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Marine Ecology. ISSN 0173-9565
ORIGINAL ARTICLE
Spatial discordance in fish, coral, and sponge assemblages
across a Caribbean atoll reef gradient
Charles Acosta1, Robin Barnes2 & Rebecca McClatchey1
1 Department of Biological Sciences, Northern Kentucky University, Highland Heights, KY, USA
2 Florida Department of Environmental Protection, Watershed Monitoring Section, Temple Terrace, FL, USA
Keywords
Belize; Caribbean; coral reef; fish diversity;
Glover’s Reef; spatial gradient; sponge
diversity.
Correspondence
Charles Acosta, Department of Biological
Sciences, Northern Kentucky University,
Highland Heights, Kentucky 41099, USA.
E-mail: [email protected]
Accepted: 12 October 2013
doi: 10.1111/maec.12129
Abstract
Certain biodiversity patterns on coral reefs are generally consistent but we still
lack fundamental insight into how assemblages vary across spatially heterogeneous reef systems. We compared fish, coral, and sponge assemblages across a
symmetrical physiographical gradient (windward forereef, lagoon patch reef,
leeward forereef) of the Glover’s Reef atoll, Belize. Species richness of fishes
and corals was highest in the deep habitat (15 m) on the windward forereef.
Sponges were diverse and abundant on both deep windward and leeward forereefs but not on the exposed shallow (5 m) windward forereef. Fish and benthic assemblages were relatively distinct in each reef zone, with the lagoon
patch reef communities consisting of a combination of leeward and windward
species. Nevertheless, there were no clear patterns in community similarity
matrices of fish and benthic assemblages, suggesting that overall coral and
sponge assemblages had weak or no direct association with patterns in fish
assemblages. A closer examination of fish trophic groups indicated that planktivores and predators were predictably associated with depth, whereas herbivores
were associated with shallow protected reefs. None was specifically associated
with spatial location along the atoll gradient. These patterns of diversity distribution are important for identifying spatial conservation priorities. A Marine
Protected Area (MPA) at Glover’s Reef encompasses substantial windward forereef and patch reef habitats. A much lesser extent of protection is afforded the
leeward forereef that supports faunal assemblages that are unique and productive, if not as diverse as the windward forereef. Isolated coral atolls can serve as
ideal systems to study spatial heterogeneity and biodiversity patterns, but more
experimental studies are needed to reveal the mechanistic processes underlying
these patterns.
Introduction
Coral reef ecosystems support highly diverse and productive faunal communities. Occupying less than 0.1% of
ocean surface area, coral reefs may contain up to 40% of
all fish species (Moyle & Cech 2003), as well as representatives of most invertebrate metazoan phyla. Much effort
in community ecology has focused on identifying and
predicting diversity patterns on coral reefs at various
scales. It is expected that reef-building corals facilitate
Marine Ecology (2014) 1–11 ª 2014 Blackwell Verlag GmbH
high diversity of other taxa by enhancing spatial heterogeneity and other ecological factors (Karlson 1999;
Pratchett et al. 2008). Yet, we do not fully understand
spatial zonation patterns of diversity and assemblage
structure within any taxonomic group and, in particular,
correlational patterns between fish and benthic communities.
Reef communities vary along certain physical gradients.
A well-known pattern is zonation of coral species and
morphotypes with wave energy stress (Darwin 1842;
1
Spatial discordance in reef assemblages
Odum & Odum 1955; Goreau 1959; Geister 1977).
Huston (1985) suggested that factors such as wave
energy, light attenuation, and plankton availability associated with depth produce the highest diversity of corals at
intermediate depths, consistent with predictions of the
intermediate disturbance hypothesis (Connell 1978). Species richness has been shown to increase with depth from
near surface to maximum at 10–30 m for both scleractinian corals (Sheppard 1980; Liddell & Ohlhorst 1981;
DeVantier et al. 1998) and gorgonians (Lasker & Coffroth
1983; Dahlgren 1989). Depth and spatial location across
reef gradients may influence morphological variability in
scleractinian corals (Madin & Connolly 2006). This may
also apply to sponges, another important functional component of the reef benthos (Diaz & R€
utzler 2001). Bell &
Barnes (2002) showed that morphological diversity of
sponges was highest at intermediate depths at 10–15 m,
but assemblage patterns were not clearly defined.
Physical stress gradients have also been linked to diversity patterns and community structure of reef fishes. Fish
diversity increases with depth, often peaking at 15–20 m
(Harborne et al. 2006; Friedlander et al. 2010). Fish
assemblage structure can also vary with reef zonation.
