Ocean Acidification and Its Potential Effects

on Marine Ecosystems
John M. Guinottea and Victoria J. Fabryb
a
Marine Conservation Biology Institute, Bellevue, Washington, USA
b
California State University San Marcos, San Marcos, California, USA

Ocean acidification is rapidly changing the carbonate system of the world oceans.
Past mass extinction events have been linked to ocean acidification, and the current
rate of change in seawater chemistry is unprecedented. Evidence suggests that these
changes will have significant consequences for marine taxa, particularly those that
build skeletons, shells, and tests of biogenic calcium carbonate. Potential changes in
species distributions and abundances could propagate through multiple trophic levels
of marine food webs, though research into the long-term ecosystem impacts of ocean
acidification is in its infancy. This review attempts to provide a general synthesis of
known and/or hypothesized biological and ecosystem responses to increasing ocean
acidification. Marine taxa covered in this review include tropical reef-building corals,
cold-water corals, crustose coralline algae, Halimeda, benthic mollusks, echinoderms,
coccolithophores, foraminifera, pteropods, seagrasses, jellyfishes, and fishes. The risk
of irreversible ecosystem changes due to ocean acidification should enlighten the ongo-
ing CO 2 emissions debate and make it clear that the human dependence on fossil fuels
must end quickly. Political will and significant large-scale investment in clean-energy
technologies are essential if we are to avoid the most damaging effects of human-induced
climate change, including ocean acidification.

Key words: ocean acidification; climate change; carbonate saturation state; seawater
chemistry; marine ecosystems; anthropogenic CO 2

Introduction overwhelming cause of ocean acidification is

anthropogenic atmospheric CO 2 , although in
The carbonate system (pCO 2 , pH, alkalin- some coastal regions, nitrogen and sulfur are
ity, and calcium carbonate saturation state) of also important (Doney et al. 2007). For the past
the world oceans is changing rapidly due to 200 years, the rapid increase in anthropogenic
an influx of anthropogenic CO 2 (Skirrow & atmospheric CO 2 , which directly leads to de-
Whitfield 1975; Whitfield 1975; Broecker & creasing ocean pH through air–sea gas ex-
Takahashi 1977; Broecker et al. 1979; Feely change, has been and continues to be caused
& Chen 1982; Feely et al. 1984; Kleypas et al. by the burning of fossil fuels, deforestation, in-
1999a; Caldeira & Wickett 2003; Feely et al. dustrialization, cement production, and other
2004; Orr et al. 2005). Ocean acidification land-use changes. The current rate at which
may be defined as the change in ocean chem- ocean acidification is occurring will likely have
istry driven by the oceanic uptake of chemi- profound biological consequences for ocean
cal inputs to the atmosphere, including carbon, ecosystems within the coming decades and
nitrogen, and sulfur compounds. Today, the centuries.
Presently, atmospheric CO 2 concentration is
Address for correspondence: John M. Guinotte, Marine Conserva- approximately 383 parts per million by volume
tion Biology Institute, 2122 112th Avenue NE, Suite B-300, Belle-
vue, WA 98004-2947. Voice: +1-425-274-1180; fax: +1-425-274-1183.
(ppmv), a level not seen in at least 650,000 years,
[email protected] and it is projected to increase by 0.5% per year
Ann. N.Y. Acad. Sci. 1134: 320–342 (2008). !
C 2008 New York Academy of Sciences.
doi: 10.1196/annals.1439.013 320
Guinotte & Fabry: Ocean Acidification and Marine Ecosystems 321

throughout the 21st century (Petit et al. 1999; on marine calcifiers. Table 1 lists carbon sys-
Houghton et al. 2001; Augustin et al. 2004; tem parameters and temperature changes for
Siegenthaler et al. 2005; Meehl et al. 2007). The surface waters based on the Intergovernmental
rate of current and projected increases in atmo- Panel on Climate Change (IPCC) IS92a CO 2
spheric CO 2 is approximately 100× faster than emission scenario.
has occurred in at least 650,000 years (Siegen- A reduction in the number of carbon-
thaler et al. 2005). In recent decades, only half of ate ions available will make it more diffi-
anthropogenic CO 2 has remained in the atmo- cult and/or require marine calcifying organ-
sphere; the other half has been taken up by the isms to use more energy to form biogenic
terrestrial biosphere (ca. 20%) and the oceans calcium carbonate (CaCO 3 ). Many marine
(ca. 30%) (Feely et al. 2004; Sabine et al. 2004). organisms form biogenic calcium carbonate
Since the Industrial Revolution, a time span of including: crustose coralline algae (the pri-
less than 250 years, the pH of surface oceans has mary cementer that makes coral reef formation
dropped by 0.1 pH units (representing an ap- possible), Halimeda (macroalgae), foraminifera,
proximately 30% increase in hydrogen ion con- coccolithophores, tropical reef-building corals,
centration relative to the preindustrial value) cold-water corals, bryozoans, mollusks, and
and is projected to drop another 0.3–0.4 pH echinoderms. The majority of marine calci-
units by the end of this century (Mehrbach et al. fiers tested to date are sensitive to changes
1973; Lueker et al. 2000; Caldeira & Wickett in carbonate saturation state and have shown
2003; Caldeira et al. 2007; Feely et al. 2008). declines in calcification rates in laboratory
[Note: The pH scale is logarithmic, and as a and mesocosm studies (Table 2). These or-
result, each whole unit decrease in pH is equal ganisms are affected and will continue to be
to a 10-fold increase in acidity.] A pH change affected by ocean acidification, but less well
of the magnitude projected by the end of this known are the ecosystem impacts on higher
century probably has not occurred for more trophic-level organisms that rely on these cal-
than 20 million years of Earth’s history (Feely cifiers for shelter, nutrition, and other core
et al. 2004). The rate of this change is cause functions.
for serious concern, as many marine organ- Decreasing pH is not the only effect on the
isms, particularly those that calcify, may not be inorganic carbon system in seawater that re-
able to adapt quickly enough to survive these sults from the ocean’s uptake of anthropogenic
changes. CO 2 . Calcite and aragonite are the major
A series of chemical reactions is initiated biogenically formed carbonate minerals pro-
when CO 2 is absorbed by seawater. ! is the duced by marine calcifiers, and the stability
calcium carbonate saturation state: of both minerals is affected by the amount
of CO 2 in seawater, which is partially deter-
! = [Ca2+ ][CO2− ∗
3 ]/Ksp
mined by temperature. Colder waters natu-
where K∗sp is the stoichiometric solubility prod- rally hold more CO 2 and are more acidic than
uct for CaCO 3 and [Ca2+ ] and [CO2− 3 ] are warmer waters. The depths of the aragonite
the in situ calcium and carbonate concentra- and calcite saturation horizons are important
tions, respectively. The end products of these to marine calcifiers because the depth of these
reactions are an increase in hydrogen ion con- horizons determines the limit at which pre-
centration (H+ ), which lowers pH (making wa- cipitation of biogenic calcium carbonate by
ters more acidic), and a reduction in the num- marine organisms is favored (shallower than
ber of carbonate ions (CO2− 3 ) available. This the saturation horizon) and at which they will
reduction in carbonate ion concentration also experience dissolution (deeper than the satu-
leads to a reduction in calcium carbonate sat- ration horizons) in the absence of protective
uration state (!), which has significant impacts mechanisms.
322 Annals of the New York Academy of Sciences

TABLE 1. Projected changes in surface ocean carbonate chemistry based on IPCC IS92a CO 2 emission
scenario (Houghton et al. 2001)a
Parameter Symbol Unit Glacial Preindustrial Present 2 × CO 2 3 × CO 2

Temperature T ◦
C 15.7 19 19.7 20.7 22.7
Salinity S 35.5 34.5 34.5 34.5 34.5
Total alkalinity AT µmol kg−1 2356 2287 2287 2287 2287
pCO 2 in seawater pCO 2 µatm 180 280 380 560 840
(−56) (0) (35.7) (100) (200)
Carbonic acid H 2 CO 3 µmol kg−1 7 9 13 18 25
(−29) (0) (44) (100) (178)
Bicarbonate ion HCO 3 −
µmol kg−1 1666 1739 1827 1925 2004
(−4) (0) (5) (11) (15)
2−
Carbonate ion CO 3 µmol kg−1 279 222 186 146 115
(20) (0) −(16) (−34) (−48)
Hydrogen ion H+ µmol kg−1 4.79 × 10−3 6.92 × 10−3 8.92 × 10−3 1.23 × 10−2 1.74 × 10−2
(−45) (0) (29) (78) (151)
Calcite saturation ! calc 6.63 5.32 4.46 3.52 2.77
(20) (0) (−16) (−34) (−48)
Aragonite saturation ! arag 4.26 3.44 2.9 2.29 1.81
(19) (0) (−16) (−33) (−47)
Dissolved inorganic DIC µmol kg−1 1952 1970 2026 2090 2144
carbon
(−1) (0) (2.8) (6.1) (8.8)
Total pH pH T 8.32 8.16 8.05 7.91 7.76
a
We assume that PO 4 = 0.5 µmol L−1 and Si = 4.8 µmol L−1 , and use the carbonic acid dissociation constants of
Mehrbach et al. (1973) as refit by Dickson and Millero (1987). pH T is based on seawater scale. Percent change from
preindustrial values are in parentheses. After Feely et al. (2008).

