Latitudinal gradients in Atlantic reef fish communities: trophic structure and spatial use patterns

Transcription

1 Journl of Fish Biology (2004) 64, doi: /j x, ville online t Ltitudinl grdients in Atlntic reef fish communities: trophic structure nd sptil use ptterns S. R. FLOETER*,C.E.L.FERREIRA, A. DOMINICI-A ROSEMENA AND I. R. ZALMON* *L. de Cieˆncis Amientis, Universidde Estdul do Norte Fluminense, Av. Alerto Lmego, 2000, Cmpos dos Goytczes, RJ, , Brsil, Depto. de Ocenogrfi, IEAPM, Ru Kioto 253, Arril do Co, RJ, , Brsil nd Center for Tropicl Mrine Ecology (ZMT), Fhrenheitstrsse 6, , Bremen, Germny (Received 1 August 2003, Accepted 19 Mrch 2004) Trophic strtegies nd sptil use hits were investigted in reef fish communities. The results supported the hypothesis of differentil use of food resources mong tropicl nd higher ltitude reef fishes, i.e. the numer of species nd reltive undnce of fishes relying on reltively low-qulity food significntly decresed from tropicl to temperte ltitudes. The species : genus rtio of low-qulity food consumers incresed towrd the tropics, nd ws higher thn the overll rtio considering ll fishes in the ssemlges. This supports the view tht higher specition rtes occurred mong this guild of fishes in wrm wters. It ws lso demonstrted tht density of herivorous fishes (the dominnt group relying on low-qulity food resources) in the western Atlntic decresed from tropicl to temperte ltitudes. Sptil use nd moility vried with ltitude nd consequently reef type nd complexity. Fishes with smll-size home rnges predominted on tropicl corl reefs. # 2004 The Fisheries Society of the British Isles Key words: community structure; herivory; ltitudinl grdient; mcroecology; reef fishes. INTRODUCTION Fish diversity chrcteristiclly decreses from tropicl to temperte ltitudes (Eeling & Hixon, 1991; Hoson, 1994; Briggs, 1995). In the Atlntic Ocen, the Crien is the centre of diversity, oth in terms of fishes nd corls (Briggs, 1995; Veron, 1995; Floeter & Gsprini, 2000). The extent to which fish trophic structure is modified etween tropicl corl reefs of the Crien nd mrginl rocky reefs of the Atlntic, however, remins unknown. A functionl ctegoriztion pproch could e useful tool for gthering rod-scle dt on community structure, trnscending txonomic oundries (Bellwood et l., 2002). Thus, it is possile to infer generl evolutionry trends sed on ecologiclly relevnt ttriutes such s feeding performnce Author to whom correspondence should e ddressed t present ddress: Ntionl Center for Ecologicl Anlysis nd Synthesis, University of Cliforni, Snt Brr, 735 Stte Street Suite 300, Snt Brr, CA , U.S.A. Tel.: þ ; fx: þ ; emil: floeter@nces.ucs.edu # 2004 The Fisheries Society of the British Isles 1680

2 REEF FISH LATITUDINAL GRADIENTS 1681 (i.e. functionl morphology, physiology nd iomechnics), moility mplitude nd resource-use ptterns used y reef fishes. Trophic strtegies, food vilility nd sptil use hits certinly ply n importnt role in shping ptterns of undnce nd hitt distriution in fishes (Hrmelin-Vivien, 1989; Bellwood et l., 2002; Winwright & Bellwood, 2002). Trophic strtegies re n importnt functionl ttriute tht could e distinct etween tropicl nd temperte regions. For exmple, the reltive diversity of herivorous fishes is known to decrese drsticlly in colder wters (Horn, 1989; Chot, 1991; Eeling & Hixon, 1991). In recent review, Hrmelin-Vivien (2002) hypothesized n evolutionry trend towrd the etter use of less energetic food resources mong tropicl reef fish communities (in contrst to temperte res), sed on qulittive comprisons etween feeding ehviours nd fish phylogeny nd iogeogrphy. She rgued tht the high diversity of fishes occurring on corl reefs is relted to the sustined higher tempertures in the tropics over geologicl time, nd to the more efficient use nd trnsfer of energy permitted y long-term temperture stility. Plnktivore, piscivore nd motile inverterte-feeding fishes tht et high protein nd energy-rich food with high ssimiltion rtes (Bowen et l., 1995) form the most diverse trophic group worldwide (Rndll, 1967; Hrmelin-Vivien, 1989; Jones et l., 1991; Ferreir et l., 2004). Mny reef fishes, however, exhiit morphologicl nd physiologicl speciliztion to exploit comprtively low-qulity resources like lge, segrsses, detritus nd sessile invertertes (e.g. sponges, cnidrins nd scidins) nd indeed sustin lrge popultions in the tropics (Chot, 1991; Bruggemnn, 1994; Dunlp & Pwlik, 1996; Hill, 1998). Although undnt nd esy to locte, these resources re usully structurl nd chemiclly defended ginst grzing (Hy, 1991, 1997; Pul, 1992; Epifˆnio et l., 1999; Burns & Iln, 2003; Burns et l., 2003) nd their processing nd ssimiltion present mjor chllenge to the digestive system (Horn, 1989; Chot, 1991; Meyln, 1991; Chot & Clements, 1998). Compred to crnivores, they hve to ingest lrger quntities of food to compenste for low nutritionl vlue (Bruggemnn et l., 1994; Bowen et l., 1995; Ferreir et l., 1998, ; Horn, 1998). For exmple, herivorous fishes my et mny times their required energetic needs in order to gin enough nitrogen from seweeds (Hy, 1991). Some prrotfishes (Scride) spend over 90% of the dy forging, tking thousnds of ites per dy (Crpenter, 1986; Hy, 1991; Bruggemnn, 1994; Bruggemnn et l., 1994), nd the sme occurs with sponge-eting ngelfishes (Pomcnthide) (Dunlp & Pwlik, 1996). Corllivores, herivores, detritivores nd omnivores lso tend to hve longer intestines thn do crnivores, whose diets re more nutritious (Goldschmid et l., 1984; Horn, 1989, 1998; Elliott & Bellwood, 2003). An explntion for this pttern is tht fishes relying on low-protein diets require longer guts, i.e. lrge surfce re reltive to volume, in order to process the lrge mount of poor-qulity food needed (Horn, 1998). Another functionl spect tht could differentite tropicl fish ssemlges from colder ones is the sptil use nd moility ptterns of fishes. At tropicl corl reefs, mny species (minly herivores or sessile inverterte feeders) hve smll-size home rnges or swim close to the corl mtrix (Hrmelin-Vivien, 1989). Some even defend their territory in very ggressive wy, like the herivorous dmselfishes (Pomcentride) (Roertson, 1996; Ceccrelli et l.,