High diversity and abundance of planktivores often occur
at intermediate depths on forereefs, whereas herbivores
are dominant on backreef habitat (Friedlander & Parrish
1998). Friedlander et al. (2010) suggested that piscivorous
species are expected to be common across most reef
zones and dominate deeper forereef habitat, but this distribution pattern is generally absent on reefs under
intense fishing pressure.
Establishing associations between diversity of fishes and
diversity of reef benthos has been a more intractable
issue. Heterogeneity of reef benthic habitat, including
corals, seagrasses, and algae, has been correlated with fish
diversity (e.g. Roberts & Ormond 1987; Grober-Dunsmore et al. 2007). Species richness and abundance of
select fish taxa are often correlated with living coral cover
(primarily corallivores such as the Chaetodontidae; Bell &
Galzin 1984; Chabanet et al. 1997; Jones et al. 2004; Bouchon-Navaro et al. 2005; Graham et al. 2006; Pratchett
et al. 2006; Messmer et al. 2011). However, some studies
failed to show a relationship between total fish diversity
and coral diversity at local scales (i.e. a diversity; Luckhurst & Luckhurst 1978; Roberts & Ormond 1987; Gratwicke & Speight 2005; Bellwood et al. 2006). Studies of
fish communities before and after severe disturbances
have revealed complex responses to loss of coral cover,
ranging from decreased species richness to changes in
community composition (see comprehensive meta-analysis by Pratchett et al. 2011). Other studies suggest that
fish diversity varies in proportion to coral diversity at larger scales across seascape gradients (b diversity; Wilson
2
Acosta, Barnes & McClatchey
et al. 2006; Arias-Gonzalez et al. 2008; Belmaker et al.
2008).
Understanding spatial patterns of biodiversity is important for planning effective conservation strategies for
coral reefs (Bellwood et al. 2004). There is a need for further corroboration of patterns of diversity and structure
of whole communities, as well as important associations
between faunal groups. We studied diversity patterns in
fish, coral, and sponge assemblages across a spatial gradient on a geomorphologically symmetrical atoll reef. The
gradient from the lagoon to the forereef on both windward and leeward fronts allowed us to compare assemblages in reef zones that were superficially similar (depth,
slope) but physiographically different (current flow, wave
exposure). We tested several specific hypotheses on spatial patterns in different reef physiographic zones.
H1: Is species richness of each taxon similar within
and among reef zones?
H2: Do species assemblages differ across the windward-leeward atoll gradient?
H3: Is diversity in assemblages correlated between
fishes and benthos (corals and sponges) in any reef
zone?
H4: Is diversity of fish trophic groups associated with
living coral and sponge abundance (percent cover)
or with the physical gradient (depth and windwardleeward location)? Elucidating such patterns has
immediate implications for reserve design and management strategies to protect high diversity assemblages, productive communities, and vulnerable
species in coral reef ecosystems.
Methods
Study area
Surveys were conducted at the Glover’s Reef atoll off the
coast of Belize in the Western Caribbean Sea in the summer months of 2003–2005 (Fig. 1). The atoll is
32 9 12 km along a N–S alignment. It is ringed by an
emergent reef crest except for three major breaks on the
windward side. Both windward and leeward forereefs
slope from the surface to 15–20 m depth, where the vertical reef wall begins. Surrounding depths range from 350
to 1000 m within 2 km from the reef crest. The shallow
coral reef community is thus isolated except for larval
connectivity with the main Belize Barrier Reef and regional reefs and atolls. The central lagoon contains over 700
patch reefs, many of which rise to near the sea surface
Marine Ecology (2014) 1–11 ª 2014 Blackwell Verlag GmbH
Acosta, Barnes & McClatchey
Spatial discordance in reef assemblages
87°45‘0“W
17°0‘0“N
Conservation Zones
200m contour
16°45‘0“N
Fig. 1. Location of the Glover’s Reef atoll in
the Western Caribbean (inset). Surveys were
conducted across the windward–leeward
(○, 5 and 15 m windward forereef; □, 5 and
15 m leeward forereefs; D, 3 m patch reefs)
gradient of the atoll. The geomorphological
cross-section (bottom; not drawn to scale)
shows the physical similarity of the
physiographical zones on the windward and
leeward fronts. The windward forereef
experiences wind and wave exposure during
most of the year, whereas the leeward
forereef is exposed only on occasion mainly
during winter months. The lagoon is
protected by an emergent reef crest with few
breaks.
from the lagoon floor at 2–18 m depth (Wallace & Schafersman 1977).