The aragonite and calcite saturation hori- Many of the areas where shoaling is predicted
zons of the world’s oceans are moving to to occur within the century are highly produc-
shallower depths due to the rapid influx of an- tive and home to many of the world’s most
thropogenic CO 2 to the oceans (Fig. 1). This important and economically lucrative commer-
process has been well documented and mod- cial fisheries.
eled at the global scale (Skirrow & Whitfield It is clear that human-induced changes in
1975; Broecker & Takahashi 1977; Feely & atmospheric CO 2 concentrations are funda-
Chen 1982; Feely et al. 1984, 1988; Kleypas mentally altering ocean chemistry from the
et al. 1999a; Broecker 2003; Caldeira & Wickett shallowest waters to the darkest depths of the
2003; Feely et al. 2004; Caldeira & Wickett deep sea. The chemistry of the oceans is ap-
2005; Orr et al. 2005). Future estimates of arag- proaching conditions not seen in many mil-
onite saturation horizon depth indicate that lions of years, and the rate at which this is
shoaling will occur in the North Pacific, North occurring is unprecedented (Caldeira & Wick-
Atlantic, and Southern Ocean within the cen- ett 2003). Caldeira and Wickett (2003, p. 365)
tury (Orr et al. 2005). The aragonite and cal- state “Unabated CO 2 emissions over the com-
cite saturation horizons in the North Pacific ing centuries may produce changes in ocean
are currently very shallow (Feely et al. 2004) pH that are greater than any experienced
and are moving toward the surface at a rate of in the past 300 million years, with the pos-
1–2 m per year (R.A. Feely pers. comm. 2007). sible exception of those resulting from rare,
TABLE 2. Changes in calcification in response to increased pCO 2 concentrations relative to calcification at present-day pCO 2 (∼380 ppmv)a
Approx.% change in calcification when pCO 2 is
Organism/System Mineralogy 2× preindustrial 3× preindustrial References Notes

Coccolithophores
Emiliania huxleyi Calcite −25 Sciandra et al. 2003
E. huxleyi &&
−9 −18 Riebesell et al. 2000; Decrease in CaCO 3 /cell
Zondervan et al. 2001
E. huxleyi &&
−40 Delille et al. 2005 Initial pCO 2 = 713 ppmv. Decrease
in net community calcification
Gephyrocapsa oceanica &&
−29 −66 Riebesell et al. 2000; Decrease in CaCO 3 /cell
Zondervan et al. 2001
Coccolithus pelagicus &&
0 0 Langer et al. 2006 No change in CaCO 3 /cell
Calcidiscus leptoporus −25 Langer et al. 2006 Decrease in CaCO 3 ; decrease
also observed at 180 ppmv
Foraminifera
Orbulina universa Calcite −8 −14 Spero et al. 1997; Decrease in shell weight
Guinotte & Fabry: Ocean Acidification and Marine Ecosystems

Bijma et al. 1999;

Bijma et al. 2002
Globigerinoides sacculifer &&
−4 to −6 −6 to −8 Bijma et al. 1999; Decrease in shell weight
Bijma et al. 2002
Scleractinian corals
Stylophora pistillata &&
−14 −20 Gattuso et al. 1998 Curve was nonlinear, linear fit
was made for ! arag from 2.0−3.9
S. pistillata &&
0 to −50 Reynaud et al. 2003 Level of response is temperature-
dependent
Acropora cervicornis Aragonite −40 −59 Renegar & Riegl 2005
323
 324

TABLE 2.
Approx.% change in calcification when pCO 2 is
Organism/System Mineralogy 2× preindustrial 3× preindustrial References Notes

Acropora eurystoma &&

−55 Schneider & Erez 2006
Acropora verweyi &&
−12 −18 Marubini et al. 2003
P. compressa + Montipora capitata &&
−40 −59 Langdon & Atkinson 2005
Porites compressa &&
−17 −25 Marubini et al. 2001
P. lutea &&
−38 −56 Ohde & Hossain 2004
P. lutea &&
−33 −49 Hossain & Ohde 2006
P. porites &&
−16 Marubini & Thake 1999
Pavona cactus &&
−14 −20 Marubini et al. 2003
Fungia sp. &&
−47 −69 Hossain and Ohde 2006
Galaxea fascicularis &&
−12 −18 Marubini et al. 2003
G. fascicularis &&
−56 −83 Marshall & Clode 2002
Turbinaria reniformis &&
−9 −13 Marubini et al. 2003
Coralline red algae
Porolithon gardineri High-Mg calcite −25 Agegian 1985
Mesocosms and field studies
Biosphere 2 Mixed −56 −83 Langdon et al. 2000 Dominated by coralline red algae
Monaco mesocosm &&
−21 Leclercq et al. 2000
Monaco mesocosm &&
−15 Leclercq et al. 2002
Bahamas Bank &&
−57 −85 Broecker & Takahashi 1966
Rukan-sho, Okinawa &&
−45 −67 Ohde & van Woesik 1999
Nature Reserve Reef, Red Sea &&
−55 Silverman et al. 2007
a
Nearly all organisms tested to date show reduced calcification in response to elevated pCO2 and decreased carbonate ion concentration and carbonate saturation state.
Modified from Kleypas et al. (2006).
Annals of the New York Academy of Sciences
Guinotte & Fabry: Ocean Acidification and Marine Ecosystems 325

Figure 1. (A) Depth of the aragonite saturation horizon (ASH), locations of deep-sea
bioherm-forming corals, and diversity contours for 706 species of azooxanthellate corals.
Projected ASH depth for year 1765 (preindustrial); pCO 2 = 278 ppmv. Green triangles
are locations of six deep-sea, scleractinian, bioherm-forming coral species (Lophelia pertusa,
Madrepora oculata, Goniocorella dumosa, Oculina varicosa, Enallopsammia profunda, and
Solenosmilia variabilis). Numerals not falling on diversity contours indicate number of azoox-
anthellate coral species. Reprinted with permission from Guinotte et al . (2006). (B) Projected
ASH depth for year 2040; pCO 2 = 513 ppmv. (C) Projected ASH depth for year 2099; pCO 2
= 788 ppmv. Black areas appearing in the Southern Ocean and North Pacific indicate areas
where the ASH depth has reached the surface. (In color in Annals online.)
326 Annals of the New York Academy of Sciences

catastrophic events in Earth history” (Caldeira Calcification and Dissolution

and Rampino 1993; Beerling and Berner Response
2002). Recent evidence suggests ocean acid-
ification was a primary driver of past mass Hermatypic Corals (Zooxanthellate)
extinctions and reef gaps, which are time The calcification response of reef-building
periods on the order of millions of years corals to decreases in aragonite saturation state
that reefs have taken to recover from mass has been well documented for a handful of se-
extinctions (Stanley 2006; Veron 2008). Za- lect species. These experiments have been con-
chos and colleagues (2005) calculated that if ducted in laboratory tanks and mesocosms, but
the entire fossil fuel reservoir (ca. 4500 GtC) to date have not been conducted in in situ field
were combusted, the impacts on deep-sea pH experiments under “natural” conditions. Evi-
and biota would probably be similar to those dence from species tested to date indicate that
in the Paleocene–Eocene Thermal Maximum the calcification rates of tropical reef-building
(PETM), 55 million years ago. The PETM corals will be reduced by 20–60% at double
likely caused a mass extinction of benthic preindustrial CO 2 concentrations (pCO 2 ca.
foraminifera (Zachos et al. 2005). Projected an- 560 ppmv) (Gattuso et al. 1998; Kleypas et al.
thropogenic carbon inputs will occur within just 1999a; Langdon et al. 2000; Kleypas & Lang-
300 years, which is thought to be much faster don 2002; Langdon et al. 2003; Reynaud et al.
than the CO 2 release during the PETM and too 2003; Langdon & Atkinson 2005; c.f. Royal
rapid for dissolution of calcareous sediments to Society 2005; c.f. Kleypas et al. 2006) (see
neutralize anthropogenic CO 2 . Consequently, Table 2). Figure 2 illustrates the projected re-
the ocean acidification-induced impacts on sur- duction in surface-water aragonite saturation
face ocean pH and biota will probably be more state through the year 2069. A reduction in cal-
severe than during the PETM (Zachos et al. cification of this magnitude could fundamen-
2005). tally alter the current structure and function of
While it is apparent changing seawater coral-reef ecosystems, as their growth is depen-
chemistry will have serious consequences for dent on their ability to accrete at faster rates
many marine calcifiers, the effects of ocean than erosional processes can break them down.
acidification on noncalcifiers and the ecosys- Reef accretion will become increasingly more
tem responses to these changes will be com- critical in the coming decades, as global sea
plex and difficult to quantify. Assessing whether levels rise and available light for photosynthe-
ocean acidification is the primary driver of sis becomes a limiting factor for corals at the
a species’ population decline will be diffi- deepest reaches of the photic zone.
cult due to the multitude of ongoing phys- A substantial decrease in the number of car-
ical and chemical changes currently occur- bonate ions available in seawater will have se-
ring in the ocean. Ocean acidification is oc- rious implications for coral calcification rates
curring in synergy with significant ongoing and skeletal formation. Weaker coral skele-
environmental changes (e.g., ocean temper- tons will probably result from a reduction in
ature increases), and these cumulative im- carbonate ions, enabling erosional processes
pacts or interactive effects of multiple stressors to occur at much faster rates than have oc-
may have more significant consequences for curred in the past, and slower growth rates
biota than any single stressor. Thus, research may also reduce corals’ ability to compete for
into the synergistic effects of these changes space and light, though no studies have been
on marine organisms and the consequent conducted to test this hypothesis (reviewed in
ecosystem responses is critical but still in its Kleypas et al. 2006). Biosphere II mesocosm ex-
infancy. periments suggest that net reef dissolution will
Guinotte & Fabry: Ocean Acidification and Marine Ecosystems 327

Figure 2. (A) Surface aragonite saturation state. Calculated preindustrial (1870) ! arag values; pCO 2
= 280 ppmv. Green dots represent present-day distribution of zooxanthellate coral reefs. Figure modified
from Guinotte et al . (2003). Figure legend classification from Kleypas et al . (1999b). (B) Surface aragonite
saturation state. Projected ! arag values, 2060–2069; pCO 2 = 517 ppmv. (In color in Annals online.)

outpace net reef calcification when carbonate Edmunds (2007) documented a decline in the
ion concentration decreases to about 150 to growth rates of juvenile scleractinian corals in
110 µmole kg−1 , a range that corresponds to the U.S. Virgin Islands and raised the possi-
atmospheric CO 2 concentrations of 560–840 bility that the effects of global climate change
ppmv (C. Langdon pers. comm. 2007). Hoegh- (increased seawater temperatures and decreas-
Guldberg and colleagues (2007) stated that ing aragonite saturation state) have already re-
aragonite saturation values will favor erosion duced the growth rate of juvenile corals.
when the carbonate ion concentration ap- Fine and Tchernov (2007a) reported two
proaches 200 µmole kg−1 (atmospheric CO 2 species of scleractinian corals were able to sur-
concentration = 480 ppmv). The effects of a vive corrosive water conditions (pH values of
reduction in calcification rates on recruitment, 7.3–7.6), which caused their skeletons to dis-
settlement, and juvenile life stages of most ma- solve completely, leaving the coral polyps ex-
rine calcifiers, including the majority of scler- posed. When water chemistry returned to nor-
actinian corals, are not well known. However, mal/ambient conditions, the coral polyps were
328 Annals of the New York Academy of Sciences

