Review paper 9 pages
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Guinotte2003.pdf
Ocean Acidification and Its Potential Effects on Marine Ecosystems
John M. Guinottea and Victoria J. Fabryb
aMarine Conservation Biology Institute, Bellevue, Washington, USA bCalifornia 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 CO2 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 CO2
Introduction
The carbonate system (pCO2, pH, alkalin- ity, and calcium carbonate saturation state) of the world oceans is changing rapidly due to an influx of anthropogenic CO2 (Skirrow & Whitfield 1975; Whitfield 1975; Broecker & Takahashi 1977; Broecker et al. 1979; Feely & Chen 1982; Feely et al. 1984; Kleypas et al. 1999a; Caldeira & Wickett 2003; Feely et al. 2004; Orr et al. 2005). Ocean acidification may be defined as the change in ocean chem- istry driven by the oceanic uptake of chemi- cal inputs to the atmosphere, including carbon, nitrogen, and sulfur compounds. Today, the
Address for correspondence: John M. Guinotte, Marine Conserva- 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. [email protected]
overwhelming cause of ocean acidification is anthropogenic atmospheric CO2, although in some coastal regions, nitrogen and sulfur are also important (Doney et al. 2007). For the past 200 years, the rapid increase in anthropogenic atmospheric CO2, which directly leads to de- creasing ocean pH through air–sea gas ex- change, has been and continues to be caused by the burning of fossil fuels, deforestation, in- dustrialization, cement production, and other land-use changes. The current rate at which ocean acidification is occurring will likely have profound biological consequences for ocean ecosystems within the coming decades and centuries.
Presently, atmospheric CO2 concentration is approximately 383 parts per million by volume (ppmv), a level not seen in at least 650,000 years, 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
TABLE 1. Projected changes in surface ocean carbonate chemistry based on IPCC IS92a CO2 emission scenario (Houghton et al. 2001)a
Parameter Symbol Unit Glacial Preindustrial Present 2 × CO2 3 × CO2 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 pCO2 in seawater pCO2 µatm 180 280 380 560 840
(−56) (0) (35.7) (100) (200) Carbonic acid H2CO3 µmol kg−1 7 9 13 18 25
(−29) (0) (44) (100) (178) Bicarbonate ion HCO3 − µmol kg−1 1666 1739 1827 1925 2004
(−4) (0) (5) (11) (15) Carbonate ion CO3 2− 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 pHT 8.32 8.16 8.05 7.91 7.76
aWe assume that PO4 = 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). pHT is based on seawater scale. Percent change from preindustrial values are in parentheses. After Feely et al. (2008).
throughout the 21st century (Petit et al. 1999; Houghton et al. 2001; Augustin et al. 2004; Siegenthaler et al. 2005; Meehl et al. 2007). The rate of current and projected increases in atmo- spheric CO2 is approximately 100× faster than has occurred in at least 650,000 years (Siegen- thaler et al. 2005). In recent decades, only half of anthropogenic CO2 has remained in the atmo- sphere; the other half has been taken up by the terrestrial biosphere (ca. 20%) and the oceans (ca. 30%) (Feely et al. 2004; Sabine et al. 2004). Since the Industrial Revolution, a time span of less than 250 years, the pH of surface oceans has dropped by 0.1 pH units (representing an ap- proximately 30% increase in hydrogen ion con- centration relative to the preindustrial value) and is projected to drop another 0.3–0.4 pH units by the end of this century (Mehrbach et al. 1973; Lueker et al. 2000; Caldeira & Wickett
2003; Caldeira et al. 2007; Feely et al. 2008). [Note: The pH scale is logarithmic, and as a result, each whole unit decrease in pH is equal to a 10-fold increase in acidity.] A pH change of the magnitude projected by the end of this century probably has not occurred for more than 20 million years of Earth’s history (Feely et al. 2004). The rate of this change is cause for serious concern, as many marine organ- isms, particularly those that calcify, may not be able to adapt quickly enough to survive these changes.
A series of chemical reactions is initiated when CO2 is absorbed by seawater. � is the calcium carbonate saturation state:
� = [Ca2+][CO2−3 ]/K∗sp where K∗sp is the stoichiometric solubility
product for CaCO3 and [Ca2+] and [CO 2− 3 ]
322 Annals of the New York Academy of Sciences
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Guinotte & Fabry: Ocean Acidification and Marine Ecosystems 323
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324 Annals of the New York Academy of Sciences
are the in situ calcium and carbonate concen- trations, respectively. The end products of these reactions are an increase in hydrogen ion con- centration (H+), which lowers pH (making wa- ters more acidic), and a reduction in the num- ber of carbonate ions (CO2−3 ) available. This reduction in carbonate ion concentration also leads to a reduction in calcium carbonate sat- uration state (�), which has significant impacts on marine calcifiers. Table 1 lists carbon sys- tem parameters and temperature changes for surface waters based on the Intergovernmental Panel on Climate Change (IPCC) IS92a CO2 emission scenario.
A reduction in the number of carbon- ate ions available will make it more diffi- cult and/or require marine calcifying organ- isms to use more energy to form biogenic calcium carbonate (CaCO3). Many marine organisms form biogenic calcium carbonate including: crustose coralline algae (the pri- mary cementer that makes coral reef formation possible), Halimeda (macroalgae), foraminifera, coccolithophores, tropical reef-building corals, cold-water corals, bryozoans, mollusks, and echinoderms. The majority of marine calci- fiers tested to date are sensitive to changes in carbonate saturation state and have shown declines in calcification rates in laboratory and mesocosm studies (Table 2). These or- ganisms are affected and will continue to be affected by ocean acidification, but less well known are the ecosystem impacts on higher trophic-level organisms that rely on these cal- cifiers for shelter, nutrition, and other core functions.
