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Faunal breaks and species composition
of Indo-Pacific corals: the role of
plate tectonics, environment and
habitat distribution
S. A. Keith1, A. H. Baird1, T. P. Hughes1, J. S. Madin3 and S. R. Connolly1,2
Research
Cite this article: Keith SA, Baird AH, Hughes
TP, Madin JS, Connolly SR. 2013 Faunal breaks
and species composition of Indo-Pacific corals:
the role of plate tectonics, environment and
habitat distribution. Proc R Soc B 280:
20130818.
http://dx.doi.org/10.1098/rspb.2013.0818
Received: 2 April 2013
Accepted: 30 April 2013
Subject Areas:
ecology
Keywords:
biogeography, colonization, macroecology,
metacommunity, nestedness, coral
Author for correspondence:
S. A. Keith
e-mail: [email protected]
Electronic supplementary material is available
at http://dx.doi.org/10.1098/rspb.2013.0818 or
via http://rspb.royalsocietypublishing.org.
1
Australian Research Council Centre of Excellence for Coral Reef Studies, and 2School of Marine and Tropical
Biology, James Cook University, Townsville, Queensland 4811, Australia
3
Department of Biological Sciences, Macquarie University, Australia, New South Wales 2109, Australia
Species richness gradients are ubiquitous in nature, but the mechanisms that
generate and maintain these patterns at macroecological scales remain unresolved. We use a new approach that focuses on overlapping geographical
ranges of species to reveal that Indo-Pacific corals are assembled within 11
distinct faunal provinces. Province limits are characterized by co-occurrence
of multiple species range boundaries. Unexpectedly, these faunal breaks are
poorly predicted by contemporary environmental conditions and the present-day distribution of habitat. Instead, faunal breaks show striking
concordance with geological features (tectonic plates and mantle plume
tracks). The depth range over which a species occurs, its larval development
rate and genus age are important determinants of the likelihood that species
will straddle faunal breaks. Our findings indicate that historical processes,
habitat heterogeneity and species colonization ability account for more of
the present-day biogeographical patterns of corals than explanations based
on the contemporary distribution of reefs or environmental conditions.
1. Introduction
More than 100 hypotheses have been proposed to explain the systematic
changes in species richness across latitude, longitude, altitude and depth,
which generate gradients in biodiversity [1,2]. The need to understand the genesis and maintenance of such patterns is becoming ever more urgent as we seek
to manage the effects of global environmental change on biodiversity [3]. However, despite the plethora of hypothesized explanations, the underlying
mechanisms driving these patterns are elusive [4,5]. The species (and genus)
richness of reef-building corals in the Indo-Pacific exhibits a peak in biodiversity in the Indo-Australian Archipelago (IAA), with a gradual decline in
richness with increasing distance from the IAA hotspot, particularly in the
highly depauperate eastern Pacific and at higher sub-tropical latitudes [6–11].
Multiple explanations have been proposed for this pattern, including hypotheses pertaining to ambient energy, habitat availability, dispersal limitation,
geometric constraints and evolutionary time [7,8,12–14]. Some degree of
empirical support has been offered for most of these hypotheses [8,14]. However, disentangling the relative importance of these different underlying
processes remains a significant challenge.
The standard approach to evaluating competing hypotheses has been to investigate relationships between species richness and variables that serve as surrogates
for the hypothesized mechanisms (e.g. temperature) using multiple regression and
related techniques. However, this approach suffers from important limitations [1].
Foremost among these is that species richness is correlated with predictions of
multiple hypotheses (i.e. multicollinearity). For example, in the Indo-Pacific,
coral species richness is correlated with sea surface temperature (SST), habitat
area, distance from the mid-domain [8] and with surrogate variables for historical
& 2013 The Author(s) Published by the Royal Society. All rights reserved.
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potential explanatory variables. To complement this approach,
we also assess whether species traits indicative of environmental tolerance, dispersal ability and evolutionary histories
can provide further evidence for potential causes of abrupt
change in species composition between faunal provinces.