able to recalcify their skeletons without any ob- rot fish, and several species of mollusks (Littler
vious detrimental effects. These findings shed & Littler 1984; Chisholm 2000; Diaz-Pulido
new light on the hypothesis that corals have a et al . 2007). CCA also provide important hard
means of alternating between soft bodies and settlement substrate for coral larvae (Heyward
skeletal forms, which are absent from the fos- & Negri 1999; Harrington et al. 2005; Diaz-
sil record during reef gaps (Stanley & Fautin Pulido et al. 2007). Coralline algae produce cal-
2001; Medina et al. 2006; Stanley 2006; Fine cium carbonate in the form of high-magnesium
& Tchernov 2007a). Fine and Tchernov’s re- calcite, a more soluble form of calcium carbon-
sults offer some hope for the future of corals ate than either calcite or aragonite, which make
in a high CO 2 world, but caution should be these species particularly sensitive to decreasing
exercised as these manipulative experiments carbonate saturation states.
did not include the effects of predation on the Mesocosm experiments exposing CCA to el-
“naked” coral polyps. Hard skeletons also pro- evated pCO 2 (2 × present day) indicate up to a
vide another core function for coral polyps by 40% reduction in growth rates, 78% decrease
protecting them from periodic natural events in recruitment, 92% reduction in total area cov-
such as tsunamis and cyclones, which can cause ered by CCA, and a 52% increase in noncal-
significant damage to coral colonies and reef cifying algae (Buddemeier 2007; Kuffner et al.
systems. 2008). Agegian (1985) also reported a reduc-
There is some discrepancy regarding the rep- tion in recruitment when CCA were exposed to
resentativeness of the coral species used in the elevated pCO 2 in aquarium experiments. Bud-
Fine and Tchernov calcification experiments. demeier (2007) states, “The combined effects of
Stanley (2007) stated the experiments may reduced carbonate production and diminished
not be representative of all coral species, par- stabilization (cementation) of coasts and shal-
ticularly zooxanthellate reef-building species, low seafloors by encrusting calcifiers are likely
which might have responded quite differently to lead to more rapid erosion and ecosystem
to the experiments because of the complex transitions (macroalgal takeover) than would
nature of their photosymbiosis. This assertion be expected on the basis of decreases in coral
was challenged by Fine & Tchernov (2007b) growth alone.” The ecological importance of
in the statement that the evolution and physi- coralline algae to reef systems and the effects
ology of the studied species are indistinguish- decreasing carbonate saturation state will have
able from tropical reef-building species. Rep- on these organisms have been overlooked to a
resentativeness aside, both parties agree that significant degree, and more research is needed
ocean acidification poses a significant threat to document CCA response to reduced car-
to coral-reef ecosystems and the services they bonate saturation states and in turn how these
provide. responses will impact reef ecosystems.

Calcifying Macroalgae Halimeda

Halimeda is a genus of green, calcifying
Coralline Algae macroalgae that forms extensive beds in cer-
Scleractinian corals are not the only reef- tain regions of the world’s oceans. Some of
calcifying organisms that are sensitive to de- the most well-developed Halimeda beds occur
creasing saturation states. Crustose coralline al- off the northeast coast of Australia, and es-
gae (CCA) are a critical player in the ecology of timates of total area covered by Halimeda in
coral-reef systems as they provide the “cement” the Great Barrier Reef region are upwards
that helps stabilize reefs, make significant sed- of 2000 km2 (reviewed by Diaz-Pulido et al.
iment contributions to these systems, and are 2007). Halimeda, along with other calcareous
important food sources for sea urchins, par- algae (Udotea, Amphiroa, and Galaxaura), are
Guinotte & Fabry: Ocean Acidification and Marine Ecosystems 329

important producers of marine sediments are six species of azooxanthellate, bioherm-

and contribute to reef accretion by filling forming, scleractinian corals (Lophelia pertusa,
voids in the reef matrix with their sediments Madrepora oculata, Goniocorella dumosa, Oculina
(Hillis-Colinvaux 1980; Davies & Marshall varicosa, Enallopsammia profunda, and Solenosmilia
1985; Drew & Abel 1988; Diaz-Pulido et al. variabilis), all of which produce calcium carbon-
2007). Reefs and Halimeda bioherms have high ate skeletons of aragonite. Cold water corals
calcification rates and are responsible for the bioherms have extremely high biodiversity and
majority of CaCO 3 production and accumu- provide habitat and nursery areas for many
lation on the continental shelf (Milliman & deep-sea organisms, including several commer-
Droxler 1996; Kleypas et al. 2006). cially important fish species (Rogers 1999; Fossa
The three-dimensional structures Halimeda et al. 2002; Husebo et al. 2002). Scleractinian
form, which can be 20 m in height, provide im- cold water corals are not the only azooxanthel-
portant habitat for adult fishes and may serve as late habitat formers.
nursery grounds for juvenile fishes and inverte- The “coral gardens” of the North Pacific are
brates (Beck et al. 2003). Calcifying macroalgae biodiversity hotspots dominated by octocorals
produce biogenic calcium carbonate in three (soft corals, stoloniferans, sea fans, gorgonians,
forms: high-magnesium calcite, aragonite, and and sea pens) and stylasterids, the majority of
calcite; all of these forms are susceptible to the which produce calcite spicules and holdfasts
negative effects of decreasing carbonate satura- (Cairns & Macintyre 1992; Guinotte et al. 2006;
tion states (Littler & Littler 1984). Few species Stone 2006). Stone (2006) reported that 85%
of Halimeda have been exposed to high pCO2 of the economically important fish species ob-
in lab experiments, but one species from the served on submersible transects in waters off
Great Barrier Reef, Halimeda tuna, displayed a the Aleutian Islands were associated with corals
negative calcification response when exposed and other emergent epifauna. The waters off
to a pH drop of 0.5 units (8 to 7.5) (Borowitzka the Aleutian Islands have the highest abun-
& Larkum 1986). dance and diversity of cold-water corals found
to date in high-latitude ecosystems (Heifetz et al.
Cold Water Corals (Azooxanthellate) 2005; Stone 2006), but well-developed scler-
actinian bioherms are curiously absent from
Cold water corals and the ecologically this region even though scleractinian bioherm-
rich bioherms they form are widely dis- forming species are found in North Pacific wa-
tributed throughout the world oceans (see ters (Guinotte et al. 2006).
Fig. 1). A great number of these highly pro- The reason scleractinian bioherms are not
ductive ecosystems have been discovered only present in North Pacific waters could be a
in the last decade, and it is thought that the function of the shallow depth of the arago-
area covered by these organisms may surpass nite saturation horizon and high dissolution
the total area of tropical zooxanthellate reef rates throughout the region (Guinotte et al.
systems (Mortensen et al. 2001; Freiwald et al. 2006). If this hypothesis is true, then decreas-
2004; Freiwald & Roberts 2005; Guinotte et al. ing carbonate saturation state will probably
2006; Turley et al. 2007). Cold water corals are impact scleractinian cold-water corals earlier
azooxanthellate, which means they do not con- than shallow-water reef builders. Cold-water
tain photosynthetic algae, and thus are not lim- corals are bathed in cold, deep waters that
ited to the photic zone. The majority of cold have naturally high levels of CO2 (global av-
water corals are found in depths of 200–1000 erage ! arag = 2). The low carbonate saturation
m or more, and some solitary colonies have state environment in which they live probably
been found at depths of several thousand me- contributes to their slow growth/calcification
ters (Freiwald 2002; Freiwald et al. 2004). There rates, which are an order of magnitude slower
330 Annals of the New York Academy of Sciences

than tropical zooxanthellate corals (global aver- that calcification rates of the mussel (Mytilus
age ! arag = 4). Indeed, some deeper cold-water edulis) and Pacific oyster (Crassostrea gigas) can
coral bioherms could already be experiencing be expected to decline linearly with increas-
corrosive conditions with respect to aragonite ing pCO 2 , 25% and 10% respectively, by the
saturation state (! arag < 1), though no evidence end of the century (ca. 740 ppmv, IPCC IS92a
of this has been documented. scenario). Both species are important coastal
Greater than 95% of the present day ecosystem engineers and represent a signif-
distribution of bioherm-forming scleractinian icant portion of global aquaculture produc-
species occur in waters that are supersaturated tion (Gazeau et al. 2007). Bivalves that settle
with aragonite (Guinotte et al. 2006). Future in coastal estuarine areas may be particularly
aragonite saturation state projections from Orr vulnerable to anthropogenic ocean acidifica-
and co-authors (2005) indicate that 70% of scle- tion. These organisms naturally experience ex-
ractinian cold-water coral bioherms could be tremely high mortality rates (>98%) in their
in undersaturated water with respect to arago- transition from larvae to benthic juveniles (re-
nite by the end of the century (Guinotte et al. viewed by Green et al. 2004), and any increase
2006; Turley et al. 2007) (see Fig. 1). Labora- in juvenile mortality due to ocean acidification
tory experiments are currently being conducted could have serious effects on estuarine bivalve
to test whether cold water corals scleractinians populations.
(Lophelia pertusa) are sensitive to decreasing arag- Kurihara and colleagues (2007) demon-
onite saturation state (Riebesell pers. comm.), strated that increased pCO 2 of seawater pro-
but no lab experiments have been conducted jected to occur by the year 2300 (pH 7.4) will
to test the sensitivity of cold-water octocorals severely impact the early development of the
and stylasterids to decreasing carbonate satu- oyster Crassostrea gigas and highlighted the im-
ration states. Manipulative CO 2 experiments portance of acidification effects on larval de-
to determine cold-water coral sensitivity and velopment stages of marine calcifiers. Because
calcification response to decreasing carbonate early life stages appear to be more sensitive
saturation states are a top priority for future to environmental disturbance than adults and
research (Guinotte et al. 2006; Kleypas et al. most benthic calcifiers possess planktonic lar-
2006; Roberts et al. 2006; Turley et al. 2007). val stages, fluctuations in larval stages due to
high mortality rates may exert a strong influ-
Benthic Mollusks, Bryozoans, ence on the population size of adults (Green
and Echinoderms et al. 2004). Kurihara and co-authors (2004)
investigated the effects of increased pCO 2 on
The physiological and ecological impacts of the fertilization rate and larval morphology of
increasing pCO 2 on benthic mollusks, bry- two species of sea urchin embryos (Hemicentrotus
ozoans, and echinoderms are not well known, pulcherrimus and Echinometra mathaei) and found
and few manipulative experiments have been the fertilization rate of both species declined
carried out to determine sensitivity to ele- with increasing CO 2 concentration. In addi-
vated pCO 2 (Kleypas et al. 2006). The nega- tion, the size of pluteus larvae decreased with
tive effects of acidic waters on bivalves have increasing CO 2 concentration and malformed
been investigated in a small number of stud- skeletogenesis was observed in larval stages of
ies (Kuwatani & Nishii 1969; Bamber 1987, both species. Kurihara and Shirayama (2004)
1990; Michaelidis et al. 2005; Berge et al. 2006), concluded that both decreasing pH and altered
and only one investigated the negative calci- carbonate chemistry affect early development
fication response to pCO 2 levels within the and life history of many marine organisms,
range predicted by the IPCC (Gazeau et al. which will result in serious consequences for
2007). Gazeau and colleagues (2007) found marine ecosystems.
Guinotte & Fabry: Ocean Acidification and Marine Ecosystems 331

