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aqua vol. 5 no. 1 - 20011

aqua, Journal of Ichthyology and Aquatic Biology

Food Resource and Habitat Sharing by the Three Western South AtlanticSurgeonfishes (Teleostei: Acanthuridae: Acanthurus) off Paraíba Coast,

North-eastern Brazil

Thelma L. P. Dias1, Ierecê L. Rosa2 & Bertran M. Feitoza3

Universidade Federal da Paraíba, CCEN, Departamento de Sistemática e Ecologia, Campus I, João Pessoa, Paraíba, Brasil, 58059-900.

E-mails: 1) [email protected]; 2) [email protected]; 3) [email protected]

Accepted: 28.09. 2001

KeywordsDiet, feeding behaviour, reef fishes, Acanthurus,

western South Atlantic, North-eastern Brazil, naturalreefs, shipwrecks.

AbstractDiet and feeding behaviour of the three western

South Atlantic acanthurids (Acanthurus bahianus, A.chirurgus, and A. coeruleus) were analysed, based onstomach contents analysis and underwater observ -ations. Data were obtained at three natural reefs andtwo shipwrecks along the coast of Paraíba State, NEBrazil. The results of Schoener’s Index suggest thatdietary overlap was not significant between speciespairs; however, some degree of microhabitat segrega-tion was observed. Juveniles of A. bahianus and A.chirurgus formed feeding aggregations, whereas juve-niles of A. coeruleus foraged solitarily. Adults of thethree studied species formed intra- or interspecificfeeding groups. Following behaviour was observedbetween acanthurids and Halichoeres spp., Pseu du -peneus maculatus, and Sparisoma spp.

ZusammenfassungNahrung und Fressverhalten wurden anhand von

Mageninhalt-Analysen und Unterwasserbeobach t -ung en an drei Acanthuriden (Acanthurus bahianus, A.chirurgus und A. coeruleus) aus dem westlichenSüdatlantik untersucht. Die Daten wurden an dreinatürlichen Riffen sowie an zwei Schiffwracks gesam-melt, entlang der Küste vom State Paraíbo, NO-Brasilien. Die Ergebnis e, auf Schöners Index ausgew-ertet, zeigen an dass Nahr ungsüberschneidung unterArtpaaren nicht von Bedeutung war; jedoch es wurdeein gewisser Grad von Mikro-Habitatunterteilungbeobachtet. Jung tiere von A. bahianus and A. chirur-gus bildeten Fütterungsgruppen, währ end junge A.coeruleus als Ein zelgänger fraßen. Adulte Exemplareder untersuchten Arten bildeten intra- oder interspez-ifische Fressgruppen. Nachfolgeverhalten wurde unterAcanthuriden und Halichoeres-Arten, Pseudo peneusmaculatus und Sparisoma-Arten beobachtet.

Résumé

Le régime et le comportement alimentaires ont étéanalysés chez trois acanthurides de l’Atlantique du Sud-Ouest (Acanthurus bahianus, A. chirurgus and A.coeruleus), grâce á l’examen du contenu stomacal etd’observations en plongée. Les données ont été recueil-lies sur trois récifs naturels et deux épaves le long de lacôte de l’état de Paraiba, nord-est du Brésil. Les résul-tats de l’index de Schoener suggèrent que le chevau -chement des régimes alimentaires entre paires d’espè -ces n’est pas significatif; toutefois, un certain degré deségrégation par microhabitat a pu être observé. Lesjeunes de A. bahianus et de A. chirurgus fourragent encom mun, cependant que les jeunes de A. coeruleuss’alimentent solitairement. Les adultes des trois espècasobservées forment des groupes d’alimentation intra- etinterspécifiques. Un comportement d’accompagnementa été noté entre les acanthurides et Halichoeres spp.,Pseudopeneus maculatus and Sparisoma spp.

SommarioSulla base del contenuto intestinale e di osserva zioni

subacquee, vengono analizzate la dieta e le abitudini ali-mentari di tre specie di pesci chirurgo dell’Atlanticosudoccidentale (Acanthurus bahianus, A. chirurgus, e A.coeruleus). I dati sono stati raccolti nei pressi di tre bar-riere naturali e di due relitti sommersi, lungo la costadello Stato di Paraiba, nel Brasile nord-orientale. Il cal-colo dell’indice di Schoener mostra che non c’è una sig-nificativa sovrapposizione alimentare tra le specie. Sonostati tuttavia osservati fenomeni di segregazione dimicrohabitat. Durante la ricerca del cibo, gli individui gio-vani di A. bahianus e A. chirurgus si uniscono in grup pi,mentre quelli di A. coeruleus hanno abitudini so li tarie. Gliadulti di tutte e tre le specie formano invece gruppi intra-e interspecifici. Sono state inoltre osservate associazionialimentari con alcune specie dei generi Ha lichoeres eSparisoma e con Pseudupeneus maculatus.