2. Methods
(a) Coral range data
(b) Biogeographical structure
To identify how coral species composition changes through
space within the Indo-Pacific, the spatial structure of scleractinian
coral species distributions was quantified using elements of
metacommunity structure (EMS) analysis [24,25]. EMS analysis
discriminates between six idealized patterns for multiple species
distributions (random, checkerboard, Clementsian, Gleasonian,
nestedness, evenly spaced) according to three elements (coherence, species replacement, species range boundary clumping)
of a sites-by-species matrix (see the electronic supplementary
material, methods (a)). The estimate of the coherence element is
biased when species with a range size of one site are included
[26], so we removed all singular occurrences (n ¼ 13; less than
2% of the total species), slightly reducing our dataset to 719
species. The estimate of species turnover within EMS analysis
is prone to error [27], so we additionally calculated the more
robust nested measure based on overlap and decreasing fills
(NODF) metric [28]. Distinct faunal provinces and associated
faunal breaks were identified and mapped on the basis of the
EMS output with a distance-based method for cluster analysis
(see the electronic supplementary material, methods (b), [29]).
(c) Geological, habitat and environmental clusters
We examined the co-location of faunal breaks with abrupt transitions in contemporary environmental conditions, present-day
spatial distribution of reef habitat and broad-scale geological
features. We identified geological clusters according to transitions in features indicative of different geological histories,
which, if co-located with faunal breaks, would suggest that
species distributions reflect long-term colonization, extinction
or speciation processes. These geological clusters were defined
by the extent of major tectonic plates [30] and mantle plume
tracks [31 – 33], which share a similar geological history
([31,34,35]; electronic supplementary material, methods (e)). To
account for the possibility that reefs on the same plate may
have a different geological history due to the formation of
more recent mantle plume tracks, we assigned an intermediate
geological distance value to reflect similar ancient ( plate), but
dissimilar recent (track), geological history. We used a similar
rule for analysing reefs along the Reunion mantle plume track
that straddles the African and Indian plates i.e. reefs that share
the track were assumed to have a similar geological history.
To investigate whether present-day spacing of reef habitat
(potentially creating barriers to dispersal) is important, we
Proc R Soc B 280: 20130818
Our primary data consist of detailed maps of reefs and of the
ranges of 732 scleractinian coral species. We compiled a database
of digitized geographical range extents of Indo-Pacific coral
species [22]. Individual reefs ([23; n ¼ 6919; electronic supplementary material, dataset S1]) were aggregated within a
radius of 100 km to produce 290 aggregated reef groups or
sites (see the electronic supplementary material, dataset S2) to
reduce false presences and to avoid exceeding the computational
memory limits of ArcGIS during analysis. The species composition was determined for each site, and a sites-by-species
incidence matrix was generated for analysis.
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processes [14]. A more recent approach involves modifying null
models of random placement of species ranges in the biogeographical domain, such that range placement is weighted
according to environmental conditions [15]. However, these
weighted randomizations also suffer from important limitations, primarily due to the use of empirical range size
frequency distributions. Such issues have led to calls for new
approaches to distinguish among the mechanisms that underpin patterns of biodiversity [1,4,16].
One approach that could improve the capacity to discriminate between competing hypotheses in biogeography is an
expansion in focus from counts of species towards species
composition more broadly (i.e. changes in species identities
as well as species richness over geographical space) [1,7].
Marine biogeographical zones have been recognized in previous work as reflecting changes in species composition
[17,18]. However, delineation of these zones has tended to be
subjective, and few of these earlier studies have focused on
the potential reasons for such large-scale changes across
faunal boundaries. A more rigorous quantitative approach to
the spatially explicit quantification of taxonomic composition
has the potential to evaluate a richer set of predictions. Specifically, using species composition rather than species richness
alone also allows investigation of how different traits of individual species influences where they reach their range
boundaries and why range boundaries can co-occur to create
provincial boundaries. For example, if dispersal limitation
drives biogeographical patterns, then species traits that influence susceptibility to dispersal barriers should be good
predictors of the locations of range limits [19]. Therefore, a
focus on species composition and distribution through space
can complement analyses focusing on species richness alone,
and afford stronger tests of macroecological hypotheses [16].
An implicit assumption of many studies of diversity gradients is that species distributions are in equilibrium with
contemporary abiotic conditions and the current geographical
distribution of habitat. However, transient non-equilibrium
dynamics can result in mismatches between present-day abiotic
conditions and species distributions (e.g. lags in ongoing species
range shifts in response to anthropogenic climate change [19,20]).