Experiments focusing on the direct effects capsa oceanica) show decreased calcification
of increasing ocean acidification on marine rates ranging from 25 to 66% when pCO 2
calcifiers have been the dominant activity to is increased to 560–840 ppmv, respectively
date, but numerous and ecologically significant (TABLE 2) in lab and mesocosm experiments. In
indirect effects are probable. Bibby and col- lab experiments with the coccolithophore Coc-
leagues (2007) documented interesting behav- colithus pelagicus, however, Langer et al. (2006)
ioral, metabolic, and morphological responses found that calcification did not change with in-
of the intertidal gastropod Littorina littorea to creased CO 2 . Moreover, there is evidence sug-
acidified seawater (pH = 6.6). This marine snail gesting that at least one coccolithophore species
produced thicker shells when exposed to preda- may have the capacity to adapt to changing
tion (crab) cues in control experiments, but this pCO 2 over long periods. Experimental manip-
defensive response was disrupted when pH was ulations show that Calcidiscus leptoporus exhibits
decreased. The snails also displayed reduced highest calcification rates at present-day CO2
metabolic rates and an increase in avoidance levels, with malformed coccoliths and cocco-
behavior, both of which could have significant spheres at both lower and higher pCO 2 (Langer
ecosystem implications via organism interac- et al. 2006). Because no malformed coccol-
tions, energy requirements, and predator–prey iths were observed in sediments from the Last
relationships. This study investigated only one Glacial Maximum (when pCO 2 levels were
species of mollusk, but other marine organisms about 200 ppmv), the authors concluded that
will probably have indirect responses to ocean C. leptoporus has adapted to present-day CO 2
acidification (Bibby et al. 2007). levels.
In lab experiments with two species of plank-
Coccolithophores, Foraminifera, tonic foraminifera, shell mass decreased as the
and Pteropods carbonate ion concentration of seawater de-
creased (Spero et al. 1997; Bijma et al. 1999,
The major planktonic producers of CaCO 3 2002). When grown in lab experiments in
are coccolithophores (single-celled algae), seawater chemistry equivalent to pCO2 val-
foraminifera (protists), and euthecosomatous ues of 560 and 740 ppmv, shell mass of the
pteropods (planktonic snails). Coccol- foraminifera Orbulina universa and Globigerinoides
ithophores and foraminifera secrete CaCO 3 in sacculifer declined by 4–8% and 6–14%, respec-
the form of calcite, whereas pteropods secrete tively, compared to the shell mass secreted at
shells made of aragonite, which is about 50% the preindustrial pCO 2 value.
more soluble in seawater than calcite (Mucci Data for a single species of shelled pteropods
1983). These planktonic groups differ with suggest that net shell dissolution occurs in live
respect to their size, trophic level, generation pteropods when the aragonite saturation is
time, and other ecological attributes. High forced to <1.0 (Orr et al. 2005; Fabry et al.
quality, quantitative data on the latitudinal and 2008). When live pteropods (Clio pyramidata)
vertical distributions and abundances of these were collected in the subarctic Pacific and ex-
calcareous taxa are lacking, and estimates of posed to a level of aragonite undersaturation
their contributions to global calcification rates similar to that projected for Southern Ocean
are poorly constrained. surface waters by the year 2100 under the IS92a
The calcification response of coccol- emissions scenario, shell dissolution occurred
ithophores, foraminifera, and pteropods to within 48 hours, even though animals were ac-
ocean acidification has been investigated to tively swimming.
date in very few species. Most studies have in- The response of planktonic calcifying or-
volved bloom-forming coccolithophores, and ganisms to elevated pCO2 may not be uni-
these species (Emiliania huxleyi and Geophyro- form among species or over time. To date,
332 Annals of the New York Academy of Sciences

published research indicates that most cal- 2004, 2005). Most experiments undertaken to
careous plankton show reduced calcification date involved altering pH to levels consistent
in response to decreased carbonate ion con- with conditions that would be present if CO 2
centrations; however, the limited number of were to be directly injected to the seafloor
species investigated precludes identification of (pH ca. 5.8–6.2). These experiments have
widespread or general trends. All studies thus shown adverse negative effects of acidified sea-
far on the impacts of ocean acidification water on fish throughout their entire life cycle
on calcareous plankton have been short-term (eggs, larvae, juveniles, and adults) (Kikkawa
experiments, ranging from hours to weeks. et al. 2003, 2004; Ishimatsu et al. 2004; Portner
Nothing is known about the long-term impacts et al. 2004).
of elevated pCO2 on the reproduction, growth, Fish in early developmental stages are more
and survivorship of planktonic calcifying or- sensitive to environmental change than adults
ganisms or their ability to adapt to changing and a limited number of studies have shown
seawater chemistry. Chronic exposure to in- this to be true when fish eggs, larvae, and juve-
creased pCO 2 may have complex effects on the niles were exposed to elevated CO2 (McKim
growth and reproductive success of calcareous 1977; Kikkawa et al. 2003, 2004; Ishimatsu
plankton or may induce adaptations that are et al. 2004). Ishimatsu and co-authors (2004)
absent in short-term experiments. No studies state, “Even if the severity of environmental
have investigated the possibility of differential hypercapnia due to CO 2 sequestration is made
impacts with life stage or age of the organism. tolerable to adults, a gradual reduction in pop-
Additional experimental evidence from plank- ulation size and changes in marine ecosystem
tonic calcifiers is urgently needed if we are structures are unavoidable consequences when
to develop a predictive understanding of the young individuals cannot survive” (p. 732). The
impacts of ocean acidification on planktonic long-term effects and adaptation potential of
communities. fishes experiencing future pCO 2 levels consis-
tent with IPCC scenarios are not known.

Physiological Reponses
Photosynthetic Organisms
Fishes
Phytoplankton and Cyanobacteria
Elevated CO2 partial pressures (hyper-
capnia) will affect the physiology of water- Most species of marine phytoplankton have
breathing animals by inducing acidosis in the carbon-concentrating mechanisms that accu-
tissues and body fluids of marine organisms, mulate inorganic carbon either as CO 2 or
including fishes (Roos & Boron 1981; Portner HCO− 3 or both (Giordano et al. 2005). Owing
et al. 2004). pH, bicarbonate, and CO 2 lev- in large part to their carbon-acquisition mech-
els within the organism are altered with long- anisms and efficiencies, most marine phyto-
term effects on metabolic functions, growth, plankton tested to date in single-species lab ex-
and reproduction, all of which could be harm- periments or natural community-perturbation
ful at population and species levels (Portner experiments show either no change or small
et al. 2004). Short-term effects of elevated CO 2 increases (generally ≤ 10%) in photosynthetic
on fishes include alteration of the acid–base rates when grown under high pCO2 condi-
status, respiration, blood circulation, and ner- tions equivalent to ca. 760 micro atmosphere
vous system functions, while long-term effects (µatm) (Tortell et al. 1997; Hein & Sand-Jensen
include reduced growth rate and reproduc- 1997; Burkhardt et al. 2001; Tortell and Morel
tion (Ishimatsu & Kita 1999; Ishimatsu et al. 2002; Rost et al. 2003; Beardall & Raven 2004;
Guinotte & Fabry: Ocean Acidification and Marine Ecosystems 333

Schippers et al. 2004; Giordano et al. 2005; 1.0 pH unit change. He concluded that small
Martin & Tortell 2006). Unlike other major changes in ambient seawater pH could affect
phytoplankton groups investigated thus far, the species growth rates, abundances, and succes-
coccolithophorid Emiliania huxleyi has low affin- sion in coastal phytoplankton communities. Eu-
ity for inorganic carbon and could be carbon- trophication and ocean acidification may act
limited in today’s ocean (Rost & Riebesell in concert to amplify the pH range found in
2004). Whether E. huxleyi will show increased coastal habitats, which in turn could lead to
rates of photosynthesis with progressive oceanic increased frequency of blooms of those species
uptake of atmospheric CO 2 , however, may de- with tolerance to extreme pH (cf. Hinga 2002).
pend on nutrient availability and light condi- In both coastal and open ocean environments,
tions (Zondervan 2007). In a recent mesocosm ocean acidification could also affect primary
CO 2 manipulation, study, Riebesell and col- productivity through pH-dependent speciation
leagues (2007) reported that CO 2 uptake by a of nutrients and metals (Zeebe & Wolf-Gladrow
phytoplankton community (primarily diatoms 2001; Huesemann et al. 2002).
and coccolithophores) in experimental pCO 2
treatments of 700 and 1050 µatm was 27% and Seagrasses
39% higher, respectively, relative to the pCO2
treatment of 350 µatm. Seagrasses represent one of the most bio-
Ocean acidification will be accompanied logically rich and productive marine ecosys-
by climate warming in large expanses of the tems in the ocean. They create critical nursery
oceans. Higher sea-surface temperatures in- grounds for juvenile fishes and important habi-
crease thermal stratification of the upper ocean, tat for adult fishes, invertebrates, and mollusks.
thereby reducing the vertical mixing of nutri- Several higher order and endangered species
ents to surface waters, and have been linked to rely on seagrasses for a significant portion of
observed decreases in phytoplankton biomass their diet (e.g., dugongs, manatees, and green
and productivity, particularly at low and mid- sea turtles). Seagrass ecosystems are a critical
latitudes (Behrenfeld et al. 2006). In warm, component to maintaining the biological diver-
nutrient-poor tropical and subtropical regions, sity of the oceans and could be one of the few
however, continued ocean absorption of an- ecosystems that stand to benefit from increas-
thropogenic CO 2 may enhance fixation of ing levels of CO 2 in seawater. Seagrasses are
atmospheric nitrogen and could lead to in- capable of dehydrating HCO− 3 , but many ap-
creased total primary productivity. Nitrogen- pear to use CO 2 (aq) for at least 50% of their
fixing cyanobacteria in the genus Trichodesmium, carbon requirements used for photosynthesis
which support a large portion of primary pro- (Palacios & Zimmerman 2007). Zimmerman
ductivity in such low-nutrient areas of the and colleagues (1997) found that short-term
world’s oceans, show increased rates of nitro- (ca. 45 days) CO 2 (aq) enrichment increased
gen and carbon fixation under elevated pCO2 photosynthetic rates and reduced light require-
(Hutchins et al. 2007; Barcelos e Ramos et al. ments for eelgrass (Zostera marina L) shoots in
2007). At CO 2 levels of 750 ppmv, Trichodesmium laboratory experiments.
increased N 2 fixation rates by 35–100% and Longer-term (1 year) experiments expos-
CO 2 fixation rates by 15–128%, relative to ing Zostera marina L to CO 2 (aq) concentra-
present-day CO 2 conditions (Hutchins et al. tions of 36–1123 µM (pH 7.75–6.2) conducted
2007). by Palacios and Zimmerman (2007) resulted
In a review of coastal marine phytoplankton, in higher reproductive output, an increase in
Hinga (2002) found that while some species below-ground biomass, and vegetative prolifer-
grow well at a wide range of pH, others have ation of new shoots when light was in abundant
growth rates that vary greatly over a 0.5 to supply. These findings suggest that as the CO 2
334 Annals of the New York Academy of Sciences