IntroductionAmong reef fishes, surgeonfishes constitute a vis -

ually important group in tropical reefs (Alevizon, 1994)and represent, among herbivore fishes, an ecologic -ally and evolutionarily important component of tropical

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Food Resource and Habitat Sharing by the Three Western South Atlantic Surgeonfishes (Teleostei: Acanthuridae: Acanthurus)

reef communities (Randall, 1965). Together withparrotfishes they constitute the largest and mostmobile group of herbivore reef fishes which contributeto the transport of large amounts of inorganic nitro-gen, thus having an important role in the nutrientregeneration and cycling (Duarte & Acero, 1988).

In Brazil, surgeonfishes are visually striking reeffishes and are subject to commercial exploitation atvarious localities, chiefly as juveniles for the aquariumtrade, and more rarely as adults for human consump-tion. Despite this, they remain virtually unstudied inBrazil, except for the work by Ferreira et al. (1998) onseasonal grazing rates and food processing inAcanthurus bahianus.

This paper compares the feeding habits, diet, andfeeding behaviour of the three species of surgeonfishesfound in the western South Atlantic - Acanthuruscoeruleus Bloch & Schneider, 1801, A. chirurgus(Bloch, 1787), and A. bahianus Castelnau, 1855. Thethree species were chosen for the following reasons:they are all diurnal (Randall, 1967) and exhibit similarfeeding strategies that could lead to competition notonly for food but also for space (Duarte & Acero, 1988).Additionally, acanthurids constitute the most abundantfish family at the reefs of Paraíba State (Rocha et al.,1998), thus baseline data on these taxa could be usedfor monitoring the reefs in the study area.

Materials And MethodsStudy sites:

The study was carried out along the coast of ParaíbaState, NE Brazil (Fig. 1), at three natural reefs (Poço,Picãozinho, and Areia Vermelha) and two shipwrecks(Queimado and Alice) (Fig. 1, Table I), which wereconsidered as artificial reefs following the terminology

adopted by Potts & Hulbert (1994).Collections and stomach contents analyses:

Collections were made monthly from April 1998 toNovember 1999 (except June, July, and August, rainymonths with low visibility). A total of 209 specimenswere captured with spear gun or dip net (juveniles< 6 cm), and placed in ice to interrupt the digestiveprocess by thermal shock, following Aguiar &Filomeno (1995). Collections and observations at thenatural reefs were made through snorkelling, and atthe artificial reefs through SCUBA dives. All speci-mens were measured (standard length - SL and totallength - TL, in mm) and weighed (g) prior to analysis.Total length of examined specimens ranged from 38to 192 (A. bahianus), 32 to 229 (A. chirurgus) and 54to 262 (A. coeruleus). Stomachs were preserved in4% formalin. Field observations were made to char-acterise each studied locality (Table I). Voucher speci -mens were deposited in the fish collection at the Uni-versidade Federal da Paraíba, Brazil (UFPB).

Food items were weighed, and identified based onliterature (Joly, 1967; Littler et al., 1989) and with theaid of specialists. Scientific names for algae followWynne (1998). Stomach contents were analysedusing the Frequency of Occurrence and Gravimetricmethods, both as revised by Hyslop (1980) andMarrero (1994).

The results of the two analyses were combined intothe Index of Relative Importance (IRI of Pinkas et al.(1971), modified by Pérez-España & Abitia-Cárdenas(1996). In our study, intersections (abundance value%) were replaced by weight (%) as follows:

IRI = %P X %F100

where F = frequency of occurrence (expressed aspercentage %) and P = weight (%) of the item.

The Shannon-Wiener diversity index (H’) was usedto assess dietary diversity and evenness for eachspecies (Ludwig & Reynolds, 1988). Wet weight wasused as a proxy for volume. The overlap among dietsof surgeonfishes was determined using Schoener’s(1986) index (D), as follows:

D = 1-0.5 ∑ | Pxi - Pyi |

where Pxi is proportional weight of alimentary com -ponent i in the species X, and Pyi is proportionalweight of alimentary component i in the species Y.This overlap index varies from 0, when the twospecies use totally different resources, to 1, when theyuse the same food categories in the same propor-tions. According to Keast (1978), an overlap equal toor above 0.6 is considered significant.Feeding Behaviour:

Feeding behaviour was recorded at the five studysites through ad libitum observations, following Lehner(1979), totalling nine hours of observations per species.Fig. 1. Map of Paraíba State coast showing study sites.

Behaviours were recorded on an underwater slate, andfeeding strategies were photo graphed. Special atten-tion was given to foraging behaviour, feeding aggrega-tions, and use of space during feeding.

ResultsFood items consumed by A. bahianus, A. chirurgus,

and A. coeruleus, as well as IRI results, are given inTable II. Of the 27 species of algae identified, 12 wereconsumed by the three species, but there were differ-ences in the amount consumed by each. There werealso differences in the number of species and theamount of algae consumed per locality. Regarding thenumber of items consumed, A. coeruleus had the mostdiversified diet, utilising 34 items, whereas A. chirurgusconsumed 22 items and A. bahianus 18. According toIRI, the most important alga ingested at the natural reefsby A. chirurgus, A. bahianus, and A. coeruleus was thebrown alga Hypnea musciformis. However, overall themost important item ingested by A. chirurgus was theorganic material presumed to be present in the ingestedsediment (Fig. 2).