Consequently, explanations for species distributions may require
consideration of historical processes as well as contemporary
environmental conditions. Within the Indo-Pacific, the influence
of historical processes has received some attention in previous
work: the region of highest species richness has shifted westwards over time, from the Mediterranean approximately
40 Ma to its present location in the IAA [21]. This suggests that
the influence of long-term processes may be apparent in the
structure of present-day Indo-Pacific biodiversity patterns.
Here, we use biogeographical patterns of species composition across 290 sites throughout the Indo-Pacific to more
comprehensively evaluate competing hypotheses that seek to
explain the diversity gradients of reef-building scleractinian
coral species. Specifically, we quantify spatial patterns in
species composition (n ¼ 719) and the extent to which range
limits co-occur among species. We then examine those patterns
to determine the influence of three potential causes that could
generate and maintain biogeographical structure: contemporary environmental conditions, the present-day spatial
distribution of reef habitat and geological history. Our
approach identifies zones of abrupt change (breaks) in species
composition, and assesses the extent to which the location of
those breaks is consistent with geographical patterns in the
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(d) Species traits
We collated eight traits for each of 480 species for which information is available (67% of the species in the EMS analysis,
electronic supplementary material, dataset S3), and tested whether
any of these traits consistently conferred a higher or lower probability that a species would straddle faunal breaks. Coral species
at faunal breaks may be selectively filtered out of the species pool
by declines in the variety of available habitat types (i.e. habitat heterogeneity [43]), in which case we would expect generalist species
to be more likely to traverse breaks. We evaluated this expectation
using three species traits: depth range, wave exposure tolerance and
turbidity tolerance. Depth range was measured in 10 m increments
from 0–10 m to more than 50 m, after Carpenter et al. [44]. Wave
and turbidity tolerance were collated from Diaz & Madin [45].
We also considered four reproductive traits that are associated with dispersal ability: reproductive mode (brooder versus
spawner), the nutritional mode of larvae, indicated by the presence or absence of symbiotic zooxanthellae, egg size and
sexuality (gonochore versus hermaphrodite). If dispersal limitation has acted individualistically on setting the range limits of
coral distributions, we would expect the species that possess
3. Results
(a) Biogeographical structure
Our analysis of spatial patterns in coral species composition
identified nine faunal provinces throughout the Indo-Pacific,
within which species composition was distinct, separated by
faunal breaks where multiple species reached their geographical
range limits (figure 1a). The provinces were significantly nested
(see the electronic supplementary material, table S1; EMS p ,
0.001; NODF ¼ 74.99, p , 0.001), which indicates that the loss
of species through space occurs in a predictable sequence such
that depauperate provinces comprise a subset of species present
within adjacent more species-rich provinces [52]. In addition,
species range limits co-occurred more frequently than expected
by chance (Morisita’s index # 15, p , 0.001). The most speciesrich province is centred on Indonesia and the Philippines
(figure 1a). The additional eight provinces, from west to east,
are: the Persian Gulf, Africa–India, Australia, Japan–Vietnam,
3
Proc R Soc B 280: 20130818
our approach takes better implicit account of spatial autocorrelation within the data, by preserving both the ordering of sites in
the sites-by-species matrix (which arises from the spatial structure in species composition), and the size distribution of
provinces. We adjusted for multiple tests using the formula
a* ¼ 1 2 (1 2 a)1/n, where a* is the corrected alpha level, a is
the critical value (0.05) and n is the number of comparisons.
traits associated with greater dispersal abilities to be the most
likely to traverse faunal breaks. For broadcast-spawning coral
species, egg size is a proxy for development rate, because small
eggs develop more rapidly [46]. Spawning species were placed
in five categories of egg size ranging from less than 100 mm to
more than 500 mm. Brooding species have an instantaneous
development rate because larvae are ready to settle upon release
[47] and, therefore, constituted an additional category that
represented the fastest development rate.
