Coral Reefs (2007) 26:435–442

DOI 10.1007/s00338-007-0214-1

REPORT

Direct evaluation of macroalgal removal by herbivorous coral reef Wshes

C. S. Mantyka · D. R. Bellwood

Received: 21 November 2006 / Accepted: 1 March 2007 / Published online: 27 March 2007© Springer-Verlag 2007

Abstract Few studies have examined the relativefunctional impacts of individual herbivorous Wsh species oncoral reef ecosystem processes in the Indo-PaciWc. Thisstudy assessed the potential grazing impact of individualspecies within an inshore herbivorous reef Wsh assemblageon the central Great Barrier Reef (GBR), by determiningwhich Wsh species were able to remove particular macroal-gal species. Transplanted multiple-choice algal assays andremote stationary underwater digital video cameras wereused to quantify the impact of local herbivorous reef Wshspecies on 12 species of macroalgae. Macroalgal removalby the Wshes was rapid. Within 3 h of exposure to herbivo-rous reef Wshes there was signiWcant evidence of intensegrazing. After 12 h of exposure, 10 of the 12 macroalgalspecies had decreased to less than 15% of their originalmass. Chlorodesmis fastigiata (Chlorophyta) and Galaxaurasp. (Rhodophyta) showed signiWcantly less susceptibility toherbivorous reef Wsh grazing than all other macroalgae,even after 24 h exposure. Six herbivorous and/or nominallyherbivorous reef Wsh species were identiWed as the domi-nant grazers of macroalgae: Siganus doliatus, Siganuscanaliculatus, Chlorurus microrhinos, Hipposcarus longi-ceps, Scarus rivulatus and Pomacanthus sexstriatus. Thesiganid S. doliatus fed heavily on Hypnea sp., whileS. canaliculatus fed intensively on Sargassum sp. Variationin macroalgal susceptibility was not clearly correlated with

morphological and/or chemical defenses that have beenpreviously suggested as deterrents against herbivory.Nevertheless, the results stress the potential importance ofindividual herbivorous reef Wsh species in removing macro-algae from coral reefs.

Keywords Herbivory · Fishes · Algal assays · Video camera · Ecosystem processes

Introduction

Herbivorous Wshes are the most important grazers of tropi-cal marine macroalgae, especially in relatively unexploitedcoral reef systems (Choat 1991; McClanahan et al. 2003;Mumby et al. 2006). Numerous experimental studies basedon the exclusion of herbivorous Wshes from areas of reefhave demonstrated that the grazing activity of Wshes cansubstantially inXuence not only the abundance of diVerentmacroalgal species (e.g., Sala and Boudouresque 1997;McClanahan et al. 2003; Ceccarelli et al. 2006; Hugheset al. 2007), but also the distribution, composition, diversityand productivity of epilithic algae on coral reefs (e.g.,Lewis 1986; Thacker et al. 2001; Russ 2003). Studies usingmacroalgal transplants have also shown that the rate ofremoval by herbivorous Wshes is relatively high on coralreefs, but that it can vary signiWcantly among reef zonesand among diVerent macroalgal species (Hay 1984; Lewis1985, 1986; Carpenter 1986; Steinberg et al. 1991). Severalmacroalgal attributes have been identiWed that may explainthe diVering eVects of herbivorous Wshes on the distributionpatterns of macroalgae on coral reefs. These attributesinclude life history characteristics such as body plans,growth rates and competitive abilities (Littler et al. 1983a;Steneck and Dethier 1994), as well as morphological and

Communicated by Ecology Editor P.J. Mumby.

C. S. Mantyka · D. R. Bellwood (&)Australian Research Council Centre of Excellence for Coral Reef Studies and School of Marine and Tropical Biology, James Cook University, Townsville, QLD 4811, Australiae-mail: david.bellwood@jcu.edu.au

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chemical defenses (Hay 1984; Lewis 1985; Hay andFenical 1988; Paul 1997).