At the shipwrecks, A. chirurgus and A. bahianus mos -

tly consumed Osmundaria obtusiloba and A. coeruleusmainly utilised H. musciformis. Contents of sedimentwas also an important component of the diet of A. bahi-anus and A. chirurgus at the shipwrecks (Fig. 3).

In terms of dietary diversity, A. coeruleus attainedthe greatest diversity, both at natural and artificialreefs (natural reefs, H’ = 2.03; shipwrecks, H’ = 1.77).At natural reefs, A. bahianus had a lower dietary diver-sity (H’ = 1.19) than A. chirurgus (H’ = 1.48), the oppo-site occurring at the shipwrecks, where A. bahianushad a greater dietary diversity (H’ = 1.33) than A. chirurgus (H’ = 1.05). At the natural reefs, A. coeruleus showed the greatest dietary evenness (E = 0 .67) followed by A. chirurgus (E = 0.52) and A. bahianus (E = 0.48). A. bahianus had the greatestdietary evenness at shipwrecks (E = 0.82), followedby A. coeruleus (E = 0.60) and A. chirurgus (E = 0.51).

Although the three species consumed large num-bers of common items (mainly algae), both at naturalreefs and shipwrecks, according to Schoner's Indexdietary overlap was not significant within any speciespairs (D<0.6) (Table III). However, between A. coeruleus and A. chirurgus Schoener’s Index value

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Thelma L. P. Dias, Ierecê L. Rosa & Bertran M. Feitoza

Locality Depth Number of Characteristics(m) specimens

Poço reef 0.5-2.5 AB = 04ACH = 30

S 07°01' ACO = 18 W 34°48'

Picãozinho 0.3-4.5 AB = 15reef ACH = 24

ACO = 16S 07°07'W 34°48'

Areia 0.5-2.5 AB = 15Vermelha ACH = 19reef ACO = 09

S 07°01'W 34°49'

Queimado 9-18 AB = 11wreck ACH = 05

ACO = 09S 07°05'W 34°44'

Alice 7-12 AB = 05wreck ACH = 14

ACO = 13S 07°03'W 34°43'

Exposed portion during low tide covered by Caulerpa racemosa. Internal pools withmarked growth of Gracilaria cervicornis, Caulerpa racemosa, and Halimeda opuntia.Dictyota spp. and Dictyopteris spp. were also found. Upper portions of the pools facingthe continent with marked growth of Caulerpa racemosa and Halimeda opuntia. Por-tions closer to the bottom with Gracilaria cervicornis, Sargassum sp., and Lobophoravariegata. In areas with sandy bottoms the main algae were Penicillus capitatus andUdotea flabellum. In sheltered areas and in crevices the most abundant alga was Gelid-ium sp. Main coral species: Siderastrea stellata, Montastrea cavernosa, and Milleporaalcicornis. Bottom: chiefly calcareous rubble (Halimeda and fragments of gastropodshells). Use of the area: small-scale fishing and tourism.

Internal pools with marked growth of Sargassum sp., Halimeda opuntia, and Dicty-opteris spp. Pools connected to the sea with a predominance of Halimeda opuntia, Dic-tyopteris spp., and Dictyota spp. Reef front mainly with Caulerpa racemosa and Hal-imeda opuntia. Main coral species: Siderastrea stellata, Mussimilia hartii, M. hispida,and Millepora alcicornis. Bottom: calcareous rubble (Halimeda) in the internal pools andfine-grained sediment in open and deeper areas. Use of the area: small-scale fisheryand intense tourism.

Pools facing the continent with abundance of Hypnea musciformis, and also Acanth -ophora spicifera, Padina sp., and Sargassum sp. Pools connected to the sea mainly withGracilaria cervicornis and Ochtodes secundiramea. Main coral species: Siderastreastellata, Millepora alcicornis, and Montastrea cavernosa. Bottom: sandy (fragments ofgastropod shells and of Foraminifera). Use of the area: intense tourism and small-scaleand recreational fisheries.

Bottom formed by pebbles covered by Osmundaria obtusiloba, Bryothamnion tri-quetrum, and Lobophora variegata. Wrecks covered by Bryopsis pennata. Presence ofdrifting Caulerpa racemosa, C. mexicana, C. cupressoides, C. prolifera, Dictyota spp.,Dictyopteris spp., and Hypnea musciformis. Use of the areas: small-scale fishery,tourism (SCUBA diving), and spearfishing.

Table I. Characteristics of the study sites, and number of specimens captured per locality. AB = Acanthurus bahianus;ACH = Acanthurus chirurgus,and ACO = Acanthurus coeruleus.

was near to significant (D = 0.59), suggesting somedegree of dietary overlap.

A. bahianus usually exploited algae located on thelateral walls of the natural reefs, only occasionallyfeeding near the substrate, in areas where the bottomwas covered by algae (Fig. 4).

At the artificial reefs, where algal growth was mostlylimited to the small rocks surrounding the wrecks, A.bahianus (as well as A. chirurgus and A. coeruleus) wasseen feeding either on the algae attached to the rocks(Fig. 5), or, more rarely, on drifting algae. A. chirurgussearched for food both in the water column (up to about10 cm below the surface) and on the bottom (Fig. 6, a-b), and was also seen consuming drifting algae.

