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Classifying the biological traits of organisms can test conceptual frameworks of life-history strategies and allow for predictions of how different species may respond to environmental disturbances. We apply a trait-based classification approach to a complex and threatened group of species, scleractinian corals. Using hierarchical clustering and random forests analyses, we identify up to four life-history strategies that appear globally consistent across 143 species of reef corals: competitive, weedy, stress-tolerant and generalist taxa, which are primarily separated by colony morphology, growth rate and reproductive mode. Documented shifts towards stress-tolerant, generalist and weedy species in coral reef communities are consistent with the expected responses of these life-history strategies. Our quantitative trait-based approach to classifying life-history strategies is objective, applicable to any taxa and a powerful tool that can be used to evaluate theories of community ecology and predict the impact of environmental and anthropogenic stressors on species assemblages.
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LETTER Evaluating life-history strategies of reef corals from species
Emily S. Darling,
Lorenzo Alvarez-Filip,
Thomas A. Oliver,
Timothy R. McClanahan
Isabelle M. Co
Classifying the biological traits of organisms can test conceptual frameworks of life-history strategies and
allow for predictions of how different species may respond to environmental disturbances. We apply a
trait-based classification approach to a complex and threatened group of species, scleractinian corals. Using
hierarchical clustering and random forests analyses, we identify up to four life-history strategies that appear
globally consistent across 143 species of reef corals: competitive, weedy, stress-tolerant and generalist taxa,
which are primarily separated by colony morphology, growth rate and reproductive mode. Documented
shifts towards stress-tolerant, generalist and weedy species in coral reef communities are consistent with
the expected responses of these life-history strategies. Our quantitative trait-based approach to classifying
life-history strategies is objective, applicable to any taxa and a powerful tool that can be used to evaluate
theories of community ecology and predict the impact of environmental and anthropogenic stressors on
species assemblages.
Community assembly, coral reefs, CSR triangle, ecological strategies, functional diversity, selection
Ecology Letters (2012)
Ecologists are increasingly realising that trait-based views of species
assemblages may be more meaningful than comparisons of species
richness or composition (Cadotte et al. 2011). Trait-based
approaches can provide general and predictable rules for community
ecology, as well as a more mechanistic understanding of community
assembly and disassembly, habitat filtering and species coexistence,
particularly in the context of global climate change and biodiversity
loss (McGill et al. 2006). Species traits also provide important infor-
mation about life-history strategies, which can broadly define how
organisms interact with one another and their environment.
Life-history strategies describe consistent and context-independent
characteristics of organisms. The classic two-strategy life-history
framework of rKmodels (Pianka 1970) is now generally seen as
oversimplified as species can occur along a continuum of ‘fast’ (r)
to ‘slow’ (K) life histories (Stearns 1977). Three-strategy frameworks
resolve some difficulties of rKselection by adding a third ‘beyond
K’ group of stress-adapted species that can persist in unfavourable
habitats (i.e., via adversity selection, Greenslade 1983). For example,
Grime’s CSR triangle describes three life-history strategies in
plants, in which species are hypothesised to evolve strategies that
promote competitive (C), stress-tolerant (S) or ruderal (R) life histo-
ries (Grime 1977; Grime & Pierce 2012). Similar triangular continu-
ums of life-history strategies have also been proposed for insects
(Greenslade 1983) and fishes (Winemiller & Rose 1992). Life-history
models with three strategies are generally recognised as having more
predictive power than the two-strategy rKframework that can fail
to recognise additional axes of life-history variation (Stearns 1977;
Winemiller & Rose 1992). Although more than two or three life-his-
tory strategies likely exist in any given community, such multi-strat-
egy frameworks are rarely quantitatively described. Moreover, many
of these life-history frameworks are based on the responses of
organisms to different environmental or habitat conditions, instead
of on inherent characteristics of species (Westoby 1998). Further-
more, such classifications are often subjective (Gitay et al. 1997),
which can bias tests of evolutionary and ecological theories that are
better addressed with quantitatively and objectively identified life-
history strategies.
Here, we evaluate if life-history strategies can be directly inferred
from species traits in a complex and threatened group of organisms,
scleractinian corals. Climate change, overexploitation, pollution and
disease have resulted in global declines of coral cover and architec-
tural complexity on coral reefs, one of the world’s most complex
and biodiverse ecosystems (Gardner et al. 2003; Pandolfi et al. 2003;
Alvarez-Filip et al. 2009). Human impacts are altering coral commu-
nities in ways that are unprecedented from the historical record
(Pandolfi & Jackson 2006; van Woesik et al. 2012) as historically
dominant corals are replaced by more persistent and opportunistic
species (Knowlton 2001; McClanahan et al. 2007; Green et al. 2008;
Alvarez-Filip et al. 2011). However, shifts in coral species can often
be overlooked for a variety of reasons: they may be subtle
species-level coral identification is challenging and changes may
occur on decadal or millennial timescales (Pandolfi & Jackson 2006;
van Woesik et al. 2012). Changes may also go unnoticed as the
baseline for what is considered a ‘normal’ community composition
is often unknown and shifts in species composition can occur
slowly over time (Pauly 1995). More importantly, a general lack of
Department of Biological Sciences, Simon Fraser University, Burnaby, British
Columbia, V5A 1S6, Canada
Healthy Reefs Initiative, 1755 Coney Drive, Belize City, Belize
Hawaiian Institute for Marine Biology, University of Hawai’i Ma
¯noa, 46-007
Lilipuna Rd, Ka
¯ne’ohe, HI, 96744, USA
Marine Programs, Wildlife Conservation Society, Bronx, NY, 10460, USA
*Correspondence: E-mail:
©2012 Blackwell Publishing Ltd/CNRS
Ecology Letters, (2012) doi: 10.1111/j.1461-0248.2012.01861.x
long-term abundance information for individual coral species makes
it difficult to identify species responses to environmental change
and anthropogenic stress, and whether these responses are predict-
There is currently no framework of life-history strategies for scle-
ractinian corals, possibly because data on species traits are too
sparse or scattered for classification or because corals do not fit well
into existing frameworks (e.g. corals are clonal invertebrates with a
complicated life cycle, Jackson & Hughes 1985). A few studies have
considered how some coral traits may relate to life-history strategies.
For example, small corals with brooding reproduction, fast growth
rates and high population turnover are expected to be ‘weedy’
(Knowlton 2001), while large, slow-growing colonies of massive
corals are expected to be more tolerant to chronically stressful or
variable environments (Jackson & Hughes 1985; Soong 1993;
Rachello-Dolmen & Cleary 2007). Similarly, variation in colony
morphology and reproductive mode are thought to suggest three
primary life histories (competitors, stress-tolerators and ruderals;
Edinger & Risk 2000; Murdoch 2007). Observations of increasing
abundances of ‘weedy’ species (Green et al. 2008) and the persis-
tence of massive species on disturbed Caribbean (Alvarez-Filip et al.
2011) and Indo-Pacific reefs (McClanahan et al. 2007; Rachello-Dol-
men & Cleary 2007) suggest that life-history traits can predict which
corals are ‘winners’ or a ‘losers’ in the face of environmental change
(Loya et al. 2001; van Woesik et al. 2012). For example, branching
and plating acroporid corals are dominant species that are very sen-
sitive to stress and disturbance (i.e., ‘losers’), while massive species
and ‘weedy’ species are more likely to be ‘winners’ and persist in
unfavourable and disturbed environments (Loya et al. 2001; McCl-
anahan et al. 2007). However, the underlying species characteristics
that may predict these responses are difficult to evaluate without a
comprehensive understanding of coral traits and associated life-his-
tory strategies.
