MARINE ECOLOGY PROGRESS SERIESMar Ecol Prog Ser

Vol. 482: 217–225, 2013doi: 10.3354/meps10250

Published May 22

INTRODUCTION

Fish assemblages of shallow coastal marine habi-tats are strongly influenced by the nature of the sur-rounding seascape (Steele & Forrester 2002, Vander -klift et al. 2007, Hitt et al. 2011). The arrangement ofthese habitats (i.e. their spatial extent and how theyare juxtaposed) influences the abundance of individ-uals and composition of species, and the rates ofimportant processes such as grazing, predation andsettlement of larvae (Almany & Webster 2006, Rilov &Schiel 2006, Wernberg et al. 2006, Grol et al. 2008).For example, the proximity between coral reefswhere adult fish reside and those habitats that juve-niles inhabit, such as seagrass beds, mangroveforests and sand flats, has been shown to have a sig-nificant influence on species composition (Milchunas

& Noy-Meir 2002, Nagelkerken et al. 2002, Steele &Forrester 2002, Grol et al. 2011), while proximity toreefs can influence the rates of processes, such asherbivory, that are important for maintaining theintegrity of coral reefs (Valentine et al. 2008).

Trophic interactions can in turn affect the land-scape within which they occur. For example, someterrestrial ecosystems that have experienced anincrease in predator abundance have shifted fromherbivore-dominated states with low plant biomassto states with a much higher biomass of plants (Ripple & Beschta 2004). Similarly, in temperaterocky reefs trophic interactions can result in changesin the abundance of habitat-forming macroalgae(Bab cock et al. 1999), although such changes canbe context-specific (Shears et al. 2008, Cook &Vander klift 2011).

© Inter-Research 2013 · www.int-res.com*Email: ryan.downie@csiro.au

Density of herbivorous fish and intensity ofherbivory are influenced by proximity to coral reefs

Ryan A. Downie1,3,*, Russell C. Babcock1,2, Damian P. Thomson1, Mathew A. Vanderklift1

1CSIRO Wealth from Oceans Flagship, Centre for Environment and Life Sciences, Western Australia 6014, Australia2CSIRO Wealth from Oceans Flagship, Ecosciences Precinct, Queensland 4001, Australia

3CSIRO Wealth from Oceans Flagship, Hobart Laboratories, Tasmania 7000, Australia

ABSTRACT: Ecosystems can be profoundly influenced by consumers, sometimes to the extent thatthe entire appearance of the ecosystem is altered. We used remotely sensed images to identify dis-tinctive halos around patch reefs in the lagoon of Ningaloo Reef, the world’s largest fringing coralreef. Thirty-four halos were identified along the length of Ningaloo Reef. Five halos located withina 122 km tract of the reef were investigated. The halos extended >90 m from each central patchreef and were found to be associated with a high biomass of, and intensive grazing by, herbivo-rous fish, especially the large-bodied Kyphosus sydneyanus. Large brown algae mainly of thegenera Sargassum, Dictyopteris and Lobophora were the dominant macroalgae, but were almostabsent immediately adjacent to the patch reefs. Other taxa of herbivorous fish were present nearthe patch reefs, including Naso spp., Siganus spp. and Scarus spp., but the biomass of each waslow and none were significant contributors to grazing. The sizes of the halos reported here aretenfold larger than those previously reported in coral reef systems and are likely to be the resultof intensive herbivory by K. sydneyanus.

KEY WORDS: Ningaloo · Macroalgae · Halo · Patch reefs · Kyphosus sydneyanus

Resale or republication not permitted without written consent of the publisher

Mar Ecol Prog Ser 482: 217–225, 2013

The extent of foraging excursions into adjacenthabitats depends on a number of influences, includ-ing proximity and extent of juxtaposed habitats,predator density and the size and mobility of individ-uals. Species exploit adjacent habitats via 2 broadstrategies: from a central place of refuge or throughflexible foraging behaviour (Lima 1998, Brown et al.1999). The term ‘central place foraging’ describes abehaviour in which individuals reside in habitats thatprovide shelter to which they can retreat in the eventof encountering a predator (Lessells & Stephens1983, Lima 1998). Central place foraging can de -crease the abundance of food resources in the imme-diate vicinity of a refuge (Lessells & Stephens 1983,Festa-Bianchet 1988), necessitating foraging at in -creasingly greater distances from shelter. The theorypredicts that the trade-off between the benefits offoraging further afield and predation risk will evenout at a maximum safe foraging distance. Flexibleforaging behaviour can minimise the risk of encoun-tering a predator, and can include passing throughnon-preferred habitat and only foraging in specificareas at times where an individual perceives the riskof predation to be relatively low (Festa-Bianchet1988, Lima 1998). For example, in tropical coral reefsystems some species of fishes display diel variationin foraging habitat, foraging in seagrass beds or low-relief habitat at night and in habitats with relativelyhigh relief such as mangroves and coral reefs duringthe day (Grol et al. 2008, 2011, Valentine et al. 2008,Luo et al. 2009).