3 1682 S. R. FLOETER ET AL. 2001). Structurl complexity hs een correlted to reef fish spce utiliztion (Luckhurst & Luckhurst, 1978) nd undnce (Bell & Glzin, 1984; Friedlnder & Prrish, 1998; S.R. Floeter, C.E.L. Ferreir & J.L. Gsprini unpul. dt) indicting tht iogenic reefs could potentilly sustin higher fish densities thn non-reef-uilding peripherl res, especilly site-ttched species. In true corl reefs, structurl complexity is ssocited with corl growth form, especilly those rorescent or rnching forms in the shllower wters. On rocky shore systems, topogrphic complexity relies mostly on the presence or sence of holes (Ferreir et l., 2001; S.R. Floeter, pers. os.). In contrst to previous pulictions (Hrmelin-Vivien, 1989, 2002), the present work exmined trophic strtegies, sptil use nd moility ptterns, sed on quntittive (i.e. reltive undnce nd density) dt collected long rod ltitudinl grdient in the Atlntic, s well s pulished dt. Two specific questions were ddressed: 1) is diversity nd undnce of fishes tht use reltively low-cloric food resources higher in the tropics thn in sutropicl or temperte regions? 2) Does fish sptil use (i.e. differentil moility nd home-rnge ptterns such s schooling ehviour nd territorility) vry ccording to ltitude nd reef type (i.e. corl v. rocky reefs)? MATERIALS AND METHODS DATASETS Three dtsets were used, the first one with reltive undnce of reef fishes derived from replicted strip trnsects: underwter visul censuses (UVC) conducted in the Bocs del Toro, Pnm (Crien), Gurpri Islnds (south-est Brzil) nd Arvoredo (south Brzil) (Tle I). The smpling design included different hitts within ech site, covering reefs of vrious depths, exposures nd complexity profiles. Replicted point-count censuses from the Cnries (Bortone et l., 1991; Flcon et l., 1996; Hjgos & Vn Tssell, 2001) were lso included in the dtse. Assemling dt from different smpling methods is lwys prolemtic for sttisticl purposes, however, in recent method re-evlution, Smoilys & Crlos (2000) did not find significnt differences etween trnsect nd point-count visul censuses for mny tx. In order to verify if the results otined from the four sites could e generlized for their entire regions, second dtse ws compiled from the literture, with the ddition of seven more sites: Florid Keys, N (Bohnsck & Bnnerot, 1986); Cyos Cochinos, Hondurs, N (Clifton & Clifton, 1998); Mnuel Luiz Reefs, north-est Brzil, S (Roch & Ros, 2001); Tmndre, north-est Brzil, S (B.P. Ferreir, unpul. dt); Arolhos Reefs, north-est Brzil, S (C.E.L. Ferreir, unpul. dt); Arril do Co, south-est Brzil, 23 S (C.E.L. Ferreir, unpul. dt); south-est Mediterrnen, Spin, N(Grcı -Chrton & Pérez-Ruzf, 2001); southern Itly, N (Mzzoldi & Girolmo, 1997). Originl densities were converted in reltive undnces in order to stndrdize dt collected through different methodologies. A third dtse ws ssemled to exmine if ctul densities support conclusions otined from reltive undnce dt. This pproch ws sed on densities derived from 20 2m (40m 2 ) stndrdized trnsects conducted in four loclities in the western Atlntic (Pnm, Arolhos Reefs, Gurpri Islnds nd Arvoredo). Censuses were performed on ll loctions, nd included juveniles of ll species. Selected similr sheltered nd shllow reefs (<10 m) were chosen on ech loction, ecuse this is the preferred hitt for herivorous species. Herivores (including detritivores, Wilson et l., 2003) were nlysed in detil due to their importnt role in the orgniztion of shllow mrine enthic communities, nd to the knowledge ccumulted out this guild in the lst decdes (Horn, 1989; Chot, 1991; Hixon, 1997; Chot & Clements, 2002; Wilson et l., 2003).

4 REEF FISH LATITUDINAL GRADIENTS 1683 TABLE I. Site chrcteristics nd numer of reef fish species richness (old) with respective reltive undnce (percentge of species numer in prenthesis) in ech diet ctegory (food qulity ¼ nutritionl vlue) nd their moility. Fish dt were derived from visul census. Ctegory definitions re the sme s in Figs 1 nd 5. Dt from south-estern Spin were dded for comprison Bocs (Crien) Gurpri Islnd (south-est Brzil) Arvoredo (South Brzil) Cnries 1 (Mcronesi) South-est Spin 2 (Mediterrnen) Ltitude 9 N 20 S S 28 N 37 N SWT rnge ( C) Corl richness (species)* Corl cover (%) Numer of census Fish diversity Numer of fish species Numer of fish gener Species : gener rtio Trophic strtegies High-qulity 63 (649) 56 (691) 39 (615) 40 (656) 33 (733) Intermedite 5 (52) 4 (49) 4 (77) 16 (262) 11 (244) Low-qulity 29 (299) 21 (259) 18 (308) 5 (82) 1 (22) Species : gener rtio Sptil use nd moility Ctegory 1 29 (299) 24 (296) 22 (346) 29 (475) 22 (512) Ctegory 2 48 (495) 38 (469) 26 (423) 17 (279) 18 (419) Ctegory 3 20 (206) 19 (235) 14 (231) 15 (246) 3 (70) *, Reef-uilding sclerctinin þ millepores; 1,F lcon et l. (1996), Bortone et l. (1991); 2, Grcı -Chrton & Pe rez-ruzf (2001); 3, Guzm n & Guevr (1998); 4, Floeter et l. (2001); 5, W. Krohling & S.R. Floeter (unpul. dt); 6, only fishes utilizing low-qulity diets.; SWT, se surfce temperture.