Decreasing pH is not the only effect on the inorganic carbon system in seawater that re- sults from the ocean’s uptake of anthropogenic CO2. Calcite and aragonite are the major biogenically formed carbonate minerals pro- duced by marine calcifiers, and the stability of both minerals is affected by the amount of CO2 in seawater, which is partially deter- mined by temperature. Colder waters natu- rally hold more CO2 and are more acidic than warmer waters. The depths of the aragonite
and calcite saturation horizons are important to marine calcifiers because the depth of these horizons determines the limit at which pre- cipitation of biogenic calcium carbonate by marine organisms is favored (shallower than the saturation horizon) and at which they will experience dissolution (deeper than the satu- ration horizons) in the absence of protective mechanisms.
The aragonite and calcite saturation hori- zons of the world’s oceans are moving to shallower depths due to the rapid influx of an- thropogenic CO2 to the oceans (Fig. 1). This process has been well documented and mod- eled at the global scale (Skirrow & Whitfield 1975; Broecker & Takahashi 1977; Feely & Chen 1982; Feely et al. 1984, 1988; Kleypas et al. 1999a; Broecker 2003; Caldeira & Wickett 2003; Feely et al. 2004; Caldeira & Wickett 2005; Orr et al. 2005). Future estimates of arag- onite saturation horizon depth indicate that shoaling will occur in the North Pacific, North Atlantic, and Southern Ocean within the cen- tury (Orr et al. 2005). The aragonite and cal- cite saturation horizons in the North Pacific are currently very shallow (Feely et al. 2004) and are moving toward the surface at a rate of 1–2 m per year (R.A. Feely pers. comm. 2007). Many of the areas where shoaling is predicted to occur within the century are highly produc- tive and home to many of the world’s most important and economically lucrative commer- cial fisheries.
It is clear that human-induced changes in atmospheric CO2 concentrations are funda- mentally altering ocean chemistry from the shallowest waters to the darkest depths of the deep sea. The chemistry of the oceans is ap- proaching conditions not seen in many mil- lions of years, and the rate at which this is occurring is unprecedented (Caldeira & Wick- ett 2003). Caldeira and Wickett (2003, p. 365) state “Unabated CO2 emissions over the com- ing centuries may produce changes in ocean pH that are greater than any experienced in the past 300 million years, with the pos- sible exception of those resulting from rare,
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); pCO2 = 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; pCO2 = 513 ppmv. (C) Projected ASH depth for year 2099; pCO2 = 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 and Rampino 1993; Beerling and Berner 2002). Recent evidence suggests ocean acid- ification was a primary driver of past mass extinctions and reef gaps, which are time periods on the order of millions of years that reefs have taken to recover from mass extinctions (Stanley 2006; Veron 2008). Za- chos and colleagues (2005) calculated that if the entire fossil fuel reservoir (ca. 4500 GtC) were combusted, the impacts on deep-sea pH and biota would probably be similar to those in the Paleocene–Eocene Thermal Maximum (PETM), 55 million years ago. The PETM likely caused a mass extinction of benthic foraminifera (Zachos et al. 2005). Projected an- thropogenic carbon inputs will occur within just 300 years, which is thought to be much faster than the CO2 release during the PETM and too rapid for dissolution of calcareous sediments to neutralize anthropogenic CO2. Consequently, the ocean acidification-induced impacts on sur- face ocean pH and biota will probably be more severe than during the PETM (Zachos et al. 2005).
While it is apparent changing seawater chemistry will have serious consequences for many marine calcifiers, the effects of ocean acidification on noncalcifiers and the ecosys- tem responses to these changes will be com- plex and difficult to quantify. Assessing whether ocean acidification is the primary driver of a species’ population decline will be diffi- cult due to the multitude of ongoing phys- ical and chemical changes currently occur- ring in the ocean. Ocean acidification is oc- curring in synergy with significant ongoing environmental changes (e.g., ocean temper- ature increases), and these cumulative im- pacts or interactive effects of multiple stressors may have more significant consequences for biota than any single stressor. Thus, research into the synergistic effects of these changes on marine organisms and the consequent ecosystem responses is critical but still in its infancy.
Calcification and Dissolution Response
Hermatypic Corals (Zooxanthellate)
The calcification response of reef-building corals to decreases in aragonite saturation state has been well documented for a handful of se- lect species. These experiments have been con- ducted in laboratory tanks and mesocosms, but to date have not been conducted in in situ field experiments under “natural” conditions. Evi- dence from species tested to date indicate that the calcification rates of tropical reef-building corals will be reduced by 20–60% at double preindustrial CO2 concentrations (pCO2 ca. 560 ppmv) (Gattuso et al. 1998; Kleypas et al. 1999a; Langdon et al. 2000; Kleypas & Lang- don 2002; Langdon et al. 2003; Reynaud et al. 2003; Langdon & Atkinson 2005; c.f. Royal Society 2005; c.f. Kleypas et al. 2006) (see Table 2). Figure 2 illustrates the projected re- duction in surface-water aragonite saturation state through the year 2069. A reduction in cal- cification of this magnitude could fundamen- tally alter the current structure and function of coral-reef ecosystems, as their growth is depen- dent on their ability to accrete at faster rates than erosional processes can break them down. Reef accretion will become increasingly more critical in the coming decades, as global sea levels rise and available light for photosynthe- sis becomes a limiting factor for corals at the deepest reaches of the photic zone.
