Overview Articles
Safety in Numbers? Abundance
May Not Safeguard Corals from
Increasing Carbon Dioxide
Marine conservation efforts are often focused on increasing stocks of species with low population abundances by reducing mortality or enhancing
recruitment. However, global changes in climate and ocean chemistry are density-independent factors that can strongly affect corals whether they
are scarce or abundant—sometimes, the abundant corals are most affected. Because reproductive corals are sessile, density-independent effects
of global changes such as physiological stress and resultant mortality can decouple stock abundance from recruitment and may accelerate the
downward spiral of their reproductive rates.
Keywords: coral, density independence, depensatory, extinction, sessile
T
he principles of basic conservation biology dictate that, all other things being equal, abundant species should have
a lower risk of extinction than rare species do. Mechanisms
for species protection—such as the International Union for
Conservation of Nature (IUCN) Red List of Endangered
Species and the US Endangered Species Act—have been
predicated on such principles. Two complications, however,
weaken the application of these principles to the current fate
of corals and some other sessile marine invertebrates. The
first is that abundance has different facets—such as population density, geographic distribution, and global population
size—that may buffer against different aspects of a threat
(e.g., reproductive failure or local disturbances). The other is
that all else is not equal; global-scale threats, such as ­carbon
dioxide (CO2)–induced changes in climate and ocean chemistry (e.g., acidification), sometimes impose radical changes
in the expected trajectories of population processes and
dynamics.
Marine conservation action is often geared toward manipulating abundance and biomass by reducing mortality (e.g.,
prohibiting harvest) or increasing potential recruitment
success (e.g., protecting fish-spawning aggregations or sea
turtle nesting beaches). Some marine reserves have been successful in meeting these immediate objectives, with increases
in the species richness, population density, recruitment, and
biomass of the target taxa, improving the resilience of communities, and facilitating community-based management.
These benefits are worthwhile and important and certainly buffer species and ecosystems from the threshold of
collapse.
However, despite these local successes, the global decline of
coral reefs has not been prevented. The Great Barrier Reef
(De’ath et al. 2012), the wider Caribbean (Gardner et al.
2003), and the Indo-Pacific region (Bruno and Selig 2007)
have all had significant losses in coral cover over decadal
scales, and even no-take reserves (Huntington et al. 2011)
and national parks (Rogers and Muller 2012) have experienced mass mortality events and coral declines. Even corals
in the Papahānaumokuākea Marine National Monument
have experienced episodes of bleaching and disease (Kenyon
et al. 2006), despite being geographically remote from human
development and being protected from direct human dis­
turbances. As of 2011, 60% of coral reefs are under immediate and direct threat from one or more local sources,
and about 75% are under threat when one includes global
threats from CO2, despite over 27% of reefs’ falling within
some degree of protection in marine reserves (Burke et al.
2011). The number and intensity of warming-induced mass
coral-bleaching events have increased since they were first
observed three decades ago (Eakin et al. 2009) and are predicted to increase to annual frequency by midcentury (van
Hooidonk et al. 2013).
Increasing the levels of protection may help buffer some of
these losses, but there are clearly problems falling beyond the
BioScience 63: 967–974. ISSN 0006-3568, electronic ISSN 1525-3244. © 2013 by American Institute of Biological Sciences. All rights reserved. Request
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reprintinfo.asp. doi:10.1525/bio.2013.63.12.9
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Charles Birkeland, Margaret W. Miller, Gregory A. Piniak, C. Mark Eakin, Mariska Weijerman,
Paul M c Elhany, Matthew Dunlap, and Russell E. Brainard
Overview Articles
scale at which management typically occurs. In this article,
we propose that the conditions driven by excess CO2 cause
density-independent mortality and physiological stress that
affect reproductive success and lead to the decline of corals—
independent of coral abundance. We explain how coral species can be abundant across a broad geographic range, but
this does not safeguard them against global threats, including changing ocean chemistry and rising temperatures.