On the Great Barrier Reef (GBR), herbivorous Wshes,particularly the roving parrotWshes, siganids and acanthur-ids are the predominant herbivores. These Wshes canachieve large sizes and high biomass (Russ 1984a, b;Choat 1991), and can remove up to 90–100% of the dailyalgal production in a community (Hatcher 1983; Poluninand Klumpp 1992). The impact of individual herbivorousWsh species on macroalgal communities is less well docu-mented. Some researchers have reported estimated grazingrates on algae for individual parrotWsh, acanthurid andpomacentrid species (e.g., Polunin and Klumpp 1992;Polunin et al. 1995; Ferreira et al. 1998), but to date therehave been few studies documenting the grazing impact,and thus the contribution and role of individualherbivorous Wsh species, in regards to removing speciWcmacroalgal species (Lewis 1985; Bellwood et al. 2006).DiVerentiation among species would provide importantinformation for coral reef management in terms of identi-fying function groups, functional redundancy and coralreef resilience (Bellwood et al. 2004; Hughes et al. 2006).Knowledge of the potential for herbivorous reef Wshes toremove macroalgae provides an indication of the natureand extent of reef resilience and the ability of reefs toprevent, or regenerate following coral-algal phase-shifts(cf. Bellwood et al. 2006).

The objective of this study, therefore, was to determineexperimentally which herbivorous reef Wsh species arecapable of removing various tropical macroalgal species onthe GBR, Australia. To do this, the rate of macroalgalremoval was determined for 12 macroalgal species throughtransplant assays in which macroalgae were exposed toherbivorous Wshes, monitored using stationary underwaterdigital video cameras.

Materials and methods

Study site and macroalgae

The study was conducted between February and March2006 at Orpheus Island (18°35�S, 146°20�E), on the innershelf of the GBR, Australia. Two fringing reef sites (3–5 mdepth) were used throughout this study, located approxi-mately 100 m apart on the northern end of Pioneer Bay, onthe leeward side of Orpheus Island. Eight of the twelvespecies of macroalgae were collected along the inner andmid intertidal reef Xat of Pioneer Bay (Table 1). Galaxaurasp. was collected from the outer reef Xat and reef crest,Chlorodesmis fastigiata from the reef crest, and Laurenciasp. 1 and Hypnea sp. were collected from a buoyed moor-ing line, in the north-west end of the bay, approximately25 m from the reef crest. The macroalgal species selectedfor this study were chosen to represent all three divisions ofmacroalgae (Chlorophyta, Rhodophyta and Phaeophyta),displayed a wide range of morphologies (Table 1), andwere the most abundant species found in Pioneer Bay.Macroalgal species were removed ensuring, where possi-ble, that the holdfast was intact and transferred to theOrpheus Island Research Station. Macroalgae were main-tained in outdoor, recirculating seawater tanks until used inthe feeding experiments (within 24 h of collection). Macro-algae were identiWed to species level where possible, but inmost cases were only identiWed to genus. However,Galaxaura sp. closely resembled Galaxaura rugosa andLaurencia sp. 1 resembled Laurencia Wliformis.

Initial macroalgal-removal trials

Multiple-choice algal assays were used to determine theremoval rates of diVerent macroalgal species after 3, 12 and

Table 1 Description and location of the 12 macroalgal species used in the present study

Species Division Morphology Location

Chlorodesmis fastigiata Chlorophyta Soft, Wlamentous Reef crest

Halimeda cylindracea Chlorophyta Calcareous, segmented Inner reef Xat

Halimeda discoidea Chlorophyta Calcareous, segmented Inner reef Xat

Halimeda opuntia Chlorophyta Calcareous, segmented Mid reef Xat

Padina sp. Phaeophyta Sheet-like, frondose Mid reef Xat

Sargassum sp. Phaeophyta Tough, leathery, branching Inner reef Xat

Turbinaria ornata Phaeophyta StiV, leathery, branching Mid reef Xat

Amphiroa sp. Rhodophyta Calcareous, brittle, branching clumps Mid reef Xat

Galaxaura sp. Rhodophyta Strong, branching clumps Outer reef Xat and crest

Hypnea sp. Rhodophyta Numerous small, coarse branches Buoyed mooring line

Laurencia sp. 1 Rhodophyta Numerous small, soft Wne branches Buoyed mooring line

Laurencia sp. 2 Rhodophyta Numerous small, coarse branches Inner and mid reef Xat

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24 h exposure to herbivorous reef Wshes. Such assayscontained one ‘proportional-sized’ specimen of each of the12 macroalgal species. Each specimen was tied in randomorder onto a 1 m long piece of Wshing line at approximately8 cm intervals. Proportional-sized algal specimens werechosen to represent algae in their natural condition (i.e.,with minimal change to their appearance). Damaged ordiscolored algae were not used in assays.