A substantial decrease in the number of car- bonate ions available in seawater will have se- rious implications for coral calcification rates and skeletal formation. Weaker coral skele- tons will probably result from a reduction in carbonate ions, enabling erosional processes to occur at much faster rates than have oc- curred in the past, and slower growth rates may also reduce corals’ ability to compete for space and light, though no studies have been conducted to test this hypothesis (reviewed in Kleypas et al. 2006). Biosphere II mesocosm ex- 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; pCO2 = 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; pCO2 = 517 ppmv. (In color in Annals online.)
outpace net reef calcification when carbonate ion concentration decreases to about 150 to 110 µmole kg−1, a range that corresponds to atmospheric CO2 concentrations of 560–840 ppmv (C. Langdon pers. comm. 2007). Hoegh- Guldberg and colleagues (2007) stated that aragonite saturation values will favor erosion when the carbonate ion concentration ap- proaches 200 µmole kg−1 (atmospheric CO2 concentration = 480 ppmv). The effects of a reduction in calcification rates on recruitment, settlement, and juvenile life stages of most ma- rine calcifiers, including the majority of scler- actinian corals, are not well known. However,
Edmunds (2007) documented a decline in the growth rates of juvenile scleractinian corals in the U.S. Virgin Islands and raised the possi- bility that the effects of global climate change (increased seawater temperatures and decreas- ing aragonite saturation state) have already re- duced the growth rate of juvenile corals.
Fine and Tchernov (2007a) reported two species of scleractinian corals were able to sur- vive corrosive water conditions (pH values of 7.3–7.6), which caused their skeletons to dis- solve completely, leaving the coral polyps ex- posed. When water chemistry returned to nor- mal/ambient conditions, the coral polyps were
328 Annals of the New York Academy of Sciences
able to recalcify their skeletons without any ob- vious detrimental effects. These findings shed new light on the hypothesis that corals have a means of alternating between soft bodies and skeletal forms, which are absent from the fos- sil record during reef gaps (Stanley & Fautin 2001; Medina et al. 2006; Stanley 2006; Fine & Tchernov 2007a). Fine and Tchernov’s re- sults offer some hope for the future of corals in a high CO2 world, but caution should be exercised as these manipulative experiments did not include the effects of predation on the “naked” coral polyps. Hard skeletons also pro- vide another core function for coral polyps by protecting them from periodic natural events such as tsunamis and cyclones, which can cause significant damage to coral colonies and reef systems.
There is some discrepancy regarding the rep- resentativeness of the coral species used in the Fine and Tchernov calcification experiments. Stanley (2007) stated the experiments may not be representative of all coral species, par- ticularly zooxanthellate reef-building species, which might have responded quite differently to the experiments because of the complex nature of their photosymbiosis. This assertion was challenged by Fine & Tchernov (2007b) in the statement that the evolution and physi- ology of the studied species are indistinguish- able from tropical reef-building species. Rep- resentativeness aside, both parties agree that ocean acidification poses a significant threat to coral-reef ecosystems and the services they provide.
Calcifying Macroalgae
Coralline Algae
Scleractinian corals are not the only reef- calcifying organisms that are sensitive to de- creasing saturation states. Crustose coralline al- gae (CCA) are a critical player in the ecology of coral-reef systems as they provide the “cement” that helps stabilize reefs, make significant sed- iment contributions to these systems, and are important food sources for sea urchins, par-
rot fish, and several species of mollusks (Littler & Littler 1984; Chisholm 2000; Diaz-Pulido et al . 2007). CCA also provide important hard settlement substrate for coral larvae (Heyward & Negri 1999; Harrington et al. 2005; Diaz- Pulido et al. 2007). Coralline algae produce cal- cium carbonate in the form of high-magnesium calcite, a more soluble form of calcium carbon- ate than either calcite or aragonite, which make these species particularly sensitive to decreasing carbonate saturation states.
Mesocosm experiments exposing CCA to el- evated pCO2 (2 × present day) indicate up to a 40% reduction in growth rates, 78% decrease in recruitment, 92% reduction in total area cov- ered by CCA, and a 52% increase in noncal- cifying algae (Buddemeier 2007; Kuffner et al. 2008). Agegian (1985) also reported a reduc- tion in recruitment when CCA were exposed to elevated pCO2 in aquarium experiments. Bud- demeier (2007) states, “The combined effects of reduced carbonate production and diminished stabilization (cementation) of coasts and shal- low seafloors by encrusting calcifiers are likely to lead to more rapid erosion and ecosystem transitions (macroalgal takeover) than would be expected on the basis of decreases in coral growth alone.” The ecological importance of coralline algae to reef systems and the effects decreasing carbonate saturation state will have on these organisms have been overlooked to a significant degree, and more research is needed to document CCA response to reduced car- bonate saturation states and in turn how these responses will impact reef ecosystems.
Halimeda
Halimeda is a genus of green, calcifying macroalgae that forms extensive beds in cer- tain regions of the world’s oceans. Some of the most well-developed Halimeda beds occur off the northeast coast of Australia, and es- timates of total area covered by Halimeda in the Great Barrier Reef region are upwards of 2000 km2 (reviewed by Diaz-Pulido et al. 2007). Halimeda, along with other calcareous algae (Udotea, Amphiroa, and Galaxaura), are
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important producers of marine sediments and contribute to reef accretion by filling voids in the reef matrix with their sediments (Hillis-Colinvaux 1980; Davies & Marshall 1985; Drew & Abel 1988; Diaz-Pulido et al. 2007). Reefs and Halimeda bioherms have high calcification rates and are responsible for the majority of CaCO3 production and accumu- lation on the continental shelf (Milliman & Droxler 1996; Kleypas et al. 2006).
The three-dimensional structures Halimeda form, which can be 20 m in height, provide im- portant habitat for adult fishes and may serve as nursery grounds for juvenile fishes and inverte- brates (Beck et al. 2003). Calcifying macroalgae produce biogenic calcium carbonate in three forms: high-magnesium calcite, aragonite, and calcite; all of these forms are susceptible to the negative effects of decreasing carbonate satura- tion states (Littler & Littler 1984). Few species of Halimeda have been exposed to high pCO2 in lab experiments, but one species from the Great Barrier Reef, Halimeda tuna, displayed a negative calcification response when exposed to a pH drop of 0.5 units (8 to 7.5) (Borowitzka & Larkum 1986).