5 1684 S. R. FLOETER ET AL. TROPHIC STRATEGIES In ll dtses every genus ws clssified ccording to its diet (i.e. trophic guild nd ssocited food qulity) nd sptil use nd moility (Tle II). They were divided in three clsses sed on food qulity: (1) high-qulity, fishes tht feed on highly energetic (with high protein content) nd esily digestile food, e.g. zooplnkton (Norrin & Bmstedt, 1984), moile invertertes nd fishes (Brey et l., 1988; Bowen et l., 1995); (2) low-qulity, fishes tht et reltively low-energy content resources, generlly with lower ssimiltion rtes nd indigestile components, e.g. high sh content (Meyln, 1991; Montgomery & Trgett, 1992; Bowen et l., 1995). Among this food re lge, segrsses nd detritus (ll reltively protein-poor), nd sessile invertertes (e.g. cnidrins, hidrozons nd sponges, usully with high percentge of inorgnic components in tissues). These resources generlly contin structurl (e.g. clcium cronte) nd chemicl defences ginst grzing such s secondry metolites (Pul, 1992; Pwlik, 1993; Pwlik et l., 1995; Hy, 1997; Burns & Iln, 2003; Burns et l., 2003). Although vrious uthors hve recently demonstrted tht the nutritionl vlue of sponges nd gorgonins (Chns & Pwlik, 1995; O Nel & Pwlik, 2002), detritus (Wilson, 2002; Wilson et l., 2003) nd endolithic lge (Bruggemn, 1994) re higher thn previously thought, these resources hve to e consumed in lrge mounts nd the costs of their processing nd ssimiltion re high (Horn, 1989; Chot, 1991; Meyln, 1991; Bowen et l., 1995; Chot & Clements, 1998); (3) intermedite-qulity, fishes tht forge oth on lge nd some protein-rich niml food, i.e. omnivores (Montgomery & Trgett, 1992). The prolem of grouping reef fishes in rod diet ctegories hs een widely discussed in recent reviews (Jones et l., 1991). Fish feeding plsticity mkes ctegoriztion into independent trophic groups difficult. In this study, however, every genus ws ssigned to one of three food qulity ctegories ssocited with eight mjor trophic guilds (Tle II) in order to serch for generl ptterns. Dominnt food items were determined from direct ehviourl oservtions, stomch content nlysis s well s the ville literture (Rndll, 1967; Froese & Puly, 2003; pers. os.). Fishes hve evolved wide vriety of wys to otin their food nd meet their energy nd nutritionl requirements (Horn, 1998). Overll diet qulity is function of the reltionship etween food composition nd digestive physiology. The three proposed ctegories sed on food qulity do not imply tht etter generl nutrition is otined y ny of the ctegories. Feeding strtegies mximizing ingestion rtes or presenting specilized digestion (e.g. microil fermenttion) re lso successful ones. Indeed, the highest growth rtes reported for freshwter fishes occur in herivorous nd detritivorous species (Bowen et l., 1995; Chot & Clements, 1998). SPATIAL USE AND MOBILITY Ech species ws lso ssigned to one of three ctegories sed on moility ptterns nd home-rnge sizes: ctegory 1, species with high moility, generlly ssocited with schooling ehviour in the wter column (i.e. mid-wter crnivores nd plnktivores) or demersl species with wide horizontl displcements (e.g. roving herivores, sprids nd mullids); ctegory 2, demersl reltively sedentry species tht live in close ssocition with the reef sustrtum, including serrnids, hemulids, lrids nd chetodontids; ctegory 3, site-ttched species with very smll home rnges, mny of them presenting territoril ehviour (e.g. dmselfishes, lrisomids nd goies). STATISTICAL ANALYSES MANOVA (repeted mesures) were used to test for differences mong loctions concerning men reltive undnces of food qulity groups nd sptil use nd moility ctegories. One-wy ANOVA were performed to nlyse totl fish densities nd densities of herivores (Zr, 1999). Approprite trnsformtions (log 10, squre root or rc-sin) were pplied when necessry in order to stilize the vrinces when necessry (Underwood, 1997). Additionl Student Newmn Keuls (SNK) multiple comprisons

6 REEF FISH LATITUDINAL GRADIENTS 1685 TABLE II. Food qulity, moility nd trophic clssifiction of reef fish gener in the four studied sites. Fmilies re rrnged ccording to Nelson (1994) Fmily Genus Trophic guild Food qulity Moility Fmily Genus Trophic guild Food qulity Moility Ogcocephlide Ogcocephlus C H 3 Spondyliosom* O I 1 Synodontide Synodus P H 3 Scinide Odontoscion C H 2 Holocentride Holocentrus MI H 2 Preques MI H 2 Myripristis PL H 2 Scien* C H 2 Srgocentrum MI H 2 Umrin MI H 2 Aulostomide Aulostomus P H 2 Mullide Mulloidichthys MI H 1 Scorpenide Scorpen C H 3 Mullus MI H 1 Centropomide Centropomus C H 1 Pseudupeneus MI H 1 Serrnide Alphestes C H 2 Chetodontide Chetodon SI L 2 Cephlopholis C H 2 Pomcnthide Holcnthus SI L 2 Dermtolepis C H 2 Pomcnthus O L 2 Diplectrum C H 2 Kyphoside Kyphosus RH L 1 Epinephelus C H 2 Cirrhitide Amlycirrhitus MI H 3 Hypoplectrus C H 2 Pomcentride Audefduf O I 1 Mycteroperc P H 2 Chromis PL H 1 Prnthis PL H 1 Microspthodon TH/D L 3 Rypticus C H 2 Stegstes TH/D L 3 Serrnus MI H 3 Lride Bodinus MI H 2 S. tortugrum PL H 2 Centrolrus* MI H 2 Grmmtide Grmm MI/PL H 3 Clepticus PL H 1 Pricnthide Heteropricnthus MI H 2 Coris* MI H 2 Pricnthus C H 2 Dortonotus MI H 2 Crngide Crngoides P H 1 Hlichoeres MI H 2 Crnx P H 1 Thlssom PL H 1 Decpterus P H 1 Xyrichthys MI H 3 Elgtis P H 1 Scride Cryptotomus RH L 1 Pseudocrnx PL H 1 Scrus RH/D L 1