Herbivorous coral reef fish and invertebrates oftenforage in seagrass- or macroalgae-dominated habitatsurrounding reefs. Randall (1965) described a patternin the Caribbean where seagrass biomass was low upto 30 ft (9.1 m) from the edge of coral reefs and patchreefs, because of grazing by herbivorous fish. Similarpatterns were described by Ogden et al. (1973) andfound to be due to grazing by sea urchins. This pattern has also been observed in the Florida Keys(USA) and on the Great Barrier Reef (Australia),where grazing halos with a maximum extent of 10 mcorresponded to increased grazing pressure adjacentto coral habitat (Valentine et al. 2007, Madin et al.2011).

Because grazing halos can be detected in clearwater by satellite and airborne remote sensing(Andréfouët et al. 2001), it has been suggested thatthey may provide a rapid and cost-effective means ofsurveying reefs and detecting changes in the inten-sity of grazing (Madin et al. 2011). However, inter-preting such patterns may be complex (Andréfouët etal. 2003, Brock et al. 2006). Factors such as local

hydrodynamic forces around patch reef structures,related sediment grain size sorting, shading and localavailability of nutrients are also potentially importantand are likely to act at similar spatial scales to previ-ously observed patterns (Randall 1965, Ogden et al.1973, DeFelice & Parrish 2001).

This study was initiated to investigate large (≥90 mradius) halos observed in aerial photographs andimages derived from a hyperspectral survey ofNingaloo Reef (Kobryn et al. 2012). Here, we quan-tify patterns in the biomass and composition of her-bivorous fish, invertebrates and macroalgae, andspecies-specific rates of grazing around 6 halos. Ourmain objective was to determine the rates of her-bivory, and the identity of the main herbivores, asso-ciated with these halos.

MATERIALS AND METHODS

We conducted our study in the Ningaloo MarinePark be tween 2008 and 2009. Ningaloo Reef is afringing reef that extends for 300 km off the WesternAustralian coast. The reef is typically

Downie et al.: Herbivory near coral reefs

edge with a single central patch reef and were >20 min radius. Based on these criteria, we identified 34halos.

Of the 34 halos, 5 were included in subsequent de - tailed surveys; these were all located within a 122 kmsection of the reef from Tantibiddi (21° 53.09’ S,113° 57.2’ E) to Coral Bay (22° 54.25’ S, 113° 47.09’ E).At each of the 5 halos the biomass and species com-position of macroalgae, herbivorous fish and largeinvertebrates and rates of herbivory were quantifiedat 5 distances relative to the central patch reef: 0(immediately adjacent to the patch reef), 30, 60, 90and 120 m.

The density estimates of all fish and invertebrateswere measured by underwater visual census using asingle transect, swum parallel to the edge of the cen-tral patch reef. Each transect was conducted by a sin-gle diver. Fish were recorded within a 30 × 5 m tran-sect on the first leg and macro-invertebrates wererecorded within a 30 × 2 m transect on the return.Fish, excluding juveniles (

Mar Ecol Prog Ser 482: 217–225, 2013

Analyses of the biomass of macroalgae, thalluslength and bite rates focused on testing for differ-ences among distances (5 levels; fixed) and sites (5levels; random). Analyses of biomass of herbivorousfish focused on distance alone, because there weresingle observations for each distance at each patchreef. Permutational analysis of variance (PERM-ANOVA) was used for analyses; in this method statis-tical significance is determined by permutation, andthere are no a priori assumptions about the distribu-tion of the data (Anderson et al. 2008). Analyses werebased on Euclidean distances. Where a statisticallysignificant effect of distance was detected, pair-wisecomparisons were used to resolve the nature of dif-ferences among distances.

