REV I EW AND
SYNTHES I S Meta-analysis reveals negative yet variable effects
of ocean acidification on marine organisms
Kristy J. Kroeker,1* Rebecca L.
Kordas,2 Ryan N. Crim2 and
Gerald G. Singh2
1Stanford University, Hopkins
Marine Station, Pacific Grove,
CA 93950, USA
2University of British Columbia,
Vancouver, BC, Canada V6T1Z4
*Correspondence: E-mail:
kkroeker@stanford.edu
Abstract
Ocean acidification is a pervasive stressor that could affect many marine organisms and
cause profound ecological shifts. A variety of biological responses to ocean acidification
have been measured across a range of taxa, but this information exists as case studies and
has not been synthesized into meaningful comparisons amongst response variables and
functional groups. We used meta-analytic techniques to explore the biological responses
to ocean acidification, and found negative effects on survival, calcification, growth and
reproduction. However, there was significant variation in the sensitivity of marine
organisms. Calcifying organisms generally exhibited larger negative responses than non-
calcifying organisms across numerous response variables, with the exception of
crustaceans, which calcify but were not negatively affected. Calcification responses varied
significantly amongst organisms using different mineral forms of calcium carbonate.
Organisms using one of the more soluble forms of calcium carbonate (high-magnesium
calcite) can be more resilient to ocean acidification than less soluble forms (calcite and
aragonite). Additionally, there was variation in the sensitivities of different develop-
mental stages, but this variation was dependent on the taxonomic group. Our analyses
suggest that the biological effects of ocean acidification are generally large and negative,
but the variation in sensitivity amongst organisms has important implications for
ecosystem responses.
Keywords
Calcification, carbonate chemistry, climate change, CO2, growth, meta-analysis, ocean
acidification, ontogeny, pH, photosynthesis, reproduction.
Ecology Letters (2010) 13: 1419–1434
I N TRODUCT ION
Ocean acidification is considered as a global threat to marine
ecosystems (Doney et al. 2009a; Fabry et al. 2009; Kleypas &
Yates 2009). It is caused by rising atmospheric carbon
dioxide (CO2) concentrations, which drive changes in
seawater carbonate chemistry and reduce pH (Gattuso &
Buddemeier 2000). This process of ocean acidification is
underway (Solomon et al. 2007) and will accelerate with
increasing CO2 emissions over the course of the current
century (Caldeira & Wickett 2003; Meehl et al. 2007). Many
marine organisms, from phytoplankton to fish, are sensitive
to changes in carbonate chemistry, and their responses to
the predicted changes could lead to profound ecological
shifts in marine ecosystems (reviewed by Doney et al.
2009b). As such, ocean acidification has become a priority
area for research, and the number of experiments examining
its effects on marine organisms has grown exponentially.
Marine organisms vary broadly in their responses to ocean
acidification, in part due to the wide variety of processes
affected (e.g., dissolution and calcification rates, growth
rates, development and survival), making it challenging to
predict how marine ecosystems will respond to ocean
acidification.
Several hypotheses have been proposed to explain the
variation in biological responses, including: (1) organisms
that have a calcium carbonate (CaCO3) structure will be
more sensitive to ocean acidification than organisms that do
not, (2) organisms with more soluble mineral forms of
CaCO3 in their structure (e.g., aragonite) will be more
sensitive than organisms with less soluble mineral forms
(e.g., calcite), (3) early life history stages will be more
Ecology Letters, (2010) 13: 1419–1434 doi: 10.1111/j.1461-0248.2010.01518.x
 2010 Blackwell Publishing Ltd/CNRS

sensitive than later life history stages, (4) highly mobile
organisms with high metabolic rates may be more capable of
compensating for changes in carbonate chemistry than
sessile organisms with low metabolic rates and (5) auto-
trophs with less efficient or absent carbon-concentrating
mechanisms (CCMs) will be more responsive than those
with efficient CCMs. Below, we briefly review the leading
hypotheses for variation in sensitivity to ocean acidification.
One of the primary hypotheses for variation in the
biological responses to ocean acidification concerns the
susceptibility of calcification. Calcification may be especially
sensitive because altered carbonate chemistry directly affects
the deposition and dissolution rates of the CaCO3 used for
structures (Gattuso & Buddemeier 2000). Reduced calcifi-
cation rates or increased dissolution rates have been
measured in tropical corals (Kleypas et al. 1999; Marubini
et al. 2003; Hoegh-Guldberg et al. 2007), planktonic organ-
isms (Riebesell et al. 2000; Orr et al. 2005), bivalves
(Michaelidis et al. 2005; Gazeau et al. 2007) and echinoderms
(Kurihara & Shirayama 2004; Shirayama & Thornton 2005)
amongst others in response to ocean acidification. The
impacts on calcification could then result in altered energy
allocation (Wood et al. 2008), lower growth rates, reduced
reproductive output and decreased survival amongst calci-
fying organisms under conditions of ocean acidification.
