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1 The Role of Herbivorous Fishes in the Organization of a Caribbean Reef Community Author(s): Sara M. Lewis Source: Ecological Monographs, Vol. 56, No. 3 (Sep., 1986), pp Published by: Ecological Society of America Stable URL: Accessed: 27/10/ :44 Your use of the JSTOR archive indicates your acceptance of JSTOR's Terms and Conditions of Use, available at JSTOR's Terms and Conditions of Use provides, in part, that unless you have obtained prior permission, you may not download an entire issue of a journal or multiple copies of articles, and you may use content in the JSTOR archive only for your personal, non-commercial use. Please contact the publisher regarding any further use of this work. Publisher contact information may be obtained at Each copy of any part of a JSTOR transmission must contain the same copyright notice that appears on the screen or printed page of such transmission. JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact support@jstor.org. Ecological Society of America is collaborating with JSTOR to digitize, preserve and extend access to Ecological Monographs.

2 Ecological Monographs, 56(3), 1986, pp C 1986 by the Ecological Society of America THE ROLE OF HERBIVOROUS FISHES IN THE ORGANIZATION OF A CARIBBEAN REEF COMMUNITY' SARA M. LEWIS2 Department of Zoology, Duke University, Durham, North Carolina USA Abstract. Experimental manipulations of grazing intensity were used to examine the role of herbivorous fishes in the families Acanthuridae (surgeonfishes) and Scaridae (parrotfishes) in determining distributions and abundances of benthic species within and among shallow tropical reef habitats. A back reef habitat along the Belizean barrie reef was characterized by a diverse benthic assemblage of algal turfs, coralline algae, and the coral Porites astreoides, but by extremely low macroalgal abundance. In contrast, several nearby shallow habitats were dominated by dense stands of several macroalgal species. Experimental reduction of herbivorous fish grazing in the back reef (achieved by constructing exclosures) rapidly and dramatically altered existing patterns of benthic species composition and species abundances. After 10 wk of reduced herbivory, total macroalgal abundance increased significantly in herbivorexclusion areas relative to unmanipulated controls, and was correlated with decreased percent cover of available space, several algal turf species, crustose coralline algae, and Porites. Some macroalgal species were able to directly overgrow and kill portions of Porites colonies within herbivore exclusion treatments. Successful recruitment and growth of several algal species under experimentally reduced herbivory indicated that macroalgal species distributions may be limited by herbivory rather than by lack of spore availability or unsuitable physical conditions. Algal turfs characteristic of many reef habitats appear to represent herbivore-tolerant assemblages, persisting under high grazing intensity but responding rapidly to reduced herbivory with increased abundances, morphological changes, and altered reproductive status. These resultsuggesthat herbivorous fish grazing profoundly influences benthic species distributions and abundances within some tropical reef habitats. Spatial variation in herbivory appears to be of fundamental importance in determining regional patterns of benthicommunity structure on tropical reefs. The spatial mosaic of benthicommunity composition among shallow reef habitats was associated with patterns of grazing intensity by herbivorous fishes. Several reef habitatsupporting dense macroalgal stands represented spatial refuges from herbivory, with low herbivorous fish densities and reduced grazing intensities. Transplant experiments revealed that algal species characteristic of these low-herbivory habitats were highly susceptible to grazing by herbivorous fishes. Spatial heterogeneity in grazing intensity may contribute to high regional diversity among tropical reef habitats by maintaining different benthic species assemblages under fundamentally distinct selective regimes. Key words: Acanthuridae; algal turfs; Caribbean; community organization; coral reefs; fish grazing; herbivory; macroalgae; nonequilibrium community, plant-herbivore interactions; Scaridae; tropical diversity. INTRODUCTION A primary objective of community ecology is a general synthesis of the roles of various physical and bi- ological factors in determining distributions and abundances of species within natural communities. Coral reef communities represent the archetype of diverse species assemblages in marine systems, and there has been considerable speculation concerning the origin and maintenance of such highly diverse tropical communities (Connell and Orias 1964, MacArthur 1965, Pianka 1966, Menge and Sutherland 1976). Several hypotheses for the maintenance of tropical diversity have emphasized the importance of competitive interactions leading to increased resource partitioning within tropical guilds (Klopfer and MacArthur 1960, MacArthur 1972, Grassle 1973). Recent experimental studies (Glynn 1976, Connell 1979, Hay 198 la, Sammarco 1982a, b, Wellington 1982, Hixon and Brostoff 1983) provide insight into the organization of coral reef benthic communities, and indicate that physical and biological disturbances may act to maintain high diversity in reef benthic communities by reducing local competitive interactions. In this paper I show that herbivorous fish grazing profoundly influences the distributions and abundances of benthic species in a Caribbean reef community, and suggest that spatial patterns of herbivory may be an important mechanism contributing to high regional diversity among tropical reef habitats. In marked contrast to temperate subtidal communities that often are dominated by dense macroalgal vegetation, algal assemblages on coral reefs are char- ' Manuscript received 27 March 1985; revised 27 January 1986; accepted 30 January acterized by a relative paucity of macroalgal species 2 Present address: Aiken Laboratory, Harvard University, and a predominance of calcified crustose algae and Cambridge, Massachusetts USA. filamentous algal turfs (reviewed by Gaines and Lub-

3 184 SARA M. LEWIS Ecological Monographs Vol. 56, No. 3 A 17 N JS -BELIZE: Carrbbean Sea Study Siees HONDURAS.... CARRIE BOW z~~ii2~ CAY 88 W B South Water Cay LY Carie Bow Cay Bank L...J 500m 50M FIG. 1. (A) Locations of study sites along the Belizean barriereef. (B) Macroalgal study sites: (3) Tobacco Reef and (4) Curlew Bank. (C) Carrie Bow Cay study sites: (1) back reef site; curving solid line represents transect location; herbivore exclusion fences, * quadrat locations; and (2) Lagoon macroalgal site. chenco 1982). Tropical macroalgal species are often patchily distributed among reef habitats, with many species restricted to deep sand plains (Dahl 1973, Hay 1981 a), to intertidal reef flats (Littler and Doty 1975, Hay 1981b, Hay et al. 1983), or to certain shallow subtidal areas (Taylor 1960, Tsuda 1972, Wanders 1976a, Adey et al. 1977, Conner and Adey 1977, Morrissey 1980). These macroalgal-dominated areas support benthic species assemblages that are quite distinct from those of other reef habitats, and such differences in species composition among habitats may be an im- portant component of regional diversity (referred to as beta-diversity; Whittaker 1960) in coral reef benthic communities (Hay 1981 a, 1985, Gaines and Lubchenco 1982). Coral reefs also support an abundant and diverse herbivore guild, including microcrustaceans, molluscs, echinoids, and fishes (Hiatt and Strasburg 1960, Ogden and Lobel 1978). Several studies have demonstrated that herbivory may influence tropical plant biomass and species composition (Stephenson and Searles 1960, Randall 1961, Earle 1972, Ogden et al. 1973, Mathieson et al. 1975, Wanders 1977, Borowitzka et al. 1978, Hay 1981 a, c, Miller 1982, Sammarco 1982a, Hatcher and Larkum 1983, Hay et al. 1983, Carpenter, in press). Herbivorous fishes in the families Acanthuridae (surgeonfishes) and Scaridae (parrotfishes) represent an ecologically and evolutionarily important component of the herbivore guild on many tropical reefs (Randall 1965, Wanders 1977, Steneck 1983, Hay 1984b, Lewis 1985, Lewis and Wainwright 1985), but the effects of grazing by herbivorous fishes on reef community organization have received little attention. Recent studies have documented considerable variation among reef habitats in both herbivorous fish abundance (Miller 1982, Russ 1984, Lewis and Wainwright 1985) and grazing intensity (Hay 1981c, Hay et al. 1983), and these spatial variations in herbivory are likely to have important implications for reef benthic communities. The study described here examined the role of herbivorous acanthurid and scarid fishes in determining benthic species composition and abundances within and among some shallow tropical reef habitats. The following hypotheses were addressed using field observations and experimental manipulations of grazing intensity: (1) herbivorous fish grazing is responsible for maintaining a shallow back reef assemblage dominated by algal turfs, crustose coralline algae, and corals, and (2) macroalgal species distributions among shallow reef habitats are restricted by herbivory, rather than by spore availability or physical conditions. The results indicate that fish grazing may profoundly influence benthic community structure within some shallow reef habitats by reducing abundances of potentially dominant macroalgal species. The disjunct distributions of several tropical macroalgal species are shown to reflect spatial refuges associated with locally reduced herbivorous fish density and grazing intensity. These results suggest that spatial heterogeneity in fish grazing intensity may be of fundamental importance in maintaining