7 1686 S. R. FLOETER ET AL. TABLE II. Continued Fmily Genus Trophic guild Food qulity Moility Fmily Genus Trophic guild Food qulity Moility Seriol P H 1 Sprisom RHD L 1 Trchinotus MI H 1 Lrisomide Lrisomus C H 3 Lutjnide Lutjnus C H 2 Mlcoctenus MI H 3 Ocyurus C H 1 Blenniide Ophiolennius TH/D L 3 Hemulide Anisotremus MI H 2 Prlennius O I 3 Hemulon MI H 2 Chenopside Emlemriopsis MI H 3 Orthopristis MI H 2 Tripterygiide Ennenectes MI H 3 Prpristipom* MI H 2 Tripterygion* MI H 3 Pomdsys MI H 2 Goiide Coryphopterus PL H 3 Spride Archosrgus O I 1 Elctinus MI H 3 Boops O I 1 Goius* MI H 3 Clmus MI H 1 Vnneugoius* O I 3 Dentex* C H 1 Acnthuride Acnthurus RH/D L 1 Diplodus O I 1 Bothide Bothus C H 3 Lithognthus* MI H 1 Blistide Blistes MI I 1 Old* O I 1 Moncnthide Aluterus O L 1 Pgellus* O I 1 Cntherhines O I 1 Pgrus C I 1 Stephnolepis O I 1 Srp* RH L 1 Ostrciide Acnthostrcion O I 1 Sprus* O I 1 Tetrodontide Cnthigster SI L 2 C, crnivore; P, piscivore; MI, moile inverterte feeder; SI, sessile inverterte feeder; PL, plnktivore; O, omnivore; RH, roving herivore; TH, territoril herivore; D, detritivore; H, high-qulity food; I, intermedite; L, low; 1, high moility; 2, reltively sedentry; 3, site ttched. *, not present in the western Atlntic.

8 REEF FISH LATITUDINAL GRADIENTS 1687 of mens test were performed s post hoc test (Zr, 1999). When trnsformtions did not produce homogeneous vrinces, ANOVA ws used nevertheless ecuse of its roustness, following Underwood s (1997) recommendtion. A setting of ¼ 001 ws used to compenste for the incresed likelihood of Type I error (Underwood, 1997). A multivrite cnonicl correspondence nlysis (CCA) ws conducted to explore the generlity of lrge-scle trends in food resource use mong 11 sites in the Atlntic, i.e. the second dtse (ter Brk & Verdonschot, 1995). The t-test ws employed for compring the verge feeding rte of the ocen surgeonfish Acnthurus hinus Cstelnu in Pnm nd south-estern Brzil. RESULTS UTILIZATION OF FOOD RESOURCES Fish species using food resources of high nutritionl vlue were dominnt in ll sites, oth in terms of diversity nd reltive undnce, rnging from 62 to 73% of the totl numer species nd 52 to 65% of counted fishes (Tle I nd Fig. 1). The numer of species nd reltive undnce of fishes relying on lowenergy food significntly decresed towrds higher ltitudes (Fig. 1 nd Tle I). The species : genus rtio of this fish guild decresed towrd colder wters (24 in Bocs, 19 in Gurpri, 16 in Arvoredo nd 10 in the Cnries) nd it ws higher thn the overll rtio considering ll fishes in the western Atlntic ssemlges (Tle I). On the other hnd, fishes tht fed on intermedite-qulity resources (i.e. lge, detritus nd lso niml protein) were highly undnt t colder peripherl sites (Arvoredo nd Cnries) nd their proportionl importnce diminished in wrmer loctions (Fig. 1). Their species richness lso incresed with ltitude (Tle I), nd the omnivorous sprids were the min speciose fmily in this guild. A shrp decrese in the importnce of fishes depending on low-cloric food could e oserved in reltion to the minimum wter temperture of loctions. A rtio of men reltive undnce of fishes tht feed on high-qulity resources divided y men reltive undnce of fishes using intermedite or low-qulity diets reveled consistent trend (Fig. 2). A CCA nlysis performed with dt from 11 sites long the Atlntic (Fig. 3) showed the sme trends oserved in the four detiled studied sites (Fig. 1), confirming tht consistent regionl generliztion could e drwn. Trophic strtegies ccounted for 456% of the vrince in the weighted verges. Tropicl sites were ll clustered following the trend of etter use of low-qulity resources (intrset correltions etween diet nd site scores ¼ 0819). On the right side of the digrm, high-qulity ( 0939) nd intermedite diets (0319) ffected the mrginl estern Atlntic nd the Mediterrnen sites. A lnce of intermedite (i.e. omnivore) nd low-qulity ctegory influenced high ltitude rocky reefs on the Brzilin cost. DENSITY OF HERBIVORES AND DETRITIVORES Stndrdized visul censuses in four sheltered nd shllow loclities in the western Atlntic provided comprle dt on densities of reef fishes long n extensive ltitudinl grdient. Totl density of fishes ws similr in ll tropicl

