Importance of Mangroves, Seagrass Beds and the Shallow Coral Reef as a Nursery for Important Coral Reef Fishes, Using a Visual Census Technique (Nagelkerken et al, 2000)
Estuarine, Coastal and Shelf Science (2000) 51, 31–44
doi:10.1006/ecss.2000.0617, available online at http://www.idealibrary.com on
Importance of Mangroves, Seagrass Beds and the
Shallow Coral Reef as a Nursery for Important Coral
Reef Fishes, Using a Visual Census Technique
I. Nagelkerkena,b, G. van der Veldea,d, M. W. Gorissena, G. J. Meijera, T. van’t Hof c
and C. den Hartoga
a
Laboratory of Aquatic Ecology, Aquatic Animal Ecology, University of Nijmegen, Toernooiveld 1,
6525 ED Nijmegen, The Netherlands
b
Carmabi Foundation, P.O. Box 2090, Piscaderabaai z/n, Curacao, Netherlands Antilles
¸
c
Marine and Coastal Resource Management, The Bottom, Saba, Netherlands Antilles
Received 19 August 1999 and accepted in revised form 29 February 2000
The nursery function of various biotopes for coral reef fishes was investigated on Bonaire, Netherlands Antilles. Length
and abundance of 16 commercially important reef fish species were determined by means of visual censuses during the
day in six different biotopes: mangrove prop-roots (Rhizophora mangle) and seagrass beds (Thalassia testudinum) in Lac
Bay, and four depth zones on the coral reef (0 to 3 m, 3 to 5 m, 10 to 15 m and 15 to 20 m). The mangroves, seagrass
beds and shallow coral reef (0 to 3 m) appeared to be the main nursery biotopes for the juveniles of the selected species.
Mutual comparison between biotopes showed that the seagrass beds were the most important nursery biotope for juvenile
Haemulon flavolineatum, H. sciurus, Ocyurus chrysurus, Acanthurus chirurgus and Sparisoma viride, the mangroves for
juvenile Lutjanus apodus, L. griseus, Sphyraena barracuda and Chaetodon capistratus, and the shallow coral reef for juvenile
H. chrysargyreum, L. mahogoni, A. bahianus and Abudefduf saxatilis. Juvenile Acanthurus coeruleus utilized all six biotopes,
while juvenile H. carbonarium and Anisotremus surinamensis were not observed in any of the six biotopes. Although fishes
showed a clear preference for a specific nursery biotope, most fish species utilized multiple nursery biotopes
simultaneously. The almost complete absence of juveniles on the deeper reef zones indicates the high dependence of
juveniles on the shallow water biotopes as a nursery. For most fish species an (partial) ontogenetic shift was observed at
a particular life stage from their (shallow) nursery biotopes to the (deeper) coral reef. Cluster analyses showed that closely
related species within the families Haemulidae, Lutjanidae and Acanthuridae, and the different size classes within species
2000 Academic Press
in most cases had a spatial separation in biotope utilization.
Keywords: fish; nursery grounds; bays; mangrove swamps; sea grasses; reefs; ontogenetic shifts; Caribbean Sea
Introduction and seagrass beds. The hypotheses are based on
avoidance of predators, the abundance of food and
Many studies in various parts of the world have
the interception of fish larvae: (a) the structural
recognized the importance of mangroves and seagrass
complexity of these biotopes provide excellent
beds as habitats for fishes. Mangroves and seagrass
shelter against predators (Parrish, 1989; Robertson
beds have been shown to contain a high diversity and
& Blaber, 1992), (b) these biotopes are often located
abundance of estuarine and/or coral reef fishes in the
at a distance from the coral reef or from off-shore
Caribbean (e.g. Springer & McErlean, 1962; Austin,
waters and are therefore less frequented by predators
1971; Weinstein & Heck, 1979; Thayer et al., 1987;
(Shulman, 1985; Parrish, 1989), (c) the relatively
Baelde, 1990; Sedberry & Carter, 1993), in the Indian
turbid water of the bays and estuaries decrease the
Ocean (e.g. Little et al., 1988; van der Velde et al.,
foraging efficiency of predators (Blaber & Blaber,
1995; Pinto & Punchihewa, 1996), and in the Pacific
1980; Robertson & Blaber, 1992), (d) these biotopes
Ocean (e.g. Blaber, 1980; Bell et al., 1984; Robertson
provide a great abundance of food for fishes (Odum
& Duke, 1987; Blaber & Milton, 1990; Morton, 1990;
& Heald, 1972; Carr & Adams, 1973; Ogden &
Tzeng & Wang, 1992).
Zieman, 1977) and (e) these biotopes often cover
Several hypotheses have been proposed to explain
extensive areas and may intercept planktonic fish
the high abundance of (juvenile) fishes in mangroves
larvae more effectively than the coral reef (Parrish,
1989).
d
Corresponding author. E-mail: gerardv@sci.kun.nl
2000 Academic Press
0272–7714/00/070031+14 $35.00/0
32 I. Nagelkerken et al.
(a) (b)
b
II
a
Gotomeer I
c 0 1000 m
IV
a+b+c+d VII b IX
6 a
5d
0 5000 m 4 a+b+c
III
Klein Bonaire
Kralendijk
Sorobon
Lac
1 a+b VIII Cai
2 a+b
Dam
V
Pekelmeer VI
3 a + b+ d isles
mangroves
A. cervicornis
F 1. (a) Map of Bonaire showing the different coral reef study sites. a=20 to 25 m, b=10 to 15 m, c=3 to 5 m,
d=0 to 3 m. (b) Map of Lac Bay showing the different mangrove (II, IV, VI, VII, VIII, IX) and seagrass bed (I, III, V)
study sites. A. cervicornis=Acropora cervicornis.
Studies on fish community structure in Caribbean focused on either mangroves or seagrass beds, and
lagoons, bays and estuaries containing mangroves or usually with a different sampling method. This makes
seagrass beds often mention high densities of juvenile a comparison between studies and biotopes difficult.
fish and state that these biotopes function as nursery Only a few studies have sampled both biotopes simul-
areas for various coral reef fish species (e.g. Austin, taneously (Thayer et al., 1987; Sedberry & Carter,
1971; Weinstein & Heck, 1979; Baelde, 1990; 1993), and even fewer have included censuses on the
Sedberry & Carter, 1993). In the Indo-Pacific, adjacent or off-shore coral reef (e.g. van der Velde
however, the nursery function of these biotopes is et al., 1992). Hence, quantitative data describing the
apparent only in some regions (Blaber, 1980; Bell ecological links of fish faunas between mangroves,
et al., 1984; Little et al., 1988; Tzeng & Wang, 1992), seagrass beds and coral reefs are largely lacking
whereas in other regions these biotopes do not appear (Ogden & Gladfelter, 1983; Birkeland, 1985; Parrish,
to be important (Quinn & Kojis, 1985; Thollot & 1989).
Kulbicki, 1988; Blaber & Milton, 1990; Thollot, To provide a better insight into the importance of
1992). mangroves, seagrass beds and depth zones of the coral
Most studies describing the nursery function of reef as nursery biotopes and their interrelationship in
mangroves and seagrass beds were based on quali- fish fauna, size frequency data were collected for
tative observations, made no distinction between 16 commercially important reef fish species in each
abundances of juvenile and adult fishes, and did not biotope, using a visual census technique. The objec-
provide quantitative data on fish size. The few studies tives of the present study were to answer the following
which did provide size data for separate species only four questions: (1) Which biotopes are used as a
mentioned the full size range of all fish caught nursery by the selected fish species? (2) Which biotope
(Springer & McErlean, 1962; Austin, 1971). Hence, is preferred by a fish species in case multiple nursery
size-frequency data of juvenile and adult reef fish are biotopes are used? (3) Do fish species show an onto-
largely lacking for these biotopes. Furthermore, many genetic shift from their nursery biotopes to other
fish species show ontogenetic shifts in habitat utiliz- biotopes when reaching a larger size? (4) Do closely
ation and migrate from their nursery grounds to an related fish species show a spatial separation in
intermediate life stage habitat or to the coral reef biotope utilization?
(Ogden & Ehrlich, 1977; Weinstein & Heck, 1979;
McFarland, 1980; Rooker & Dennis, 1991). The size
range and the biotopes where these shifts occur have Materials and methods
also not been described accurately for many fish
Lac Bay is the largest bay of Bonaire with an area of
species.
approximately 8 km2 and is situated on the exposed
Studies referring to the nursery function of lagoons,
eastern side of the island [Figure 1(a)]. The bay
bays and estuaries in the Caribbean have mostly
Nursery function of mangroves, seagrass beds and the shallow coral reef 33
T 1. Depth, temperature and salinity of the seawater in snappers (Lutjanidae): yellowtail snapper Ocyurus
the six different biotopes chrysurus, mahogany snapper Lutjanus mahogoni,
schoolmaster L. apodus, and gray snapper L. griseus;
Depth (m) Temperature ( C) Salinity
three species of surgeonfishes (Acanthuridae): doctor-
fish Acanthurus chirurgus, ocean surgeon A. bahianus,
Seagrass bed 0·4–1·4 28·6–33·4 37–44 and blue tang A. coeruleus; one species of barracuda
Mangroves 0·3–1·2 28·5–34·0 39–44
(Sphyraenidae): great barracuda Sphyraena barracuda;
Coral reef 0–3 29·0–29·8 n.d.
one species of parrotfish (Scaridae): stoplight
Coral reef 3–5 27·1–29·3 n.d.
parrotfish Sparisoma viride; one species of damselfish
Coral reef 10–15 27·1–29·8 n.d.
Coral reef 20–25 26·8–29·5 n.d. (Pomacentridae): sergeant major Abudefduf saxatilis;
and one species of butterflyfish (Chaetodontidae):
n.d.=no data. foureye butterflyfish Chaetodon capistratus.
The selected fish species were studied using a
visual census technique in six different biotopes, viz.
mangrove prop-roots and seagrass beds, and the
consists of a shallow basin (0 to 3 m deep) and is
coral reef of 0 to 3 m, 3 to 5 m, 10 to 15 m and 15
protected from wave exposure by a shallow barrier of
to 20 m [Figure 1(a,b)]. Water clarity for visual
dead and living corals [Figure 1(b)]. The bay is
censuses was good in all six biotopes, even in the
connected to the sea by a narrow channel which is
mangroves. The visual census technique was based
about 8 m deep. The soft-bottom flora of the bay
on best estimation by eye of abundance and body
is dominated by the seagrass Thalassia testudinum and
length of the selected fish species in permanent belt
the calcareous alga Halimeda opuntia. Other common
transects in all six biotopes. Size classes of 5 cm were
vegetation consists of the seagrass Syringodium
used for the estimation of body length (TL). The
filiforme and the alga Avrainvillea nigricans. The bay
usage of smaller size classes was avoided to reduce
is bordered almost completely by the mangrove
differences in size class estimation between ob-
Rhizophora mangle. In front of the bay the coral
servers. For the large-sized Sphyraena barracuda size
reef is situated, which runs around the island. The
classes of 15 cm were used. Length estimation was
reef consists of a shallow reef terrace which sharply
practiced prior to the censuses on objects with
drops off at an angle of 45 to 60 at a depth of
known length lying on the sea bottom. In addition,
8 to 12 m.
the underwater slates for data recording were
The maximum tidal range on Bonaire is 30 cm (van
marked with a ruler for guidance in size estimation.
Moorsel & Meijer, 1993). The seagrass beds and
Visual census estimations of fish abundance were
mangrove prop-roots at the study sites were not
compared with catches at two seagrass sites using the
exposed at low tide and ranged in depth from 0·3 to
drop net quadrat method (Hellier, 1958). At sites
1·4 m (Table 1). The temperature, measured during
VIII and IX [see Figure 1(b)] a drop net of
the entire study period, ranged from 28·5 to 34·0 C
10 10 m was installed on the seagrass bed. During
in the bay, and was on average higher than on of the
the morning (09.00–10.00h) the net was lowered
coral reef where it ranged from 26·8 to 29·8 C. The
onto the sea bottom and all fishes within the net
salinity, measured at the beginning and at the end of
were caught, identified and counted. A total of seven
the study period, ranged from 37 to 44 in the seagrass
drop net catches were made at the two seagrass sites
beds and from 39 to 44 in the mangroves. The water
during August to December 1981. In addition, dif-
of the bay is quite clear and horizontal Secchi visibility
ferences in estimation of abundance was statistically
ranges from 4·6 to 21·6 m in the central parts of the
tested (t-test) between the two observers for each
bay (van Moorsel & Meijer, 1993).
species in each biotope (96 cases).
Sixteen reef fish species were selected in the present
Advantages of visual censuses are that they are
study. Species were selected which were abundant,
rapid, non-destructive, inexpensive, can be used for all
not too shy, easy to identify in the field and had a
selected biotopes of this study, the same areas can be
non-cryptic life style. Further selection was on
resurveyed through time, and the results can be com-
basis of their economic value (i.e. reef fisheries,
pared with many other studies (English et al., 1994).
aquarium fisheries, attraction for diving industry).