Algal assays were transported in plastic self-sealed bagsto the reef and deployed at haphazard locations within thereef crest of each site (the habitat with the highest feedingrates by herbivorous Wshes; Bathgate and Bellwood 2007).Algal assay lines were secured at each end to a piece ofcoral or rock. The 3 h macroalgal-removal trials com-menced at 0800 and 1300 hours for 7 days, a total of 28replicates; 14 at each site, 7 each in the morning/afternoon).The 12 and 24 h macroalgal-removal trials commenced at0600 hours and continued until 1800 or 0600 hours the fol-lowing day. Three replicates were carried out on the crestof each site for both the 12 h (n = 6) and 24 h (n = 6) trials.Macroalgae were blotted to remove excess water andweighed to the nearest 0.01 g prior to each macroalgal-removal trial and then again after exposure. Macroalgalremoval rates were calculated as mass loss for each speciesover that time period and remaining mass presented as aproportion of initial algal mass.

Video analysis

A stationary underwater digital video (DV) camera wasplaced on a tripod approximately 1–2 m from the multiple-choice algal assays to record the feeding activity of the her-bivorous reef Wshes during the Wrst 3 h. Stationary under-water DV cameras are advantageous because they oVer ameans of recording algal removal in the Weld without thepresence of an observer (Bellwood et al. 2006). The pres-ence of a video camera, however, may have an impact onthe behavior of some reef Wshes, although this eVect islikely to be minimal.

Filmed feeding trials commenced at 0800 and1300 hours, in order to capture the morning and afternoonfeeding activity of herbivorous reef Wshes, for 7 days. Feed-ing activity was recorded for three continuous hours and nodisturbances occurred apart from the brief 5 min tapechange at 0930 hours and at 1430 hours. A total of 28Wlmed feeding trials (84 h) were recorded, 14 on the crestof each site (half in the morning and the other half in theafternoon using two cameras simultaneously, one for eachsite).

To quantify the relative macroalgal removal rates byspeciWc herbivorous reef Wsh species the entire 84 h ofvideo footage was viewed and the total number of bitestaken per Wsh species on each macroalgal species was

recorded, for the full 180 min of each feeding trial. Allcommon herbivorous Wsh species located the multiple-choice algal assay within the Wrst 3 h of every macroalgal-removal trial. The functionally most signiWcant species (asindicated by bite rates) all arrived within the Wrst 30 min. A“bite” was recorded only if the Wsh could be seen to applyits jaws to the algae and close the mouth. Rapid bites inquick succession that could not be separated were countedas a single bite. Bites were not counted if dislodged mate-rial was ejected. The eVect of diVerent Wsh sizes on macro-algal removal was taken into account by dividingindividuals of each Wsh species into seven size classes:5–7.5, 7.6–10, 10.1–15, 15.1–20, 20.1–25, 25.1–30, and>30 cm (a quadrat in the Weld of view prior to Wlmingprovided a scale). Total number of bites per Wsh specieswas then converted to a standardized bite impact (totalbites £ body mass in kilograms) using published length–weight relationships (Kulbicki et al. 2005), with Wsh lengthtaken as the midpoint of the respective size class. Thisenabled us to concentrate on the functionally dominantspecies in the local assemblage.

Statistical analyses

To investigate change in macroalgal mass loss betweensites and time of day, a two-way ANOVA was conductedfor each macroalgal species, with site and time of daytreated as Wxed factors. Assumptions of normality andhomoscedasticity were inspected via residual plots. Datafor C. fastigiata and Padina sp. were log(x + 1) trans-formed in order to meet the assumptions.

Among-species diVerences in the proportion of macroal-gal mass remaining after 3 h of exposure to herbivorousreef Wshes were analyzed using a Friedman test. The Fried-man test is a non-parametric technique that may be usedwhen samples are not independent as in the case of the mul-tiple-choice algal assay design (for comparisons amongspecies) where the removal of one algal species may bedependent on the presence of other algal species in a trial.When diVerences in the proportions of macroalgal massremaining were found to be signiWcant, a Friedmana posteriori multiple comparisons test was used to investi-gate those diVerences (Conover 1999).

A linear regression was used to examine whether propor-tion of algal mass loss after 3 h was related to the initialalgal mass. Mean values for each of the 12 macroalgal spe-cies were used in the regression. The assumptions of nor-mality and homoscedasticity were tested via residual plots.Mass also addresses, to some extent, variation in apparency(i.e., larger algae would be more visible).

