Seasonal and ontogenetic patterns of habitat use in coral reef fish juveniles

Estuarine, Coastal and Shelf Science 75 (2007) 481e491 www.elsevier.com/locate/ecss

Seasonal and ontogenetic patterns of habitat use in coral reef fish juveniles C. Mellin a,*, M. Kulbicki b, D. Ponton a a

Institut de Recherche pour le Developpement (IRD), UR 128 Coreus, 101 promenade Laroque, BP A5, 98848 Noume´a Cedex, New Caledonia Institut de Recherche pour le Developpement (IRD), UR 128, 52 Av. Paul Alduy, Universite´ de Perpignan, 66860 Perpignan Cedex, France

b

Received 5 October 2006; accepted 11 May 2007 Available online 5 July 2007

Abstract We investigated the diversity of patterns of habitat use by juveniles of coral reef fishes according to seasons and at two spatial scales (10e100 m and 1e10 km). We conducted underwater visual censuses in New Caledonia’s Lagoon between 1986 and 2001. Co-inertia analyses highlighted the importance of mid-shelf habitats at large spatial scale (1e10 km) and of sandy and vegetated habitats at small spatial scale (10e100 m) for most juveniles. Among all juvenile species, 53% used different habitats across seasons (e.g. Lutjanus fulviflamma and Siganus argenteus) and 39% used different habitats as they grow (e.g. Lethrinus atkinsoni and Scarus ghobban). During their ontogeny, at large and small scales, respectively, 21% and 33% of the species studied showed an increase in the number of habitats used (e.g. L. fulviflamma, L. atkinsoni), 10% and 3% showed a decrease in the number of habitats used (e.g. Amphiprion melanopus, Siganus fuscescens), 23% and 3% showed a drastic change of habitat used (e.g. S. ghobban, Scarus sp.) whereas 46% and 61% showed no change of habitat used (e.g. Lethrinus genivittatus, Ctenochaetus striatus). Changes in habitat use at both small and large spatial scales occurred during the ontogeny of several species (e.g. S. ghobban, Scarus sp.). Results pointed out the different spatial and temporal scales of juvenile habitat use to account for in conservation decisions regarding both assemblage and species-specific levels. Ó 2007 Elsevier Ltd. All rights reserved. Keywords: coral reef fish; habitat; assemblage; season; ontogeny; spatial scale

1. Introduction One of the most fundamental challenges in ecology is to understand how animals distribute themselves among available habitats (Gaston, 2000; Arrington et al., 2005) and how their spatial distribution varies during ontogeny (De Roos et al., 2002; Wilson et al., 2006). For coral reef fishes, settlement to benthic habitats and subsequent habitat shifts has been found to be critical in their life cycle (e.g. Mc Cormick and Makey, 1997; Leis and McCormick, 2002; Lecchini and Galzin, 2005). At the end of the pelagic phase, the habitat selected by pre-settlement larvae strongly influences their survival and thus determines the spatial distribution of young juveniles (for

* Corresponding author. E-mail address: [email protected] (C. Mellin). 0272-7714/$ - see front matter Ó 2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.ecss.2007.05.026

recent review, see Doherty, 2002). At large scales (1e10 km), cross-shelf distributions of newly settled juveniles may result from distributions of larvae within suitable pelagic habitats, which vary from near-shore to oceanic waters (Williams, 1991). At smaller scales (10e100 m), the spatial distribution of juveniles has been found to vary as a function of depth (Srinivasan, 2003), substratum composition (Depczynski and Bellwood, 2004; Sale et al., 2005), and type of benthic coverage (Adams et al., 2004; Depczynski and Bellwood, 2004; Sale et al., 2005). The spatial distribution of older juveniles can then be modified by different mortality rates among habitats (Booth, 1992; Frederick, 1997) and/or ontogenetic habitat shifts (Mc Cormick and Makey, 1997; Dahlgren and Eggleston, 2000). Habitat use from juvenile to adulthood is usually inferred by comparing the spatial distributions of successive sizegroups of individuals (e.g. Shapiro, 1987; Gillanders et al.,

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2003; Adams and Ebersole, 2004; Lecchini and Galzin, 2005). Four patterns of habitat use between juvenile and adulthood are generally observed: (1) an increase in the number of habitats used; (2) a decrease in the number of habitats used; (3) a drastic change in habitat; and (4) no change in habitat. This latter pattern is further subdivided in, according to the habitat fish that are associated with: (4a) coral reef fish species; (4b) seagrass fish species; and (4c) coral-seagrass fish species. In the Indo-Pacific Islands, the diversity of patterns in juvenile fish habitat use has rarely been assessed (see for exceptions Nakamura and Sano, 2004; Lecchini and Galzin, 2005). Indeed, such studies require the consideration of the entire juvenile phase of each species in the assemblage (Mc Cormick and Makey, 1997; Dahlgren and Eggleston, 2000) and need extensive sampling schemes in space, to cover all potential habitats, and in time to take into account seasonal variations in juvenile abundance (Robertson and Kaufmann, 1998). The diversity of patterns in juvenile habitat use has thus always been assessed at a small spatial scale, so the influence of cross-shelf location on these patterns remains unclear. Additionally, whether or not the same changes of habitat use as existing between juveniles and adults also occur between successive juvenile size classes remain unknown. The aims of the present study were as follows: (1) to characterize the major assemblages of reef fish juveniles both at small and large spatial scales and their seasonal variations; (2) to highlight habitat shifts between successive size classes or between seasons for the dominant species; and (3) to assess the diversity of patterns in habitat use during the juvenile period of reef fishes.