4 September 1986 HERBIVORY ON A TROPICAL REEF 185 distinct species assemblages in different reef habitats, and may thus enhance overall benthic species diversity on tropical reefs. TABLE 1. Major benthic species present in approximately bimonthly collections from the back reef study site from January 1982 to June This list represents common species and is not meant to be exhaustive.t STUDY SITES This study was conducted at the Smithsonian Institution's field station at Carrie Bow Cay, Belize, Central America (16?48' N, 88?05' W; Fig. 1) from January 1982 to December The topography, geology, and biological zonation of this portion of the Belizean barrier reef are described in detail in Rutzler and Macintyre (1982). Norris and Bucher (1982) provide floristic accounts for this region. The primary study site was located directly landward of the intertidal reef crest east of Carrie Bow Cay at m water depth (Fig. 1 C). This back reef habitat is typical of the shoreward border along much of the Belizean barrier reef (James et al. 1976, Burke 1982). The substratum consisted of relatively flat, consolidated coral rubble overlain by coarse sand. The back reef benthic community comprised four major groups of primary producers (Table 1): algal turfs, scleractinian corals, crustose coralline algae, and macroalgae (defined here as plants > 2 cm in height). The predominant group consisted of an inconspicuous, highly diverse assemblage of filamentous algal species, referred to here as algal turfs (sensu Dahl 1972: a heterospecific assemblage of fleshy and filamentous algae <2 cm in height). Similar algal turf assemblages are ubiquitous in shallow reef habitats throughou the tropics (Bakus 1969, Taylor 1971, Dahl 1972, Wanders 1976b, Morrissey 1980, Borowitzka 1981). Porites astreoides was the most common coral species in the back reef habitat. Heavily calcified crustose coralline algae, primarily Hydrolithon, were moderately abundant, while macroalgal abundance was extremely low, the macroalgae consisting mainly of two species of the calcified green alga Halimeda. Other macroalgal species (Padina, Turbinaria, Sargassum, Laurencia, Coelothrix) occurred only rarely in nearby areas of the back reef and reef crest, and were restricted to territories aggressively defended by adult damselfishes of the genus Stegastes. Similar microhabitat refuges from grazing fishes in damselfish territories have been described in previous studies (Brawley and Adey 1977, Hixon and Brostoff 1983, Sammarco 1983). The back reef habitat was characterized by high densities of herbivorous fishes, primarily surgeonfishes (Acanthurus) and parrotfishes (Sparisoma, Scarus). These fishes are visually orienting and highly mobile herbivores (Randall 1967, Earle 1972, Ogden and Lobel 1978). The most common herbivorous fish species in the back reef were: Acanthurus bahianus Castelnau, A. coeruleus (Bloch), Scarus iserti Bloch, Sparisoma chrysopterum (Bloch & Schneider), S. viride (Bonnaterre), and S. rubripinne (Cuvier & Valenciennes). The diurnal pattern of acanthurid and scarid activity in the back reef is shown for April 1982 in Fig. 2. These fishes Algal turfs Chlorophyta Caulerpa ambigua Okamura Cladophoropsis macromeres Taylor' Cladophoropsis membranacea (C. Agardh) B0rgesen Pseudendonclonium submarinum Wille' Valonia aegagropila C. Agardh2 Valonia ocellata Howe2 Phaeophyta Dictyota bartayresii Lamouroux Padina jamaicensis (Collins) Papenfuss (turf form) Sphacelaria nova-hollandiae Sonder' Sphacelaria tribuloides Meneghini' Rhodophyta Amphiroa fragillissima (Linnaeus) Lamouroux3 Centroceras clavulatum (C. Agardh) Montagne' Ceramium spp. Chondria sp. Coelothrix irregularis (Harvey) B0rgesen Digenia simplex (Wulfen) C. Agardh (turf form) Gelidiella acerosa Feldman & Hamel (turf form) Gelidium pusillum (Stackhouse) Le Jolis4 Herposiphonia tenella (C. Agardh) Ambronn' Jania adherens Lamouroux3 Laurencia spp. Lophosiphonia cristata Falkenberg' Polysiphonia scopularum var. villum (J. Agardh) Hollenberg' Polysiphonia spp.' Pterocladiamericana Taylor4 Taenioma nanum (Kutzing) Papenfuss' Wrangeliargus Montagnel Wurdemannia miniata (Draparnaud) Feldman & Hamel4 Cyanophyta Schizothrix mexicana Gomont' Microcoleus lyngbyaceus (Kutzing) Crouan' Corals Porites astreoides Lamarck Siderastrea siderea (Ellis & Solander) Crustose coralline algae Hydrolithon boergesonii (Foslie) Foslie5 Neogoniolithon sp. 15 Macroalgae Chlorophyta Halimeda opuntia (Linnaeus) Lamouroux6 Halimeda tuna (Ellis & Solander) Lamouroux6 Rhodophyta Galaxaura subverticillata Kjellman t Taxonomically closely related algal species and several small algal turf species were pooled into the following functional groups for data analysis in the herbivore exclusion ex- periment (species composition of each group is indicated by superscripts): (1) microturfs (filamentous algal species <300,um diameter), (2) Valonia, (3) articulated corallines, (4) Gelidium, (5) crustose corallines, (6) Halimeda. migrated into the back reef shortly before sunrise, foraged singly or in small schools throughouthe day, and left at sunset for shelter in deeper reef areas. Repeated censuses from April 1982 to March 1983 (Table 2) indicated that species composition and relative abun-

5 186 SARA M. LEWIS Ecological Monographs Vol. 56, No. 3 cam 200 E QD 160 Q D - I I T _ ACANTHURUS SPARISOMA e ; XSCARUS U) Z TIME OF DAY FIG. 2. Diurnal variation in abundance of acanthurid and scarid fishes (total density X + SEM; n = 10 for each time period). Visual censuses were conducteduring April 1982 along transects (50 x 2 m) through the back reef habitat. Solid bar along horizontal axis indicates times of sunrise and sunset. dances of herbivorous fishes were relatively stable. Other groups constituted minor components ofthe herbivorous fish guild in the back reef habitat; in > 1200 h of observations underwater, Cantherhines pullus (filefishes) and kyphosids (sea chubs) were seen only rarely, occurring in densities << 1 individual/400 M2. Territorial damselfishes were not abundant in the area of the back reef chosen for study; in March 1983, mean (?SEM) damselfish density within 10 replicate 10-M2 plots was 0.5? 0.3 individuals/10 M2, and all of the individuals were juveniles. The sea urchin Diadema was also rare in the back reef (perhaps due to the limited shelter provided by Porites astreoides colonies); in March 1983 (before Diadema mass mortality; Lessios et al. 1984), daytime Diadema density was 2 individuals per 100-M2 transect in the back reef study site, and observations at night indicated negligible immigration from adjacent habitats. The back reef habitat provided an excellent opportunity to investigate ex- perimentally the role of herbivorous fishes in structuring reef benthic communities, because of the absence of confounding influences from other macroherbivore groups, as well as the fact that the shallow site facilitated construction and maintenance of experimental manipulations. In contrast to the sparse macroalgal assemblage of the back reef habitat, several nearby habitats in shallow water were dominated by luxuriant growth of several species of macroalgae. The three areas selected as macroalgal sites (Fig. 1B, C) closely resembled the back reef site in substratum characteristics (consolidated coral rubble and coarse sand) and water depth ( m). Plant species composition in these macroalgal sites was similar to that reported from other macroalgal stands in the Caribbean, although species relative abundances vary among Caribbean locations (see Wanders 1976a, Adey et al. 1977, Conner and Adey 1977 for detailed descriptions of several shallow macroalgal stands). The three macroalgal sites considered in this study were referred to as Lagoon, Tobacco Reef, and Curlew Bank. Descriptions of their major vegetational components (dominance determined by visual inspection) follow. Lagoon (site 2, Fig. 1C): Several sections of beach- rock off the northwest shore of Carrie Bow Cay supported dense stands of Padina jamaicensis (Collins) Papenfuss (designated P. sanctae-crucis in Taylor 1960) and Digenia simplex (Wulfen) C. Agardh. In surrounding sandy bottom, Laurencia papillosa (Forsskal) Greville was commonly attached to small pieces of coral rubble. TABLE 2. Acanthurid and scarid species abundances (X? SEM) and relative abundances (%) in the back reef habitat as measured by replicate visual transect censuses conducted between 0800 and 1600 on four sampling dates. April 1982 June 1982 November 1982 March 1983 (n = 50) (n =8) (n =6) (n =6) Herbivore species No./400 m2 % No./400 m2 % No./400 m2 % No./400 m2 % Acanthurus bahianus 72.5? ? ? ? Scarus iserti 20.0? ? ? ? Sparisoma chrysopterum 19.1? ? ? ? Acanthuruscoeruleus 7.8? ? ? ? Sparisoma viride 9.7? ? ? ? Sparisoma rubripinne 3.5+? ? ? ? Otherst 13.4? ? ? ? Total ? ? ? ? 11.9 t Includes Acanthurus chirurgus, Scarus vetula, Sparisoma aurofrenatum, and juvenile Sparisoma spp.