Analysis of the standardized bite impact of Wshesrevealed that there were six dominant reef Wsh species thathad greater than 1,000 standardized bites (i.e., 1,000 kg bites)

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of macroalgae, summed over all feeding trials (the remainderall had fewer than 600 standardized bites). The patterns ofmacroalgal feeding by these six dominant species wereexamined using a principal component analysis (PCA)using standardized bite data and a covariance matrix.

Results

There were no signiWcant diVerences detected in macroal-gal losses between sites or between time of day, and nosigniWcant interaction between these two factors, after 3 hof exposure for any of the 12 macroalgal species used in themacroalgal-removal trials (ANOVA). All subsequent anal-yses were therefore based on pooled site and morning andafternoon trials.

Macroalgal removal rates

Macroalgal removal rates varied signiWcantly among the 12macroalgal species (Friedman tests, P < 0.001; Fig. 1).After 3 h of exposure to herbivorous reef Wshes, there was asigniWcant diVerence in the proportion of algal massremaining for the green alga C. fastigiata (95 § 5% SE

remaining) and the red alga Galaxaura sp. (90 § 2% SEremaining) when compared to all other macroalgae (Fried-man test, X2 = 177.97, P < 0.001; Fig. 1a). The proportionof algal mass remaining for C. fastigiata and Galaxaura sp.was not signiWcantly diVerent but both were signiWcantlygreater than any of the other algae. The other ten macroal-gal species had 60% or more of their initial algal massremoved after 3 h exposure. Although there appeared to beminimal variation among these ten other macroalgal spe-cies, the three Halimeda species (Chlorophyta: H. cylindra-cea, H. discoidea, and H. opuntia) showed slightly lessreduction in mass compared to many of the brown and redalgae, with Galaxaura sp. as an exception. After 12 h ofexposure to herbivorous reef Wshes, C. fastigiata (89 § 8%SE remaining) and Galaxaura sp. (78 § 6% SE remaining)were relatively intact. In contrast, the other ten macroalgalspecies were either completely removed (H. opuntia,Sargassum sp., Turbinaria ornata, Amphiroa sp., Hypneasp., Laurencia sp.1 and Laurencia sp.2) or only remainedas small fragments (H. cylindracea, H. discoidea andPadina sp.). After 24 h of exposure, C. fastigiata and Gal-axaura sp. decreased in mass to 54 § 21 and 60 § 13% SEof their initial biomass respectively, while all other macro-algae exposed were completely removed or no longerrecognizable.

Macroalgal removal rates did not appear to be related toinitial algal mass. Among the 12 macroalgal species used inthe multiple-choice algal assays, the relationship betweenproportion of mass lost after 3 h and initial mass was highlyvariable. Mean initial macroalgal mass ranged from 1.1 g inC. fastigiata to 62.6 g in Galaxaura sp. The initial massused and the proportion of mass lost for the other ten mac-roalgal species ranged from 6.8 to 45.7 g and lost 67 to100%, respectively. There was no statistically signiWcantrelationship between macroalgal mass loss and initial massof macroalgae (Linear regression, r2 = 0.074, P = 0.39).

Impact of speciWc herbivorous reef Wsh species

A total of 19 herbivorous and “nominally” herbivorous reefWsh species was observed feeding on the multiple-choicealgal assays. These Wshes included members of the familiesAcanthuridae (Acanthurus sp. and Naso unicornis), Kyph-osidae (Kyphosus vaigiensis), Pomacanthidae (Pomacan-thus sexstriatus), Pomacentridae (Abudefduf bengalensisand Neoglyphidodon melas), Labridae (Cetoscarus bicolor,Chlorurus microrhinos, Hipposcarus longiceps, Scarusaltipinnis, Scarus Xavipectoralis, Scarus rivulatus andScarus schlegeli) and Siganidae (Siganus canaliculatus,Siganus doliatus, Siganus vulpinus, Siganus punctatus,Siganus puellus and Siganus lineatus). Two of these spe-cies were accountable for 72% of the total number ofbites from macroalgae. S. doliatus contributed 50% and

Fig. 1 Proportion of initial algal mass remaining after a 3 h and b 12 hexposure to herbivorous reef Wshes. Bars represent means § SE.Analysis for a 3 h exposure is by a Friedman test followed by aFriedman multiple comparisons test. Letters indicate homogenoussubgroups

(a)

(b)

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S. canaliculatus contributed a further 22% of the total bites.However, when total impact of a Wsh species was expressedas standardized bite impact per Wsh species, six reef Wshspecies were found to represent 87% of the total standardizedbites. From most important to least, measured as contribu-tion in number of standardized bites, the six reef Wshspecies were: S. doliatus, C. microrhinos, S. canaliculatus,H. longiceps, Scarus rivulatus and P. sexstriatus. These sixreef Wsh species all had greater than 1,000 standardizedbites and, based on their dominant impact, were selected asthe focal species in subsequent analyses.