Cold Water Corals (Azooxanthellate)
Cold water corals and the ecologically rich bioherms they form are widely dis- tributed throughout the world oceans (see Fig. 1). A great number of these highly pro- ductive ecosystems have been discovered only in the last decade, and it is thought that the area covered by these organisms may surpass the total area of tropical zooxanthellate reef systems (Mortensen et al. 2001; Freiwald et al. 2004; Freiwald & Roberts 2005; Guinotte et al. 2006; Turley et al. 2007). Cold water corals are azooxanthellate, which means they do not con- tain photosynthetic algae, and thus are not lim- ited to the photic zone. The majority of cold water corals are found in depths of 200–1000 m or more, and some solitary colonies have been found at depths of several thousand me- ters (Freiwald 2002; Freiwald et al. 2004). There
are six species of azooxanthellate, bioherm- forming, scleractinian corals (Lophelia pertusa, Madrepora oculata, Goniocorella dumosa, Oculina
varicosa, Enallopsammia profunda, and Solenosmilia variabilis), all of which produce calcium carbon- ate skeletons of aragonite. Cold water corals bioherms have extremely high biodiversity and provide habitat and nursery areas for many deep-sea organisms, including several commer- cially important fish species (Rogers 1999; Fossa et al. 2002; Husebo et al. 2002). Scleractinian cold water corals are not the only azooxanthel- late habitat formers.
The “coral gardens” of the North Pacific are biodiversity hotspots dominated by octocorals (soft corals, stoloniferans, sea fans, gorgonians, and sea pens) and stylasterids, the majority of which produce calcite spicules and holdfasts (Cairns & Macintyre 1992; Guinotte et al. 2006; Stone 2006). Stone (2006) reported that 85% of the economically important fish species ob- served on submersible transects in waters off the Aleutian Islands were associated with corals and other emergent epifauna. The waters off the Aleutian Islands have the highest abun- dance and diversity of cold-water corals found to date in high-latitude ecosystems (Heifetz et al. 2005; Stone 2006), but well-developed scler- actinian bioherms are curiously absent from this region even though scleractinian bioherm- forming species are found in North Pacific wa- ters (Guinotte et al. 2006).
The reason scleractinian bioherms are not present in North Pacific waters could be a function of the shallow depth of the arago- nite saturation horizon and high dissolution rates throughout the region (Guinotte et al. 2006). If this hypothesis is true, then decreas- ing carbonate saturation state will probably impact scleractinian cold-water corals earlier than shallow-water reef builders. Cold-water corals are bathed in cold, deep waters that have naturally high levels of CO2 (global av- erage �arag = 2). The low carbonate saturation state environment in which they live probably contributes to their slow growth/calcification rates, which are an order of magnitude slower
330 Annals of the New York Academy of Sciences
than tropical zooxanthellate corals (global aver- age �arag = 4). Indeed, some deeper cold-water coral bioherms could already be experiencing corrosive conditions with respect to aragonite saturation state (�arag < 1), though no evidence of this has been documented.
Greater than 95% of the present day distribution of bioherm-forming scleractinian species occur in waters that are supersaturated with aragonite (Guinotte et al. 2006). Future aragonite saturation state projections from Orr and co-authors (2005) indicate that 70% of scle- ractinian cold-water coral bioherms could be in undersaturated water with respect to arago- nite by the end of the century (Guinotte et al. 2006; Turley et al. 2007) (see Fig. 1). Labora- tory experiments are currently being conducted to test whether cold water corals scleractinians (Lophelia pertusa) are sensitive to decreasing arag- onite saturation state (Riebesell pers. comm.), but no lab experiments have been conducted to test the sensitivity of cold-water octocorals and stylasterids to decreasing carbonate satu- ration states. Manipulative CO2 experiments to determine cold-water coral sensitivity and calcification response to decreasing carbonate saturation states are a top priority for future research (Guinotte et al. 2006; Kleypas et al. 2006; Roberts et al. 2006; Turley et al. 2007).
Benthic Mollusks, Bryozoans, and Echinoderms
The physiological and ecological impacts of increasing pCO2 on benthic mollusks, bry- ozoans, and echinoderms are not well known, and few manipulative experiments have been carried out to determine sensitivity to ele- vated pCO2 (Kleypas et al. 2006). The nega- tive effects of acidic waters on bivalves have been investigated in a small number of stud- ies (Kuwatani & Nishii 1969; Bamber 1987, 1990; Michaelidis et al. 2005; Berge et al. 2006), and only one investigated the negative calci- fication response to pCO2 levels within the range predicted by the IPCC (Gazeau et al. 2007). Gazeau and colleagues (2007) found
that calcification rates of the mussel (Mytilus edulis) and Pacific oyster (Crassostrea gigas) can be expected to decline linearly with increas- ing pCO2, 25% and 10% respectively, by the end of the century (ca. 740 ppmv, IPCC IS92a scenario). Both species are important coastal ecosystem engineers and represent a signif- icant portion of global aquaculture produc- tion (Gazeau et al. 2007). Bivalves that settle in coastal estuarine areas may be particularly vulnerable to anthropogenic ocean acidifica- tion. These organisms naturally experience ex- tremely high mortality rates (>98%) in their transition from larvae to benthic juveniles (re- viewed by Green et al. 2004), and any increase in juvenile mortality due to ocean acidification could have serious effects on estuarine bivalve populations.
