Shifts in coral-assemblage composition do not ensure persistence of reef functionality

Abstract

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.

Full text

Shifts in coral-assemblage composition
do not ensure persistence of reef
functionality
Lorenzo Alvarez-Filip
1
, Juan P. Carricart-Ganivet
2
, Guillermo Horta-Puga
3
& Roberto Iglesias-Prieto
2
1
Healthy Reefs Initiative, Puerto Morelos, Quintana Roo, Me
´
xico,
2
Unidad Acade
´
mica de Sistemas Arrecifales, Instituto de Ciencias
del Mar y Limnologı
´
a, Universidad Nacional Auto
´
noma de Me
´
xico, Puerto Morelos, Quintana Roo, Me
´
xico,
3
UBIPRO, Facultad de
Estudios Superiores Iztacala, Universidad Nacional Auto
´
noma de Me
´
xico, Tlalnepantla, Me
´
xico, Me
´
xico.
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.
C
oral reefs are biologically diverse ecosystems that provide goods and services, including coastal protection
and food security to a large human population. These benefits primarily rely on the ability of reef-building
corals to deposit large quantities of calcium carbonate and form complex three-dimensional structures. A
wide range of stressors including diseases, overfishing, pollution and climate change are now forcing many of
these ecosystems to move away from coral-dominated communities
1,2
. Probably, the most evident transitions on
coral reefs are the ecological shifts from coral to macroalgae-dominated states
3,4
, which have severe consequences
on carbonate budgets and reef complexity
2,5
. However, ecological shifts may also occur within guilds of founda-
tion species, as observed in tropical forest ecosystems
6,7
. Reef corals are a diverse group and present a wide range of
responses to environmental change, and while the populations of some coral species are likely to decrease, others
may remain stable or even increase. In the last few decades, coral communities have experienced unprecedented
modifications
8,9
. The Caribbean, for example, underwent rapid losses of the structurally important acroporid
corals from the white band disease epizootic in the late 1970s and early 1980s
10
. Since then, the spread of several
emergent diseases, combined with recent bleaching events and other biotic disturbances, resulted in high rates of
mortality in other major reef-building species, such as Orbicella spp.
11–13
(5 Montastraea, sensu Budd et al.
14
).
Throughout the Caribbean, the few species responsible for most of the structural complexity
8,15,16
have been now
replaced by opportunistic species
13,17
. Although we are only beginning to understand the consequences of these
ecological shifts, it is likely that they will affect structural complexity and functioning of coral reefs
1,2,13
.
A key question in this context is whether flexible patterns of dominance in coral communities can maintain reef
functionality under future climate change scenarios. Recently, based on the recognition that climate-related
pressures such as ocean warming and acidification do not affect all species equally
9,18
, it has been suggested that
ecosystem collapse is not necessarily the fate of coral reefs, because the populations of coral species that remain or
increase could maintain ecosystem integrity
19
. This interpretation assumes that both species sets have similar
functional attributes (e.g., reef-building capacity) despite differences in their physiological thresholds to envir-
onmental conditions. There is, however, little support for this assumption, as physiological attributes tend to be
strongly linked to ecological functioning, and therefore species reshuffling tends to produce significant changes in
ecosystem structure and functioning
20–22
.
The functioning of coral-reef ecosystems is in large part dependent on the life-history strategies of corals, as
they are strongly linked to the morphological and physiological attributes of the species
23
. For example, in the
Caribbean, coral species with brooding reproduction and high population turnover are generally tolerant to
OPEN
SUBJECT AREAS:
ECOLOGICAL
MODELLING
CONSERVATION
CORAL REEFS
CLIMATE-CHANGE ECOLOGY
Received
28 May 2013
Accepted
27 November 2013
Published
12 December 2013
Correspondence and
requests for materials
should be addressed to
R.I.-P. (iglesias@cmarl.
unam.mx)
SCIENTIFIC REPORTS | 3 : 3486 | DOI: 10.1038/srep03486 1

environmental change, but are predominantly small colonies that
contribute little to reef accretion or habitat provisioning. Whereas
massive corals that contribute considerably to calcium carbonate
accumulation, and serve as refuge substrate to many other species,
are expected to be less tolerant to variable environments
23
. The com-
position of species determines how the system responds to envir-
onmental change
6,24
and, in this context, we can expect that the loss of
certain species, or the loss of functional groups, severely compromise
reef function by reducing calcium carbonate production and decreas-
ing the complexity of reef topography.