The PCA of the 12 macroalgal species revealed the vari-ation in the number of standardized bites taken from themacroalgae by the six herbivorous reef Wsh species (Fig. 2).In this analysis, the Wrst two components explained 79.2and 14.5% of the variation in the number of standardizedbites, respectively. One of the strongest divisions to arisefrom the PCA was the distinct separation of Sargassum sp.from all other macroalgae based on the grazing by S. canal-iculatus; S. canaliculatus’ feeding was strongly associatedwith Sargassum sp. The second distinctive division wasbetween Hypnea sp. and S. doliatus; i.e., S. doliatus’ feed-ing was strongly associated with Hypnea sp. The remainingfour Wsh species contributed little to the separation of theremaining ten macroalgal species.

Discussion

The 12 tropical macroalgal species were rapidly removedby herbivorous reef Wshes in Pioneer Bay. Within 3 h ofexposure there was signiWcant evidence of intense brows-ing on many macroalgal species, and after 12 h of exposure10 of the 12 macroalgal species decreased to less than 15%of their original mass. The rates of macroalgal removalreported here reXect those of previous investigations on theeVects of herbivorous reef Wsh grazing on macroalgal abun-dance and/or biomass. In the Caribbean, for example,Lewis (1985, 1986) found similar species of macroalgae asin the present study, such as Laurencia papillosa, Padinajamaicensis, Dictyota cervicornis and Turbinaria turbi-nata, to be 100% removed after 8 hrs in transplant trials.Hay (1984) also found transplanted species of Sargassumand Turbinaria to be signiWcantly reduced within days (seealso Hay et al. 1983; Carpenter 1986). On the GBR, Stein-berg et al. (1991) demonstrated signiWcant reduction inmacroalgal tissue weight within one day using Sargassumfrom nearby reefs. Nevertheless, the present study revealsthe speed and extent of macroalgal removal at some inshoreGBR sites.

Most herbivore exclusion studies have also produceddramatic changes in algal community structure. Exclusionof herbivorous Wshes has shown to signiWcantly increase

the standing crop and biomass of algal turfs on the GBR(Russ 2003; Ceccarelli et al. 2006), and in the Caribbean(Lewis 1986; McClanahan et al. 2003). Similarly, exclu-sion of herbivorous Wshes has also been shown to signiW-cantly increase abundances and biomass of macroalgae(Sala and Boudouresque 1997; Ceccarelli et al. 2006; Bell-wood et al. 2006; Hughes et al. 2007).

In contrast, however, McCook (1997) found that it tookmonths to signiWcantly reduce macroalgal transplants from

Fig. 2 Variation in browsing activity by Wshes among coral reef mac-roalgae. A principal components analysis is used to show variation instandardized bites taken from 12 macroalgal species by 6 herbivorousreef Wsh species. The upper section shows the similarity among algaein terms of the number of mass standardized bites received from her-bivorous Wshes. The Wsh taxa responsible for the ordination are shownby the species vector loadings on the lower panel. Each value is basedon the mean of 28 feeding trials

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reef Xat zones to a seaward coral zone on Great Palm Island(an island approximately 15 km to the south of the studysite). Variation in removal rates among studies most likelyreXects low browsing herbivorous reef Wsh abundance onreef slope and inner reef Xat study sites compared to reefcrest sites (Hatcher 1981; Klumpp and Polunin 1990; Russ2003; Bathgate and Bellwood 2007), and the diVerences inabundances of herbivorous reef Wshes between study reefs(Carpenter 1986). Methodological diVerences and broadertemporal or spatial variation may also contribute. Neverthe-less, the grazing intensity of herbivorous reef Wshes at thestudy location appears to be relatively high and is consis-tent with previous studies of relatively unexploited reefs(cf. Mumby et al. 2006; Hughes et al. 2006). The study siteis exposed to no commercial or recreational Wshing, and incommon with the rest of the GBR, there is no commercialWshery for herbivorous Wshes.