Disadvantages are the differences in accuracy in esti-
The 16 species consisted of five species of grunts
mation of numbers and sizes by the observers, and
(Haemulidae): French grunt Haemulon flavolineatum,
fishes may be attracted or scared off by the observers
bluestriped grunt H. sciurus, smallmouth grunt H.
(English et al., 1994; Cheal & Thompson, 1997;
chrysargyreum, Caesar grunt H. carbonarium, and
Thompson & Mapstone, 1997).
black margate Anisotremus surinamensis; four species of
34 I. Nagelkerken et al.
T 2. Mean density (1000 m 2) of the 16 fish species in the six different biotopes surveyed by visual census, and mean
density on the seagrass beds based on drop net catches
Seagrass bed
Coral reef Coral reef Coral reef Coral reef
drop net visual census Mangroves 0–3 m 3–5 m 10–15 m 20–25 m
Haemulon flavolineatum 782·5 115·3 59·9 52·4 37·4 12·4 2·9
H. sciurus 12·7 5·5 4·3 0·4 0·4 9·6 0·5
H. chrysargyreum 0·0 0·01 0·0 64·7 53·9 0·0 0·0
H. carbonarium 0·0 0·0 0·0 0·0 0·0 5·4 0·1
Anisotremus surinamensis 0·0 0·0 0·0 0·0 0·0 0·8 0·1
Ocyurus chrysurus 20·6 16·4 1·2 0·0 1·1 24·7 11·8
Lutjanus mahogoni 0·0 1·1 0·0 9·6 1·7 12·6 2·3
L. apodus 30·2 8·1 65·8 0·5 0·0 9·7 3·4
L. griseus 4·8 8·7 29·9 0·0 0·0 0·0 0·04
Acanthurus chirurgus 0·0 9·2 0·8 5·6 0·1 0·6 0·8
A. bahianus 27·0 3·3 0·2 86·6 19·3 5·6 4·4
A. coeruleus 0·0 1·1 2·6 10·2 21·8 7·7 4·5
Sphyraena barracuda 6·3 0·9 5·1 0·0 0·0 0·1 0·2
Sparisoma viride 60·3 26·1 1·4 11·1 34·6 11·4 6·3
Abudefduf saxatilis 0·0 0·2 3·9 65·2 0·3 16·8 0·1
Chaetodon capistratus 12·7 4·9 16·7 2·7 14·4 23·1 9·6
In each of the six biotopes, permanently marked between species without the data being affected by
belt transects were established. In the seagrass beds, differences in total fish densities.
a transect of 300 3 m was established at three
different sites. In the mangroves, nine transects were
Results
established of 3 m wide and 25 to 100 m long. On the
coral reef, six sites were selected and at each site,
Drop net catches vs visual census
transects of 3 100 m were established at two to four
depth zones [Figure 1(a)]. During May to November Catches with the drop net showed higher abundances
1981, visual censuses were done by two trained for some fish species than estimations with the
observers together in the morning (09.00–11.00h) and visual census technique (Table 2), especially for H.
in the afternoon (14.00–16.00h) by means of flavolineatum. On the other hand, visual estimations of
snorkelling or SCUBA diving. The census in each abundance of A. chirurgus were much higher than with
transect was repeated at monthly intervals. The the drop net quadrat method. For the visual censuses,
fish counts in transects at the different sites, of the only in 8 out of 61 cases a significant difference
morning and afternoon survey, and of all seven (P<0·05, t-test) was found in estimation of abundance
months were pooled and averaged per area. They are between the two observers (for 35 cases insufficient
expressed as the average fish density per 1000 m2 for data were available for statistical testing).
each size class of each species in each biotope.
Cluster analyses were carried out using the com-
Biotope utilization of Haemulidae
puter programme CLUSTAN1C2 (Wishart, 1978).
The average-linkage method (Sokal & Michener, Juveniles of Haemulidae were restricted to shallow
1958) was used in combination with the Bray-Curtis water biotopes (i.e. seagrass beds, mangroves and reef
coefficient. Separate analyses were carried out for of 0 to 3 m), whereas adults were found on the deeper
closely related species belonging to a single family reef (>3 m) (Figure 2, Table 3). An exception was
(Haemulidae, Lutjanidae, Acanthuridae) using log- formed by adult Haemulon chrysargyreum which were
transformed data of the densities in the different size also found on the reef of 0 to 3 m. Large juveniles of
classes and biotopes. Cluster analysis of all species H. sciurus utilized the mangroves as an intermediate
together was carried out on data in which densities life stage biotope, in their ontogenetic shift from the
per size class for each biotope were transformed to seagrass beds to the coral reef. Haemulon flavolineatum
percentages of total composition of a particular showed significant temporal differences in total
species. This was done to compare biotope utilization density in the seagrass beds (Friedman’s test,
Nursery function of mangroves, seagrass beds and the shallow coral reef 35
120 8
(a) Coral reef 20–25 m (b)
Summed mean density
Summed mean density
7
Coral reef 10–15 m
100
Coral reef 3–5 m 6
Coral reef 0–3 m
(1000 m–2)
(1000 m–2)
80
5
Seagrass bed
Mangroves
60 4
3
40
2
20
1
0 0
0–5 5–10 10–15 15–20 20–25 0–5 5–10 10–15 15–20 20–25 25–30 30–35
Size class (cm) Size class (cm)
60 4
(c) (d)
Summed mean density
Summed mean density
50
3
(1000 m–2)
(1000 m–2)
40
30 2
20
1
10
0 0
0–5 5–10 10–15 15–20 20–25 0–5 5–10 10–15 15–20 20–25 25–30 30–35
Size class (cm) Size class (cm)
0.5
(e)
Summed mean density
0.4
(1000 m–2)
0.3
0.2
0.1
0.0
0–5 5–10 10–15 15–20 20–25 25–30 30–35 35–40
Size class (cm)
F 2. Summed mean densities of Haemulidae in different biotopes. (a) Haemulon flavolineatum; (b) H. sciurus;
(c) H. chrysargyreum; (d) H. carbonarium; (e) Anisotremus surinamensis.
P<0·05), increasing from 25·4 per 1000 m2 in May to H. carbonarium and A. surinamensis showed some
178·9 per 1000 m2 in October. similarity in biotope utilization, but the former was
Cluster analysis of all size classes of all haemulids much more abundant than the latter (Figure 2).
also showed a spatial separation in biotope utilization Considering the entire species size range, H.
among the different size classes and/or species, with flavolineatum dominated over its related species in the
juveniles found in the mangroves and seagrass beds, seagrass beds, mangroves and reef of 20 to 25 m, but
medium-sized individuals on the reef and partly still in co-occurred with H. chrysargyreum on the reef of 0 to
the mangroves, and very large individuals on the deep 5 m [Figure 5(a), Table 2]. Haemulon sciurus and
reef (Figure 3). Haemulon chrysargyreum formed a H. carbonarium co-occurred with H. flavolineatum on
separate cluster since adults partly co-occurred with the reef of 10 to 15 m. Anisotremus surinamensis was
the juveniles in their nursery habitat. not dominant in any of the biotopes.
Species of Haemulidae showed a spatial separation
in biotope utilization and occurred in different biotope
Biotope utilization of Lutjanidae
clusters as calculated by cluster analysis (Figure 4).
Furthermore, the Haemulidae were not found Juveniles of Lutjanidae were restricted to the shallow
together in a single cluster with any species belonging water biotopes (Figure 6, Table 3). Only juveniles of
to the same feeding guild (Figure 4, Table 3). Only L. mahogoni were also partly found deeper on the reef
36 I. Nagelkerken et al.
T 3. Importance (+) of the six different biotopes for juveniles and adults of the different fish species. *Indicates most important biotope for juveniles. Maturation
size refers to that of the smallest individuals and not to the species average. Maturation data are from De Sylva (1963), Starck and Schroeder (1971); Munro (1983).
Ontogenetic migration indicates the migration of juveniles to the (deeper) coral reef when reaching adult sizes; +/ = partial ontogenetic migration (i.e. part of the
fish population). Feeding guilds: BI=benthic invertebrate feeder, PI=planktonic invertebrate feeder, P=piscivore, H=herbivore, O=omnivore. Ontogenetic shifts in
feeding guild are indicated as that of juveniles/adults
Juveniles Adults
Maturation
Feeding size Seagrass Reef Reef Reef Reef Seagrass Reef Reef Reef Reef Ontogenetic
guild (cm) bed Mangroves 0–3 m 3–5 m 10–15 m 20–25 m bed Mangroves 0–3 m 3–5 m 10–15 m 20–25 m migration
Haemulon flavolineatum BI >10 +* + + + + +
H. sciurus BI >15 +* + + +
H. chrysargyreum BI >15 +* + + +/
H. carbonarium BI >15 + ?
Anisotremus surinamensis BI >20 + ?
Ocyurus chrysurus PI >25 +* + + +
Lutjanus mahogoni BI/P >20 + +* + + + +
L. apodus BI/P >25 + +* + + + +
L. griseus BI/P >15 + +* +
Acanthurus chirurgus H >15 +* + + + + +/
A. bahianus H >10 + +* + + +/
A. coeruleus H >10 + + + + + + + + +/
Sphyraena barracuda P >45 + +* + + + + +/
Sparisoma viride H >15 +* + + + + + +/
Abudefduf saxatilis O >10 +* + + +/
Chaetodon capistratus H/BI >5 + +* + + + + +
Nursery function of mangroves, seagrass beds and the shallow coral reef 37
0.9
0.8
0.7
0.6
Dissimilarity
0.5
0.4
0.3
0.2
0.1
0.0
A. su. 25–30
H. ca. 25–30
A. su. 30–35
A. su. 35–40
H. ca. 30–35
H. sc. 5–10
H. fl. 20–25
H. ca. 20–25
H. fl. 0–5
H. sc. 10–15
H. fl. 15–20
H. sc. 25–30
H. sc. 0–5
H. sc. 30–35
H. ca. 15–20
H. ch. 15–20
A. su. 20–25
H. sc. 15–20
H. fl. 5–10
H. fl. 10–15
H. sc. 20–25
H. ch. 10–15
H. ch.20–25
H. ch. 5–10
H. ch. 0–5
Seagrass and mangrove Coral reef and mangrove Shallow reef Seagrass Deep reef
F 3. Cluster analysis of all size classes of Haemulidae in different biotopes. H. fl.=Haemulon flavolineatum,
H. sc.=H. sciurus, H. ch.=H. chrysargyreum, H. ca.=H. carbonarium, A. su.=Anisotremus surinamensis. The numbers indicate
the size classes.
0.9
0.8
0.7
0.6
Dissimilarity
0.5
0.4
0.3
0.2
0.1
0.0
H. carbonarium
H. flavolineatum
A. chirurgus
H. chrysargyreum
A. surinamensis
A. bahianus
A. coeruleus
C. capistratus
S. viride
A. saxatilis
H. sciurus
O. chrysurus
L. mahogoni
L. griseus
L. apodus
1 2 3 4 5 6 7 8 9
F 4. Cluster analysis of all 16 fish species based on the abundance of each size class in the different biotopes.
in the seagrass beds from 0·9 per 1000 m2 in May
of 3 to 5 m. All species, except L. griseus, showed an
to 17·2 per 1000 m2 in October. Ocyurus chrysurus
ontogenetic shift to the (deeper) coral reef. Lutjanus
apodus and L. griseus also occurred as adults in the increased in density in the seagrass beds from 4·4 per
1000 m2 in June to 41·4 per 1000 m2 in November.
mangroves. Lutjanus apodus showed significant tem-
poral differences in total density (Friedman’s test, Cluster analysis of all size classes of all lutjanids also
P<0·05), increasing in the mangroves from 57·7 per revealed a clear separation between adults and large
1000 m2 in May to 92·3 per 1000 m2 in August, and individuals (except L. griseus) on the deep reef (10 to
38 I. Nagelkerken et al.
25 m), and juveniles in the shallow water biotopes
(a)
(Figure 7).
100%
Species of Lutjanidae showed a spatial separation in
biotope utilization, except L. griseus and L. apodus
80%
which showed some degree of similarity in biotope
utilization and also belonged to the same feeding guild
60%
(Figure 4, Table 3). Considering the entire species
size range, L. apodus dominated over its related
40%
species in the mangroves, while for L. mahogoni
and O. chrysurus this was the case on the reef of 0
20%
to 3 m and on the reef of 20 to 25 m, respectively
0% [Figure 5(b), Table 2]. In the other three biotopes,
H. flavolineatum H. sciurus
lutjanids co-occurred without a single species showing
H. chrysargyreum H. carbonarium
an overall dominance.
