Post-settlement Life Cycle Migration Patterns and Habitat Preference of Coral Reef Fish that use Seagrass and Mangrove Habitats as Nurseries

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1 Esturine, Costl nd Shelf Science (2) 55, doi:1.16/ecss.1.97, ville online t on Post-settlement Life Cycle Migrtion Ptterns nd Hitt Preference of Corl Fish tht use Segrss nd Mngrove Hitts s Nurseries E. Cocheret de l Morinière, B. J. A. Pollux, I. Ngelkerken nd G. vn der Velde, Deprtment of Animl Ecology nd Ecophysiology, University of Nijmegen, Toernooiveld 1, 6525 ED Nijmegen, The Netherlnds Received 14 My 1 nd ccepted in revised form 8 Octoer 1 Mngroves nd segrss eds hve received considerle ttention s nurseries for reef fish, ut comprisons hve often een mde with different methodologies. Thus, reltive importnce of different hitts to specific size-clsses of reef fish species remins uncler. In this study, 35 trnsects in 11 sites of mngroves, segrss eds nd corl reef were surveyed dily, in nd in front of mrine y on the islnd of Curço (Netherlnds Antilles). The density nd size-frequency of nine reef fish species (including herivores, zooenthivores nd piscivores) ws determined during five-month period using single methodology, viz. underwter visul census. All species were nursery species in terms of their high densities of juveniles in mngroves or segrss eds. Reltive density distriution of the size-clsses of the selected species over mngroves nd segrss eds suggested high levels of preference for either mngroves or segrss eds of some species, while other species used oth hitts s nursery. Sptil size distriution of the nine species suggested three possile models for Post-settlement Life Cycle Migrtions (PLCM). Hemulon sciurus, Lutjnus griseus, L. podus, nd Acnthurus chirurgus pper to settle nd grow up in y hitts such s mngroves nd segrss eds, nd in lter stge migrte to the corl reef (Long Distnce PLCM). Juveniles of Acnthurus hinus nd Scrus teniopterus were found only in y hitts t close proximity to the corl reef or on the reef itself, nd their migrtion pttern concerns limited sptil scle (Short Distnce PLCM). Some congeneric species crry out either Long Distnce PLCM or Short Distnce PLCM, therey temporrily lleviting competition in reef hitts. Hemulon flvolinetum, Ocyurus chrysurus nd Scrus iserti displyed Stepwise PLCM pttern in which smllest juveniles dwell in the mouth of the y, lrger individuls then move to hitts deeper into the y, where they grow up to (su-) dult size t which they migrte to nery corl reef hitts. This type of stepwise migrtion in opposite directions, comined with different preference for either mngroves or segrss eds mong (size-clsses of) species, shows tht reef fish using in-y hitts during post-settlement life stges my do so y choice nd not merely ecuse of stochstic dispersl of their lrve, nd underline the necessity of these hitts to Crien corl reef systems. 2 Elsevier Science Ltd. All rights reserved. Keywords: fish; nursery grounds; mngrove swmps; segrss; corl reef; Crien Se; migrtion; Curço Introduction In mny studies, juveniles of reef fish species were found in high densities in non-reef hitts, while the dults were found lmost exclusively on the corl reef itself (Pollrd, 1984; Prrish, 1989). From this sptilly heterogeneous size-frequency distriution, Post-settlement Life Cycle Migrtion (PLCM) ptterns were suggested tht gve irth to the nursery concept. Mngroves nd segrss eds re considered nurseries to some reef fish species in the Western Atlntic, Indin Ocen nd Pcific Ocen (Pollrd, 1984; Prrish, 1989). Severl uthors hve suggested the enefits of nurseries to juvenile reef fish, vrying from high food vilility to lower predtion Corresponding uthor. E-mil: gerrdv@sci.kun.nl efficiency, lower predtor undnce, nd high interception rte of the vegettion to plnktonic lrve (Odum & Held, 1972; Crr & Adms, 1973; Ogden & Ziemnn, 1977; Bler & Bler, 198; Shulmn, 1985; Prrish, 1989; Heck & Crowder, 1991; Roertson & Bler, 1992). Most uthors, however, hve focused on one or two hitts of the mngrove-segrss-reef continuum, often with different smpling methods, thus complicting comprisons mong studies nd mong hitts (e.g. Roertson & Duke, 1987; Thyer et l., 1987; Yáñez-Arncii et l., 1988; Bler et l., 1989; Belde, 199; Rooker & Dennis, 1991; Sederry & Crter, 1993; Legdsgrd & Johnson, 1). Quntittive dt on ontogenetic shifts in hitt use from nursery to dult reef ssocition re /1/ $35./ 2 Elsevier Science Ltd. All rights reserved.