Kurihara and colleagues (2007) demon- strated that increased pCO2 of seawater pro- jected to occur by the year 2300 (pH 7.4) will severely impact the early development of the oyster Crassostrea gigas and highlighted the im- portance of acidification effects on larval de- velopment stages of marine calcifiers. Because early life stages appear to be more sensitive to environmental disturbance than adults and most benthic calcifiers possess planktonic lar- val stages, fluctuations in larval stages due to high mortality rates may exert a strong influ- ence on the population size of adults (Green et al. 2004). Kurihara and co-authors (2004) investigated the effects of increased pCO2 on the fertilization rate and larval morphology of two species of sea urchin embryos (Hemicentrotus pulcherrimus and Echinometra mathaei) and found the fertilization rate of both species declined with increasing CO2 concentration. In addi- tion, the size of pluteus larvae decreased with increasing CO2 concentration and malformed skeletogenesis was observed in larval stages of both species. Kurihara and Shirayama (2004) concluded that both decreasing pH and altered carbonate chemistry affect early development and life history of many marine organisms, which will result in serious consequences for marine ecosystems.
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Experiments focusing on the direct effects of increasing ocean acidification on marine calcifiers have been the dominant activity to date, but numerous and ecologically significant indirect effects are probable. Bibby and col- leagues (2007) documented interesting behav- ioral, metabolic, and morphological responses of the intertidal gastropod Littorina littorea to acidified seawater (pH = 6.6). This marine snail produced thicker shells when exposed to preda- tion (crab) cues in control experiments, but this defensive response was disrupted when pH was decreased. The snails also displayed reduced metabolic rates and an increase in avoidance behavior, both of which could have significant ecosystem implications via organism interac- tions, energy requirements, and predator–prey relationships. This study investigated only one species of mollusk, but other marine organisms will probably have indirect responses to ocean acidification (Bibby et al. 2007).
Coccolithophores, Foraminifera, and Pteropods
The major planktonic producers of CaCO3 are coccolithophores (single-celled algae), foraminifera (protists), and euthecosomatous pteropods (planktonic snails). Coccol- ithophores and foraminifera secrete CaCO3 in the form of calcite, whereas pteropods secrete shells made of aragonite, which is about 50% more soluble in seawater than calcite (Mucci 1983). These planktonic groups differ with respect to their size, trophic level, generation time, and other ecological attributes. High quality, quantitative data on the latitudinal and vertical distributions and abundances of these calcareous taxa are lacking, and estimates of their contributions to global calcification rates are poorly constrained.
The calcification response of coccol- ithophores, foraminifera, and pteropods to ocean acidification has been investigated to date in very few species. Most studies have in- volved bloom-forming coccolithophores, and these species (Emiliania huxleyi and Geophyro-
capsa oceanica) show decreased calcification rates ranging from 25 to 66% when pCO2 is increased to 560–840 ppmv, respectively (TABLE 2) in lab and mesocosm experiments. In lab experiments with the coccolithophore Coc- colithus pelagicus, however, Langer et al. (2006) found that calcification did not change with in- creased CO2. Moreover, there is evidence sug- gesting that at least one coccolithophore species may have the capacity to adapt to changing pCO2 over long periods. Experimental manip- ulations show that Calcidiscus leptoporus exhibits highest calcification rates at present-day CO2 levels, with malformed coccoliths and cocco- spheres at both lower and higher pCO2 (Langer et al. 2006). Because no malformed coccol- iths were observed in sediments from the Last Glacial Maximum (when pCO2 levels were about 200 ppmv), the authors concluded that C. leptoporus has adapted to present-day CO2 levels.
In lab experiments with two species of plank- tonic foraminifera, shell mass decreased as the carbonate ion concentration of seawater de- creased (Spero et al. 1997; Bijma et al. 1999, 2002). When grown in lab experiments in seawater chemistry equivalent to pCO2 val- ues of 560 and 740 ppmv, shell mass of the foraminifera Orbulina universa and Globigerinoides sacculifer declined by 4–8% and 6–14%, respec- tively, compared to the shell mass secreted at the preindustrial pCO2 value.
Data for a single species of shelled pteropods suggest that net shell dissolution occurs in live pteropods when the aragonite saturation is forced to <1.0 (Orr et al. 2005; Fabry et al. 2008). When live pteropods (Clio pyramidata) were collected in the subarctic Pacific and ex- posed to a level of aragonite undersaturation similar to that projected for Southern Ocean surface waters by the year 2100 under the IS92a emissions scenario, shell dissolution occurred within 48 hours, even though animals were ac- tively swimming.
The response of planktonic calcifying or- ganisms to elevated pCO2 may not be uni- form among species or over time. To date,
332 Annals of the New York Academy of Sciences
published research indicates that most cal- careous plankton show reduced calcification in response to decreased carbonate ion con- centrations; however, the limited number of species investigated precludes identification of widespread or general trends. All studies thus far on the impacts of ocean acidification on calcareous plankton have been short-term experiments, ranging from hours to weeks. Nothing is known about the long-term impacts of elevated pCO2 on the reproduction, growth, and survivorship of planktonic calcifying or- ganisms or their ability to adapt to changing seawater chemistry. Chronic exposure to in- creased pCO2 may have complex effects on the growth and reproductive success of calcareous plankton or may induce adaptations that are absent in short-term experiments. No studies have investigated the possibility of differential impacts with life stage or age of the organism. Additional experimental evidence from plank- tonic calcifiers is urgently needed if we are to develop a predictive understanding of the impacts of ocean acidification on planktonic communities.
Physiological Reponses
Fishes
Elevated CO2 partial pressures (hyper- capnia) will affect the physiology of water- breathing animals by inducing acidosis in the tissues and body fluids of marine organisms, including fishes (Roos & Boron 1981; Portner et al. 2004). pH, bicarbonate, and CO2 lev- els within the organism are altered with long- term effects on metabolic functions, growth, and reproduction, all of which could be harm- ful at population and species levels (Portner et al. 2004). Short-term effects of elevated CO2 on fishes include alteration of the acid–base status, respiration, blood circulation, and ner- vous system functions, while long-term effects include reduced growth rate and reproduc- tion (Ishimatsu & Kita 1999; Ishimatsu et al.