A. surinamensis
(b)
100%
Biotope utilization of Acanthuridae
Juveniles of Acanthuridae were restricted to the
80%
shallow water biotopes, whereas adults were found on
Composition
60% the reef (Figure 8, Table 3). Adults were also found in
the juvenile nursery habitat (i.e. reef of 0 to 3 m),
40%
however, co-occurring with the juveniles. For larger
juveniles of A. coeruleus the reef of 3 to 5 m was also of
20%
importance. Acanthurus bahianus showed significant
temporal differences in total density (Friedman’s
0%
test, P<0·05), with peak abundances in the seagrass
O. chrysurus L. mahogoni
beds of around 5 per 1000 m2 in July, October, and
L. griseus L. apodus
November. Acanthurus coeruleus increased in density
(c)
on the reef of 3 to 5 m from 5·4 per 1000 m2 in May
100%
to 47·1 per 1000 m2 in September.
Cluster analysis of all size classes of all acanthurids
80%
also showed a separation between juveniles in the
seagrass beds and mangroves, and medium-sized and
60%
larger individuals on the reef (Figure 9).
Species of Acanthuridae showed a spatial separation
40%
in biotope utilization and occurred in different biotope
clusters (Figure 4). Of the Acanthuridae, only A.
20%
coeruleus was found with another herbivore species
0% (S. viride) in a single cluster, although the dissimilarity
s
es
m
m
m
m
ds
in biotope utilization between the two species was still
be gra
ov
–3
–5
15
25
gr
f0
f3
0–
0–
a
high (Figure 4, Table 3). Considering the entire
an
Se
f1
f2
ee
ee
M
R
R
ee
ee
species size range, each species dominated over its
R
R
related species in a particular biotope: A. chirurgus in
A. bahianus A. coeruleus
the seagrass beds, A. coeruleus in the mangroves, and
A. chirurgus
A. bahianus on the coral reef of 0 to 3 m [Figure 5(c),
F 5. Biotope partitioning between closely related
Table 2). In the other reef zones, A. coeruleus and
species: (a) Haemulidae, (b) Lutjanidae, (c) Acanthuridae.
A. bahianus co-occurred in almost equal densities.
The abundance of each species is expressed as the percent-
age composition of the total abundance of all related species
within a single family for each biotope. The entire size range
Biotope utilization of other species
of a species is pooled per biotope, although preferences may
differ among size classes. For the specific differences among
For the remaining four species, juveniles were also
size classes see Figures 2, 6 and 8.
restricted to the shallow water biotopes, whereas
adults occurred on the coral reef (Figures 10–13,
Table 3). Exceptions were adult S. barracuda which
Nursery function of mangroves, seagrass beds and the shallow coral reef 39
20 7
Mangroves Seagrass bed
(a) (b)
Summed mean density
Summed mean density
6
Coral reef 0–3 m Coral reef 3–5 m
Coral reef 10–15 m Coral reef 20–25 m
15 5
(1000 m–2)
(1000 m–2)
4
10
3
2
5
1
0 0
0–5 5–10 10–15 15–20 20–25 25–30 30–35 35–40 0–5 5–10 10–15 15–20 20–25 25–30 30–35
Size class (cm) Size class (cm)
25 14
(c) (d)
Summed mean density
Summed mean density
12
20
10
(1000 m–2)
(1000 m–2)
15 8
6
10
4
5
2
0 0
0–5 5–10 10–15 15–20 20–25 25–30 30–35 35–40 40–45 0–5 5–10 10–15 15–20 20–25 25–30 30–35 35–40 40–45 45–50
Size class (cm) Size class (cm)
F 6. Summed mean densities of Lutjanidae in different biotopes. (a) Ocyurus chrysurus; (b) Lutjanus mahogoni;
(c) L. apodus; (d) L. griseus.
0.9
0.8
0.7
Dissimilarity
0.6
0.5
0.4
0.3
0.2
0.1
0.0
O. ch. 10–15
L. gr. 0–5
L. gr. 35–40
L. gr. 30–35
L.gr. 5–10
L.gr. 10–15
L. gr. 15–20
L. ap. 5–10
L. ap. 10–15
L. gr. 20–25
L. gr. 25–30
L. ap . 0–5
L. ap. 15–20
L. ap. 20–25
O. ch. 0–5
O. ch. 5–10
L. gr. 40–45
L. gr. 45–50
L. ma. 0–5
L. ma. 5–10
L. ma. 10–15
L. ap. 25–30
L. ap. 30–35
O. ch. 15–20
L. ap. 35–40
O. ch. 35–40
L. ma. 20–25
L. ma. 25–30
O. ch. 30–35
O. ch. 20–25
O. ch. 25–30
L. ma. 15–20
L. ap. 40–45
L. ma. 30–35
f1 3m
ss
e
5d
m
m
ss
e
m
ov
ov
–1 an
ra
ra
m
–5
25
25
gr
gr
–
ag
ag
10 ve
R d0
f0
0–
0–
an
an
se
Se
ef ro
f1
ee
M
an
M
re ang
d
R
ee
ee
an
25
R
M
0–
e
ov
f1
gr
ee
an
R
M
Bay and shallow reef Deep reef
F 7. Cluster analysis of all size classes of Lutjanidae in different biotopes. L. gr.=Lutjanus griseus, L. ap.=L. apodus,
L. ma.=L. mahogoni, O. ch.=Ocyurus chrysurus. The numbers indicate the size classes.
also used the seagrass beds and mangroves as a life A. saxatilis co-occurred with the juveniles on the
stage biotope, and juvenile S. viride which also used shallow reef. Sphyraena barracuda showed significant
the reef of 3 to 5 m as a nursery biotope. Some adult temporal differences in total density (Friedman’s test,
40 I. Nagelkerken et al.
10 50
Coral reef 20–25 m
(a) (b)
Summed mean density
Summed mean density
Coral reef 10–15 m
8 40
Coral reef 3–5 m
Coral reef 0–3 m
(1000 m–2)
(1000 m–2)
Seagrass bed
6 30
Mangroves
4 20
2 10
0 0
0–5 5–10 10–15 15–20 20–25 25–30 0–5 5–10 10–15 15–20 20–25 25–30
Size class (cm) Size class (cm)
20
(c)
Summed mean density
16
(1000 m–2)
12
8
4
0
0–5 5–10 10–15 15–20 20–25
Size class (cm)
F 8. Summed mean densities of Acanthuridae in different biotopes. (a) Acanthurus chirurgus; (b) A. bahianus;
(c) A. coeruleus.
1.0
0.9
0.8
0.7
Dissimilarity
0.6
0.5
0.4
0.3
0.2
0.1
0.0
A. ba. 15–20
A. ba 10–15
A. ba 0–5
A. ch. 15–20
A. co. 15–20
A. ba. 5–10
A. ch. 5–10
A. co. 10–15
A. ba. 25–30
A. ch. 0–5
A. co. 20–25
A. ch. 20–25
A. ch. 25–30
A. ba. 20–25
A. ch. 10–15
A. co. 0–5
A. co. 5–10
Seagrass and reef Reef 0–25 m Reef and bay Reef
0–3 m 0–25 m
F 9. Cluster analysis of all size classes of Acanthuridae in different biotopes. A. ba.=Acanthurus bahianus,
A. ch.=A. chirurgus, A. co.=A. coeruleus. The numbers indicate the size classes.
beds from 12·7 per 1000 m2 in June to 43·1 per
P<0·05), with densities in the mangroves about two
1000 m2 in November, and C. capistratus from 2·0 per
times higher in August–November than in May–July.
1000 m2 in May to 8·0 per 1000 m2 in November.
Sparisoma viride increased in density in the seagrass
Nursery function of mangroves, seagrass beds and the shallow coral reef 41
3 Coral reef 20–25 m
Coral reef 20–25 m
Coral reef 10–15 m
Summed mean density
Coral reef 10–15 m
Coral reef 3–5 m
Coral reef 3–5 m
Coral reef 0–3 m
Summed mean density
Coral reef 0–3 m
(1000 m–2)
2 Seagrass bed
60
Seagrass bed
Mangroves
Mangroves
(1000 m–2)
50
1 40
30
0 20
0–15
15–30
30–45
45–60
60–75
75–90
90–105
105–120
120–135
135–150
150–165
165–180
180–195
195–210
10
0
Size class (cm) 0–5 5–10 10–15
Size class (cm)
F 10. Summed mean densities of Sphyraena barracuda
in different biotopes. F 13. Summed mean densities of Chaetodon
capistratus in different biotopes.
30
Coral reef 20–25 m of fish abundance. This variation is assumed to be
Coral reef 10–15 m
Summed mean density
25 comparable for the different biotopes, making a com-
Coral reef 3–5 m
Coral reef 0–3 m parison among the biotopes possible. Differences in
20
(1000 m–2)
Seagrass bed
estimation of abundance between observers were
Mangroves
15 present, but not consistent. Although density esti-
mations in seagrass beds are more accurate with
10
the drop net quadrat method, the total surface area
sampled (100 m2) was much smaller than with the
5
visual censuses (900 m2), resulting in large variations
0
0–5 5–10 10–15 15–20 20–25 25–30 30–35 35–40 among the transects and a restricted sampling of the
Size class (cm) biotope studied.
The present study shows the importance of
F 11. Summed mean densities of Sparisoma viride in
different biotopes. different shallow water biotopes as a nursery for
economically important reef fish species. All 14
species for which juveniles were observed used either
60
the mangroves, seagrass beds or the shallow reef of
Coral reef 20–25 m
Summed mean density
Coral reef 10–15 m
50 0 to 3 m, or a combination of these biotopes, as a
Coral reef 3–5 m
nursery. The high dependence of juveniles on
Coral reef 0–3 m
(1000 m–2)
40
Seagrass bed these biotopes can be deduced from the fact that
Mangroves
30
juveniles were exclusively present or highly dominant
in these biotopes and not on the deeper reef (i.e.
20
>3 m).
10
The data show that not only mangroves and
0 seagrass beds are important nursery biotopes for
0–5 5–10 10–15 15–20 20–25
juvenile fishes (e.g. Austin, 1971; Weinstein & Heck,
Size class (cm)
1979; Baelde, 1990; Sedberry & Carter, 1993)
F 12. Summed mean densities of Abudefduf saxatilis in
but also the shallow coral reef. Two reasons why
different biotopes.
mangroves and seagrass beds may contain high
densities of juvenile fish is their structural complexity
Discussion which provides a hiding place against predators (Bell
& Westoby, 1986; Robertson & Blaber, 1992), and
For several fish species in the seagrass beds the visual
because they are often located at a distance from
census technique showed lower densities than the
the coral reef and are therefore less frequented by
catches with the drop net quadrat method. Especially
predators (Shulman, 1985; Parrish, 1989). These two
H. flavolineatum was underestimated in the visual
factors also apply to the shallow coral reef of Bonaire,
censuses. The formation of large schools in this and
which mostly consists of living and dead colonies of
other species and the continuous movement of the
Acropora palmata, Millepora complanata and other
fishes caused a reduced accuracy in the estimation
42 I. Nagelkerken et al.
corals. The dead and living corals provide an ideal mangroves. For some species, the ontogenetic shift to
hiding space and can house relatively high densities of the (deeper) coral reef was partial and a part of the
(juvenile) fish (Nagelkerken, 1974). Furthermore, the large and adult fish could still be found in their nursery
shallow reef is separated from the main coral reef and biotope.
its predators by a shallow reef terrace of about 75 to The present study shows the importance of Lac Bay
125 m in width (van Duyl, 1985). Shulman (1985) for a number of reef fish species. It is not known,
showed that at just 20 m from the main reef, in however, how much Lac Bay contributes to the reef
an exposed sandy location, predation on juvenile fish stocks of Bonaire. Effective areas of all biotopes
haemulids was considerably lower than at the edge of should therefore be measured and the turnover rate
the main reef. of fishes from the bay to the reef be quantified.
Biotope utilization appears to be very specific for Furthermore, it should be noted that Lac Bay is not
the different species and their size classes, each having comparable to many other mangrove and seagrass
a different niche. A clear spatial separation in biotope habitats, particularly in the Indo-Pacific. These
utilization was found among closely related species habitats often have a muddy substratum, are very
and among different size groups within species, sug- turbid, and show fluctuating salinities and a greater
gesting avoidance of competition. Biotope partitioning tidal range. These features influence the nursery
was observed for only a small size range of mostly one function of mangroves and seagrass beds (Blaber,
or two related species. Likewise, fish species belong- 1997). As the characteristics which are usually associ-
ing to the same feeding guild showed differences in ated with these habitats are reduced in Lac Bay, the
biotope utilization. Spatial variation across different mechanisms at work responsible for the nursery
biotopes often occurs among sympatric fish species function of this bay may differ from those in several
(Lewis & Wainwright, 1985; McAfee & Morgan, other bays, lagoons and estuaries which have been
1996). Comparable to the present study, Lewis and studied so far.