Here we present a model of four Caribbean genera, which shows
how shifting coral assemblages influence coral community calcifica-
tion rates and reef rugosity. Considering that climate change is
perceived to be the major driver for the rapid decline of coral reefs
worldwide
1
, we also compare calcification variations derived from
changes in the dominance patterns of the coral assemblage, with those
attributed to ocean warming and ocean acidification. Although these
are simplified models of reef communities, we consider that they
provide a robust theoretical framework to assess the effects of species
turnover on ecosystem functioning.
Results
In the first model, which assess the effects of species turnover on reef
functioning, shifts in the composition and dominance of coral
assemblages result in rapid losses in coral community calcification
rates and reef rugosity, independent of changes in the total abund-
ance of reef corals (Fig. 1A, 1B). Reef calcification and topographic
reef structure were severely affected by the loss of Acropora and to a
lesser extent by the loss of Orbicella in both scenarios (steady coral
cover decline, and gradual coral cover increase; Fig. 1C). Even assum-
ing rapid increases in the abundance of other coral species, the loss of
Acropora was so important for reef development that community
calcification rates and reef complexity did not recover, resulting in a
reef with limited structural complexity. Only when coral cover
shifted from 10% Acropora to 45% Porites did reef rugosity show
signs of stability (Fig. 1C).
To compare community calcification variations resulting from
changes in the dominance patterns with those attributed to cli-
mate change and ocean acidification, we modeled a theoretical
coral community in which coral cover was maintained at a constant
52% (Fig. 2A). Our second model showed that the reductions in
10
8
6
4
2
0
1
1.2
1.4
1.6
1.8
2
1
0.5
0
A
B
C
Reef rugosity
Relative
abundance
Community calcification
(kg CaCO m yr )
3
-2
-1
ii
i
Time
Figure 1
|
Shifts in coral assemblages result in rapid losses in coral-community calcification and reef rugosity. Changes in community calcification and
reef structure in shifting coral assemblages of four genera ((A); left to right Acropora, Orbicella, Porites , Agaricia). (B) Relative abundances over time.
(C) Community calcification (continuous lines) and reef rugosity (dotted lines) in two hypothetical scenarios: (i) steady coral cover decline from 45% to
10% (red lines) and (ii) gradual coral cover increase from 10% to 45% (blue lines). Yellow band represents the current state of many Caribbean reefs.
Pictures in the figure where taken by R. I.-P. and H. Bahena-Basave.
www.nature.com/scientificreports
SCIENTIFIC REPORTS | 3 : 3486 | DOI: 10.1038/srep03486 2

calcification attributed to the effects of thermal stress and ocean
acidification result in comparatively minor changes, when compared
with the effect of changes in the patterns of dominance. These pat-
terns were only detected once the community was dominated by
opportunistic species (Fig. 2B). The extraordinary difference in the
calcification rates of the four genera employed in the second model
explains this difference in community calcification (Table 1). Similar
to the results of the first model (Fig. 1), the most dramatic change in
community calcification is derived from the rapid replacement of
Acropora by Porites and Agaricia, which resulted in a 56% loss of the
calcification potential of the community after only seven years
(Fig. 2B).
Discussion
In the Caribbean, the loss of a key reef-building species has substan-
tially reduced the structural and functional integrity of the reef.
Collectively, our models indicate that the reshuffling of coral species,
by itself, does not ensure coral-reef function. On the contrary, the
replacement of major reef-building coral species (i.e., losers) by
opportunistic forms (i.e., winners) drastically reduce the capacity
of the coral assemblages to deposit calcium carbonate at rates higher
than the rate of erosion. These changes will therefore compromise
the structural complexity of the ecosystem and the long-term
stability of reef-associated biodiversity
25
. Our first model shows that
only reef rugosity remains stable when coral cover shifts from 10% of
Acropora to 45% of Porites. Although reaching this scenario is pos-
sible with effective management policies
26
, the reef will still have low
structural complexity–similar to a degraded reef, and therefore the
ecosystem’s structure and functioning would still be compromised
5
.
The magnitude of the structural and functional losses portrayed by
our models may represent a de facto state transition, similar to the
transition from forest to grassland in terrestrial systems.