2 31 E. Cocheret de l Morinière et l. lrgely lcking (Ogden & Ehrlich, 1977; Weinstein & Heck, 1979; Rooker & Dennis, 1991; Appeldoorn et l., 1997; Ngelkerken et l., ) nd the reltive importnce of these nurseries to different size-clsses of reef fish species is still poorly known (Ogden & Gldfelter, 1983; Birkelnd, 1985). In recent underwter visul surveys in seven different hitts in mrine islnd y in Curço (Netherlnds Antilles), numer of reef fish species of which juveniles were highly undnt in y environments were identified nd grouped s nursery species (Ngelkerken et l., ). Ngelkerken et l. () used low frequency of surveys in lrge numer of trnsects, nd focused on fish community structure in rnge of hitts (mngroves, segrss eds, lgl eds, chnnel, fossil reef terrce notches, oulders, corl reef). Of ll hitts in tht study, segrss medows proved to contin highest totl numers of fish, clculted from oserved density nd totl surfce re. In the sme cler wter mrine y in the Crien, selection of seven nursery species of which juvenile individuls hd een found in lrge numers in mngroves nd segrss eds ws studied in detil (Acnthurus chirurgus, Hemulon flvolinetum, H. sciurus, Lutjnus podus, L. griseus, Ocyurus chrysurus, nd Scrus iserti). In ddition to this set of herivorous, zooenthivorous nd piscivorous fish, two congeneric species were selected tht were encountered in significnt quntities in some segrss eds ner the djcent fringing reef (Scrus teniopterus nd Acnthurus hinus). Using dytime underwter visul census s single method to quntify the undnce of the nine selected species nd estimte their size, heterogeneity of the sptil size-frequency distriution of these fish species in reef hitts, mngroves nd segrss medows ws tested. In this wy, ssocition of specific size-clsses of reef fish with specific hitts or sptilly seprted sites provides informtion from which Post-settlement Life Cycle Migrtion (PLCM) ptterns cn e derived, tking dy-to-dy vrition over five month period into ccount. Additionlly, differences in sptil distriution nd hitt preference cn e compred mong species. The questions tht will e ddressed re: 1. Do size-clsses of the selected species disply ny preference for mngrove or segrss hitts in terms of densities? 2. Do hitts differ in the size-structure of the supopultions tht they hrour? 3. Which sptil migrtion ptterns cn e inferred from verge densities nd sizes y comprison of the supopultions t the vrious sites? Methods Study re The present study ws crried out in Spnish Wter By in Curço, Netherlnds Antilles (Figure 1). This 3 km 2 y is shllow (lrgely <6 m deep), hrours extensive segrss medows nd is fringed y mngroves (Rhizophor mngle). Wter depths under mngrove cnopies rnged etween 8 m nd 1 8 m. These cnopies provide drk hitts (verge light extinction underwter ws 85%, s opposed to 4% over segrss eds). The segrss eds re dominted y monospecific stnds of Thlssi testudinum (Kuenen & Derot, 1995). Men shoot density ( SD) in the segrss trnsects ws 246 m 2 ( 11) nd segrss cnopy height verged 28 cm ( 11 5). There is no freshwter input into the y other thn rin, nd slinity (vg. 35 4) is slightly higher thn on the reef (vg. 34 6). By wter temperture verged 3 1 C ( 8), while wter temperture on the reef verged 28 4 C ( 9). Visiility ws high t ll sites, nd vried etween n verge of 6 5 m ( 1 8) in the y nd 21 4 m ( 3 1) on the reef s mesured y mens of horizontl Secchi disk. The verge tidl mplitude in the re is 3 cm (De Hn & Zneveld, 1959). The y hs long (1 km) nd nrrow ( 7 m) entrnce tht connects it to the djcent fringing reef. This reef is prt of mrine prk tht stretches up to the southwest tip of the islnd. The reef system strts with shllow reef flt (from 2 7 m depth), typiclly covered y gorgonins, t the edge of which the drop-off is locted (t 5 1 m depth). Corl cover on the drop-off nd reef wll is predominted y the stony corl Montstre nnulris. A detiled description of the reefs in the Netherlnds Antilles cn e found in Bk (1975). Smpling design A totl of 35 permnent trnsects were used in 11 sites on the reef nd in the y (Tle 1), covering totl re of out 45 m 2. Ech of the trnsects ws censused 29 times on verge, during dytime in My through to Septemer In Spnish Wter By, six segrss sites were selected (Figure 1). At ech segrss site, three permnent 3 y 5 m elt trnsects were plced, which were surveyed y snorkelling. Averge wter depth of these trnsects ws etween 8 nd 2 4 m. Adjcent to four of the segrss sites (numered 2, 3, 4 nd 6) ws mngrove site (Figure 1). The mngrove stnds consist of strips of vegettion