2. Methods 2.1. Study area The present study was carried out in New Caledonia (southwest Pacific, 166 E, 22 S). The lagoon covers an area of 24,000 km2 with the barrier reef lying between 1 and 65 km from the coast. At these latitudes seasonal variations are observed in water temperatures, wind intensity and wind direction, and rainfall (Douillet et al., 2001; Ouillon et al., 2005). Sixteen years of underwater visual census of the fish fauna (Kulbicki, 1997, 2006) enabled us to investigate seasonal patterns in juvenile habitat use, as these have been suggested to be stronger than interannual variations in settlement intensity at these latitudes (Robertson and Kaufmann, 1998). 2.2. Sampling strategy Between 1986 and 2001, diurnal underwater visual censuses were carried out on 816 strip transects heterogeneously distributed in the south-west lagoon, between the coast and the barrier reef (Fig. 1). The position of each transect during each sampling campaign was such as the distance between transects was sufficient to insure independence of the data, i.e. no fish was likely to be counted twice and fish abundances at a given sampled place were not likely to influence fish abundances at other sampled places. Of the 816 transects, 78 were performed in summer (December 21steMarch 20th), 196 in autumn (March 21steJune 20th), 294 in winter (June 21steSeptember 20th) and 246 in spring (September

167°E

166°E

22°S

N 0

165°E

10km

168°E 20°S

Ne w

Ca led on ia

23°S 23°S

Fig. 1. Position of transects in the south-western part of the New Caledonia Lagoon. Due to the size of the map, all transects are not presented and dots may correspond to several transects.

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21steDecember 20th). Summer is the cyclonic season during which weather (wind, rain) or water (turbidity) conditions were often unsuitable for underwater visual censuses, resulting in fewer transects performed during this season. Each transect was sampled only once between 1986 and 2001. Each 10 m wide  100 m long transect was set at a random location and parallel to the isobaths. First, each transect was designated on the seafloor with a 100 m long measuring tape. Then, two experienced divers, separated by 5 m, swam slowly parallel to this line and simultaneously identified and counted all fish individuals to 2.5 m on either side of the respective diver, in adjacent 5-m wide swaths. Each diver estimated the total length (TL, in cm) of each encountered and identified fish. Individuals smaller than 3 cm were not recorded. When fish were forming a school, the mean TL and the total number of all individuals in the school were estimated. The size at first maturity Sm of each species (Table 1), i.e. the minimum size at which a mature female was observed based on the gonad status of at least 20 females of each species (Kulbicki, 2006), was used to separate adults from juveniles. Based on the ratio between TL and Sm we distinguished small, newly settled juveniles when TL  Sm/3, medium juveniles when Sm/3 < TL  2(Sm/3) and large juveniles close to recruitment to the adult population when 2(Sm/3) < TL
483

considered as predictors, usually the environmental variables, and one set of variables considered as response variables, usually the faunistic variables (Jongman et al., 1995). By contrast, CIA is a multivariate method based on the statistic of coinertia, which measures the co-structure between environmental and faunistic data sets that are equally considered (Dole´dec and Chessel, 1994). CIA aims to find a vector in the environmental space and a vector in the faunistic space with maximal co-inertia between them. These two vectors thus define the new ordination plan on which environmental and faunistic variables are separately projected and compared. As for other multivariate methods, graphical results are interpreted regarding the distance of each environmental or faunistic variable from the origin, which measures its contribution to the new ordination plan, and the angle between faunistic and environmental variables, which measures the correlation between these two variables. The four faunistic tables and the eight habitat tables were first separately analyzed by a Principal Components Analysis (PCA). Then, for each season (N ¼ 4) and each spatial scale (N ¼ 2), a co-inertia analysis was conducted between the ‘transect-by-juveniles’ table and the corresponding ‘transect-by-habitat variables’ table. The eight co-structures were separately determined by the maximization of the square-rooted projected inertia (which defines the structure of each table separately) and of the correlation between the two sets of projected coordinates (Dole´dec and Chessel, 1994). The significance of each resulting correlation was tested by a Monte-Carlo method with 1000 random permutations of the rows of the faunistic and habitat tables. Finally, for each season (N ¼ 4) and each spatial scale (N ¼ 2), a hierarchical clustering using centroid aggregation (Jongman et al., 1995; Lebart et al., 1995) was performed by taking the coordinates of species-size class combinations on all axes of co-inertia analysis. This approach, similar to the Ward’s method (Jongman et al., 1995), allows the number of clusters to be defined a priori. The number of clusters was defined in order to ensure the relevance of the clusters of species-size class combinations according to the ordination of habitat variables in each co-inertia analysis. For instance, the localisation of hard and soft bottom habitat variables on each side of Axis 1 of co-inertia lead to identify two clusters of juveniles, located on opposite sides of Axis 1. Each cluster of species-size class combinations was thus defined: (1) by their close ordination on the biplot; and (2) according to habitat variables at the spatial scale considered. Species-size class combinations that contributed the most to co-inertia were considered as characteristic of the assemblage to which they belonged. All analyses were performed with ADE-4 software (Thioulouse et al., 1997).1 3. Results We recorded a total of 74,097 juveniles belonging to 161 species of 46 families. Eleven families for which taxa were 1

Freely available at: http://pbil.univ-lyon1.fr/ADE-4/home.php?lang¼eng.