A. coeruleus fed mostly on the apical portions of thealgae located on the upper portions of the lateral walls

of the reef. On one occasion one specimen was seenfeeding on the bottom, where one specimen of A.chirurgus was also found. The A. chirurgus reactedaggressively to the presence of the intruder, andchased it away. We also occasionally observed sol -itary juvenile specimens of A. coeruleus foraging withA. bahianus and A. chirurgus (Fig. 7).

A. bahianus formed feeding aggregations both at thenatural reefs and shipwrecks; however, at the naturalreefs juveniles and adults seemed to be spatially seg-regated, with the former occupying the shallowerpools, and the latter utilising the deeper pools or thereef front. Occasionally adults were seen in the shallow pools, but they did not form aggregations.

In all aggregations of juveniles of A. bahianus, aswell as those of young A. chirurgus, or in mixed aggre-

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Species A. bahianus A. chirurgus A. coeruleus

NR SW NR SW NR SW

Division RhodophytaAcanthophora spicifera 0.321 0.004 0.268Botryocladia occidentalis 0.004 0.032 <0.001Bryothamnion seaforthii <0.001 0.081 0.004 0.198Bryothamnion triquetrum 0.017 0.006 14.210Ceramium sp. <0.001 0.010Corallinaceae <0.001 <0.001 0.012 0.117Cryptonemia crenulata <0.001 0.010 0.031Gelidiella sp. 0.005Gelidium sp. 0.003 0.695Gracilaria caudata 0.049 <0.001 0.027Gracilaria cervicornis 1.309 1.351 3.756Gracilaria sp. 1.149 8.544 0.093 4.490 0.197 1.007Hypnea musciformis 37.866 5.075 0.123 10.112 15.424Osmundaria obtusiloba 14.825 5.411 <0.001 8.588Unidentified Rhodophyta 0.217 0.005 0.012 0.037 0.439

Division PhaeophytaDictyota sp. 0.063 <0.001 0.057 1.015 0.560Dictyopteris sp. 0.009 0.021 3.436Lobophora variegata 0.003 0.015 0.126Spatoglossum schoederi 0.024

Division ChlorophytaBryopsis pennata <0.001 <0.001Caulerpa cupressoides 0.312Caulerpa mexicana 0.072 0.026Caulerpa prolifera 0.158Caulerpa racemosa 0.667 0.342 5.067Caulerpa sertularioides <0.001Udotea flabellum <0.001Unidentified Chlorophyta <0.001 <0.001 0.003

Diatoms <0.001Phylum Porifera <0.001Phylum Cnidaria

Class Hydrozoa <0.001 <0.001 0.004 0.005Phylum Mollusca

Class Gastropoda 0.065 <0.001Phylum Arthropoda

Class Crustacea (fragment) <0.001 Silt 0.062 <0.001Unidentified Vegetable Organic Matter 0.383 3.123 0.028 0.578 0.155 1.477Sediment 0.654 8.905 18.508 36.356 0.023

Total Number of Items Ingested 15 6 20 9 27 22

Table II. Food items consumed by A. bahianus, A. chirurgus, and A. coeruleus at natural reefs (NR) and shipwrecks (SW),as expressed by the IRI.

chirurgus, A. bahianus, Spar isoma axillare (Scar idae)Halichoeres brasiliensis, and H. maculipinna (Labri-dae).

No solitary juveniles of A. bahianus were seen, andgroups of juveniles were mostly found in depths ofless than 1 m. On the other hand, adult specimens ofA. bahianus were seen either solitary or in schools,usually in areas deeper than 1 m. At the shipwrecks,A. bahianus was frequently seen feeding in conspec -ific schools and also forming feeding aggregationswith A. chirurgus, S. axillare, H. brasiliensis, H. mac-ulipinna, H. bivittatus, and Pseudupeneus maculatus(Mullidae). On various occasions, while specimens of

gations of young of both species, we observed at leastone specimen of parrotfish (Sparisoma radians or S.axillare) (Fig. 8) feeding with the surgeonfishes. AtPicãozinho reef, on one occasion we sighted a rela-tively large school (approximately 100 specimens) ofyoung A. bahianus (average size about 50 mm TL).The individuals grazed repeatedly, but not in a syn-chronous way, as they swam over areas occupied bythe damselfish Stegastes fuscus (Pomacentr idae).The damselfishes attacked the passing school, whichin turn avoided the attack by temporarily splitting upand then moving away from the territory. We alsosighted heterospecific feeding groups formed by A.

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Fig. 2. IRI values of Acanthurus bahianus (a),A. chirurgus (b), and A. coeruleus (c) at natural reefs.

Fig. 3. IRI values of Acanthurus bahianus (a),A. chirurgus (b), and A. coeruleus (c) at shipwrecks.

P. maculatus probed the substrate with their barbels,A. bahianus and A. chirurgus fed on the turned-overmaterial. During this feeding interaction, P. maculatusexhibited a red coloration resembling that of the sub-strate, and after cessation of the behaviour it resumedits usual whitish background coloration with longitud -inal black spots. Both juveniles and adults of A. chirur-gus formed feeding aggregations at the natural reefs,as well as mixed schools with Abudefduf saxatilis(Pomacentridae), S. axillare, and Halichoeres spp.