Shifts in the structure and composition of Caribbean coral com-
munities produced substantial changes in reef accretion and rugosity
beyond any recent effect attributed to climate change. Our second
model suggests that the loss of acroporids from many Caribbean
reefs represented a major loss in coral community calcification,
and that any recent effect attributed to thermal stress and ocean
acidification is comparatively minor. However, changes in the com-
position of species are in part driven by changes in the temperature
and chemistry of the oceans
18
, and thus the two effects shown in
figure 2 could synergistically influence the rates of calcification on
coral reefs. To increase our understanding of the possible trajectories
that reefs will follow under rapid climate change and ocean acidifica-
tion, it will be necessary to explore possible trade-offs between the
abilities of corals to deposit calcium carbonate and their capacity to
tolerate thermal stress and ocean acidification. It has been shown that
corals harboring thermally tolerant symbiotic algae exhibit reduced
calcification rates when compared with specimens containing tem-
perature-sensitive symbionts
27
. This trait appears to be related to the
greater capacity of temperature-sensitive symbionts to provide the
host with the photosynthates required for calcification
28,29
. In this
context, acclimation to higher temperatures by acquiring thermally
tolerant symbiotic algae will further compromise the calcification
potential of the species.
Coral community shifts have also been reported in other regions of
the world, highlighting the need to fully understand how global
change is modifying reef structure in regions with a more diverse
and different array of coral assemblages
23
. Species richness may pre-
vent or delay ecosystem collapse in diverse ecosystems, as the prob-
ability that at least some species continue to function under changing
environments increases
19,30
. However, this only applies if the
increased number of species also increases the species responses to
environmental fluctuations (i.e., functional redundancy), and species
with different functional properties are maintained under the new
environmental conditions
30–32
. Because of inherent redundancy, it is
possible that the highly diverse coral reefs in the Indo-Pacific could
partially retain a degree of functionality under rapid changing envir-
onmental conditions, however, the evidence from the less-diverse
A
Cover per genus (%)
35
30
25
20
15
10
5
B
Community calcification
(kg CaCO m yr )
3
-2
-1
Time (years)
9
8
7
6
5
4
3
30201005 15 25
Figure 2
|
Shifting dynamics of a theoretical coral assemblage of four
genera with constant coral cover (52%). (A) Changes in coral cover per
genera through time. Acropora (red line) Orbicella, (blue line) Porites,
(black line) and Agaricia (green line). (B) Changes in community
calcification through time (red line). The shaded area in grey represents the
potential negative impacts on community calcification associated with
thermal stress and ocean acidification excluding coral bleaching and
assuming no changes in the coral assemblage. The red shaded area
represents the potential losses in community calcification due to ocean
warming and acidification.
Table 1
|
Mean extension rate (cm year
21
), mean density (g cm
23
),
estimated calcification rate (kg m
22
year
21
) and mean colony
rugosity of the four genera used to construct the modeled hypothet-
ical scenarios presented in figures 1 and 2. Acropora 5 A. palmata
1 A. cervicornis, Orbicella 5 O. annularis 1 O. faveolata, Porites
5 P. astreoides, and Agaricia 5 A. agaricites. In parenthesis the
number of colonies used to calculate mean colony rugosity per
genus
Genus
Extension
rate Density
Calcification
rate Colony rugosity
Acropora 8.84 6 4.33 1.88 6 0.26 22.30 3.33 6 1.31 (n 5 13)
Orbicella 0.85 6 0.32 1.59 6 0.25 13.80 1.87 6 0.44 (n 5 46)
Porites 0.41 6 0.13 1.48 6 0.16 6.12 1.49 6 0.40 (n 5 51)
Agaricia 0.25 6 0.04 1.92 6 0.05 2.43 1.52 6 0.43 (n 5 73)
www.nature.com/scientificreports
SCIENTIFIC REPORTS | 3 : 3486 | DOI: 10.1038/srep03486 3

Caribbean indicates that new coral assemblages are becoming domi-
nated by species with substantially reduced capacity to produce and
maintain reef framework
13,15,17
.
Total coral cover has been commonly used to assess changes in
coral-reef ecosystem condition or health
33,34
. However, our findings
imply that opportunistic coral species, although highly competitive
in impacted environments, will probably not have the capacity to
maintain reef development, even in communities with high coral
cover. Thus, important information regarding the current state
and recovery potential of coral reefs might be missing if all coral
species are clustered in one single category (i.e., coral cover).