The range sizes of coral species have been hypothesized to be
larger for older taxa ([10], but see [13]). If so, older species might
be more likely to straddle faunal breaks. To test this hypothesis,
we included the species trait of genus age, as determined from
the fossil record (species level ages cannot be obtained reliably
[48]). Age was partitioned into six categories (0–19, 20–39,
40–59, 60–79, 80–99 and more than or equal to 100 Ma) reflecting
precision in the available estimates (Paleobiology Database, http://
paleodb.org; M. Kosnik 2006, unpublished data).
The likelihood of species with particular traits consistently crossing faunal breaks was analysed with a generalized linear mixed
model (GLMM; electronic supplementary material, methods (g)).
The model included three random effects: faunal break, clade [49]
and suborder [50]; the latter two were nested and included to account
for any phylogenetic non-independence that was not explicitly captured within sexuality or genus age [51]. We investigated all
combinations of main effects and interaction terms that were
judged to be biologically feasible (see the electronic supplementary
material, methods (g)). The best models were selected as those
within three DAICc (Akaike’s information criterion) units
of the best model, and were model averaged to estimate effects of
particular trait variables [51].
The significance of individual species traits within the best
models was evaluated with 95 per cent CIs on model-averaged
odds ratios. Odds ratios represent the likelihood that a species
with a particular trait state will successfully traverse faunal
breaks. This likelihood is expressed in comparison with the reference category for dichotomous variables, or as the change in
likelihood with one unit difference for a continuous variable. An
odds ratio of one indicates that all trait states are equally likely to
cross faunal boundaries, less than one indicates the reference category or lowest value is more probable, and greater than one
indicates that the non-reference category or highest value is more
probable for species that successfully straddle faunal breaks compared with species that do not. Traits with confidence intervals
that overlap one indicate that species with either trait state do
not differ significantly in their likelihood of crossing faunal breaks.
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identified clusters of reefs separated by a given distance threshold.
We repeated this analysis for a range of distance thresholds from
125 to 250 km, with increments of 25 km (see the electronic supplementary material, methods (d)). We chose the lower limit of
this range to ensure the distance exceeded the aggregation distance used to generate reef groups comprising each of the 290
sites. Distances from 200 to 250 km generated identical clusters,
therefore, we set our upper limit at 200 km.
Boundaries in environmental conditions were established
using an iterative self-organizing cluster procedure within
ArcGIS ver. 10 [36] based on the spatial distribution of four
environmental variables: SST mean, SST range, salinity and nitrate
concentration ([37]; electronic supplementary material, methods
(c)). Mean SST, SST range and nitrate concentrations are common
proxies for available energy, environmental stability and productivity [8,14,38]. The geographical location of transitions
between environmental clusters indicated breaks in environmental
conditions, and we used these boundaries to classify reefs into
regions with similar environmental conditions.
Reef groups were assigned to the environmental, habitat and
geological clusters with which they spatially co-occurred. The
extent to which faunal provinces were correlated with clusters
based on these three sets of potential explanatory variables was
quantified using Mantel tests on group contrast matrices [39].
Mantel R2M is consistently lower than the more familiar Pearson’s
r 2 [40]. Specifically, a simulation study suggested that r 2 ¼ 0.25
was roughly equivalent to R2M ¼ 0:05, and that a large coefficient
of determination (R2 ffi 0:80) produced by trend surface analysis
was equivalent to R2M ffi 0:25 [41]. However, this approach has
been criticized because it assumes that locations are statistically
independent of one another (i.e. it fails to account for spatial
autocorrelation), leading to an increased type I error rate [42].
To address this limitation, we evaluated statistical significance
using an area-weighted permutation procedure that randomly
relocated breaks along the spatially ordered matrix generated
from EMS analysis, while maintaining province sizes (see the
electronic supplementary material, methods (f )). Therefore, the
"qffiffiffiffiffiffiffi#
null distribution of Mantel rM statistics
R2M generated by
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(a) faunal provinces
Fiji–Caroline Islands
Tonga–Samoa
Australia
(b) geological clusters
2
RM
= 0.301
Eurasian plate
Filipino plate
Arabian plate
African plate
Pacific plate
Tonga plate
Australian plate
Polynesian track
Hawaiian track
Red Sea
Fijian plate
Indian plate
Reunion track
(c) distance-based clusters
2
RM
= 0.104
cluster 1
cluster 2
cluster 3
cluster 4
cluster 5
cluster 6
cluster 7
cluster 8
cluster 9
cluster 10
cluster 11
cluster 12
(d) environmental clusters
2
RM
= 0.100
cluster 1
cluster 2
cluster 3
cluster 4
cluster 5
cluster 6
cluster 7
cluster 8
cluster 9
cluster 10
cluster 11
Figure 1. Indo-Pacific reef clusters derived from (a) species composition (i.e. faunal provinces), (b) geology, (c) distance and (d) environmental conditions. Black
lines are faunal breaks (dashed for those separating Red Sea and Andaman – Nicobar Islands provinces). Results of the Mantel correlation of faunal provinces with
clusters based on potential drivers are shown in the upper right corner of (b –d ). The distance-based and environmental clusters depicted are for the best threshold
(175 km) and variable combination (SST mean, nitrate, salinity), as defined from the number of clusters and the Mantel correlation with faunal provinces.