3 Migrtion ptterns nd hitt preference of corl reef fishes N N Curço 15 Crien Se Trde wind 1 Spnish Wter By m 5 m 5 m 5 5 m 5 m 1 m m 1 m 5 m m 1 Mngroves Segrss eds Corl reef Spnish Wter By 7 FIGURE 1. Loction of the study sites in Spnish Wter By. At sites 1 6 the segrss eds were censused, while t site 2, 3, 4, nd 6 mngroves were lso surveyed. Site 7 ws the reef site. hnging over from fossil reef ledges, hence providing structurl complexity from prop roots or rnches in the wter column eneth the mngrove cnopy. The eight mngrove trnsects were nrrow underwter hitts, nd were censused y snorkelers. In the mngroves, trnsect width ws etween 1 1 nd 2 1 m (Tle 1). At the reef site (numered 7, Figure 1), three permnent 3 y 5 m elt trnsects were plced t three depths (5, 1 nd 15 m) prllel to the costline, using nylon twine. The three 5 m deep trnsects were plced where the sndy reef flt ends t the strt of the drop-off, the three 1 m deep trnsects

4 312 E. Cocheret de l Morinière et l. TABLE 1. Surfce re of the 35 trnsects in ll sites nd hitts. Site numers correspond to Figure 1. On the corl reef, 3 trnsects were used t ech depth, s indicted etween rckets Site Hitt Trnsect Width (m) Length (m) Are (m 2 ) 1 6 Segrss Mngrove (3 t 5 m depth) (3 t 1 m depth) (3 t 15 m depth) were locted on the drop-off wheres the three 15 m deep trnsects were situted on the reef slope. At ech depth, the three trnsects were plced 5 m prt from ech other. The depth rnge ws sed on pilot-study tht showed tht the selected species reched highest densities t depths less thn 15 m. sites were censused y Scu diving. During visul surveys, individuls of the selected species were counted nd their sizes estimted in size-clsses of 2 5 cm. Underwter size estimtors were trined with ojects of known size. The three oservers censused ll trnsects using n lternting system so tht ny is in size-estimtion is eqully represented in every trnsect. The oserver effect ws tested using ANOVA (see Sttisticl nlysis for further explntion). All juvenile fishes oserved in this study were lrger thn 1 cm t settlement. Juvenile scrids smller thn 5 cm (TL) could not e identified in the field. Scrids of sizes smller thn 5 cm were left out of the dt sets of Scrus iserti nd S. teniopterus. Juveniles nd su-dults of these two scrids tht were lrger thn 5 cm (TL) could e distinguished y the chrcteristics shown in Humnn (1996). All other species could e identified t ll sizes. Sttisticl nlysis For ech species, men size (cm) nd totl density (N 1 m 2 ) of the oserved individuls ws clculted t ech survey of trnsect (ech of the 35 trnsects ws censused 29 times on verge). Dt were logtrnsformed nd nlysed in nested ANOVA (GLM, SPSS 8.) for unequl smple sizes, where sites were nested in hitts nd individul surveys of the trnsects were treted s replictes within sites. Multiple comprisons of mens within hitts (mong sites) nd mong hitts were nlysed using Tukey HSD Spjotvoll/Stoline test (Sokl & Rohlf, 1995). Oserver effect ws tested y one-wy ANOVA on ech of the 35 trnsects, with oserver identity s n independent vrile nd men size or totl density in the surveys s dependent vrile. None of the 35 ANOVAs on oserver effect produced significnt differences (P< 5) in vrince mong size or density estimtion mong oservers. Since there is vriety of previling hitts in Spnish Wter By (mngroves, segrss eds, lgl eds, chnnel, fossil reef terrce notches, oulders, corl reef; see Ngelkerken et l., ), nd the selected species use these shllow hitts s dily resting sites to which they return every dy fter nocturnl migrtions to deeper feeding or sleeping grounds (Ngelkerken et l., ), their dytime density distriution cn e viewed s mtter of choice. Therefore, the density of size-clss of fish species in mngroves reltive to its density in segrss eds is viewed s level of hitt preference. The level of preference for either mngroves or segrss eds ws tested sed on densities of the size-clsses of ech fish species occurring in mngroves nd segrss eds t site numers 2, 3, 4 nd 6 (Figure 1). Only these sites were used for nlysis of hitt preference ecuse oth segrss nd mngrove hitts were surveyed t those sites. For ech sizeclss of ech species, the verge density in mngroves t site ws divided y the sum density of tht size-clss in mngroves nd segrss eds t tht site. These mngrove-to-segrss preference levels of the size-clsses of the species t the four sites were then clustered using City-lock (Mnhttn) distnces (Sttistic for Windows 4 5). In the Mnhttn distnces mesure, the effect of single lrge differences (outliers) is dmpened (in the Eucliden distnce mesure, differences re squred). Results Hitt preference Men densities (1 m 2 ) of most species re significntly lower on the corl reef thn in segrss or mngrove hitts, with the exception of Ocyurus chrysurus (corl reef densities similr to densities in segrss eds nd lowest densities in mngroves) nd