Young specimens of A. chirurgus fed on algaelocated on the top of the reef, whereas adults wereusually found in depths greater than 1 m. Specimenslarger than 20 cm TL were solitary whenever found indepths of less than 1 m (Fig. 9). At the shipwrecks,individuals of A. chirurgus larger than 6 cm TL formedmixed schools with A. bahianus, whereas smallerindividuals formed only conspecific schools.

Contrary to the pattern observed in A. bahianus and

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Fig. 4. Juvenile Acanthurus bahianus swimming over analgae-covered bottom at Areia Vermelha reef, Paraíba,Brazil. Note the presence of one specimen of parrotfish(Sparisoma axillare). Photo by B. M. Feitoza.

Fig. 5. Adult Acanthurus bahianus feeding on algaeattached to the rocks at Queimado wreck, Paraíba,Brazil. Photo by B. M. Feitoza.

Fig. 7. Solitary juvenile Acanthurus coeruleus foragingwith juvenile A. bahianus and A. chirurgus at Picãozinhoreef, Paraíba, Brazil. Photo by B. M. Feitoza.

Fig. 6. (a) Foraging group of Acanthurus chirurgus feeding on substrate at Picãozinho reef, Paraíba, Brazil; (b) Solitaryadult of Acanthurus chirurgus feeding on hard substrate at Picãozinho reef, Paraíba, Brazil. Photos by B. M. Feitoza.

a b

A. chirurgus, juveniles of A. coeruleus were not seenforming feeding aggregations, either at the naturalreefs or at the shipwrecks. The few juveniles sightedwere solitary and occupied shallow and isolatedpools, generally in areas close to crevices wherethese individuals could take refuge (Fig. 10). Interest-ingly, many individuals larger than 100 mm TL seenat the shipwrecks retained the juvenile-phase colourpattern (completely yellow or blue body with yellowtail). At both natural and artificial reefs, adults of A.coeruleus formed large schools (with about 30 indiv -iduals) which were commonly seen feeding on thenatural reef walls, or around the wrecks. Schools were

generally monospecific, however mixed schools of A.coeruleus, A. chirurgus, and A. bahianus were alsooccasionally observed.

Our data indicate that red algae predominated in thediet of the basically herbivorous A. coeruleus, andalso constituted an important component of the diet ofA. bahianus and A. chirurgus. According to Duarte &Acero (1988), the last-named two species are consid-ered to be omnivores that supplement a herbivorousdiet with detritus and the microfauna associated withthe benthos, and in captivity can even become carni-vores. It is known that herbivorous fishes have a highrate of food ingestion but a low assimilation rate (Ogden

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Fig. 10. Solitary juvenile of Acanthurus coeruleus neara crevice at Picãozinho reef, Paraíba, Brazil. Photo by B. M. Feitoza.

Fig. 9. Solitary adult of Acanthurus chirurgus in a shallow pool at Picãozinho reef, Paraíba, Brazil.Photo by B. M. Feitoza.

Fig. 8. Mixed foraging group of juvenile Acanthurus bahianus and A. chirurgus feeding on Dictyopteris sp. in the upperportions of the Picãozinho reef, Paraíba, Brazil. Note one juvenile specimen of parrotfish on lefthand side. Photo by B. M. Feitoza.

& Lobel, 1978). This could lead some species, as in thecase of A. bahianus and A. chirurgus, to seek alterna-tive food sources such as sediment, which, as pointedout by Duarte & Acero (1988), may contain a rich inter-stitial community.

Previous work on the feeding habits of acanthurids (egRandall, 1967; Clavijo, 1974; Duarte & Acero, 1988)noted a greater dietary similarity between A. bahianusand A. chirurgus than between either species and A.coeruleus. This similarity was associated by Clavijo(1974) with a relatively greater similarity in the morpho -logy of their branchial arches and pharyngeal teeth, andin the stomach wall. Randall (1967), Clavijo (1974),Duarte & Acero (1988), and Bölhke & Chaplin (1993)remarked that A. bahianus and A. chirurgus have athicker-walled stomach, adapted to the consumption offine sedimentary particles, organic debris, and filament -ous algae, whereas A. coeruleus possesses a thin-walled stomach and seems to be best adapted to pro-cessing filamentous algae and harder plants. Based onthese observations, Duarte & Acero (1988) hypothe-sised that A. chirurgus and A. bahianus (but not A.coeruleus) shared a common niche, and indicated that,as the food items eaten by A. chirurgus, A. bahianus, andA. coeruleus were close to one another, the threespecies would compete not only for food but also forspace.

In our study, despite the observed similarities in termsof feeding habits and of food items consumed by thethree acanthurids, the overall feeding niche overlapwas low and not significant (D < 0.6), and this could beseen as an indication of low competition. However, theobserved lack of dietary overlap could be a conse-quence of Schoener’s index placing a strongeremphas is on the proportional weight of the items thanon their occurrence in the diet, and does not necessar-ily provide evidence for food resource segregation. Fur-thermore, as mentioned by Clavijo (1974), it is probablethat A. bahianus, A. chirurgus, and A. coeruleus main-tain their identities as different species because of sub-tle differences in other aspects of their biology.

