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Caribbean coral reefs are becoming structurally simpler, largely due to human impacts. The consequences of this trend for reef-associated communities are currently unclear, but expected to be profound. Here, we assess whether changes in fish assemblages have been non-random over several decades of declining reef structure. More specifically, we predicted that species that depend exclusively on coral reef habitat (i.e., habitat special- ists) should be at a disadvantage compared to those that use a broader array of habitats (i.e., habitat generalists). Analysing 3727 abundance trends of 161 Caribbean reef-fishes, surveyed between 1980 and 2006, we found that the trends of habitat-generalists and habitat-specialists differed markedly. The abundance of specialists started to decline in the mid-1980s, reaching a low of ~60% of the 1980 baseline by the mid-1990s. Both the average and the variation in abundance of specialists have increased since the early 2000s, although the average is still well below the baseline level of 1980. This modest re- covery occurred despite no clear evidence of a regional recovery in coral reef habitat qual- ity in the Caribbean during the 2000s. In contrast, the abundance of generalist fishes remained relatively stable over the same three decades. Few specialist species are fished, thus their population declines are most likely linked to habitat degradation. These results mirror the observed trends of replacement of specialists by generalists, observed in terrestrial taxa across the globe. A significant challenge that arises from our findings is now to investigate if, and how, such community-level changes in fish populations affect ecosystem function.
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Simplification of Caribbean Reef-Fish
Assemblages over Decades of Coral Reef
Lorenzo Alvarez-Filip
*, Michelle J. Paddack
, Ben Collen
, D. Ross Robertson
Isabelle M. Côté
1Unidad Académica de Sistemas Arrecifales, Instituto de Ciencias del Mar y Limnología, Universidad
Nacional Autónoma de México, Puerto Morelos, Quintana Roo, México, 2Department of Biological
Sciences, Simon Fraser University, Burnaby, BC, V5A 1S6, Canada, 3Department of Biology, Santa
Barbara City College, Santa Barbara, California, 93109, United States of America, 4Centre for Biodiversity
and Environment Research, University College London, Gower Street, London, WC1E 6BT, United Kingdom,
5Smithsonian Tropical Research Institute, Balboa, Republic of Panamá
Caribbean coral reefs are becoming structurally simpler, largely due to human impacts.
The consequences of this trend for reef-associated communities are currently unclear, but
expected to be profound. Here, we assess whether changes in fish assemblages have
been non-random over several decades of declining reef structure. More specifically, we
predicted that species that depend exclusively on coral reef habitat (i.e., habitat special-
ists) should be at a disadvantage compared to those that use a broader array of habitats
(i.e., habitat generalists). Analysing 3727 abundance trends of 161 Caribbean reef-fishes,
surveyed between 1980 and 2006, we found that the trends of habitat-generalists and
habitat-specialists differed markedly. The abundance of specialists started to decline in
the mid-1980s, reaching a low of ~60% of the 1980 baseline by the mid-1990s. Both the
average and the variation in abundance of specialists have increased since the early
2000s, although the average is still well below the baseline level of 1980. This modest re-
covery occurred despite no clear evidence of a regional recovery in coral reef habitat qual-
ity in the Caribbean during the 2000s. In contrast, the abundance of generalist fishes
remained relatively stable over the same three decades. Few specialist species are
fished, thus their population declines are most likely linked to habitat degradation. These
results mirror the observed trends of replacement of specialists by generalists, observed
in terrestrial taxa across the globe. A significant challenge that arises from our findings is
now to investigate if, and how, such community-level changes in fish populations affect
ecosystem function.
PLOS ONE | DOI:10.1371/journal.pone.0126004 April 14, 2015 1 / 14
Citation: Alvarez-Filip L, Paddack MJ, Collen B,
Robertson DR, Côté IM (2015) Simplification of
Caribbean Reef-Fish Assemblages over Decades of
Coral Reef Degradation. PLoS ONE 10(4):
e0126004. doi:10.1371/journal.pone.0126004
Academic Editor: Christopher J Fulton, The
Australian National University, AUSTRALIA
Received: November 7, 2013
Accepted: March 27, 2015
Published: April 14, 2015
Copyright: © 2015 Alvarez-Filip et al. This is an
open access article distributed under the terms of the
Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any
medium, provided the original author and source are
Funding: Compilation of the original database by
MJP was funded by the UKs Natural Environment
Resource Council, NE/C004442/1. LA-F was
supported by the Mexican Council of Science and
Technology (CONACYT; 160230), and by the Natural
Sciences and Engineering Council of Canada
(NSERC). BC is supported by the Rufford
Foundation, IMC is funded by a Discovery Grant from
NSERC, and DRR is supported by the Smithsonian
Tropical Research Institute. The funders had no role
in study design, data collection and analysis, decision
to publish, or preparation of the manuscript.
Habitat degradation modifies the structure of ecological assemblages by altering biotic interac-
tions and ecosystem dynamics. The extent of a speciesreliance on specific habitat features is
one of the characteristics that should determine how well it will fare under most scenarios of
habitat change [1,2]. While habitat specialists should be relatively sensitive to the degradation
of their preferred habitat, generalists may be less affected, or could even benefit from new habi-
tat arrangements or from the reduction in abundance or disappearance of other species (i.e.,
predators and competitors) via ecological compensation [3,4]. Across various taxa and geo-
graphical regions, specialist species appear to be declining and experiencing higher extinction
risk in response to habitat change compared to generalist species, leading to homogenization
and simplification of communities over time [5]. Measuring how species or groups of function-
ally similar species within communities differ in their responses to habitat change is therefore
crucial to understand and predict the consequences of habitat loss and environmental degrada-
tion for species assemblages and ecosystem functioning. In fact, trends in the abundance of
specialist species are now used as national and international indicators of development sustain-
ability (e.g., [6]).
Coral reefs are changing rapidly, worldwide. This is particularly evident in the Caribbean
where the structural complexity of many reefs has greatly declined, due to loss of coral cover
and changes in the composition of coral assemblages [79]. The ecological repercussions of
long-term decline in architectural complexity are likely to be substantial. For many reef fishes
and invertebrates, the risk of predation is influenced by access to refuges; thus, the richness,
abundance and biomass of these species are influenced by habitat complexity [10,11]. The con-
sequences for coral reef fishes are of particular concern because this group plays key roles in
ecosystem functioning (e.g., [12,13]) and reef fisheries are important for the livelihood of many
human coastal communities [14]. In a large-scale meta-analysis, Paddack et al. [15] found that
since the late 1990s the overall density of Caribbean reef fishes has declined consistently across
the region. This reduction was attributed in part to declines in coral cover and reef complexity,
which began as early as the 1970s [7,16].