2004, 2005). Most experiments undertaken to date involved altering pH to levels consistent with conditions that would be present if CO2 were to be directly injected to the seafloor (pH ca. 5.8–6.2). These experiments have shown adverse negative effects of acidified sea- water on fish throughout their entire life cycle (eggs, larvae, juveniles, and adults) (Kikkawa et al. 2003, 2004; Ishimatsu et al. 2004; Portner et al. 2004).
Fish in early developmental stages are more sensitive to environmental change than adults and a limited number of studies have shown this to be true when fish eggs, larvae, and juve- niles were exposed to elevated CO2 (McKim 1977; Kikkawa et al. 2003, 2004; Ishimatsu et al. 2004). Ishimatsu and co-authors (2004) state, “Even if the severity of environmental hypercapnia due to CO2 sequestration is made tolerable to adults, a gradual reduction in pop- ulation size and changes in marine ecosystem structures are unavoidable consequences when young individuals cannot survive” (p. 732). The long-term effects and adaptation potential of fishes experiencing future pCO2 levels consis- tent with IPCC scenarios are not known.
Photosynthetic Organisms
Phytoplankton and Cyanobacteria
Most species of marine phytoplankton have carbon-concentrating mechanisms that accu- mulate inorganic carbon either as CO2 or HCO−3 or both (Giordano et al. 2005). Owing in large part to their carbon-acquisition mech- anisms and efficiencies, most marine phyto- plankton tested to date in single-species lab ex- periments or natural community-perturbation experiments show either no change or small increases (generally ≤ 10%) in photosynthetic rates when grown under high pCO2 condi- tions equivalent to ca. 760 micro atmosphere (µatm) (Tortell et al. 1997; Hein & Sand-Jensen 1997; Burkhardt et al. 2001; Tortell and Morel 2002; Rost et al. 2003; Beardall & Raven 2004;
Guinotte & Fabry: Ocean Acidification and Marine Ecosystems 333
Schippers et al. 2004; Giordano et al. 2005; Martin & Tortell 2006). Unlike other major phytoplankton groups investigated thus far, the coccolithophorid Emiliania huxleyi has low affin- ity for inorganic carbon and could be carbon- limited in today’s ocean (Rost & Riebesell 2004). Whether E. huxleyi will show increased rates of photosynthesis with progressive oceanic uptake of atmospheric CO2, however, may de- pend on nutrient availability and light condi- tions (Zondervan 2007). In a recent mesocosm CO2 manipulation, study, Riebesell and col- leagues (2007) reported that CO2 uptake by a phytoplankton community (primarily diatoms and coccolithophores) in experimental pCO2 treatments of 700 and 1050 µatm was 27% and 39% higher, respectively, relative to the pCO2 treatment of 350 µatm.
Ocean acidification will be accompanied by climate warming in large expanses of the oceans. Higher sea-surface temperatures in- crease thermal stratification of the upper ocean, thereby reducing the vertical mixing of nutri- ents to surface waters, and have been linked to observed decreases in phytoplankton biomass and productivity, particularly at low and mid- latitudes (Behrenfeld et al. 2006). In warm, nutrient-poor tropical and subtropical regions, however, continued ocean absorption of an- thropogenic CO2 may enhance fixation of atmospheric nitrogen and could lead to in- creased total primary productivity. Nitrogen- fixing cyanobacteria in the genus Trichodesmium, which support a large portion of primary pro- ductivity in such low-nutrient areas of the world’s oceans, show increased rates of nitro- gen and carbon fixation under elevated pCO2 (Hutchins et al. 2007; Barcelos e Ramos et al. 2007). At CO2 levels of 750 ppmv, Trichodesmium increased N2 fixation rates by 35–100% and CO2 fixation rates by 15–128%, relative to present-day CO2 conditions (Hutchins et al. 2007).
In a review of coastal marine phytoplankton, Hinga (2002) found that while some species grow well at a wide range of pH, others have growth rates that vary greatly over a 0.5 to
1.0 pH unit change. He concluded that small changes in ambient seawater pH could affect species growth rates, abundances, and succes- sion in coastal phytoplankton communities. Eu- trophication and ocean acidification may act in concert to amplify the pH range found in coastal habitats, which in turn could lead to increased frequency of blooms of those species with tolerance to extreme pH (cf. Hinga 2002). In both coastal and open ocean environments, ocean acidification could also affect primary productivity through pH-dependent speciation of nutrients and metals (Zeebe & Wolf-Gladrow 2001; Huesemann et al. 2002).
Seagrasses
Seagrasses represent one of the most bio- logically rich and productive marine ecosys- tems in the ocean. They create critical nursery grounds for juvenile fishes and important habi- tat for adult fishes, invertebrates, and mollusks. Several higher order and endangered species rely on seagrasses for a significant portion of their diet (e.g., dugongs, manatees, and green sea turtles). Seagrass ecosystems are a critical component to maintaining the biological diver- sity of the oceans and could be one of the few ecosystems that stand to benefit from increas- ing levels of CO2 in seawater. Seagrasses are capable of dehydrating HCO−3 , but many ap- pear to use CO2 (aq) for at least 50% of their carbon requirements used for photosynthesis (Palacios & Zimmerman 2007). Zimmerman and colleagues (1997) found that short-term (ca. 45 days) CO2 (aq) enrichment increased photosynthetic rates and reduced light require- ments for eelgrass (Zostera marina L) shoots in laboratory experiments.