In this study, we describe a novel, quantitative method that can
be used to evaluate and identify life-history strategies from species
traits using hierarchical clustering and random forests analyses. We
compile a global database of species traits for reef-building corals
and classify taxa into life-history strategies that can be used to eval-
uate ongoing community shifts on coral reefs. Our approach to
objectively classify life-history strategies is applicable to any species
group and can be used to establish trait-based life-history frame-
works, find general rules of community ecology and predict the
impacts of environmental and anthropogenic impacts on ecological
Coral species traits
To evaluate life-history strategies in reef corals, we collected infor-
mation on 11 commonly available species traits: colony growth
form, solitary colony formation, reproductive mode and fecundity,
maximum colony size, corallite diameter, depth range, generation
time, growth rate, skeletal density and symbiotic zooxanthellae
(Symbiodinium) associations (Table 1; see also Appendix S1 in Sup-
porting Information). We specifically focused on traits that were
expected to affect coral population dynamics, and for which quanti-
tative data were available at a global scale. All life-history traits are
variable and phenotypic plasticity within species is ubiquitous. Cor-
als, in particular, have notoriously variable life-history traits, and
there can be extensive phenotypic plasticity within populations and
species (Todd 2008). However, the goal of our study was to provide
a broad, global comparison of life-history traits across species and
not focus on intraspecific variation. Thus, we conducted an exten-
sive literature survey to provide the most accurate ‘average’ descrip-
tion of species-specific traits, and we leave in-depth assessments of
intraspecific variability to future investigations.
We collected trait information for 847 scleractinian corals, com-
prising 101 western Atlantic and Caribbean (hereafter referred to as
Atlantic) species and 746 Indo-Pacific species. This information
came from 236 sources, including taxonomic monographs, regional
identification guides, published literature, secondary sources and
online databases (see Appendices S1S2). Only taxa with informa-
tion for more than 60% of the species traits were included in the
analysis (i.e., species with data for at least 7 of 11 traits, n=143
species: 32 Atlantic and 111 Indo-Pacific species from 51 genera
and 19 families). Our cut-off of 60% trait coverage was a trade-off
between the number of species included in the analysis and compre-
hensive trait information for each species. For example, only a small
subset of species (n=20; 8 Atlantic and 12 Indo-Pacific species)
had complete (100%) trait information. We conducted a sensitivity
analysis and found clusters to be qualitatively unchanged from 100
to 60% trait information. With information on less than 60% of
traits, clustering patterns became more variable, although generally
similar to clustering analyses with more trait coverage.
Classifying life-history strategies
We took a data-driven approach to classify life-history strategies
using a posteriori group classification of Ward’s hierarchical clustering
analyses (e.g. Gitay et al. 1997), followed by random forests analyses
to identify influential traits, and Principal Coordinates ordination to
visually show species life-history strategies and traits in multivariate
We used hierarchical clustering and non-parametric multivariate
analyses of variance (MANOVAs) as an objective and quantitative
method to identify life-history strategies. First, we established a trait
dendrogram of species relationships using Ward’s hierarchical clus-
tering of a Gower dissimilarity matrix. We chose the Gower dissimi-
larity index to compare the multivariate trait distance between
species because it allows for mixed types of data, missing values
and can weight individual traits differently (Laliberte´ & Legendre
2010). The 11 traits were independent characteristics (variance infla-
tion factors <5 for all continuous variables) and all traits were
weighted equally in the analysis, except two traits, colony growth
form and reproductive mode, which were each reclassified into sep-
arate binary variables (branching, plating and domed colony growth
forms; brooding and spawning reproductive modes; see Appendix
S1). The three binary states for growth form were weighted by 0.33
and the two binary states for reproductive mode were weighted by
0.5, to avoid artificially inflating the effect of these traits (Laliberte´
& Legendre 2010). Dissimilarity indices and clustering were per-
formed using the ‘FD’ package (Laliberte´ & Legendre 2010) in R
(2012) R Development Core Team (2010).
We evaluated the ‘best-fit’ number of clusters by testing how
many clusters maximised both within-cluster homogeneity and
between-cluster dissimilarity. We used non-parametric MANOVAs to
evaluate different groupings of species by comparing the coefficient
©2012 Blackwell Publishing Ltd/CNRS
2E. S. Darling et al. Letter
of determination (R
) across nine different clustering scenarios
(between two and 10 clusters). We then identified a cut-off or
‘elbow’ where further clustering resulted in a sharp decrease
(>15%) in the amount of explained variance; clusters above this
cut-off were deemed to be the ‘best-fit’ clusters (see Fig. S1). This
is comparable to the use of scree plots to evaluate the number of
principal components to include in a principal components analysis.
After identifying the number of ‘best-fit’ clusters, we calculated the
mean and standard deviation of trait values within each cluster and
tested for mean differences in multivariate traits across clusters
using non-parametric MANOVAs. We also compared the variability of
species strategies within life-history clusters using a multivariate
homogeneity of variance test, which calculates the average distance
of each species to median group trait values, followed by Tukey’s
Honestly Significant Differences tests to identify pairwise differ-
ences between groups (Oksanen et al. 2011).
In addition to classifying species into life-history strategies, we
also wanted to identify traits that were the best predictors of coral
life-history strategies. We used random forests analyses to evaluate
the relative importance of different traits. Random forests are a
machine-based learning method that estimates variable importance
by combining many classification trees through bootstrap sampling
and model averaging, and can also account for multicollinearity
among variables (Cutler et al. 2007). During each iteration of the
classification tree, a random subset of three traits (out of 11) was
used to classify species into life-history groups, and the final tree
was then compared with the original ‘blueprint’ trait dendrogram
produced by Ward’s hierarchical clustering of the full set of 11
traits. After 20 000 iterations, we compared the increase in the
cluster misclassification rate for each trait when it was excluded,
and all other traits were held constant, to assess the relative
importance of each trait; traits that resulted in the greatest increase
in misclassifications when excluded were identified as the most
important (Cutler et al. 2007). Prior to random forests analysis,
missing species trait values were filled in using standard data impu-
tation through proximity (Liaw & Wiener 2002; Cutler et al. 2007)
for each cluster, missing values of continuous traits were
replaced with the median of the trait within the cluster, and miss-
ing values of categorical traits were replaced with the most fre-
quent level of the trait in the cluster. In total, 288 missing values
out of 2002 data points, or 14.4%, were replaced by imputation
for the random forests analysis. We assessed the model accuracy
of classification trees and random forests using standard metrics
(e.g. out-of-bag error rate; Cutler et al. 2007). We used the
‘randomForest’ package (Liaw & Wiener 2002) in R (2012) R
Development Core Team (2010) for these analyses.
Finally, we used a Principal Coordinates Analysis (PCoA)
ordination of the Gower dissimilarity matrix to visually show the
life-history groups and species traits in multivariate space. However,
this ordination is purely descriptive and does not provide statistical
tests of clustering structure among species (Borcard et al. 2011).
Following species ordination, we projected each trait onto the plot
a posteriori using a double projection method based on correlations
of the species traits with the PCoA axes; species traits were standar-
dised prior to ordination and negative eigenvectors were adjusted
using the Cailliez correction (Borcard et al. 2011). Multivariate analy-
ses were performed using the ‘vegan’ (Oksanen et al. 2011) and
‘FD’ (Laliberte´ & Legendre 2010) packages in R (2012) R Develop-
ment Core Team (2010).
Life-history strategies of reef corals
Models with two, three and four clusters of coral species received
the most support in the hierarchical clustering analyses (Table 2,
Fig. 1, see Figs. S1S3). The two-cluster scenario identified a ‘fast’
life history of large, branching and plating corals and a ‘slower’ life
history of smaller, slower-growing corals (see Table S1; Fig S2). The
three-cluster scenario distinguished a third group of small, brooding
corals, which would fit with a ruderal or opportunistic life history
of three-strategy frameworks (see Table S2, Fig. S3; Grime 1977;
Grime & Pierce 2012). The four-strategy clustering scenario (Table
2; Fig. 1) added a ‘generalist’ group of species that appear to have
some traits of each life history identified in the three-cluster sce-
nario. We focus on the four-cluster scenario for a discussion of reef
coral life histories. These four clusters describe significantly differ-
ent groupings of species traits (non-parametric MANOVA,P=0.001)
and random forests analyses identified colony growth form, growth
rate and reproductive mode as the most influential traits responsible
for clustering the different groups (Fig. 2; see also Fig. S4).