6 September 1986 HERBIVORY ON A TROPICAL REEF 187 Tobacco Reef (site 3, Fig. 1B): This section of the cinity of grazing trials in any of the study sites, and it Belizean barrier reef begins ; 1 km north of Carrie Bow is assumed that measured rates of consumption were Cay. Dense stands of Sargassum polyceratium var. not confounded by differences among habitats in backovatum (Collins) Taylor and Turbinaria turbinata (L.) ground availability of these plant species. Kuntze extended along the length of Tobacco Reef m behind the barrier reef crest. The shallow-water form Effects of fish herbivory in the of Lobophora variegata (Lamouroux) Womersley (see back reef habitat Norris and Bucher 1982) was also abundant on coral An experimental reduction of grazing intensity was rubble. conducted from March to June 1983 to examine the Curlew Bank (site 4, Fig. 1 B): Several beachrock sec- role of herbivorous fishes in maintaining the algal-turftions in shallow water near this submerged sand cay dominated benthic community in the back reef habitat. were densely covered with Gelidiella acerosa Feldman Thirty 50 x 70 cm quadrats were permanently marked & Hamel, Padina jamaicensis, and Turbinaria turbi- along a transect established through the back reef habnata. In nearby sand and rubble areas, Laurencia pap- itat, running parallel to and 8 m behind the reef crest illosa and Digenia simplex were common. (Fig. ic). On 31 March 1983 two large-scale herbivore exclusion fences were constructed, each measuring 10 x 5 METHODS m and consisting of galvanized chicken wire (2.5-cm mesh) supported by concrete-reinforcing rods. These Herbivore density and grazing intensity fences were anchored to the substratum and extended To examine differences in herbivory among shallow z0.5 m above the water surface. Each herbivore exreef habitats, herbivorous fish abundance and grazing clusion fence was situated to enclose eight 0.35-iM2 intensity were determined at each of the three mac- quadrats near one end of the transect (Fig. 1C). Fourroalgal sites and in the back reef habitat. Population teen unmanipulated 0.35-iM2 control quadrats were densities of parrotfishes and surgeonfishes were esti- distributed upcurrent of, downcurrent of, and between mated by visual censuses of individuals within 1 m on the two exclusion fences. These herbivore exclusion each side of a 50-m transect laid out within each study fences excluded all adult Acanthurus and all adult Sparsite. Visual censuses of these herbivorous fishes were isoma while allowing free movement of all Acanthurus conducted between 1000 and 1400 h over several days <60 mm standard length and Sparisoma <70 mm in March-May and December 1983 in the back reef standard length, as well as most Scarus iserti. By sub- (n = 16) and at each of the macroalgal sites (n = 8 for jective evaluation there were no apparent differences each). In the back reef habitat, diurnal variation in fish in abundances of small herbivorous fishes inside and density was monitored by conducting replicate visual outside the exclusion treatments. censuses (n = 10 for each 2-h period) during April Algal and coral species abundances were measured Additional details of herbivore censusing methods are as areal cover within experimental quadrats in March provided by Lewis and Wainwright (1985). and December 1982, in March 1983 immediately be- Herbivore grazing intensity was measured at each fore experimental manipulation (week 0), and then at study site during December 1983 using consumption 2, 4, 8 and 10 wk after construction of herbivore exrates of two plant species in a modification of the stan- clusion fences. Because of the wide size range of benthic dardized assay for herbivorous fish grazing developed organisms considered in this study, three scales of samby Hay (1981 c). The seagrass Thalassia testudinum pling were necessary to estimate benthic community and the red alga Acanthophora spicifera are preferen- structure. (1) Coral cover within each 0.35-iM2 quadrat tially consumed by scarid and acanthurid fishes, re- was measured photographically using a Nikonos cam- spectively (Lewis 1985). Grazing assays utilizing these two plants provided estimates of grazing due to these two components of the herbivore guild. Freshly collected Thalassia and Acanthophora were spun dry for 1 min (Copco salad spinner, Copco Incorporated, New York, New York, USA) weighed to the nearest 0.1 g, and placed in weighted clothespin holders as described by Hay (1981c). The precision of the spun wet mass estimates was? 3% (coefficient of variation for 10 replicate weighings). Plants (n = 8 for Thalassia, n = 8 for Acanthophora) were placed alternately 1 m apart in linear arrays within each study site at 1030 and collected at Plants were reweighed and consumption rates were expressed as percentage mass loss for Thalassia and Acanthophora over the 4-h period. Neither of these two plant species occurred in the vi- era with a 15 mm UW-Nikkor lens set on a PVC quadrapod. In the laboratory, coral percent cover was determined by projecting developed transparencies (Kodachrome 25) and measuring the proportion of the total quadrat area occupied by coral colonies using a LI-COR Model 3100 area meter. (2) Areal cover of algal turf and macroalgal species was estimated in the field by determining species occurring directly below a single array of 100 stratified random points arranged on two superimposed (to avoid parallax) monofilament grids. Plant height off the substratum operationally defined the categories of algal turf (plants < 2 cm height) and macroalgae (plants > 2 cm height); this distinction allowed different life history stages or morphologies of a single algal species to be placed in different categories. Bare sand and coral rubble substratum were recorded

7 188 SARA M. LEWIS Ecological Monographs Vol. 56, No. 3 as available space. All macroalgae and most algal turf rats at 8 and 10 wk after initiation of the experiment. species with filament diameters > 300,um were readily identifiable in situ with periodic supplemental laboratory identifications. (3) Some smaller algal turf species were not identifiable in the field, and their abundance Both groups of micrograzer showed patchy distributions, and no significant differences were found between herbivore exclusion quadrats (n = 16) and controls (n = 14) at either sampling date (Cerithium density was estimated by presence/absence in turf subsamples. At each of the five sampling dates beginning in March 1983, a 3-cm2 area of substratum with associated algal turf was collected along the 70-cm midline of each quadrat and later examined with a dissecting microscope. These smaller turf species represented minor components of algal turfs by areal cover, and species present in a subsample were arbitrarily assigned an abundance of 0.25%. Subsampled turf species along with other turf species having filament diameters < 300,um are hereafter collectively termed microturfs (see Table 1 for microturf species composition). For macroalgae, additional measures of abundance included plant density (number of individuals per quadrat), maximum canopy height, and presence/absence within experimental quadrats. Primary references for algal taxonomy were B0rgesen ( ), Taylor (1960), and Norris and Bucher (1982). Voucher specimens of algal species were preserved in 4% buffered Formalin in seawater, and have been deposited in the Algal Collection of the United States National Herbarium, Smithsonian Institution, Washington, D.C. Several potential artifacts of this experimental design were examined. Measurements of water flow immediately inside and outside exclusions in the vicinity of control quadrats were made under a range of ambient flow conditions (2-22 cm/s) using a General Oceanics Model 2030-R2 current meter. There was no measur- able effect of herbivore exclusion fences on water flow (P >.5, t test of paired comparisons with 9 df, t = 0.61). Exclusion fences were regularly cleaned and checked daily for damselfishes, which occasionally mi- grated into exclusion treatments and were removed. Roofless herbivore exclusion fences were assumed to have negligible light-shading effects. Increased densities of micrograzers (including small gastropods, decapods, and microcrustaceans) represent a potentially confounding factor in the interpretation of experimental manipulations involving caging treatments (Dayton and Oliver 1980, Brawley and Adey 1981). The mesh size of herbivore exclusion fences used in this study was chosen to allow free passage of several labrid species that are fish predators on micrograzers. The wrasses Thalassoma bifasciatum and Halichoeres bivittatus, two important predators on gastropods, decapods, and small crustaceans (Randall 1967), moved freely through exclusion fences and were commonly observed feeding within exclusions. The possibility of an artifactual change in densities of two common micrograzers, the gastropod Cerithium literatum and hermit crabs occupying discarded Cerithium shells, was examined directly by measuring densities in all experimental quad- at 10 wk within exclusions [X? 1 SEM]: 1.13? 0.51 individuals per quadrat; within controls: 1.11? 0.47 individuals per quadrat; P >.5, t test. Hermit crab density at 10 wk within exclusions: 0.50? 0.24 individuals per quadrat; within controls: 0.64? 0.35 individuals per quadrat; P >.5, t test). Additional indirect evidence that micrograzer densities were not abnormally elevated was a greater abundance of filamentous algal epiphytes on plants collected from herbivore exclusions than from controls at 10 wk. Macroalgal transplant studies To determine the effects of herbivorous fish grazing on macroalgal biomass, plants were transplanted from macroalgal sites into the back reef habitat. Spun wet masses were determined for freshly collected plants, and specimens placed in weighted clothespin holders were randomly assigned to one of the following experimental treatments: (1) plants transplanted into the back reef exposed to herbivore grazing, (2) plants transplanted into the back reef protected by 20 x 20 x 50 cm cages constructed of 0.5-cm mesh hardware cloth that excluded all herbivorous fishes, or (3) plants transplanted back to their original collection site exposed to ambient herbivore grazing. All plants were set out at 0830, collected at 1630, and reweighed. Data analysis The large-scale herbivore exclusion fences used in the present experiment were designed to minimize experimental artifacts often associated with small, replicated exclosure treatments, such as shading and use of cages as refuges by small grazers. However, exper- imental quadrats were not strictly independent replicates because random assignment of quadrats to treatments was not possible (i.e., in the terminology of Hurlbert 1984, there was pseudoreplication). Seriously biased estimation of potential treatment effects may result from this design if spatially segregated groups of quadrats differed in some important initial attributes, in response to experimental treatments, or in response to chance events in the course of the experiment. At the outset of the experiment in March 1983, comparison of species abundances revealed no significant differences in initial species abundances between quadrats assigned to herbivore exclusions and controls; in separate Model I analyses of variance (ANOVA) on 18 species (see Results), F values ranged from F[1,28] = 3.73 (P =.064) to F[1,28] = 0.06 (P =.80). An additional analysis using two-way Model I ANOVA was conducted to examine possible location effects on individual species responses after 10 wk. Exclusion areas and controls were divided into two blocks according