Wainwright (1985) found a differential biotope
utilization for the three species of Acanthuridae and
Conclusions
suggested this to be determined by complex inter-
actions of several factors, such as density of com- The questions asked in this study can be answered as
petitors, food availability, proximity to shelter, and follows. (1) Of all 14 fish species for which juveniles
predator abundance. Munro (1983) stated that inter- were observed, the mangroves, seagrass beds, shallow
specific competition for food is probably small for reef of 0 to 3 m, or a combination of these biotopes
Haemulidae since the different species each favour a were used as a nursery by the juveniles. (2) The
certain type of food (Randall, 1967). Nagelkerken seagrass beds were the most important nursery biotope
et al. (2000), however, found H. flavolineatum and H. for juvenile Haemulon flavolineatum, H. sciurus,
sciurus to have similar diets on seagrass beds, which Ocyurus chrysurus, Acanthurus chirurgus and Sparisoma
may explain the separation in biotope utilization of the viride, the mangroves were the most important biotope
different size classes. Lutjanidae show a high overlap for juvenile Lutjanus apodus, L. griseus, Sphyraena
in diet, with exception of Ocyurus chrysurus (Randall, barracuda and Chaetodon capistratus, the shallow coral
1967; Nagelkerken et al., 2000). As biotope utiliz- reef was the most important biotope for juvenile H.
ation differed only slightly between Lutjanus mahogoni chrysargyreum, L. mahogoni, A. bahianus and Abudefduf
and L. griseus, which both occurred in similar saxatilis, Acanthurus coeruleus did not show a prefer-
densities, a high degree of competition may be present ence for a particular nursery habitat, and for H.
between these two species. carbonarium and Anisotremus surinamensis it could not
When fishes become too large for optimal protection be established which biotope was used as a nursery by
by the seagrass shoots and mangrove prop-roots they the juveniles. (3) For most fish species, the juveniles
often migrate to the coral reef. This migration pattern were found in shallow-water biotopes and the large
has largely been described qualitatively for only few and adult fish on the (deeper) coral reef. (4) Closely
species (e.g. Ogden & Ehrlich, 1977; Weinstein & related species showed a spatial separation in biotope
Heck, 1979; McFarland, 1980; Rooker & Dennis, utilization. This was also observed for different size
1991). The present study shows that most of the classes within species.
selected species use the shallow water biotopes as nurs-
eries during their juvenile stage, but migrate perma-
Acknowledgements
nently to the (deeper) coral reef when reaching a
specific size class. An exception was Lutjanus griseus This study was funded by grants to MWG and
of which the entire size range was found in the GJM from the Stichting Werkgroep Studiereizen
Nursery function of mangroves, seagrass beds and the shallow coral reef 43
McAfee, S. T. & Morgan, S. G. 1996 Resource use by five
Ontwikkelingslanden, the Beijerinck-Popping Fonds,
sympatric parrotfishes in the San Blas Archipelago, Panama.
and the Natuurwetenschappelijke Studiekring voor Marine Biology 125, 427–437.
Suriname en de Nederlandse Antillen. We would McFarland, W. N. 1980 Observations on recruitment in haemulid
fishes. Proceedings of the Gulf and Caribbean Fisheries Institute 32,
like to thank E. Newton of Stinapa Bonaire (Bonaire)
132–138.
and the staff of the Carmabi Foundation (Curacao)
¸ Morton, R. M. 1990 Community structure, density and standing
for their co-operation. We furthermore thank crop of fishes in a subtropical Australian mangrove area. Marine
Biology 105, 385–394.
Dr M. de Kluijver for doing the CLUSTAN analyses
Munro, J. L. 1983 Caribbean coral reef fishery resources. ICLARM
and Dr S. Rajagopal for his comments on the studies and reviews 7.
manuscript. Nagelkerken, W. P. 1974 On the occurrence of fishes in relation to
corals in Curacao. Studies on the Fauna of Curacao and other
¸ ¸
Caribbean Islands 45, 118–141.
Nagelkerken, I., Dorenbosch, M., Verberk, W. C. E. P., Cocheret
de la Moriniere, E. & van der Velde, G. 2000 Day-night shifts
`
References
of fishes between shallow-water biotopes of a Caribbean bay,
with emphasis on the nocturnal feeding of Haemulidae and
Austin, H. M. 1971 A survey of the ichtyofauna of the mangroves of
Lutjanidae. Marine Ecology Progress Series 194, 55–64.
western Puerto Rico during December, 1967–August, 1968.
Odum, W. E. & Heald, E. J. 1972 Trophic analyses of an estuarine
Caribbean Journal of Science 11, 27–39.
mangrove community. Bulletin of Marine Science 22, 671–738.
Baelde, P. 1990 Differences in the structures of fish assemblages in
Ogden, J. C. & Ehrlich, P. R. 1977 The behavior of heterotypic
Thalassia testudinum beds in Guadeloupe, French West Indies,
resting schools of juvenile grunts (Pomadasyidae). Marine Biology
and their ecological significance. Marine Biology 105, 163–173.
42, 273–280.
Bell, J. D. & Westoby, M. 1986 Abundance of macrofauna in dense
Ogden, J. C. & Gladfelter, E. H. (eds) 1983 Coral reefs, seagrass
seagrass is due to habitat preference, not predation. Oecologia 68,
beds, and mangroves: their interaction in the coastal zones of the
205–209.
Caribbean. UNESCO Reports in Marine Science 23, 133 pp.
Bell, J. D., Pollard, D. A., Burchmore, J. J., Pease, B. C. &
Ogden, J. C. & Zieman, J. C. 1977 Ecological aspects of coral
Middleton, M. J. 1984 Structure of a fish community in a
reef-seagrass bed contacts in the Caribbean. Proceedings of the
temperate tidal mangrove creek in Botany Bay, New South
Third International Coral Reef Symposium 1, 377–382.
Wales. Australian Journal of Marine and Freshwater Research 35,
Parrish, J. D. 1989 Fish communities of interacting shallow-water
33–46.
habitats in tropical oceanic regions. Marine Ecology Progress Series
Birkeland, C. 1985 Ecological interactions between mangroves,
58, 143–160.
seagrass beds, and coral reefs. In Ecological Interactions Between
Pinto, L. & Punchihewa, N. N. 1996 Utilisation of mangroves and
Tropical Coastal Ecosystems (Birkeland, C. & Grosenbaugh, D.,
seagrasses by fishes in the Negombo Estuary, Sri Lanka. Marine
eds). UNEP Regional Seas Reports and Studies No. 73, 1–26.
Biology 126, 333–345.
Blaber, S. J. M. 1980 Fish of the Trinity inlet system of north
Quinn, N. J. & Kojis, B. J. 1985 Does the presence of coral reefs
Queensland with notes on the ecology of fish faunas of tropical
in proximity to a tropical estuary affect the estuarine fish
Indo-Pacific estuaries. Australian Journal of Marine and Freshwater
assemblage? Proceedings of the Fifth International Coral Reef
Research 31, 137–146.
Congress 5, 445–450.
Blaber, S. J. M. 1997 Fish and Fisheries of Tropical Estuaries.
Randall, J. E. 1967 Food habits of reef fishes in the West Indies.
Chapman and Hall, London.
Studies in Tropical Oceanography 5, 665–847.
Blaber, S. J. M. & Blaber, T. G. 1980 Factors affecting the Robertson, A. I. & Blaber, S. J. M. 1992 Plankton, epibenthos and
distribution of juvenile estuarine and inshore fish. Journal of Fish fish communities. In Tropical Mangrove Ecosystems (Robertson,
Biology 17, 143–162. A. I. & Alongi, D. M., eds). Coastal and Estuarine Studies
Blaber, S. J. M. & Milton, D. A. 1990 Species composition, No. 41, 173–224.
community structure and zoogeography of fishes of mangrove Robertson, A. I. & Duke, N. C. 1987 Mangroves as nursery sites:
estuaries in the Solomon Islands. Marine Biology 105, 259–267. comparisons of the abundance and species composition of fish
Carr, W. E. S. & Adams, C. A. 1973 Food habits of juvenile marine and crustaceans in mangroves and other nearshore habitats in
fishes occupying seagrass beds in the estuarine zone near Crystal tropical Australia. Marine Biology 96, 193–205.
River, Florida. Transactions of the American Fisheries Society 102, Rooker, J. R. & Dennis, G. D. 1991 Diel, lunar and seasonal
511–540. changes in a mangrove fish assemblage off southwestern Puerto
Cheal, A. J. & Thompson, A. A. 1997 Comparing visual counts Rico. Bulletin of Marine Science 49, 684–698.
of coral reef fish: implications of transect width and species Sedberry, G. R. & Carter, J. 1993 The fish community of a shallow
selection. Marine Ecology Progress Series 158, 241–248. tropical lagoon in Belize, Central America. Estuaries 16, 198–215.
De Sylva, D. P. 1963 Systematics and life-history of the great Shulman, M. J. 1985 Recruitment of coral reef fishes: effects of
barracuda Sphyraena barracuda (Walbaum). Studies in Tropical distribution of predators and shelter. Ecology 66, 1056–1066.
Oceanography 1, 179. Sokal, R. R. & Michener, C. D. 1958 A statistical method for
English, S., Wilkinson, C. & Baker, V. (eds) 1994 Survey Manual evaluating systematic relationships. Kansas University Science
for Tropical Marine Resources. ASEAN-Australia Marine Bulletin 38, 1409–1438.
Science Project: Living Coastal Resources. Australian Institute Springer, V. G. & McErlean, A. J. 1962 Seasonality of fishes on a
of Marine Science, Townsville, pp. 68–80. south Florida shore. Bulletin of Marine Science of the Gulf and
Hellier, T. R. 1958 The drop-net quadrat, a new population Caribbean 12, 39–60.
sampling device. Publications of the Institute for Marine Science of Starck, W. A. & Schroeder, R. E. 1971 Investigations on the gray
the University of Texas 5, 165–168. snapper, Lutjanus griseus. Studies in Tropical Oceanography 10.
Lewis, S. M. & Wainwright, P. C. 1985 Herbivore abundance Thayer, G. W., Colby, D. R. & Hettler, W. F. 1987 Utilization of
and grazing intensity on a Caribbean coral reef. Journal of the red mangrove prop root habitat by fishes in south Florida.
Experimental Marine Biology and Ecology 87, 215–228. Marine Ecology Progress Series 35, 25–38.
Little, M. C., Reay, P. J. & Grove, S. J. 1988 The fish community Thollot, P. 1992 Importance of mangroves for Pacific reef fish
of an East African mangrove creek. Journal of Fish Biology 32, species, myth or reality? Proceedings of the Seventh International
729–747. Coral Reef Symposium 2, 934–941.
44 I. Nagelkerken et al.
Thollot, P. & Kulbicki, M. 1988 Overlap between the fish fauna Kenya (Indian Ocean): a study with nets and stable isotopes. In
inventories of coral reefs, soft bottoms and mangroves in Monsoons and Coastal Ecosystems in Kenya (Heip, C. H. R.,
Saint-Vincent Bay (New Caledonia). Proceedings of the Sixth Hemminga, M. A. & de Bie, M. J. M., eds). Netherlands Indian
International Coral Reef Symposium 2, 613–618. Ocean Programme Cruise Reports No. 5, 39–50.