Cluster 1 describes large, branching and plating species that grow
quickly, occur at shallow depths and reproduce by broadcast spawn-
ing (Table 2). This group includes the staghorn and bottlebrush cor-
als in the genus Acropora in the Atlantic and Indo-Pacific, Dendrogyra
cylindricus in the Atlantic and species of Montipora, Pocillopora and Tur-
binaria in the Indo-Pacific. We suggest that cluster 1 describes a
Table 1 Summary of 11 species traits used to classify life-history strategies of
scleractinian reef corals. Detailed descriptions and source references for each trait
can be found in Appendices S1 and S2
Species trait Description Type of data
growth form
plating, domed*
Solitary colonies Solitary or
colonial colonies
broadcast spawning*
Colony size Largest recorded
size of colony, cm
Average size
of corallites, cm
Depth range Median depth
(m) of reported
depth range
Fecundity Number of eggs
per polyp or
Number of years
between generations
Growth rate Average annual
growth rate,
mm year
Skeletal density Average density
of CaCO
g cm
Rarefaction curve of
Symbiodinium genotypic
richness corrected for
sampling effort
*Colonies can have more than one characteristic.
Domed corals include massive, submassive and encrusting morphologies.
©2012 Blackwell Publishing Ltd/CNRS
Letter Life-history strategies of reef corals 3
‘competitive’ life-history strategy that is typically efficient at using
resources and can dominate communities in productive environ-
ments (Grime 1977; Grime & Pierce 2012). Branching and plating
corals often grow quickly into large, arborescent colonies that can
create canopies to shade out competitors for light and plankton
prey, making them effective competitors in shallow, high light and
low water flow environments (Baird & Hughes 2000). However,
these species are extremely sensitive to breakage and dislodgement
during storms (Madin 2005) and often exhibit high mortality follow-
ing temperature anomalies and coral bleaching (McClanahan et al.
2007), suggesting they are only dominant in ideal environments.
Interestingly, previous qualitative studies have classified species of
Acropora and Montipora as a ruderal or weedy life history because of
their fast growth and good colonising characteristics (Edinger &
Risk 2000; Rachello-Dolmen & Cleary 2007). However, the ability
of these species to competitively dominate coral assemblages in the
Indo-Pacific (Baird & Hughes 2000; Hughes et al. 2012) and their
sensitivity to environmental change and marked declines from his-
torical dominance in the Atlantic (Alvarez-Filip et al. 2011) suggest,
instead, that acroporids may be associated with a competitively
dominant life-history strategy.
Species within cluster 2 can reproduce by brooding and have
smaller colony sizes. This cluster includes branching Porites species
in the Atlantic and Indo-Pacific, species of Madracis and Agaricia in
the Atlantic, some pocilloporids (Pocillopora damicornis,Stylophora pistil-
lata,Seriatopora hystrix) and some faviids (e.g., species of Cyphastrea,
Goniastrea and Leptastrea) in the Indo-Pacific. Cluster 2 appears to
describe a weedy or ruderal strategy of species that can opportunis-
tically colonise recently disturbed habitats (Grime 1977; Grime &
Pierce 2012). Ecological theory suggests that successful weeds
reproduce faster and survive better than non-weedy species. While
species in cluster 2 displayed some traits of fast reproduction (e.g.,
shorter generation time, on average), they did not have higher
fecundity (as measured by eggs per polyp) than the other clusters
(Table 2). Moreover, this lack of a fecundity advantage could be
compounded by their smaller colony sizes (Table 2; Soong 1993).
The reproductive advantage of weedy corals may instead lie in a
correlate of their brooding reproductive mode. Although brooders
produce relatively large offspring (Knowlton 2001), which is associ-
ated with high parental investment and would be an unusual charac-
teristic of weeds, some brooding corals can produce larvae via
parthenogenesis (Ayre & Miller 2004). Parthenogenesis might allow
for successful reproduction at low population densities, which may
often occur on recently disturbed reefs. In contrast, many common
broadcast spawning species are vulnerable to Allee effects and can
fail to reproduce in small populations (Knowlton 2001). Further-
more, as population size increases, brooders can also disperse sexu-
ally produced larvae that may favour genetically diverse colonists
(Ayre & Resing 1986). Weedy corals may also be better survivors
than non-weedy corals because they show the most variation in
their species traits compared the other life-history strategies (multi-
variate homogeneity of variances test, P=0.009, Fig. 3), which may
allow these taxa to colonise a variety of disturbed environments,
such as heavily fished reefs or shallow back reef lagoons.
If clusters 1 and 2 describe competitive and weedy life-history
strategies, theory would suggest that one of the remaining clusters
(3 or 4) might represent a stress-tolerant strategy. Species in cluster
4 appear to be the best candidates for a stress-tolerant life history.
This cluster includes slow-growing species that reproduce by broad-
Table 2 Summary of species traits across four life-history strategies of (a) global (n=143 species), (b) Atlantic (n=32) and (c) Indo-Pacific (n=111 species) reef corals. For categorical traits (colony growth form,
solitary colonies and reproductive mode), the per cent of species with each trait characteristic is presented; mean (standard deviation) is reported for continuous traits
Life history
size (cm)
range (m)
(eggs polyp
Growth rate
(mm year
(a) Global
1Competitive 46 95.7 0 39.1 0 0 100 259.32 (314.68) 2.70 (1.31) 12.53 (5.50) 20.04 (32.39) 9.72(1.11) 49.83(41.28) 1.51 (0.34) 1.78 (1.28)
2Weedy 23 39.1 56.5 21.7 0 100 18.2 105.54 (138.54) 4.45 (5.86) 20.58 (14.91) 19.70 (14.26) 9.41 (1.56) 11.35 (10.04) 1.73(0.41) 1.70 (1.61)
3Generalist 14 35.7 100 100 0 0 100 248.77 (243.39) 3.56 (3.55) 17.95 (5.05) 18.46 (9.26) 10.00(0.00) 19.18 (11.58) 1.62 (0.34) 1.79(0.63)
4Stress-tolerant 60 0 100 1.7 5 3.4 100 137.81 (285.26) 8.57 (9.83) 19.50 (10.45) 372.45 (694.15) 10.17(1.52) 7.98 (6.69) 1.54 (0.28) 1.42(0.86)
(b) Atlantic
1Competitive 3 100 0 0 0 0 100 304.80 (61.00) 2.52 (3.02) 21.10 (8.67) 63.34 (83.71) 10.00 (0.00) 71.09 (50.13) 1.45 (0.58) 1.07(0.56)
2Weedy 15 26.7 60 33.3 0 100 0 69.80 (97.12) 5.30 (6.85) 26.26 (16.13) 23.00 (16.61) 10.00 (0.00) 6.99 (7.14) 1.72 (0.50) 1.19(0.68)
3Generalist 2 0 100 100 0 0 100 166.97(46.70) 2.58 (0.02) 23.88 (5.13) 17.31 (13.59) 10.00 (0.00) 7.40(1.07) 1.31 (0.18) 2.50 (0.30)
4Stress-tolerant 12 0 100 8.3 0 0 100 105.75(48.55) 7.15 (5.18) 32.42 (14.62) 100.68 (123.74) 10.00 (0.00) 5.53(2.00) 1.51 (0.43) 1.26(0.84)
(c) Indo-Pacific
1Competitive 43 95.3 0 41.9 0 0 100 252.14 (338.70) 2.71 (1.15) 11.93 (4.82) 14.39 (16.31) 9.70 (1.15) 47.18(40.52) 1.52 (0.32) 1.83(1.30)
2Weedy 8 62.5 50 0 0 100 50 177.02 (186.01) 2.86 (3.24) 10.62 (2.37) 14.74 (9.76) 8.38 (2.33) 16.97 (10.90) 1.73 (0.27) 2.67 (2.37)
3Generalist 12 41.7 100 100 0 0 100 263.64 (263.22) 3.73 (3.86) 16.96 (4.50) 19.60 (8.20) 10.00(0.00) 23.11 (10.65) 1.77 (0.30) 1.68(0.60)
4Stress-tolerant 48 0 100 0 6.2 4.3 100 146.97 (322.75) 9.01 (10.89) 16.28 (5.82) 472.58 (790.45) 10.21 (1.70) 8.82 (7.53) 1.55 (0.19) 1.46(0.87)
©2012 Blackwell Publishing Ltd/CNRS
4E. S. Darling et al. Letter
Figure 1 Hierarchical cluster analysis of global scleractinian corals based on species traits. The analysis includes 143 species with "60% trait coverage (i.e., information
for at least 7 of 11 traits). Clustering scenarios with two, three and four groups received the strongest model support (see Figs. S1S3); a four-cluster scenario is shown
here. Boxes indicate Atlantic (Atl) or Indo-Pacific (IP) distributions.