9 1688 S. R. FLOETER ET AL. 100 Men reltive undnce c c c d 0 Bocs Gurpri Arvoredo Cnries FIG. 1. Men þ S.D. reltive undnce of food qulity ctegories: high-qulity (&) (fishes tht feed on high protein nd energy content food, which re highly digestile, e.g. mcro-plnkton, moile invertertes nd fishes), low-qulity (&) (fishes tht et reltively low-energy content resources, with indigestile components such s lge, segrsses, detritus, sponges nd cnidrins nd intermedite-qulity (&) (fishes tht forge oth on lge nd protein-rich niml food, i.e. omnivores). MANOVA showed tht ll ctegories vried significntly etween loctions (P < 0001); different lower cse letters indicte significntly different (Student Newmn Keuls test, P < 001) vlues nd those with the sme lower cse letter re not significntly different (P > 001). sites: Bocs del Toro, Pnm, Arolhos, north-est Brzil nd Gurpri, south-est Brzil ( fishes 100 m 2 ) nd only hlf of it ws found on Arvoredo (92 fishes 100 m 2 ) in the southern Brzil (Fig. 4). Totl density nd reltive proportion of herivores follow cler significnt ltitudinl trend (158 fishes 100 m 2 constituting 79% of fishes counted in Bocs del Toro, Pnm, High: (low + intermedite) food qulity Minimum sewter temperture ( C) FIG. 2. High-qulity: (intermedite þ low) qulity food rtio in reltion to minimum wter temperture. Dt from reltive undnces derived from visul censuses: Bocs del Toro, Pnm, 9 N; Arolhos Reefs, north-est Brzil, S (C.E.L. Ferreir unpul. dt); Gurpri Islnds, south-est Brzil 20 S; Arvoredo, S; Cnries, Mcronesi, 28 N (Fálcon et l., 1996; Bortone et l., 1991; Hjgos & Vn Tssell, 2001); south-est Mediterrnen, Spin, N (Grcí-Chrton & Pérez-Ruzf, 2001); Snt Ctlin Islnd, Cliforni, U.S.A N(Hoson & Chess, 2001).

10 REEF FISH LATITUDINAL GRADIENTS 1689 Intermedite Axis 1 (32. 2%) Low High Axis 2 (13. 4%) FIG. 3. Cnonicl correspondence nlysis ordintion digrm with reef sites nd diet ctegories ( ) (see Fig. 1). The sites were: tropicl () [Florid Keys, N (Bohnsck & Bnnerot, 1986); Cyos Cochinos, Hondurs, N (Clifton & Clifton, 1998); Bocs del Toro, Pnm, 9 N; Mnuel Luiz Reefs, north-est Brzil, S (Roch & Ros, 2001); Tmndré, north-est Brzil, S (B.P. Ferreir unpul. dt); Arolhos Reefs, north-est Brzil, S (C.E.L. Ferreir unpul. dt); Gurpri Islnds, south-est Brzil 20 S], south-est (.) nd southern Brzil (&) [Arril do Co, south-est Brzil, 23 S (C.E.L. Ferreir unpul. dt); Arvoredo, southern Brzil S] nd north-est Atlntic (n) [Cnries, Mcronesi, 28 N (F lcon et l., 1996; Bortone et l., 1991; Hjgos & Vn Tssell, 2001); south-est Mediterrnen, Spin, N (Grcí- Chrton & Pérez-Ruzf, 2001); southern Itly, N (Mzzoldi & Girolmo, 1997)]. 99 nd 57% on Arolhos Reefs, north-est Brzil, 41 nd 23% on Gurpri Islnd, south-est Brzil, nd 19 nd 21% on Arvoredo Archipelgo in the south). MOBILITY AND HOME-RANGE PATTERNS Regrding the mplitude of fish sptil use nd moility, the ctegory 1 (high moility generlly ssocited with schooling ehviour) is proportionlly more diverse in the Cnries (Tle 1) where it lso chieves significntly higher reltive undnce (Fig. 5). Schooling sprids nd the omnivorous pomcentrid genus Audefduf re undnt in the mrginl sites. On the Cnrin Archipelgo, the plnktivorous Thlssom nd Chromis re lso very undnt. Reltively sedentry species (ctegory 2) re diverse group in tropicl sites (Tle I), nd re highly undnt in the Brzilin sites (Fig. 5). This is ecuse of the high reltive undnce of hemulids, holocentrids nd the lrid genus Hlichoeres on Gurpri Islnds, nd serrnids (primrily Mycteroperc) nd the puffers (Sphoeroides) on Arvoredo. Site-ttched species (ctegory 3) re the dominnt group in the Crien in terms of undnce (665% of the counted fishes; Fig. 5). Goiids nd territoril dmselfishes re minly responsile for

11 1690 S. R. FLOETER ET AL. Fish density (numer per 100 m 2 ) c d Bocs Arolhos Gurpri Arvoredo FIG. 4. Men þ S.E. totl fish densities (&) nd herivores only (&) t four sites in ltitudinl grdient long the western Atlntic. Dt were derived from 20 2 m trnsects (visul censuses) in selected shllow (<10 m deep) sheltered hitts t: Bocs del Toro, Punt Hospitl, 9 N(n ¼ 60); Arolhos, Times reefs, S (n ¼ 56); Gurpri Islnd, 20 S (n ¼ 84); Arvoredo, S (n ¼ 85). ANOVA showed tht ll ctegories vried significntly etween loctions (P < 0001); different lowercse letters indicte significntly different (Student Newmn Keuls test, P < 001) vlues nd those with the sme lower cse letter re not significntly different (P > 001). these figures. On the Brzilin cost, site-ttched species ccount for 15 30% decresing to just 13% in the Cnries. Mny fishes in ctegory 3 re smll nd cryptic nd re often underestimted y UVC (Willis, 2001). Their diversity nd undnce re proly higher thn indicted in Fig. 5, especilly on tropicl reefs. Men reltive undnce c c c d 0 Bocs Gurpri Arvoredo Cnries FIG. 5. Men þ S.D. reltive undnces of ctegories of sptil use (moility nd home-rnge size): ctegory 1, (&) (species with high moility, generlly ssocited with schooling ehviour in the wter column or demersl species with wide horizontl displcements); ctegory 2 (&) (demersl reltively sedentry species tht live in close ssocition with the reef sustrtum, including serrnids, hemulids, lrids nd chetodontids); ctegory 3 (&) (site-ttched species with very smll home-rnges, mny of them presenting territoril ehviour). MANOVA showed tht ll ctegories vried significntly etween loctions (P < 0001); different lower cse letters indicte significntly different (Student Newmn Keuls test, P < 001) vlues nd those with the sme letter were not significntly different (P > 001).