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Table 1 List of fish species for which juveniles were observed on more than 200 transects over the 816 performed and accounting for 90% of total abundances of juveniles at each season. The size at first maturity (Sm), the abundances of individuals total length (TL)  Sm/3 (small), Sm/3 < TL  2(Sm/3) (medium) and 2(Sm/3) < TL
Species

Sm (mm)

Lutjanidae

Lutjanus fulviflamma (Forsska˚l, 1775) Lutjanus gibbus (Forsska˚l, 1775) Lutjanus kasmira (Forsska˚l, 1775)

195 215 165

2 9 0

93 26 8

313 128 104

408 163 112

Lethrinidae

Lethrinus Lethrinus Lethrinus Lethrinus

atkinsoni (Seale, 1910) genivittatus (Valenciennes, 1830) harak (Forsska˚l, 1775) nebulosus (Forsska˚l, 1775)

230 105 220 195

17 71 0 3

276 65 25 56

62 198 161 50

355 334 186 109

Mullidae

Mulloidichthys flavolineatus (Lacepe`de, 1801) Parupeneus indicus (Shaw, 1803) Parupeneus multifasciatus (Quoy & Gaimard, 1824) Parupeneus spilurus (Bleeker, 1854)

110 190 180 160

0 21 0 1

1 36 168 49

45 18 390 81

46 75 558 131

Chaetodontidae

Chaetodon Chaetodon Chaetodon Chaetodon Chaetodon Chaetodon

155 100 95 90 115 120

94 2 0 0 0 2

389 141 14 3 78 107

413 1560 212 207 323 279

896 1703 226 210 401 388

Pomacentridae

Amphiprion melanopus (Bleeker, 1852) Chromis chrysura (Bliss, 1883) Neoglyphidodon polyacanthus (Ogilby, 1889) Stegastes nigricans (Lacepe`de, 1802)

100 85 90 90

8 0 0 0

216 311 59 242

190 8024 329 516

414 8335 388 758

Labridae

Choerodon graphicus (De Vis, 1885) Coris aygula (Lacepe`de, 1801) Halichoeres trimaculatus (Quoy & Gaimard, 1834) Stethojulis bandanensis (Bleeker, 1851) Thalassoma lunare (Linnaeus, 1758)

260 450 105 85 120

31 12 1 0 8

193 129 130 94 257

658 125 650 305 2145

882 266 781 399 2410

Scaridae

Scarus altipinnis (Steindachner, 1879) Scarus ghobban (Forsska˚l, 1775) Scarus sp.

420 410 290

0 218 223

112 573 1626

179 261 3435

291 1052 5284

Mugiloididae

Parapercis australis (Bloch, 1792) Parapercis hexophtalma (Cuvier, 1829)

95 170

4 2

335 35

471 141

810 178

Acanthuridae

Acanthurus dussumieri (Valenciennes, 1835) Acanthurus mata (Cuvier, 1829) Acanthurus nigrofuscus (Forsska˚l, 1775) Acanthurus triostegus (Linnaeus, 1758) Ctenochaetus striatus (Quoy & Gaimard, 1825) Zebrasoma scopas (Cuvier, 1829)

250 280 115 105 120 80

53 4 0 1 0 0

176 364 296 25 57 53

338 391 1330 96 108 703

567 759 1626 122 165 756

Siganidae

Siganus argenteus (Quoy & Gaimard, 1825) Siganus fuscescens (Houttuyn, 1782)

200 170

0 1646

457 507

1531 285

1988 2438

7782 21.0

26,755 72.4

Number of juveniles Small

auriga (Forsska˚l, 1775) lunulatus (Quoy & Gaimard, 1825) mertensi (Cuvier, 1831) pelewensis (Kner, 1868) trifascialis (Quoy & Gaimard, 1825) vagabundus (Linnaeus, 1758)

Total abundances Relative abundances (%)

observed on at least 200 transects were used for analysis. For co-inertia analysis, we used only the most abundant speciessize class combinations which together represented 90% of total abundances in each season (Table 1). Among these species-size class combinations, only 6.6% were small juveniles, against 21.0% medium and 72.4% large juveniles. However, for some species (e.g. Scarus ghobban and Siganus fuscescens) a larger proportion of small juveniles (respectively, 20.7% and 67.5%) was observed. Distributions of habitat data showed that the mean depth and the relative importance of the various benthic categories spanned the same range of values

2433 6.6

Medium

Large

Total

36,970 100

for each season (Table 2). The lowest visibility was 3 m and was only recorded on two transects in autumn and two transects in winter. The deepest transects were sampled in spring and the most shallow transects in summer. There were slightly more transects far from the coast in autumn. 3.1. Structure of juvenile fish assemblages at a large spatial scale (1e10 km) The total co-inertia between habitat characteristics at a large spatial scale and the faunistic table was partitioned on the first

C. Mellin et al. / Estuarine, Coastal and Shelf Science 75 (2007) 481e491 Table 2 Habitat characteristics (mean, std. dev.: standard deviation and range) recorded for transects at each season Summer

Autumn

Winter

Spring

Visibility (m)

Mean 10.7 10.2 11.9 12.6 Std. dev. 4.5 4.4 4.6 4.6 Range 5.0e23.0 3.0e23.0 3.0e23.0 4.0e23.0