RESULTS

The biomass of macroalgae was significantlyhigher with increasing distance from the centralpatch reefs (Fig. 2A, Table 1). Hydroclathrus clathra -tus and Lobophora variegata were the only largemacroalgae found within 30 m of patch reefs, butboth occurred in relatively low biomass (Fig. 2B).Dictyopteris serrata and Sargassum sp. were thedominant macroalgae found at distances >90 m frompatch reefs, with Cystoseira trinodis, Sargassumdecurrens and Lobophora variegata co-occurring atlower densities (Fig. 2B). A statistically significantinteraction between distance and site (F = 13.0, p <0.001; Table 1) was detected, indicating that themagnitude of the difference was not consistent at all5 reefs, although the direction of the difference was(Table A1 in the Appendix provides a summary ofpairwise comparisons for each site × distance combi-nation).

Herbivorous fish assemblages associated with thecentral patch reef were comprised predominantly ofKypho sus sydneyanus, Naso fageni, Siganus fusces -cens, Acanthurus dussumieri, A. grammo ptilus andScarus ghobban. The majority of individuals werefound immediately adjacent to the patch reefs (0 m),with no herbivorous fish observed be yond 30 m frompatch reefs (Fig. 3A, Table 2). Herbivorous fishassemblages were dominated by K. sydneyanus,which accounted for more than half of the total bio-mass (Fig. 3B).

Individual Kyphosus sydneyanus were generallylarge (40−60 cm total length [TL], 2.2 ± 1.3 kg) andwere commonly observed in schools of >50 ind. Thesimilarly sized Naso unicornis (40− 60 cm TL, 3.2 ±0.8 kg) were usually observed as single individuals or

occasionally in small groups. Naso fageni, Siganusfus ce scens and Acanthurus dus su mi eri were smaller(20−30 cm TL,

Downie et al.: Herbivory near coral reefs

and showed no consistent pattern with distance fromcentral patch reefs (Table 3).

Rates of consumption of tethered algae were high-est adjacent to the central patch reef (Fig. 4A) andalgae were consumed at a mean rate of 5.2 ± 1.5 cm12 h−1, dropping significantly to 2.9 ± 1.6 cm 12 h−1 at30 m (Fig. 4A, Table 4). There was also a statisticallysignificant distance × site interaction, indicating thatthe magnitude of the difference was not consistent at

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Source df MS F p

Distance 4 8340.4 11.644

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all 5 reefs, although the direction of the differencewas consistent, showing less consumption with in -creasing distance from patch reef.

Species-specific bite rates determined from videoobservations were highest (177.8 ± 69 bites h−1) forKyphosus sydneyanus immediately adjacent to thepatch reefs (0 m; Fig. 4B). Bite rates for Acanthurusdussumieri and Naso fageni were considerably lower(32 and 6 bites h−1, respectively) than for K. syd-neyanus. Acanthurus dussumieri was observed tofeed at greater distances from the patch reefs (60 and90 m) than either K. sydneyanus or N. fageni. Othercommonly observed species of herbivorous fish, suchas Siganus fuscescens, Acanthurus grammoptilusand Scarus ghobban, were not recorded grazing ontethered algae. Analysis of the species-specific biterates (Table 5) indicated that bite rates varied signif-icantly with distance from patch reef; pairwise com-parisons revealed that bite rates were highest imme-diately adjacent to the reefs (0 m). Most bites weretaken by K. sydneyanus (Fig. 4B).

DISCUSSION

The strong relationships between the distancefrom patch reefs, the biomass of macroalgae and her -bi vorous fish (especially Kyphosus sydneyanus), andthe rates of consumption of tethered algae supportthe inference that grazing by K. sydneyanus main-tains the low biomass of macroalgae we ob servedclose to patch reefs. Kyphosus sydneyanus was pres-ent in greater abundance and higher biomass thanany other species of herbivorous fish at all sites; itsbiomass was more than twice that of N. fageni, andtenfold greater than siganids, acanthurids and scarids(Fig. 3), and most of the bites ob served on tetheredalgae were by K. sydneyanus.