5 Migrtion ptterns nd hitt preference of corl reef fishes 313 TABLE 2. Averge size (cm) nd density (N 1 2 ) per species in ech hitt, nd their stndrd errors etween rckets. Among sizes, significnt (P< 5) differences re indicted with,, nd c for ech species. Among densities, significntly different mens re mrked d, e, or f for ech species. Different letters ( f) men tht verges re significntly different Size Densities Mngrove Segrss Mngrove Segrss Acnthurus hinus 4 4 ( 4) 12 9 ( 6) 4 3 d ( 5) 4 9 d (1 6) Acnthurus chirurgus 13 ( 3) 11 ( 3) 17 c ( 5) 3 3 d ( 3) 9 e ( 2) 2 8 f ( 9) Hemulon flvolinetum 8 8 ( 2) 7 7 ( 1) 15 1 c ( 2) 99 8 d (12 2) 32 1 e (1 7) 3 2 f ( 4) Hemulon sciurus 12 3 ( 2) 11 5 ( 1) 21 5 c ( 3) 18 2 d (1 2) 5 7 e ( 3) 3 f ( ) Lutjnus podus 12 3 ( 2) 11 3 ( 5) 18 5 ( 5) 24 7 d (1 4) 3 e ( 1) 1 f ( 1) Lutjnus griseus 14 2 ( 3) 12 6 ( 3) 16 6 (1 1) 8 1 d ( 8) 5 e ( 1) f ( ) Ocyurus chrysurus 9 3 ( 4) 9 8 ( 2) 17 1 ( 3) 2 1 d ( 4) 3 6 e ( 4) 4 1 e ( 5) Scrus iserti 8 1 ( 3) 7 8 ( 1) 11 9 ( 3) 11 5 d (2 ) 13 3 d (1 3) 2 9 e ( 2) Scrus teniopterus 6 3 ( ) 6 4 ( 1) 16 4 ( 3) 6 3 d (1 3) 1 7 e ( 3) 3 6 f ( 2) Acnthurus hinus (not oserved in mngroves, nd segrss densities not significntly different from reef densities) (Tle 2). Overll densities of Scrus iserti, Ocyurus chrysurus, nd Acnthurus hinus re higher in segrss eds thn in mngroves, while the reverse is true for the remining species (Tle 2). In order to determine the level of hitt preference, mngrove-to-segrss density rtios (see Sttisticl nlysis) were determined for ech size-clss t four sites where oth mngroves nd segrss eds were surveyed. Cluster nlysis of these mngrove-tosegrss density rtios t the four sites (numered 2, 3, 4, nd 6 in Figure 1) yielded three distinct groups of size-clsses of fishes t linkge distnce 2 (Figure 2). Cluster A hd n verge mngrove-to-segrss density rtio of 18% (rnge 46%); in cluster B, tht rtio is 6% (34 75%), nd in cluster C it is 93% (64 1%). All size-clsses of Lutjnus podus nd Hemulon sciurus elonged to cluster C, reflecting strong preference for mngroves t ll size-clsses. Lutjnus griseus lso seems to prefer mngroves over segrss eds, since ll size-clsses were memers of cluster C, nd one size-clss (7 5 1 cm) ws in cluster B. Acnthurus hinus ws only oserved in segrss hitts, nd therefore ll size-clsses were memers of cluster A. Acnthurus chirurgus distriuted itself over mngroves nd segrss eds (most sizeclsses re memers of cluster B), with few individuls of the lrgest size-clss found only in mngroves (nd therefore prt of cluster C). Ocyurus chrysurus ws oserved in oth segrss eds nd mngroves (size-clsses re prt of clusters A nd B). Scrus iserti occurred mostly in segrss eds (cluster A), ut mngrove preference seems to increse with size (lrgest sizes in cluster B). Hemulon flvolinetum is represented y size-clsses in ll three clusters, with ever-lrger sizes found in clusters with n incresing mngrove-to-segrss density rtio. The ltter two species suggest tht their smllest juveniles re most commonly found in segrss eds, while mngrove preference increses with size of the juveniles. Only one size-clss (5 7 5 cm) of Scrus teniopterus ws oserved in the mouth of the y, of which individuls were oserved in mngroves nd segrss eds (cluster B). Size-distriution over hitts In Figure 3, reltive densities of the selected species in the three hitts re depicted for ech size-clss. All selected species were nursery species, in the sense tht high densities of juveniles were found in mngroves or segrss eds, while most dults were oserved on the reef. All three hitts differed significntly in the verge sizes of individuls of Hemulon flvolinetum, H. sciurus, nd Acnthurus chirurgus tht they hroured (Tle 2). Ocyurus chrysurus, Lutjnus podus, Scrus iserti, nd S. teniopterus showed no difference in verge sizes etween mngroves nd segrss eds, ut individuls on the reef were significntly lrger. Acnthurus hinus ws never found in mngroves, nd the verge size of the individuls of this species oserved in segrss eds ws smller thn on the reef. Averge size of Lutjnus griseus ws significntly smller in segrss eds thn in mngroves nd on the corl reef, while the ltter two hitts showed verge sizes tht were similr to ech other. Men size of ll nine species on the reef (Tle 2) ws lwys smller thn or corresponded to the pproximte men totl lengths t which these species ecome sexully mture (see Figure 3).