Depth (m)

Mean 3.7 Std. dev. 2.4 Range 0.7e9.5

Distance to the main island (km)

Mean 14.5 22.2 16.6 15.5 Std. dev. 7.7 16.6 20.9 19.3 Range 0.0e30.0 0.0e50.0 0.0e47.0 0.0e52.0

4.5 4.4 5.1 4.1 3.6 4.0 0.8e19.0 0.7e16.0 0.8e25.6

Distance to the barrier reef (km)

Mean 22.2 10.4 17.5 15.4 Std. dev. 10.5 9.5 15.0 10.3 Range 0.0e40.0 0.0e40.0 0.0e48.0 0.0e35.0

Sand/mud (%)

Mean 31.1 39.3 39.1 38.5 Std. dev. 32.6 33.0 31.6 31.4 Range 0.0e100.0 0.0e100.0 0.0e100.0 0.0e100.0

Hard bottom (%)

Mean 39.2 25.9 32.2 30.0 Std. dev. 22.4 19.6 22.7 23.0 Range 0.0e87.9 0.0e78.9 0.0e100.0 0.0e90.9

Living coral (%)

Mean 33.5 19.3 21.2 24.3 Std. dev. 25.9 20.8 19.4 22.7 Range 0.0e100.0 0.0e76.2 0.0e81.6 0.0e71.4

Seaweed/seagrass (%) Mean 11.2 4.4 5.6 5.2 Std. dev. 21.0 12.2 13.0 12.0 Range 0.0e100.0 0.0e55.4 0.0e68.6 0.0e56.3

two axes of co-inertia analysis (Table 3). We found significant correlation between habitat and faunistic tables for all seasons (Monte-Carlo test, P < 0.001), with the highest correlation in autumn (Table 3). The distance to the barrier reef and the distance to the main island were separated by Axis 2 in all seasons (Fig. 2); Axis 1 thus represented the coast-barrier reef gradient along which species-size class combinations were distributed. For each season, we therefore identified three clusters of species-size class combinations (Table 4): one associated with coastal habitats, one associated with mid-shelf habitats, and one associated with barrier reef habitats. All seasons combined, a total of 64 species-size class combinations, including 17% of Scaridae, were associated with barrier reef habitats. Medium to large juveniles of Scarus sp. (97e 290 mm TL) were characteristic of barrier reef assemblages in nearly all seasons. A total of 31 species-size class combinations that included 29% of Chaetodontidae were associated with coastal habitats. Large juveniles of Chaetodon vagabundus (80e120 mm TL) and Neoglyphidodon polyacanthus (60e90 mm TL), as well as medium to large juveniles Parapercis australis (32e95 mm TL) were characteristic of coastal assemblages (Fig. 2). Assemblages associated with mid-shelf habitats were the most important, with 90 species-size class combinations, including 21% of Acanthuridae and 20% of Labridae. Mid-shelf assemblages were characterized by medium to large juveniles of Stegastes nigricans (60e90 mm TL) and large juveniles of Thalassoma lunare (80e120 mm TL). All juveniles of Labridae and Scaridae (except small,

485

Table 3 Inertia (in %) explained by the first two axes of the PCA analyses (PCA1 and PCA2) on habitat (two scales) and on faunistic tables for each season. Total co-inertia (in %) between the habitat (two scales) and faunistic tables explained by the first two axes of co-inertia analyses (CI1 and CI2) for each season. Correlation coefficient (range for all axes) between the two sets of projected coordinates. Large scale habitat characteristics are the shortest distance to the coast or the barrier reef. Small scale habitat characteristics are the average depth of the transect and its mean percentage of hard bottoms, of mud or sand, of living coral, and of seaweeds or seagrasses. Faunistic tables correspond to the log(X þ 1) abundances of each species-size class combination at each season. We found highly significant correlation between habitat and faunistic tables in all co-inertia analyses (Monte-Carlo’s test, P < 0.001) Summer

Autumn

Inertia (in %) explained by PCA1 and PCA2 Large scale 100.0 100.0 habitat table Small scale 68.0 61.2 habitat table Faunistic table 29.7 26.1 Total co-inertia (in %) explained by CI1 and CI2 Large scale 100.0 100.0 habitat  faunistic tables Small scale 90.5 73.0 habitat  faunistic tables

Winter

Spring

100.0

100.0

60.9

62.7

23.9

28.0

100.0

100.0

80.4

88.3

Correlation coefficient range between the two sets of coordinates Large scale 0.35e0.43 0.52e0.64 0.23e0.58 0.35e0.53 habitat  faunistic tables Small scale 0.28e0.63 0.41e0.58 0.39e0.57 0.26e0.53 habitat  faunistic tables

TL < 137 mm, Scarus ghobban) and most juveniles of Lethrinidae, Acanthuridae and Siganidae species were mainly found in mid-shelf and barrier reef habitats (Table 4). Habitats used by juveniles of Pomacentridae varied between species: juveniles of N. polyacanthus were characteristic of coastal habitats while juveniles of Chromis chrysura were characteristic of barrier reef habitats, and juveniles of S. nigricans were mainly observed in mid-shelf habitats. 3.2. Structure of juvenile fish assemblages at a small spatial scale (10e100 m) The total co-inertia between habitat characteristics at a small scale and the faunistic table was best explained by Axes 1 and 2 of the co-inertia analysis in summer and spring (Table 3). We found a significant correlation between habitat and faunistic tables in all co-inertia analyses (Monte-Carlo test, P < 0.001). For all seasons, the relative abundance of living coral and hard bottom was correlated and opposed to the relative abundance of mud or sand, and seaweed or seagrass (Fig. 3). For each season, we thus identified two clusters of species-size class combinations: one associated with living coral and hard bottom, the other associated with mud or sand with seaweed or seagrass (Fig. 3 and Table 4).