Thompson, A. A. & Mapstone, B. D. 1997 Observer effects and van Duyl, F. C. 1985 Atlas of the living reefs of Curacao and Bonaire
¸
training in underwater visual surveys of reef fishes. Marine Ecology (Netherlands Antilles). Foundation for scientific research in
Progress Series 154, 53–63. Surinam and the Netherlands Antilles, no. 117, Utrecht,
Tzeng, W.-N. & Wang, Y.-T. 1992 Structure, composition and The Netherlands.
seasonal dynamics of the larval and juvenile fish community in van Moorsel, G. W. N. M. & Meijer, A. J. M. 1993 Base-line
the mangrove estuary of Tanshui River, Taiwan. Marine Biology Ecological Study van het Lac op Bonaire. Bureau Waardenburg bv,
113, 481–490. Culemborg, The Netherlands.
van der Velde, G., Gorissen, M. W., den Hartog, C., van’t Hof, T. Weinstein, M. P. & Heck, K. L. 1979 Ichtyofauna of seagrass
& Meijer, G. J. 1992 Importance of the Lac-lagoon (Bonaire, meadows along the Caribbean coast of Panama and in the gulf of
´
Netherlands Antilles) for a selected number of reef fish species. Mexico: composition, structure and community ecology. Marine
Hydrobiologia 247, 139–140. Biology 50, 97–107.
van der Velde, G., van Avesaath, P. H., Ntiba, M. J., Mwatha, Wishart, D. 1978 CLUSTAN User Manual. Programme Library
G. K., Marguillier, S. & Woitchik, A.-F. 1995 Fish fauna of Unit, Edinburgh University, Edinburgh.
mangrove creeks, seagrass meadows and sand flats in Gazi Bay,
doi:10.1006/ecss.2000.0617, available online at http://www.idealibrary.com on
Importance of Mangroves, Seagrass Beds and the
Shallow Coral Reef as a Nursery for Important Coral
Reef Fishes, Using a Visual Census Technique
I. Nagelkerkena,b, G. van der Veldea,d, M. W. Gorissena, G. J. Meijera, T. van’t Hof c
and C. den Hartoga
a
Laboratory of Aquatic Ecology, Aquatic Animal Ecology, University of Nijmegen, Toernooiveld 1,
6525 ED Nijmegen, The Netherlands
b
Carmabi Foundation, P.O. Box 2090, Piscaderabaai z/n, Curacao, Netherlands Antilles
¸
c
Marine and Coastal Resource Management, The Bottom, Saba, Netherlands Antilles
Received 19 August 1999 and accepted in revised form 29 February 2000
The nursery function of various biotopes for coral reef fishes was investigated on Bonaire, Netherlands Antilles. Length
and abundance of 16 commercially important reef fish species were determined by means of visual censuses during the
day in six different biotopes: mangrove prop-roots (Rhizophora mangle) and seagrass beds (Thalassia testudinum) in Lac
Bay, and four depth zones on the coral reef (0 to 3 m, 3 to 5 m, 10 to 15 m and 15 to 20 m). The mangroves, seagrass
beds and shallow coral reef (0 to 3 m) appeared to be the main nursery biotopes for the juveniles of the selected species.
Mutual comparison between biotopes showed that the seagrass beds were the most important nursery biotope for juvenile
Haemulon flavolineatum, H. sciurus, Ocyurus chrysurus, Acanthurus chirurgus and Sparisoma viride, the mangroves for
juvenile Lutjanus apodus, L. griseus, Sphyraena barracuda and Chaetodon capistratus, and the shallow coral reef for juvenile
H. chrysargyreum, L. mahogoni, A. bahianus and Abudefduf saxatilis. Juvenile Acanthurus coeruleus utilized all six biotopes,
while juvenile H. carbonarium and Anisotremus surinamensis were not observed in any of the six biotopes. Although fishes
showed a clear preference for a specific nursery biotope, most fish species utilized multiple nursery biotopes
simultaneously. The almost complete absence of juveniles on the deeper reef zones indicates the high dependence of
juveniles on the shallow water biotopes as a nursery. For most fish species an (partial) ontogenetic shift was observed at
a particular life stage from their (shallow) nursery biotopes to the (deeper) coral reef. Cluster analyses showed that closely
related species within the families Haemulidae, Lutjanidae and Acanthuridae, and the different size classes within species
2000 Academic Press
in most cases had a spatial separation in biotope utilization.
Keywords: fish; nursery grounds; bays; mangrove swamps; sea grasses; reefs; ontogenetic shifts; Caribbean Sea
Introduction and seagrass beds. The hypotheses are based on
avoidance of predators, the abundance of food and
Many studies in various parts of the world have
the interception of fish larvae: (a) the structural
recognized the importance of mangroves and seagrass
complexity of these biotopes provide excellent
beds as habitats for fishes. Mangroves and seagrass
shelter against predators (Parrish, 1989; Robertson
beds have been shown to contain a high diversity and
& Blaber, 1992), (b) these biotopes are often located
abundance of estuarine and/or coral reef fishes in the
at a distance from the coral reef or from off-shore
Caribbean (e.g. Springer & McErlean, 1962; Austin,
waters and are therefore less frequented by predators
1971; Weinstein & Heck, 1979; Thayer et al., 1987;
(Shulman, 1985; Parrish, 1989), (c) the relatively
Baelde, 1990; Sedberry & Carter, 1993), in the Indian
turbid water of the bays and estuaries decrease the
Ocean (e.g. Little et al., 1988; van der Velde et al.,
foraging efficiency of predators (Blaber & Blaber,
1995; Pinto & Punchihewa, 1996), and in the Pacific
1980; Robertson & Blaber, 1992), (d) these biotopes
Ocean (e.g. Blaber, 1980; Bell et al., 1984; Robertson
provide a great abundance of food for fishes (Odum
& Duke, 1987; Blaber & Milton, 1990; Morton, 1990;
& Heald, 1972; Carr & Adams, 1973; Ogden &
Tzeng & Wang, 1992).
Zieman, 1977) and (e) these biotopes often cover
Several hypotheses have been proposed to explain
extensive areas and may intercept planktonic fish
the high abundance of (juvenile) fishes in mangroves
larvae more effectively than the coral reef (Parrish,
1989).
d
Corresponding author. E-mail: gerardv@sci.kun.nl
2000 Academic Press
0272–7714/00/070031+14 $35.00/0
32 I. Nagelkerken et al.
(a) (b)
b
II
a
Gotomeer I
c 0 1000 m
IV
a+b+c+d VII b IX
6 a
5d
0 5000 m 4 a+b+c
III
Klein Bonaire
Kralendijk
Sorobon
Lac
1 a+b VIII Cai
2 a+b
Dam
V
Pekelmeer VI
3 a + b+ d isles
mangroves
A. cervicornis
F 1. (a) Map of Bonaire showing the different coral reef study sites. a=20 to 25 m, b=10 to 15 m, c=3 to 5 m,
d=0 to 3 m. (b) Map of Lac Bay showing the different mangrove (II, IV, VI, VII, VIII, IX) and seagrass bed (I, III, V)
study sites. A. cervicornis=Acropora cervicornis.
Studies on fish community structure in Caribbean focused on either mangroves or seagrass beds, and
lagoons, bays and estuaries containing mangroves or usually with a different sampling method. This makes
seagrass beds often mention high densities of juvenile a comparison between studies and biotopes difficult.
fish and state that these biotopes function as nursery Only a few studies have sampled both biotopes simul-
areas for various coral reef fish species (e.g. Austin, taneously (Thayer et al., 1987; Sedberry & Carter,
1971; Weinstein & Heck, 1979; Baelde, 1990; 1993), and even fewer have included censuses on the
Sedberry & Carter, 1993). In the Indo-Pacific, adjacent or off-shore coral reef (e.g. van der Velde
however, the nursery function of these biotopes is et al., 1992). Hence, quantitative data describing the
apparent only in some regions (Blaber, 1980; Bell ecological links of fish faunas between mangroves,
et al., 1984; Little et al., 1988; Tzeng & Wang, 1992), seagrass beds and coral reefs are largely lacking
whereas in other regions these biotopes do not appear (Ogden & Gladfelter, 1983; Birkeland, 1985; Parrish,
to be important (Quinn & Kojis, 1985; Thollot & 1989).
Kulbicki, 1988; Blaber & Milton, 1990; Thollot, To provide a better insight into the importance of
1992). mangroves, seagrass beds and depth zones of the coral
Most studies describing the nursery function of reef as nursery biotopes and their interrelationship in
mangroves and seagrass beds were based on quali- fish fauna, size frequency data were collected for
tative observations, made no distinction between 16 commercially important reef fish species in each
abundances of juvenile and adult fishes, and did not biotope, using a visual census technique. The objec-
provide quantitative data on fish size. The few studies tives of the present study were to answer the following
which did provide size data for separate species only four questions: (1) Which biotopes are used as a
mentioned the full size range of all fish caught nursery by the selected fish species? (2) Which biotope
(Springer & McErlean, 1962; Austin, 1971). Hence, is preferred by a fish species in case multiple nursery
size-frequency data of juvenile and adult reef fish are biotopes are used? (3) Do fish species show an onto-
largely lacking for these biotopes. Furthermore, many genetic shift from their nursery biotopes to other
fish species show ontogenetic shifts in habitat utiliz- biotopes when reaching a larger size? (4) Do closely
ation and migrate from their nursery grounds to an related fish species show a spatial separation in
intermediate life stage habitat or to the coral reef biotope utilization?
(Ogden & Ehrlich, 1977; Weinstein & Heck, 1979;
McFarland, 1980; Rooker & Dennis, 1991). The size
range and the biotopes where these shifts occur have Materials and methods
also not been described accurately for many fish
Lac Bay is the largest bay of Bonaire with an area of
species.
approximately 8 km2 and is situated on the exposed
Studies referring to the nursery function of lagoons,
eastern side of the island [Figure 1(a)]. The bay
bays and estuaries in the Caribbean have mostly
Nursery function of mangroves, seagrass beds and the shallow coral reef 33
T 1. Depth, temperature and salinity of the seawater in snappers (Lutjanidae): yellowtail snapper Ocyurus
the six different biotopes chrysurus, mahogany snapper Lutjanus mahogoni,
schoolmaster L. apodus, and gray snapper L. griseus;
Depth (m) Temperature ( C) Salinity
three species of surgeonfishes (Acanthuridae): doctor-
fish Acanthurus chirurgus, ocean surgeon A. bahianus,
Seagrass bed 0·4–1·4 28·6–33·4 37–44 and blue tang A. coeruleus; one species of barracuda
Mangroves 0·3–1·2 28·5–34·0 39–44
(Sphyraenidae): great barracuda Sphyraena barracuda;
Coral reef 0–3 29·0–29·8 n.d.
one species of parrotfish (Scaridae): stoplight
Coral reef 3–5 27·1–29·3 n.d.
parrotfish Sparisoma viride; one species of damselfish
Coral reef 10–15 27·1–29·8 n.d.
Coral reef 20–25 26·8–29·5 n.d. (Pomacentridae): sergeant major Abudefduf saxatilis;
and one species of butterflyfish (Chaetodontidae):
n.d.=no data. foureye butterflyfish Chaetodon capistratus.
The selected fish species were studied using a
visual census technique in six different biotopes, viz.
mangrove prop-roots and seagrass beds, and the
consists of a shallow basin (0 to 3 m deep) and is
coral reef of 0 to 3 m, 3 to 5 m, 10 to 15 m and 15
protected from wave exposure by a shallow barrier of
to 20 m [Figure 1(a,b)]. Water clarity for visual
dead and living corals [Figure 1(b)]. The bay is
censuses was good in all six biotopes, even in the
connected to the sea by a narrow channel which is
mangroves. The visual census technique was based
about 8 m deep. The soft-bottom flora of the bay
on best estimation by eye of abundance and body
is dominated by the seagrass Thalassia testudinum and
length of the selected fish species in permanent belt
the calcareous alga Halimeda opuntia. Other common
transects in all six biotopes. Size classes of 5 cm were
vegetation consists of the seagrass Syringodium
used for the estimation of body length (TL). The
filiforme and the alga Avrainvillea nigricans. The bay
usage of smaller size classes was avoided to reduce
is bordered almost completely by the mangrove
differences in size class estimation between ob-
Rhizophora mangle. In front of the bay the coral
servers. For the large-sized Sphyraena barracuda size
reef is situated, which runs around the island. The
classes of 15 cm were used. Length estimation was
reef consists of a shallow reef terrace which sharply
practiced prior to the censuses on objects with
drops off at an angle of 45 to 60 at a depth of
known length lying on the sea bottom. In addition,
8 to 12 m.
the underwater slates for data recording were
The maximum tidal range on Bonaire is 30 cm (van
marked with a ruler for guidance in size estimation.
Moorsel & Meijer, 1993). The seagrass beds and
Visual census estimations of fish abundance were
mangrove prop-roots at the study sites were not
compared with catches at two seagrass sites using the
exposed at low tide and ranged in depth from 0·3 to
drop net quadrat method (Hellier, 1958). At sites
1·4 m (Table 1). The temperature, measured during
VIII and IX [see Figure 1(b)] a drop net of
the entire study period, ranged from 28·5 to 34·0 C
10 10 m was installed on the seagrass bed. During
in the bay, and was on average higher than on of the
the morning (09.00–10.00h) the net was lowered
coral reef where it ranged from 26·8 to 29·8 C. The
onto the sea bottom and all fishes within the net
salinity, measured at the beginning and at the end of
were caught, identified and counted. A total of seven
the study period, ranged from 37 to 44 in the seagrass
drop net catches were made at the two seagrass sites
beds and from 39 to 44 in the mangroves. The water
during August to December 1981. In addition, dif-
of the bay is quite clear and horizontal Secchi visibility
ferences in estimation of abundance was statistically
ranges from 4·6 to 21·6 m in the central parts of the
tested (t-test) between the two observers for each
bay (van Moorsel & Meijer, 1993).
species in each biotope (96 cases).
Sixteen reef fish species were selected in the present
Advantages of visual censuses are that they are
study. Species were selected which were abundant,
rapid, non-destructive, inexpensive, can be used for all
not too shy, easy to identify in the field and had a
selected biotopes of this study, the same areas can be
non-cryptic life style. Further selection was on
resurveyed through time, and the results can be com-
basis of their economic value (i.e. reef fisheries,
pared with many other studies (English et al., 1994).
aquarium fisheries, attraction for diving industry).