©2012 Blackwell Publishing Ltd/CNRS
Letter Life-history strategies of reef corals 5
cast spawning and have primarily domed morphologies, large coral-
lites and high fecundity. Examples include the lobe and brain corals
Montastraea annularis and M. cavernosa,Colpophyllia natans and species
of Diploria in the Atlantic, and massive Porites species and many
faviids (e.g. Favia,Favites,Platygyra,Goniastrea) in the Indo-Pacific.
Slow growth, longer generation times, large corallites, which pro-
mote energy storage (van Woesik et al. 2012), and high fecundity
during episodic spawning events may all be advantageous traits in
chronically harsh environments with, for example, low light or high
sedimentation. These traits have previously been assigned to a sub-
dominant, stress-tolerant life history (Edinger & Risk 2000; Rac-
hello-Dolmen & Cleary 2007). Long-lived corals can also persist in
the absence of recruitment and can withstand sustained recruitment
failure for decades, which may increase their long-term survival in
stressful environments (Hughes & Tanner 2000). Interestingly, clus-
ter 4 is the most species-rich group, possibly because stress can be
caused by many environmental factors, including depth and low
light, wave exposure, sedimentation and temperature variability,
which may create many ecological axes that can promote speciation
within this group.
The remaining group, cluster 3, includes an assortment of species
that show some overlap with the competitive, weedy and stress-toler-
ant life histories in the Principal Coordinates ordination (Table 2;
Fig. 3). These taxa occur as domed and plating colonies (but can also
have branching growth forms), with moderate growth rates and can
reach large colony sizes. This group includes species of Echinopora,
Hydnophora, Montipora, Turbinaria and Pachyseris in the Indo-Pacific, and
two Atlantic species, Montastraea faveolata and M. franksi. These species
may represent a ‘generalist’ life-history strategy that can do well in
habitats where competition is limited by low levels of stress (Grime
1977; Winemiller & Rose 1992). Alternatively, this cluster may repre-
sent a subgroup of stress-tolerant taxa that are somewhat more com-
petitive than average for that group, with horizontally spreading
plating colonies and faster growth rates. For now, we label this cluster
as a ‘generalist’ life-history strategy and more trait information is
needed to discern whether species within this cluster are a separate
life-history strategy, a type of stress-tolerant life history, or even a
slower-growing subset of ‘subdominant’ competitive taxa.
Three of the coral clusters emerging from our analysis resemble
three-strategy life-history frameworks, such as Grime’s triangle of
–0.3 –0.2 –0.1 0.0 0.1 0.2 0.3 0.4
PCoA axis 2
PCoA axis 1
PCoA axis 2
PCoA axis 1 (6.0%)
12 Fun fung
Hel act
Pav dec
Fav fr
Alv fen
Aga lam
Fun gr
(a) (b)
Figure 3 Grime’s triangle of life-history strategies applied to reef corals. (a) The conceptual framework of Grime’s three primary life-history strategies and the
hypothetical environmental conditions associated with each strategy. (b) Principal Coordinates ordination of 143 coral species with four life-history strategies (red:
competitive, green: weedy, blue: stress-tolerant, grey: generalist). Open circles are Atlantic taxa and filled circles are Indo-Pacific taxa. Arrows indicate trait loadings; traits
are numbered from most important to least important in differentiating the life-history strategies: (1) domed morphology; (2) growth rate; (3) brooding reproduction; (4)
fecundity; (5) broadcast spawning reproduction; (6) branching morphology; (7) colony size; (8) skeletal density; (9) plating morphology; (10) corallite diameter; (11) depth;
(12) symbiont diversity; (13) generation length and (14) solitary colonies.
Solitary colonies
Generation length
Symbiont diversity
Depth range
Corallite diameter
Growth form, plating
Skeletal density
Colony size
Growth form, branching
Reproduction, spawning
Reproduction, brooding
Growth rate
Growth form, domed
Figure 2 Importance of individual traits for differentiating the four clusters of
global, Atlantic and Indo-Pacific reef corals as determined by random forests
analyses (see also Fig. S4). Circle size indicates rank of trait importance; larger
circles represent more influential traits than smaller circles. A summary of
species traits is given in Table 1.
©2012 Blackwell Publishing Ltd/CNRS
6E. S. Darling et al. Letter
primary plant life-history strategies (Grime 1977; Grime & Pierce
2012; Fig. 3). It is perhaps not surprising that reef-building corals
and plants can share some similarities in their life-history strategies.
Corals and plants are both sessile and clonal organisms (Jackson &
Hughes 1985), structured by competition for space (Lang et al. 1990;
Karlson & Hurd 1993), gradients of environmental productivity via
light and food availability (Anthony & Connolly 2004), and distur-
bance (Connell 1978; Karlson & Hurd 1993). Previous studies inves-
tigating coral morphology (Edinger & Risk 2000; Murdoch 2007),
the recruitment of juvenile corals (Bak & Engel 1979) and the
response of coral assemblages to depth gradients (Jackson & Hughes
1985), bleaching stress (Obura 2001) and pollution (Rachello-Dol-
men & Cleary 2007) have also suggested three major life-history
strategies of reef corals, which are similar to those we describe quan-
titatively here, although with different species classifications (e.g.,
acroporids were classified as ruderal, and domed and plating species
with moderate growth rates were classified as competitive).
Complexities of coral life histories
Although Grime’s triangle can reflect important life-history patterns
across species, this framework has been criticised for being too gen-
eral and for failing to consider the many complexities associated
with life-history strategies (e.g., the GrimeTilman debate summar-
ised by Aerts 1999; see also Westoby 1998). These drawbacks apply
here, even though the CSR framework appears to have some
application to reef corals. For example, ‘faster’ or ‘slower’ life histo-
ries, and competitive, stress-tolerant and weedy life histories, are
end point life-history strategies (e.g., located at the ‘tips’ of Grime’s
triangle), but species can have suites of traits that place them along
a continuum between primary strategies (Grime 1977; Winemiller &
Rose 1992; Grime & Pierce 2012). This appears to be the case for
species we have labelled as generalists (cluster 3), which display
traits that occur in between competitive, weedy and stress-tolerant
life histories (i.e., ‘CSR’ strategy, Grime 1977; Grime & Pierce
2012; Fig. 3). It is also the case for a few species that were placed
in one of the three conventional strategies. For example, four
stress-tolerant species (Alveopora fenestrata,Favia fragum and two fun-
giids, Fungia fungites and Heliofungia actiniformis) overlap with the
weedy group, suggesting these species may be part of a secondary
strategy of species adapted to lightly disturbed and unproductive
habitats (i.e., ‘SR’ strategy; Grime 1977; Grime & Pierce 2012).
‘Mixing and matching’ of traits in the generalist life history, and
overlap between primary strategies, suggests there may be a variety
of environmental selection pressures and trade-offs shaping life-
history strategies in reef corals. This may explain why we observed
some trait combinations in coral life histories that are not usually
associated with these strategies. For example, fast growth and high
fecundity are expected to be weedy traits (Grime 1977; Grime &
Pierce 2012), but competitive corals have the fastest growth rates
and stress-tolerant corals, the highest fecundities (Table 2). Brood-
ing reproduction is another example of an unusual trait in coral life
histories. Brooding is associated with parental investment, which is
usually considered a competitive (K) trait (Winemiller & Rose 1992).
However, in reef corals, brooding predominates among weedy,
opportunistic species (Table 2). Brooding in weedy corals may
reflect the need for asexual reproduction by isolated colonies
following disturbance, but may also entail a trade-off between
reproductive output and genetic heterozygosity in environments
where competition is low. Conversely, broadcast spawning in com-
petitive, stress-tolerant and generalist species may increase genetic
heterozygosity where competition is high, but might also result in a
limited ability to recover from small population sizes following dis-
turbance (e.g. Allee effects, Knowlton 2001). Consequently, the
reproductive mode of corals may be a response to the trade-off
between colonisation ability and competition, thus giving rise to
intermediate strategies and seemingly unusual trait combinations
that attempt to optimise these trade-offs.
Corals do not occupy all of the trait space of the hypothetical tri-
angle framework (Fig. 3b). This may be because most reef corals are
good competitors, compared with other benthic components of coral
reefs (Lang et al. 1990), moving species towards the competitive side
of the triangle. We hypothesise that other components of the coral
reef benthic community, such as sponges, soft corals and algae, might
primarily occupy trait space within the weedy and stress-tolerant
zones to further complete the life-history triangle. Future efforts to
quantify life-history strategies for the entire benthic community
would also be more comparable to the larger groups of taxa (i.e.,
plants, Grime 1977; fishes, Winemiller & Rose 1992; Grime & Pierce
2012) for which life-history theories were originally developed.