C. Mellin et al. / Estuarine, Coastal and Shelf Science 75 (2007) 481e491

486 dist

f

e to anc

tan

st coa

to

nce

dista

-0.10

ce

reef

ier barr

to

co

nce

to

rr ba

ta dis

as

t

-0.40

ree

ier

0.10

dis

0.15

0.40

0.25

21 Dec. - 20 Mar. (summer)

-0.10

-0.10

0.04 paaus2

lufuf3 chvag3 -0.08

C

B

21 Mar. - 20 June (autumn) 0.025 thlun3 hatri3 siarg2 scsp12

nepol3 0.10

scsp13 scsp12 chlut3

-0.20

M

B

nepol3 C

M

paaus2

thlun3 stnig3

chchr3 scsp13

-0.08

paaus3

-0.015

f

ee

rr

ie arr

a st to

0.02

t

as

21 June - 20 Sep. (winter)

-0.05

ob

dis

co

t

as

co

c tan

e

to

-0.20

0.20

f

ee

et

nc

ce an

-0.20

to

a

st

di

e nc

ba

rr

0.10

di

e rri

st

di

0.10

0.20

0.30

21 Sep. - 20 Dec. (spring)

-0.05 0.05 acnio3

-0.10 B

M

0.10 C chvag3 paaus3 scalt2

chaur2

scsp12 chaur3 chgra3 stnig3

paaus20.20

-0.15 B

M chaur3

chlut3 scsp13 -0.06

C chaur2 chvag3

chtri3 scsp13 scsp12 -0.05

Fig. 2. Seasonal co-inertia analyses between large scale habitat characteristics (shortest distance to the main island of the main island and shortest distance to the barrier reef) and log(X þ 1) transformed abundances of species-size class combinations. Species-size class combinations associated with coastal (C), mid-shelf (M), or barrier reef (B) habitats were identified by hierarchical clustering. Only the codes of the three species-size class combinations contributing the most to co-inertia are presented for each cluster for better readability. See Table 4 for the codes of species-size class combinations presented and for all species-size class combinations in each cluster.

All seasons combined, 54 species-size class combinations were associated with habitats of living coral and hard bottom, including most juveniles of Chaetodontidae, Pomacentridae, Scaridae and Acanthuridae. Large juveniles of Chaetodon lunulatus (66e100 mm TL) and medium to large juveniles of Scarus sp. (97e290 mm TL) were characteristic of this assemblage. By contrast, 131 species-size class combinations were associated with sandy and vegetated habitats including most juveniles of the Lutjanidae, Lethrinidae, Mullidae, Labridae and Siganidae. Large juveniles of Halichoeres trimaculatus

(70e105 mm TL) and medium to large juveniles of Parapercis australis (32e95 mm TL) were characteristic of this assemblage (Fig. 3). 3.3. Seasonal differences in habitat use Some dominant species-size class combinations showed differences in the habitat they were associated with across seasons (Table 4). Among all species-size class combinations, 23% were associated with different large scale habitats across

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Table 4 Habitat for species-size class combinations accounting for 90% of total abundances at each season. Species codes are followed by one for small juveniles, two for medium juveniles, and three for large juveniles. Ranges of sizes for each size class are in mm. Large scale habitat B: barrier, M: mid-shelf, C: coast, small scale habitat co: living coral and hard bottoms and sg: seagrass and seaweed beds with soft bottoms, and seasons sum: summer, aut: autumn, win: winter, spr: spring Genus