Prevailing wind direction is typically from the ENE,
except during occasional frontal systems that approach
from the NNW during December to March. Therefore, the
shallow windward forereef experiences vigorous wave
energy most of the year, but the leeward reefs are relatively
calm except occasionally during winter. The Western
Caribbean gyre flows in a southerly direction in this region.
Tidal amplitude is relatively small (<0.5 m). Therefore, the
lagoon is not vigorously flushed on a regular basis.
The atoll is currently zoned for various usages, including a Marine Protected Area (MPA) where fishing is
prohibited (Fig. 1). Established in 1998, the main
Conservation Zone of the MPA is triangular in shape and
encompasses 24% of the atoll area. It incorporates more
than 10 km of the windward reef but less than 2 km of
Marine Ecology (2014) 1–11 ª 2014 Blackwell Verlag GmbH
the leeward reef. Commercial fishing activity is primarily
focused on benthic invertebrates (spiny lobster Panulirus
argus and queen conch Strombus gigas; Acosta 2002), but
high value fish species (e.g. lutjanids, serranids) are often
targeted by spearfishing or handline fishing. The use of
fish traps, trawling, and other destructive fishing practices
is prohibited. Many of the shallow patch reefs in the
lagoon have undergone a significant phase shift from
coral-dominated to algal-dominated (McClanahan &
Muthiga 1998). However, the underlying cause for this
disturbance is still not well understood.
Field surveys
Reef communities were surveyed across the windward–
leeward gradient of the atoll (Fig. 1). Five reef
physiographic zones were sampled: (i) windward forereef
3
Spatial discordance in reef assemblages
at 15 m depth near the reef wall (six sites); (ii) windward
forereef at 5 m (seven sites); (iii) lagoon patch reefs at 2–
3 m (nine sites); (iv) leeward forereef at 5 m (eight sites);
(v) leeward forereef at 15 m (six sites). Depths of sites
were determined using a hand-held depth sounder, and
locations were mapped using global positioning satellite
(GPS) coordinates. Replicate sites within a reef zone were
separated by a minimum of 1 km.
Pairs of divers using SCUBA surveyed fish and benthic
communities along transects parallel to the N–S reef
alignment. One diver swam 2–3 m above the reef and
used a digital video camera to record all fishes in a 5-m
wide belt transect. The second diver simultaneously
placed a 10-m transect tape tautly over the benthic substratum. The second diver used the video camera to
record the benthos 1 m on both sides along the transect
tape (i.e. a 2-m belt transect). The first diver then conducted stationary visual surveys for cryptic or resting
nocturnal fishes in large coral heads and other crevice
shelters; three 5-min observations were done along each
transect. The recorded video and data sheets were later
transcribed in the laboratory.
Fishes were identified to species level (B€
ohlke & Chaplin 1993), and the abundance of each species was enumerated for each transect. Fishes were also classified into
general trophic groups (piscivores, herbivores, omnivores,
planktivores, corallivores) based on available life history
information. Species known to occasionally feed on
sponges (i.e. angelfishes, boxfishes, filefishes; Pawlik 1998)
were placed with the omnivores. Corals and sponges were
also identified to species level (Humann 1994a,b). Our
species data for the benthos is conservative and likely to
underestimate true diversity because of phenotypic plasticity, which requires microscopic analysis, especially for
the sponges (Diaz & R€
utzler 2001).
Data analysis
We first examined species richness graphically using rarefaction curves and their 95% confidence intervals (Colwell et al. 2012). The null hypothesis was that species
richness of fishes, corals, and sponges was not significantly different in the reef physiographic zones. Abundance data were pooled from transects in each of the five
zones, and the expected number of species was estimated
from 1000 permutations. Rarefaction curves were also
used to assess whether any zone was insufficiently sampled. The number of common species (encountered in all
zones) and rare species (encountered in one zone only)
was also examined graphically. Estimates of b diversity
were calculated as Whittaker’s bW on presence–absence
data (Koleff et al. 2003) for the overall windward–leeward
gradient and between pairs of adjacent reef zones.
4
Acosta, Barnes & McClatchey
To further compare assemblages of faunal groups
within and among reef zones, we used non-metric multidimensional scaling (nMDS) on Bray–Curtis matrices
using raw abundance data (Quinn & Keough 2002). Separate tests were conducted on fish, coral, and sponge
communities. Analysis of similarities (ANOSIM; Clarke
1993) was then used to corroborate significant differences
in assemblage structure between pairs of reef zones. Similarity percentages (SIMPER; Clarke 1993) were used to
identify the species with the most influential abundance
patterns between reef zones.