The results of the present study also showed marked var-iation among tropical macroalgae in their susceptibility toremoval by herbivorous reef Wshes. Mean macroalgal massloss after exposure to herbivorous reef Wshes for 3 h rangedfrom 8 to 100% of the original mass. These diVerences insusceptibility were not related to initial mass of algae usedin the trials, and, in addition, were poorly correlated withthe algal defenses that have been previously proposed asdeterrents against Wsh grazing (Paul and Hay 1986; Hayand Fenical 1988; Hay 1997; Paul 1997). For example,Sargassum sp. and T. ornata showed high susceptibility tograzing despite their tough, leathery growth forms and pres-ence of phlorotannins (Norris and Fenical 1982; Hay andFenical 1988). Similarly, Laurencia sp.1, and Laurenciasp.2 showed high susceptibility despite Laurencia speciespossessing halogenated phenolics (Cardellina et al. 1982;Norris and Fenical 1982; Paul and Hay 1986; Hay andFenical 1988; Hay 1997). The three Halimeda species(H. cylindracea, H. discoidea, and H. opuntia) also suVeredrelatively high mass losses to herbivory despite their sub-stantial calciWcation of tissue and the presence of the unusualcompound diterpenoid trialdehyde halimedatrial (Paul andFenical 1983; Hay and Fenical 1988). Amphiroa sp.likewise showed high losses in spite of its calciWed tissues.

In contrast, C. fastigiata and Galaxaura sp. were the twomacroalgal species that demonstrated the least susceptibil-ity to Wsh grazing. In C. fastigiata this is expected as theWlaments contain high levels of chlorodesmin, a secondarymetabolite with strong herbivore-deterrent properties(Ducker 1967; Paul et al. 1990). However, Galaxaura sp.does not appear to contain high concentrations of any sec-ondary compounds, although it is a robust and structurallydefended alga (Paul et al. 1990; Meyer et al. 1994). Theseresults oVer only partial support for previous Wndings.Although C. fastigiata has been previously reported ashighly herbivore-deterrent (Ducker 1967; Paul et al. 1990),

and transplanted specimens of Sargassum, Turbinaria,Padina, Hypnea and Laurencia have all been reported to besubject to high grazing losses (Hay et al. 1983; Hay 1984;Lewis 1985, 1986; Carpenter 1986; Steinberg et al. 1991),the results of the present study are unusual in that signiW-cant removal of the calciWed Halimeda species occurred.Most previous studies have reported low susceptibility ofHalimeda to Wsh grazing (e.g., Hay et al. 1983; Littler et al.1983b; Lewis 1985; Hay and Fenical 1988). Such diVer-ences in susceptibility between studies may represent geo-graphical or individual variation in algal chemistry (e.g.,Van Alstyne 1988; Bolser and Hay 1996; Van Alstyne et al.2001; Hemmi and Jormalainen 2004), as well as diVerencesin herbivorous reef Wsh community composition. Themajority of previous studies, for example, were based in theCaribbean.

The variation in macroalgal susceptibility to herbivorousreef Wshes shown in the present study reXects macroalgaldistributions within the study area. Macroalgal species col-lected from the inner and mid reef Xat of Pioneer Bay (H.cylindracea, H. discoidea, H. opuntia, Padina sp., Sargas-sum sp., T. ornata, Amphiroa sp. and Laurencia sp.2) andfrom the buoyed mooring line (Hypnea sp. and Laurenciasp.1), all showed relatively high levels of susceptibility,whereas the other two macroalgal species collected fromthe outer reef Xat and crest (Galaxaura sp. and C. fastigi-ata) were found to be less susceptible to grazing. This pat-tern is consistent with previous studies (Hay et al. 1983;Littler et al. 1983b; Lewis 1985, 1986; McCook 1997), sug-gesting that macroalgal species that occur primarily in ref-uge areas, such as inner-mid reef Xats, lagoons and deepsand plains are very susceptible to herbivory and are rap-idly consumed when moved to areas of high grazing pres-sure (i.e., reef crests).