Species seldom all respond similarly to changes in habitat. In the Indo-Pacific region, for ex-
ample, a variety of species in a range of taxa depend nearly exclusively on live coral for food or
shelter and, predictably, these specialists have often declined more precipitously in response to
coral loss than less dependent species [10,1719]. In the Caribbean, very few reef fishes are as
heavily reliant on live corals as their Indo-Pacific counterparts [20]. However, this does not
mean that all Caribbean reef fishes are generalists. Ecological specialization is not a dichoto-
mous state but instead ranges along a continuum [21]. Caribbean reef fishes vary in terms of
the extent to which they use non-reef as well as reef habitats, and the extent to which they clear-
ly associate with specific features of reef structure or microhabitats (e.g., [2224]). The recent
changes in Caribbean reef fish density could therefore have been accompanied by shifts in rela-
tive abundance of slightly more and slightly less specialised species that are more subtle than
those observed in the Indo-Pacific region.
The rate of change in population size is one of the most sensitive metrics for assessment of
long-term biodiversity change [2528]. Changes in abundance provide information about both
variability and quantity of biodiversity (25,27), and can be used to detect shifts in community
composition (26) and to infer changes in habitats and/or intensity of threats, such as exploita-
tion (25). Here, we test the hypothesis that fishes that are more specialised in terms of coral
reef habitat use have declined more in abundance than have habitat-generalists at the same lo-
cations across reef distributed throughout much of the Caribbean. We apply a novel method
designed to measure the state of biodiversity based on species population trends [29] to a large,
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Competing Interests: The authors have declared
that no competing interests exist.
regional-level database of temporal variation in the abundances of Caribbean reef fishes to ex-
amine large-scale trends of change in habitat-specialists and habitat-generalists. Furthermore,
by examining the trends for fished and unfished species in those two groups, we test whether
any differences in trajectories are attributable to fishing rather than causes such as changes in
habitat structure.
Database and species grouping
We used a subset of the database that was compiled by Paddack et al. [15] of temporally repli-
cated, quantitative data on Caribbean reef fish density (individuals m
) from in situ surveys
conducted by trained scientific observers (see details in Paddack et al. [15]). To be included,
each study needed to have (i) reported a density estimate of at least one reef fish species from a
reef site within the Caribbean region, (ii) surveyed the same species at the same site over more
than one year, and (iii) replicated measurements during each survey. In the current analysis we
used only common species, which we defined as those observed in at least 50% of the surveys
in a time series. With this restriction, we aimed to control for the potentially influential effect
of zero-density values in short (25 years) time series.
Specialization can be quantified by measuring the narrowness of use of a particular gradient
of resource or habitat [25]. Because no Caribbean fish species relies exclusively on live corals
and very few are closely associated with live coral [30,31], we based our specialization catego-
ries on the strength of association with coral reef habitat in general. Thus we classed as special-
iststhose species that are only found on coral reefs, and as generalists, those species that are
associated with a broader range of habitat types, including less complex habitats such as sea-
grass beds, gorgonian fields, sponge beds and macroalgal stands. For our analyses we used the
specialist/generalist assignation of species made by Luiz et al. [32] who categorized fish species
using data on habitat-use and latitudinal-range obtained from bibliographic sources and online
databases, supplemented with field records (see Luiz et al. [32] for details). Species were classi-
fied as specialists or generalists prior to analyses and before exploring the general trends from
each group in the database. In total we categorized 81 species from 27 families as habitat-spe-
cialists and 80 species from 26 families as habitat-generalists (S1 Table). Fish species in each of
the two habitat-use groups were also separated into two sub-groups based on their level of ex-
ploitation. We obtained the fishing status categorization from Paddack et al. [15] and FishBase
[33]. Unfished species included those that are not marketed, have unknown fishing status, or
are targeted only lightly by the aquarium trade. Fished species included those that are marketed
as food-fish or are heavily targeted by the aquarium trade.
The majority of the data came from studies that methodically collected abundance estimates
for many species in each reef fish assemblage (see [15]). As such, our study is unlikely to over-
represent species of special interest (e.g., threatened species), which is a common caveat in
studies of this kind (e.g., [29,34]).
Trend analysis
To generate overall density trends for habitat-specialist and habitat-generalist species we used
an aggregated index of change in abundance. This index of abundance was developed to pro-
vide scientists, policy-makers, and the general public with information on trends in the abun-
dance of vertebrate populations across the globe [35]. This index represents an effective
heuristic instrument for indicating trends in global biodiversity [29], and has been adopted as a
key indicator of the state of global biological diversity at the international level [28,36]. In
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addition, it can be used to evaluate broad scale trends for biogeographic realms, biomes, habi-
tats, and particular taxonomic groups (e.g., [29,34]).
We outline the main steps for abundance-index computation here, although a more thor-
ough description of the method and equations is provided in S1 Appendix. For each time se-
ries, the change in density from each year to the next was calculated. In the case of incomplete
time series, zero values were replaced by one percent of the mean population value for the
whole time series, and missing values for yearly censuses were derived from interpolation of
the preceding and the subsequent years with measured values (see [29]). Missing value interpo-
lations were applied to most of the time series, given the gaps in data collection in the majority
of monitoring schemes (S1 Fig). Two different methods were then used to generate estimates
of change for each time series: log-linear models (the chain method in Loh et al. [35]) were
used to compute values for short time series (n <6 time intervals; 70% of the total), and gener-
alized additive models were used to compute values for all other time series. The use of this
smoothing approach accounts better for non-linear variation [29,37].
Trends of all populations of the same species were averaged to produce species-specific
trends. The average rate of change in each year across all species was then calculated. Finally,
the average annual species change in each year was chained to the previous year to generate a
continuous index, starting with an initial value of 1 in the first year of the database, which was
1980 in this study. All populations within species were given equal weight in the calculation of
species-specific trends because we had no information on the relative importance of different
populations to region-wide species abundance. Similarly, each species contributed equally to
the calculation of the index. An advantage of giving equal weighting to all species is that com-
mon species or highly abundant populations do not have a disproportionate influence on the
index trajectory. Separate indices were computed for habitat-specialist and habitat-generalist
species and then, for fished and unfished species within each of those two habitat-use groups.