Longer-term (1 year) experiments expos- ing Zostera marina L to CO2 (aq) concentra- tions of 36–1123 µM (pH 7.75–6.2) conducted by Palacios and Zimmerman (2007) resulted in higher reproductive output, an increase in below-ground biomass, and vegetative prolifer- ation of new shoots when light was in abundant supply. These findings suggest that as the CO2
334 Annals of the New York Academy of Sciences
content of the surface ocean rises, so too will the productivity of seagrass meadows, which in turn may positively influence invertebrate and fish populations. This increase in produc- tivity will probably be true for other seagrass species as most appear to be photosynthetically limited by the present-day availability of CO2 (Durako 1993; Invers et al. 2001; Palacios and Zimmerman 2007). Palacios and Zimmerman (2007) noted that a significant indirect effect of increased eelgrass density could be an in- crease in sediment retention, which could lead to increased water clarity and an expansion in the depth distribution of eelgrasses to deeper waters.
Community Impacts
Seagrasses, Coral Reefs, and Fishes
Seagrass meadows and mangroves provide important nursery areas for juvenile fishes, many of which migrate to coral reefs as adults, and enhance fish diversity and abundance on coral reefs adjacent to these ecosystems (Pollard 1984; Parrish 1989; Beck et al. 2001; Sheridan & Hays 2003; Mumby et al. 2004; Dorenbosch et al. 2005). The net effect of increasing CO2 on seagrass ecosystems will probably be increased seagrass biomass and productivity, assuming water quality and clarity (low suspended sed- iment) are sufficient for photosynthesis to oc- cur. Under these conditions, it is probable that an increase in total seagrass area will lead to more favorable habitat and conditions for asso- ciated invertebrate and fish species. However, the net effect of ocean acidification on coral reef ecosystems will probably be negative as many reef-building marine calcifiers will be heavily impacted by the combined effects of increasing sea-surface temperatures (coral bleaching) and decreasing carbonate saturation states of sur- face waters in the coming decades (Guinotte et al. 2003; Buddemeier et al. 2004). The mag- nitude of both ecosystem responses to ocean acidification and other environmental changes working in synergy is difficult to predict as are
the net effects on fish abundance and diver- sity. Predicting the net effects on fish popula- tions is further complicated by the plethora of unknowns surrounding the long-term effects of increasing CO2 on fish physiology, metabolism, and probable range shifts due to ocean warming.
Cold-water Corals and Fishes
The ecology and species relationships of cold-water coral ecosystems are not as ad- vanced as the state of knowledge for shallow- water coral-reef systems, which is due in large part to logistical challenges and the expense of operating vessels and submersibles in the deep sea. However, cold-water coral ecosys- tems are thought to provide important habi- tat, feeding grounds, and recruitment/nursery functions for many deep-water species, includ- ing several commercially important fish species (Mortensen 2000; Fossa et al. 2002; Husebo et al. 2002; Roberts et al. 2006). Many of the species relationships are thought to be facultative, but nonetheless, high fish densities have been re- ported for these structure-forming ecosystems (Husebo et al. 2002; Costello et al. 2005; Stone 2006). Populations of grouper, snapper, and amberjack use the Oculina varicosa reefs off the Florida coast as feeding and spawning ar- eas (Reed 2002), even though their numbers have been dramatically reduced by commer- cial and recreational fishing in recent decades (Koenig et al. 2000). Large aggregations of red- fish (Sebastes spp.), ling (Molva molva), and tusk (Brosme brosme Ascanius) have been documented in the Lophelia pertusa reefs of the North Atlantic (Husebo et al. 2002), and strong fish–coral asso- ciations exist in the cold-water coral ecosystems of the North Pacific (Stone 2006).
Ocean acidification could have significant indirect effects on fishes and other deep- sea organisms that rely on cold-water coral ecosystems for protection and nutritional re- quirements. Roberts and Gage (2003) docu- mented over 1300 species living on the Lophelia
Guinotte & Fabry: Ocean Acidification and Marine Ecosystems 335
pertusa reefs in the NE Atlantic. Future depth projections for the aragonite saturation hori- zons indicate 70% of cold-water scleractinians will be in undersaturated waters by the end of the century, and significant decreases in cal- cification rate could occur well before corals experience undersaturated conditions as arag- onite saturation state decreases progressively over time (Guinotte et al. 2006). Quantifying the indirect impacts of ocean acidification on coral-associated fishes is not possible due to uncertainties surrounding facultative and ob- ligate species relationships, but the net effects are likely to be negative as cold-water coral growth, distribution, and area decrease.
Plankton
If reduced calcification decreases a calci- fying organism’s fitness or survivorship, then some planktonic calcareous species may un- dergo shifts in their distributions as the inor- ganic carbon chemistry of seawater changes. Calcifying species that are CO−2 sensitive could potentially be replaced by noncalcifying species and/or those species not sensitive to elevated pCO2.
By 2100, surface waters of polar and sub- polar regions are projected to become un- dersaturated with respect to aragonite (Orr et al. 2005). Pteropods are important com- ponents of the plankton in high-latitude sys- tems, with densities reaching thousands of in- dividuals m−3 (e.g., Bathmann et al. 1991; Pane et al. 2004). If pteropods require sea- water that is supersaturated with respect to aragonite, then their habitat would become in- creasingly limited, first vertically in the water column and then latitudinally, by the shoal- ing of the aragonite saturation horizon over the next century (Feely et al. 2004; Orr et al. 2005). If high-latitude surface waters do be- come undersaturated with respect to arago- nite, pteropods could eventually be eliminated from such regions, with consequences to food- web dynamics and other ecosystem processes (Fabry et al. 2008). In the subarctic Pacific,
for example, pteropods can be important prey for juvenile pink salmon (Oncorhynchus gobuscha), as well as chum and sockeye salmon, pollock, and other commercially important fishes (Ay- din pers. comm.). Armstrong and co-authors (2005) reported interannual variability in the diet of juvenile pink salmon, with a single species of pteropod (Limacina helicina) compris- ing 15 to 63% by weight of pink salmon di- ets during a 3-year study. Because Pacific pink salmon have a short, 2-year life cycle, prey quality and abundance during the salmon’s ju- venile stage may strongly influence the pink salmon’s adult population size and biomass (Aydin et al. 2005).