We then assessed whether any particular fish and benthic assemblages were correlated in a reef zone. We used
partial Mantel tests on Bray–Curtis matrices to test the
null hypothesis that fish assemblages are not correlated to
coral assemblages, controlling for sponge assemblage in
each reef zone. P-values were calculated from Monte Carlo permutation tests on correlations between two matrices
(Manly 2006). Only those species present in at least one
sample in a zone (i.e. non-zero abundances) were
included in the matrix.
To determine whether the distribution of fish species
diversity by trophic group was predictable across the atoll
gradient, we compared trophic groups with percent cover
of living corals and sponges, reef depth, and location on
the windward–leeward gradient. Canonical correspondence analysis (CCA) was conducted on Shannon H’
diversity indices for fish trophic groups scaled with the
three environmental variables at each zone. Permutation
tests on trace statistics were non-significant for all tests.
We started with the neutral assumption that all observed
fish species in a zone were part of the community,
regardless of whether a species could be regarded as a
transient or a habitat specialist. The life histories (including home ranges, habitat specificity, and other factors)
are not well known for a substantial number of reef fish
species, so we considered all observed species part of the
zonal assemblage. Trophic groups were broadly categorized as piscivores, herbivores, omnivores, and planktivores. Due to low non-zero abundances of three species
of known corallivores, this group was not included in the
final analysis; a strong positive relationship between corallivore diversity and live coral cover is well established
in previous studies (see Introduction).
Results
Patterns in species richness
A diverse fish and benthic fauna inhabited shallow reef
habitats of the Glover’s Reef atoll. We documented 108
species of fish and, at least 49 species of corals and 33
species of sponges in less than 1 ha of reef surface area
Marine Ecology (2014) 1–11 ª 2014 Blackwell Verlag GmbH
Acosta, Barnes & McClatchey
Spatial discordance in reef assemblages
(Table 1). We identified 36% (26 species) of 72 scleractinian corals listed by Humann (1994a) for the tropical
Western Atlantic. By comparison, we sampled 61% of
sponge species and 24% of reef fish species (excluding
pelagics like sharks) listed by Humann (1994b,c). The
deep windward forereef at 15 m had more rare species
(encountered in one zone only) of fishes and corals than
other zones, but there were more rare species of sponges
on the deep leeward forereef (Fig. 2). Rarefaction curves
indicated that sampling was adequate for corals and
sponges at most sites, but the slopes of some rarefaction
curves for fishes were still increasing, indicating some
underestimation (Fig. 3).
Fishes
80
Table 1. Summary of fish, coral, and sponge fauna sampled at the
Glover’s Reef atoll, Belize. Corals include both scleractinians and gorgonians. Sponges are listed as ‘Individuals’ but existed in complex
forms including encrusting, boring, and multi-branched/tube. The
Total column shows absolute values for all sites across the atoll; the
number of species/families does not match because of common taxa
found in more than one zone. Zone designations are windward forereef at 15 m (WFR15), windward forereef at 5 m (WFR5), lagoon
patch reefs at 3 m (PR3), leeward forereef at 5 m (LFR5), and leeward
forereef at 15 m (LFR15).
60
40
WFR5
WFR15
LFR5
LFR15
PR3
20
0
0
number
of
WFR15
WFR5
PR3
LFR3
LFR15
total
Individuals
Species
Families
Colonies
Species
Families
Individuals
Species
Families
935
73
26
1301
43
15
318
20
6
699
59
21
793
49
15
60
5
5
948
58
19
1220
30
13
451
22
2
953
56
15
1826
36
14
228
18
4
583
45
15
1121
34
14
268
23
3
4118
108
34
6261
49
16
1325
33
12
sponges
60
600
800
1000
40
30
20
10
0
0
Fish
Coral
Sponge
50
Number of species
Expected species richness
corals
400
Corals
50
fishes
200
400
600
800
1000 1200 1400 1600 1800
Sponges
25
40
200
20
30
15
20
10
10
5
0
Common
WFR5
WFR15
LFR5
LFR15
PR
Rare
Species distribution
0
0
100
200
300
400
Abundance
Fig. 2. Comparison of the ubiquity of species of fishes, corals, and
sponges at the Glover’s Reef atoll. Graph shows the number of
common species encountered in all zones versus rare species found in
only one reef zone. Zone designations are windward forereef at 5 m
(WFR5), windward forereef at 15 m (WFR15), leeward forereef at
5 m (LFR5), leeward forereef (LFR15) and lagoon patch reefs at 3 m
(PR3).