Species

Size class

Code

Sum

Aut

Win

Spr

Lutjanus

fulviflamma

65e130 130e195 144e215 110e165

lufuf2 lufuf3 lugib3 lukas3

B-sg C-sg B-sg B-sg

e M-co e e

e C-sg e M-sg

e C-sg M-sg e

<77 77e154 154e230 <35 70e105 147e220 65e130 130e195

leatk1 leatk2 leatk3 legen1 legen3 lehar3 leneb2 leneb3

B-sg B-sg C-sg e e e e C-sg

e M-sg e e e M-sg e M-sg

e M-sg e M-sg M-sg M-sg e e

e M-sg e e e e M-sg e

gibbus kasmira Lethrinus

atkinsoni

genivittatus harak nebulosus Mulloidichthys

flavolineatus

74e110

mufla3

e

e

e

M-sg

Parupeneus

indicus multifasciatus

<63 60e120 120e180 106e160

paind1 pamul2 pamul3 paspi3

e e e B-sg

M-sg M-sg B-sg M-sg

e e B-sg M-sg

e M-sg B-sg e

<52 52e104 104e155 33e66 66e100 64e95 60e90 76e115 40e80 80e120

chaur1 chaur2 chaur3 chlut2 chlut3 chmer3 chpel3 chtri3 chvag2 chvag3

e C-sg B-sg B-sg B-co e e B-co C-sg C-sg

M-sg C-sg B-co M-co M-co B-co B-co B-co e C-sg

e C-co M-co M-sg B-co B-sg B-sg B-co M-sg C-co

e C-sg M-sg M-sg B-co B-sg M-co M-co e C-sg

spilurus Chaetodon

auriga

lunulatus mertensii pelewensis trifascialis vagabundus Amphiprion

melanopus

33e66 66e100

ammel2 ammel3

B-sg B-sg

M-co M-co

M-sg e

C-sg e

Chromis

chrysura

28e56 56e85

chchr2 chchr3

B-sg e

M-sg B-co

e B-sg

M-sg B-sg

Neoglyphidodon

polyacanthus

30e60 60e90

nepol2 nepol3

C-sg C-sg

e C-co

e M-co

e C-sg

Stegastes

nigricans

30e60 60e90

stnig2 stnig3

M-sg M-sg

e M-co

M-sg M-sg

e M-sg

Choerodon

graphicus

<87 87e174 174e260

chgra1 chgra2 chgra3

B-sg B-sg B-sg

e M-sg M-co

e M-sg M-co

e e M-sg

Coris

aygula

150e300 300e450

coayg2 coayg3

e e

e e

M-sg e

M-sg B-sg

Halichoeres

trimaculatus

35e70 70e105

hatri2 hatri3

e e

e B-sg

M-sg B-sg

e B-sg

Stethojulis

bandanensis

28e56 56e85

stban2 stban3

B-sg e

e M-sg

e M-sg

e M-sg

Thalassoma

lunare

40e80 80e120

thlun2 thlun3

e M-co

M-sg M-sg

M-sg M-co

M-sg M-sg

Scarus

altipinnis

140e280 280e420 <137 137e174 174e410 0e97 97e194 194e290

scalt2 scalt3 scgho1 scgho2 scgho3 scsp11 scsp12 scsp13

e e C-sg B-co B-sg e M-co B-co

e B-co C-sg B-co B-co M-sg M-co B-co

e M-co C-sg M-co M-co e B-co B-co

M-co M-co C-sg M-sg M-sg e B-co B-co

ghobban

sp.

(continued on next page)

C. Mellin et al. / Estuarine, Coastal and Shelf Science 75 (2007) 481e491

488 Table 4 (continued ) Genus

Species

Size class

Code

Sum

Aut

Win

Spr

Parapercis

australis

32e64 64e95 114e170

paaus2 paaus3 pahex3

B-sg B-sg e

C-sg C-sg e

C-sg C-sg B-sg

C-sg e e

83e166 166e250 38e76 76e115 93e186 186e280 35e70 70e105

acdus2 acdus3 acnio2 acnio3 acmat2 acmat3 actri2 actri3

B-sg B-sg e C-sg e e e e

M-sg M-co M-sg M-sg B-co B-co e e

M-sg M-co M-sg B-co B-sg B-co M-sg B-sg

M-sg M-sg M-sg B-co M-sg M-sg e e

hexophtalma Acanthurus

dussumieri nigrofuscus mata triostegus

Ctenochaetus

striatus

40e80 80e120

ctstr2 ctstr3

e e

M-sg M-sg

e M-sg

e e

Zebrasoma

scopes

27e54 54e80

zesco2 zesco3

B-sg e

e M-sg

e B-co

e M-co

Siganus

argenteus

67e134 134e200 57e114 114e170

siarg2 siarg3 sifus2 sifus3

e B-co e e

M-sg e M-sg e

e M-sg M-sg e

e B-sg C-sg C-sg

fuscescens

seasons. For instance medium juveniles of Scarus sp. (97e 194 mm TL) were observed in mid-shelf habitats in summer and autumn, and in barrier reef habitats in winter and spring. Only 8% of species-size class combinations were associated with different small scale habitats across seasons, like large juveniles of Stegastes nigricans (60e90 mm TL) that were associated with living coral only in autumn. Last, 22% of species-size class combinations were associated with different habitats across seasons, both at small and large spatial scales. Large juveniles of Lutjanus fulviflamma (130e195 mm TL) were found in mid-shelf habitats with living coral only in autumn. Large juveniles of Acanthurus nigrofuscus (76e115 mm TL) and Siganus argenteus (134e200 mm TL) were found in barrier reef habitats with living coral, only in winter and spring for A. nigrofuscus, and only in summer for S. argenteus. Species-size class combinations (47%) were associated with the same habitats all year long.

3.4. Size class differences in habitat use Some juveniles were associated with different habitats during their ontogeny. Small juveniles of Scarus ghobban (TL < 137 mm) were associated with sandy and vegetated habitats while large individuals were associated with coral reef habitats. Similarly, small juveniles of Lethrinus atkinsoni (TL < 77 mm) were associated with barrier reef habitats, whereas medium juveniles (77e154 mm TL) were associated with barrier reef and mid-shelf habitats, and large individuals (TL > 154 mm) with coastal habitats. Thus, at a large spatial scale 21% of the taxa observed showed an increase in the number of habitats they were associated with as they grew (e.g. Lethrinus atkinsoni); 10% showed a decrease in the number of habitats they were associated with (e.g. Siganus fuscescens); 23% showed a radical change in the habitat they were associated with (e.g. Scarus

ghobban, Scarus sp.) and 46% showed no change at all (the last group comprising 39% of juveniles found in mid-shelf habitats, e.g. Lethrinus genivittatus). At a small spatial scale, 33% of the taxa presented an increase in the number of habitats they were associated with as they grew (e.g. Lutjanus fulviflamma); 3% showed a decrease in the number of habitats they were associated with (e.g. Amphiprion melanopus); 3% showed a radical change in the habitat they were associated with (e.g. S. ghobban, Scarus sp.) and 61% showed no change (the last group comprising 75% of juveniles found in seaweed and seagrass beds, e.g. S. fuscescens).