The uncertainty of the index estimates was assessed with bootstrapped 95% confidence in-
tervals (CI). For each year, 1000 index values were calculated from randomly sampled species-
specific population changes [35]. We considered a divergence of the overall trend as significant
when the CI did not encompass the overall population baseline (i.e., Index of Abundance = 1).
Results and Discussion
Our analysis included 3727 population trends for 161 common reef fishes from sites distribut-
ed throughout the wider Caribbean region (Fig 1A). As is common in this type of study, the
number of sites and times series represented in the analyses tended to increase over time (Fig
1B and 1C); however, the geographical representativeness of the data has been regionally com-
prehensive since the 1990s (S1 Fig). We found that abundance trends differed markedly be-
tween habitat-generalists and habitat-specialists. The abundance of specialists began declining
in the mid-1980s, reaching a low of ~60% of the 1980 baseline abundance by the late-1990s
(Fig 2A). Average abundance and variation have increased somewhat since the early 2000s, al-
though the average is still well below the baseline level of 1980. In contrast, the abundance of
generalist species has remained relatively stable since 1980, with a marked but non-significant
upswing since 2000 (Fig 2B). The trends of change of specialists and generalists were signifi-
cantly different from each other between late-1980s and late-1990s, but the differences became
less apparent during the 2000s due to the high variability associated with both trends (see CIs
in Fig 2A and 2B; and S2 Fig). The patterns uncovered here are not due to the presence of dif-
ferent time series in different parts of the study period. Monitoring at many sites used in the
analyses ceased or began in the late-1990s (S1 Fig); however, when only time series that span
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most of the study duration are used, the average trends are similar, albeit with larger confidence
intervals owing to the smaller sample sizes (S3 Fig).
The decline of habitat-specialist fishes we find here began soon after periods of rapid de-
clines in coral cover and reef complexity during the early 1980s [7,16,38](S4 Fig). The wide-
spread mortality of morphologically complex, branching Acropora corals in the Caribbean,
owing to white-band disease starting in the mid-1970s [39], likely accounts for some of these
early changes to reef habitats. Caribbean Acropora reefs tend to support higher fish abundance
and species richness than areas with lower structural complexity [40]. Thus, it is likely that the
near-disappearance of these corals from many areas reduced drastically the amount of a major
structural habitat feature throughout the 1980s [39], and affected populations of a number of
reef fishes. While it is not possible to determine whether the decline of specialist species began
before 1980, the ~45 years of relative stability at the start of the temporal trend suggest that
populations of those species were not already undergoing a steep decline at that time (Fig 2A).
Thus, specialist species may have experienced a lagged response to the loss of reef complexity,
which started a few years earlier ([7,16]; Fig 2A). Several factors may have contributed to this
delayed effect: (i) a lag in the degradation of microhabitat structure sufficient to have a mea-
sureable effect on specialist populations; (ii) reduced recruitment by fishes that need fine-scale
structure as settlement microhabitat; and (iii) reductions in survivorship and/or reproductive
output of specialists, owing to loss of shelter or food resources [10,17,41].
The decline in abundance of habitat-specialists continued steadily through the 1990s, with
some evidence of modest recovery since 2000 (Fig 1A). This pattern of increase is unlikely to
be the result of any improvement in habitat quality on Caribbean reefs, as it occurred in a de-
cade when, at the regional scale, coral cover remained relatively low and reef architectural com-
plexity declined steeply [7,16,38](S4 Fig). The overall increase in the index values of specialist
species in the 2000s is accompanied by an increasing variance (Fig 2A): while some populations
were recovering, many more were continuing to decline (Figs 3and 4). Biological traits and
geographic distribution are usually poor predictors of population change on a broad scale (e.g.,
[42,43]); hence we did not attempt to investigate the identity or location of the species driving
changes in the abundance of either specialists or generalists. However, we found no evidence
that the increasing trend during the 2000s is related to positive changes in the abundance of a
discrete subset of specialist species: most species show a mixture of declining and increasing
populations during the 2000s (Fig 3). There were some geographic differences in recovery,
with the Greater Antilles posting relatively more recovering than declining populations of habi-
tat-specialists during the 2000s (Fig 4). This pattern contributed to the large confidence inter-
vals that characterize all of the overall trends (Fig 2) in the last decade of the study period.
Understanding the reasons for this geographic pattern will require further investigation.
In contrast to specialist fishes, the abundance of generalists on Caribbean reefs has remained
relatively constant throughout the three decades spanned by this study (Fig 2B). This pattern
suggests that fishes in this group were not negatively affected by changes occurring on coral
reefs, and some may even have benefited from the reduced abundance of some other species
(e.g., of food competitors) and/or from the loss of reef architectural complexity [3,5,44]. Gen-
eralist reef fishes may have relatively plastic preferences for settlement microhabitats, allowing
them to recruit more successfully onto degraded reefs and alternative habitats than habitat spe-
cialists. For example, parrotfishes that sometimes exhibit strong recruitment associations with
Fig 1. Spatial and temporal distribution of time-series of abundance of Caribbean reef fishes. (A)
Location of the study sites is shown as black dots (note that one dot usually represents multiple reefs).
Numbers of time series (black dots) and sites (red bars) included in the Index of Abundance for (B) habitat-
specialists, and (C) habitat-generalists.
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specific coral microhabitats (e.g., [24]) also recruit onto macroalgae on reefs with low coral
cover [45]. It has been suggested that fishes at higher trophic levels (which are mostly general-
ists; S1 Table) might experience lagged reductions due to declines in habitat-dependent prey
fishes [10]. However, we did not find any evidence in support of this in our regional analysis.
The abundance of generalist species remained relatively constant independently of the declines
in the abundance of specialist species.
Fishing could be inferred to drive overall changes in Caribbean reef fish assemblages if
fished species declined while unfished species did not. We found no evidence for such a fishing
effect. Fished and unfished specialists show much the same abundance dynamics (Fig 2C vs.