6 314 E. Cocheret de l Morinière et l. Linkge distnce O. chrys 17.5 O. chrys O. chrys A. h A. h A. h A. h A. h A. h 2.5 S. iser S. iser O. chrys O. chrys S. iser H. flv H. flv H. flv 2.5 O. chrys 22.5 O. chrys 2.5 S. ten O. chrys O. chrys H. flv H. flv A. chir L. gris S. iser A. chir A. chir A. chir S. iser A. chir 22.5 A. chir A. chir A. chir 17.5 A. chir 2.5 L. po L. po L. po L. gris L. po L. po L. po L. gris 17.5 L. po 17.5 H. flv L. po L. po L. po 22.5 L. po 2.5 L. gris 22.5 A. chir H. sci 17.5 L. gris H. sci 22.5 L. gris L. gris L. gris H. flv H. sci H. sci H. sci H. sci H. sci H. sci H. sci 2.5 A B C FIGURE 2. Complete linkge of reltive (mngrove-to-segrss) densities of the size-clsses of the study species in four sites (numered 2, 3, 4 nd 6; see Figure 1), using City-lock (Mnhttn) distnces. Species re indicted y the following codes: A. h=acnthurus hinus, A. chir=acnthurus chirurgus, H. flv=hemulon flvolinetum, H. sci=hemulon sciurus, L. po=lutjnus podus, L. gris=lutjnus griseus, O. chrys=ocyurus chrysurus, S. iser=scrus iserti, S. ten=scrus teniopterus. Size-clsses (cm) re indicted y the numers ehind the species codes.

7 Migrtion ptterns nd hitt preference of corl reef fishes 315 Sptil migrtion ptterns The size-frequency distriution of Hemulon flvolinetum, H. sciurus, Acnthurus chirurgus, Lutjnus podus, Scrus iserti, nd Ocyurus chrysurus in mngroves nd segrss eds nd on the reef suggests size-rnge for ech species over which the juveniles strt migrting to the corl reef (Figure 3). In the cse of Scrus teniopterus this migrtion from nursery hitt to corl reef ppers to tke plce rther ruptly, while individuls of Acnthurus hinus my migrte to reef hitts t ll sizes. When size-frequencies were compred mong y sites within ech hitt (ANOVA), heterogeneous distriution ptterns over sites emerged for some species (Tle 3). For H. sciurus, the extremely low ( 9 1 m 2 ) densities of smll individuls t site 2 re responsile for significnt differences mong segrss sites. Hemulon flvolinetum, Scrus iserti, nd Ocyurus chrysurus displyed size-frequency distriution in which high densities of smll individuls were found in mngroves nd segrss eds in the mouth of the y (t site numers 1 nd 2, Figure 1), medium-sized fishes deeper in the y, nd lrge fishes on the reef [Figure 4(, nd c)]. This indictes Postsettlement Life Cycle Migrtion (PLCM) pttern with two chnges of direction. Both Acnthurus hinus nd Scrus teniopterus were only encountered t sites 1 nd 2, which re locted in the mouth of the y (see Figure 1), nd on the reef. They were not oserved t sites locted deeper into the y. In oth cses, high densities of smll juveniles were detected in the mouth of the y [Figure 4(d nd e)], while sttisticlly lower densities nd lrger individuls of these species occurred on the reef (Tle 2). Their distriution indictes PLCM pttern tht is restricted to segrss nd mngrove sites in the close vicinity of the reef, nd does not include temporry residence deeper in the y. Discussion Hitt preference From previous studies in the sme y (Ngelkerken et l.,, ), it is known tht fish hve numer of occurring hitts to choose from in Spnish Wter By (mngroves, segrss eds, lgl eds, chnnel, fossil reef terrce notches, oulders). These shllow hitts re used s dily resting sites, to which the fishes return every dy fter nocturnl migrtions to deeper feeding or sleeping grounds (Ngelkerken et l., ). Therefore, the reltive density distriution of fish species over mngroves nd segrss eds t dytime is considered here s mtter of choice. Cluster-nlysis of the mngrove-to-segrss density rtios of ech size-clss, t four sites tht hroured oth hitts showed different levels of hitt preference. Lutjnus podus nd Hemulon sciurus showed strong preference for mngroves over segrss eds t ll size-clsses. L. griseus ws lso strongly ssocited with mngroves t ll size-clsses, nd modertely y one size-clss. Acnthurus hinus ws not oserved in mngroves, reflecting strong preference for segrss eds. Ocyurus chrysurus nd Acnthurus chirurgus utilized oth hitts. Scrus iserti nd Hemulon flvolinetum lso used oth hitts, ut there ws trend of incresed preference for mngroves with incresing fish