4. Discussion At a large spatial scale (1e10 km), species-size class combinations were partitioned along a coast-barrier reef gradient. Our results highlighted the role of mid-shelf habitats for the juveniles of a large number of reef fish species, especially for Lethrinidae, Labridae and Mullidae for which, respectively, 70%, 69% and 60% of the species-size class combinations were found in mid-shelf habitats. Similarly, in the Caribbean mid-shelf habitats were used by juveniles of Labridae and Scaridae as a step during ontogenetic migrations between coastal and reef habitats (Cocheret de la Morinie`re et al., 2002). Mid-shelf habitats provide a diversity of biotopes with sandy areas, seaweed and seagrass beds and patch reefs, and often hold lower abundances of predators than do barrier reef habitats (Parrish, 1989). Strategically, some juvenile fish may find in mid-shelf habitats the resource and refuge needed to reach a sufficient size before migrating on the barrier reef. At a small spatial scale, 54 species-size class combinations (mostly consisting of Chaetodontidae, Pomacentridae and Scaridae) were associated with living coral and hard bottom while 131 species-size class combinations (mostly consisting of Lutjanidae, Lethrinidae, Mullidae, Labridae and Siganidae)

mu d

co

ral

0.50

489

or sa nd

ge de

ing

avera

sa

nd

-0.50

0.20

liv

depth

or

e averag

0.30

m

ud

pth

C. Mellin et al. / Estuarine, Coastal and Shelf Science 75 (2007) 481e491

se aw ee d

or s

ea gr as s

0.20 -0.30 har living c o db 21 Mar. - 20 June sea otto ral 21 Dec. - 20 Mar. s w m ms eed (summer) (autumn) otto or s b eag d rass har -0.30 -0.10 0.08 0.05

-0.15

0.35 sg 0.20

-0.20 co lufuf3

scsp13

chlut3

chlut3

thlun3

co

sg paaus3

paaus2 chvag3 scsp12

nepol3

nepol3

scsp13

-0.10

g co

ge de

nd r sa do mu 0.20

se

21 Sep. - 20 Dec. (spring)

ee

aw d or

0.15

ag

se

chchr3

ss

ra

livin gc ora l d an s r ral o -0.30 d u m -0.30 0.20 s ottom s sea 21 June - 20 Sep. hard b we hard bottom e (winter) d -0.10 -0.10 or se 0.15 chchr3 ag ra ss livin

avera

pth

0.20

average de

0.30

pth

-0.15

chlut3 chlut3 -0.25

0.10 co

scsp13

-0.30

0.10 co

sg hatri3 paaus3

thlun3 -0.10

scsp13

sg

scsp12 stnig3

hatri3

-0.10

Fig. 3. Seasonal co-inertia analyses between small scale habitat characteristics (average depth of the transect, relative importance of hard bottom, living coral, mud or sand, and seaweed or seagrass) and log(X þ 1) transformed abundances of species-size class combinations. Species-size class combinations associated with hard bottom and living coral (co), or sand or mud with seaweed or seagrass (sg) habitats were identified by hierarchical clustering. Only the codes of the three speciessize class combinations contributing the most to co-inertia are presented for each cluster for better readability. See Table 4 for the codes of species-size class combinations presented and for all species-size class combinations in each cluster.

were associated with seaweed or seagrass beds with mud or sand. The fact that more than two-thirds of the species-size class combinations were associated with sandy and vegetated habitats underlines the important role of these habitats for the juveniles of a wide range of coral reef fish species. In the IndoPacific, this relationship had already been observed at small spatial scale for several Lethrinidae, Mullidae, Labridae and Siganidae in Japan (Nakamura and Sano, 2004) and in the Philippines (Kochzius, 1999). According to our results the importance of vegetated areas is also consistent when considering larger spatial scales. Several hypotheses have been suggested to explain the important role of these habitats:

they may provide shelter against predators (Parrish, 1989), high abundance of food (Cocheret de la Morinie`re et al., 2002; Nagelkerken et al., 2006) or simply intercept more efficiently planktonic larvae (Parrish, 1989; Nakamura and Sano, 2004). A number of studies have also demonstrated that microhabitat selection occurs early during settlement (Eggleston, 1995; Friedlander and Parrish, 1998; Andrews and Anderson, 2004) through chemical or visual cues (Booth, 1992; Ault and Johnson, 1998) that contribute to establish the initial patterns of spatial distribution in juvenile fishes. For example, the use of seagrass beds by juveniles of Lethrinus nebulosus showed in the present study corroborates similar observations