2E). Note, however, that the uncertainty is high for exploited specialist fishes, probably due to
the relatively low sample size. This observation supports our view that declines in the abun-
dance of specialist species through the 1980s and 1990s were likely a consequence of reef degra-
dation. The trends of fished and unfished generalists are not significantly different from each
other (CIs overlap in Fig 2D vs. 2F). Although the uncertainty in the trends of both fishes and
unfished habitat-generalists is large, particularly over the last five years of the series (Fig 1F),
fished generalists increased distinctly more than unfished generalists during the last third of
the study period (Fig 2D). In a previous study, Paddack et al. [15] also found similar rates of
change of fished and unfished species in general, supporting the notion that fishing has not
been a main driver of the recent changes in the abundance of reef fishes. It remains possible
that fishing pressure and indiscriminate fishing methods may have affected unfished species in-
directly through bycatch or by altering food-web dynamics (e.g., predation release; [46]). How-
ever, such effects would be difficult to assess with our data.
The slight increase in abundance of many fished generalist species in the last decade of the
study is surprising because it is produced largely by significant increases in species of commer-
cial importance such as groupers and snappers (S5 Fig). Changes in fisheries management are
unlikely to be responsible for this pattern. The number and extent of species, gear and other ef-
fort restrictions vary widely across Caribbean nations [47]. For this reason, and because of
poor compliance and enforcement remain problems in the region [48], it seems unlikely that a
regional-scale increase in abundance of exploited generalist species is the result of multiple in-
dependent changes in national catch and effort regulations. Similarly, it is unlikely that the in-
creasing use of marine protected areas (MPAs) as fishery management tools (cf., [49]) explains
the increase in abundance of fished generalists. Only 8% of our time series stemmed from mon-
itoring sites in marine protected areas, and the number of populations from such sites actually
decreased over time (S6 Fig). The relative increase in abundance of fished species in the last
third of our study period may be a reflection of the time horizon of our study. Many of the pop-
ulations of exploited generalist species likely were already heavily depleted well before the start
of our study [50,51]. Hence, the increase we recorded since the turn of the millennium is likely
to be relatively small in comparison to original population sizes. That is, a shifting baselineef-
fect, due to a heavily depressed level at the start of the study (1980), may have amplified the ap-
parent size of any subsequent increase. Although it remains difficult to understand why this
mechanism would affect fished generalists more than their unfished counterparts, it is impor-
tant to remember that the apparent increase in abundance of fished generalists does not neces-
sarily indicate healthy populations of commercially important species, or that the negative
effects of fishing have ceased in the Caribbean. Fishing often truncates the age and size
Fig 2. Temporal trends in overall Caribbean reef fish abundance, relative to 1980 as depicted by the Index of Abundance. Plots show average
change (+/- 95% CI, see Methods), with dashed line at y = 1 indicating the 1980 value. The numbers of species and populations used to generate each panel
are indicated. (A) all habitat-specialists; (B) all habitat-generalists; (C) habitat-specialists targeted by fisheries; (D) habitat-generalists targeted by fisheries;
(E) unfished habitat-specialists; and (F) unfished habitat-generalists.
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Fig 3. Percentage of time-series (= populations) of each habitat-specialist species that declined
between the first and the last year of their monitoring period between 2000 and 2007. This time period
spans the apparent partial recovery of specialist species in the early 2000s (see Fig 2A). The total number of
time-series by habitat-specialist species is indicated in parentheses. The 72 species are ranked from the
highest to the lowest percentage of declining time-series. Habitat-specialist species with 50% or more of
declining time-series (black bars), and less than 50% (grey bars) are identified. In total, 557 populations
declined, 446 increased and 64 were stable (no change). Note that this figure does not show the magnitude
of the changes.
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structure of populations [52]. Thus, the trend of commercially important generalists might be
driven by increases in the abundance of small-sized individuals (e.g., juveniles) rather than in-
creases in individual size and biomass that are needed to effect population recovery. Shifts in
species composition from large-bodied to smaller-bodied species via a compensatory response
are also possible.
Our results indicate that Caribbean reef-fish assemblages have been experiencing profound
changes in community composition since 1980, probably largely due to habitat degradation.
We found evidence of an apparent replacement of habitat-specialists by generalist species over
a 30-year period. Such a shift is symptomatic of disturbed ecosystems around the world [4,6]
and, in some cases, results in large-scale spatial homogenisation of previously diverse species
assemblages [5,53]. The ecological replacement of specialized species by generalists could have
consequences for ecosystem integrity and function. For example, the loss of specialist species is
likely to reduce the variability in community responses to disturbances and environmental
change, and modify species interaction networks, which could result in the loss of key ecosys-
tem functions [1,5,21,54]. Further research assessing the links between habitat specialisation
and ecosystem functioning, in terms of species replacement triggering trophic cascades, alter-
ing energy flux, and changing functional redundancy, is crucial to fully understand the conse-
quences of habitat degradation for coral reef diversity and for the resources they provide to
Fig 4. Number of time series (= populations) of habitat-specialist species that show a decline, a recovery or remained stable between the first and
last year of their monitoring period. The data are presented by geographical region (as in S1 Fig) and for two time periods (1980s-1990s, and 2000s).
These two time periods were selected based on the overall trend of Fig 2A, which shows partial recovery of specialist species in the early 2000s. In the
1980s-1990s, a total of 443 populations declined, 351 increased and 42 were stable (no change). In the 2000s, a total of 562 species declined, 441
increased, and 64 remained stable. Note that this figure does not show the magnitude of the changes.
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Supporting Information
S1 Appendix. Calculation of the Abundance Index.
S1 Fig. Time series of data available from different census sites that, together, provided the
3727 populations included in this study. Each line showed the time span of a time series. Time
series are colour-coded by sub-region of the Caribbean to show the geographic spread of the data.
S2 Fig. Significance (pvalues) of the annual difference between the trends of habitat-gener-
alists and habitat-specialists shown in Fig 2A and 2B.pvalues were derived from T tests
comparing the final index values and 95% CIs of the specialist and generalist trends. The
dashed line shows the critical value below which differences are statistically significant.
S3 Fig. Temporal trends in the Abundance Index (+/- 95% CI, see Methods for calculations)
of habitat-specialist (left column) and habitat-generalist (right column) Caribbean reef-
fish species in long time-series that either stop in 1998 (top row) or span 1998 (middle
row). The baseline year is indicated by a dashed line. Panels (A) and (B) from Fig 2 are shown
to facilitate the visual interpretation.