968 BioScience • December 2013 / Vol. 63 No. 12
The principle of allocation refers to the trade-offs among
alternative energy allocations (e.g., a few large, well-endowed
eggs or many eggs with larvae that feed themselves) or among
alternative morphological traits (e.g., dense and massive skeletons that provide structural strength or thinner and porous
branching or tabular skeletons that provide height and more
rapid growth).
(see box 1) predicts that when the physical environment is
idyllic, corals that shed the cost of physiological complexities in exchange for rapid growth prevail in competition
for space and become dominant but lose when the physical
environments become harsh. The clonal reproduction of
branching corals facilitates a rapid takeover of space, results
in a competitive advantage, and is potentially selected by
greater fecundity from the larger surface area, but large
clonal populations do not necessarily indicate a greater
adaptive capacity for climate change (figure 1). The present
interglacial period has been “particularly favorable” for reefbuilding corals (Kleypas et al. 2001, p. 430), and the rapidly
growing representatives of the genus Acropora have been
favored by natural selection (figure 2), but natural selection
neither effectively predicts nor equips populations for the
future.
What does it mean for a coral species to be
abundant?
Since the inception of coral-monitoring techniques, the main
aim has been to determine how much coral a reef contains.
The percentage cover has been a primary metric for decades,
although in some widely adopted methods (e.g., Atlantic and
Gulf Rapid Reef Assessment), a greater emphasis has recently
been placed on measuring coral density or size–frequency
distribution. If density and size information are combined,
such metrics are vast improvements over coral cover and may
give managers a better grasp of how much coral there is.
However, such population-demographic methods have some
caveats. It is easy to scale up density measures over large scales
(e.g., to estimate the number of Orbicella in the Florida
Keys), but doing so requires assumptions about the uniformity of density and certainly loses relevance if variations in
colony-size distributions are not accounted for. Even counting an individual in a population can be problematic, given
the vagaries of defining an individual in the field (e.g., ­colony
fragments, partial mortality, interwoven clusters of branching species) and the scarcity of genotypic information at
the relevant scales (Baums et al. 2006). A species may be
abundant because of a wide geographic or habitat distribution, characteristics that should convey lesser vulnerability
to local habitat degradation or episodic disaster. However,
local population density is a key factor in sustaining coral
populations, and ­density-­independent mortality or stress
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The track record of abundant corals
On the basis of the geologic record, there is no compelling
reason to predict that abundant or dominant coral species
are more likely to survive global environmental changes than
are less abundant corals. In the Upper (Norian) Triassic, the
large (delicate to robust) branching Retiophyllia (formerly
Thecosmillia) was a major reef-framework builder, probably
grew rapidly, and contributed to widespread reefs in Japan,
Asia, Indonesia, Russia, Europe, and western America, from
Alaska and Vancouver Island through Oregon and Mexico
to Peru and northern Chile—but this coral went extinct
at the end of the Triassic, whereas a smaller phaceloid—
subcerioid coral, Phacelostylophyllum from central Asia,
southern Europe, and northern Africa—survived into the
Jurassic (Wood 1999). Likewise, in the Cretaceous–Tertiary
mass extinction, the coral genera that survived were slowgrowing, massive, columnar or encrusting forms, whereas
the branching corals that today tend to win the competition
for space originated after the extinction event. Van Woesik
and colleagues (2012) showed that the branching corals
Pocillopora and Stylophora were dominant in the greater
Caribbean area in the Pliocene, but “widespread d
­ istribution
did not equate with immunity” (p. 2448). Likewise, Pandolfi
and colleagues (2001) reported on the geologically sudden
extinction of two widespread dominant Caribbean corals
within the past 82,000 years, although several rare corals
survived. They concluded that population size was a poor
predictor of extinction for those corals. Extinction was based
on morphological and physiological traits rather than on
random episodes that favor corals with a wide geographic
distribution or a large global population size.
A modern example is that of Acropora palmata and
Acropora cervicornis, which are fast growing and were major
reef builders in many parts of the greater Caribbean, but
their abundance and dominance did not protect them
from huge declines from disease at the end of the t­ wentieth
century (Vollmer and Palumbi 2007). The abundant, massive species of the Orbicella (formerly Montastraea) annularis complex appear to be following in the same path
(Hernández-Pacheco et al. 2011). In contrast, Dendrogyra
cylindrus may be characteristically rare but show high resistance to partial mortality, bleaching, and disease (Acosta
and Acevedo 2006), which would tend to physiologically
favor species persistence.