Proc R Soc B 280: 20130818
Polynesia
Hawaii–Line Islands
Red Sea
Andaman–Nicobar Islands
Unclustered reefs
4
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N
Indonesia
Japan–Vietnam
Persian Gulf
Africa–India
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rM
R2M
P
clusters
tectonic plates and mantle plume tracks
0.551
0.304
<0.001
13
distance-based
125 km
150 km
0.389
0.164
0.151
0.027
<0.001
0.005
23
14
175 km
0.322
0.104
<0.001
12
200 km
SST mean, SST range, salinity, nitrate
0.297
0.167
0.088
0.028
<0.001
<0.001
8
12
0.122
20.070
0.015
0.005
0.052
1.000
9
11
SST mean, nitrate, salinity
0.316
0.100
<0.001
11
SST range, nitrate, salinity
SST mean, SST range
0.292
20.022
0.085
,0.001
<0.001
1.000
14
9
SST mean, salinity
SST mean, nitrate
0.208
0.216
0.043
0.046
0.011
0.004
5
8
SST range, salinity
SST range, nitrate
0.254
0.020
0.065
,0.001
<0.001
0.137
7
3
Salinity, nitrate
0.208
0.043
0.011
5
environment
SST mean, SST range, nitrate
SST mean, SST range, salinity
Fiji–Caroline Islands, Tonga–Samoa, Polynesia and Hawaii–
Line Islands.
Of the 290 sites, 59 were not of sufficient similarity to any
other to be placed within a province (figure 1a). The reef areas
encompassed by both the Red Sea and the Andaman and Nicobar Islands were very large, comparable to several of the
provinces identified elsewhere (see the electronic supplementary
material, figure S1). These two locations were not identified as
‘provinces’ simply because the reefs within these regions
were so close together that they clustered as a single site. Consequently, we designated the Red Sea and the Andaman–Nicobar
Islands as two additional provinces (figure 1a).
(b) Geological, habitat and environmental clusters
Geological clusters, based on tectonic plate boundaries and
mantle plume tracks, were strikingly coincident with the
faunal provinces (figure 1b; Mantel test, R2M ¼ 0:301; p , 0.05,
table 1; and electronic supplementary material, figure S2),
which suggests species distributions reflect long-term colonization, extinction or speciation processes. Moreover, the number
of geological clusters (n ¼ 13) was very similar to the number
of faunal provinces (n ¼ 11). The additional geological clusters
arose because the Africa–India faunal province in the western
Indo-Pacific was split into three geological clusters: the African
plate, the Indian plate and the Reunion Track. Furthermore, in
the east, the Fijian plate isolates Fiji from the Caroline Islands,
splitting another faunal province. Conversely, two geological
clusters combine faunal provinces: the Eurasian plate contains
the Indonesian and Andaman–Nicobar Islands provinces,
while the Pacific plate cluster links the Tonga–Samoa province
with the Caroline Islands.
The spatial distribution of reef habitat is a substantially
weaker predictor of provincial structure than geological features, indicating that species are unlikely to be distributed
according to dispersal processes, because faunal breaks do
not coincide with large expanses of ocean lacking reef habitat.