size, while the smllest juveniles of these species were highly ssocited with segrss eds. Though seemingly mrginl hitts, strips of mngroves of no more thn 1 y 4 m t times my contin hundreds of individuls in resting schools. The preference of Scrus teniopterus for mngroves my e exggerted (mngrove-to-segrss density rtio ws out 6% : 4%), since juveniles smller thn 5 cm were excluded from the dt set. Unidentifile scrid juveniles of this size were mostly found in the mouth of the y (verge density m 2 in the mouth of the y s opposed to 8 1 m 2 in trnsects deeper in the y) in segrss eds. Ngelkerken et l. (, c) hve found similr overll density distriutions of these species in mngrove hitts nd segrss hitts in Curço nd Bonire. The level of preference of these fish species for mngroves or segrss eds in the sitution where oth hitts occur, however, is no indiction of the level of dependence on these hitts. From comprisons mong ys with nd without mngroves or segrss eds (Ngelkerken et l., 1), it is known tht species tht showed strong preference for mngroves in the present study (Lutjnus podus, L. griseus, Hemulon sciurus) depend lrgely on the presence or sence of segrss eds. Given the choice, such species pprently prefer mngroves s dytime resting sites for shelter, while their dependence on segrss eds is est explined y the lrger undnce of food in segrss hitts in which they forge t night. Size-distriution nd sptil migrtion ptterns All selected species proved to e nursery species in the sense tht juveniles were much more undnt in mngroves or segrss eds thn on the reef, s expected from our previous study (Ngelkerken et l., ). Of nine species, six (Hemulon flvolinetum,

8 316 E. Cocheret de l Morinière et l. Averge density (%) Averge density (%) Averge density (%) Averge density (%) Averge density (%) Segrss Mngrove Segrss Mngrove Segrss Mngrove () H. flvolinetum Mngrove (c) A. chirurgus (e) L. podus Segrss Segrss (g) Scrus iserti (i) A. hinus Size-clsses (cm) Averge density (%) Averge density (%) Averge density (%) Averge density (%) (d) Scrus teniopterus Mngrove Segrss Segrss Mngrove Segrss () H. sciurus Segrss Mngrove (h) Ocyurus chrysurus (f) L. griseus Mngrove Size-clsses (cm)

9 Migrtion ptterns nd hitt preference of corl reef fishes 317 TABLE 3. Anlysis of vrince of sizes mong sites within y hitts. Bold print represents P-vlues smller thn 5. ANOVA could not e pplied to A. hinus nd S. teniopterus. Significnt P-vlues indicte tht vrince of sizes of fishes is not homogeneously distriuted over sites within tht hitt Mngrove Segrss Acnthurus hinus 44 Acnthurus chirurgus 16 Hemulon flvolinetum Hemulon sciurus Lutjnus podus Lutjnus griseus Ocyurus chrysurus 1 Scrus iserti Scrus teniopterus H. sciurus, Lutjnus podus, Ocyurus chrysurus, Acnthurus chirurgus, nd Scrus iserti) showed sptil distriutions in which smllest individuls were only found in y hitts. The lrgest individuls of Hemulon flvolinetum, Lutjnus podus, Ocyurus chrysurus, nd Scrus iserti were found only on the djcent reef, while dults of Hemulon sciurus, nd Acnthurus chirurgus were found oth in reef hitts s well s in y hitts (mngrove or segrss). Averge size of these six species ws lrgest on the reef. The size t which these species ecome sexully mture (Roertson & Wrner, 1978; Munro, 1983; Munro pers. comm.) lwys corresponded to or ws lrger thn the verge size t which they were found on the corl reef. The results suggest Postsettlement Life Cycle Migrtion (PLCM) pttern over considerle distnce, in which juveniles settle nd grow up in lterntive hitts such s segrss eds nd mngroves, fter which the su-dults migrte to reef hitts where they ecome sexully mture. Tht pttern is nmed Long Distnce PLCM. Averge size of Lutjnus griseus ws smllest in segrss eds, while verge sizes in mngroves nd on reefs were similr. The size t which Lutjnus griseus ecomes sexully mture is out 25 cm (Strck, 1971; Clro, 1983), nd individuls of this size hve een oserved in mngroves s well s on the reef. Since smll juveniles of Lutjnus griseus were only oserved in y hitts, nd spwning occurs on the reef or shelf edge (Clro, 1983), it is ssumed tht it is nursery species s well, nd tht