Regarding space utilisation, a possible segregationwas observed in the distinct food-search patterns of thethree species. In the case of A. bahianus and A. chirurgus, although they ingested relatively largeamounts of sedimentary material, few individuals of theformer species were seen feeding directly on the sub-strate, suggesting that in A. bahianus sedimentarymaterial was obtained mainly from the ingested algae

rather than from the reef bottom where A. chirurgus for-aged. In the case of A. coeruleus and A. chirurgus, theformer species searched for food on the upper portionsof the lateral walls of the reefs, and did not utilisesedimentary material, differing in this respect from A.chirurgus and also from A. bahianus.

The values of Schoener’s Index were generally lowerat the natural reefs, possibly because of their greaterstructural complexity and shallower location, whichresulted in greater availability of algae. Parameterssuch as luminosity and site topography were probablythe main reasons for the observed differences in algaeabundance between coastal reefs and shipwrecks. Theapparently lower abundance of green algae on the arti-ficial reefs possibly results from their deeper location,and consequent lower light penetration.

In terms of feeding categories (sensu Jones, 1968),A. bahianus and A. chirurgus are considered to be"grazers" that ingest inorganic material with the algae,and A. coeruleus is considered to be a "browser" thatingests food with little or no inorganic material (Randall,1967; Clavijo, 1974). Randall (1965, 1967) suggestedthat the large amounts of inorganic material ingested byadults of A. bahianus and A. chirurgus are used forgrinding the ingested algae into finer particles. How-ever, in our study the grinding role of the sediment wasnot so apparent in A. chirurgus, as the algal piecesfound in its stomach and intestine did not visually differfrom one another in terms of size and consistency.Regarding the number of items consumed, A.coeruleus exhibited the most diversified diet, not show-ing a marked preference for any particular food item,which resulted in the relatively high evenness valuesobtained both at the natural reefs and at the ship-wrecks. However A. bahianus was responsible for thehighest evenness values obtained in this study, eventhough its dietary diversity was relatively low in com-parison to that of A. coeruleus.

In the three species studied, there seemed to be arelationship between resource availability and con-sumption which could be interpreted as an indication oflow selectivity on the part of the acanthurids. However,similar to what has been observed by Clavijo (1974),some visibly abundant algae such as Halimeda opun-tia, Udotea flabellum, Penicillus capitatus, Padina gym-nospora, and Sargassum sp. were not consumed, orwere ingested in extremely low amounts, perhaps sug-gesting an avoidance on the part of the surgeonfishes.According to Hay (1991), the resistance to herbivoryexhibited by many species of Halimeda can be attrib-uted to both morphological (calcification) and chemicaldefences. The same author also suggested that thedefences developed by Halimeda may be responsiblefor its abundance in most of the shallow reef habitats,characterised by intense herbivory by grazers. In fact,various studies (eg Norris & Fenical, 1982; Lewis et al.1987; Paul, 1987) indicate that, in response to herb -ivory, many species of algae develop different methods

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Schoener Index Value

Species pair Natural Reefs Shipwrecks

A. bahianus - A. chirurgus 0.46 0.39A. bahianus - A. coeruleus 0.40 0.52A. coeruleus - A. chirurgus 0.24 0.59

Table III. Dietary overlap in Acanthurus bahianus,A. chirurgus, and A. coeruleus.

of resistance, by means of considerable morphologicalvariations and production of poisonous metabolites,such that many of the relatively abundant algae acces-sible to herbivores contain biologically active sub-stances.

On the other hand, Paul (1987) mentioned that themain natural products of Udotea and Halimeda may notbe effective against grazers. Furthermore, as pointed outby Norris & Fenical (1982), in some cases spec ialisedherbivores have seemingly co-evolved with their foodsource and acquired tolerance of chemical deterrents,and even use them in their own defences against preda-tors. Additionally, it is worth nothing that one of the algaeconsumed by the species studied, particularly by A.coeruleus at the natural reefs, was Caulerpa racemosa,an abundant alga at the sites studied. In much the sameway, Randall (1967) and Earle (1972), studying A. bahi-anus, A. coeruleus, and A. chirurgus in the VirginIslands, recorded Sargassum spp., Halimeda spp., andUdotea sp. in their diets, but, as the amounts ingested bythe species are not given in those two studies, a directcomparison with our data is not possible. Although noexperiment was conducted to test the toxicity of C. race-mosa, the family Caulerpaceae, to which that speciesbelongs, is known to include species capable of produc-ing secondary metabolites, such as caulerpina, whichcan act as ichthyotoxins (Paul & Fenical, 1986).

In tropical waters, the family Acanthuridae is char -acterised by forming mono- or heterospecific “foraginggroups" (Ogden & Lobel, 1978). These groups prob ablyfunction as a protection against predators and toincrease efficiency during feeding, especially in areaswhere territorial fishes control part of the availableresources for feeding (Robertson et. al., 1976; Alevizon,1994).