A moderate distance-threshold (175 km) produced clusters
that were the most similar to faunal provinces, based on correlation and on the overall number of clusters, but the
correlation was approximately one-third of that found for
geological features (R2M ¼ 0:104, p , 0.001; n ¼ 12; figure 1c
and table 1). Larger distance thresholds generated fewer
clusters and had a lower correlation with faunal provinces
(n ¼ 8, R2M ¼ 0:088,). Conversely, smaller distance thresholds
generated clusters that far exceeded the number of provinces
(n ¼ 23 for 125 km), or had a much lower correlation
(R2M ¼ 0:027 for 150 km).
The correlation of faunal provinces with clusters of sites
generated from combinations of environmental variables
was statistically significant ( p , 0.004) for five variable
combinations, all of which included either the mean or
range of SST. The highest correlation was with environmental
clusters based on SST mean, nitrate and salinity (R2M $ 0:100,
p , 0.05; figure 1d) which generated 11 clusters—equal to the
number of faunal provinces. However, these environmental
clusters of sites were geographically widespread, and many
of the reefs within the same cluster were far apart (e.g. the
dark blue cluster in figure 1d includes reefs around
Madagascar, Fiji and Japan). Furthermore, the Mantel correlation was three times lower than the correlation with
geological clusters.
Overall, these results suggest that faunal breaks coincide
predominantly with geological features, and to a lesser (but
statistically significant) degree with contemporary environmental conditions and the spatial distribution of habitat. In
all tests, our modified permutation test produced null distributions that were substantially more conservative than the
traditional approach that assumes no spatial structure in the
data (see the electronic supplementary material, figure S2).
Proc R Soc B 280: 20130818
geology
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Table 1. Spatial co-occurrence of faunal provinces throughout the Indo-Pacific with clusters derived from geological features, distance and environmental
conditions. Significance values were assessed based on a correction for multiple tests. The corrected 5% alpha value for distance-based clusters (n ¼ 4) was
0.012, and for environmental clusters (n ¼ 11) was 0.004, and significant correlations according to the corrected value are in bold.
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6
large
small
wave exposure
specialized
and turbidity tolerance
species trait
propagule
nutritional mode
broad
azooxanthellate
zooxanthellate
brooder
young
old
genus age
(gonochore)
young
old
development rate
(hermaphrodite)
development rate
(gonochore)
fast
slow
fast
slow
0.4
spawner
1.0
1.5
odds ratio
Figure 2. Association of species traits with the likelihood of a species crossing Indo-Pacific faunal breaks. Values plotted are model-averaged odds ratios (points) with 95%
CIs (solid horizontal lines). Where confidence intervals do not encompass 1 (vertical dotted line), the trait state (label within box) was significantly more likely among
species that crossed breaks. Genus age and development rate interacted significantly with sex, so gonochores and hermaphrodites are shown separately for these traits.
(c) Species traits and faunal breaks
Among the species traits we examined, depth range was a strong
predictor of the likelihood that a species occurred on both sides of
a faunal break (see figure 2 and electronic supplementary
material, table S2). Specifically, for each 10 m increase in depth
range, species were 27 per cent more likely to straddle faunal
breaks. In other words, as provinces decrease in richness, the
species within them become skewed towards a greater proportion of depth generalists. Three other species traits (tolerance
to wave exposure and turbidity, propagule nutritional mode
and reproductive mode) were included within the set of best predictive models for whether species crossed faunal breaks, but do
not appear to strongly influence biogeographical patterns (estimates of their effects were small in magnitude and 95% CIs for
odds ratios overlapped 1; figure 2). In addition, the influence of
larval development rate and genus age on biogeographical patterns differed among gonochores and hermaphrodites.
Gonochores with fast larval development rates were more
likely to occur on both sides of faunal breaks (28% more likely
for each decrease in development rate class), but this trait did
not affect the likelihood of hermaphrodite species spanning
faunal breaks. However, the occurrence of hermaphrodites
across faunal breaks was well predicted by the final trait we examined, which was genus age: species were 30 per cent more likely to
straddle breaks with each 20 Ma increase in genus age. Genus age
was not an important predictor for gonochores.