8 September 1986 HERBIVORY ON A TROPICAL REEF 189 TABLE 3. Species composition and abundances of acanthurid and scarid fishes at four shallow reef habitats, as determined from visual transect censuses conducted between 1000 and 1400 in March-May and December Values given are numbers of individuals per 100 m2 (X? SEM). Macroalgal sites Herbivore group Back reef Curlew Bank Tobacco Reef Lagoon Adults Acanthurus bahianus 10.4? ? ? 0.2 0? 0 Acanthurus coeruleus 2.4? 0.3 0? 0 0? 0 0? 0 Acanthurus chirurgus 0? 0 0? 0 0.5? 0.5 0? 0 Sparisoma chrysopterum 2.9? ? 0.7 0? 0 0? 0 Sparisoma rubripinne 1.8? 0.2 0? 0 0? 0 0? 0 Sparisoma viride 1.0? 0.4 0? 0 0? 0 0? 0 Sparisoma radians 0? 0 0.3? ? 0.6 0? 0 Scarusiserti 7.7? 1.1 0?0 0?0 0?0 Total adultst 26.5? ? ? 1.0 0? 0 Juvenilest Acanthurus 5.2? ? ? ? 0.4 Sparisoma 3.3? ? ? 0.7 0? 0 Scarus 0? 0 0.7? ? 1.5 0? 0 Total juvenilest 8.5? ? ? ? 0.4 Number of transects t Underlining indicates homogeneous subgroups by Dunn's multiple comparison procedure (a =.05). t Juveniles defined as: Acanthurus <70 mm total length (TL), Scarus <50 mm TL, Sparisoma (except S. radians) <100 mm TL, S. radians <30 mm TL. to position along the northern or southern portion of the transect. These analyses indicated a significant location main effect for only 1 of 18 benthic species (for Gelidium, F[3,26] for location = 15.54, P =.0005: for the remaining 17 species, values for location effects ranged from F[3,26] = to F[3,26] = 2.05, with corresponding probabilities from P =.92 to P =.16). Since there appeared to be no systematic bias due to quadrat location on the spatial scale examined in this experiment, results are presented as means of herbivore exclusion quadrats (n = 16) and controls (n = 14). In the herbivore exclusion experiment, benthic community structure for each quadrat at each sampling date was represented as a vector of species abundances. Taxonomically closely related algal species and several small algal turf species were pooled into six functional groups for analysis (species composition of these groups is indicated in Table 1): Halimeda, Valonia, Gelidium, articulated corallines, crustose corallines, and microturfs. Species abundance data (proportionate cover data) were angularly transformed (Bartlett 1947) prior to analysis to reduce heteroscedacity. Species responses within the benthic community were analyzed using multivariate analysis of variance (MANOVA) since species abundances are potentially interdependent. Univariate analyses were conducted for each species to complement interpretation of multivariate results, although there is an increased likelihood of type I error accumulating from multiple tests. Multivariate analysis used principal components analysis (PCA) of the sample variance-covariance ma- trix of transformed species abundances. PCA allowed the data on species abundances within the benthic com- munity to be summarized by a much smaller set of derived variables (principal components). Principal components represent linear combinations of the original species variables, with coefficients determined by the elements of the eigenvectors associated with the largest eigenvalues of the sample covariance matrix. Principal component scores for each quadrat at each sampling date provided a concise description of benthic community structure. Product-moment correlations of PCA scores with species abundances allowed interpretation of principal components with respect to original species variables. Although PCA is most often used as a descriptive technique, PCA scores can also be used as variables in statistical comparisons of dif- ferences in community structure between experimental treatments. In the present study, two multivariate analyses of variance were used to determine whether benthic community structure differed significantly between herbivore exclusions and controls at the initiation and again at the conclusion of the experiment. MANOVAs were performed on the first three principal compo- nents, and significance was assessed using Wilks' lambda criterion (Morrison 1976, Timm 1975) as a test statistic. Univariate analyses of variance (Model I ANOVA) were performed for each species to test the null hypotheses of identical means between herbivore exclusions and controls at the outset of the experiment. For later sampling dates, analyses of covariance (AN- COVA) were performed for individual species, using initial species abundance as a covariate. Covariance analysis allowed variation among quadrats in initial species abundances to be removed from the error vari-