it migrtes ccording to the ove mentioned Long Distnce PLCM pttern. This distriution pttern fits the oserved size-distriution y other uthors well (e.g. Prrish, 1989 nd references therein; Rutherford et l., 1989; Appeldoorn et l., 1997), with lrger individuls found progressively off-shore. Three species, Hemulon flvolinetum, Ocyurus chrysurus nd Scrus iserti, showed similr sizefrequency distriution ptterns with three sptilly seprted groups tht were sttisticlly different: smll juveniles in the mouth of the y, lrger individuls in segrss eds nd mngroves locted deeper into the y nd (su-) dults on the reef. This sptil distriution suggests Life Cycle Migrtion tht involves more thn one direction of migrtion, nd is hence termed Stepwise PLCM. Post-lrve of these species settle in the mouth of the y, fter which they migrte deeper into the y to grow up to size lrge enough to migrte to nd dwell on the reef. Most migrnts into costl regions come from the open se (Bler, 1997). These re in-out migrtions: juveniles or dults or oth migrte into n esturine or costl re for certin period, fter which they return to the open se or corl reef. De Sylv (1963) descries distriution pttern of Sphyren rrcud tht is coherent to the Stepwise PLCM ptterns tht were found in our study. Post-lrve nd juveniles of this piscivore move from costl shllows to reed eds or mngroves, followed y migrtion to open se. Juveniles of Scrus teniopterus nd Acnthurus hinus were only found in the mouth of the y nd on the reef. Smll juveniles of Acnthurus hinus were only oserved in segrss eds in the mouth of the y nd in the reef flts, while dults occurred lmost exclusively on the reef. These two species disply type of Short Distnce PLCM in which lrve prtly settle in the mouth of the y nd prtly in the reef flts, to rech size t which they migrte to deeper reef hitts. Interestingly, some congeneric species ppered to disply different directions of migrtion t similr sizes. Scrids of similr sizes re found mixed in the mouth of the y, ut one species then migrtes to reef hitts (Scrus teniopterus), nd the other migrtes deeper into the y nd only dwells on the reef t lrger sizes (Scrus iserti). Leving unidentifile scrids smller thn 5 cm out of the dt sets FIGURE 3. Averge reltive density of individuls of the selected species in three hitts, clculted per size-clss. The rrows indicte pproximte length t sexul mturity (mturity dt from Munro, 1983; Strck, 1971; Clro, 1983).

10 318 E. Cocheret de l Morinière et l. Men size (cm) () cd d ce e M2 M3 M4 M6 S1 S2 S3 S4 S5 S6 Sites () M2 M4 c c M6 S1 S2 S3 S4 S5 S6 Sites 24 (c) 24 (d) Men size (cm) c cd d Men size (cm) M2 M3 M4 M6 S1 S2 S3 S4 S5 S6 Sites (e) S1 S2 Sites ± Std. Dev. Men M2 S1 S2 Sites FIGURE 4. Men nd stndrd devition of size-distriution of Hemulon flvolinetum (), Scrus iserti (), Ocyurus chrysurus (c) Scrus teniopterus (d) nd Acnthurus hinus (e) t ech site. Within ech hitt (indicted with S, M, or, for segrss, mngrove nd reef hitts, respectively), sttisticlly significnt differences mong sites (Tukey HSD) re presented y letters only when the species ws found in tht hitt t more thn one site. Different letters men tht the verges of the sites re sttisticlly different. did not ffect conclusions regrding the sptil migrtion ptterns of these species, since this sizeclss ws lmost exclusively found in the mouth of the y. Apprently, oth scrids settle in segrss eds nd mngroves locted in the mouth of the y, fter which ech migrtes in n opposite direction. The sme difference is oserved when compring the migrtion ptterns of Acnthurus chirurgus nd A. hinus. Of Acnthurus hinus it is known tht ehviourl interctions re size-relted nd cn ffect distriution, undnce nd erly post-settlement persistence of settlers (Risk, 1998), while postsettlement hitt selection is importnt in creting sptil ptterns of recruitment (Sponugle & Cowen, 1996). This mens tht competitive congeneric species cn llevite competition on the reef y temporry sptil seprtion. Possile explntions for different sptil sizefrequency distriutions of post-settlement fishes involve vriility in mortlity rtes, growth,