S4 Fig. Long-term trajectories of change in coral cover, reef rugosity and habitat-specialist
fishes on Caribbean reefs. A) Region-wide changes in mean coral cover and reef rugosity
based on a meta-analysis of ecological studies across the Caribbean from 1977 to 2008 (Re-
drawn from Alvarez-Filip et al. 2011; Global Change Biol. 17:24702477). B) Temporal trends
in the overall abundance of habitat-specialist fishes, relative to 1980 as depicted by the Abun-
dance Index (Redrawn from Fig 2A). The grey dotted line indicates the year 2000, when at the
regional scale, the abundance of habitat-specialist fishes started to recover but coral cover and
reef rugosity continued to decline. The two panels derive from different data sources due to the
lack of site overlap between the habitat (coral cover and reef rugosity) and fish datasets.
S5 Fig. Temporal trends in aggregate abundance (Abundance Index, with 95% CI) of two
major taxa of commercially important Caribbean reef fishes: Serranidae (groupers) and
Lutjanidae (snappers). Baseline year is 1986 (dashed line at y = 1).
S6 Fig. Number of populations (i.e., time series) collected from inside (red bars) and out-
side (blue bars) Marine Protected Areas in the Caribbean in each year of the study. Between
1980 and 1988 all times series for inside MPAs are from only one study in Florida, USA. From
1991 to 2007, the number of studies contributing information for sites inside MPAs ranged be-
tween one and two, and represented only three other countries/territories (Saba, Costa Rica
and Curaçao). Due to the scatter spatial and temporal distribution of the data, it was not possi-
ble to further explore the trends of change inside MPAs with the Abundance Index.
S1 Table. Species included in this study, their habitat categorisation according to the use of
reef habitats. Specialists use only coral reef habitats, and generalists use coral reefs as well as
one or more other coastal habitats (classification from Luiz et al. 2012). Fishing status is from
Paddack et al. (2009). See Methods for description.
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Compilation of the original database by MJP was funded by the UKs Natural Environment Re-
source Council, NE/C004442/1. LA-F was supported by the Mexican Council of Science and
Technology (CONACYT; 160230), and by the Natural Sciences and Engineering Council of
Canada (NSERC). BC was partly supported by the Rufford Foundation. IMC is funded by a
Discovery Grant from NSERC. DRR is supported by the Smithsonian Tropical Research
Author Contributions
Conceived and designed the experiments: LAF IMC. Analyzed the data: LAF BC. Contributed
reagents/materials/analysis tools: LAF MJP DRR BC IMC. Wrote the paper: LAF MJP DRR BC
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... In many areas, Caribbean coral reef degradation far surpasses that of Indo-Pacific coral reefs, so the Caribbean has become the focal area for studies analyzing the response of reef fishes to this rapid loss of reef structural complexity. Long-term studies following species-specific responses to coral decline found that 43 out of the 72 fish species censused had experienced declines greater than 50% [21][22][23][24][25][26][27][28][29]. Other studies have found similar trends, with estimated density losses of 2.7-6.0% ...
... Previous studies have assessed reef fish community responses to coral decline [6,24,27,29] and the use of ARs [32,33,36,37,39], and predicted how reef fish communities may be structured in the future [31], but there is little research investigating how reef fish are utilizing the structures that remain in the Caribbean. The goal of the present study was to investigate how reef fishes utilize both natural and artificial structures, identify structural characteristics that may influence their use, and assess whether reef location and topographic complexity influence the use of structure by different functional feeding guilds. ...
... Each video was analyzed to identify both the fish species present and any behavioral interactions with the substrate including, but not limited to, using substrate for shelter or as a food resource. Fish species were classified into one of four functional feeding guilds (Table S1): herbivores, omnivores, invertivores, and piscivores [25,29,47]. Analysis of fish feeding guilds has been found to be adequate for comparing reef fish community structures and can distinguish functionally diverse communities from seemingly diverse communities that have functional redundancy [48][49][50]. ...
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Throughout the Caribbean, coral reefs are transitioning from rugose, coral-dominated communities to flat, soft coral-dominated habitats, triggering declines in biodiversity. To help mitigate these losses, artificial structures have been used to recreate substrate complexity and support reef inhabitants. This study used natural and artificial structures to investigate the factors influencing the use of habitat by reef fish. During 2018 and 2019, divers added artificial structures and monitored the fish assemblages associating with both the artificial structures and naturally occurring corals. Overall, there were more fish on natural structures than on artificial structures. While structure shape did not influence fish use, there was a non-significant trend for increased use of larger structures. Fish observations did not differ across a gradient of shallow, complex reefs to deeper, flatter reefs; however, analyses of feeding guilds revealed clearer patterns: herbivores and omni-vores were positively associated with low rugosity reefs where macroalgal abundance was higher, whereas invertivores preferred more rugose reefs. These results suggest that as reefs lose structural complexity, fish communities may become dominated by herbivores and omnivores. It also appears that the addition of artificial structures of the type used here may not mitigate the effects of structure loss on reef fish assemblages.
... In Bocas del Toro, Specialist species with unique functional roles were likely replaced by opportunistic and generalist species, as disturbance tends to favor fewer generalist species that can tolerate or adapt to new conditions and thus competitively dominate the ecosystem (Clavel et al., 2011;Darling et al., 2012;Alvarez-Filip et al., 2015). Generalist species like Orbicella faveolata, which increasingly dominated forereefs, can acclimate to novel environmental conditions created by high sea surface temperatures (Grottoli, 2014). ...
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Coral species, which function to build the framework structure of reef ecosystems, vary across sheltered to exposed environmental gradients. For centuries, conditions in sheltered environments that impact lagoonal reefs have been altered by local anthropogenic disturbances, while conditions in exposed environments that impact forereefs have largely buffered the effects of local anthropogenic disturbances. Yet, bleaching events induced by global anthropogenic disturbances challenge how we predict changes in reef composition and function across environmental gradients. Here, we quantify spatio-temporal variation in the composition and function of 11 coral reefs across sheltered to exposed environmental conditions over 15 years and 3 bleaching events in Bocas del Toro, Panama. We find that the composition and function of lagoonal reefs and forereefs were distinct and shaped by an environmental gradient altered by anthropogenic disturbance. Lagoonal reefs lacked major reef-building species and experienced greater losses in coral species and diversity over time. Although only lagoonal reefs changed in coral species composition, both lagoonal reefs and forereefs became functionally similar over time. Our findings indicate that lagoonal reefs may be less resilient to global environmental change than forereefs due to long-term effects of local anthropogenic disturbances. Additionally, increasing global anthropogenic disturbances might lead to the homogenization of reef function, as reefs adapt to novel environmental conditions.