9 190 SARA M. LEWIS Ecological Monographs Vol. 56, No A B reef site than at any of the three macroalgal sites (P < 80 * Back reef? 60 Curlew Bank 0 ) Tobacco Reef CD 40 :I 12 Lagoon rn , SNK tests on rank sums), as measured both by Thalassia consumption (which reflects parrotfish grazing mostly due to large Sparisoma) and by Acanthophora consumption (primarily due to surgeonfishes). These results indicate marked spatial heterogeneity in herbivorous fish abundance and grazing intensity, and suggest that shallow macroalgal-dominated habitats represent spatial refuges from herbivorous fish grazing. Thalassia Acanthophora Response to experimental FIG. 3. Variation among shallow subtidal habitats in grazreduction of herbivory ing intensity on two plant species used to assay herbivory The benthic community in the back reef habitat at (percentage mass loss, X + SEM): (A) Thalassia (n = 8). (B) the beginning of the herbivore exclusion experiment Acanthophora (n = 8). Grazing rates on both Thalassia and was characterized by a high proportion of available Acanthophora were significantly greater in the back reef habitat than at all other sites (P <.01, SNK tests on rank sums). space (22% of total substratum area; Table 4). Algal turfs (plants <2 cm height) were initially major space occupants in the back reef benthic community, totalance. All statistical analyses used Statistical Analysis ling :56% areal cover. At week 0 the major groups System Version 82.3 (SAS 1982), installed at the Tri- comprising algal turfs were Gelidium, Valonia, articangle Universities Computation Center, Research Tri- ulated corallines, Digenia, Dictyota, Gelidiella, and Paangle Park, North Carolina. dina. Initial macroalgal abundance was low, consisting Differences in herbivore density and grazing inten- only of Halimeda (-2.5% of cover; Table 4). Crustose sity among sites were analyzed using nonparametric coralline algae comprised 5% of total substratum area, Kruskal-Wallis significance tests on ranked variates be- and the coral Porites astreoides occupied 16% of total cause assumptions of analysis of variance models were area. There were no significant differences in species violated by extreme nonhomogeneity of variances. relative abundances between herbivore exclusions and Treatment differences in macroalgal transplant exper- controls at the beginning of the experiment (all P > iments were also analyzed using Kruskal-Wallis tests..05, individual ANOVAs; Table 4). Multiple comparison tests were conducted using the Experimental reduction of herbivorous fish grazing nonparametric analogue of the Student-Newman-Keuls rapidly altered total macroalgal abundance (Fig. 4), as procedure (SNK on rank sums; Zar 1984) for equal well as individual species abundances within the bensample sizes, and Dunn's (1964) multiple comparison thic community (Table 4). During a 12-mo period beprocedure on average ranks for unequal sample sizes. fore experimental exclusion of herbivores, macroalgal Both tests control experimentwise type I erro rates. cover in all quadrats remained at /2%(Fig. 4). After RESULTS 10 wk of reduced herbivory total macroalgal cover had increased to 30% within exclusions, while macroalgal Herbivore abundance and grazing intensity cover in controls remained essentially unchanged. The herbivorous fish guild present at macroalgal sites differed markedly from that of the back reef habitat in Several brown algal species showed increased abundances in response to experimentally reduced herbivoboth total adult abundance and species composition ry. Padina jamaicensis was present in low abundance (Table 3). The back reef habitat was characterized by in algal turfs at the beginning of the experiment (_ 2% high densities of adults of several Acanthurus, Scarus, total area; Table 4). The turf morphology of Padina and Sparisoma species. Acanthurus was the most abun- consisted of prostrate, branching plants closely adherdant genus in the back reef (51% of all individuals), ent to the substratum. Padina exhibited dramatically followed by Sparisoma (26%) and Scarus (22%). Mac- increased abundance following reduced herbivory roalgal sites were characterized by significantly lower within exclusions (Fig. 5A). By the 10th wk of the adult herbivorous fish densities than the back reef experiment, Padina occupied 23% of the total sub- (P <.001, Kruskal-Wallis test on total adult density; stratum area in herbivore exclusions, representing a multiple comparison results are shown in Table 3). highly significant increase relative to controls (P = Adult Sparisoma radians, a small parrotfish often found.0001, ANCOVA; Table 4). Padina growth under rein seagrass beds, occurred only at Tobacco Reef and duced herbivory was accompanied by a change in mor- Curlew Bank sites. Juveniles predominated the her- phology from a prostrate, turf morphology to the more bivorous fish guild at the macroalgal sites (Table 3). Patterns of grazing intensity on transplanted Thatypical macroalgal form with erect, fan-shaped fronds. Dictyota bartayresii (Fig. 5B), another brown algal lassia and Acanthophora plants reflectedifferences species present in low abundance at the outset of the among habitats in herbivorous fish abundance (Fig. 3). experment, also increased significantly within herbi- Grazing intensity was significantly higher at the back vore exclusions relative to controls by 10 wk (P =.0002,

10 September 1986 HERBIVORY ON A TROPICAL REEF 191 TABLE 4. Percentage cover in herbivore exclusions and controls at initiation of experiment (week 0) and after 10 wk (untransformed X? SEM; herbivore exclusion, n = 16; control, n = 14). Week 0 Week 10 Species group Control Exclusion Pt Control Exclusion Pt Available space 22.3? ? ? ? Porites 16.3? ? ? ? Gelidium 13.1? ? ? ? Valonia 8.9? ? ? ? Crustosecorallines? 5.4? ? ? ? Coelothrix irregularis 5.2? ? ? ? Articulated corallines? 5.1? ? ? ? Digenia simplex 4.1? ? ? ? Microturfs? 3.4? ? ? ? Halimeda 2.6? ? ? ? Dictyota bartayresii 4.7? ? ? ? Gelidiella acerosa 3.8? ? ? ? Padina jamaicensis 1.9? ? ? ? Turbinaria turbinata ? ? Dictyota cervicornis ? t Significance levels given for treatment effects at week 0 are from individual ANOVA performed on angularly transformed proportionate abundances; Ho: C = AEt Significance levels at week 10 are from individual ANCOVA using initial abundances as covariates; Ho: Atc = UE*? See Table 1 for species composition of these functional groups. ANCOVA; Table 4). Dictyota cervicornis (Fig. 5C) was initially absent in the back reef habitat and remained absent throughouthe experiment in controls. Within herbivore exclusions, however, D. cervicornis increased significantly (P =.0004, ANCOVA; Table 4), apparently through spore recruitment and subsequent vegetative growth. Several algal species exhibited responses to reduced herbivory with higher frequency of occurrence in experimental quadrats, increased plant height, or altered reproductive status after 10 wk (Table 5). A number of species showing increased frequency in herbivore exclusion quadrats remained absent in controls throughouthe experiment (Dictyota cervicornis, Sargassum polyceratium, Ceramium nitens, Laurencia papillosa, and Caulerpa racemosa). Many species exhibited greater maximum plant height in exclusions relative to controls at 10 wk (Table 5), which in both Padina jamaicensis and Digenia simplex was accompanied by major morphological changes (S. M. Lewis et al., personal observation). Three algal species (Padina jamaicensis, Digenia simplex, and Gelidiella acerosa) also showed altered reproductive status under reduced herbivory, as determined by presence of tetrasporangial plants; none of these species was ever found reproductive in controls (Table 5). The brown alga Turbinaria turbinata showed marked increases in both spore recruitment (Fig. 6) and plant growth (Fig. 7) under reduced herbivory. Before initiation of the experiment Turbinaria occurred in both herbivore exclusions and controls in similarly low densities, and only as newly germinated sporelings: at week 0 Turbinaria density in exclusions (X? SEM) was sporelings per quadrat, and in controls sporelings per quadrat (P >.5, t test). These sporelings generally reached maximun heights of 0.5 cm, with filiform, recurving leaves. New sporelings were distinguished by the absence of the pyramidal leaves characteristic of older plants. Successful Turbinaria spore recruitment increased under reduced herbivory, as measured by density of new Turbinaria sporelings in herbivore exclusion and control quadrats (Fig. 6). At 10 wk exclusions exhibited significantly greater Turbinaria sporeling density than did controls (.02 < P <.05, Mann-Whitney U test). Turbinaria plants grew rapidly once established in herbivore exclusions, as estimated by a plant size index determined by sum- ming widths of all pyramidal leaves for each plant (Fig. 7). At 10 wk values of this Turbinaria size index were significantly higher in herbivore exclusions than in controls (.01 < P <.02, Mann-Whitney U test), and in- U <5 OU 30-.i..EXCLUSION E ~~~~~~~~~~~~~~CONTROL MARCH DECEMBER MARCH APRIL APRIL JUNE JUNE FIG. 4. Total macroalgal abundance (plants > 2 cm height) as percent cover in the back reef habitat before and following reduction of herbivorous fish grazing. Herbivore exclusion treatments were established on 31 March 1983; controls were nearby unmanipulated quadrats. Data are X? SEM for herbivore exclusion (n = 16) and control (n = 14) quadrats.

