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

Estuarine, Coastal and Shelf Science 75 (2007) 481e491
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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 Nouméa Cedex, New Caledonia
Institut de Recherche pour le Developpement (IRD), UR 128, 52 Av. Paul Alduy, Université 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.,
C. Mellin et al. / Estuarine, Coastal and Shelf Science 75 (2007) 481e491
482
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.
C. Mellin et al. / Estuarine, Coastal and Shelf Science 75 (2007) 481e491
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 <Sm.
For each season, two spatial scales of habitat were considered. At a large spatial scale (1e10 km), we measured the
shortest distance to the barrier reef and the shortest distance
to the main island for each transect. There were slightly
more transects far from the coast in autumn (Table 2). After
each fish census we recorded the average depth (in m) and estimated the visibility (in m), defined here as the minimum distance to which a diver could accurately identify a 3 cm TL fish
and estimate its total length. Using a series of 10 5 m quadrates located on each side of the 100 m median line we visually estimated the percent cover of four benthic categories
including: hard substrate, mud or sand, living coral, and seaweeds or seagrasses. Values were averaged over 20 quadrates.
2.3. Statistical analysis
In order to reduce the effect of high abundance values, we
used log(X þ 1) transformations on abundance data of each
transect. Faunistic data were organized with abundances for
species-size class combinations in columns and the different
transects in rows. Habitat data were organized with habitat
variables at both small and large spatial scales in columns
and the different transects in rows. For each season we created
one faunistic and one habitat table.
We investigated the relationship between juvenile fish and
habitat with co-inertia analysis. Co-inertia analysis (CIA) is
a multivariate method for coupling faunistic and environmental tables and for measuring their adequacy (Dolédec and
Chessel, 1994; Dray et al., 2003). It is a general method that
is more flexible and thus often more relevant for ecological
studies than canonical correspondence analysis (CCA). CCA
aims to study the relationship between one set of variables
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 (Dolédec
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 (Dolédec 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.
C. Mellin et al. / Estuarine, Coastal and Shelf Science 75 (2007) 481e491
484
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 <Sm (large juveniles), and total abundances per species and per size class are given
Family
Species
Sm (mm)
Lutjanidae
Lutjanus fulviflamma (Forsskål, 1775)
Lutjanus gibbus (Forsskål, 1775)
Lutjanus kasmira (Forsskål, 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 (Forsskål, 1775)
nebulosus (Forsskål, 1775)
230
105
220
195
17
71
0
3
276
65
25
56
62
198
161
50
355
334
186
109
Mullidae
Mulloidichthys flavolineatus (Lacepède, 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 (Lacepède, 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 (Lacepède, 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 (Forsskål, 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 (Forsskål, 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 (Forsskål, 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
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-0.40
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21 Dec. - 20 Mar.
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-0.10
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21 Mar. - 20 June
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-0.20
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21 June - 20 Sep.
(winter)
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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
C. Mellin et al. / Estuarine, Coastal and Shelf Science 75 (2007) 481e491
487
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 Morinière
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 Morinière 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 Morinière 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
Développement’ (IRD) and by the French ‘Ministère de
l’Outre-Mer’. We wish to thank Gérard Mou-Tham for invaluable field assistance. We are also very grateful to David Lecchini for helpful comments on the manuscript.
C. Mellin et al. / Estuarine, Coastal and Shelf Science 75 (2007) 481e491
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