content of the surface ocean rises, so too will the net effects on fish abundance and diver-
the productivity of seagrass meadows, which sity. Predicting the net effects on fish popula-
in turn may positively influence invertebrate tions is further complicated by the plethora of
and fish populations. This increase in produc- unknowns surrounding the long-term effects of
tivity will probably be true for other seagrass increasing CO 2 on fish physiology, metabolism,
species as most appear to be photosynthetically and probable range shifts due to ocean
limited by the present-day availability of CO2 warming.
(Durako 1993; Invers et al. 2001; Palacios and
Zimmerman 2007). Palacios and Zimmerman
Cold-water Corals and Fishes
(2007) noted that a significant indirect effect
of increased eelgrass density could be an in- The ecology and species relationships of
crease in sediment retention, which could lead cold-water coral ecosystems are not as ad-
to increased water clarity and an expansion in vanced as the state of knowledge for shallow-
the depth distribution of eelgrasses to deeper water coral-reef systems, which is due in large
waters. part to logistical challenges and the expense
Community Impacts of operating vessels and submersibles in the
deep sea. However, cold-water coral ecosys-
Seagrasses, Coral Reefs, and Fishes tems are thought to provide important habi-
tat, feeding grounds, and recruitment/nursery
Seagrass meadows and mangroves provide functions for many deep-water species, includ-
important nursery areas for juvenile fishes, ing several commercially important fish species
many of which migrate to coral reefs as adults, (Mortensen 2000; Fossa et al. 2002; Husebo et al.
and enhance fish diversity and abundance on 2002; Roberts et al. 2006). Many of the species
coral reefs adjacent to these ecosystems (Pollard relationships are thought to be facultative, but
1984; Parrish 1989; Beck et al. 2001; Sheridan nonetheless, high fish densities have been re-
& Hays 2003; Mumby et al. 2004; Dorenbosch ported for these structure-forming ecosystems
et al. 2005). The net effect of increasing CO 2 on (Husebo et al. 2002; Costello et al. 2005; Stone
seagrass ecosystems will probably be increased 2006). Populations of grouper, snapper, and
seagrass biomass and productivity, assuming amberjack use the Oculina varicosa reefs off
water quality and clarity (low suspended sed- the Florida coast as feeding and spawning ar-
iment) are sufficient for photosynthesis to oc- eas (Reed 2002), even though their numbers
cur. Under these conditions, it is probable that have been dramatically reduced by commer-
an increase in total seagrass area will lead to cial and recreational fishing in recent decades
more favorable habitat and conditions for asso- (Koenig et al. 2000). Large aggregations of red-
ciated invertebrate and fish species. However, fish (Sebastes spp.), ling (Molva molva), and tusk
the net effect of ocean acidification on coral reef (Brosme brosme Ascanius) have been documented
ecosystems will probably be negative as many in the Lophelia pertusa reefs of the North Atlantic
reef-building marine calcifiers will be heavily (Husebo et al. 2002), and strong fish–coral asso-
impacted by the combined effects of increasing ciations exist in the cold-water coral ecosystems
sea-surface temperatures (coral bleaching) and of the North Pacific (Stone 2006).
decreasing carbonate saturation states of sur- Ocean acidification could have significant
face waters in the coming decades (Guinotte indirect effects on fishes and other deep-
et al. 2003; Buddemeier et al. 2004). The mag- sea organisms that rely on cold-water coral
nitude of both ecosystem responses to ocean ecosystems for protection and nutritional re-
acidification and other environmental changes quirements. Roberts and Gage (2003) docu-
working in synergy is difficult to predict as are mented over 1300 species living on the Lophelia
Guinotte & Fabry: Ocean Acidification and Marine Ecosystems 335

pertusa reefs in the NE Atlantic. Future depth for example, pteropods can be important prey
projections for the aragonite saturation hori- for juvenile pink salmon (Oncorhynchus gobuscha),
zons indicate 70% of cold-water scleractinians as well as chum and sockeye salmon, pollock,
will be in undersaturated waters by the end of and other commercially important fishes (Ay-
the century, and significant decreases in cal- din pers. comm.). Armstrong and co-authors
cification rate could occur well before corals (2005) reported interannual variability in the
experience undersaturated conditions as arag- diet of juvenile pink salmon, with a single
onite saturation state decreases progressively species of pteropod (Limacina helicina) compris-
over time (Guinotte et al. 2006). Quantifying ing 15 to 63% by weight of pink salmon di-
the indirect impacts of ocean acidification on ets during a 3-year study. Because Pacific pink
coral-associated fishes is not possible due to salmon have a short, 2-year life cycle, prey
uncertainties surrounding facultative and ob- quality and abundance during the salmon’s ju-
ligate species relationships, but the net effects venile stage may strongly influence the pink
are likely to be negative as cold-water coral salmon’s adult population size and biomass
growth, distribution, and area decrease. (Aydin et al. 2005).
Jellyfish blooms (scyphomedusae, hydrome-
Plankton dusae, and cubomedusae) have increased over
the last several decades (Purcell et al. 2007), but
If reduced calcification decreases a calci- it is too soon to determine whether such recent
fying organism’s fitness or survivorship, then jellyfish increases will persist or the populations
some planktonic calcareous species may un- will fluctuate with climatic regime shifts, par-
dergo shifts in their distributions as the inor- ticularly those at decadal scales, as has been
ganic carbon chemistry of seawater changes. observed previously (Purcell 2005). Attrill and
Calcifying species that are CO− 2 sensitive could colleagues (2007) reported a significant corre-
potentially be replaced by noncalcifying species lation of jellyfish frequency in the North Sea
and/or those species not sensitive to elevated from 1971 to 1995 with decreased pH (from
pCO 2 . 8.3 to 8.1) of surface waters. Although the
By 2100, surface waters of polar and sub- causative mechanism is not known, Attrill and
polar regions are projected to become un- colleagues (2007) suggest that projected climate
dersaturated with respect to aragonite (Orr change and declining ocean pH will increase
et al. 2005). Pteropods are important com- the frequency of jellyfish in the North Sea
ponents of the plankton in high-latitude sys- over the next century. Jellyfish are both preda-
tems, with densities reaching thousands of in- tors and potential competitors of fish and may
dividuals m−3 (e.g., Bathmann et al. 1991; substantially affect pelagic and coastal ecosys-
Pane et al. 2004). If pteropods require sea- tems (Purcell & Arai 2001; Purcell 2005). It is
water that is supersaturated with respect to important to resolve possible linkages between
aragonite, then their habitat would become in- jellyfish blooms and ocean acidification and de-
creasingly limited, first vertically in the water termine whether continued changes in the sea-
column and then latitudinally, by the shoal- water inorganic carbon system will exacerbate
ing of the aragonite saturation horizon over problematic increases in jellyfish that have been
the next century (Feely et al. 2004; Orr et al. associated with climate change, overfishing, eu-
2005). If high-latitude surface waters do be- trophication, and other factors (Purcell et al.
come undersaturated with respect to arago- 2007).
nite, pteropods could eventually be eliminated Planktonic ecosystems are complex nonlin-
from such regions, with consequences to food- ear systems, and the consequences of ocean
web dynamics and other ecosystem processes acidification on such ecosystems are largely un-
(Fabry et al. 2008). In the subarctic Pacific, known. Substantial changes to species diversity
336 Annals of the New York Academy of Sciences

and abundances, food-web dynamics, and Future ocean acidification research needs in-
other fundamental ecological processes could clude increased resources and efforts devoted
occur; however, the interactions and feedbacks to lab, mesocosm, and in situ experiments, all
among the effects of chronic, progressively in- of which will aid in determining the biological
creasing ocean acidification and other environ- responses of marine taxa to increased pCO2 .
mental variables are difficult to predict. Ecosys- Mesocosm and in situ experiments may simu-
tem responses will also depend on the ability of late and/or provide more natural conditions
biota to adapt to seawater chemistry changes than single-species lab experiments, but they
that are occurring at rates they have not en- have thus far used abrupt changes in seawater
countered in their recent evolutionary history chemistry which do not allow for potential ac-
(Siegenthaler et al. 2005). Future progress will climation or adaptation by marine organisms.
likely require integrated approaches involving There is an additional need for experiments
manipulative experiments, field observations, on taxa with no commercial value but which
and models, particularly at regional scales. provide critical habitat and occupy impor-
tant trophic levels within marine food webs.
Direct CO 2 experiments on commercially im-
Summary and Conclusions portant species are clearly necessary, but non-
commercial species play crucial roles in marine
The scientific knowledge base surround- ecosystems and the life history of most com-
ing the biological effects of ocean acidifica- mercial species. The effects of ocean acid-
tion is in its infancy and the long-term con- ification on less charismatic species and/or
sequences of changing seawater chemistry on species with no economic value should not
marine ecosystems can only be theorized. Most be overlooked. The biological response of ma-
is known about the calcification response for rine organisms (both commercial and noncom-
shallow-water scleractinian corals. Some data mercial) to ocean acidification will be key to
sets allow the identification of “tipping points” making informed policy decisions that con-
or “thresholds” of seawater carbonate chem- form to sound ecosystem-based management
istry when ocean acidification will cause net principles.
calcification rates to be less than net dissolu- There is a critical need for well-developed
tion rates in coral reef systems (Yates & Halley spatial and temporal models that give accu-
2006; Hoegh-Guldberg et al. 2007). In contrast, rate present day and future estimates of arago-
the potential effects ocean acidification may nite and calcite saturation states in the coastal
have for the vast majority of marine species zones. The shallow continental shelves are
are not known. Research into the synergistic some of the most biologically productive ar-
effects of ocean acidification and other human- eas in the sea and are home to the majority
induced environmental changes (e.g., increas- of the world’s fisheries, but accurate carbonate
ing sea temperatures) on marine food webs saturation state data do not currently exist for
and the potential transformative effects these most coastal regions. Ocean acidification in-
changes could have on marine ecosystems is formation should also be integrated into exist-
urgently needed. It is important to have a firm ing ecosystem models, which attempt to predict
understanding of the degree to which ocean the effects of environmental changes on ma-
acidification influences critical physiological rine populations and ecosystem structure (e.g.,
processes such as respiration, photosynthesis, Ecopath and Ecosim). Development of these
and nutrient dynamics, as these processes are tools is essential to making credible predictions
important drivers of calcification, ecosystem of future ocean acidification effects on marine
structure, biodiversity, and ultimately ecosys- ecosystems and will aid in guiding management
tem health. decisions.
Guinotte & Fabry: Ocean Acidification and Marine Ecosystems 337