12 REEF FISH LATITUDINAL GRADIENTS 1691 DISCUSSION Species richness declines from Bocs del Toro to the Cnries conforming to the generl trend of decresing fish diversity from tropicl to temperte ltitudes (Hoson, 1994; Briggs, 1995). These trends could e relted to: (1) differentil extinction rtes suffered in peripherl res due to se-level nd temperture chnges over geologicl time (Briggs, 1966, 1995; Vermeij & Rosenerg, 1993), (2) differences in recent specition rtes, decresing from tropicl to temperte sites, s indicted y the species per genus rtios found (Tle I), nd (3) hitt vilility (nd heterogeneity) nd resource diversity nd temporl persistence (tropicl v. temperte reefs; Holrook et l., 1990). IS THERE A TREND TOWARD THE USE OF LOW-ENERGY FOOD RESOURCES AMONG TROPICAL REEF FISHES? Hrmelin-Vivien (2002) presented qulittive dt of herivorous fish species nd their significnt correltion with ltitude (incresing richness towrds the equtor), nd lso showed tht the percentge of lge in the diet of lenniid nd goiid fish species on corl reefs ws higher thn in wrm-temperte wters. In the present study, it ws unequivoclly demonstrted tht lthough plnktivores, piscivores nd crnivores preying on motile invertertes dominted in ll sites, the reltive undnce of fishes tht fed on lge, orgnic detritus nd sessile invertertes decresed from tropicl to temperte ltitudes. These differences re proly not relted to differences in the undnce of food resources etween ltitudes, ecuse lge, segrsses nd sessile invertertes (except for reef-uilding corls) re lso undnt nd ville (lthough sesonl for some lge species) for feeding in temperte zones (Holrook et l., 1990; Fsol et l., 1997; Pwlik, 1998; Hrmelin-Vivien, 2002; Pihl & Wennhge, 2002). Differences, however, could e driven y lge productivity (Russ, 2003) nd rte of detritus decomposition (higher on tropicl reefs; Cerin, 2002). The species : genus rtio of low-qulity food consumers incresed towrds the tropics, nd ws higher thn the overll rtio considering ll fishes in the ssemlges. This supports the view tht higher specition rtes occurred mong this guild of fishes in wrm wters. Indeed, low-qulity feeders contin the morphologiclly derived tx, indicting reltionship etween rdition nd the energetic vlue of the food (Tle II; Bruggemnn, 1994; Hrmelin- Vivien, 2002). The higher diversity nd undnce of low-qulity feeders (i.e. herivores nd sessile inverterte feeders) in lower ltitudes compred to mrginl res could e viewed s reflection of progressive dpttion to the use low-energy food sources (Hrmelin-Vivien, 2002). Although herivory, spongivory nd corllivory y fishes is known to ffect distriution nd undnce of enthic orgnisms (Lewis, 1985; Horn, 1989; Hixon, 1997; Hill, 1998; Pwlik, 1998), these feeding strtegies re reltively recent evolutionry phenomenon (Wood, 1999; Bellwood & Winwright, 2002; Bellwood, 2003). Herivores nd sessile inverterte rowsers re found in the most derived fmilies (Tle II), nd within these fmilies extended dpttions to use poor-qulity resources re found in the morphologiclly most derived gener (Mott, 1989; Bellwood, 1994; Hrmelin-Vivien, 2002). Cooper & Vitt

13 1692 S. R. FLOETER ET AL. (2002) found the sme trend in lizrds. The Cenozoic mrine grzing revolution ppers to mrk mjor shift in the ecologicl structure of corl reefs due to chnges in the nture of fish-sed predtion. During this trnsition, fish funs went from primrily crnivorous in the Mesozoic to lrge vriety of grzers or rowsers in the Cenozoic (Wood, 1999; Bellwood & Winwright, 2002; Bellwood, 2003). In colder peripherl sites, such s the southern Brzilin cost, the Cnries or the Mediterrnen, fishes tht feed on intermedite-qulity food (e.g. omnivorous sprids) hve higher undnce nd diversity, compred to wrmer sites. It seems tht these fishes could exploit low-nutritionl resources only if they re ssocited with sustntil portions of highly digestile niml protein. So, they could fulfil their metolic needs to live in hrsh colder environments. Bowen et l. (1995) interpreted omnivory s compromise strtegy in which protein from scrce niml prey is complemented y energy from undnt primry foods. At Snt Ctlin, Cliforni, U.S.A. two nominlly herivores, Girell nigricns (Ayres) nd Medilun cliforniensis (Steindchner), differ from most tropicl herivores in consuming reltively lrge numer of invertertes on sesonl sis (Holrook et l., 1990; Hoson & Chess, 2001). In winter, when preferred lge re scrce nd when fermenttive digestion processes could e less efficient, it seems necessry to increse feeding on niml protein. In North Crolin, U.S.A., similr ehviour ws oserved (M. Hy, pers. comm.) with omnivorous fishes shifting diets with chnges in temperture. When it ws wrm, they consumed more seweed. As temperture dropped they consumed more niml mteril, nd eventully refused to et ny seweed once tempertures were <17 C. HERBIVOROUS FISHES: A TROPICAL PHENOMENON? The density (nd reltive proportion) of herivores nd detritivores censused in similr hitts, with stndrdized procedures, significntly decreses towrd higher ltitudes. Meekn & Chot (1997) when compring the Crien nd the Gret Brrier Reef to New Zelnd reefs lso found the sme pttern. Within the herivores, some differences were ovious. Fishes tht hve n importnt prt of their diet constituted y detritus nd clcified mteril (scrids nd cnthurids) chieve higher densities in wrmer sites (Bruggemnn, 1994; Ferreir et l., 2004). Conversely, kyphosids nd some sprisomtines tht feed on mcrolge increse their reltive undnce t higher ltitudes on the Brzilin cost (Ferreir et l., 2004). On the Gret Brrier Reef, scrids on the southern limit of their rnge consume more mcroscopic lge compred to those on lower ltitudes (J.H. Chot, pers. comm.). The domintion of exclusive selective mcrolge feeders, which use specil digestion y hind gut fermenttion nd symionts ( true herivores ; Chot & Clements, 2002) such s kyphosids, odcids, plodctylids nd sticheids) is lso found in New Zelnd temperte rocky reefs (Jones, 1988; Meekn & Chot, 1997; Chot & Clements, 1998; Mountfort et l., 2002). Other counter-exmples, however, complicte the sitution (e.g. the rowsing cnthurid Acnthurus coeruleus Bloch & Schneider re only found in the tropicl Atlntic, nd mcrolge eting signids re more diverse nd undnt t lower ltitudes in the Pcific).