11 192 SARA M. LEWIS Ecological Monographs Vol. 56, No. 3 As a partial test of whether plants appearing under reduced herbivory represented recruitment of spores or vegetative growth of established plants, five cinderblock settling plates were set out in March 1983 in the....*' B... 5 v _ ~~~~~CNROL back reef with the top surfaces (20 x 40 cm) protected from fish grazing by 0.5-cm wire mesh cages. By the conclusion of the herbivore exclusion experiment in EXCLUSION mid-june, recruitment and growth of Dictyota cervi- 10 cornis, Turbinaria turbinata, and Sargassum polycera- - 4 Dictyota bartayresis tium had occurred on these settling blocks. While successful recruitment onto settling blocks suggests spore 0 10 B availability for these algal species in the back reef habitat, increased species abundances within herbivore exclusions may have been due either to spore recruitment or to vegetative growth of previously established turf CONTROL... XCLUSION plants The availability of unoccupied substratum showed a steady decline under reduced herbivory, from 19% (B week ityt 0 (before ararsl.()dictyota cervicornis 8 TE~~~~~~XCLUSION to 4% of total substratum area within herbivore exclusions (Fig. 8A). At 10 wk exclusions showed significantly lower available space compared to controls (P =.0001, ANCOVA; Table 4). Within individual quadi... CONTROL rats this decline in available space over 10 wk was 0 T highly negatively correlated with change in total mac roalgal abundance (r = -0.64, 28 df, P =.0002). Sev- WEEKS eral algal species, particularly Padina jamaicensis, Dic- FIG. 5. Percent cover (X? SEM) for algal species in her- tyota bartayresii, Gelidiella acerosa, and Dictyota bivore exclusion (n = 16) and control (n = 14) quadrats at cervicornis, rapidly occupied bare sand or rock subweek 0 (before construction of exclusion fences) and following strata. Abundances of crustose coralline algae and mireduction of fish grazing intensity. (A) Padina jamaicensis. croturfs (Fig. 8B) and Valonia also declined signifi- (B) Dictyota bartayresii. (C) Dictyota cervicornis. cantly in herbivore exclusions relative to controls by 10 wk (all P <.01, ANCOVA; Table 4). Increased canopy heights (Table 5) and rapid growth of macroalgal Padina, Dictyota, Gelidiella, and Turbinaria enabled plants of these species to overgrow smaller algal dividual plants had attained heights up to 7 cm within exclusions. However, this size increase was not reflected in increased Turbinaria abundance as measured by areal coverage (P =.21, ANCOVA; Table 4), partly because plants grew erect from a single holdfast occupying little horizontal space. turf species, crustose corallines, and portions of Porites colonies. Field observations of these overgrowth interactions indicated that overgrowth by macroalgae was frequently associated with death of underlying crustose TABLE 5. Frequency of occurrence, maximum plant height off substratum, and reproductive status of algal species at 10 wk in herbivore exclusion (n = 16) and control (n = 14) quadrats. Frequency (%) Maximum height (cm) Reproduction Control Exclusion Control Exclusion Control Exclusion Phaeophyta Dictyota cervicornis no Dictyota bartayresii no no Padina jamaicensis no tetraspores Sargassum polyceratium var. ovatum no Turbinaria turbinata no no Rhodophyta Ceramium nitens no Digenia simplex no tetraspores Gelidiella acerosa no tetraspores Laurencia papillosa no Chlorophyta Caulerpa racemosa no Caulerpa sertularioides var. farlowii no

12 September 1986 HERBIVORY ON A TROPICAL REEF 193!_ Turbinaria turbinata algal turf species Gelidium and articulated corallines. At the beginning of the experiment, community struc- < EXCLUSION ture within herbivore exclusion quadrats closely re- (r) 2- I I CONTROL sembled that of control quadrats (Fig. 10). Under re- (I duced herbivory, however, a new community trajectory developed that resulted in marked divergence from this 0, initial structure by 10 wk. Herbivore exclusion quada- rats at 10 wk showed higher values for both first and second components, representing a shift in community structure to increased abundances of macroalgal species WEEKS and concomitant reduction of several algal turf species, Halimeda, and crustose coralline algae. FIG. 6. Density (X + SEM) of newly germinated Turbinaria turbinata sporelings (before development of first pyramidal Multivariate analysis of variance of principal comleaves) in herbivorexclusion (n = 16) and control (n = 14) ponents was used to determine whether benthic comquadrats before and following reduction of fish grazing inten- munity structure differed significantly between herbisity. vore exclusions and controls (Table 7). Before experimental reduction of herbivory, no significant difference in overall community composition was found corallines, Gelidium, Valonia, and Halimeda, indicated by visible bleaching of plant thalli. After 10 wk of reduced herbivory, macroalgal Padina, Gelidiella, Turbinaria, and Dictyota plants had also overgrown portions of Porites colonies, resulting in a significant rebetween exclusions and controls (P =.89). However, after 10 wk of reduced herbivory, a highly significant difference in community composition had developed between the herbivore exclusions and controls (P <.0001). duction in Porites abundance within herbivore exclusions relative to controls (P =.0002, ANCOVA; Table 4). Coral polyps were killed and surrounding skeleton was bleached in areas of Porites colonies overgrown by these plants (Fig. 9). Increased macroalgal abundance in individual quadrats over the course of the experiment was significantly inversely correlated with changes in abundance of several benthic species that were overgrown (with Porites: r = -0.65, P =.0002; with Gelidium: r = -0.51, P =.004; with Valonia: r = -0.51, P =.004; with microturfs: r =-0.40, P =.04; with crustose corallines: r = 0.61, P=.0003; 28 df in each case). Species diversity within the benthic community was initially similar in herbivore exclusions and controls: at week 0 Shannon-Wiener H' (X? SEM) for exclusions (n = 16) = 2.83? 0.05, for controls (n = 14) H' = 2.77? At 10 wk, species diversity had increased within herbivore exclusions relative to controls (for exclusions H' = , for controls H' = 2.88? 0.05; P =.0004, t test). Multivariate analysis of response to reduced herbivory The principal components analysis of benthic community structurexplained 59% of the total variance in species abundances in the firsthree principal components (Table 6). First and second principal components represented decreases in algal turf, Halimeda, and coralline algal abundances concomitant with increased abundances of Padina jamaicensis, Dictyota cervicornis, Dictyota bartayresii, Gelidiella acerosa, Turbinaria turbinata, and Coelothrix irregularis. The third principal component contrasted abundances of crustose corallines and Halimeda with those of the Reintroduction of herbivorous fishes At the conclusion of the herbivore exclusion experiment on 13 June 1983, fences were carefully dismantled and herbivore exclusion areas became available to herbivorous fishes. Within several hours scarid fishes were observed feeding on Padina, Turbinaria, and Dictyota cervicornis that had been within the exclusion areas, and acanthurids were seen grazing Gelidiella and Dictyota cervicornis. Within 48 h there was evidence of intense grazing on some algal species; the frequency of occurrence of plants within former exclusion quadrats decreased from 100% to 0% for both Dictyota E6- Turbinaria turbinata 13 x - 13 j1 j EXCLUSION Z w 4- C,,, < ~~~4 2,,' z ' ~~~~ ^ CONTROL WEEKS FIG. 7. Turbinaria plant size index (X? SEM) for herbivore exclusion and control quadrats before and following reduction of fish grazing intensity. Plant size index was determined by summing widths of pyramidal leaves on each plant (excluding new sporelings). Total number of plants (n) shown above each data point.

13 194 SARA M. LEWIS Ecological Monographs Vol. 56, No. 3 TABLE 6. Summary of principal components analysis (PCA) of transformed species abundances. Entries are Pearson product-moment correlation coefficients between species A abundances and PCA scores with associated probability levels (n = 60, pooled week 0 and week 10 observations) o 1 1''- De ) U Microturfs + Corallines 20- CONTROL 10 B.... i EXCLUSION WEEKS FIG. 8. Percent cover of (A) Available space, and (B) Microturfs (<300 gum diameter) and crustose coralline algae. Data are X? SEM for herbivorexclusion (n = 16) and control (n = 14) quadrats before and following reduction of fish grazing intensity. cervicornis and the macroalgal form of Padina, and from 94% to 6% for Turbinaria. Thus, the reintroduction of herbivorous fishes resulted in rapid removal of some macroalgal species that had become established within the exclusion treatments. Macroalgal transplant studies Algal species predominant in macroalgal sites showed highly significant biomass losses when transplanted into the back reef and exposed to herbivorous fish grazing, compared to control plants protected from herbivory (Table 8). During 8-h transplant trials, mean biomass loss for macroalgae exposed to herbivorous fishes ranged from 44 to 100% of original plant wet biomass. For several macroalgal species (Laurencia papillosa, Dictyota cervicornis, Padina jamaicensis, and Turbinaria turbinata), all replicates exposed to herbivores were completely consumed. There were no significant differences in biomass loss between plants transplanted back to their original habitats and plants that were protected from fish grazing in the back reef (Table 8), indicating that macroalgal sites represent local reductions in herbivory on these algal species. DISCUSSION Herbivory and benthicommunity organization within the back reef habitat The results of this study indicate that herbivory may be of fundamental importance in determining algal and Principal component Species group Padina jamaicensis 0.91*** 0.30* 0.08 Dictyota cervicornis 0.77*** Dictyota bartayresii 0.72*** Gelidiellacerosa 0.60*** -0Q55*** Turbinaria turbinata 0.43*** Coelothrix irregularis 0.28* 0.34** -0.25* Valonia *** 0.01 Crustose corallines *** 0.47*** Articulated corallines -0.31* 0Q37** -0.37** Porites Microturfs -0.34** -0.41*** Halimeda -0.37** *** Digenia simplex -0.51*** 0.74*** 0.02 Gelidium -0.57*** *** % of total variance *01 < P c 05; **.00l < P 01; ***P 00 1 **.4.:N. ri,~~~~~~~~~~~~~~~~l.1 FIG. 9. Overgrowth of the coral Porites astreoides by macroalgae in the back reef habitat under experimental reduction of herbivory by a fence extending above the water surface: (A) Macroalgae (including Padinajamaicensis) growing over Porites colony after 10 wk of reduced herbivory. (B) Fortyeight hours following reintroduction of herbivorous fishes, the macroalgae were completely consumed and the underlying bleached and dead portions of the Porites colony were revealed. Scale bar in (B) represents 2 cm.