Foraging groups or feeding aggregations were fre-quently observed for the studied species of Acanth urus.Contrary to the results obtained by Lawson et al. (1999)in Barbados, where no schools of juvenile A. bahianuswere seen, in our study large groups of juv eniles of thatspecies were sighted at the natural reefs, especially inshallow pools. Interspecific groups formed by juvenilesof A. bahianus and A. chirurgus were seen frequentlyaccompanied by parrotfishes (Sparisoma axillare and S.radians) mostly in areas occupied by damselfishes (Ste-gastes variabilis and S. fuscus). Perhaps, as observedby Lawson et. al. (1999), school size can be related tothe density of territorial fishes, supporting the hypothesisthat the large schools of acanthurids seen in our studypermit exploitation of the high quality food found insidethe territories of the damselfishes. Risk (1998) showedthat recruits of A. bahianus preferred places with con-specifics and avoided places where Stegastes leucos-tictus occurred. Robertson et. al. (1976) suggested thatthe presence of parrotfish can reduce the impact ofaggressive attacks on the part of territorial fishes.

Juveniles of A. coeruleus, on the other hand, weremostly solitary (even while searching for food), a

pattern also observed by Clavijo (1974) and Bell &Kramer (2000), although on a few occasions juvenileindividuals were seen feeding with other acanthurids orparrotfishes, perhaps seizing upon the temporary pro-tection offered by the group.

The following behaviour observed among A. bahianus,A. chirurgus, and the goatfish Pseudupeneus macula-tus (Mullidae) has also been recorded by Earle (1972).According to Strand (1988), invertebrates which burrowin the sand are flushed out by the foraging activity ofstingrays, goatfishes, and other sand-flat foragers, andspecies in or under algal coverings are displaced by thegrazing of herbivores. Small generalised pred ators (thefollowers) are able to capitalise upon this displacementor uncovering of prey items. In the case where Acan-thurus chirurgus and A. bahianus foraged in a mixedgroup composed of Halichoeres spp., Pseudup eneusmaculatus, and Sparisoma axillare, we observed thatwhile the Acanthurus species fed on the materialflushed by Pseudupeneus maculatus, the goatfish andHalichoeres species preyed upon organisms displacedby the foraging activities of the Acanthurus species andSparisoma axillare, possibly resulting in benefits to boththe surgeonfishes and the other followers.

In general, A. coeruleus can be considered a morespecialised feeder, ingesting almost exclusively algae,and generally foraging on the upper portions of reefwalls. A. bahianus and A. chirurgus are more “general-ist” species which obtain additional food items throughthe ingestion of sedimentary material. Some degree offood resource and microhabitat partitioning was foundduring this study, but this does not provide an argu-ment for competition among the three studied acan-thurids. As pointed out by Sala & Ballesteros (1997),experimental studies are needed to ascertain whetheror not the observed patterns are a result of competitionbetween species.

AcknowledgementsWe are grateful to Amélia Kanagawa and George

Miranda for help in algae identification, Ismar Just forproviding SCUBA gear, Cristina Buitron for help infield activities, Marileide Miranda and João Feitoza forlogistical support, and CNPq (Conselho Nacional deDesenvolvimento Científico e Tecnológico) for financ -ial support.

ReferencesAguiar, J. B. S. & M. J. B. Filomeno, 1995. Hábitos

alimentares de Orthopristis ruber (CUVIER, 1830),(Osteichthyes - Haemulidae) na Lagoa da Con-ceição, SC, Brasil. Biotemas 8 (2): 41-49.

Alevison, W. S., 1994. Caribbean Reef Ecology.Pisces Books, Houston. 115 pp.

Bell, T. & D. L. Kramer, 2000. Territoriality and habitatuse by juvenile blue tangs, Acanthurus coeruleus.Environmental Biology of Fishes 58: 401-409.

Böhlke, J. E. & C. C. G. Chaplin,1993. Fishes of the

aqua vol. 5 no. 1 - 20019


Bahamas and Adjacent Tropical Waters (2nd edition).University of Texas Press, Austin. 771 pp.

Clavijo, I. E., 1974. A contribution to the Feeding Habitsof Three Species of Acanthuridae (Pisces) from theWest Indies. Master’s Thesis, Florida Atlantic Univer-sity, Boca Ratón, U.S.A. 44 pp.

Duarte C. S. A. & A. Acero P.,1988. Hábitos alimenta-res de los peces del género Acanthurus (Perciformes:Acanthuridae) en la región de Santa Marta (CaribeColombiano). Revista de Biologia Tropical 36 (2B):399-405.

Earle, S. A., 1972. The influence of herbivores on themarine plants of Great Lameshur Bay, with an annot -ated list of plants. In: Collette, B. B. & S. A. Earle,(eds.), Results of the Tektite Program: ecology of coralreef fishes. Natural History Museum, LosAngeles County, Science Bulletin 14: 17-44.

Ferreira, C. E. L., Peret, A. C. & R. Coutinho, 1998.Seasonal grazing rates and food processing by trop -ical herbivorous fishes. Journal of Fish Biology 53(Supplement A): 222-235.