Marine Ecology (2014) 1–11 ª 2014 Blackwell Verlag GmbH
Fig. 3. Rarefaction curves for expected species richness (1000
permutations) for fishes, corals, and sponges at the Glover’s Reef
atoll. To maintain clarity, 95% confidence limits are not shown, but
limits were significantly different only for fishes and for corals at site
WFR15. There was a paucity of sponges on the shallow windward
forereef at 5 m. Zone designations are as listed in Fig. 2.
5
Spatial discordance in reef assemblages
Patterns in community assemblages
Taken as whole assemblages, there were distinct distributional patterns within faunal assemblages across the atoll
gradient (H2). Although there was some overlap in
similarity of fish assemblages, the nMDS plot shows clus6
1.0
Fishes 0.71
Corals 0.37
Sponges 0.74
0.8
0.6
bW
Expected fish species richness was highest on the deep
windward forereef at 15 m, with about 3.6 species
encountered for every 25 individuals sampled (Fig. 3).
This was significantly different (at the 95% confidence
limit) from species richness on the deep leeward reef at
15 m (2.6 species per 25 individuals). Confidence limits
overlapped for all zones except for the deep windward
reef. Species richness for corals was also higher with marginal significance on the deep windward forereef, with
one new species expected for every 46 colonies encountered (Fig. 3). At the local scale, this reef zone was very
heterogeneous in species composition, ranging from
dense thickets of branching corals (Acropora cervicornis,
Acropora palmata), diverse gorgonian stands, and a variety of small mound corals. In contrast, the leeward forereef was dominated by a few species of very large mound
corals (Montastraea annularis, Montastraea cavernosa,
Diploria labyrinthiformes). The leeward forereef also had
higher average percent cover per transect (35%) relative
to the windward forereef (29%). Sponge species richness
was also highest on the deep forereefs, with the highest
species richness and abundance on the deep leeward forereef (Fig. 3). The patch reef environment also had a relatively diverse sponge community consisting of species
found on both shallow and deep forereefs.
Estimates of species turnover based on presence–
absence data indicated that the sponge fauna on the
windward forereef differed from that on the other reef
zones (Fig. 4). This was due primarily to the low number
of species in the wave-exposed shallow windward forereef
at 5 m. This species-poor site is primarily characterized
by coral spur-and-groove formations and experiences the
highest wave energy from prevailing winds, tropical
storms, and backflow. When the shallow windward forereef zone is removed and species turnover is recalculated,
bW ranges from 0.28 to 0.35 between the deep windward
forereef and the other reef zones. This is well within the
b diversity range for the coral and fish fauna among all
zones. The species turnover patterns then becomes similar
among all three faunal groups, suggesting more dynamic
assemblages on the windward forereef, with the lagoon
patch reefs as a transition zone. On the basis of these
results, the species richness (H1) of fishes and corals was
significantly higher on the deep windward forereef but
sponges were consistently diverse and abundant on the
deep leeward forereef.
Acosta, Barnes & McClatchey
0.4
0.2
0.0
WFR15 ----- WFR5 ------ PR3 ------ LFR5 ------ LFR15
Reef zone
Fig. 4. Comparison of species turnover (b diversity) across the
windward–leeward gradient at the Glover’s Reef atoll. Whittaker’s b
(bW) is calculated using presence–absence data for pairs of adjacent
reef zones, 0 = no difference in species assemblages to 1 = 100%
difference in assemblages. Sponge species turnover was impacted by
the low diversity on the shallow windward forereef (WFR5); with this
outlier removed, bW estimates between WFR15 and other zones were
reduced to 0.28–0.35. Global bW for the windward–leeward gradient
are shown next to each plot. Zone designations are as listed in Fig. 2.
tering of windward reefs with some separation from the
cluster of leeward and patch reefs (Fig. 5). ANOSIM tests
support this general pattern (overall R = 0.30; P < 0.001)
with significant differences in assemblages on windward
versus leeward/patch reefs, as well as between windward
shallow and windward deep reefs (Table 2). SIMPER
comparisons indicate that this pattern is due to numerical
dominance of a relatively few species, namely bluehead
wrasse Thalassoma bifasciatum and bicolor damselfish
Stegastes partitus on windward reefs. Blue chromis Chromis cyanea were ubiquitous on deeper forereef habitats.
Large schools of blue tang Acanthurus coeruleus were frequently encountered on shallow windward forereefs but
were rare on leeward forereef or lagoon patch reefs.