Jellyfish blooms (scyphomedusae, hydrome- dusae, and cubomedusae) have increased over the last several decades (Purcell et al. 2007), but it is too soon to determine whether such recent jellyfish increases will persist or the populations will fluctuate with climatic regime shifts, par- ticularly those at decadal scales, as has been observed previously (Purcell 2005). Attrill and colleagues (2007) reported a significant corre- lation of jellyfish frequency in the North Sea from 1971 to 1995 with decreased pH (from 8.3 to 8.1) of surface waters. Although the causative mechanism is not known, Attrill and colleagues (2007) suggest that projected climate change and declining ocean pH will increase the frequency of jellyfish in the North Sea over the next century. Jellyfish are both preda- tors and potential competitors of fish and may substantially affect pelagic and coastal ecosys- tems (Purcell & Arai 2001; Purcell 2005). It is important to resolve possible linkages between jellyfish blooms and ocean acidification and de- termine whether continued changes in the sea- water inorganic carbon system will exacerbate problematic increases in jellyfish that have been associated with climate change, overfishing, eu- trophication, and other factors (Purcell et al. 2007).
Planktonic ecosystems are complex nonlin- ear systems, and the consequences of ocean acidification on such ecosystems are largely un- known. Substantial changes to species diversity
336 Annals of the New York Academy of Sciences
and abundances, food-web dynamics, and other fundamental ecological processes could occur; however, the interactions and feedbacks among the effects of chronic, progressively in- creasing ocean acidification and other environ- mental variables are difficult to predict. Ecosys- tem responses will also depend on the ability of biota to adapt to seawater chemistry changes that are occurring at rates they have not en- countered in their recent evolutionary history (Siegenthaler et al. 2005). Future progress will likely require integrated approaches involving manipulative experiments, field observations, and models, particularly at regional scales.
Summary and Conclusions
The scientific knowledge base surround- ing the biological effects of ocean acidifica- tion is in its infancy and the long-term con- sequences of changing seawater chemistry on marine ecosystems can only be theorized. Most is known about the calcification response for shallow-water scleractinian corals. Some data sets allow the identification of “tipping points” or “thresholds” of seawater carbonate chem- istry when ocean acidification will cause net calcification rates to be less than net dissolu- tion rates in coral reef systems (Yates & Halley 2006; Hoegh-Guldberg et al. 2007). In contrast, the potential effects ocean acidification may have for the vast majority of marine species are not known. Research into the synergistic effects of ocean acidification and other human- induced environmental changes (e.g., increas- ing sea temperatures) on marine food webs and the potential transformative effects these changes could have on marine ecosystems is urgently needed. It is important to have a firm understanding of the degree to which ocean acidification influences critical physiological processes such as respiration, photosynthesis, and nutrient dynamics, as these processes are important drivers of calcification, ecosystem structure, biodiversity, and ultimately ecosys- tem health.
Future ocean acidification research needs in- clude increased resources and efforts devoted to lab, mesocosm, and in situ experiments, all of which will aid in determining the biological responses of marine taxa to increased pCO2. Mesocosm and in situ experiments may simu- late and/or provide more natural conditions than single-species lab experiments, but they have thus far used abrupt changes in seawater chemistry which do not allow for potential ac- climation or adaptation by marine organisms. There is an additional need for experiments on taxa with no commercial value but which provide critical habitat and occupy impor- tant trophic levels within marine food webs. Direct CO2 experiments on commercially im- portant species are clearly necessary, but non- commercial species play crucial roles in marine ecosystems and the life history of most com- mercial species. The effects of ocean acid- ification on less charismatic species and/or species with no economic value should not be overlooked. The biological response of ma- rine organisms (both commercial and noncom- mercial) to ocean acidification will be key to making informed policy decisions that con- form to sound ecosystem-based management principles.
There is a critical need for well-developed spatial and temporal models that give accu- rate present day and future estimates of arago- nite and calcite saturation states in the coastal zones. The shallow continental shelves are some of the most biologically productive ar- eas in the sea and are home to the majority of the world’s fisheries, but accurate carbonate saturation state data do not currently exist for most coastal regions. Ocean acidification in- formation should also be integrated into exist- ing ecosystem models, which attempt to predict the effects of environmental changes on ma- rine populations and ecosystem structure (e.g., Ecopath and Ecosim). Development of these tools is essential to making credible predictions of future ocean acidification effects on marine ecosystems and will aid in guiding management decisions.
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The overwhelming volume of scientific evi- dence collated by the IPCC documenting the dangers of human-induced climate change, of which ocean acidification is only one, should end the lingering CO2 emissions reduction de- bate. The global CO2 experiment which has been under way since the Industrial Revolution and the potentially dire consequences this uncontrolled experiment poses for marine or- ganisms and indeed, all life on Earth, leave no doubt that human dependence on fossil fuels must end as soon as possible. International col- laboration, political will, and large-scale invest- ment in clean energy technologies are essen- tial to avoiding the most damaging effects of human-induced climate change.
Acknowledgments
This work was supported in part by MCBI grants from the Edwards Mother Earth Foun- dation, Marisla Foundation, Moore Family Foundation, and Mark and Sharon Bloome. Support for VJF was provided in part by National Science Foundation grants OCE- 0551726 and ANT-0538710. We would like to thank RW Buddemeier, RA Feely, and an anonymous reviewer for constructive inputs on an early draft.
Conflict of Interest
The authors declare no conflicts of interest.
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