Recent large-scale mortalities have shown the same pattern of winners and losers (van Woesik et al. 2011). The
pervasive evolutionary and ecological principle of allocation
Box 1. The principle of allocation.
Overview Articles
will eventually reduce density (see the discussion below).
Overall, abundance does not help us determine whether
we have a population of ghosts—that is, a possibly large
population that is failing to replace itself—nor does ­rarity
predispose a population to mortality. The reliance of many
corals on vegetative reproduction can result in very large
populations consisting of clones from very few genets and
little genetic variability. Nevertheless, how much coral
there is does matter ecologically (see below) and possibly
evolutionarily if larger populations contain more variability
and, therefore, a greater adaptive capacity. However, most
mechanisms for species protection—such as the IUCN Red
List and the US Endangered Species Act—are largely based
on how few corals there are.
Reduction in population density affects the
reproductive success of sessile animals
Corals form the physical structure of the habitat they typify,
and they are almost all sessile as adults. Being sessile makes
reproductively mature coral colonies especially vulnerable to
depensatory processes (see box 2). In a depensatory process,
a reduced population density can lead to low reproduction, which, in turn, can create an even smaller population with even lower reproduction, which will create an
www.biosciencemag.org ­ever-­accelerating rush toward functional extinction. There
is some evidence of this sort of process occurring in corals.
There have been substantial declines in coral recruitment
over large scales from 1977 to 1993 in Jamaica (Hughes
and Tanner 2000) and from 1979 to 2004 in Curaçao (Bak
et al. 2005), which are in accord with large-scale declines in
coral cover in the region (e.g., Gardner et al. 2003); these
declines suggest that density is a key to successful reproduction. Examples of positive-feedback depensatory reproductive processes that worsen as population size decreases
are a reduction in fecundity, the failure of fertilization,
and a disruption of genetic connectivity among populations. All of these depensatory factors are worsened by
density-­independent mortality, in which some fraction of
the population dies regardless of the total abundance. The
physiological stress caused by global change effects may
act as a source of density-independent mortality. In particular, density-independent effects on fecundity, fertilization, and connectivity can lead to subsequent depensatory
declines.
Fecundity. The number of eggs or larvae produced by a
population of corals can be decreased by physical damage or
by physiological stress. The energy available for producing
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Figure 1. During idyllic ocean conditions, the fast-growing branching forms of coral take over space from the more
physiologically hardy and resilient mound forms of coral. Photograph: Charles Birkeland.
Overview Articles
Box 2. Depensatory processes.
Depensatory processes, also called Allee effects
and inverse density dependence, are self-­reinforcing
or positive-feedback processes by which a
per capita decrease in successful reproduction
or survival accelerates as the population density declines, resulting in a downward spiral of
abundance or function.
Figure 2. (a) Colonies of Acropora species on
Aunu’u Island, American Samoa, in 1979,
a few days before they were eliminated by
predation from crown-of-thorns seastars.
The fast-growing species dominate the area
through competition for space, but after
predation becomes an overwhelming factor,
the slow-growing mound corals are all that
will remain. Photograph: Charles Birkeland.
(b) Acropora hyacinthus and a few Acropora
cytherea in Fagatele Bay National Marine
Sanctuary in August 2007. The A. hyacinthus
populations were devastated between 1977
and 1994, because they were especially
susceptible to crown-of-thorns outbreaks
(1977–1979), cyclones (1981, 1990, 1991),
and major bleaching associated with warm
seawater (1994), but they demonstrated
episodic recruitment in the early 2000s.