Coral assemblages showed an even stronger distribution pattern between windward and leeward reefs (Fig. 5).
Patch reef assemblages again appeared to have some similarity with leeward reef assemblages (AnoSim overall
R = 0.71; P < 0.0001; Table 2). Gorgonian diversity
(Pseudopterogorgia spp., Gorgonia spp.) was particularly
high on windward reefs relative to other sites, whereas
calcareous hydrozoa Millepora, sea rods Eunicea, and
mound corals were abundant on leeward and patch reefs.
Sponge assemblages on lagoon patch reefs were relatively
distinct from any particular forereef assemblage, but this
may be an artifact of patch reefs having many species in
common with both windward and leeward reefs (Fig. 5).
The abundance of erect rope Amphimedon compressa,
brown variable Anthosigmella varians, and scattered pore
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Acosta, Barnes & McClatchey
Spatial discordance in reef assemblages
Table 2. Results of ANOSIM tests on Bray–Curtis distance matrices of
fish, coral, and sponge assemblages at the Glover’s Reef atoll. Overall
R coefficients indicate strong separation (>0.75), some overlap (0.75–
0.25) or no separation (<0.25). Shown are Bonferroni-corrected P-values for significant correlations between pair of zones across the windward–leeward gradient. Zone designations are as described in
Table 1.
0.3
Fishes
0.2
0.1
0.0
WFR5
WFR15
LFR5
LFR15
PR3
–0.1
–0.2
Stress = 0.23
–0.3
–0.3
–0.2
–0.1
0.0
0.1
0.2
0.3
0.4
0.4
Corals
0.3
Axis 2
0.2
0.1
0.0
–0.1
–0.2
Stress = 0.19
–0.3
–0.3
–0.2
fisha
WFR15
WFR5
PR
LFR15
LFR5
coralb
WFR15
WFR5
PR
LFR15
LFR5
spongec
WFR15
WFR5
PR
LFR15
LFR5
WFR15
WFR5
PR
LFR15
0.0188
0.0008
0.0051
0.0004
0.0001
0.0024
0.0015
0.1665
0.0762
0.243
0.085
0.006
0.03
0.007
0.008
0.027
0.012
0.016
0.003
0.007
0.139
0.011
0.066
0.585
0.008
0.07
1
0.042
0.14
1
LFR5
Overall R = 0.30; P < 0.001.
Overall R = 0.71; P = 0.0001.
c
Overall R = 0.38; P = 0.0001.
a
–0.1
0.0
0.1
0.2
0.3
0.3
Sponges
b
0.2
0.1
0.0
–0.1
–0.2
Stress = 0.14
–0.3
–0.3
–0.2
–0.1
0.0
0.1
0.2
0.3
Axis 1
Fig. 5. Non-metric multidimensional scaling (nMDS) plots are shown
for fishes, corals, and sponges at the Glover’s Reef atoll across reef
physiographical zones. Log and square-root transformation of the
data did not improve stress, so raw data were used in all simulations.
Follow-up ANOSIM tests largely corroborated these patterns (see
Table 2). Zone designations are as listed in Fig. 2.
sponge Aplysina fulva mainly contributed to the distinctiveness of the sponge assemblage in patch reef habitat
(overall ANOSIM R = 0.38; P < 0.001).
We found no direct association patterns between fish
and benthic assemblages in any reef physiographic zone
(H3). Partial Mantel correlations between fish and coral
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Bray–Curtis matrices (controlling for sponge assemblages)
were non-significant for all reef zones (Table 3). This was
supported by our examination of the distribution of fish
trophic groups across the environmental gradients of live
coral/sponge cover, depth, and windward–leeward site
location (H4). With corallivores removed, only omnivorous fishes showed a strong relationship with percent
cover of live corals and sponges (Fig. 6). Planktivores,
and to a lesser extent piscivores, were associated with
increasing depth, whereas herbivorous species were associated with shallow reef habitats. No fish trophic groups
were specifically associated with spatial location on the
leeward–windward reef gradient.
Discussion
Coral reefs are highly heterogeneous ecosystems with
complex physical structure and biotic interactions. Even
so, the atoll configuration at Glover’s Reef was amenable
to a comparison of species richness and assemblage patterns in diverse reef habitats across a windward–leeward
physiographical zonation. Exposure to such physical stress
gradients may influence corals and associated communities in predictable ways (Huston 1985). The diversity of
7
Spatial discordance in reef assemblages
Acosta, Barnes & McClatchey
Table 3. Partial Mantel tests on Bray–Curtis distance matrices for correlations between fish and coral assemblages, controlling for sponge
assemblages. Only species present on at least one transect in a zone
were used in the matrix. Partial R correlations are calculated from
5000 permutations. P-value represents the probability that the matrices are not correlated. Zone designations are as defined in Table 1.