... If the MPA exhibited significant changes in these indices, we assessed how variation at the species level contributed to observed trends. For this, we selected common species as those that were present in over 50% of the total surveys at each MPA (Cabo Pulmo = 21 out of 97 total species, Espíritu Santo = 26 out of 99 total species, Loreto = 27 out of 103 total species), in order to control the influence of zero-density values in short time series (Alvarez-Filip et al., 2015). Then, using data on presence and density (rounded to an integer), we performed individual generalized mixed effect models (GLMM) with binomial and negative binomial distributions, respectively (Zuur et al., 2009). ...
Conservation strategies, such as the establishment of Marine Protected Areas (MPAs), aim to safeguard biodiversity and to promote resilience of ecosystems by increasing their capacity to maintain key functions and processes following disturbance. However, the extent to which ecosystems in MPAs exhibit resilience remains debated. To address this question, we evaluated changes in reef fish species and functional diversity over time in relation to environmental and anthropogenic disturbances at multiple locations in the Gulf of California, Mexico. From 2005 to 2017, we assessed reef fish species richness and abundance in three MPAs: one no-take marine reserve (Cabo Pulmo) and two multi-use marine protected areas (MUMPAs: Espíritu Santo and Loreto). To examine change in functional diversity and composition, we calculated three functional diversity indices – functional richness, functional dispersion and functional originality – using six functional traits (size, mobility, activity, gregariousness, water column position, and diet). Species richness, density and functional diversity were maintained over time (resilience) in the no-take marine reserve. In contrast, MUMPAs showed temporal decline in species richness, which translated into decreases in functional richness and increases in functional dispersion. These differences were also observed at the species level: in Cabo Pulmo, only two ‘loser’ species declined in density, while Espíritu Santo and Loreto showed declines of 12 and 17 species, respectively. The two MUMPAs also shared 9 of the total 22 ‘loser’ species, which are generally abundant and common in the Gulf of California. Density declines were attributed to the combined effect of environmental (sea surface temperature and chlorophyll anomalies) and anthropogenic (fishing, tourism and coastal population density) disturbances. Given the regional decline and the ecological importance of dominant species, long-term decreases in their populations can profoundly modify processes and reef ecosystem services in this region. Thus, local management strategies should be implemented to try to reverse the observed recent decline in fish diversity in MUMPAs.
... CPNP is located off the southern tip of the Baja California peninsula (23°25′N, 109°25′ W) at the entrance of the Gulf of California, where tropical and subtropical waters mix (Fig. 1). Such a setting provides the conditions for a highly biodiverse ecosystem with species of different biogeographic provinces; it is the northernmost coral reef in the eastern Pacific (Alvarez-Filip et al. 2015). Cabo Pulmo is characterised by strong tidal mixing and the alternation of tropical and subtropical conditions (Zaitsev et al. 2014). ...
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In the southwestern Gulf of California one of the most successful marine protected areas (MPA) worldwide is found: Cabo Pulmo National Park (CPNP). Due to the level of protection and availability of prey, a large population of bull sharks (Carcharhinus leucas) exists in this MPA. Historical records about the abundance and distribution of these sharks in the park are scarce. Here we describe the movement patterns of 32 bull sharks within CPNP using a passive acoustic telemetry array (N = 13) located along the park to examine how the residency of the species change spatially and temporally. Environmental variables were taken in situ (HOBOs) and complemented with satellite information (MODIS aqua). The mean residence index (RI) was 0.365 (SD ± 0.2143). Sharks were resident from December to May, whereas they were absent from August to October. Most bull sharks preferred water temperatures below 28 ºC and depths as shallow as 14 m as well as deeper waters ranging from 70 to 160 m. They thus occupy a wide range of habitats with diverse prey, from shallow to mesophotic reefs. Differences in the residency of males and females occur in response to temperature during the different seasons, resulting in sexual segregation. Our results suggest that females segregate from males probably for reproductive reasons (pupping in another area) or to feed on more energy-rich prey resulting in increased growth rates. This study provides information germane to the protection and management of bull sharks in CPNP.
... En el caso de la Bahía de La Paz, una de las estrategias que representantes de gobierno y de organizaciones civiles han planteado como opción, es la llamada "jardinería coralina", que consiste en acelerar el proceso de reproducción y asentamiento del coral mediante el trasplante de colonias adultas sanas, provenientes de la misma zona, o de una parte del sistema que no haya sido perturbado en exceso. De esta manera, se trataría de mejorar el nivel de resiliencia del ecosistema mediante la reducción de la pérdida de estructura física, la cual es fundamental para mantener la biodiversidad local (Epstein et al., 2003;Alvarez Filip et al., 2015). ...
... En el caso de la Bahía de La Paz, una de las estrategias que representantes de gobierno y de organizaciones civiles han planteado como opción, es la llamada "jardinería coralina", que consiste en acelerar el proceso de reproducción y asentamiento del coral mediante el trasplante de colonias adultas sanas, provenientes de la misma zona, o de una parte del sistema que no haya sido perturbado en exceso. De esta manera, se trataría de mejorar el nivel de resiliencia del ecosistema mediante la reducción de la pérdida de estructura física, la cual es fundamental para mantener la biodiversidad local (Epstein et al., 2003;Alvarez Filip et al., 2015). ...
Resumen Las investigaciones sobre corales arrecifales se han desarrollado en la Bahía de La Paz desde el siglo XIX, y los avances en el conocimiento han sido sustanciales. Aquí presentamos una revisión de la información más relevante sobre las formaciones coralinas de esta región. Se discuten tópicos como historia de la investigación, 10
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Understanding the mechanisms that allow the permanence of coral reefs and the constancy of their characteristics is necessary to alleviate the effects of chronic environmental changes. After a disturbance, healthy coral reefs display trajectories that allow regaining coral cover and the establishment of framework building corals. Through a comparative approach, in a patch reef partially affected by a ship grounding, we analyzed the successional trajectories in affected and unaffected sectors. Fleshy algae (which do not promote the recruitment of corals) dominated the reef surface irrespective of the impact of the ship grounding incident. Acropora species had near-zero contributions to community structure, whereas non-framework building corals like Porites sp. had a slightly higher recruitment. Cover of coral and calcareous crustose algae decreased over time, and neither the latter nor adult coral colonies had any effect on the occurrence probabilities of small corals. Sea urchin (Diadema antillarum) densities were generally low, and thus unlikely to contribute to reverting algal dominance. The successional trajectories of the community in the impacted and non-impacted sectors of the coral patch reef agree with the inhibition successional model, leading to the development of a degraded state dominated by fleshy algae. It is probable that the stability and resilience of this degraded state are high due to the ability of fleshy algae to monopolize space, along with low coral recovery potential.