Understanding the life-history strategies of the entire coral reef ben-
thic community might also reveal whether ongoing shifts towards
non-coral assemblages (Norstro
¨met al. 2009) are associated with dif-
ferent life-history strategies. Overall, this highlights the need for
more trait information within coral species and other benthic groups.
Biogeographic and phylogenetic patterns
The life-history strategies we have identified appear largely
independent of biogeography as Atlantic and Indo-Pacific species
occur within each cluster (Fig. 1). For example, two lower-level
clusters of weedy taxa are apparent in the PCoA ordination and
each sub-cluster includes Atlantic and Indo-Pacific species (Fig. 1;
Fig. 3b). One sub-cluster includes shallow, fast-growing, branching
taxa, such as Pocillopora damicornis,Seriatopora hystrix,Stylophora pistillata
and species of digitate Porites from the Indo-Pacific (P. cylindrica,
P. rus) and two Atlantic taxa (P. furcata and P. porites), while a
slower-growing domed and plating sub-cluster includes species of
Agaricia,Porites astreoides,Siderastrea radians in the Atlantic, and several
faviid species from the Indo-Pacific (Cyphastrea ocellina,Goniastrea
aspera,Leptastrea purpurea). However, different traits nevertheless
separated regional taxa within the four clusters. Random forests
identified growth rate and colony growth form as the most impor-
tant traits differentiating clusters of Indo-Pacific species, while
reproductive mode and colony size were the most important traits
differentiating Atlantic species (Fig. 2; see also Fig. S4).
One of the more remarkable differences observed between the
regions was the larger proportion of weedy taxa in the Atlantic (15
weedy species of 32 total species, ~47%) than the Indo-Pacific (8 of
111, ~7%). This pattern likely reflects the overabundance of brood-
ers (a trait of weedy corals) in the Atlantic, which has been hypoth-
esised to be associated with colonisation history: more brooding
species may have been able to colonise Atlantic reefs from the east-
ern Pacific because brooded autotrophic larvae can be effective
long-distance dispersers (Baird et al. 2009). The overabundance of
brooders could also reflect the higher survival of brooding taxa fol-
lowing regional patterns of extinction over longer time scales
(Edinger & Risk 1995; van Woesik et al. 2012).
©2012 Blackwell Publishing Ltd/CNRS
Letter Life-history strategies of reef corals 7
Many life-history traits are phylogenetically conserved and our
classifications may in part reflect evolutionary relationships. For
example, most life-history classifications are consistent within gen-
era. Of the 22 genera with more than two species included in our
analysis, only seven genera (Cyphastrea,Goniastrea,Montipora,
Pocillopora,Porites, Siderastrea and Turbinaria) have species in different
life-history groups. This suggests that for most taxa (15 of 22, or
68%), genus-level identification may be sufficient to classify coral
life histories. There was more variability within families. Of the 15
families (based on Fukami et al. 2008) with more than one species,
10 had multiple life-history classifications. This suggests that sclerac-
tinian families often include species with diverse life histories,
although continued reconstruction of reef coral phylogenies may
also resolve some of this variability.
Forecasting the future of coral communities and the usefulness of
a trait-based approach
A key question arising from our results is whether we can predict
shifts in coral communities on the basis of life-history strategies. We
hypothesise that while competitive species can dominate less
impacted reefs, increasing stress and disturbance from human
impacts (fishing, pollution and sedimentation) or environmental con-
ditions (thermal stress and ocean acidification) can lead to the loss of
these sensitive competitive corals and their replacement with stress-
tolerant, weedy and generalist species, which may be better able to
persist in unproductive conditions and recolonise disturbed reefs.
There is some evidence that shifts from competitive to stress-tol-
erant, weedy and generalist life histories have occurred on contem-
porary coral reefs. Following the precipitous loss of competitive
acroporid corals from Caribbean reefs in the 1970s, stress-tolerant
and generalist Montastraea corals dominated communities until dis-
ease, bleaching and other disturbances led to high mortality of
Montastraea and other stress-tolerant species (Alvarez-Filip et al.
2011). Currently, reefs are often dominated by weedy Agaricia and
Porites corals (Aronson et al. 2004; Green et al. 2008), although even
these species have experienced population declines, likely associated
with recruitment failure (Hughes & Tanner 2000). Furthermore,
weedy and generalist species went regionally extinct from the Carib-
bean during large-scale climate disturbances of the PlioPleistocene
(van Woesik et al. 2012), suggesting even more ‘hardy’ life histories
may be vulnerable to population losses. Such shifts away from
architecturally complex competitive species towards the simpler
morphologies of stress-tolerant, weedy and generalist life histories
may underlie the ‘flattening’ of Caribbean coral reefs observed in
the past decades (Alvarez-Filip et al. 2009, 2011) and may also be
associated with region-wide declines in Caribbean reef fish popula-
tions linked to habitat degradation (Paddack et al. 2009). Compara-
ble community shifts have been reported on Indo-Pacific reefs
(McClanahan et al. 2007; Rachello-Dolmen & Cleary 2007; Hughes
et al. 2012), although further studies are needed to fully evaluate
hypotheses of life-history replacement within coral assemblages.
Species traits are implicit in life-history theory, yet the lack of
quantitative, trait-based methods to classify life-history strategies has
impeded the evaluation and adoption of life-history frameworks
(Westoby 1998). There are advantages to identifying such frame-
works. Trait-based life-history strategies may contribute to the gen-
erality of community ecology through a more mechanistic
understanding of community assembly and species coexistence (e.g.,
McGill et al. 2006). Furthermore, objectively quantifying life-history
strategies directly from species traits may be a pragmatic approach
to predict the increasing impacts of environmental and anthropo-
genic stressors on diverse species assemblages. Here, we have pro-
vided an objective, statistical approach to identify life-history
strategies from species traits that can be applied to any ecological
community. Our findings in relation to corals are consistent with
findings for communities of plants, insects and fishes, which sug-
gests that there may be a limited number of life-history strategies
available to organisms (Stearns 1977; Grime & Pierce 2012). The
next step may be to simplify the assignment of species to concep-
tual strategies described by multiple traits by defining the axes of
life-history variation using single traits (e.g. the leafheightseed
strategy; Westoby 1998), which can allow for even more direct glo-
bal comparisons across species. Establishing simple and universal
frameworks of species life histories can be used to understand fun-
damental axes of life-history variation and identify general patterns
in community ecology.
N. Dulvy, C. Harley, D. Braun, S. Green, S. Anderson and the
Earth to Ocean research group at Simon Fraser University contrib-
uted to the conceptual framework and statistical analyses of this
project. We thank Andrew Baird, Sean Connolly, and three anon-
ymous reviewers for comments on the manuscript. ESD and IMC
were supported by the Natural Sciences and Engineering Research
Council of Canada; ESD was also supported by graduate funding
from Simon Fraser University. The Mexican Council of Science and
Technology (CONACYT; 160230) supported LAF. TAO acknowl-
edges the Palumbi research group at Stanford University. TRM was
supported by the Wildlife Conservation Society through grants from
the John D. and Catherine T. MacArthur Foundation.
ESD, LAF, TRM and IMC designed the study, ESD and TAO
collected data, ESD analysed the data; all authors contributed to
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©2012 Blackwell Publishing Ltd/CNRS
Letter Life-history strategies of reef corals 9
... Because coral species are expected to occupy delimited ecological niches distinguished by environmental preferences [7,29,42], we tested whether the spatial distribution of ecological windows would be reflected in coral competitive outcomes. In general, a deeper understanding of coral competition can help a better characterization of coral life-strategies, which at this stage predominantly relies on qualitative assumptions of species competitive abilities based on taxonomic traits and demographic performances [28,43]. A better understanding of coral competition can also inform on the ecological processes underlying species coexistence and the exceptional biodiversity of coral reefs. ...