14 REEF FISH LATITUDINAL GRADIENTS 1693 Herivory pressure seems to e lower in higher ltitudes not only due to lower density of herivores, ut ecuse feeding rtes (ites per unit time) re generlly lower too (Chot & Clements, 1993), which is proly reflection of lowered metolism in colder wter. For exmple, prrotfishes of the genus Sprisom hve verge iting rtes during the dytime ( hours) of ites per 5 min in south-est Brzil (Ferreir et l., 1998) nd Azores (J.P. Brreiros, pers. comm.), nd of ites per 5 min in Pnm (C.E.L. Ferreir & S.R. Floeter, unpul. dt). Also, the roving cnthurid Acnthurus hinus Cstelnu hve n verge grzing rte of ites per 5 min (men S.D.) in south-est Brzil, where wter temperture usully flls to C (Ferreir et l., 1998), nd more thn the doule ( ites per 5 min) in the tropicl Bocs del Toro, Pnm (t-test, d.f. ¼ 121, P < 00001). This pttern seems to indicte tht elow criticl temperture, nutrient ssimiltion my fll elow metolic requirements, thus physiologicl constrints ssocited with size nd n ectothermic metolism could e excluding mny herivorous fishes from temperte nd higher ltitudes (Gines & Luchenco, 1982; Horn, 1989). Further studies should lso consider if productivity nd lge nd detritus chemicl composition re linked with the herivorous fish undnce ptterns found. It is worth noting tht the cpcity to mke living from plnt mteril hs een found for long time in terrestril verterte popultions, proly since the Permin (Sues & Reisz, 1998). In fishes there is clerly much lter timehorizon in the ppernce of herivory (Bellwood & Winwright, 2002). Although some fishes occupying cold wter hitts (down to 45 S) re herivores, feeding exclusively on mcroscopic lge nd mintining rtes of fermenttive digestion in similr wy to terrestril endotherms (Mountfort et l., 2002), the gret mjority of mrine fish herivores hve tropicl ffinities nd re rre in temperte environments in the Atlntic. These fishes find their optiml environmentl fctors in the tropics (Chot, 1991; Bruggemnn, 1994; Ferreir et l., 2004). It is thus cler tht the rel trophic sttus of herivorous fishes in the Atlntic requires further detiled studies (Chot & Clements, 2002). DO FISH SPATIAL USE AND MOBILITY VARY WITH LATITUDE AND REEF TYPE? Differentil moility nd home rnge ptterns (e.g. schooling ehviour nd territorility) re expected to occur if: 1) distinct forging strtegies re used to ccess unpredictle nd spced resources (e.g. plnkton) nd 2) there is vrition in reef type nd complexity (e.g. corl nd rocky). Horizontl nd verticl fish distriution in spce is not uniform cross the reef complex. Its heterogeneity opertes t two scles, the geomorphologicl reef zones (mcrohitt), nd the specific fish hitts (microhitt). Bellwood et l. (2002) found highly congruent ptterns of hitt use (sheltered v. exposed) of lrids, in terms of functionl chrcteristics t glol iogeogrphicl scles. On high-ltitude reefs, fishes presenting high moility or wide horizontl displcements (ctegory 1) re proportionlly more diverse nd chieve significntly higher undnces. These fishes generlly exhiit schooling ehviour, which is the privileged forging tctic used y fishes tht hve to rom over