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gametes is reduced when corals expend energy
to resist physiologically stressful conditions,
and so fecundity is reduced by local stressors
such as sedimentation (Kojis and Quinn 1984)
or pollution (Ward and Harrison 2000) that
induce tissue damage or partial mortality. The
repair of damaged tissue in Goniastrea favulus
costs energy to the coral colony otherwise allocated for gamete production (Kojis and Quinn
1985), and damage can suspend gamete production for several years (Lirman 2000). Bleaching
in response to seawater warming produces similar reductions in fecundity (Omori et al. 2001),
and prolonged temperature-induced bleaching
can prevent gametogenesis the following year
(Szmant and Gassman 1990).
In addition to reducing the energy available
for the production of gametes, the densityindependent mortality effects of climate and
ocean changes from increasing CO2 can reduce
the number of colonies and the average size of
colonies in the population. Fewer or smaller
Overview Articles
colonies produce fewer eggs (Babcock 1991). Gardner and
colleagues (2003) determined an 80% decline in living coral
cover from 1977 to 2001 across the greater Caribbean, in
parallel with major coral recruitment reductions over the
same period (Hughes and Tanner 2000, Bak et al. 2005).
Younger corals will also be less fecund than older colonies of
the same size, so that when disturbance increases population
turnover, the fecundity can be reduced even if the overall living coral cover is the same (Kojis and Quinn 1985).
in order to become closer to their mates, as the population
size decreases, the average distance between them often
increases, and the spawned gametes are diluted. The evolutionary arguments, including the strong synchrony of coral
mass-spawning events centered at seasonal times with less
water motion (Oliver and Babcock 1992), the c­ ommonality
of buoyant gamete bundles that concentrate gametes in two
dimensions, and evidence that a 1–2-hour separation of
spawning time is adequate to maintain species boundaries
between hybridizable congeners (Levitan et al. 2004), all
strongly suggest that corals must combat fertilization limitation by dilution.
The importance of high sperm concentration to effectively fertilize spawned coral eggs has been repeatedly demonstrated in a range of lab studies with a range of species.
This relationship of sperm concentration to fertilization
success is often parabolic, with the optimal range of 105 to
106 sperm per milliliter (Oliver and Babcock 1992, Levitan
et al. 2004).
Direct evidence of how a threshold sperm concentration
corresponds to a threshold density of spawning colonies in
the field is extremely difficult to obtain. In a few studies,
the intercolony distance has been estimated at 2–5 meters
(mushroom corals in the lab: Lacks 2000; octocorals in
the field: Coma and Lasker 1997). Levitan and colleagues
(2004) reported rigorous field observations of the density
of spawning colonies with fertilization potential for the
common Caribbean spawner Orbicella franksi, showing
essentially zero fertilization potential when the density of
the colonies spawning on a given night dropped below
approximately one colony per 100 square meters. Only an
estimated 20%–30% of O. franksi colonies spawn on a given
night (Levitan et al. 2004), so this threshold would translate to an absolute colony density of three to four colonies
per 100 square meters. Combined with the observation
that spawned gametes are only viable for a few hours, this
implies that fertilization success will drop off rapidly as
the distance between spawning colonies increases. Reduced
fertilization leads to fewer larvae, fewer recruits, and fewer
adults. Fewer adults create fewer gametes, which are then
more readily diluted, and so the positive feedback accelerates into a downward spiral.
Meanwhile, it is highly likely that the density-independent
effects of warming temperatures and acidification exacerbate fertilization limitations. For example, Albright and
www.biosciencemag.org Connectivity. The effective distances between subpopulations
of a species (metapopulation) increase as habitat patches
become farther apart and as planulae become capable of
traveling only shorter distances. The patches might become
farther apart as intermediate patches are killed by local
­processes, such as disease, coastal construction, sedimentation, and the removal of herbivores, and by the effects of
global change, such as bleaching from higher temperatures
or physical damage from frequent storms. These same
processes not only extirpate patches of coral directly but,
along with the reductions seen in successful larval meta­
morphosis at lower pH levels, also thin out the populations
by attrition. Coastal development not only decreases the
connectivity among populations through distance but can
also establish barriers between formerly interconnected
populations by decreasing water quality (Puritz and Toonen
2011).