The overwhelming volume of scientific evi- Augustin, L. et al. 2004. Eight glacial cycles from an
dence collated by the IPCC documenting the Antarctic ice core. Nature 429: 623–628.
dangers of human-induced climate change, of Aydin, K.Y. et al. Linking oceanic foodwebs to coastal
production and growth rates to Pacific salmon (On-
which ocean acidification is only one, should corhynchus spp.), using models on three scales. Deep Sea
end the lingering CO 2 emissions reduction de- Res. II 52: 757–780.
bate. The global CO 2 experiment which has Bamber, R.N. 1990. The effects of acidic seawater on 3
been under way since the Industrial Revolution species of lamellibranch mollusk. J. Exp. Mar. Biol.
and the potentially dire consequences this Ecol. 143: 181–191.
Bamber, R.N. 1987. The effects of acidic sea water on
uncontrolled experiment poses for marine or-
young carpet-shell clams Venerupis decussata (L.)
ganisms and indeed, all life on Earth, leave no (Mollusca: Veneracea). J. Exp. Mar. Biol. Ecol. 108:
doubt that human dependence on fossil fuels 241–260.
must end as soon as possible. International col- Barcelos e Ramos, J. et al. 2007. Effect of rising atmo-
laboration, political will, and large-scale invest- spheric carbon dioxide on the marine nitrogen fixer
ment in clean energy technologies are essen- Trichodesmium. Global Biogeochem. Cycles 21: np.
Bathmann, U. et al. 1991. Short-term variations in par-
tial to avoiding the most damaging effects of ticulate matter sedimentation off Kapp Norvegia,
human-induced climate change. Weddell Sea, Antarctica: relation to water mass ad-
vection, ice cover, plankton biomass and feeding ac-
tivity. Polar Biol. 11: 185–195.
Acknowledgments Beardall, J. & J.A. Raven. 2004. The potential effects of
global climate change in microalgal photosynthesis,
This work was supported in part by MCBI growth and ecology. Phycologia 43: 31–45.
grants from the Edwards Mother Earth Foun- Beck, M.W. et al. 2001. The identification, conservation,
dation, Marisla Foundation, Moore Family and management of estuarine and marine nurseries
for fish and invertebrates. Bioscience 51: 633–641.
Foundation, and Mark and Sharon Bloome.
Beck, M.W. et al. 2003. The role of nearshore ecosystems
Support for VJF was provided in part by as fish and shellfish nurseries. Issues Ecol. 11: 1–12.
National Science Foundation grants OCE- Beerling, D.J. & R.A. Berner. 2002. Biogeochemical con-
0551726 and ANT-0538710. We would like straints on the Triassic-Jurassic boundary carbon cy-
to thank RW Buddemeier, RA Feely, and an cle event. Global Biogeochem. Cycles 16: 101–113.
anonymous reviewer for constructive inputs on Behrenfeld, M.J. et al. 2006. Climate-driven trends in
contemporary ocean productivity. Nature 444: 752–
an early draft. 755.
Berge, J.A. et al. 2006. Effects of increased sea water con-
centrations of CO 2 on growth of the bivalve Mytilus
Conflict of Interest edulis L. Chemosphere 62: 681–687.
Bibby, R. et al. 2007. Ocean acidification disrupts induced
The authors declare no conflicts of interest. defences in the intertidal gastropod Littorina littorea.
Biol. Lett. 3: 699–701.
Bijma, J., H.J. Spero, & D.W. Lea. 1999. Reassessing
References foraminiferal stable isotope geochemistry: Impact of
the oceanic carbonate system (experimental results).
Agegian, C.R. 1985. The Biogeochemical Ecology of In Use of Proxies in Paleoceanography: Examples from the
Porolithon gardineri (Foslie). Ph.D. thesis, University South Atlantic. G. Fischer & G. Wefer, Eds.: 489–512.
of Hawaii, Honolulu. Springer-Verlag. New York.
Armstrong, J.L. et al. 2005. Distribution, size, and interan- Bijma, J., B. Honisch, & R.E. Zeebe. 2002. The im-
nual, seasonal and diel food habits of northern Gulf pact of the ocean carbonate chemistry on living
of Alaska juvenile pink salmon, Oncorhyncus gorbuscha. foraminiferal shell weight: Comment on “Carbon-
Deep-Sea Res. II 52: 247–265. ate ion concentration in glacial-age deep waters of
Attrill, M., J. Wright & M. Edwards. 2007. Climate- the Caribbean Sea” by W.S. Broecker & E. Clark.
related increases in jellyfish frequency suggest a more Geochem. Geophys. Geosyst. 3: 1064.
gelatinous future for the North Sea. Limnol. Oceanogr. Borowitzka, L.J. & A.W.D. Larkum 1986. Reef algae.
52: 480–485. Oceanus 29: 49–54.
338 Annals of the New York Academy of Sciences

Broecker, W.S. 2003. The Ocean CaCO 3 Cycle. In The Oceans Delille, B. et al. 2005. Response of primary production
and Marine Geochemistry. H. Elderfield, Ed.: 1–21. and calcification to changes of pCO 2 during exper-
Treatise on Geochemistry, Elsevier Pergamon. Ox- imental blooms of the coccolithophorid Emiliania
ford. huxleyi. Global Biogeochem. Cycles 19: np.
Broecker, W.S. et al. 1979. Fate of fossil fuel carbon dioxide Diaz-Pulido, G. et al. 2007. Vulnerability of macroalgae of
and the global carbon budget. Science 206: 409–418. the Great Barrier Reef to climate change. In Climate
Broecker, W.S. & T. Takahashi. 1966. Calcium carbonate Change and the Great Barrier Reef . J.E. Johnson & P.A.
precipitation on the Bahama Banks. J. Geophys. Res. Marshall, Eds.: 154–192. Great Barrier Reef Marine
71: 1575–1602. Park Authority and Australian Greenhouse Office,
Broecker, W.S. & T. Takahashi. 1977. Neutralization of Australia.
fossil fuel CO 2 by marine calcium carbonate. In The Dickson, A.G. & F.J. Millero. 1987. A comparison of the
Fate of Fossil Fuel in the Oceans. N.R. Andersen & A. equilibrium constants for the dissociation of carbonic
Malahoff, Eds.: 213–241. Plenum Press. New York. acid in seawater media. Deep-Sea Res. A 34: 1733–
Buddemeier, R.W., J.A. Kleypas & R. Aronson. 2004. 1743.
Coral Reefs and Global Climate Change. Potential Doney, S.C. et al. 2007. The impacts of anthropogenic
Contributions of Climate Change to Stresses on nitrogen and sulfur deposition on ocean acidification
Coral Reef Ecosystems. Pew Center for Global Climate and the inorganic carbon system. Proc. Natl. Acad. Sci.
Change. Arlington, VA. 42 pp. 104: 14580–14585.
Buddemeier, R.W. 2007. The future of tropical reefs and coast- Dorenbosch, M. et al. 2005. Indo-Pacific seagrass beds and
lines. Presented at the American Association for the Advance- mangroves contribute to fish density and diversity on
ment of Science Annual Meeting. San Francisco, CA, Feb adjacent coral reefs. Mar. Ecol. Prog. Ser. 302: 63–76.
16. Drew, E.A., & K.M. Abel. 1988. Studies on Halimeda
Burkhardt, S. et al. 2001. CO 2 and HCO 3 uptake in ma- I. The distribution and species composition of Hal-
rine diatoms acclimated to different CO 2 concentra- imeda meadows throughout the Great Barrier Reef
tions. Limnol. Oceanogr. 46: 1378–1391. Province. Coral Reefs 6: 195–205.
Cairns, S.D. & I.G. Macintyre. 1992. Phylogenetic im- Durako, M.J. 1993. Photosynthetic utilization of CO 2 (aq)
plications of calcium carbonate mineralogy in the and HCO 3 in Thalassia testudinum (Hydrocharita-
Stylasteridae (Cnidaria:Hydrozoa). Palaios 7: 96– cae). Mar. Biol. 115: 373–380.
107. Edmunds, P.J. 2007. Evidence for a decadal-scale decline
Caldeira, K. & M.R. Rampino. 1993. Aftermath of the in the growth rates of juvenile scleractinian corals.
end-Cretaceous mass extinction: possible biogeo- Mar. Ecol. Prog. Ser. 341: 1–13.
chemical stabilization of the carbon cycle and cli- Fabry, V.J. et al. 2008. Impacts of ocean acidification on
mate. Paleoceanography 8: 515–525. marine fauna and ecosystems processes. J. Mar. Sci.
Caldeira, K. & M.E. Wickett. 2003. Anthropogenic car- In Press.
bon and ocean pH. Nature 425: 365. Feely, R.A. et al. 1988. Winter-summer variations of calcite
Caldeira, K. & M.E. Wickett. 2005. Ocean model pre- and aragonite saturation in the northeast Pacific.
dictions of chemistry changes from carbon dioxide Mar. Chem. 25: 227–241.
emissions to the atmosphere and ocean. J. Geophys. Feely, R.A., & C.T.A. Chen. 1982. The effect of excess
Res. 110: np. CO 2 on the calculated calcite and aragonite satura-
Caldeira, K. et al. 2007. Comment on “Modern- tion horizons in the Northeast Pacific. Geophys. Res.
age buildup of CO2 and its effects on seawa- Lett. 9: 1294–1297.
ter acidity and salinity” by Hugo A. Loaiciga. Feely, R.A. et al. 2008. Present and future changes in
Geophysical Research Letters 34: L18608. doi: seawater chemistry due to ocean acidification. AGU
10.1029/2006GL027288. Monograph, The Science and Technology of CO 2 Seques-
Chisholm, J.R.M. 2000. Calcification by crustose tration. In Press.
coralline algae on the northern Great Barrier Reef, Feely, R.A. et al. 2004. Impact of anthropogenic CO 2
Australia. Limnol. Oceanogr. 45: 1476–1484. on the CaCO 3 system in the oceans. Science 305:
Costello, M. et al. 2005. Role of cold-water Lophelia 362–366.
pertusa coral reefs as fish habitat in the NE At- Feely, R.A. et al. 1984. Factors influencing the degree of
lantic. In Cold-water Corals and Ecosystems. A. Freiwald saturation of the surface and intermediate waters of
& J.M. Roberts, Eds.: 771–805. Springer-Verlag. the North Pacific Ocean with respect to aragonite.
Berlin, Heidelberg. J. Geophys. Res. 89: 631–640.
Davies, P.J. & J.F. Marshall. 1985. Halimeda bioherms – low Fine, M. & D. Tchernov. 2007a. Scleractinian coral
energy reefs, northern Great Barrier Reef. Proceedings species survive and recover from decalcification.
of the Fifth International Coral Reef Congress 1: 1–7. Science 315: 1811.
Guinotte & Fabry: Ocean Acidification and Marine Ecosystems 339