14 September 1986 HERBIVORY ON A TROPICAL REEF A 0 CONTROL WEEKO A EXCLUSION WEEK A CONTROL WEEK 10 A EXCLUSION WEEK 10 Z o A A z A A AA 0 A :11E 0 A O 0 A A U ~~~~~L0AA A A 0A 0 A_} * I I I IA PRINCIPAL C IA) Al COMPONENTi z Q AA -0.2 A A 0 6 A FIG. 10. Patterns of benthicommunity structure within individual herbivorexclusion and control quadrats represented by first and second principal component scores (see Table 6 for species correlations with PCA scores). coral species abundances within the back reef habitat. Experimental reduction of grazing intensity by adult acanthurids and scarids resulted in a rapid and dramatic shift in benthic community structure. After 10 wk of reduced herbivory, Padina jamaicensis, Dictyota bartayresii, Gelidiella acerosa, and Dictyota cervicornis represented 510% of total algal cover. Total macroalgal abundance increased significantly and was correlated with decreased abundances of algal turfs, crustose coralline algae, and the coral Porites astreoides. Under conditions of reduced herbivory, portions of Porites colonies were overgrown and subsequently killed by some macroalgal species, indicating that fish herbivory may mediate interactions among coral and algal species. Several algal species initially absent from this back reef habitat showed successful spore recruitment and subsequent growth under experimentally reduced herbivory, demonstrating that these species may be excluded from the back reef by herbivory, not by lack of spore availability or physical conditions unsuitable for plant germination and growth. Herbivorous fish grazing ap- pears to maintain a tropical benthic assemblage dominated by algal turfs and crustose coralline algae by reducing abundances of macroalgal species with superior overgrowth abilities. The diverse algal turfs characteristic of many reef habitats represent herbivore-tolerant benthic assemblages consisting of filamentous algal species able to persist under high grazing intensity. Many of these algal turf species responded rapidly to experimentally reduced herbivory, exhibiting increased species abundances as well as altered morphology and reproductive status. While the present study does not provide a direct evaluation of competitive rankings among benthic species, potential competitive dominance by macro- algae might be inferred from greater canopy heights of macroalgae, as well as from inverse correlations in abundance between macroalgae and several other benthic groups under conditions of reduced herbivory. If we accept the premise that macroalgae may represent potential competitive dominants in this tropical benthic system, then continued reduction of herbivory TABLE 7. Principal component scores (X? SEM) for herbivore exclusion (n = 16) and control (n = 14) quadrats before and after 10 wk of reduced fish herbivory. Principal component Week 0 Exclusion -0.13? ? ? 0.03 Control -0.13? ? ? 0.02 Week 10 Exclusion +0.31? ? ? 0.03 Control -0.08? ? ? 0.03 MANOVA test criteria: Week 0 Wilks' X = P =.89 Week 10 Wilks'X = P <.0001

15 196 SARA M. LEWIS Ecological Monographs Vol. 56, No. 3 TABLE 8. Results of macroalgal transplant studies: percentage change in biomass of plants under three experimental treatments during 8-h trials. Data for some species from Lewis (1985). Treatmentt Exposed to Protected from herbivores in herbivores in Exposed in back reef back reef original habitat Macroalgal species Collection site X? SEM n X? SEM n X? SEM n Rhodophyta Coelothrix irregularis pomacentrid territories -86.2? 7 12 ** -6.0? 5 7 -: Digenia simplex Lagoon -96.5? 3 13 ** -7.6? 3 5 NS -1.7? 2 7 Gelidiella acerosa Curlew Bank -44.2? 6 15 ** -10.0? 5 12 Laurenciapapillosa Lagoon ? 0 10 ** -2.5? 1 5 NS -7.1? 2 8 Phaeophyta Dictyota cervicornis experimental exclusions ? 0 5 ** -9.4? 4 5 Lobophora variegata Tobacco Reef -99.8? 1 22 ** -13.5? 3 16 NS -3.4? 1 10 Padina jamaicensis Lagoon ? 0 25 ** -1.1? 5 5 NS -30.1? 17 7 Sargassum polyceratium Tobacco Reef -87.2? 5 25 ** -3.4? 1 18 NS -3.7? 2 12 Turbinaria turbinata Tobacco Reef ? 0 17 ** -2.9? 1 16 NS -3.7? 1 17 t Differences between adjacent means tested by Dunn's test on average ranks: ** P <.01; NS, P >.05. t - indicates treatment not conducted. might be predicted to lead to increasing dominance of the back reef benthic community by a few macroalgal species. However, cautious extrapolation from results of the present study is necessary due to the short-term nature of this investigation, and in light of limited knowledge of competitive relationships within this tropical benthic assemblage. Alternative hypotheses for community trajectories under long-term reduction of grazing intensity include eventual reduction of macroalgal abundance by senescence or detachment due to physical disturbances, including heavy wave action in storms. In addition, other potentially important determinants of response to reduced herbivory include initial community composition, local nutrient levels, and temporal patterns of spore and propagule availability for various benthic species. This study provides an experimental evaluation of responses of a Caribbean reef community to acanthurid and scarid grazing. The results complement those of other investigations on effects of tropical herbivores on subtidal benthic assemblages. A trend toward dominance by a few of the same macroalgal species (Padina jamaicensis, Turbinaria turbinata, Dictyota sp.) was observed following experimental removal of the sea urchin grazer Diadema antillarum from patch reefs in St. Croix (Sammarco et al. 1974). Similar reduction of grazing by echinoids in Jamaica resulted in algal species overgrowing adult coral colonies (Sammarco 1982b). Studies on artificial substrates have indicated that herbivorous fish grazing increases coral recruitment and early survivorship (Birkeland 1977, Brock 1979), and growth of crustose corallines was also found to be enhanced by fish grazing (Wanders 1977). Additional descriptive evidence has suggested that reef eutrophication may increase algal growth rates and result in extensive macroalgal overgrowth and mortality of coral colonies (Fishelson 1973, Banner 1974). Experimental studies of guilds at several trophic levels have indicated that guild structure may be maintained below competitive equilibrium by consumers that reduce abundances of potentially dominant prey (reviewed by Connell 1975, Menge and Sutherland 1976, Harper 1977, Lubchenco and Gaines 1981, Morin 1983). Although much of this work has been done on relatively simple systems involving single consumer species, recent studies on the organization of reef communities (Glynn 1976, Hay 1981 a, Wellington 1982, Hixon and Brostoff 1983), including the present study, suggest that similar ecological mechanisms may also be operative in complex and diverse tropical systems. Spatial patterns of herbivory Spatial heterogeneity in herbivore grazing appears to represent a biotically generated mechanism contributing to high regional diversity among reef habitats (see also Hay 1981 a, Gaines and Lubchenco 1982, Hay 1985). The spatial mosaic of benthic community composition observed among shallow habitats along the Belizean barrier reef corresponded closely to patterns of grazing intensity by herbivorous fishes. Several shallow habitats supporting dense stands of macroalgal species were found to represent spatial refuges from herbivory, with locally reduced densities and grazing intensities of adult acanthurid and scarid fishes. Algal species composition in the back reef habitat under ex- perimentally reduced herbivory showed a trend toward that of macroalgal-dominated habitats, associated with recruitment and growth of several macroalgal species. Spatial variation in herbivore grazing may act to maintain different benthic species assemblages under fundamentally distinct selective regimes. Similar local reductions in grazing intensity associated with distinct algal species assemblages have been found in other reef habitats. Hay (1981 a, b) and Hay

