauker (1984)showed the upright portion of Corallilla offieillalis (AG6) is more productive and more susceptible lO disturbancethan the crustose holdfast (AG 7). For a gi ven morph-ologically complex alga, thallus longc\'ity and mass-spe-cifíc productivity of their individual modular componentsprobably correspond to the relationships summarized inFig. 3. Thus one may expect "Ieaves" al' SargasSLtm to bemore productive (Kilar et al. 1989) but have a shorterlongevity (due lO senescence and increased grazer sus-ceptibility) relative to its crustose holdfasl. For example.Hay et al. (1987) described amphipod grazing on Sargas-

sum as being largely confíned to leaves. This provides anew way 01' considering ecological pr{)cesses such asrecruitment. production, competition and predation byconsidering each relative to the module al' interest. Thisshould complement the modular demography discussedfor higher plants by Harper (1977), and for other clonalorganisms by Jackson et al. (\985).

Stability at the functional group level

While stability at the species (i.e .. population) level isnotoriously difficult to define and demonstrate (Connelland Sousa 1983, Connell 1986). stability at the functionalgroup level may be the norm in nalllre. 11' leveIs 01'productivity potential and disturbance do not change.then algal community structure (relalive abundance,

492

dominan.:.: ami funclional group div.:rsity) ,hould notchange. e\ en though spccies lIi ~c\,1Waybe high. Thuseven though a community having a high dislUrbanccpotential i~ conslantly perturbed (in terms of biomassbeing removed and perhaps 01' species being driven tolocal extinction), if Ihat level 01' perturbation is nOI al-tered. the ~tructure of Ihe algal assell1blage should remainstable at Ihe functional group level.

Algal cOll1munities on reefs provide good examples ofstability 3,1 Ihe functional group leve!. despite high ratesof disturbance (Hatcher 1983, Carpenter 1986 J. Shallowforereef zones are ch,i)f3.cterized as having high levels ofherbivory \Ogden and Lobel 1978. Hay 1981 c. Hay et al.1983, Le\\i~ and Wainwright 1985) and lo\\' algal bio-ll1ass ("turt's", e.g .. Carpenter 1986_ LinIer et al. 1991).Turfs are composed primarily of fi!amentous and mi-croalgal species and although they are highly di\'erse withwell over 100 species on Caribbean reefs (Adey et al.1981 l, only 30 te 50 01' these species are comll1or, at anytime (Adey and Steneck 1985). We found (Fig. 6A) thalonIy a fe\\ species persisted al' remained abundant fromone season lO the next but that the community is season-ally relati\-ely stable when examined at a functional grouplevel (fig. óB).

Long lerm stabililY and evidence for multipl.: stablepoints is e\-ident in the structure of forereef communitiesat Oisco\'ery Bay. Jamaica. The reef was described dec-ades ago as having Iow algal biomass, virtual absence ofmacroalgae and an abundance of corals (Goreau 1959)which was Iypical of forereefs throughout the Caribbean(e.g., RanJall 1961. Earle 197:~. Van den Hoek et al.1975). Qu:mtitative data from that reef in 1978 :1nd 1982(Table -+) show thal the dominant components changedliule over Ihe decades despite intervening hurricanes (seeResults). However. Ihe mas s mortality of the sea urchin.Diadema (II/Ii/larlllll. in 1983 significantly reduced thedisturbance potelllial of the shallow forereef (i.e .. highproducti\'ilY potential) environment. The rise to dom-inance of macroalgae corresponded with the decrease incoral co\-er (Table -+). The forercef community has re-mained in Ihis stale sinee, suggesting that multiple stablepoints (Sulherland 1974) may operate at a functionalgroup leve! when ehanges occur in the disturbance poten-tial or productivity potential of the environment. Themode! (Fig. 50) predicts that Ihe greatest change incommunity structure wil! occur with changes in disturb-ance potential where productivity potential is high. Thismay explain why liule change was observed in algalcommunity structure in zones having had eonsistentlylower population densities of Diadema before the mortal-¡ty (i.e., lower disturbance potential. such as in the back-reef: Table 4), 01' having both lower producli\-ity anddisturbance potentials such as deep cryptie reef habitats(lachon and Kaufman 1987, Morrison 1988).

OIKOS 6Y:.111994)

Conclusions

Liltler and Linier (198~: 31) nOle lhal. by using a func-

tional group approach. it is possible 10 ••... predict com-

munity composilion froll1 knowledge of disturbance le v-

els in given environments. or lhe reverse. Further, the

approach is applicable anywhere the predominant algal

abundances are known wilhout being restricted by phylo-

genelic group. habitat. or geological era". Our general

model (Fig. 50) provides a simple way to predict algal

commllnity composition based on two environmental

axes: or conversely. to gain insight about ¡he environ- .,

mental conditions in an area by examining lhe algae.

Strong palterns emerge in how algae of specitlc forms

relate to the environment because strucluring processes

(disturbance and pwductivity potentials) impinge in a

form-specific manner. The degree to which our commu-

nity structurc model describes lhe strllcture of several

disparate marine communilies suggesls thal the relatively

few variables we have isolated are fundamentally impor-

tant. It follows that natural or man-made allerations of

one or bOlh of these parameters will cause prediclable

changes in algal community struclure. Thus. while we

cannot predicl how a given species will respond 10 a

deerease in physiolQgical stress in ilS environment or 10

an inerease in herbivory over geologieal time. we can

predict how the assemblage of algae will change al lhe

funetional group leve!. Algal fllnctional groups. like all

human-imposed aggregations (Orians 1981). have limila-

tions in the precisions of lheir boundaries and lhe level of

queslions they address. Our approach does nOl deny lhe

ulililY or neeessílY of ecological study al lhe species

level, bUl we conclllde lhat it is useflll to examine sorne

communíly-Ievel qllestions aboul structuring processes.

diversity. dominance. relative abundanee. stability and

paleoecology at the level of functional groups.