... Coral overgrowth and overreach performances differed among taxa as expected for species exhibiting contrasting life-history traits, with differences in growth form and rate, in tentacle size and reach, etc. [23,34,43]. Yet, contrasting responses to ecological gradients provided deeper insights into distinct lifestrategies as reflected by different patterns of competitive performance across life-stages, as well as contrasting susceptibilities to environmental variation as reflected by segregated environmental optima. ...
... Larger battlefields were associated with higher overgrowth in some taxa, such as Millepora and Montipora (+2 cm in net overgrowth), showing high capacities in waging large-scale competitive endeavours to the detriment of others such as Porites, in which a threshold in the capacity to hold space against competitors was observed (−10 cm in net overgrowth, with again a sizethreshold at approximately 15 cm diameter, figure 3b). Overall, extended battlefield perimeters were associated with higher overgrowth performance in encrusting and columnar species and decreasing in branching and massive taxa, reflecting evolutionary differences in competitive abilities among morphological groups [24,43]. Figure 2. Changes in coral competitive performance as measured by net overreach distance along multiple ecological gradients, encompassing the effects of features associated with coral individuals (e.g. ...
Full-text available
Amidst global environmental changes, predicting species' responses to future environments is a critical challenge for preserving biodiversity and associated human benefits. We explored the original idea that coral competitive performances, the ability of corals to preempt ecological space on the reef through territorial warfare, serve as indicators of species’ ecological niches and environmental windows, and therefore, responses to future environments. Our surveys indicated that coral performances varied with taxonomic identity, size and position along environmental gradients, highlighting complex interplays between life-history, warfare-strategy and niche segregation. Our results forewarn that growing alterations of coastal environments may trigger shifts in coral dominance, with the decline of major reef-building taxa like acroporids, and emphasize the importance of limiting human impacts for coastal resilience. Our empirical approach untangles the complexity of species' battle-like interactions and can help identify winners and losers in various communities caught in the interplay between ecological niches, environmental windows and global changes.
... However, this is especially challenging in diverse ecosystems because of the numerous potential ways traits could combine and interact to govern resilience. The prevalence of important trade-offs among functional traits (Grime, 1977;Darling et al., 2012;Díaz et al., 2016) narrows down these possibilities and offers the opportunity to define predictive frameworks (Suding et al., 2008;Carturan et al., 2018). Combining conventional experimental approaches with trait-based frameworks is an optimal strategy to piece together multiple lines of evidence. ...
... The red, black, blue, and green dots represent the competitive, generalist, stress-tolerant, and weedy species, respectively (cf. Darling et al. (2012) classification). Biplot (B) describes the species density with color gradient and contour lines (based on kernel density estimation). ...
... The positive selection effect occurred because communities with higher FRic were more likely to have such morphologically complex and competitive species (Figure 5). Note that our categorization of competitive species is independent from, but similar to, those of Darling et al. (2012) (Figure 2). The selection effect was particularly important for communities dominated by morphologically simple species (i.e., with high PC.1) because higher FRic provided a chance to avoid total collapse; this is reflected in the significant and positive interaction between FRic and PC.1 for resilience rugosity and resilience cover (Figures 4C,F). ...
Full-text available
Within the Anthropocene the functional diversity of coral communities is changing rapidly, putting the resilience of many coral reef ecosystems in jeopardy. A better understanding of the relationship between coral functional diversity and reef resilience could reveal practical ways to achieve increased resilience. However, manipulating coral diversity experimentally is challenging, and consequently the links between coral functional diversity, resilience, and ecosystem functioning remain obscure. We used an ecologically detailed agent-based model to conduct a virtual experiment in which functional diversity was manipulated over the entire trait space of scleractinian corals. Using an imputed trait dataset of 798 coral species and eight key functional traits, we assembled 245 functionally distinct coral communities, which we subjected to a cyclone and bleaching event. We then measured four different aspects of their resilience and quantified for each measure the respective effect of (i) the functional richness (FRic), and (ii) community-weighted means (CWM) of four types of trait: effect, resistance, recovery, and competitive. FRic represents the volume occupied by a community in the functional space, while CWM indicates the location of the communities’ centroid in the functional space. We found a significant and positive effect of FRic on three measures of resilience: communities with higher FRic recovered surface cover faster and had more rugosity and cover 10 years after the disturbances. In contrast, the resistance of the coral community—i.e., the capacity to maintain surface cover when subjected to the disturbances—was independent of FRic and was determined primarily by the CWM of resistance traits. By analyzing community dynamics and functional trade-offs, we show that FRic increases resilience via the selection and the insurance effects due to the presence of competitive species in the functional space, i.e., those highly dominant species that contribute the most to the complexity of the habitat and recover quickly from disturbances. Building from the results of our experiment and the trait correlation analysis, we discuss the potential for FRic to serve as a proxy measure of resilience and we present a strategy that can provide direction to on-going reef restoration efforts, and pave the way for sustaining coral communities in a context of rapid global change.
... Further research is needed to identify whether the roles served by mangroves are also reflected in CMC types, and if these are geographically distinct. Many of the most commonly observed coral genera found in CMC habitats are considered stress tolerant (Siderastrea, Favia) or weedy (Porites, Manicina, Millepora, Agaricia) coral taxa [78,79], which have replaced more sensitive, competitive, branching coral genera on degrading reefs [79,80]. These coral species have life-history characteristics that allow them to thrive in patch, chronically disturbed environments [81], which may be why they are so common in mangrove fringe communities. ...
... Further research is needed to identify whether the roles served by mangroves are also reflected in CMC types, and if these are geographically distinct. Many of the most commonly observed coral genera found in CMC habitats are considered stress tolerant (Siderastrea, Favia) or weedy (Porites, Manicina, Millepora, Agaricia) coral taxa [78,79], which have replaced more sensitive, competitive, branching coral genera on degrading reefs [79,80]. These coral species have life-history characteristics that allow them to thrive in patch, chronically disturbed environments [81], which may be why they are so common in mangrove fringe communities. ...
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Marine ecosystems are structured by coexisting species occurring in adjacent or nested assemblages. Mangroves and corals are typically observed in adjacent assemblages (i.e., mangrove forests and coral reefs) but are increasingly reported in nested mangrove-coral assemblages with corals living within mangrove habitats. Here we define these nested assemblages as “coexisting mangrove-coral” (CMC) habitats and review the scientific literature to date to formalize a baseline understanding of these ecosystems and create a foundation for future studies. We identify 130 species of corals living within mangrove habitats across 12 locations spanning the Caribbean Sea, Red Sea, Indian Ocean, and South Pacific. We then provide the first description, to our knowledge, of a canopy CMC habitat type located in Bocas del Toro, Panama. This canopy CMC habitat is one of the most coral rich CMC habitats reported in the world, with 34 species of corals growing on and/or among submerged red mangrove aerial roots. Based on our literature review and field data, we identify biotic and abiotic characteristics common to CMC systems to create a classification framework of CMC habitat categories: (1) Lagoon, (2) Inlet, (3) Edge, and (4) Canopy. We then use the compiled data to create a GIS model to suggest where additional CMC habitats may occur globally. In a time where many ecosystems are at risk of disappearing, discovery and description of alternative habitats for species of critical concern are of utmost importance for their conservation and management.
... These varying responses to individual and repeat heatwaves are likely driven by differences in life history traits of coral taxa, a better understanding of which may allow for improved predictions of community responses to repeat heatwaves. For example, coral species that are weedy, stress-tolerant, or generalists (sensu Darling et al. 2012) may be more likely to survive a single heatwave relative to fast-growing competitive taxa (e.g., branching and plating Acroporids) due to differences ...
... in reproductive strategies (e.g., brooding vs. spawning), algal symbiont associations (e.g., flexible vs. rigid), and/or morphological differences (e.g., thick vs. thin tissues; branching vs. massive morphologies) (Loya et al. 2001;Darling et al. 2012). However, species-specific responses to repeat heatwaves (i.e., acclimatization vs. sensitization) are complex (Table 1), and a better understanding of which traits and environmental histories is more likely to lead down which trajectory is needed. ...