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The persistence and resilience of marginal shallow coral reefs at their limits of environmental tolerance have declined due to chronic environmental degradation and climate change. However, the consequences for the natural recovery ability of reefs of disturbance remain poorly understood. This study considered the potential for natural recovery through coral recruitment on fringing reefs across different geographic regions under contrasting environmental conditions in Puerto Rico. Reefs in areas with significant water quality degradation and more severe physical impacts of hurricanes were expected to have lower coral recruit density and diversity, and therefore less potential for recovery. Sixteen reefs were assessed across three geographic regions. Degraded reefs sustained a lower percentage of live coral cover and had higher macroalgae and turf algae abundance. Locations affected by high PO4, NH3+ and optical brightness concentrations, high turbidity, and high sea surface temperature anomalies, chlorophyll-a concentration and light attenuation Kd490 evidenced significantly lower coral recruit density and diversity. Hurricane-decimated reefs also exhibited impoverished coral recruit assemblages. Low coral recruitment could have important long-term implications under projected climate change and sea level rise, particularly in coastal urban habitats. There is a need to implement effective environmental conservation, ecological restoration and community participation strategies that facilitate enhanced coral recruitment success and assistedrecovery processes.
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Three-dimensional (3D) habitat complexity is a primary driver of organism distribution and community structure across ecosystems. Identifying the specific metrics and spatial scales at which complexity is functionally important for communities is therefore a critical component in forecasting ecosystem function. Here we pair fish species traits with multiple metrics from habitat photogrammetry to evaluate the most important measures and scales of 3D complexity driving ecological functions within one of the most structurally diverse ecosystems on the planet: coral reefs. From May to July 2019, we collected high-resolution (1 cm) large- and small-scale intra-habitat (25 m²) structural complexity data across eight reefscapes (∼2500 m²) and conducted co-located fish functional group surveys in the Florida Keys, FL, USA. We used a hierarchical clustering analysis to group 80 observed fish species by four traits related to habitat use (social level, body size, crypsis, activity period) and feeding guild to generate mechanistic predictions about fish-habitat relationships. Evaluating relationships between the resulting trait-based functional groups (k = 9) and four metrics of intra-habitat complexity (large-scale vertical relief, and small-scale vector ruggedness [VRM], VRM deviation, and profile curvature) revealed that trait groups respond independently to the various measures and scales of reef complexity. While large-scale complexity (relief) is strongly related to the presence of solitary, cryptic, nocturnal carnivores, likely due to prey availability as well as day-time refuge opportunities, herbivore abundance is unaffected by increasing vertical relief, potentially due to predator avoidance. Instead, gregarious (i.e., schooling) herbivores increase with small-scale complexity measured by VRM and VRM deviation across reefscapes, while less gregarious herbivores only respond to small-scale complexity when these same measures occur in low-relief habitat, possibly due to a tradeoff between grazing resource availability and predator visibility. Our results reveal how unique elements of complexity provided by both biotic benthic communities as well as large-scale habitat features like vertical relief are differentially important to fish functional groups. The general relationships we identified using traits provide a framework for predicting fish community responses to changes in specific measures of structural complexity on coral reefs globally. Our work illustrates how preserving 3D habitat complexity by protecting or augmenting (e.g., via restoration) structure-forming organisms can support diverse organismal communities and overall ecosystem productivity.
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Structural complexity provided by the living coral reef framework is the basis of the rich and dynamic biodiversity in coral reefs. In many cases today, the reduction in habitat complexity, from live coral to dead coral and rubble, has altered the abundance and diversity of many reef species with impacts on community structure, food webs and ecosystem functioning. Yet, the complex microhabitat provided by rubble can too support a great density and diversity of reef organisms, often with explicit roles in ecosystem functioning. This literature review synthesises available knowledge on the biology and ecology of coral rubble. We highlight key methodologies used to sample rubble communities, and the biological and ecological consequences of ongoing habitat degradation from coral to rubble reefs under future scenarios. We conclude with a number of key research themes that may enhance our capacity to understand the current contribution of rubble communities to reef functioning and predict their ability to modulate future impacts as net framework erosion amplifies.
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Individual adults of three Caribbean damselfishes defend feeding areas that do not overlap with those of conspecific adults. The feeding areas of adults of the two smaller species, Stegastes dorsopunicans and S. Planifrons, do not overlap interspecifically. However, feeding areas of adults of the largest species, Microspathodon chrysurus, are superimposed on feeding areas of adults and juveniles of the two Stegastes species. The large species aggressively dominates its smaller interspecific cohabitants. Cohabitant individuals of each species eat the same types of benthic microalgae. M. Chrysurus has the same daily cycle of feeding activity as the two small species, uses the same feeding microhabitats as they do, and feeds almost exclusively in their feeding areas. Cohabitants defend their feeding areas against the same set of other herbivorous fishes, but M. Chrysurus is involved in defensive actions much less frequently than is either of its small cohabitants. M. Chrysurus also is much less effective at such defense than at least one cohabitant, S. Dorsopunicians. S. Dorsopunicans on a reef from which M. Chrysurus were removed increased their body mass more and had larger fat deposits than conspecifics on a control reef. Thus adults of M. chrysurus appear to be dependents that use their size-based dominance ability to obtain food from their cohabitants. Juveniles of M. Chrysurus and S. Dorsopunicans exhibit small-scale habitat segregation and segregated use of feeding substrates in a shared microhabitat, which may facilitate the recruitment of both species.
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Predictive models of biodiversity change are required to inform conservation policy decisions.