The sensitivity of calcification to ocean acidification may
vary amongst calcifying organisms. Sensitivity may depend
on the mineral form of CaCO3 used by the organism,
with the solubility and susceptibility increasing from low-
magnesium calcite to aragonite and high-magnesium calcite
(Morse et al. 2006; Ries et al. 2009). However, some species
may be better able to control pH near calcification sites
under differing external conditions, and thereby may be
better equipped to cope with ocean acidification (Berry et al.
2002; Cohen & McConnaughey 2003; Taylor et al. 2007).
Additionally, some organisms may be able to compensate
for changes in carbonate chemistry by increasing calcifica-
tion rates (Gutowska et al. 2008). Finally, the sensitivity of
calcification processes may be buffered for calcifying algae
and corals with symbiotic autotrophs due to interactions
between photosynthesis and calcification. It is known that
photosynthesis can stimulate calcification across numerous
taxa (Borowitzka 1982; Gattuso et al. 1999, 2000; Rost &
Riebesell 2004). If photosynthesis increases in these
organisms under ocean acidification, it could potentially
buffer the negative effects on calcification (Ries et al. 2009).
In addition, early life history stages may be more
vulnerable to ocean acidification than adults. The larval
and juvenile stages of marine organisms are typically more
sensitive to environmental conditions (Pechenik 1987), and
can suffer extremely high mortality (Gosselin & Qian 1997).
Additionally, some invertebrates begin calcifying during the
larval (echinoderms and molluscs) or juvenile (corals and
crustaceans) phases (Kurihara 2008). During these phases of
calcification, they may rely on a more soluble mineral form
of CaCO3 than the mineral used as an adult (Weiss et al.
2002; Addadi et al. 2003). Indeed, some echinoderms have
shown delayed development or high mortality during larval
stages when exposed to ocean acidification (Dupont et al.
2008).
Organisms may also vary in their sensitivity to ocean
acidification in other physiological processes. Reduced
seawater pH can disrupt the acid–base status of extracellular
body fluid (e.g., blood or hemolymph). Highly mobile
organisms such as fish, cephalopods and some crustaceans
that are capable of controlling extracellular pH through
active ion transport are predicted to be more tolerant of
acidification (Gutowska et al. 2008; Po¨rtner 2008; Melzner
et al. 2009). In turn, organisms unable to compensate for the
reductions in extracellular pH have shown depressed
metabolism, growth and fitness (Po¨rtner et al. 2004;
Michaelidis et al. 2005; Siikavuopio et al. 2007). Higher
maintenance costs in stressful abiotic environments could
cause changes in energy allocation to reproduction and
somatic growth.
The ability of marine autotrophs to increase photosyn-
thetic rates under ocean acidification could also contribute
to variation in organismal responses. Marine autotrophs rely
on CO2(aq) or the bicarbonte ion (HCO3
)) for photosyn-
thesis, which will both increase in concentration with ocean
acidification. However, many marine autotrophs utilize
CCMs and do not appear carbon limited under current
conditions (Raven & Beardall 2003). Yet there is variation in
the efficiency of CCMs, and marine phytoplankton with less
efficient CCMs have shown the capacity to increase
photosynthetic rates in carbon and nutrient replete condi-
tions (Rost & Riebesell 2004; Engel et al. 2005; Riebesell
et al. 2007). In addition, seagrasses primarily rely on CO2(aq)
and have shown increased photosynthesis and growth under
conditions of ocean acidification (Zimmerman et al. 1997;
Palacios & Zimmerman 2007; Hall-Spencer et al. 2008).
A recent quantitative review concluded that most
biological processes are not significantly affected by near-
future ocean acidification (Hendriks et al. 2010). However,
that review did not use the standard methods for meta-
analyses – quantitative methods for combining the results of
several studies into an overall mean effect – which
standardize studies for precision, account for variation
between studies, and test for heterogeneity in effect sizes.
Significant heterogeneity suggests there may be differences
in responses between groups of studies, which can have
ecologically important implications and guide the interpre-
tation of the overall results of the meta-analyses (Hedges &
Olkin 1985; Gurevitch & Hedges 1999; Rosenberg et al.
2000). For these reasons, heterogeneity is of primary interest
when trying to quantify the variability or draw general
1420 K. J. Kroeker et al. Review and Synthesis
 2010 Blackwell Publishing Ltd/CNRS