A commonly held perspective is that long-distance dispersal provides the main mechanism for genetic exchange
in coral populations and for recovery from extensive coral
mortality. Some corals can certainly have a broad window
of larval competency, which enables both local recruitment and long-distance dispersal. For example, Pocillopora
damicornis can settle successfully after 4 hours but can
potentially delay successful settlement for at least 212 days
(Harrigan 1972). However, genetic studies have shown that
populations of both brooding and spawning coral species
are more structured than would be expected if the larvae
were dispersing over long distances and reefs were well
interconnected (Vollmer and Palumbi 2007, Zvuloni et al.
2008), which suggests that long-distance dispersal may be
an unusual event.
Successful dispersal can become increasingly difficult as
local- or global-stress-related mortality increases the distance between coral patches. More important, additional
density-independent factors may shorten the distance over
which larvae are effectively dispersed, further limiting the
recolonization potential of remote habitat patches. First,
reduced population fecundity (as a result of, e.g., smaller living coral cover, greater population turnover, more metabolic
energy spent on physiological stress and repair) and larval
supply imply that, as fewer larvae enter the treacherous
long-distance dispersal pipe, fewer will emerge successfully
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Fertilization. Since individuals of sessile species cannot travel
colleagues (2010) showed that elevated-CO2 conditions
impair fertilization at lower sperm concentrations, and
Omori and colleagues (2001) found that after densityindependent bleaching, fertilization success was significantly
decreased, even with the abundant Acropora species. The
common Pacific species Acropora millepora is sensitive to
temperature at early life stages (Negri et al. 2007), and its
f­ ertilization ­success is impaired at 32 degrees Celsius (°C)
and non­existent at 34°C, whereas three nonacroporids were
not affected. Similar results were seen in the formerly abundant A. palmata (Randall and Szmant 2009). Again, there is
not always safety in numbers.
Overview Articles
Implications for conservation actions
The awareness that protecting and building resilience in
local habitats and populations was not adequate in developing resistance to changes in ocean chemistry and climate
began with Allison and colleagues (1998). They noted that
reserves provide special protection for unique habitats and
escape routes for intensely harvested resources and act as
insurance against unpredicted events or serious management errors. However, they further recognized that local
management and reserves, no matter how large, could not
protect against climatic and oceanographic changes, because
area-based protection of large populations defends against
extraction but does not defend against changes in climate
and ocean chemistry. The location of the reserve also matters. Variability in bleaching, disease, aragonite saturation,
and other stressors presently occurs at large and small scales
and has protected some reefs. Efforts to identify areas with
the greatest resilience for siting marine protected areas are
crucial as long as such heterogeneity persists. However,
model-based calculations predict that, alongside the increasing atmospheric CO2 concentrations, the decrease in aragonite saturation will become much more geographically
homogeneous by 2050 (Feely et al. 2009). Over the last three
decades, both mass coral bleaching and disease have resulted
972 BioScience • December 2013 / Vol. 63 No. 12
in the widespread loss of the most abundant species of
c­ orals in all ocean basins—even in strictly protected areas.
As mortality events increase in frequency and intensity while
global stressors become more homogenous, local protection
becomes both more important and less sufficient to prevent
extinction.
IUCN listings raise conservation awareness, whereas listings under the US Endangered Species Act and similar legislation impart a responsibility for governments to recover
imperiled species. The success of either of these listings
necessarily relies on human behavior. Ultimately, they are
aimed at threat reduction, but most protective actions rely
on increasing population size. Threats to coral populations
change dramatically with scale between the global threats
created by excess CO2 and the local depensatory threats to
reproduction that reduce fecundity and isolate sessile colonies. The combination of the two scales of threat may act
to synergistically accelerate the process of species decline.
Although they are beneficial, efforts to increase the distribution, abundance, and population density probably are
not of key importance in resistance to global-scale threats;
for example, decreases in ocean pH are likely to affect coral
recruits, and major changes in seawater temperature will
affect the relations between adult coral colonies and their
zooxanthellae, regardless of their distribution, abundance,
or population density.