16 September 1986 HERBIVORY ON A TROPICAL REEF 197 et al. (1983) showed that algal species characteristic of deep sand plains and intertidal reef flats may be restricted from reef slopes by herbivory, and suggested that these species would represent potentially dominant competitors on the reef slope in the absence of herbivory. Grazing intensity may also vary on a microhabitat scale, and numerous studies have shown that territorial pomacentrids reduce grazing by other herbivorous fishes and thus provide microhabitat refuges for many algal species (Brawley and Adey 1977, Lobel 1980, Hixon and Brostoff 1983, Sammarco 1983). Both among-habitat and within-habitat variation in herbivory, coupled with potentially high rates of spore dispersal, might be expected to select for inducible plant defenses against herbivory (Hay 1984a). While tropical algal species exhibit many characteristics that may be interpreted as defenses against herbivory (reviewed by Norris and Fenical 1982, Hay 1984a, Littler and Littler 1984, Lewis 1985), few facultative algal defenses have as yet been identified. Some algal turf species in the present study exhibited morphological plasticity, which may have represented an induced response to different grazing regimes. These species, including Padina ja- maicensis, persist in a prostrate, turf morphology under high grazing intensity, but are able to respond rapidly to reduced herbivory through a morphological shift to an erect, macroalgal form. Macroalgal species characteristic of low-herbivory habitats were found in this study to be highly susceptible to grazing by herbivorous fishes. Other studies have indicated that many algal species characteristic of habitats with high grazing intensities are resistant to herbivorous fish grazing (Hay 1981 c, 1984b, Littler et al. 1983, Lewis 1985). These results are consistent with the hypothesis of an ecological and evolutionary trade-off in algal resource allocation either to potential competitive ability or to predator resistance, as has been suggested for many, taxonomically diverse assemblages ofprey species (Lubchenco 1978, Rhoades 1979, Littler and Littler 1980, Hay 1981 a, Lubchenco and Gaines 1981, Morin 1983). Factors affecting spatial distributions of herbivorous fishes Spatial variations across reef habitats in both fish grazing intensity (Vine 1974, Hay 1981c, 1984a, b, Hatcher 1982, Hay et al. 1983) and herbivorous fish abundance (Miller 1982, Russ 1984, Lewis and Wainwright 1985) have been described for several tropical reef locations, but the factors influencing habitat distributions of herbivorous fishes are not well understood. Intertidal reef flats and remote sand plains appear to act as temporal or spatial refuges from herbivory (Hay 1981 a, b, Lubchenco and Gaines 1981, Hay et al. 1983), but there is no a priori reason to expect reduced grazing in shallow subtidal areas dominated by macroalgal stands, such as those in the present study. Several hypotheses have been proposed for the occur- rence of similar shallow macroalgal stands throughout the Caribbean, including reduced grazer densities resulting from wave exposure and turbulence (Van den Hoek et al. 1975, Wanders 1976a, Adey et al. 1977, Conner and Adey 1977). However, macroalgal sites examined in the present study were sheltered from direct wave action by the barrier reef crest, yet still exhibited low densities of adult acanthurids and scarids. One factor limiting herbivore abundances in these areas may be a critical distance from shelter in nearby, topographically complex reef habitats; macroalgal sites ranged from 75 to 100 m behind the topographically complex reef crest, while the back reef habitat was directly adjacent to the reef crest. Proximity to suitable shelter was first recognized as a critical factor determining herbivore foraging ranges by Randall (1965), who described halos of bare sand surrounding patch reefs in tropical seagrass beds. This phenomenon was subsequently observed on deep sand plains adjoining reef slopes (Earle 1972, Hay 1981a). Several other fac- tors are also likely to mediate foraging ranges of herbivorous acanthurids and scarids, including predator density, abundance and nature of available food resources, and density of territorial competitors. Tropical herbivore guilds These experimental results may provide insight into some of the ecological consequences of variation in the composition of herbivore guilds on differentropical reefs. Many previous studies on Caribbean reefs have focussed on grazing by sea urchins, particularly Diadema antillarum (Ogden et al. 1973, Sammarco et al. 1974, Sammarco 1980, 1982a, b, Carpenter 1981). Although herbivorous fishes have been shown to represent an important selective force on tropical algae (Hay et al. 1983, Littler et al. 1983, Hay 1984a, Lewis 1985), there have been remarkably few experimental evaluations of the effects of acanthurid and scarid grazing on Caribbean reef communities. This is partially due to geographical differences among Caribbean reefs in the relative contributions of herbivorous fishes and sea urchins to total grazing pressure. Considerable variation in the composition of herbivore guilds appears to be associated with patterns of human fishing pressure (Hay 1984b). Grazing fishes represent dominant components of the herbivore guild on relatively undisturbed Caribbean reefs (Wanders 1977, Hay et al. 1983, Hay 1984b, Lewis and Wainwright 1985), while until recently Diadema grazing was more important on reefs subject to intense fishing pressure. During 1983 mass mortality of Diadema virtually eliminated this grazer on reefs throughout the Caribbean (Lessios et al. 1984). Results of the present study may be of particular interest in light of recent evidence of increased fish herbivory associated with reduced Diadema populations, perhaps as a compensatory response (Hay and Taylor 1985, Carpenter 1986; D. Morrison, personal communication).

17 198 SARA M. LEWIS Ecological Monographs Vol. 56. No. 3 In addition, the major role played by herbivorous West Indies: Pt. I. Chlorophyceae. Pt. II. Phaeophyceae. acanthurids and scarids in the organization of a Beli- Pt. III. Rhodophyceae. Dansk Botanisk Arkiv 1(1913): 1-158, 2(1914):1-66, 3(1920): zean back reef community supports the contention that Borowitzka, M. A Algae and grazing in coral reef the evolutionary origin and diversification of herbiv- ecosystems. Endeavour 5: orous fishes in the Eocene had important consequences Borowitzka, M. A., A. W. D. Larkum, and L. J. Borowitzka. for tropical benthic communities over geological time A preliminary study of algal turf communities of a (Vermeij 1977, Steneck 1983). Steneck (1983) has spec- shallow coral reef lagoon using an artificial substratum. Aquatic Botany 5: ulated that shallow reef communities in the Paleozoic Brawley, S. H., and W. H. Adey Territorial behavior and Mesozoic may have been dominated by large mac- of threespot damselfish (Eupomacentrus planifrons) inroalgal forests, and that the advent of herbivorous fish- creases reef algal biomass and productivity. Environmental es contributed substantially to the development of Biology of Fishes 2: modem reef assemblages. Although direct fossil evi- Brawley, S. H., and W. H. Adey The effects of micrograzers on algal community structure in a coral reef midence for or against Paleozoic macroalgal forests is not crocosm. Marine Biology (Berlin) 61: likely to become available, macroalgal overgrowth of Brock, R. E An experimental study on the effects of corals under experimentally reduced fish herbivory grazing by parrotfishes and role of refuges in benthicomprovides support for the role of herbivorous fishes in munity structure. Marine Biology (Berlin) 51: Burke, R. B Reconnaissance study of the geomorthe development and maintenance of modem reefs phology and benthicommunities of the outer barriereef dominated by scleractinian corals. platform, Belize. In K. Riitzler and I. G. Macintyre, editors. The Atlantic Barrier Reef Ecosystem at Carrie Bow Cay, ACKNOWLEDGMENTS Belize. Smithsonian Contributions to the Marine Sciences This paper is based on a dissertation submitted in partial 12: fulfillment of the Ph.D. requirements at Duke University. The Carpenter, R. C Grazing by Diadema antillarum members of my doctoral committee, Peter Klopfer, John (Philippi) and its effects on the benthic algal community. Sutherland, Stephen Wainwright, Henry Wilbur, Richard Journal of Marine Research 39: Searles, Donald Burdick, Mark Hay, and Jim Norris, all made Mass-mortality of a Caribbean sea urchin: many contributions to myriad aspects of this research. I also immediateffects on community metabolism and other thank Randy Baker (deceased), Regina Lewis, Peter Reinthal, herbivores. Proceedings of the National Academy of Sci- Barry Spracklin, and Peter Wainwright for invaluable field ences (USA), in press. assistance, and Katy Bucher, Suzanne Frederiq, Jim Norris,. In press. Partitioning herbivory and its effects on and Rick Searles for assistance in algal determinations. I am coral reef algal communities. Ecological Monographs. grateful to Jim Bohnsack, Mark Hay, Mark and Diane Littler, Connell, J. H Some mechanisms producing structure Thomas Michel, Jim Norris, and Klaus Riftzler for providing in natural communities. Pages in M. L. Cody and insight, advice, and encouragement throughout this study. C. J. Diamond, editors. Ecology and evolution of communi- H. Peterson, M. Hay, and two anonymous reviewersub- ties. Belknap Press, Cambridge, Massachusetts, USA. stantially improved earlier versions of this paper. 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