Acknowledgelllellls - We gralefully acknowledge the help wereceived fram many colleagues Wilh \Vhom \Ve ha\'e shared lheideas. especially: the 1978 Coral Reef Ecology class at Disco\'-ery Bay jamaica (\Vho heard the concepls fírsl). IN. Adey. R.Carpemer. S. Hacker. M. Hay. J. B. C. Jaekson. 1. Lubchenco. F.McKinney. D. McNaughl. M. Nitecki. R. T. Paine. A. Palma. C.Plister. J. Portero S. Slanley. R. L. Yadas. G. Vermeij and L.Watling. G. M. Branch. S. Brawley. S. Dudgeon. D. O. Duggins.S. Hacker. M. Hay. B. Jones. S. Le\Vis. :-'1. and D. Linier. H. andK. Nielsen. T. MoskovilZ. P. Ojeda. C. Pfisler. and B. Sanlelicescritiqued drafts of lhis manuscripl. Spaee and logislical supportwere provided al the West Indies LabofillOry in SI. Croix by J.Ogden and R. Dill. Discovery Bay Marine Laboralory in Ja-maica bv J. Woodley. Darling Marine Center in :v!aine bv L.Watling: Friday Harbor LaboralOries in WashinglOn by A. O. D.Willows. Access 10 field siles al TalOosh ¡sland. WashinglOnwas arranged by R. T. Paine and granled by the Makah T;:¡balCouncil and lhe U.S. Coast Guard. The Nalure Conservancvallowed us 10 work on Yellow [sland. and B. and S. Ragenprovided access to their shoreline on San Juan [sland. P. Mace.K. PaulI. K. [rons. and D. Duggins helped in lhe fíe Id inWashingwn. M. Britlsan. B. Milliken. K. Paull. C. Plister and S.Stilwell-helped in fíeld work and dala analysis in Maine. To allwe are grateful. This research \Vas primari Iy funded by gramsfrom the Nalional Science Foundation IOCE 8315136 and OCE8600262) wilh additional funding from se\'eral sources. Sludies

OIKOS 69:3 IIQq~1

of de~p waler algae in the Gulf 01' Maine \Vere fundcd by a grantfmm :"IOAA's National Undersea Research Center at lhe Univ.01' Conneclicul. Olher rescarch in Maine was funded by UMIUNH Sea GrJnt (RJFMD-169. NA8óAA-D-SG-047). Researchin SI. Croi", was funded by NOAAINURC/FDU grants (82-6.87-5\. This is contrihution number 269 01' lhe Darling MarineCenter. -

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497

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_.-_.'

Appendix.Maximum lhallus long.:vities reponed fOl" alga.:. Functional group designalion number (i.e .. Fig. 1) fOl" each algal specics IS

rcpresented in the column lubeled "Algal group"

Reference Species A!gal group Max. age (yr)

Palrick 1970 OialOms 0.5Sleneck unpubl. Ulothrix flacca 2 0.3Mumford 1973 Porphyra spp. 3 0.8Harlin 1971 Smitlrora haiadum 3 0.75Steneck unpubl. Emeromorpha 3 0.5Sleneck unpubl. Halosaccion glandiforole 3 0.5Hansen 1977 lridaea splendens 3.5 1Slocum 1980 Mastocarpus papillatas :-. -1 0.9Goff and Cole 1976 Odontlralia floccosa '- -1 1O'Antonio 1986 Neorhodomela larix •• 2Steneck unpubl. Ascoplry/lum nodosum 5 15Khailov 1979 C"stoseira barbata 5 18Hay 1979 Durvillea antarctica 5 Q

Black 197-1 Egregia laevigata J 1.25Connell 1986 Eisellia arborea 5 5Widdowson 1965 Hedoplryllum sessile 5

,OU8gins 1980 Lamillaria sp. 5 7Vad:ls <lnd 5teneck 1938 Lamilla.'((l sp. 5 ~

I

Kain 1971 wminaria hvperborea 5 13Norton el aL 1977 wminaria lryperborea 5 9Klinger and OeWreede 1983 Laminaria setclrellii 5 17Paine Pers. Comm. OCI. 1987 Lessoniopsis littoratis 5 25OaylOn 1973. Paine 1979 Postelsia palmae!onllis 5 1Paine Pers. Comm. OCI. 1987 Pter.-goplrora californica 5 20MacMillan. 1!iD2 Pterygophora califomica 5 i7De Wreede 198.1 Pter"gophora cal/fornica 5 9Steneck el ,Ji. 1977 Clathromorp/lUm compactulll 7 40Lebednik 1977 CllIIhromorphum nereostratllln 7 100Edvvean and Ford 1984 Lithophyllum incrustans 7 34Pafne el al. 1979 "Pelrocelis" 7 85Oelhier 1931 <l.b "Ralfsia californica" 7 1

(

.•.

498 OIKOS 69'3 (1\~)'¡l

.'.

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