At the two most peripheral faunal breaks we considered
(between Africa–India and the Persian Gulf; and between
Fiji–Caroline Islands and the Hawaii–Line Islands), species
were less likely to occur on both sides than at the more centrally
located boundaries (see the electronic supplementary material,
figure S3). This suggests that these faunal boundaries are
more distinctive. Overall, 42 per cent of the variance within
the model was explained by baseline differences (specifically,
among-break variation in intercept estimates from the model)
in the likelihood of species ranges spanning the individual
breaks. Phylogenetic effects, represented by clade nested
within suborder, accounted for less than 1 per cent of the
variation within the model. However, sexuality, in addition to
providing information about colonization potential, is highly
conserved within clades [53] and, therefore, may implicitly
incorporate a phylogenetic signal. This interpretation is supported by the fact that phylogenetic random effects become
more important if sexuality was dropped from the analysis.
4. Discussion
Indo-Pacific corals are spatially assembled at large scales, generating distinct faunal provinces that are delineated by sharp faunal
breaks at which multiple species reach their geographical range
limits. These provinces and breaks have not been identified in
previous analyses of corals, which have focused principally on
species richness [14], or on species turnover at smaller scales
[54,55]. The provinces we have identified share some similarities
with the global marine provinces proposed by Spalding et al. [17].
However, their zoning scheme identified more than 30 IndoPacific provinces, most of which are subsets of the Indonesian
and Australian provinces, which our analyses indicate have a
relatively homogenous coral fauna. Moreover, Spalding
et al.’s [17] provinces were principally based on qualitative assessment of the global distribution of endemic species, whereas
endemics are relatively uncommon among scleractinian coral
faunas in most parts of the Indo-Pacific [56]. Other previous
schemes differ more substantially from our own, classifying
most of the Indo-Pacific as a single province [18,57]. These
disparities point to the need for a more rigorous data-driven,
quantitative approach to identifying large-scale marine zones
or biogeographical provinces, such as that presented here.
Unexpectedly, the provincial boundaries we identified do
not coincide with breaks in contemporary environmental conditions or present-day habitat distribution. Instead, faunal
boundaries show striking concordance with geological features (i.e. tectonic plates and mantle plume tracks), which
suggests a role for long-term historical processes in the generation of biogeographical structure of Indo-Pacific corals [58].
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reproductive
mode
genus age
(hermaphrodite)
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depth range
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Understanding the mechanisms that link biogeographical
structure and geological features requires consideration of ecological and evolutionary processes that operate over long
temporal scales. At convergent plate boundaries, one plate is
subsumed under another forming a subduction zone, which
is characterized topographically by a trench on the subducting
side, and by island arcs (linear archipelagos) on the consuming
side (e.g. west of Sumatra [31]). These arcs, which run parallel
to plate boundaries, can act as stepping stones for dispersal
and colonization within a tectonic plate over long geological
timescales [35]. For example, the Izu–Bonin–Volcano Island
arc connects otherwise isolated islands parallel to the Filipino
plate boundary within the Japan–Vietnam province. Mantle
plume tracks, which form volcanic island chains as tectonic
plates move over a stationary plume [35], could also link
reefs within the Africa–India province, Hawaii–Line Islands
province, and the Polynesian province. Stepping stone colonization has received empirical support. On some islands, taxa
are older than the geological age of those islands, indicating
that these taxa originated elsewhere and later colonized the
younger islands. For example, two islands along the track
within the Africa–India province are 2–3 million years old,
but host an endemic plant family that molecular dating has
estimated as 52 million years old [59].
During the process of migration along stepping stones,
species with strong dispersal and/or establishment abilities
may be favoured, observable as selective colonization. This
mechanism is often invoked to explain nested diversity structures
[60] and therefore fits well with our findings. For example, Tonga
and Samoa are geologically young (approx. 4–5 Ma), so may
have experienced selective colonization of species from the geologically older islands of Fiji (approx. 35 Ma [35]), potentially
explaining the faunal break between these islands. Moreover,
when an island is created through geological separation from
the mainland, resultant vicariant speciation events can be followed by selective colonization of a new island species back to
the mainland. Molecular evidence suggests that such ‘reverse
colonization’ has occurred for some species of Indian Ocean chameleons, which originated in Madagascar after the break-up of
Gondwana, and subsequently colonized the mainland of
Africa and India, and the Seychelles [61].