Several researchers have predicted that macroalgal spe-cies that are excluded from reef crests because of high graz-ing pressure often have high productivity and maypotentially represent dominant competitors of more resis-tant macroalgae in the absence of herbivory (Hay et al.1983; Holt et al. 1994; Thacker et al. 2001). As a result, ithas been proposed that rapidly growing macroalgal speciesare often more susceptible to herbivory than the slowergrowing forms (Littler et al. 1983b; Hay 1984) and growthrates appeared to be positively correlated with competitiveability (Lubchenco and Gaines 1981; Lewis 1986; Hixon1997). The results of this study again oVer only partialsupport for this hypothesis. Although highly productive,fast-growing taxa such as Sargassum and Padina weremore susceptible to Wsh grazing than slow-growing algaesuch as C. fastigiata, the three Halimeda species were allsusceptible to herbivorous reef Wsh grazing despite theirreported low productivity and slow growth rates (Hay et al.1983; Littler et al. 1983b). Individual macroalgae, including

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Halimeda species, are capable of increasing their growthrates in relation to seasons, depth, and nutrient availability(Smith et al. 2004). Growth rate variation may thereforehelp to explain this contradiction.

Remote video observations identiWed six reef Wsh spe-cies as the dominant grazers of macroalgae on the reef crestof Pioneer Bay. This included two siganids, three par-rotWshes and one pomacanthid. Herbivorous reef Wsheswere the only consumers observed feeding on the multiple-choice algal assays in this study (the pomacanthid, how-ever, appears to be a facultative omnivore, Allen et al.1998). Although video observations identiWed six dominantherbivorous reef Wsh species, the most striking aspect wasthe extent of variation displayed between species, with thestrong suggestion of selectivity. S. doliatus was notable inthat it fed heavily on Hypnea sp. In contrast, S. canalicula-tus fed intensively on Sargassum sp. The three parrotWshes:C. microrhinos, H. longiceps and Scarus rivulatus as agroup were the dominant grazers of the three calciWed Hali-meda species and Amphiroa sp. Interestingly, however, theparrotWshes did not feed on the red macroalga Galaxaurasp., despite appearing to be physically/morphologicallycapable of consuming this robust and structurally defendedalga. It was also particularly striking that the dominantgrazer of large macroalgal strands at this site, the batWshPlatax pinnatus (Bellwood et al. 2006), was not recordedfeeding from any of the small-scale transplants in the pres-ent study.

Such variation among herbivorous Wsh species has notbeen widely documented, especially in the Indo-PaciWc. Inthe Caribbean, Lewis (1985), using direct observations,found that the brown algae Sargassum polyceratium, Turbi-naria turbinata, and Padina jamaicensis were more vulner-able to parrotWshes (especially Sparisoma rubripinne andSparisoma chrysopterum). In contrast, the red algae: Lau-rencia papillosa, Digenia simplex, Acanthophora spiciferaand Coelothrix irregularis were more vulnerable to acan-thurids (e.g., Acanthurus bahianus and Acanthurus coeru-leus). Lewis suggested that the jaw morphology of theherbivorous Wshes played a role in generating these diVer-ences. There has also been extensive feeding preferenceexperiments conducted in the laboratory that support thetheory that similar herbivorous Wsh species may vary intheir macroalgal preferences (e.g., Tsuda and Bryan 1973;Paul et al. 1990; Pillans et al. 2004).

In summary, the results of the present study highlight thepotential importance of herbivorous reef Wshes in removingmacroalgae from Indo-PaciWc coral reefs. However, macro-algal patterns of susceptibility diVer from previous studies,and emphasize the importance of caution when generaliz-ing about the ecological impact of algal defenses and theireVects on grazing or browsing by herbivorous reef Wshes.Nevertheless, variation in susceptibility of macroalgae to

browsing was marked and probably does reXect diVerencesin macroalgal growth rates, distributions within the studyarea, and the nature of structural and chemical defenses.

Six herbivorous reef Wsh species were identiWed as thedominant grazers of macroalgae on the reef crest of PioneerBay, Orpheus Island. However, they appear to vary widelyin patterns of feeding. In order to understand the signiW-cance of each Wsh species’ role in macroalgal removal inthis reef system, it will be necessary to quantify the extentof feeding selectivity of each Wsh species. Only then can westart to understand the relative impact these reef Wsh speciesmay have on algal community structure.

Acknowledgments We thank: the Orpheus Island Research StationstaV, T. Sunderland and M. Pringle for invaluable Weld assistance; A.Hoey for assistance with algal and Wsh identiWcations; R. Bonaldo, A.Hoey, N. Paul, G. Russ and two anonymous reviewers for insightfuldiscussions and/or helpful comments. Financial support was providedby the Australian Research Council (D.R.B.).

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