Video observations, consumption of tethered algaeand estimates of fish biomass provided little indica-tion as to why the 60 and 90 m sampling distanceswere consistently observed to be devoid of macro-

algae. The biomasses of herbivorous invertebrateswere consistently low at all distances and inverte-brates were not observed consuming tetheredmacroalgae. However, Acanthurus dussumieri wasre corded grazing at greater distances from patchreefs than Kyphosus sydneyanus, suggesting thathalos may be maintained by multiple species. WhileK. sydneyanus was not observed beyond 30 m duringcensuses or in video footage, it was observed bydivers 60 to 80 m from patch reefs on other occasions,suggesting that infrequent foraging at greater dis-tances (not detected by our methods) might occur.

The large scale and symmetry of the features wehave described further support the inference thatgrazing, rather than hydrodynamic features, main-tains these halos. Factors such as wave energy andtidal flow around reef features generate turbulence,and have been demonstrated to influence benthic al-gal communities (Hurd 2000, Toohey 2007). Taebi etal. (2011) demonstrated that hydrodynamic flow in la-goon waters of Ningaloo is parallel to the shore andexits through reef passes. Should these processes in-fluence the patterning of macroalgal beds aroundpatch reefs, one would expect axes to align with dom-inant currents, while the halos we have described arelargely symmetrical.

Significant grazing by Kyphosus vaigiensis hasbeen observed on the Great Barrier Reef (Choat et al.2004, Hoey & Bellwood 2008, Bennett & Bellwood2011); however, it was the dominant grazer only inthe southern Great Barrier Reef (>21° S) (Bennet etal. 2010). Similarly, large schools of Kyphosus arecommon at Ningaloo Reef (Babcock et al. 2009), mostlikely due to its high-latitude location (21°−23° S).Kyphosids are reported to be relatively more abun-dant at higher latitudes in other coral reef bioregions(Floeter et al. 2005), and it is possible that large halofeatures such as those we have described (>10 m)may be restricted to high-latitude coral reefs. Pat-terns are also likely to be species-specific. Kyphosussydneyanus and K. vaigiensis feed primarily onbrown algae (Moran & Clements 2002, Choat et al.2002), but other species such as K. cornelii prefer redalgae (Rimmer 1986) and may also display otherbehaviours such as territoriality that result in differ-ent spatial patterns in benthic macroalgae (Berry &Playford 1992).

The processes driving halo development are knownto vary, although these do not necessarily lead to visi-ble differences in halo dimensions. Randall (1965)demonstrated that halos in the British Virgin Islandswere maintained by acanthurids and scarids and hada maximum extent of 10 m. Ogden et al. (1973) de-

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Source df SS MS F p

Site 5 52296 10459 0.74286 0.611Distance 4 217430 54357 4.7397 0.004Site × Distance 20 224080 11204 0.79577 0.613Residuals 20 281590 14080

Table 5. Multivariate permutational analysis of variance(PERMANOVA) analysing species-specific bite rate by site

and distance

Downie et al.: Herbivory near coral reefs 223

scribed similar patterns in the American Virgin Is-lands that, while similar in size to those reported byRandall (maximum extent of 10 m), were maintainedby the sea urchin Diadema antillarum. The findingsof these 2 studies raise an important point that halosof similar extent are found throughout the Caribbean,but are driven by different herbivores.

It is therefore important to understand the variabil-ity in patterns observed and in the processes that leadto these patterns. All halos described to date are fromcoral reef lagoon habitats and to that extent are com-parable. Halos reported here are ≥90 m in radius andattributed to herbivorous fish grazing, while those re-ported elsewhere are have been

Mar Ecol Prog Ser 482: 217–225, 2013

Acknowledgements. We thank Halina Kobryn (MurdochUniversity, Western Australia) for supplying remotelysensed imagery; Fiona Graham for assistance with data col-lection; Toby Patterson for support and initial review of themanuscript; and Yardie Creek caravan park for serviceswhile in the field.

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Group Number of sites Percentage

0 > 30 2 400 > 60 2 400 > 90 4 800 > 120 5 10030 > 60 2 4030 > 90 4 8030 > 120 5 10060 > 90 4 8060 > 120 5 10090 > 120 2 40

Appendix. Post hoc test outputs for significantinteraction effects

Table A1. Algal biomass analysis, pairwise comparison of site× distance interaction. Group states the comparison for dis-tance from patch reef. Numbers and percentage of significant

sites are also shown

Editorial responsibility: Tim McClanahan, Mombasa, Kenya

Submitted: August 7, 2012; Accepted: January 3, 2013Proofs received from author(s): April 3, 2013

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