LFR15
partial R
P-value
0.373
0.8056
LFR5
WFR15
0.3529
0.1014
0.3173
0.0788
WFR5
PR3
0.2268
0.7656
0.2226
0.1968
0.06
Substratum percent cover
Depth
0.04
Omnivores
0.02
Planktivores
Axis 2
0.00
Piscivores
–0.02
Herbivores
–0.04
–0.06
–0.08
–0.10
–0.3
Windward-Leeward gradient
–0.2
–0.1
0.0
0.1
0.2
0.3
Axis 1
Fig. 6. Canonical correspondence analysis (CCA) biplot is shown for
diversity of fish trophic groups (Shannon Hʹ) against environmental
variables at the Glover’s Reef atoll. Environmental variables were
substratum percent cover of live corals and sponges, depth (3, 5, and
15 m), and spatial position on the windward–leeward gradient
(shallow and deep windward forereef, lagoon patch reef, shallow and
deep leeward forereef). Omnivores include occasional spongivores.
Corallivores were removed from the analysis due to low abundances.
Planktivores were associated with the depth gradient, whereas the
greatest diversity of herbivores was found in shallow habitat.
Omnivorous species were distributed with increasing live coral–
sponge percent cover. Zone designations are as listed in Fig. 2.
corals is expected to be low near the surface with high
wave energy and ultraviolet exposure, and in deep habitats where light becomes limiting.
At Glover’s Reef, the windward forereef at 15 m had
the highest species richness of corals compared with
other reef zones. This is consistent with patterns of coral
diversity peaking at depths of less than 20 m in studies
of various forereef ecosystems (Geister 1977; Sheppard
1980; Liddell & Ohlhorst 1981; Huston 1985; DeVantier
et al. 1998). However, this pattern was not repeated on
the leeward forereef, which is structurally similar to the
windward forereef but less exposed to wave and storm
stresses. Instead, older massive colonies of important
reef-builders such as Montastraea and Diploria were
dominant on both shallow and deep leeward reefs. These
8
types of species are important for providing structural
habitat for other taxa and for coral recruit production
(DeVantier et al. 1998). As such, reliance on species
richness alone as a conservation metric would likely
result in undervaluing this productive leeward coral
community.
Sponges were also highly diverse and abundant on the
leeward forereef, as well as the deep windward forereef.
Sponges with larger robust morphologies, such as barrel
sponge Xestospongia and vase sponge Callyspongia, were
abundant in the deeper habitats. These large sponges may
provide important structural habitat, similar to the role
of massive mound corals. Indeed, Arias-Gonzalez et al.
(2008) also found that a high diversity of fishes was associated with high sponge diversity in deeper forereef habitat. The patch reefs at 3 m depth in the Glover’s Reef
lagoon harbored diverse assemblages of sponges, having
many species in common with the forereef. Only a few
species, dominated by encrusting and boring sponges,
occupied the shallow windward forereef where wave stress
was maximum.
The literature on coral reef fish diversity has grown
extensively in recent years. The diversity of reef-associated
fishes is predictably higher on larger three-dimensional
reef structure than on low-relief reefs (e.g. Chabanet et al.
1997; Friedlander & Parrish 1998; Acosta & Robertson
2002; Gratwicke & Speight 2005; Arias-Gonzalez et al.
2008) or reefs undergoing degradation due to loss of reefbuilding corals (Jennings et al. 1996; Findley & Findley
2001; Jones et al. 2004; Graham et al. 2006). Similarly, the
diversity of reef-dwelling invertebrates has also been
shown to increase with the complexity of reef habitat (Idjadi & Edmunds 2006). Physical factors such as wave
energy exposure may also structure some fish assemblages,
such as small cryptic species (Depczynski & Bellwood
2005). Fish species richness and abundance commonly
peak at intermediate depths of 10–20 m, increasing from
backreef to deep forereef (Friedlander & Parrish 1998;
Arias-Gonzalez et al. 2008; Friedlander et al. 2010). In our
study, the windward forereef at 15 m had the highest
diversity of fishes, whereas the leeward forereef had lower
diversity. Friedlander et al. (2010) noted that windward
and leeward forereefs of the Kingman Reef atoll in the
Pacific had similar fish species richness and abundance,
but the configuration and exposure gradient appear to be
different from those at the Glover’s Reef atoll. Our data
also did not reveal any clear patterns of increasing diversity from lagoon patch reefs to the deep forereef. In fact,
the fish fauna was relatively diverse and abundant on
lagoon patch reefs (see also Acosta & Robertson 2002;
Karnauskas et al. 2012). Similarity metrics for fishes and
corals within any zone were not correlated, suggesting that
overall patterns in assemblage structures were not directly
Marine Ecology (2014) 1–11 ª 2014 Blackwell Verlag GmbH
Acosta, Barnes & McClatchey
associated with each other. This does not necessarily contradict evidence that fish communities respond negatively
to a decline in coral cover, as this is often a lagged
response to disturbances (Wilson et al. 2006).