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Climate change is generating novel communities composed of new combinations of species. These result from different degree of species adaptations to changing biotic and abiotic conditions, and from differential range shifts of species. To determin whether the responses of organisms are determined by particular species traits and how species interactions and communit dynamics are likely to be disrupted is a challenge. Here, we focus on two key traits: body size and ecological specialization. We present theoretical expectations and empirical evidence on how climate change affects these traits within communities. We then explore how these traits predispose species to shift or expand their distribution ranges, and associated changes o community size structure, food web organization and dynamics. We identify three major broad changes: (i) Shift in the distributio of body sizes towards smaller sizes, (ii) dominance of generalized interactions and the loss of specialized interactions and (iii) changes in the balance of strong and weak interaction strengths in the short term. We finally identify two majo uncertainties: (i) whether large-bodied species tend to preferentially shift their ranges more than small-bodied ones, an (ii) how interaction strengths will change in the long term and in the case of newly interacting species.
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Coral communities are changing rapidly worldwide through loss of coral cover and shifts in species composition. Although many reef-building corals are likely to decline, some weedy opportunistic species might increase in abundance. Here we explore whether the reshuffling of species can maintain ecosystem integrity and functioning. Using four common Caribbean reef-building coral genera we modeled rates of reef construction and complexity. We show that shifting coral assemblages result in rapid losses in coral-community calcification and reef rugosity that are independent of changes in the total abundance of reef corals. These losses are considerably higher than those recently attributed to climate change. Dominance patterns of coral assemblages seem to be the most important driver of the functioning of coral reefs and thus, the future of these ecosystems might depend not only on reductions of local and global stressors, but also on the maintenance of keystone coral species.
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Introduction 2 Methods 3 Spatial scale of climate vulnerability assessment 3 The three components of vulnerability 3 Exposure 4 Abstract Anthropogenic global warming has significantly influenced physical and biological processes at global and regional scales. The observed and anticipated changes in global climate present significant opportunities and challenges for societies and economies. We compare the vulnerability of 132 national economies to potential climate change impacts on their capture fisheries using an indicator-based approach. Countries in Central and Western Africa (e.g. Malawi, Guinea, Senegal, and Uganda), Peru and Colombia in northwestern South America, and four tropical Asian countries (Bangladesh, Cambodia, Pakistan, and Yemen) were identified as most vulnerable. This vulnerability was due to the combined effect of predicted warming, the relative importance of fisheries to national economies and diets, and limited societal capacity to adapt to potential impacts and opportunities. Many vulnerable countries were also among the world's least developed countries whose inhabitants are among the world's poorest and twice as reliant on fish, which provides 27% of dietary protein compared to 13% in less vulnerable countries. These countries also produce 20% of the world's fish exports and are in greatest need of adaptation planning to maintain or enhance the contribution that fisheries can make to poverty reduction. Although the precise impacts and direction of climate-driven change for particular fish stocks and fisheries are uncertain, our analysis suggests they are likely to lead to either increased economic hardship or missed opportunities for development in countries that depend upon fisheries but lack the capacity to adapt.
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Live corals are the key habitat forming organisms on coral reefs, contributing to both biological and physical structure. Understanding the importance of corals for reef fishes is, however, restricted to a few key families of fishes, whereas it is likely that a vast number of fish species will be adversely affected by the loss of live corals. This study used data from published literature together with independent field based surveys to quantify the range of reef fish species that use live coral habitats. A total of 320 species from 39 families use live coral habitats, accounting for approximately 8 % of all reef fishes. Many of the fishes reported to use live corals are from the families Pomacentridae (68 spp.) and Gobiidae (44 spp.) and most (66 %) are either planktivores or omnivores. 126 species of fish associate with corals as juveniles, although many of these fishes have no apparent affiliation with coral as adults, suggesting an ontogenetic shift in coral reliance. Collectively, reef fishes have been reported to use at least 93 species of coral, mainly from the genus Acropora and Porities and associate predominantly with branching growth forms. Some fish associate with a single coral species, whilst others can be found on more than 20 different species of coral indicating there is considerable variation in habitat specialisation among coral associated fish species. The large number of fishes that rely on coral highlights that habitat degradation and coral loss will have significant consequences for biodiversity and productivity of reef fish assemblages.
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Coral cover has declined on reefs worldwide with particularly acute losses in the Caribbean. Despite our awareness of the broad-scale patterns and timing of Caribbean coral loss, there is little published information on: (1) finer-scale, subregional patterns over the last 35 yr, (2) regional-scale trends since 2001, and (3) macroalgal cover changes. We analyzed the spatiotemporal trends of benthic coral reef communities in the Caribbean using quantitative data from 3777 coral cover surveys of 1962 reefs from 1971 to 2006 and 2247 macroalgal cover surveys of 875 reefs from 1977 to 2006. A subset of 376 reefs was surveyed more than once (monitored). The largest 1 yr decline in coral cover occurred from 1980 to 1981, corresponding with the beginning of the Caribbean-wide Acropora spp. white band disease outbreak. Our results suggest that, regionally, coral cover has been relatively stable since this event (i.e. from 1982 to 2006). The largest increase in macroalgal cover was in 1986, 3 yr after the regional die-off of the urchin grazer Diadema antillarum began. Subsequently, macroalgal cover declined in 1987 and has been stable since then. Regional mean (±1 SE) macroalgal cover from 2001 to 2005 was 15.3 ± 0.4% (n = 1821 surveys). Caribbeanwide mean (±1 SE) coral cover was 16.0 ± 0.4% (n = 1547) for this same time period. Both macroalgal and coral cover varied significantly among subregions from 2001 to 2005, with the lowest coral cover in the Florida Keys and the highest coral cover in the Gulf of Mexico. Spatio-temporal patterns from the subset of monitored reefs are concordant with the conclusions drawn from the entire database. Our results suggest that coral and macroalgal cover on Caribbean reef benthic communities has changed relatively little since the mid-1980s.
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Specialization is a concept based on a broad theoretical framework developed by evolutionary biologists and ecologists. In the past 10 years, numerous studies have reported that - in many contexts - generalist species are "replacing" specialist species. We review recent research on the concept of the ecological niche and species specialization, and conclude that (1) the observed worldwide decline in specialist species is predicted by niche theory, (2) specialist declines cause "functional homogenization" of biodiversity, and (3) such homogenization may be used to measure the impact of disturbance on communities. Homogenization at the community level could alter ecosystem functioning and productivity, as well as result in the deterioration of ecosystem goods and services. We propose community-level specialization as an indicator of the impact of global changes (habitat and climate disturbances) on biodiversity.