Disadvantages are the differences in accuracy in esti-
The 16 species consisted of five species of grunts
mation of numbers and sizes by the observers, and
(Haemulidae): French grunt Haemulon flavolineatum,
fishes may be attracted or scared off by the observers
bluestriped grunt H. sciurus, smallmouth grunt H.
(English et al., 1994; Cheal & Thompson, 1997;
chrysargyreum, Caesar grunt H. carbonarium, and
Thompson & Mapstone, 1997).
black margate Anisotremus surinamensis; four species of
34 I. Nagelkerken et al.
T 2. Mean density (1000 m 2) of the 16 fish species in the six different biotopes surveyed by visual census, and mean
density on the seagrass beds based on drop net catches
Seagrass bed
Coral reef Coral reef Coral reef Coral reef
drop net visual census Mangroves 0–3 m 3–5 m 10–15 m 20–25 m
Haemulon flavolineatum 782·5 115·3 59·9 52·4 37·4 12·4 2·9
H. sciurus 12·7 5·5 4·3 0·4 0·4 9·6 0·5
H. chrysargyreum 0·0 0·01 0·0 64·7 53·9 0·0 0·0
H. carbonarium 0·0 0·0 0·0 0·0 0·0 5·4 0·1
Anisotremus surinamensis 0·0 0·0 0·0 0·0 0·0 0·8 0·1
Ocyurus chrysurus 20·6 16·4 1·2 0·0 1·1 24·7 11·8
Lutjanus mahogoni 0·0 1·1 0·0 9·6 1·7 12·6 2·3
L. apodus 30·2 8·1 65·8 0·5 0·0 9·7 3·4
L. griseus 4·8 8·7 29·9 0·0 0·0 0·0 0·04
Acanthurus chirurgus 0·0 9·2 0·8 5·6 0·1 0·6 0·8
A. bahianus 27·0 3·3 0·2 86·6 19·3 5·6 4·4
A. coeruleus 0·0 1·1 2·6 10·2 21·8 7·7 4·5
Sphyraena barracuda 6·3 0·9 5·1 0·0 0·0 0·1 0·2
Sparisoma viride 60·3 26·1 1·4 11·1 34·6 11·4 6·3
Abudefduf saxatilis 0·0 0·2 3·9 65·2 0·3 16·8 0·1
Chaetodon capistratus 12·7 4·9 16·7 2·7 14·4 23·1 9·6
In each of the six biotopes, permanently marked between species without the data being affected by
belt transects were established. In the seagrass beds, differences in total fish densities.
a transect of 300 3 m was established at three
different sites. In the mangroves, nine transects were
Results
established of 3 m wide and 25 to 100 m long. On the
coral reef, six sites were selected and at each site,
Drop net catches vs visual census
transects of 3 100 m were established at two to four
depth zones [Figure 1(a)]. During May to November Catches with the drop net showed higher abundances
1981, visual censuses were done by two trained for some fish species than estimations with the
observers together in the morning (09.00–11.00h) and visual census technique (Table 2), especially for H.
in the afternoon (14.00–16.00h) by means of flavolineatum. On the other hand, visual estimations of
snorkelling or SCUBA diving. The census in each abundance of A. chirurgus were much higher than with
transect was repeated at monthly intervals. The the drop net quadrat method. For the visual censuses,
fish counts in transects at the different sites, of the only in 8 out of 61 cases a significant difference
morning and afternoon survey, and of all seven (P<0·05, t-test) was found in estimation of abundance
months were pooled and averaged per area. They are between the two observers (for 35 cases insufficient
expressed as the average fish density per 1000 m2 for data were available for statistical testing).
each size class of each species in each biotope.
Cluster analyses were carried out using the com-
Biotope utilization of Haemulidae
puter programme CLUSTAN1C2 (Wishart, 1978).
The average-linkage method (Sokal & Michener, Juveniles of Haemulidae were restricted to shallow
1958) was used in combination with the Bray-Curtis water biotopes (i.e. seagrass beds, mangroves and reef
coefficient. Separate analyses were carried out for of 0 to 3 m), whereas adults were found on the deeper
closely related species belonging to a single family reef (>3 m) (Figure 2, Table 3). An exception was
(Haemulidae, Lutjanidae, Acanthuridae) using log- formed by adult Haemulon chrysargyreum which were
transformed data of the densities in the different size also found on the reef of 0 to 3 m. Large juveniles of
classes and biotopes. Cluster analysis of all species H. sciurus utilized the mangroves as an intermediate
together was carried out on data in which densities life stage biotope, in their ontogenetic shift from the
per size class for each biotope were transformed to seagrass beds to the coral reef. Haemulon flavolineatum
percentages of total composition of a particular showed significant temporal differences in total
species. This was done to compare biotope utilization density in the seagrass beds (Friedman’s test,
Nursery function of mangroves, seagrass beds and the shallow coral reef 35
120 8
(a) Coral reef 20–25 m (b)
Summed mean density
Summed mean density
7
Coral reef 10–15 m
100
Coral reef 3–5 m 6
Coral reef 0–3 m
(1000 m–2)
(1000 m–2)
80
5
Seagrass bed
Mangroves
60 4
3
40
2
20
1
0 0
0–5 5–10 10–15 15–20 20–25 0–5 5–10 10–15 15–20 20–25 25–30 30–35
Size class (cm) Size class (cm)
60 4
(c) (d)
Summed mean density
Summed mean density
50
3
(1000 m–2)
(1000 m–2)
40
30 2
20
1
10
0 0
0–5 5–10 10–15 15–20 20–25 0–5 5–10 10–15 15–20 20–25 25–30 30–35
Size class (cm) Size class (cm)
0.5
(e)
Summed mean density
0.4
(1000 m–2)
0.3
0.2
0.1
0.0
0–5 5–10 10–15 15–20 20–25 25–30 30–35 35–40
Size class (cm)
F 2. Summed mean densities of Haemulidae in different biotopes. (a) Haemulon flavolineatum; (b) H. sciurus;
(c) H. chrysargyreum; (d) H. carbonarium; (e) Anisotremus surinamensis.
P<0·05), increasing from 25·4 per 1000 m2 in May to H. carbonarium and A. surinamensis showed some
178·9 per 1000 m2 in October. similarity in biotope utilization, but the former was
Cluster analysis of all size classes of all haemulids much more abundant than the latter (Figure 2).
also showed a spatial separation in biotope utilization Considering the entire species size range, H.
among the different size classes and/or species, with flavolineatum dominated over its related species in the
juveniles found in the mangroves and seagrass beds, seagrass beds, mangroves and reef of 20 to 25 m, but
medium-sized individuals on the reef and partly still in co-occurred with H. chrysargyreum on the reef of 0 to
the mangroves, and very large individuals on the deep 5 m [Figure 5(a), Table 2]. Haemulon sciurus and
reef (Figure 3). Haemulon chrysargyreum formed a H. carbonarium co-occurred with H. flavolineatum on
separate cluster since adults partly co-occurred with the reef of 10 to 15 m. Anisotremus surinamensis was
the juveniles in their nursery habitat. not dominant in any of the biotopes.
Species of Haemulidae showed a spatial separation
in biotope utilization and occurred in different biotope
Biotope utilization of Lutjanidae
clusters as calculated by cluster analysis (Figure 4).
Furthermore, the Haemulidae were not found Juveniles of Lutjanidae were restricted to the shallow
together in a single cluster with any species belonging water biotopes (Figure 6, Table 3). Only juveniles of
to the same feeding guild (Figure 4, Table 3). Only L. mahogoni were also partly found deeper on the reef
36 I. Nagelkerken et al.
T 3. Importance (+) of the six different biotopes for juveniles and adults of the different fish species. *Indicates most important biotope for juveniles. Maturation
size refers to that of the smallest individuals and not to the species average. Maturation data are from De Sylva (1963), Starck and Schroeder (1971); Munro (1983).
Ontogenetic migration indicates the migration of juveniles to the (deeper) coral reef when reaching adult sizes; +/ = partial ontogenetic migration (i.e. part of the
fish population). Feeding guilds: BI=benthic invertebrate feeder, PI=planktonic invertebrate feeder, P=piscivore, H=herbivore, O=omnivore. Ontogenetic shifts in
feeding guild are indicated as that of juveniles/adults
Juveniles Adults
Maturation
Feeding size Seagrass Reef Reef Reef Reef Seagrass Reef Reef Reef Reef Ontogenetic
guild (cm) bed Mangroves 0–3 m 3–5 m 10–15 m 20–25 m bed Mangroves 0–3 m 3–5 m 10–15 m 20–25 m migration
Haemulon flavolineatum BI >10 +* + + + + +
H. sciurus BI >15 +* + + +
H. chrysargyreum BI >15 +* + + +/
H. carbonarium BI >15 + ?
Anisotremus surinamensis BI >20 + ?
Ocyurus chrysurus PI >25 +* + + +
Lutjanus mahogoni BI/P >20 + +* + + + +
L. apodus BI/P >25 + +* + + + +
L. griseus BI/P >15 + +* +
Acanthurus chirurgus H >15 +* + + + + +/
A. bahianus H >10 + +* + + +/
A. coeruleus H >10 + + + + + + + + +/
Sphyraena barracuda P >45 + +* + + + + +/
Sparisoma viride H >15 +* + + + + + +/
Abudefduf saxatilis O >10 +* + + +/
Chaetodon capistratus H/BI >5 + +* + + + + +
Nursery function of mangroves, seagrass beds and the shallow coral reef 37
0.9
0.8
0.7
0.6
Dissimilarity
0.5
0.4
0.3
0.2
0.1
0.0
A. su. 25–30
H. ca. 25–30
A. su. 30–35
A. su. 35–40
H. ca. 30–35
H. sc. 5–10
H. fl. 20–25
H. ca. 20–25
H. fl. 0–5
H. sc. 10–15
H. fl. 15–20
H. sc. 25–30
H. sc. 0–5
H. sc. 30–35
H. ca. 15–20
H. ch. 15–20
A. su. 20–25
H. sc. 15–20
H. fl. 5–10
H. fl. 10–15
H. sc. 20–25
H. ch. 10–15
H. ch.20–25
H. ch. 5–10
H. ch. 0–5
Seagrass and mangrove Coral reef and mangrove Shallow reef Seagrass Deep reef
F 3. Cluster analysis of all size classes of Haemulidae in different biotopes. H. fl.=Haemulon flavolineatum,
H. sc.=H. sciurus, H. ch.=H. chrysargyreum, H. ca.=H. carbonarium, A. su.=Anisotremus surinamensis. The numbers indicate
the size classes.
0.9
0.8
0.7
0.6
Dissimilarity
0.5
0.4
0.3
0.2
0.1
0.0
H. carbonarium
H. flavolineatum
A. chirurgus
H. chrysargyreum
A. surinamensis
A. bahianus
A. coeruleus
C. capistratus
S. viride
A. saxatilis
H. sciurus
O. chrysurus
L. mahogoni
L. griseus
L. apodus
1 2 3 4 5 6 7 8 9
F 4. Cluster analysis of all 16 fish species based on the abundance of each size class in the different biotopes.
in the seagrass beds from 0·9 per 1000 m2 in May
of 3 to 5 m. All species, except L. griseus, showed an
to 17·2 per 1000 m2 in October. Ocyurus chrysurus
ontogenetic shift to the (deeper) coral reef. Lutjanus
apodus and L. griseus also occurred as adults in the increased in density in the seagrass beds from 4·4 per
1000 m2 in June to 41·4 per 1000 m2 in November.
mangroves. Lutjanus apodus showed significant tem-
poral differences in total density (Friedman’s test, Cluster analysis of all size classes of all lutjanids also
P<0·05), increasing in the mangroves from 57·7 per revealed a clear separation between adults and large
1000 m2 in May to 92·3 per 1000 m2 in August, and individuals (except L. griseus) on the deep reef (10 to
38 I. Nagelkerken et al.
25 m), and juveniles in the shallow water biotopes
(a)
(Figure 7).
100%
Species of Lutjanidae showed a spatial separation in
biotope utilization, except L. griseus and L. apodus
80%
which showed some degree of similarity in biotope
utilization and also belonged to the same feeding guild
60%
(Figure 4, Table 3). Considering the entire species
size range, L. apodus dominated over its related
40%
species in the mangroves, while for L. mahogoni
and O. chrysurus this was the case on the reef of 0
20%
to 3 m and on the reef of 20 to 25 m, respectively
0% [Figure 5(b), Table 2]. In the other three biotopes,
H. flavolineatum H. sciurus
lutjanids co-occurred without a single species showing
H. chrysargyreum H. carbonarium
an overall dominance.