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Marine heatwaves are occurring more frequently as climate change intensifies, resulting in global mass coral bleaching events several times per decade. Despite the time between marine heatwaves decreasing, there is evidence that reef-building corals can develop increased bleaching resistance across repetitive marine heatwaves. This phenomenon of acclimatization via environmental memory may be an important strategy to ensure coral persistence; however, we still understand very little about the apparent acclimatization or, conversely, sensitization (i.e. stress accumulation or weakening) of reef-building corals to consecutive heatwaves and its implications for the trajectory and resilience of coral reefs. Here, we highlight that not only will some corals become stress hardened via marine heatwaves, but many other individuals will suffer sensitization during repeat heatwaves that further exacerbates their stress response during repeat events and depresses fitness. Under current and predicted climate change, it is necessary to gain a better understanding of the acclimatization vs. sensitization trajectories of different species and individuals on the reef, as well as identify whether changes in bleaching susceptibility relates to physiological acclimatization, trade-offs with other biological processes, and ultimately coral persistence in the Anthropocene.
... For instance, under high temperature stress coral species are able to avoid colony death following bleaching events by down-regulating caspase activity (Tchernov et al., 2011). Thus, at the expense of growth, this strategy might cause the least harm to the overall survival of the colony despite its weedy life-history (Darling et al., 2012). ...
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Ocean acidification (OA) poses a major threat to calcifying organisms such as reef-building corals, typically leading to reduced calcification rates. Mechanisms to compensate the effects of OA on coral growth may, however, involve processes other than calcification. Yet, the physiological patterns mediating coral growth under OA are not fully understood, despite an extensive body of literature characterizing physiological changes in corals under OA. Therefore, we conducted a three-month laboratory experiment with six scleractinian coral species (Acropora humilis, Acropora millepora, Pocillopora damicornis, Pocillopora verrucosa, Porites cylindrica, and Porites lutea) to assess physiological parameters that potentially characterize growth (calcification, volume, and surface area), maintenance (tissue biomass, and lipid and protein content), and cellular stress (apoptotic activity) response under ambient (pH 7.9) and low pH (pH 7.7). We identified genus- and species-specific physiological parameters potentially mediating the observed growth responses to low pH. We found no significant changes in calcification but species showed decreasing growth in volume and surface area, which occurred alongside changes in maintenance and cellular stress parameters that differed between genera and species. Acropora spp. showed elevated cellular stress and Pocillopora spp. showed changes in maintenance-associated parameters, while both genera largely maintained growth under low pH. Conversely, Porites spp. experienced the largest decreases in volume growth but showed no major changes in parameters related to maintenance or cellular stress. Our findings indicate that growth- and calcification-related responses alone may not fully reflect coral susceptibility to OA. They may also contribute to a better understanding of the complex physiological processes leading to differential growth changes of reef-building corals in response to low pH conditions.
... Acropora and other acroporids like Montipora are amongst the most sensitive scleractinian coral taxa to environmental stressors, including bleaching (Marshall and Baird 2000;Loya et al. 2001;van Woesik et al. 2011;Wilson et al. 2012;Clark et al. 2017). Along with other corals displaying 'competitive' life trait strategies (Darling et al. 2012), Acropora are often among the first corals to disappear in unfavourable and disturbed environments (Loya et al. 2001;McClanahan et al. 2007). However, they frequently exhibit steady recovery due to fast growth rates and high fecundity; studies have shown the complete recovery of Acropora populations following acute thermal stress, for example, after seven years in Palau (Golbuu et al. 2007) and in 15 year cycles in the Arabian Gulf (Riegl and Purkis 2009). ...
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Mass coral bleaching events may have disproportionate effects on branching corals, leading to coral community restructuring, reduced biodiversity, and decreased structural complexity. This affects overall reef health and resilience. Functionally important, fast-growing branching Acropora corals were a historically dominant and vital component of Indonesian reefs throughout the twentieth century, yet the genus is also one of the most vulnerable to external stressors. This study used long-term annual reef monitoring data from Indonesia’s Wakatobi Marine National Park (WMNP) to investigate the effects of a mass bleaching event in 2010 on Acropora and other branching corals, evaluate their post-disturbance recovery trajectories, and analyse shifts in coral community composition. Post-bleaching scleractinian coral cover decreased across study sites, with losses in branching corals especially evident. Long-term branching Acropora cover decreased significantly and failed to demonstrate the significant post-disturbance recovery of other branching corals (especially Porites). In areas characterised by relatively high branching Acropora cover (> 15% mean cover) prior to bleaching, long-term coral community composition changes have trended predominately towards branching and massive Porites and branching Montipora. The novelty and key contribution of this study is that results suggest suppressed recovery of Acropora in the WMNP. Contributing factors may include the Allee effect (inhibition of reproduction at low population densities), other forms of inhibited larval recruitment, direct and indirect spatial competition, and changes in the physical reef habitat. These findings have critical implications for this functionally important taxon, future reef conservation efforts, and overall reef health and resilience in the park.
... Thermal sensitivity is expected to vary with various coral morphologies and physiologies, life histories, and lead to considerable diversity of responses and adaptation rates (Wooldridge 2014, McClanahan et al 2020b. While there has been a focus on the symbiont-host interaction, there are multiple other life histories characteristics of corals that will be important influences on sensitivity and adaptation rates (Darling et al 2012, Van Woesik et al 2012, Torda et al 2017. ...
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A brief historical narrative of coral responses to climate change exposures is followed by a review of evidence. I trace the history of investigations and summarize the findings from 112 multiple-site field studies that examined environmental exposure variables and coral bleaching and mortality response relationships. A total of 59 environmental variables in 6 topic areas were studied of which excess thermal exposure was the most common topic and variable. Investigations were broadly classified into two categories; those focused on either excess thermal stress thresholds (TM) or on continuous variables (VM). The TM investigations considered a total of 28 variables, but only 1.7 ± 1.3 (SD) variables per publication, and only 11% completed a variable selection process that competed variables for fit or parsimony. The 65 VM publications considered 59 variables, more variables per publication (4.1 ± 4.3), and 43% of the studies followed a variable selection procedure. TM investigations received more citation and were most frequently used to identify future climate change impacts and sanctuaries. VM investigations often report excess heat threshold variables as weak single predictors of coral bleaching and mortality. Coral responses to exposure favors mechanisms of causation that are additive and interactive; specifically, the interactions between chronic and acute stresses within the geographic and habitat contexts of local environmental and coral genetic histories. Some of the potentially most important variables for predicting coral responses to exposure have seldom been studied or modelled. The implication is that the future status and health of coral reefs will be better than predicted by TMs. Moreover, impacts and sanctuaries are expected to be patchy and influenced by space, time, genetics, and taxa heterogeneity that will reflect a mix of avoidance, resistance, and recovery processes and their associated sanctuary locations.
... Mouillot et al., 2013;Madin et al., 2016), these have been largely limited to specific taxonomic groups (e.g. fish Brandl et al., 2016;Richardson et al., 2018] or scleractinian corals [Darling et al., 2012;Denis et al., 2017;McWilliam et al., 2018;Kubicek et al., 2019]). Relatively few take an ecosystem approach in applying trait or function schemes to the entire benthos. ...
Coral reef decline has accelerated in the last two decades resulting in substantial research into the phenomenon of ‘phase shifts’ or ‘regime shifts’. However, the conclusions drawn from this research have been varied. Some of this variability may stem from methodological approaches, although the extent to which these factors have shaped our understanding remain largely unexplored. To examine this, we conducted a systematic review of the literature. In doing so, we revealed marked variability in the approaches used for studying phase shifts. Notably, very few studies clearly defined what they meant by phase shifts. Therefore, we developed a clarified definition of phase shifts, which specifically defined persistence and dominance. The applicability of this definition was tested on multi-decadal benthic composition data on the Great Barrier Reef. The number of shifts depended critically on the definition selected, suggesting that this may be a primary reason underpinning the variability in past results.
... Following this line of reasoning, the immediate way how to test conceptual trade-off models has been the use of species' life history, morphological and physiological traits (Westoby and Wright, 2006). Several tests of the ECSS with three endpoint strategies using the life-history traits of insects (Greenslade, 1983), fish (Winemiller and Rose, 2011), corals (Darling et al., 2012) and vascular plants (e.g. Grime, 1997) found three major life-history syndromes conforming to the expectations of the triangular C-S-R model proposed by Grime (1977) (Fig. 1a). ...