15 1694 S. R. FLOETER ET AL. lrge res to find ptchy or rndomly distriuted food (e.g. plnkton nd smll clupeids). High-ltitude environments re generlly ffected y sesonl temperture chnges nd unpredictle upwelling processes (Eeling & Hixon, 1991; Sl & Boudouresque, 1997; Pihl & Wennhge, 2002). High moility fishes, usully in lrge schools, re less relint on the reef sustrtum for protection, nd seem to respond more redily to environmentl fluctutions, i.e. they re etter le to move mong reefs nd verticlly in the wter column in response to the vilility of resources or to stisfy their environmentl preferences, such s optiml temperture. Among fishes tht thrive well in these mrginl reefs re the omnivorous schooling sprids (Diplodus), the srgent mjor (Audefduf), nd the plnktivorous Chromis. In highly complex sustrtum, species sheltering in reef crevices or holes or in ner-reef snd or rule re expected. Structurl complexity or ottom relief hs een positively correlted to reef fish undnce in corl reefs (Bell & Glzin, 1984; Friedlnder & Prrish, 1998), tropicl nd sutropicl rocky shores (Aurto-Oropez & Blrt, 2001; Ferreir et l., 2001; S.R. Floeter, unpul. dt), nd temperte reefs (Grcı -Chrton & Pe rez-ruzf, 1998). On tropicl reefs, reltively sedentry tx (ctegory 2) such s the lrid genus Hlichoeres, hemulids, chetodontids nd serrnids form the most diverse group detected y UVC. In terms of undnce, fishes with smll-size home rnges (ctegory 3) predominte on corl reefs (67% of the counted fishes in Bocs del Toro, Pnm). Similr vlues re found on corl reefs worldwide (72% t Tuler, Mdgscr; 61% t Moore, French Polynesi; Hrmelin- Vivien, 1989). Sustrtum complexity promoted y corl growth (especilly rnching forms) seems to provide dequte microhitts for smll territoril fishes such s pomcentrids nd goies. On mny tropicl reefs, territoril dmselfishes re extremely undnt, nd the res they defend cn occupy >70 80% of the surfce of some reef hitts (Roertson & Lssig, 1980; Ferreir et l., 1998; Ceccrelli et l., 2001). The higher diversity nd undnce of type 3 species cn lso e lso linked to their diets. Most of them defend lge or feed on detritus which is more ville in the tropics. In other words, home rnge size nd food security re proly linked nd confounding fctors. In summry, the dt support the sitution proposed y Hrmelin-Vivien (2002) tht trophic structure of tropicl fish communities contrst with those from temperte regions in terms of more efficient use of reltively low-qulity food resources. In reltion to the sptil use nd moility, reltively sedentry species form the most diverse group on tropicl reefs, lthough fishes with smll-size home rnges dominte in terms of undnce. Not ll ptterns found in the Atlntic, however, re likely to e generl t the glol-scle ecuse of the different evolutionry histories nd diversity profiles mong ocen sins (Vn Alstyne et l., 2001; Bellwood & Winwright, 2002). For exmple, significnt decrese in the proportion of species nd densities of herivorous fishes from tropicl to temperte wters is oserved worldwide (Horn, 1989; Meekn & Chot, 1997; S.R. Floeter nd C.E.L. Ferreir, unpul. dt), ut in terms of reltive iomss, temperte New Zelnd is n exception with herivores presenting similr vlues s tropicl loctions (Jones, 1988). Thus, further comprtive studies etween the Atlntic nd the Indo-Pcific

16 REEF FISH LATITUDINAL GRADIENTS 1695 regions regrding functionl chrcteristics of species (e.g. sptil use, moility nd resource-use ptterns) re needed. We thnk J.L. Gsprini, O.J. Luiz-Ju nior, W. Krohling, M. Hostin, J.P. Brreiros, J.G. Domı nguez, I. Bethncourt, A. Cstillo, W. Pomre, L.C. Gerhrdinger, A.G.V. Floeter, IEAPM nd D.R. Roerston (STRI) for invlule help in the field nd logisticl support. M. Kulicki, J.H. Chot, M. Hrmelin-Vivien, J.P. Brreiros, B.P. Ferreir, M. Hy, J.-C. Joyeux, M.S.G. Floeter, M. Wolff, O. Ocn, R. Stevens, D. V zquez, A. Moles nd J. Pwlik for exchnging ides, unpulished records nd provision of literture. Smithsonin Tropicl Reserch Institute (STV grnt), Pdi Awre Foundtion, Fundção O Botic rio de Protec o ` Nturez, WWF, UENF, nd the Center for Tropicl Mrine Ecology (ZMT) for essentil funding. This work ws prtly conducted t the Ntionl Center for Ecologicl Anlysis nd Synthesis, Snt Brr, CA, U.S.A. where S.R.F. is postdoctorl ssocite. References Aurto-Oropez, O. & Bllrt, E. F. (2001). Community structure of reef fish in severl hitts of rocky reef in the Gulf of Cliforni. PSZN Mrine Ecology 22, Bell, J. D. & Glzin, R. (1984). Influence of live corl cover on corl-reef fish communities. Mrine Ecology Progress Series 15, Bellwood, D. R. (1994). A phylogenetic study of the prrotfishes fmily Scride (Pisces: Lroidei), with revision of gener. Records of the Austrlin Museum, Supplement 20, Bellwood, D. R. (2003). Origins nd escltion of herivory in fishes: functionl perspective. Pleoiology 29, Bellwood, D. R. & Winwright, P. C. (2002). The history nd iogeogrphy of fishes on corl reefs. In Corl Reef Fishes: Dynmics nd Diversity in Complex Ecosystem (Sle, P. F., ed.), pp Sn Diego, CA: Acdemic Press. Bellwood, D. R., Winwright, P. C., Fulton, C. J. & Hoey, A. (2002). Assemly rules nd functionl groups t glol iogeogrphicl scles. Functionl Ecology 16, Bohnsck, J. A. & Bnnerot, S. P. (1986). A sttionry visul technique for quntittively ssessing community structure of corl reef fishes. NOAA Techicl Report NMFS 41, Bortone, S. A., Vn Tssell, J., Brito, A., Flco n, J. M. & Bundrick, C. M. (1991). A visul ssessment of the inshore fishes nd fishery resources off El Hierro, Cnry Islnds: seline survey. Scienti Mrin 55, Bowen, S. H., Lutz, E. V. & Ahlgren, M. O. (1995). Dietry protein s determinnts of food qulity: trophic strtegies compred. Ecology 76, ter Brk, C. J. F. & Verdonschot, P. F. M. (1995). Cnonicl correspondence nlysis nd relted multivrite methods in qutic ecology. Aqutic Sciences 57, Brey, T., Rumohr, H. & Ankr, S. (1988). Energy content of mcroenthic invertertes: generl conversion fctors from weight to energy. Journl of Experimentl Mrine Biology nd Ecology 117, Briggs, J. C. (1966). Ocenic islnds, endemism nd mrine pleotempertures. Systemtic Zoology 15, Briggs, J. C. (1995). Glol Biogeogrphy. Developments in Pleontology nd Strtigrphy. Amsterdm: Elsevier. Bruggemnn, J. H. (1994). Prrotfish grzing on corl reefs: trophic novelty. PhD Thesis, University of Groningen, Netherlnds. Bruggemnn, J. H., Begemn, J., Bosn, E. M., Verug, P. & Breemn, A. M. (1994). Forging y the stoplight prrotfish Sprisom viride. II. Intke nd ssimiltion of food, protein, nd energy. Mrine Ecology Progress Series 112,

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