Fine, M. & D. Tchernov. 2007b. Response to “Ocean Hossain, M.M.M. & S. Ohde. 2006. Calcification of cul-
acidification and scleractinian corals”. Science 317: tured Porites and Fungia under different aragonite
1032–1033. saturation states of seawater. Proc. 10th Int.Coral
Fossa, J.H., P.B. Mortensen, & D.M. Furevik. 2002. The Reef Sym. Jpn. Coral Reef Soc. 597–606.
deep-water coral Lophelia pertusa in Norwegian wa- Houghton, J.T. et al. 2001. Climate Change 2001: The Scientific
ters: distribution and fishery impacts. Hydrobiologia Basis. Cambridge University Press. Cambridge, UK.
13: 1–12. Huesemann, M.H., A.D. Skillman, & E.A. Crecelius.
Freiwald, A. 2002. Reef-forming cold-water corals. In 2002. The inhibition of marine nitrification by ocean
Ocean Margin Systems. G. Wefer, D. Billett, D.B.B. disposal of carbon dioxide. Mar. Pollut. Bull. 44: 142–
Hebbeln Jorgensen, et al., Eds.: 365–385. Springer. 148.
Heidelberg. Husebo, A. et al. 2002. Distribution and abundance of fish
Freiwald, A. et al. 2004. Coldwater Coral Reefs. UNEP- in deep-sea coral habitats. Hydrobiologia 471: 91–99.
WCMC, Cambridge, UK. Hutchins, D.A. et al. 2007. CO 2 control of Trichodesmium
Freiwald, A. & J.M. Roberts. 2005. Cold-Water Corals and N2 fixation, photosynthesis, growth rates, and el-
Ecosystems. Springer. Heidelberg. emental ratios: implications for past, present, and
Gattuso, J.-P. et al. 1998. Effect of calcium carbonate satu- future ocean biogeochemistry. Limnol. Oceanogr. 52:
ration of seawater on coral calcification. Global Planet. 1293–1304.
Change 18: 37–46. Invers, O. et al. 2001. Inorganic carbon sources for sea-
Gazeau, F. et al. 2007. Impact of elevated CO 2 on grass photosynthesis: an experimental evaluation of
shellfish calcification. Geophys. Res. Lett. L07603, bicarbonate use in species inhabiting temperate wa-
doi:10.1029/2006GL028554. ters. J. Exp. Mar. Biol. Ecol. 265: 203–217.
Giordano, M., J. Beardall & J.A. Raven. 2005. CO 2 con- Ishimatsu, A. et al. 2005. Physiological effects on fishes in
centrating mechanisms in algae: mechanisms, en- a high-CO 2 world. J. Geophys. Res. 110: np.
vironmental modulation, and evolution. Annu. Rev. Ishimatsu, A. et al. 2004. Effects of CO 2 on marine fish:
Plant Biol. 56: 99–131. larvae and adults. J. Oceanogr. 60: 731–741.
Green, M.A. et al. 2004. Dissolution mortality of juvenile Ishimatsu, A. & J. Kita. 1999. Effects of environmental
bivalves in coastal marine deposits. Limnol. Oceanogr. hypercapnia on fish, Jpn. J. Ichthyol. 46: 1–13.
49: 727–734. Kikkawa, T., A. Ishimatsu & J. Kita. 2003. Acute CO 2
Guinotte, J.M., R.W. Buddemeier, & J.A. Kleypas. 2003. tolerance during the early developmental stages of
Future coral reef habitat marginality: temporal and four marine teleosts. Environ. Toxicol. 18: 375–382.
spatial effects of climate change in the Pacific basin. Kikkawa, T., J. Kita, & A. Ishimatsu. 2004. Comparison
Coral Reefs 22: 551–58. of the lethal effect of CO 2 and acidification on red
Guinotte, J.M. et al. 2006. Will human induced changes sea bream (Pagrus major) during the early develop-
in seawater chemistry alter the distribution of deep- mental stages. Mar. Pollut. Bull. 48: 108–110.
sea scleractinian corals? Front. Ecol. Environ. 4: 141– Kleypas, J.A. et al. 1999a. Geochemical consequences of
146. increased atmospheric carbon dioxide on coral reefs.
Harrington, L. et al. 2005. Synergistic effects of diuron Science 284: 118–120.
and sedimentation on photosynthesis and survival of Kleypas, J.A. et al. 1999b. Environmental limits to coral
crustose coralline algae. Mar. Pollut. Bull. 51: 415– reef development: where do we draw the line? Am
427. Zool 39: 146–159.
Heifetz, J. et al. 2005. Corals of the Aleutian Islands. Fish- Kleypas, J.A. et al. 2006. Impacts of Ocean Acidifica-
eries Oceanogr. 14: 131–138. tion on Coral Reefs and Other Marine Calcifiers:
Hein, M. & K. Sand-Jensen. 1997. CO 2 increases oceanic A Guide for Future Research, report of a workshop
primary production. Nature 388: 526. held 18–20 April 2005, St. Petersburg, FL, sponsored
Heyward, A.J. & A.P. Negri. 1999. Natural inducers of by NSF, NOAA, and the U.S. Geological Survey, 88
coral larval metamorphosis. Coral Reefs 18: 273– pp.
279. Kleypas, J.A. & C. Langdon. 2002. Overview of CO 2 -
Hillis-Colinvaux, L. 1980. Ecology and taxonomy of Hal- induced changes in seawater chemistry. World Coral
imeda: primary producers of coral reefs. Adv. Mar. Biol. Reefs in the New Millennium: Bridging Research
17: 1–327. and Management for Sustainable Development. In
Hoegh-Guldberg, O. et al. 2007. Coral reefs under rapid Proceedings of the 9th International Coral Reef
climate change and ocean acidification. Science 318: Symposium, 2. M.K. Moosa, S. Soemodihardjo, A.
1737–1742. Soegiarto, et al., Eds.: 1085–1089. Ministry of Envi-
Hinga, K.R. 2002. Effects of pH on coastal marine phy- ronment, Indonesian Institute of Sciences, Interna-
toplankton. Mar.Ecol.Prog.Ser. 238: 281–300. tional Society for Reef Studies, Bali, Indonesia.
340 Annals of the New York Academy of Sciences

Koenig, C. et al. 2000. Protection of fish spawning habitat Martin, C.L. & P.D. Tortell. 2006. Bicarbonate trans-
for the conservation of warm- temperate reef-fish port and extracellular carbonic anhydrase activity in
fisheries of shelf-edge reefs of Florida. Bull. Mar. Sci. Bering Sea phytoplankton assemblages: Results from
66: 593–616. isotope disequilibrium experiments. Limnol. Oceanogr.
Kuffner, I.B. et al. 2008. Decreased abundance of crus- 51: 2111–2121.
tose coralline algae due to ocean acidification. Nature Marubini, F., C. Ferrier-Pagés & J.P. Cuif. 2003. Sup-
Geoscience In Press. pression of skeletal growth in scleractinian corals by
Kurihara, H., S. Kato, & A. Ishimatsu. 2007. Effects of decreasing ambient carbonate-ion concentration: a
increased seawater pCO 2 on early development of crossfamily comparison. Proc. Roy. Soc. Lond. B 270:
the oyster Crassostrea gigas. Aquat. Biol. 1: 91–98. 179–184.
Kurihara, H., S. Shimode, & Y. Shirayama. 2004. Sub- Marubini, F., H. Barnett, C. Langdon & M.J. Atkinson.
lethal effects of elevated concentration of CO 2 on 2001. Dependence of calcification on light and car-
planktonic copepods and sea urchins. J. Oceanogr. 60: bonate ion concentration for the hermatypic coral
743–750. Porites compressa. Mar. Ecol.-Prog. Ser. 220: 153–162.
Kurihara, H. & Y. Shirayama. 2004. Effects of increased Marubini, F. & B. Thake. 1999. Bicarbonate addition
atmospheric CO 2 on sea urchin early development. promotes coral growth. Limnol. Oceanogr. 44: 716–
Mar. Ecol. Prog. Ser. 274: 161–169. 720.
Kuwatani, Y. & T. Nishii. 1969. Effects of decreased pH McKim, J.M. 1977. Evaluation of tests with early life
of culture water on the growth of the Japanese pearl stages of fish for predicting long- term toxicity. J.
oyster. Bull. Jap. Soc. Sci. Fish. 35: 342–350. Fish. Res. Board Can. 34: 1148–1154.
Langdon, C. et al. 2000. Effect of calcium carbonate sat- Medina, M.A. et al. 2006. Naked corals: skeleton loss in
uration state on the calcification rate of an experi- Scleractinia. Proc. Natl. Acad. Sci. USA 103: 9096–
mental coral reef. Global Biogeochem. Cy. 14: 639–654. 9100.
Langdon, C. et al. 2003. Effect of elevated CO2 on Meehl, G.A. et al. 2007. Global Climate Projections. In
the community metabolism of an experimental Climate Change 2007: The Physical Science Basis. Contribu-
coral reef. Global Biogeochem. Cy. 17: 1011, doi: tion of Working Group I to the Fourth Assessment Report of the
10.1029/2002GB001941. Intergovernmental Panel on Climate Change. S. Solomon,
Langdon, C. & M.J. Atkinson. 2005. Effect of elevated D. Qin, M. Manning, et al., Eds.: Cambridge Uni-
pCO 2 on photosynthesis and calcification of corals versity Press. Cambridge, UK, and New York, NY.
and interactions with seasonal change in tempera- Mehrbach, C. et al. 1973. Measurement of apparent
ture/irradiance and nutrient enrichment. J. Geophys. dissociation constants of carbonic acid in seawater
Res. 110: np. at atmospheric pressure. Limnol. Oceanogr. 18: 897–
Langer, M.R. et al. 2006. Species-specific responses of cal- 907.
cifying algae to changing seawater carbonate chem- Michaelidis, B.C. et al. 2005. Effects of long-term moder-
istry. Geochem. Geophys. Geosyst. 7: np. ate hypercapnia on acid-base balance and growth
Leclercq, N., J.-P. Gattuso, & J. Jaubert. 2000. CO 2 par- rate in marine mussels Mytilus galloprovincialis,
tial pressure controls the calcification rate of a coral Mar. Ecol. Prog. Ser. 293: 109–118.
community. Global Change Biol. 6: 329–334. Milliman, J.D. & A.W. Droxler. 1996. Neritic and pelagic
Leclercq, N. et al. 2002. Primary production, respiration, carbonate sedimentation in the marine environment:
and calcification of a coral reef mesocosm under Ignorance is not bliss. Geol. Rundsch. 85: 496–504.
increased CO 2 partial pressure. Limnol. Oceanogr. 47: Mortensen, P.B. et al. 2001. Distribution, abundance and
558–564. size of Lophelia pertusa coral reefs in mid-Norway in
Littler, M.M. & D.S. Littler. 1984. Models of tropical reef relation to seabed characteristics. J. Mar. Biol. Assoc.
biogenesis: the contribution of algae. Prog. Phycol. Res. UK. 81: 581–597.
3: 323–364. Mortensen, P.B. 2000. Lophelia pertusa (Scleractinia) in
Lueker, T.J., A.G. Dickson, & C.D. Keeling. 2000. Ocean Norwegian waters; distribution, growth, and asso-
pCO 2 calculated from dissolved inorganic carbon, ciated fauna. Ph.D. thesis, University of Bergen,
alkalinity, and equations for K1 and K2: validation Bergen, Norway.
based on laboratory measurements of CO 2 in gas Mucci, A. 1983. The solubility of calcite and aragonite
and seawater at equilibrium. Mar. Chem. 70: 105– in seawater at various salinities, temperatures, and
119. one atmosphere total pressure. Am. J. Sci. 283: 780–
Marshall, A.T. & P.L. Clode. 2002. Effect of increased 799.
calcium concentration in sea water on calcification Mumby, P.J. et al. 2004. Mangroves enhance the biomass
and photosynthesis in the scleractinian coral Galaxea of coral reef fish communities in the Caribbean.
fascicularis. J. Exp. Biol. 205: 2107–2113. Nature 427: 533–536.
Guinotte & Fabry: Ocean Acidification and Marine Ecosystems 341