Hay, M. E., 1991. Fish-Seaweed interactions on coralreefs: effects of herbivorous fishes and adaptations oftheir prey. 96-119. In: Sale, P.F. (ed.). The Ecology ofFishes on Coral Reefs. Academic Press, Inc., 754 pp.

Hyslop. E. J., 1980. Stomach contents analysis - areview of methods and their application. Journal ofFish Biology 17: 411-429.

Joly, A .B., 1967. Gêneros de Algas Marinhas daCosta Atlântica Latino-Americana. Editora da Univer-sidade de São Paulo, São Paulo. 461 pp.

Jones, R. S., 1968. Ecological relationships in Hawai-ian and Johnston Island Acanthuridae (surgeon-fishes). Micronesica 4: 309-361.

Keast, A., 1978. Trophic and spatial interrelationshipsin the fish species of an Ontario temperate lake.Environmental Biology of Fishes 3: 7-31.

Lawson, G. L., Kramer, D. L. & W. Hunte., 1999. Size-related habitat use and schooling behavior in twospecies of surgeonfish (Acanthurus bahianus and A.coeruleus) on a fringing reef in Barbados, WestIndies. Environmental Biology of Fishes 54: 19-33.

Lehner, P. N., 1979. Handbook of Ethological Methods.Garland STPM Press, New York. 403 pp.

Lewis, S. M., Norris, J. N. & R. B. Searles, 1987. Theregulation of morphological plasticity in tropical reefalgae by herbivory. Ecology 68 (3): 636-641.

Littler, D. S., Littler, M. M., Bucher, K. E., & J. N. Nor-ris, 1989. Marine Plants of the Caribbean: a fieldguide from Florida to Brazil. Smithsonian InstitutionPress, Washington. 263 pp.

Ludwig, J. A. & J. F. Reynolds, 1988. Statistical eco -logy. John Wiley and Sons, Inc., New York. 337 pp.

Marrero, C., 1994. Métodos para Cuantificar Con-tenidos Estomacales en Peces. Talleres Gráficos deLiberil, Caracas, Venezuela. 37 pp.

Norris, J. N. & W. Fenical, 1982. Chemical defense intropical marine algae. 417-431. In: Rützler, K. & I.G.

Macintyre (eds.), The Atlantic Barrier Reef Ecosystemat Carrie Bow Cay, Belize. 1. Structure and Communi-ties. Smithsonian Contributions to the Marine Sci-ences 12, 539 pp

Ogden, J. C. & P. S. Lobel, 1978. The role of herbivor -ous fishes and urchins in coral reef communities.Environmental Biology of Fishes 3: 49-63.

Paul, V. J. 1987. Feeding deterrent effects of algal nat-ural products. Bulletin of Marine Science 41 (2): 514-522.

Paul, V. J. & W. Fenical, 1986. Chemical defense intropical green algae, order Caulerpales. MarineEcology Progress Series 34: 157-169.

Pérez-España, H. & L. A. Abitia-Cárdenas, 1996.Description of the digestive tract and feeding habits ofthe King angelfish and the Cortes angelfish. Journalof Fish Biology 48: 807-817.

Pinkas, L., Oliphant, M. S., & I. L. K. Iverson, 1971.Food habits of albacore, bluefin tuna and bonito inCalifornia waters. Fishery Bulletin 152: 1-105.

Potts, T. A. & A. W. Hulbert, 1994. Structural influencesof artificial and natural habitats on fish aggregations inOnslow Bay, North Carolina. Bulletin of Marine Sci-ence 55 (2): 609-622.

Randall, J. E., 1965. Grazing effects on sea grasses byherbivorous reef fishes in the West Indies. Ecology 46(3): 255-260.

Randall, J. E., 1967. Food habits of reef fishes of theWest Indies. Studies in Tropical Oceanography 5:665-847.

Risk, A., 1998. The effects of interactions with reefsresidents on the settlement and subsequent persist ence of ocean surgeonfish, Acanthurus bahianus.

Environmental Biology of Fishes 51: 377-389.Robertson, D. R., Sweatman, H. P. A., Fletcher, E. A.,

& M. G. Cleland, 1976. Schooling as a mechanism forcircumventing the territoriality of competitors. Ecology57 (6): 1208-1220.

Rocha, L. A., Rosa, I. L. & R. S. Rosa, 1998. Peixesrecifais da costa da Paraíba, Brasil. Revista Brasileirade Zoologia 15 (2): 553-566.

Sala, E. & E. Ballesteros, 1997. Partitioning of foodand space resources by three fish of the genus Diplo-dus (Sparidae) in a Mediterranean rocky infra littoralecosystem. Marine Ecology Progress Series 152:273-283.

Schoener, T. S., 1986. The Anolis lizards of Bimini:resource partitioning in a complex fauna. Ecology 49:704-725.

Strand, S., 1988. Following behavior: interspecific for-aging associations among Gulf of California reeffishes. Copeia 1988: 351-357.

Wynne, M. T., 1998. A checklist of benthic marine algaeof the tropical and subtropical Western Atlantic (firstrevision). Nova Hedwigia, J. Cramer, Stuttgart. 155 pp.

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