11 Migrtion ptterns nd hitt preference of corl reef fishes 319 FIGURE 5. Three types of migrtion mong nurseries nd the corl reef. Route 1 depicts the Short Distnce PLCM, route 2 Stepwise PLCM, nd route 3 Long Distnce PLCM (explntion see text). settlement ptterns nd migrtion ptterns. Since the undnce of predtors is much lower in the y thn on the reef s is generlly the cse (Shulmn, 1985; Prrish, 1989), differences in mortlity rtes my explin the high undnce of juveniles in y hitts nd the reduced numers on the corl reef. In fct, reduced mortlity mong juveniles in nursery hitts is often scried to reduced predtor undnce or efficiency (e.g. Heck & Crowder, 1991; Roertson & Bler, 1992). This, however, cnnot explin the lower numer of (su-)dults in mngrove nd segrss hitts or the low numers of the smllest juveniles in the hitts tht re locted deep in the y. Also, undnce nd vilility of food items (such s enthic nd plnktonic invertertes, epifun nd epiphytes) is much higher in the y hitts of Spnish Wter By thn on the nery corl reef (Cocheret de l Morinière et l., unpulished), which could not result in lower growth rtes of fishes in the y. Vriility in growth rte is therefore nother unlikely explntory fctor for the fct tht the lrgest individuls of nursery species re usully found on the corl reef. The spwning sesons of the selected species re lrgely during the study period (Munro et l., 1973), nd regulr settlement (no mjor peks) of postlrve ws oserved for most of the species during the study. Considering ll these processes, migrtion from nursery ground to corl reef hitt seems logicl explntion for the sptil distriution of size-clsses of these fish species, nd migrtory ptterns cn e inferred. The stility of such ptterns nd vlidity of ctul migrtions must e tested in further studies. Conclusions Tking dy-to-dy vritions in fish density nd sizefrequency into ccount over five-month period, sptil ptterns emerge for the selected fish species. Of some species, ll size-clsses tht occurred in y hitts ppered to prefer mngroves s dytime resting sites, while others were only found in segrss eds. Other species utilized nd preferred mngroves nd segrss eds t different sizes, nd preference for mngroves of some species incresed with incresing size-clss. The size-frequency distriution ptterns of Hemulon flvolinetum, H. sciurus, Acnthurus chirurgus, Lutjnus podus, Scrus iserti, nd Ocyurus chrysurus in mngroves nd segrss eds nd on the reef suggest size-rnge for ech species over which the juveniles strt migrting to the corl reef (Figure 3). In the cse of Scrus teniopterus this migrtion from nursery hitt to corl reef ppers to tke plce rther ruptly, while individuls of Acnthurus hinus my migrte to reef hitts t ll sizes. Hemulon sciurus, Lutjnus podus, L. griseus, nd Acnthurus chirurgus disply Long Distnce PLCM; Hemulon flvolinetum, Ocyurus chrysurus nd Scrus iserti use Stepwise PLCM; Scrus teniopterus nd Acnthurus hinus re retined within smll distnce from the reef (Short Distnce PLCM). These different migrtion ptterns re depicted in Figure 5. The fct tht some species crry out specific directionl migrtions nd congeners my migrte to different res rises questions concerning the mechnisms tht trigger these migrtionl options,

12 3 E. Cocheret de l Morinière et l. nd their ecologicl or evolutionry mening. This lso encourges scientists to view the nursery question not only from the point of view of enevolence of nursery res, ut lso to elucidte why species shows prticulr migrtion pttern or why it does not. Acknowledgements We would like to thnk ll personnel of the Crmi Foundtion, where the reserch ws crried out. The reserch ws funded y the Netherlnds Foundtion for the Advncement of Tropicl Reserch (WOTRO). The Stichting Nijmeegs Universiteitsfonds (SNUF) funded B. J. A. Pollux. Furthermore, we thnk E. Krdinl for supplying us with mp of the Spnish Wter By nd the Winkel fmily for the use of their pier. Finlly, we would like to thnk Blu Formn for her help with the grph on migrtion ptterns, nd P. H. Nienhuis for useful comments on the mnuscript. References Appeldoorn, R. S., Recksiek, C. W., Hill, R. L., Pgn, F. E. & Dennis, G. 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