A. surinamensis
(b)
100%
Biotope utilization of Acanthuridae
Juveniles of Acanthuridae were restricted to the
80%
shallow water biotopes, whereas adults were found on
Composition
60% the reef (Figure 8, Table 3). Adults were also found in
the juvenile nursery habitat (i.e. reef of 0 to 3 m),
40%
however, co-occurring with the juveniles. For larger
juveniles of A. coeruleus the reef of 3 to 5 m was also of
20%
importance. Acanthurus bahianus showed significant
temporal differences in total density (Friedman’s
0%
test, P<0·05), with peak abundances in the seagrass
O. chrysurus L. mahogoni
beds of around 5 per 1000 m2 in July, October, and
L. griseus L. apodus
November. Acanthurus coeruleus increased in density
(c)
on the reef of 3 to 5 m from 5·4 per 1000 m2 in May
100%
to 47·1 per 1000 m2 in September.
Cluster analysis of all size classes of all acanthurids
80%
also showed a separation between juveniles in the
seagrass beds and mangroves, and medium-sized and
60%
larger individuals on the reef (Figure 9).
Species of Acanthuridae showed a spatial separation
40%
in biotope utilization and occurred in different biotope
clusters (Figure 4). Of the Acanthuridae, only A.
20%
coeruleus was found with another herbivore species
0% (S. viride) in a single cluster, although the dissimilarity
s
es
m
m
m
m
ds
in biotope utilization between the two species was still
be gra
ov
–3
–5
15
25
gr
f0
f3
0–
0–
a
high (Figure 4, Table 3). Considering the entire
an
Se
f1
f2
ee
ee
M
R
R
ee
ee
species size range, each species dominated over its
R
R
related species in a particular biotope: A. chirurgus in
A. bahianus A. coeruleus
the seagrass beds, A. coeruleus in the mangroves, and
A. chirurgus
A. bahianus on the coral reef of 0 to 3 m [Figure 5(c),
F 5. Biotope partitioning between closely related
Table 2). In the other reef zones, A. coeruleus and
species: (a) Haemulidae, (b) Lutjanidae, (c) Acanthuridae.
A. bahianus co-occurred in almost equal densities.
The abundance of each species is expressed as the percent-
age composition of the total abundance of all related species
within a single family for each biotope. The entire size range
Biotope utilization of other species
of a species is pooled per biotope, although preferences may
differ among size classes. For the specific differences among
For the remaining four species, juveniles were also
size classes see Figures 2, 6 and 8.
restricted to the shallow water biotopes, whereas
adults occurred on the coral reef (Figures 10–13,
Table 3). Exceptions were adult S. barracuda which
Nursery function of mangroves, seagrass beds and the shallow coral reef 39
20 7
Mangroves Seagrass bed
(a) (b)
Summed mean density
Summed mean density
6
Coral reef 0–3 m Coral reef 3–5 m
Coral reef 10–15 m Coral reef 20–25 m
15 5
(1000 m–2)
(1000 m–2)
4
10
3
2
5
1
0 0
0–5 5–10 10–15 15–20 20–25 25–30 30–35 35–40 0–5 5–10 10–15 15–20 20–25 25–30 30–35
Size class (cm) Size class (cm)
25 14
(c) (d)
Summed mean density
Summed mean density
12
20
10
(1000 m–2)
(1000 m–2)
15 8
6
10
4
5
2
0 0
0–5 5–10 10–15 15–20 20–25 25–30 30–35 35–40 40–45 0–5 5–10 10–15 15–20 20–25 25–30 30–35 35–40 40–45 45–50
Size class (cm) Size class (cm)
F 6. Summed mean densities of Lutjanidae in different biotopes. (a) Ocyurus chrysurus; (b) Lutjanus mahogoni;
(c) L. apodus; (d) L. griseus.
0.9
0.8
0.7
Dissimilarity
0.6
0.5
0.4
0.3
0.2
0.1
0.0
O. ch. 10–15
L. gr. 0–5
L. gr. 35–40
L. gr. 30–35
L.gr. 5–10
L.gr. 10–15
L. gr. 15–20
L. ap. 5–10
L. ap. 10–15
L. gr. 20–25
L. gr. 25–30
L. ap . 0–5
L. ap. 15–20
L. ap. 20–25
O. ch. 0–5
O. ch. 5–10
L. gr. 40–45
L. gr. 45–50
L. ma. 0–5
L. ma. 5–10
L. ma. 10–15
L. ap. 25–30
L. ap. 30–35
O. ch. 15–20
L. ap. 35–40
O. ch. 35–40
L. ma. 20–25
L. ma. 25–30
O. ch. 30–35
O. ch. 20–25
O. ch. 25–30
L. ma. 15–20
L. ap. 40–45
L. ma. 30–35
f1 3m
ss
e
5d
m
m
ss
e
m
ov
ov
–1 an
ra
ra
m
–5
25
25
gr
gr
–
ag
ag
10 ve
R d0
f0
0–
0–
an
an
se
Se
ef ro
f1
ee
M
an
M
re ang
d
R
ee
ee
an
25
R
M
0–
e
ov
f1
gr
ee
an
R
M
Bay and shallow reef Deep reef
F 7. Cluster analysis of all size classes of Lutjanidae in different biotopes. L. gr.=Lutjanus griseus, L. ap.=L. apodus,
L. ma.=L. mahogoni, O. ch.=Ocyurus chrysurus. The numbers indicate the size classes.
also used the seagrass beds and mangroves as a life A. saxatilis co-occurred with the juveniles on the
stage biotope, and juvenile S. viride which also used shallow reef. Sphyraena barracuda showed significant
the reef of 3 to 5 m as a nursery biotope. Some adult temporal differences in total density (Friedman’s test,
40 I. Nagelkerken et al.
10 50
Coral reef 20–25 m
(a) (b)
Summed mean density
Summed mean density
Coral reef 10–15 m
8 40
Coral reef 3–5 m
Coral reef 0–3 m
(1000 m–2)
(1000 m–2)
Seagrass bed
6 30
Mangroves
4 20
2 10
0 0
0–5 5–10 10–15 15–20 20–25 25–30 0–5 5–10 10–15 15–20 20–25 25–30
Size class (cm) Size class (cm)
20
(c)
Summed mean density
16
(1000 m–2)
12
8
4
0
0–5 5–10 10–15 15–20 20–25
Size class (cm)
F 8. Summed mean densities of Acanthuridae in different biotopes. (a) Acanthurus chirurgus; (b) A. bahianus;
(c) A. coeruleus.
1.0
0.9
0.8
0.7
Dissimilarity
0.6
0.5
0.4
0.3
0.2
0.1
0.0
A. ba. 15–20
A. ba 10–15
A. ba 0–5
A. ch. 15–20
A. co. 15–20
A. ba. 5–10
A. ch. 5–10
A. co. 10–15
A. ba. 25–30
A. ch. 0–5
A. co. 20–25
A. ch. 20–25
A. ch. 25–30
A. ba. 20–25
A. ch. 10–15
A. co. 0–5
A. co. 5–10
Seagrass and reef Reef 0–25 m Reef and bay Reef
0–3 m 0–25 m
F 9. Cluster analysis of all size classes of Acanthuridae in different biotopes. A. ba.=Acanthurus bahianus,
A. ch.=A. chirurgus, A. co.=A. coeruleus. The numbers indicate the size classes.
beds from 12·7 per 1000 m2 in June to 43·1 per
P<0·05), with densities in the mangroves about two
1000 m2 in November, and C. capistratus from 2·0 per
times higher in August–November than in May–July.
1000 m2 in May to 8·0 per 1000 m2 in November.
Sparisoma viride increased in density in the seagrass
Nursery function of mangroves, seagrass beds and the shallow coral reef 41
3 Coral reef 20–25 m
Coral reef 20–25 m
Coral reef 10–15 m
Summed mean density
Coral reef 10–15 m
Coral reef 3–5 m
Coral reef 3–5 m
Coral reef 0–3 m
Summed mean density
Coral reef 0–3 m
(1000 m–2)
2 Seagrass bed
60
Seagrass bed
Mangroves
Mangroves
(1000 m–2)
50
1 40
30
0 20
0–15
15–30
30–45
45–60
60–75
75–90
90–105
105–120
120–135
135–150
150–165
165–180
180–195
195–210
10
0
Size class (cm) 0–5 5–10 10–15
Size class (cm)
F 10. Summed mean densities of Sphyraena barracuda
in different biotopes. F 13. Summed mean densities of Chaetodon
capistratus in different biotopes.
30
Coral reef 20–25 m of fish abundance. This variation is assumed to be
Coral reef 10–15 m
Summed mean density
25 comparable for the different biotopes, making a com-
Coral reef 3–5 m
Coral reef 0–3 m parison among the biotopes possible. Differences in
20
(1000 m–2)
Seagrass bed
estimation of abundance between observers were
Mangroves
15 present, but not consistent. Although density esti-
mations in seagrass beds are more accurate with
10
the drop net quadrat method, the total surface area
sampled (100 m2) was much smaller than with the
5
visual censuses (900 m2), resulting in large variations
0
0–5 5–10 10–15 15–20 20–25 25–30 30–35 35–40 among the transects and a restricted sampling of the
Size class (cm) biotope studied.
The present study shows the importance of
F 11. Summed mean densities of Sparisoma viride in
different biotopes. different shallow water biotopes as a nursery for
economically important reef fish species. All 14
species for which juveniles were observed used either
60
the mangroves, seagrass beds or the shallow reef of
Coral reef 20–25 m
Summed mean density
Coral reef 10–15 m
50 0 to 3 m, or a combination of these biotopes, as a
Coral reef 3–5 m
nursery. The high dependence of juveniles on
Coral reef 0–3 m
(1000 m–2)
40
Seagrass bed these biotopes can be deduced from the fact that
Mangroves
30
juveniles were exclusively present or highly dominant
in these biotopes and not on the deeper reef (i.e.
20
>3 m).
10
The data show that not only mangroves and
0 seagrass beds are important nursery biotopes for
0–5 5–10 10–15 15–20 20–25
juvenile fishes (e.g. Austin, 1971; Weinstein & Heck,
Size class (cm)
1979; Baelde, 1990; Sedberry & Carter, 1993)
F 12. Summed mean densities of Abudefduf saxatilis in
but also the shallow coral reef. Two reasons why
different biotopes.
mangroves and seagrass beds may contain high
densities of juvenile fish is their structural complexity
Discussion which provides a hiding place against predators (Bell
& Westoby, 1986; Robertson & Blaber, 1992), and
For several fish species in the seagrass beds the visual
because they are often located at a distance from
census technique showed lower densities than the
the coral reef and are therefore less frequented by
catches with the drop net quadrat method. Especially
predators (Shulman, 1985; Parrish, 1989). These two
H. flavolineatum was underestimated in the visual
factors also apply to the shallow coral reef of Bonaire,
censuses. The formation of large schools in this and
which mostly consists of living and dead colonies of
other species and the continuous movement of the
Acropora palmata, Millepora complanata and other
fishes caused a reduced accuracy in the estimation
42 I. Nagelkerken et al.
corals. The dead and living corals provide an ideal mangroves. For some species, the ontogenetic shift to
hiding space and can house relatively high densities of the (deeper) coral reef was partial and a part of the
(juvenile) fish (Nagelkerken, 1974). Furthermore, the large and adult fish could still be found in their nursery
shallow reef is separated from the main coral reef and biotope.
its predators by a shallow reef terrace of about 75 to The present study shows the importance of Lac Bay
125 m in width (van Duyl, 1985). Shulman (1985) for a number of reef fish species. It is not known,
showed that at just 20 m from the main reef, in however, how much Lac Bay contributes to the reef
an exposed sandy location, predation on juvenile fish stocks of Bonaire. Effective areas of all biotopes
haemulids was considerably lower than at the edge of should therefore be measured and the turnover rate
the main reef. of fishes from the bay to the reef be quantified.
Biotope utilization appears to be very specific for Furthermore, it should be noted that Lac Bay is not
the different species and their size classes, each having comparable to many other mangrove and seagrass
a different niche. A clear spatial separation in biotope habitats, particularly in the Indo-Pacific. These
utilization was found among closely related species habitats often have a muddy substratum, are very
and among different size groups within species, sug- turbid, and show fluctuating salinities and a greater
gesting avoidance of competition. Biotope partitioning tidal range. These features influence the nursery
was observed for only a small size range of mostly one function of mangroves and seagrass beds (Blaber,
or two related species. Likewise, fish species belong- 1997). As the characteristics which are usually associ-
ing to the same feeding guild showed differences in ated with these habitats are reduced in Lac Bay, the
biotope utilization. Spatial variation across different mechanisms at work responsible for the nursery
biotopes often occurs among sympatric fish species function of this bay may differ from those in several
(Lewis & Wainwright, 1985; McAfee & Morgan, other bays, lagoons and estuaries which have been
1996). Comparable to the present study, Lewis and studied so far.