The development of Ecological Strategy Schemes (ECSSs) reflects ecologists' long-standing efforts to identify repeatable patterns in nature. All the previous ECSSs are essentially spaces thought to be shaped by biological trade-offs among underlying organismal features. This has pushed research towards the identifications of the organismal trait syndromes setting the spaces’ limits. Recently, a stress tolerance trade-off space (STS) was put forth, defining the limits of abiotic stress tolerance strategies of woody plants worldwide. Here, we propose the STS as a tool for framing the abiotic stress tolerance landscape of woody plants using multiple ecological dimensions, such as traits and habitat climate. We used a recent conceptual framework proposed by Winemiller et al. on “periodic tables of niches” to propose developing a “periodic table” of abiotic stress tolerance of woody plants. We argue that the STS is an essential tool to do that as it allows for mapping important biological features in a single abiotic stress tolerance framework. Adopting this approach will shed light on the multidimensional nature of woody plants’ abiotic stress tolerance strategies.
... Corals with this growth form are still vulnerable to longer term, severe thermal stress events, which are predicted to recur at an increasing frequency in the near future. If these corals experience high levels of mortality, they are unlikely to be able to recover due to their slow growth rates and reproductive strategies (Darling et al., 2012). However, reefs may be able to survive at mid-depths, maintaining ecosystem functions and providing remnant populations for post-disturbance recovery. ...
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1. Urbanized coral reefs experience anthropogenic disturbances caused by coastal development, pollution, and nutrient runoff, resulting in turbid, marginal conditions in which only certain species can persist. Mortality effects are exacerbated by increasingly regular thermal stress events, leading to shifts towards novel communities dominated by habitat generalists and species with low structural complexity. 2. There is limited data on the turnover processes that occur due to this convergence of anthropogenic stressors, and how novel urban ecosystems are structured both at the community and functional levels. As such, it is unclear how they will respond to future disturbance events. 3. Here, we examine the patterns of coral reef community change and determine whether ecosystem functions provided by specialist species are lost post-disturbance. We present a comparison of community and functional trait-based changes for scleractinian coral genera and reef fish species assemblages subject to coastal development, coastal modification, and mass bleaching between two time periods, 1975–1976 and 2018, in Nakagusuku Bay, Okinawa, Japan. 4. We observed an increase in fish habitat generalists, a dominance shift from branching to massive/sub-massive corals and increasing site-based coral genera richness between years. Fish and coral communities significantly reassembled, but functional trait-based multivariate space remained constant, indicating a turnover of species with similar traits. A compression of coral habitat occurred, with shallow (<5 m) and deep (>8 m) coral genera shifting towards the mid-depths (5–8 m). 5. We show that although reef species assemblages altered post disturbance, new communities retained similar ecosystem functions. This result could be linked to the stressors experienced by urban reefs, which reflect those that will occur at an increasing frequency globally in the near future. Yet, even after shifts to disturbed communities, these fully functioning reef systems may maintain high conservation value.
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Approximately half of the Caribbean Oligocene reef coral fauna became locally extinct during the Early Miocene; roughly two thirds of the genera driven to local extinction still survive in the Indo-Pacific. Coral genera with lecithotrophic larvae (brooders) preferentially survived, over those with planktotrophic larvae (broadcasters). Among 37 genera for which we inferred reproductive mode, 73% of brooding genera survived the Oligocene/Miocene extinction events, while only 29% of the broadcasting genera survived. The proportion of brooders to broadcasters also increased markedly. During the late Oligocene, 47% of Caribbean reef coral genera were broadcasters, but in the middle Miocene, only 32% of the genera were broadcasters. Survivorship in Puerto Rican reefs was correlated with tolerance of cold and turbid conditions. Genera tolerant of both cold water and turbidity had much higher survival rates than those tolerant of turbidity alone. Only 25% of the genera that could tolerate neither cold water nor turbidity survived. Most of the eurytopic genera were brooders, while most of the stenotypic genera were broadcasters. We present two hypotheses that may account for the preferential survivorship of brooders: the recruitment hypothesis, and the dispersal hypothesis. The recruitment hypothesis holds that brooders survive preferentially because lecithotrophic larvae have higher recruitment success than do planktotrophic larvae in marginal habitats, such as upwelling zones. This is supported by the correlation of brooding and eurytopy. The dispersal hypothesis suggests that brooders survive preferentially because lecithotrophic larvae, which typically inherit zooxanthellae from the egg, have a longer larval lifespan and, hence, a wider potential dispersal range, than planktotrophic larvae, which typically capture zooxanthellae from the water column. Biogeographic range data, however, do not support this second hypothesis: modern Indo-Pacific brooding and broadcasting genera have nearly identical ranges, and many brooding species have narrower longitudinal ranges than do broadcasting species. Preferential survivorship of brooding corals contrasts sharply with survivorship patterns among molluscs during extinction events; among molluscs, broadcasters are favored over brooders. A major increase in upwelling at the Oligocene/Miocene boundary was probably responsible for this extinction/geographic restriction event. Preferential survival of brooding and mixed mode coral genera appears to be a product of their being better able to recruit and survive in marginal conditions such as upwelling zones.
In Florida the functional-group approach provided new insights into the manner in which varying levels of disturbance affected species richness across sites. Despite the chaotic patterns in biomass displayed by each assemblage of coral species when separately plotted across reefs, each functional group of corals responded to direct and indirect gradients of disturbance in a orderly and group-specific manner. Functional groups displayed a nested distributional pattern, indicating that negative interactions between functional groups are probably weak. Terrestrial and marine ecologists have found that a functional group approach can accurately predict how organisms will respond to changes in environment conditions. A functional group approach categorizes organisms, regardless of phylogeny, according to similarities and differences in life history and other ecologically relevant traits. One such model, the "CSR plant strategy theory" developed by Phillip Grime in 1973 for terrestrial plants, predicts the assemblage structure of biota over gradients of stress and disturbance. To test the CSR model, coral assemblages on reefs from Florida and Bermuda were assessed at the hierarchical levels of species and functional groups. The data were used to address the question of whether the functional-level approach provides information about community structure that species-level analysis fails to provide. Additionally, the predictions of the CSR model were tested regarding how coral cover, species diversity and assemblage structure should vary in habitats characterized by differing levels of disturbance and resource-limitation. In Bermuda, functional groups of corals also displayed a nested pattern across sites located over a range of depths and reef zones. When species were aggregated according to shared habitat, species from the same genus co-occurred in almost every case. This implies that these closely related species also share many functional traits and yet still coexist in many habitats. The Adaptive Strategies Theory provides a series of simple, testable hypotheses that can be used to guide ecological research in an iterative and informative manner. The Adaptive Strategies Theory is a powerful theoretical framework, which can be modified to give it great heuristic value for guiding ecological research.
Initial conditions can generate differences in the biotic composition of spatially disjunct communities, but intense, large-scale perturbations have the potential to reduce or eliminate those historical differences. The latter possibility is of particular concern with respect to coral reefs, which have undergone dramatic changes in the last 25-30 years. This paper reports a case in which two reef systems with different biotic histories were recently perturbed to a single, novel state. We compared millennial-scale records of species dominance from reefs in Bahia Almirante, a coastal lagoon in northwestern Panama, to previously published records from reefs in the shelf lagoon of Belize. Reef cores extracted from Bahia Almirante at 5-10 in water depth revealed that the Panamanian reefs were persistently dissimilar from the Belizean reefs for at least 2000-3000 years prior to the last several decades. The Panamanian reefs were dominated continuously by branching finger corals, Porites spp. (primarily P. furcata). Shifts from the Porites-dominated state to dominance by other coral species were rare, were restricted to small areas, and lasted for decades to centuries. The Belizean reefs were dominated continuously by the staghorn coral Acropora cervicornis in the same depth range during the same period. Excursions from the Acropora-dominated state were again rare and spatially localized. Populations of Ac. cervicornis in the Belizean lagoon were nearly extirpated by an outbreak of white-band disease in the late 1980s, and changes in water quality were apparently detrimental to branching Porites in Bahia Almirante in recent decades. These large-scale perturbations caused the two reef systems to converge on a third, historically unprecedented state: dominance by the lettuce coral Agaricia tenuifolia. Ag. tenuifolia possesses life-history attributes and environmental tolerances that enabled it to become dominant in both disturbed ecosystems. Although the two phase shifts to Ag. tenuifolia differed in both their general mechanisms and specific causes, they had the effect of eliminating the salient difference in benthic composition between the Panamanian and Belizean reefs. The changes in species composition thus obliterated the influence of several thousand years of reef history.