Local-scale and regional assessment of the state of world’s coral reefs
should therefore aim to evaluate changes in composition and dom-
inance patterns of reef-building corals. Our models provide a sim-
plified view of the effects of the changing dominance patterns on the
potential of community calcification. Future analyses should incorp-
orate information about changes in the susceptibility of different
coral communities to the destructive forces of erosion. Recent ana-
lyses of the carbonate budget trajectories in Caribbean reefs under
several future scenarios, indicate that maintenance of positive reef-
carbonate budgets requires a combination of local conservation mea-
surements, effective fisheries management, and significant global
reductions in the emissions of greenhouse gases
1
. The future of coral
reefs will ultimately depend not only on the reduction of local and
global stressors, but also on management actions that guarantee the
survival and propagation of keystone reef-building coral species and
not just on those actions that focus on maintaining high coral cover.
Methods
Models. We generated two simple theoretical models that include four coral genera:
two important Caribbean reef-building corals, Acropora (A. palmata 1 A.
cervicornis) and Orbicella (O. annularis 1 O. faveolata), and two highly competitive
weedy corals that form smaller and less-complex colonies, Porites astreoides and
Agaricia agaricites. First, to assess the effects of species turnover on reef functioning,
we modeled changes in the relative abundance of these genera over time by simulating
species dominance turnovers. Identical Gaussian curves were used to model the
change in the relative abundance of Acropora, Orbicella, Porites and Agaricia
(Fig. 1A). Curves were lagged along the temporal axis following a successional order
in such a way that, at any point in time, the sum of all relative abundances was one
(Fig. 1B). Species succession was constructed following a hierarchical order in
calcification rates (Table 1), but it also resembled recent shifts in the composition of
coral species in the Caribbean. Community calcification and reef rugosity were
calculated at each point in time by weighing the mean calcification rate and colony
rugosity (see below for mean calcification rates and rugosity calculations) with the
relative abundance of each genus for two hypothetical scenarios: steady coral cover
decline from 45% to 10%, and increase from 10% to 45%. With this method we only
simulate the reef rugosity of these four genera, assuming that the rest of the reef is flat
(rugosity index 5 1).
Second, to compare community calcification variations derived from changes in
the dominance patterns of the coral assemblage with those attributed to climate
change and ocean acidification, we modeled a theoretical coral community in which
coral cover was maintained at a constant 52%, w hich is the mean coral cover for the
Caribbean in the late-1970s
33
(Fig. 2). In this model we simulated an exponential loss
of Acropora with a rate constant of 3.5% year
21
, a reciprocal increase in the relative
abundance of Porites and Agaricia, and a linear reduction in the relative abundance of
Orbicella. The species turnover employed in the simulation is consistent with the
community changes observed during the last 30 years in the Caribbean, as it captures
the widespread mortality of acroporids in the 1980s, the recent decline of Orbicella,
and the increase in the relative abundance of opportunistic and weedy corals
13,15,17
.
Reductions in community calcification derived from climate change and/or ocean
acidification were assumed at 10% per decade, an estimation that incorporated inter-
specific variability reported in the literature
9,35–39
.
Calcification rates. Mean annual extension rates (cm year
21
) and mean skeletal
densities (g cm
23
) per genus were calculated by averaging the values in locations
where previous reports existed in the Caribbean for colonies of these genera growing
between 2- and 10-m depths (see references in Supplementary Online Material;
Table 1).
Acropora mean annual calcification rate was calculated with the help of field data.
In 2012, sixteen 1 3 1 m quadrats were surveyed in a reef portion dominated by A.
palmata in Puerto Morelos, Mexican Caribbean. At each quadrat the number of all
branch tips was counted. Then, in ten randomly selected branches of each quadrat,
branch thickness in the apical zone and at 8.8 cm from the tip (i.e., the mean annual
extension rate for the genus; Table 1), and branch width, were measured. For each
branch, annual calcification rate was then calculated as
CR~ TH1zTH2ðÞ=2ðÞ|BW|ER|DðÞ=1000
Where:
CR ~ annual calcification rate kg cm
{2
year
{1
!"