Wainwright (1985) found a differential biotope
utilization for the three species of Acanthuridae and
Conclusions
suggested this to be determined by complex inter-
actions of several factors, such as density of com- The questions asked in this study can be answered as
petitors, food availability, proximity to shelter, and follows. (1) Of all 14 fish species for which juveniles
predator abundance. Munro (1983) stated that inter- were observed, the mangroves, seagrass beds, shallow
specific competition for food is probably small for reef of 0 to 3 m, or a combination of these biotopes
Haemulidae since the different species each favour a were used as a nursery by the juveniles. (2) The
certain type of food (Randall, 1967). Nagelkerken seagrass beds were the most important nursery biotope
et al. (2000), however, found H. flavolineatum and H. for juvenile Haemulon flavolineatum, H. sciurus,
sciurus to have similar diets on seagrass beds, which Ocyurus chrysurus, Acanthurus chirurgus and Sparisoma
may explain the separation in biotope utilization of the viride, the mangroves were the most important biotope
different size classes. Lutjanidae show a high overlap for juvenile Lutjanus apodus, L. griseus, Sphyraena
in diet, with exception of Ocyurus chrysurus (Randall, barracuda and Chaetodon capistratus, the shallow coral
1967; Nagelkerken et al., 2000). As biotope utiliz- reef was the most important biotope for juvenile H.
ation differed only slightly between Lutjanus mahogoni chrysargyreum, L. mahogoni, A. bahianus and Abudefduf
and L. griseus, which both occurred in similar saxatilis, Acanthurus coeruleus did not show a prefer-
densities, a high degree of competition may be present ence for a particular nursery habitat, and for H.
between these two species. carbonarium and Anisotremus surinamensis it could not
When fishes become too large for optimal protection be established which biotope was used as a nursery by
by the seagrass shoots and mangrove prop-roots they the juveniles. (3) For most fish species, the juveniles
often migrate to the coral reef. This migration pattern were found in shallow-water biotopes and the large
has largely been described qualitatively for only few and adult fish on the (deeper) coral reef. (4) Closely
species (e.g. Ogden & Ehrlich, 1977; Weinstein & related species showed a spatial separation in biotope
Heck, 1979; McFarland, 1980; Rooker & Dennis, utilization. This was also observed for different size
1991). The present study shows that most of the classes within species.
selected species use the shallow water biotopes as nurs-
eries during their juvenile stage, but migrate perma-
Acknowledgements
nently to the (deeper) coral reef when reaching a
specific size class. An exception was Lutjanus griseus This study was funded by grants to MWG and
of which the entire size range was found in the GJM from the Stichting Werkgroep Studiereizen
Nursery function of mangroves, seagrass beds and the shallow coral reef 43
McAfee, S. T. & Morgan, S. G. 1996 Resource use by five
Ontwikkelingslanden, the Beijerinck-Popping Fonds,
sympatric parrotfishes in the San Blas Archipelago, Panama.
and the Natuurwetenschappelijke Studiekring voor Marine Biology 125, 427–437.
Suriname en de Nederlandse Antillen. We would McFarland, W. N. 1980 Observations on recruitment in haemulid
fishes. Proceedings of the Gulf and Caribbean Fisheries Institute 32,
like to thank E. Newton of Stinapa Bonaire (Bonaire)
132–138.
and the staff of the Carmabi Foundation (Curacao)
¸ Morton, R. M. 1990 Community structure, density and standing
for their co-operation. We furthermore thank crop of fishes in a subtropical Australian mangrove area. Marine
Biology 105, 385–394.
Dr M. de Kluijver for doing the CLUSTAN analyses
Munro, J. L. 1983 Caribbean coral reef fishery resources. ICLARM
and Dr S. Rajagopal for his comments on the studies and reviews 7.
manuscript. Nagelkerken, W. P. 1974 On the occurrence of fishes in relation to
corals in Curacao. Studies on the Fauna of Curacao and other
¸ ¸
Caribbean Islands 45, 118–141.
Nagelkerken, I., Dorenbosch, M., Verberk, W. C. E. P., Cocheret
de la Moriniere, E. & van der Velde, G. 2000 Day-night shifts
`
References
of fishes between shallow-water biotopes of a Caribbean bay,
with emphasis on the nocturnal feeding of Haemulidae and
Austin, H. M. 1971 A survey of the ichtyofauna of the mangroves of
Lutjanidae. Marine Ecology Progress Series 194, 55–64.
western Puerto Rico during December, 1967–August, 1968.
Odum, W. E. & Heald, E. J. 1972 Trophic analyses of an estuarine
Caribbean Journal of Science 11, 27–39.
mangrove community. Bulletin of Marine Science 22, 671–738.
Baelde, P. 1990 Differences in the structures of fish assemblages in
Ogden, J. C. & Ehrlich, P. R. 1977 The behavior of heterotypic
Thalassia testudinum beds in Guadeloupe, French West Indies,
resting schools of juvenile grunts (Pomadasyidae). Marine Biology
and their ecological significance. Marine Biology 105, 163–173.
42, 273–280.
Bell, J. D. & Westoby, M. 1986 Abundance of macrofauna in dense
Ogden, J. C. & Gladfelter, E. H. (eds) 1983 Coral reefs, seagrass
seagrass is due to habitat preference, not predation. Oecologia 68,
beds, and mangroves: their interaction in the coastal zones of the
205–209.
Caribbean. UNESCO Reports in Marine Science 23, 133 pp.
Bell, J. D., Pollard, D. A., Burchmore, J. J., Pease, B. C. &
Ogden, J. C. & Zieman, J. C. 1977 Ecological aspects of coral
Middleton, M. J. 1984 Structure of a fish community in a
reef-seagrass bed contacts in the Caribbean. Proceedings of the
temperate tidal mangrove creek in Botany Bay, New South
Third International Coral Reef Symposium 1, 377–382.
Wales. Australian Journal of Marine and Freshwater Research 35,
Parrish, J. D. 1989 Fish communities of interacting shallow-water
33–46.
habitats in tropical oceanic regions. Marine Ecology Progress Series
Birkeland, C. 1985 Ecological interactions between mangroves,
58, 143–160.
seagrass beds, and coral reefs. In Ecological Interactions Between
Pinto, L. & Punchihewa, N. N. 1996 Utilisation of mangroves and
Tropical Coastal Ecosystems (Birkeland, C. & Grosenbaugh, D.,
seagrasses by fishes in the Negombo Estuary, Sri Lanka. Marine
eds). UNEP Regional Seas Reports and Studies No. 73, 1–26.
Biology 126, 333–345.
Blaber, S. J. M. 1980 Fish of the Trinity inlet system of north
Quinn, N. J. & Kojis, B. J. 1985 Does the presence of coral reefs
Queensland with notes on the ecology of fish faunas of tropical
in proximity to a tropical estuary affect the estuarine fish
Indo-Pacific estuaries. Australian Journal of Marine and Freshwater
assemblage? Proceedings of the Fifth International Coral Reef
Research 31, 137–146.
Congress 5, 445–450.
Blaber, S. J. M. 1997 Fish and Fisheries of Tropical Estuaries.
Randall, J. E. 1967 Food habits of reef fishes in the West Indies.
Chapman and Hall, London.
Studies in Tropical Oceanography 5, 665–847.
Blaber, S. J. M. & Blaber, T. G. 1980 Factors affecting the Robertson, A. I. & Blaber, S. J. M. 1992 Plankton, epibenthos and
distribution of juvenile estuarine and inshore fish. Journal of Fish fish communities. In Tropical Mangrove Ecosystems (Robertson,
Biology 17, 143–162. A. I. & Alongi, D. M., eds). Coastal and Estuarine Studies
Blaber, S. J. M. & Milton, D. A. 1990 Species composition, No. 41, 173–224.
community structure and zoogeography of fishes of mangrove Robertson, A. I. & Duke, N. C. 1987 Mangroves as nursery sites:
estuaries in the Solomon Islands. Marine Biology 105, 259–267. comparisons of the abundance and species composition of fish
Carr, W. E. S. & Adams, C. A. 1973 Food habits of juvenile marine and crustaceans in mangroves and other nearshore habitats in
fishes occupying seagrass beds in the estuarine zone near Crystal tropical Australia. Marine Biology 96, 193–205.
River, Florida. Transactions of the American Fisheries Society 102, Rooker, J. R. & Dennis, G. D. 1991 Diel, lunar and seasonal
511–540. changes in a mangrove fish assemblage off southwestern Puerto
Cheal, A. J. & Thompson, A. A. 1997 Comparing visual counts Rico. Bulletin of Marine Science 49, 684–698.
of coral reef fish: implications of transect width and species Sedberry, G. R. & Carter, J. 1993 The fish community of a shallow
selection. Marine Ecology Progress Series 158, 241–248. tropical lagoon in Belize, Central America. Estuaries 16, 198–215.
De Sylva, D. P. 1963 Systematics and life-history of the great Shulman, M. J. 1985 Recruitment of coral reef fishes: effects of
barracuda Sphyraena barracuda (Walbaum). Studies in Tropical distribution of predators and shelter. Ecology 66, 1056–1066.
Oceanography 1, 179. Sokal, R. R. & Michener, C. D. 1958 A statistical method for
English, S., Wilkinson, C. & Baker, V. (eds) 1994 Survey Manual evaluating systematic relationships. Kansas University Science
for Tropical Marine Resources. ASEAN-Australia Marine Bulletin 38, 1409–1438.
Science Project: Living Coastal Resources. Australian Institute Springer, V. G. & McErlean, A. J. 1962 Seasonality of fishes on a
of Marine Science, Townsville, pp. 68–80. south Florida shore. Bulletin of Marine Science of the Gulf and
Hellier, T. R. 1958 The drop-net quadrat, a new population Caribbean 12, 39–60.
sampling device. Publications of the Institute for Marine Science of Starck, W. A. & Schroeder, R. E. 1971 Investigations on the gray
the University of Texas 5, 165–168. snapper, Lutjanus griseus. Studies in Tropical Oceanography 10.
Lewis, S. M. & Wainwright, P. C. 1985 Herbivore abundance Thayer, G. W., Colby, D. R. & Hettler, W. F. 1987 Utilization of
and grazing intensity on a Caribbean coral reef. Journal of the red mangrove prop root habitat by fishes in south Florida.
Experimental Marine Biology and Ecology 87, 215–228. Marine Ecology Progress Series 35, 25–38.
Little, M. C., Reay, P. J. & Grove, S. J. 1988 The fish community Thollot, P. 1992 Importance of mangroves for Pacific reef fish
of an East African mangrove creek. Journal of Fish Biology 32, species, myth or reality? Proceedings of the Seventh International
729–747. Coral Reef Symposium 2, 934–941.
44 I. Nagelkerken et al.
Thollot, P. & Kulbicki, M. 1988 Overlap between the fish fauna Kenya (Indian Ocean): a study with nets and stable isotopes. In
inventories of coral reefs, soft bottoms and mangroves in Monsoons and Coastal Ecosystems in Kenya (Heip, C. H. R.,
Saint-Vincent Bay (New Caledonia). Proceedings of the Sixth Hemminga, M. A. & de Bie, M. J. M., eds). Netherlands Indian
International Coral Reef Symposium 2, 613–618. Ocean Programme Cruise Reports No. 5, 39–50.
Thompson, A. A. & Mapstone, B. D. 1997 Observer effects and van Duyl, F. C. 1985 Atlas of the living reefs of Curacao and Bonaire
¸
training in underwater visual surveys of reef fishes. Marine Ecology (Netherlands Antilles). Foundation for scientific research in
Progress Series 154, 53–63. Surinam and the Netherlands Antilles, no. 117, Utrecht,
Tzeng, W.-N. & Wang, Y.-T. 1992 Structure, composition and The Netherlands.
seasonal dynamics of the larval and juvenile fish community in van Moorsel, G. W. N. M. & Meijer, A. J. M. 1993 Base-line
the mangrove estuary of Tanshui River, Taiwan. Marine Biology Ecological Study van het Lac op Bonaire. Bureau Waardenburg bv,
113, 481–490. Culemborg, The Netherlands.
van der Velde, G., Gorissen, M. W., den Hartog, C., van’t Hof, T. Weinstein, M. P. & Heck, K. L. 1979 Ichtyofauna of seagrass
& Meijer, G. J. 1992 Importance of the Lac-lagoon (Bonaire, meadows along the Caribbean coast of Panama and in the gulf of
´
Netherlands Antilles) for a selected number of reef fish species. Mexico: composition, structure and community ecology. Marine
Hydrobiologia 247, 139–140. Biology 50, 97–107.
van der Velde, G., van Avesaath, P. H., Ntiba, M. J., Mwatha, Wishart, D. 1978 CLUSTAN User Manual. Programme Library
G. K., Marguillier, S. & Woitchik, A.-F. 1995 Fish fauna of Unit, Edinburgh University, Edinburgh.
mangrove creeks, seagrass meadows and sand flats in Gazi Bay,