A logical prediction of selective colonization as a mechanism for provincial differences is that species with efficient
colonization abilities and broad environmental tolerance
would be disproportionately present in low richness provinces. Our species trait analysis is generally consistent
with this prediction. Generalist species with broader depth
ranges were more likely to straddle faunal breaks, which
suggests that species are selectively filtered according to
their environmental tolerance. In contrast, gonochoristic
(b) Contemporary environmental conditions
The relatively low concordance between faunal breaks and transitions in environmental conditions suggests that geographical
variation in contemporary environment is unlikely to play a
dominant role in determining the changes in species composition that occur along Indo-Pacific biodiversity gradients,
despite the fact that some previous work has found SST to be
a strong statistical predictor of coral species richness [8,14].
Our finding illustrates the insight that can be gained by expanding the focus of analysis beyond species richness alone, to
encompass other aspects of species composition. The Mantel
correlation coefficients between species composition and
environmental conditions in our study are similar in magnitude
to those found between oceanographic conditions (temperature,
pH and productivity) and bivalve occurrence on a global scale
[55], although our modification of the Mantel permutation test
to account for spatial autocorrelation produces a much lower
estimate of statistical significance than the standard test. Moreover, our analysis found that, for corals, species composition
exhibits a much stronger relationship with geological clusters
than with present-day environmental conditions.
The relatively weak association between faunal breaks
and transitions in environmental conditions does not necessarily imply that environmental conditions have no effect on
faunal breaks in the Indo-Pacific at all. For instance, ecologically, localities with high habitat heterogeneity tend to be
associated with the presence of both generalist and specialist
species because a greater variety of habitats are available to
accommodate the specialists, and this contributes to a high
diversity of species [43,63]. The Indonesian and Philippine
region holds a diverse array of different reef habitats, including large areas of shallow shelves and areas where reefs
flourish in turbid waters. Moving away from this region,
habitat heterogeneity decreases. For example, within the central and eastern Pacific, fringing reefs and atolls are the
dominant reef type [31,35]. Thus, as the variety of available
habitats progressively decreases in these more peripheral
regions, specialist species would be expected to be filtered
out of the regional species pool [43]. This expectation is consistent with our results, which show that specialist species are
indeed disproportionately filtered out at faunal breaks.
(c) Dispersal limitation
The present-day spatial distribution of reef habitat appears to
be of relatively low importance for structuring broad-scale
7
Proc R Soc B 280: 20130818
(a) Historical mechanisms
species with slower development rates (and therefore, potentially longer pelagic larval durations), indicated by a large
egg size, were less likely to cross faunal breaks. While this
result is inconsistent with the conventional view that long
pelagic larval durations should lead to more long-distance
dispersal, it is consistent with more recent work suggesting
that species with shorter pelagic durations are more successful at consolidating range expansions because the offspring of
colonizers are more likely to recruit back to the new population [19,46], as well as recent work showing weak pelagic
larval duration –dispersal links in fishes [62]. Hermaphroditic
coral species within younger genera are also more likely to
reach range limits at faunal breaks compared with hermaphroditic species within older genera, which may be explained
by the increased time available for species of an older age
to have colonized peripheral regions [10].
rspb.royalsocietypublishing.org
The influence of history on the distribution of marine organisms has long been recognized [11,34,35,58]. However,
attempts to identify the effect of history on present-day
coral biogeography have been hindered by the use of species
richness rather than composition as the principal response
variable [14]. Our analyses of species traits also revealed
that the depth range over which a species occurs, the rate
of larval development in gonochores, and the genus age of
hermaphrodites are important determinants of the likelihood
that species will straddle faunal breaks.
Downloaded from http://rspb.royalsocietypublishing.org/ on January 25, 2017
Our results identify a striking, unexpected concordance
between geological features and coral biogeographical structure, suggesting a substantial role for long-term processes in
the generation and maintenance of coral biodiversity on IndoPacific reefs. The weaker, but still statistically significant, concordance with contemporary environmental conditions and spatial
6. Data accessibility
— Digitized reef polygons uploaded as electronic supplementary material;
— coral species range boundaries: Hughes et al. [22];
— centroids of merged reef groups uploaded as electronic
supplementary material; and
— species traits data uploaded as electronic supplementary
material.
We thank the Australian Research Council for financial support. We
also acknowledge the support from the Queensland and Australian
government for the high-performance computing facility at James
Cook University.
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