490

C. Mellin et al. / Estuarine, Coastal and Shelf Science 75 (2007) 481e491

in Japan which were related to olfactive cues orientating the selection of seagrass beds by settling juveniles of this species (Arvedlund and Takemura, 2006). Given the high diversity of species using seagrass beds highlighted in the present study, our results warrant further investigations on the potential diversity of mechanisms implicated in the selection of these habitats by settling juveniles. Whereas 47% of species-size class combinations showed no seasonal differences in the habitat they were associated with, 8% showed seasonal differences at a small spatial scale, 23% at a large spatial scale and 22% at both spatial scales. For instance large Lutjanus fulviflamma, Acanthurus nigrofuscus, and Siganus argenteus were associated with coral reef habitats only in autumn, winter and spring, and summer, respectively, and also showed seasonal differences in the habitat they were associated with at a large spatial scale. Few studies have considered seasonal variability in the habitat use of juvenile reef fishes although it has already been proven to be crucial when studying post-settlement stages of coral reef fishes (Robertson and Kaufmann, 1998; Bergenius et al., 2005). Possible explanations for these differences are that these species move between seasons, or that they have a better survival in habitats where resources are abundant and where predation is less intense. Indeed, seasonal variations in temperature and salinity in the New Caledonia Lagoon, which are amplified near-shore, are responsible for seasonal differences in the spatial distribution of detritic matter and benthic invertebrates (Ouillon et al., 2005) on which juvenile fishes can prey. Although seasonal habitat shifts in adult temperate scorpaenids result from such trophic relationships (Ebeling and Hixon, 1991), such habitat shifts have never been studied for reef fish juveniles. However, juveniles can rapidly acquire the ability of adults to forage in schools over long distances, and eventually move between habitats to feed on benthic micro-invertebrates (Mc Cormick and Makey, 1997). Our results showed that different species-specific patterns in the habitat use of reef fish juveniles occurred during the juvenile period, both at large and small spatial scales. These patterns were mainly based upon the habitat use of medium and large juveniles because few small juveniles were observed during fish censuses; small juveniles were thus little represented in co-inertia analyses. Underwater visual censuses offered a unique opportunity to consider juvenile habitat use at large spatial and temporal scales. However, this method was insufficient in detecting the smallest juveniles, stressing the need for further studies using other sampling techniques (e.g. seine nets or artificial moorings) or other methods of visual census more adapted to the size and home range of the smallest juvenile fish. Observed patterns in juvenile habitat use included: (1) an increase in the number of habitats used during the juvenile period (e.g. Lutjanus fulviflamma, Lethrinus atkinsoni); (2) a decrease in the number of habitats used (e.g. Amphiprion melanopus, Siganus fuscescens); (3) a drastic change in habitat (e.g. Scarus ghobban, Scarus sp.); and (4) no change in habitat (e.g. Lethrinus genivittatus, Ctenochaetus striatus). The latter pattern was the most frequently observed in the present study and confirmed that a majority of species used mid-shelf and

vegetated habitats during their entire juvenile period, as discussed previously. An increase or, to a lesser extent a decrease in the number of habitats used was also well represented within juvenile assemblages, although not found to be characteristic of any family. This result may reflect either differences in ecological requirements during ontogeny that induce a diversification (or a specialization) of habitat use (Dahlgren and Eggleston, 2000), or the consequences of differential survival and growth rates among habitats (Bergenius et al., 2005). Drastic changes of habitat use were detected for a few species only but are consistent with other studies. We showed that medium and large juveniles of Parupeneus multifasciatus were abundant in soft and vegetated habitats, and also that medium size juveniles were abundant in mid-shelf habitats while large juveniles occupied barrier reef habitats. These findings are consistent with the three distinct post-settlement shifts in habitat observed on the Great Barrier Reef for P. multifasciatus juveniles (Mc Cormick and Makey, 1997). Similarly, we observed that all juvenile size classes of L. atkinsoni were characteristic of seagrass or seaweed beds but we also detected a drastic habitat shift at large scales, where small juveniles were observed in barrier reef habitats, medium juveniles in mid-shelf habitats and large juveniles in coastal habitats. Between juvenile and adulthood, ontogenetic shifts in habitat use were observed at a small spatial scale for L. atkinsoni in the Ryukyu Islands (Japan) where juveniles were found mostly in seagrass beds while adults were observed on coral patches (Nakamura and Sano, 2004). Lastly, our results suggest that habitat shifts may occur concurrently at two spatial scales during the juvenile period. Co-inertia analyses showed marked changes in habitat use of Scarus ghobban and Scarus sp. between successive size classes that occurred both at large and small spatial scales. Numerous studies indicate habitat shifts of juveniles from sandy and vegetated areas to coral habitats as they grow (Appeldoorn et al., 1997; Ohman et al., 1998; Dahlgren and Eggleston, 2000; Cocheret de la Morinie`re et al., 2002; Gillanders et al., 2003). Our findings indicate the possibility of a simultaneous change of cross-shelf location for juveniles of several species. Considering the spatial scales at which habitat shifts occur during the juvenile phase may be crucial for the design and management of marine protected areas and particularly for conservation decisions regarding specific species. All these results finally underline that improving our knowledge about the ecology of juvenile reef fishes relies on the understanding of the degree to which their assemblages vary across space, what factors can account for such variations, and whether these factors are scale dependent (Chittaro, 2004; Habeeb et al., 2005). Acknowledgements This project was funded by ‘Institut de Recherche pour le De´veloppement’ (IRD) and by the French ‘Ministe`re de l’Outre-Mer’. We wish to thank Ge´rard Mou-Tham for invaluable field assistance. We are also very grateful to David Lecchini for helpful comments on the manuscript.

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