Conclusions
Successful reproduction and, therefore, the capacity for adequate dispersal can be strongly affected by local population
density and reproductive output. However, these are both
at risk from global CO2 effects. If all individuals are equally
at risk, it may not matter whether a species is distributed
from the east coast of Africa to the west coast of Central
America, nor if there are millions of living colonies of the
species across the oceans. If all colonies of a coral species
are separated by more than a minimum distance necessary
for effective fertilization (perhaps about 5–10 meters), the
species may be functionally extinct. Over long time scales,
the biogeography of adult corals will most likely eventually reflect the dispersal potential of their pelagic larvae.
However, the projected rates of climate and ocean chemistry
changes suggest that time is not a friend and that corals
may not have time to rely on rare events such as prolonged
pelagic larval duration and long-distance dispersal. Perhaps
the long-term survival of many coral species will require
some degree of assisted migration by the same humans causing the threats in the first place.
Because success in fixing local-scale problems, such as
sedimentation, overfishing, and pollution, does not secure
success at the global scale, it is commonly stated that focusing on maintaining local populations is like arranging deck
chairs on the Titanic. However, these local actions are essential to maintaining an adequate coral population density for
successful reproduction and to maintain genetic diversity.
The emerging picture, however, is that we cannot rely on
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at the other end. Meanwhile, many larvae complete development faster at higher water temperatures, which yields a
shorter pipe. For example, when P. damicornis larvae were
raised in Palau, at 26°C–30°C, they remained free-swimming
planulae only half as long as those raised in Hawaii at
24°C–27°C (Harrigan 1972). In addition, the larvae of some
species have been shown to suffer increased mortality and
decreased settlement success under warmer temperatures
(Randall and Szmant 2009), and most spawning corals disperse at the warmest time of year.
Even if planulae successfully reach an appropriate settlement substrate, lower seawater pH is likely to affect successful recruitment over the coming decades (Webster et al.
2013). Although the physiological process of coral larval
settlement appears to be relatively resistant to higher CO2
concentrations, there is growing evidence that indirect
effects resulting from alterations in benthic communities
and settlement cues will greatly affect coral settlement success (Webster et al. 2013).
Therefore, the long-distance dispersal pipe is getting
shorter (accelerated larval development) and more treacherous (higher mortality and lower settlement success)
under warming temperatures, with few candidates entering the challenge (lowered larval supply), which makes
the successful connection to remote subpopulations less
likely. Overall, the depensatory processes that worsen as
population size decreases are all exacerbated by densityindependent changes in oceanic conditions brought about
by increased CO2, producing positive-feedback downward
spirals in coral recruitment, even in species that are currently abundant.
Overview Articles
local protection by marine reserves alone or on replenishing damaged systems; rather, we must actually fix the core
problems caused by increased CO2 if even abundant coral
species are to persist in supporting reef-associated ecosystem
services. The greatest value of listing species as threatened
or endangered may not lie in the legal enhancement of local
protection but in the potential, albeit currently remote, of
such listing for helping us act to reduce anthropogenic CO2
in our atmosphere.
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Charles Birkeland ([email protected]) is an emeritus professor in the
Department of Biology at the University of Hawaii at Manoa, in Honolulu.
Margaret W. Miller is a research ecologist at the Southeast Fisheries Science
Center, National Marine Fisheries Service, in Miami, Florida. Gregory A.
Piniak is a supervisory ecologist at the US National Oceanic and Atmospheric
Administration’s (NOAA) National Ocean Service National Centers for
Coastal Ocean Science, in Silver Spring, Maryland. C. Mark Eakin is the coordinator of the NOAA Coral Reef Watch, at the Center for Satellite Applications
and Research, in College Park, Maryland. Mariska Weijerman is a coral
ecology researcher and Matthew Dunlap is a marine ecosystems research
specialist at the Joint Institute for Marine and Atmospheric Research, at the
University of Hawaii at Manoa. Paul McElhany is a research ecologist with
the Northwest Fisheries Science Center, National Marine Fisheries Service, in
Seattle, Washington. Russell E. Brainard is the division chief of the Coral Reef
Ecosystem Division of the Pacific Islands Fisheries Science Center, National
Marine Fisheries Service, in Honolulu, Hawaii.
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