Ohde, S. & M.M.M. Hossain. 2004. Effect of CaCO 3 Riebesell, U. et al. 2007. Enhanced biological carbon con-
(aragonite) saturation state of seawater on calcifica- sumption in a high CO 2 ocean. Nature 450: 545–548.
tion of Porites coral. Geochem. J. 38: 613–621. Roberts, J.M., J.D. Gage & the ACES party. 2003. As-
Ohde, S. & R. Van Woesik. 1999. Carbon dioxide flux sessing biodiversity associated with cold-water coral
and metabolic processes of a coral reef. Bull. Mar. Sci. reefs: Pleasures and pitfalls. Erlanger Geol. Abh. 4: 73.
65: 559–576. Roberts, J.M., A.J. Wheeler, & A. Freiwald. 2006. Reefs
Orr, J.C. et al. 2005. Anthropogenic ocean acidification of the deep: the biology and geology of cold-water
over the twenty-first century and its impact on calci- coral ecosystems. Science 312: 543–547.
fying organisms. Nature 437: 681–686. Rogers, A.D. 1999. The biology of Lophelia pertusa (Lin-
Palacios, S. & R.C. Zimmerman. 2007. Response of eel- naeus 1758) and other deep- water reef-forming
grass Zostera marina to CO 2 enrichment: possible corals and impacts from human activities. Int. Rev.
impacts of climate change and potential for reme- Hydrobiol. 84: 315–406.
diation of coastal habitats. Mar. Ecol. Prog. Ser. 344: Roos, A. & W.F. Boron. 1981. Intracellular pH. Physiol.
1–13. Rev. 61: 296–434.
Pane, L. et al. 2004. Summer coastal zooplankton biomass Rost, B., U. Riebesell & S. Burkhardt. 2003. Carbon ac-
and copepod community structure near the Italian quisition of bloom-forming marine phytoplankton.
Terra Nova Base (Terra Nova Bay, Ross Sea, Antarc- Limnol. Oceanogr. 48: 55–67.
tica). J. Plank. Res. 26: 1479–1488. Rost, B. & U. Riebesell. 2004. Coccolithophores and
Parrish, J.D. 1989. Fish communities of interacting the biological pump: responses to environmental
shallow-water habitats in tropical oceanic regions. changes. In Coccolithophores—From Molecular Processes
Mar. Ecol. Prog. Ser. 58: 143–160. to Global Impact. H.R. Thierstein & J.R. Young, Eds.:
Petit, J.R. et al. 1999. Climate and atmospheric history 76–99. Springer. Berlin Heidelberg.
of the past 420000 years from the Vostok ice core, Royal Society. 2005. Ocean Acidification Due to Increasing At-
Antarctica. Nature 399: 429–436. mospheric Carbon Dioxide. Policy Document 12/05. The
Pollard, D.A. 1984. A review of ecological studies on sea- Royal Society. London, UK.
grass fish communities, with particularly reference to Sabine, C.L. et al. 2004. The oceanic sink for anthro-
recent studies in Australia. Aquat. Bot. 18: 3–42. pogenic CO 2 . Science 305: 367–371.
Portner, H.O., M. Langenbuch & A. Reipschlager. 2004. Schippers, P., M. Lurling & M. Scheffer. 2004. Increase of
Biological impacts of elevated ocean CO 2 concen- atmospheric CO 2 promotes phytoplankton produc-
trations: lessons from animal physiology and earth tivity. Ecol. Lett. 7: 446–451.
history. J. Oceanogr. 60: 705–718. Schneider, K. & J. Erez. 2006. The effect of carbon-
Purcell, J.E. 2005. Climate effects on formation of jellyfish ate chemistry on calcification and photosynthesis in
and ctenophore blooms: a review. J. Mar Biol. Ass. UK the hermatypic coral Acropora eurystoma. Limnol.
85: 461–476. Oceanogr. 51: 1284–1293.
Purcell, J.E. & M.N. Arai. 2001. Interactions of pelagic Sciandra, A. et al. 2003. Response of coccolithophorid
cnidarians and ctenophores with fishes: a review. Emiliania huxleyi to elevated partial pressure of CO 2
Hydrobiologia 451: 27–44. under nitrogen limitation. Mar. Ecol.-Prog. Ser. 261:
Purcell, J.E., S. Uye & W.-T. Lo. 2007. Anthropogenic 111–122.
causes of jellyfish blooms and their direct conse- Sheridan, P. & C. Hays. 2003. Are mangroves nursery
quences for humans: a review. Mar. Ecol. Prog. Ser. habitat for transient fishes and decapods? Wetlands
350: 153–174. 23: 449–458.
Reed, J.K. 2002. Deep-water Oculina coral reefs of Siegenthaler, U. et al. 2005. Stable carbon cycle-climate
Florida: biology, impacts and management. Hydro- relationship during the late Pleistocene. Science 310:
biologia 471: 43–55. 1313–1317.
Renegar, D.A. & B.M. Riegl. 2005. Effect of nutrient Silverman, J., B. Lazar & J. Erez. 2007. Effect of aragonite
enrichment and elevated CO 2 partial pressure on saturation, temperature, and nutrients on the com-
growth rate of Atlantic scleractinian coral Acropora munity calcification rate of a coral reef. J. Geophys.
cervicornis. Mar. Ecol.-Prog. Ser. 293: 69–76. Res. 112: C05004, doi:10.1029/2006JC003770.
Reynaud, S. et al. 2003. Interacting effects of CO 2 partial Skirrow, G. & M. Whitfield. 1975. The effect of in-
pressure and temperature on photosynthesis and cal- creases in the atmospheric carbon dioxide content
cification in a scleractinian coral. Global Change Biol. on the carbonate ion concentration of surface water
9: 1660–1668. at 25◦ C. Limnol. Oceanogr. 20: 103–108.
Riebesell, U. et al. 2000. Reduced calcification of marine Spero, H.J. et al. 1997. Effect of seawater carbonate con-
plankton in response to increased atmospheric CO 2 . centration on foraminiferal carbon and oxygen iso-
Nature 407: 364–367. topes. Nature 390: 497–500.
342 Annals of the New York Academy of Sciences

Stanley, G.D., Jr. 2006. Photosymbiosis and the evolution Whitfield, M. 1975. Future impact of fossil CO 2 on sea–
of modern coral reefs. Science 312: 857–858. Reply. Nature 254: 274–275.
Stanley, G.D., Jr. 2007. Ocean acidification and sclerac- Yates, K.K. & R.B. Halley. 2006. CO 3 concentration and
tinian corals. Science 317: 1032–1033. pCO 2 thresholds for calcification and dissolution on
Stanley, G.D., Jr. & D.G. Fautin. 2001. The Origin of the Molokai reef flat, Hawaii. Biogeosciences 3: 357–
Modern Corals. Science 291: 1913–1914. 369.
Stone, R.P. 2006. Coral habitat in the Aleutian Islands Zachos, J.C. et al. 2005. Rapid acidification of the ocean
of Alaska: depth distribution, fine-scale species as- during the Paleocene-Eocene Thermal Maximum.
sociations, and fisheries interactions. Coral Reefs 25: Science 308: 1611–1615.
229–238. Zeebe, R.E. & D. Wold-Gladrow. 2001. CO 2 in Seawater:
Tortell, P.D. & F.M.M. Morel. 2002. Sources of inorganic Equilibrium, Kinetics, Isotopes. Elsevier Oceanography
carbon for phytoplankton in the eastern Subtropical Series 65. Amsterdam. pp. 346.
and Equatorial Pacific Ocean. Limnol. Oceanogr. 47: Zimmerman, R.C. et al. 1997. Impacts of CO 2 -
1012–1022. enrichment on productivity and light requirements
Tortell, P.D., J.R. Reinfelder, & F.M.M. Morel. 1997. Ac- of eelgrass. Plant Physiol. 115: 599–607.
tive uptake of bicarbonate by diatoms. Nature 390: Zondervan, I. 2007. The effects of light, macronutri-
243–244. ents, trace metals and CO 2 on the production of
Turley, C.M., J.M. Roberts, & J.M. Guinotte. 2007. calcium carbonate and organic carbon in coccol-
Corals in deep-water: will the unseen hand of ocean ithophores – A review. Deep Sea Res. II 54: 521–
acidification destroy cold-water ecosystems? Coral 537.
Reefs 26: 445–448. Zondervan, I. et al. 2001. Decreasing marine biogenic
Veron, J.E. 2008. A Reef in Time: The Great Barrier Reef calcification: A negative feedback on rising at-
from Beginning to End. Harvard University Press. Cam- mospheric pCO 2 . Global Biogeochem. Cy. 15: 507–
bridge, MA. 516.