,
TH1 ~ thickness in the apical zone cmðÞ,
TH2 ~ thickness at 8:8 cm from the branch tip cmðÞ,
BW ~ branch width cmðÞ,
ER ~ mean annua l extension rate for the genus cm year
{1
; Table 1
!"
,
D ~ mean density for the genus g cm
{3
; Table 1
!"
Mean annual calcification rate for Acropora (kg m
22
year
21
; Table 1) was then
calculated as the product of the average annual calcification rate of all measured
branches by the mean number of branch tips in the sixteen 1 3 1 m quadrats (43.2 6
19.3 SD).
Considering the mean annual extension rate and mean skeletal density of Orbicella
and Porites (Table 1), the mean annual calcification rates (kg m
22
year
21
; Table 1) of
these genera were calculated as the CaCO
3
increment of a hemisphere with a basal
area of 1 m
2
. Agaricia agaricites has several colony growth forms including dome-
shaped and plate-like
40
. Thus, for dome-shaped Agaricia colonies, the mean annual
calcification rate was calculated using its mean annual extension rate and mean
skeletal density (Table 1) in the same manner as for Orbicella and Porites. However,
for plate-like Agaricia colonies, the CaCO
3
increment was calculated considering the
mean annual extension rate and mean skeletal density (Table 1) of the growth margin
of a 0.5-cm-thick disc with an area of 1 m
2
. It was assumed that the contribution of
each of these two growth forms of Agaricia was equal; therefore the mean annual
calcification rate (kg m
22
year
21
; Table 1) was calculated as an average of the two.
Colony level rugosity. Colony level rugosity for A. palmata, A. cervicornis, O.
annularis, O. faveolata, A. agaricites and P. astreoides was measured following a
standard me thodology commonly used to measure reef rugosity. This consisted of
calculating the ratio of the contour to the linear distance between the start and end
point of the colony’s longest axis. A perfectly flat colony would have a rugosity index
of one with larger indices indicating more complex colonies. Coral colony rugosity of
183 colonies was measured in Cozumel (2009) and Puerto Morelos (2012), Mexico in
a depth range between 2 and 12 m. The mean rugosity of the genus was obtained by
averaging all the colonies of each genus (Table 1). It is important to note we did not
include colony size in the index. However, the inclusion of this variable would only
make more evident the pattern depicted by Figure 1 because the more structurally
complex corals are also the ones with the largest colonies in our model (i.e., Acropora
and Orbicella). Although, colony morphology and size can vary in relation to
environmental conditions, we do consider that our estimates of colony-level rugosity
are representative and informative because the morphological variability within
species (e.g., platy vs massive agaricids) will be less than the morphological variability
between species (e.g., Agaricia vs Orbicella).
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Acknowledgments
We thank Rosa E. Rodrı
´
guez-Martı
´
nez and Aurora U. Beltra
´
n-Torres for their assistance in
the field. We also thank Isabelle M. Co
ˆ
te
´
, Emily S. Darling for helpful comme nts on the
manuscript, as well as Anastazia T. Banaszak and Paul Blanchon for the editorial assistance.
The research leading to these results has received funding from the European Union 7
th
Framework programme (P7/2007–2013) under grant agreement No. 244161 to J.P.C.-G.
and R.I.-P. (http://force-project.eu), Canon Foundation to R.I.-P. CONABIO to G.H-P.
(GM005), and CONACyT to L.A.-F. (160230).
Author contributions
L.A.F., J.P.C.-G., G.H.-P. and R.I.-P. contributed equally to the development of the models
and to the preparation of the manuscript. L.A.F. and J.P.C.-G. performed the field
measurements. All authors reviewed the manuscript.
Additional information
Supplementary information accompanies this paper at http://www.nature.com/
scientificreports
Competing financial interests: The authors declare no competing financial interests.
How to cite this article: Alvarez-Filip, L., Carricart-Ganivet, J.P., Horta-Puga, G. &
Iglesias-Prieto, R. Shifts in coral-assemblage composition do not ensure persistence of reef
functionality. Sci. Rep. 3, 3486; DOI:10.1038/srep03486 (2013).
This work is licensed under a Creative Commons Attribution-
NonCommercial-NoDerivs 3.0 Unported license. To view a copy of this license,
visit http://creativecommons.org/licenses/by-nc-nd/3.0
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SCIENTIFIC REPORTS | 3 : 3486 | DOI: 10.1038/srep03486 5