Among fish assemblages, our observations agreed with
previous studies that show plankivorous reef fishes and
predators are associated with the depth gradient, and herbivorous fishes are associated with shallower reef habitat
(Gladfelter et al. 1980; Friedlander et al. 2010). However,
there were no clear relationships between fish trophic
groups and spatial location across the atoll windward–leeward gradient. This might simply reflect selective pressure
for feeding strategies being dictated at the local habitat
level rather than along this particular spatial gradient.
The lagoonal patch reefs at Glover’s Reef had diverse
communities of fishes and sponges but depauperate coral
communities. Hundreds of the shallowest patch reefs
have undergone a drastic ecological phase shift in which
turf algae have replaced corals over the last three decades
(McClanahan & Muthiga 1998). We specifically chose
patch reefs sites at a deeper depth to survey the remaining coral and sponge communities in the lagoon. Corals
occupying the lagoon patch reefs consisted of more gorgonians than scleractinians. Overall coral diversity was
lower than in other reef zones and qualitatively much
lower than in early reports (Wallace & Schafersman 1977;
McClanahan & Muthiga 1998). It is likely that the fish
and sponge communities will also deteriorate with loss of
scleractinian corals as reef erosion exceeds reef building.
It is widely accepted that coral reef MPAs often have
positive impacts on fish diversity and biomass which, in
turn, have positive influences on benthic community
structure (e.g. Newman et al. 2006). Fishing impacts in
and around the MPA at Glover’s Reef have not been
quantified, and so the impacts on diversity and abundance of various fish trophic levels are unknown. While
macroalgal dominance on shallow patch reefs in the
lagoon is problematic, our work shows that the deeper
patch reefs still contain vital and dynamic communities
of fishes, sponges, and some corals such as gorgonians.
Additionally, the relatively diverse and productive deeper
forereef communities likely function as sources of recruitment to all habitats of the atoll. Both windward and leeward environments contain unique faunal assemblages
with high conservation value. With proper management
and areal coverage of protection, these reefs provide
insurance for continued resilience and rehabilitation of
stressed reefs in the regional ecosystem.
Conclusions
Assemblages of fishes, corals, and sponges were relatively
distinct on similar reef physiographic zones across a
Marine Ecology (2014) 1–11 ª 2014 Blackwell Verlag GmbH
Spatial discordance in reef assemblages
windward–leeward spatial gradient. The high diversity of
branching, encrusting, and other coral morphotypes on
the windward forereef was replaced by fewer species,
dominated by older massive mound and boulder corals
on the leeward reef. Fish species richness also peaked on
the deeper windward forereef but overall zone-specific
diversity patterns did not correlate well with diversity of
corals and sponges. Sponge assemblages were highly
diverse on more sheltered reefs, especially on the leeward
exposure. Coral species richness patterns are consistent
with predictions of the intermediate disturbance hypothesis (Connell 1978; Huston 1985) but where depth is less
important than exposure between the dynamic windward
forereef and the sheltered leeward forereef. However, patterns in fish and benthic assemblages are not in general
agreement. Coral and fish diversity is high on deeper
windward forereefs, but this does not diminish the
importance of the deeper leeward habitat, where sponge
diversity is very high. We need to move beyond simplifying assumptions (e.g. fish–coral correlations) to a more
wholistic and encompassing perspective of reef ecosystems.
Acknowledgements
This research was funded by grants to C.A. from the Global Conservation Program of the Wildlife Conservation
Society. R.M. and R.B. were funded by Northern Kentucky University Greaves Research Fellowships. We thank
Janet Gibson and the staff of the Glover’s Reef Research
Station at Middle Cay for excellent logistical support.
Danny Westby and Andrew Branson provided invaluable
field assistance. We thank two anonymous reviewers
whose suggestions greatly improved the manuscript. The
authors declare that there are no conflicts of interest
associated with this paper.
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