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Ocean Acidification The Other CO2 Problem

Ocean Acidi?cation:

The Other CO 2Problem

Scott C.Doney,1Victoria J.Fabry,2Richard A.Feely,3and Joan A.Kleypas 4

Marine Chemistry and Geochemistry,Woods Hole Oceanographic Institution,Woods Hole,Massachusetts 02543;email:sdoney@https://www.wendangku.net/doc/723199691.html,

Department of Biological Sciences,California State University,San Marcos,California 92096;email:fabry@https://www.wendangku.net/doc/723199691.html,

Paci?c Marine Environmental Laboratory,National Oceanic and Atmospheric Administration,Seattle,Washington 98115;email:Richard.A.Feely@https://www.wendangku.net/doc/723199691.html,

Institute for the Study of Society and Environment,National Center for Atmospheric Research,Boulder,Colorado 80307;email:kleypas@https://www.wendangku.net/doc/723199691.html,

Annu.Rev.Mar.Sci.2009.1:169–92

First published online as a Review in Advance on August 29,2008

The Annual Review of Marine Science is online at https://www.wendangku.net/doc/723199691.html,

This article’s doi:

10.1146/annurev.marine.010908.163834Copyright c

1941-1405/09/0115-0169$20.00

Key Words

biogeochemistry,calci?cation,carbon dioxide,climate change,coral,ecosystem

Abstract

Rising atmospheric carbon dioxide (CO 2),primarily from human fossil fuel combustion,reduces ocean pH and causes wholesale shifts in seawater car-bonate chemistry.The process of ocean acidi?cation is well documented in ?eld data,and the rate will accelerate over this century unless future CO 2emissions are curbed dramatically.Acidi?cation alters seawater chemical spe-ciation and biogeochemical cycles of many elements and compounds.One well-known effect is the lowering of calcium carbonate saturation states,which impacts shell-forming marine organisms from plankton to benthic molluscs,echinoderms,and corals.Many calcifying species exhibit reduced calci?cation and growth rates in laboratory experiments under high-CO 2conditions.Ocean acidi?cation also causes an increase in carbon ?xation rates in some photosynthetic organisms (both calcifying and noncalcifying).The potential for marine organisms to adapt to increasing CO 2and broader implications for ocean ecosystems are not well known;both are high priori-ties for future research.Although ocean pH has varied in the geological past,paleo-events may be only imperfect analogs to current conditions.

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Further

ANNUAL REVIEWS

ppmv:parts per million by volume pH:a measure of ocean acidity and hydrogen ion H +concentration;

pH =?log 10[H +]Ocean acidi?cation:the addition of carbon dioxide in seawater that causes a reduction in ocean pH and shifts in carbonate speciation HOT:Hawaii Ocean Time-Series

pCO 2:carbon dioxide partial pressure Dissolved inorganic carbon (DIC):sum of aqueous CO 2gas,carbonic acid,bicarbonate,and carbonate ions Saturation state:thermodynamic

condition of seawater that describes the degree of

supersaturation or undersaturation with respect to the

particular phase of the CaCO 3mineral Geochemical Sections

(GEOSECS):

a global-scale 1970s chemical

oceanography survey Calcite:a mineral form of calcium carbonate found in many marine plankton and invertebrates that is less soluble than high-magnesium

calcite,which is found in some marine taxa such as echinoderms and coralline algae

INTRODUCTION

Over the past 250years,atmospheric carbon dioxide (CO 2)levels increased by nearly 40%,from preindustrial levels of approximately 280ppmv (parts per million volume)to nearly 384ppmv in 2007(Solomon et al.2007).This rate of increase,driven by human fossil fuel combustion and deforestation,is at least an order of magnitude faster than has occurred for millions of years (Doney &Schimel 2007),and the current concentration is higher than experienced on Earth for at least

the past 800,000years (L ¨uthi et al.2008).Rising atmospheric CO 2is tempered by oceanic uptake,

which accounts for nearly a third of anthropogenic carbon added to the atmosphere (Sabine &Feely 2007,Sabine et al.2004),and without which atmospheric CO 2would be approximately 450ppmv today,a level of CO 2that would have led to even greater climate change than witnessed today.Ocean CO 2uptake,however,is not benign;it causes pH reductions and alterations in fundamental chemical balances that together are commonly referred to as ocean acidi?cation.Because climate change and ocean acidi?cation are both caused by increasing atmospheric CO 2,acidi?cation is commonly referred to as the “other CO 2problem”(Henderson 2006,T urley 2005).Ocean acidi?cation is a predictable consequence of rising atmospheric CO 2and does not suffer from uncertainties associated with climate change forecasts.Absorption of anthropogenic CO 2,reduced pH,and lower calcium carbonate (CaCO 3)saturation in surface waters,where the bulk of oceanic production occurs,are well veri?ed from models,hydrographic surveys,and time series data (Caldeira &Wickett 2003,2005;Feely et al.2004,2008;Orr et al.2005;Solomon et al.2007).At the Hawaii Ocean Time-Series (HOT)station ALOHA the growth rates of surface water pCO 2and atmospheric CO 2agree well (T akahashi et al.2006)(Figure 1),indicating uptake of anthropogenic CO 2as the major cause for long-term increases in dissolved inorganic carbon (DIC)and decreases in CaCO 3saturation state.Correspondingly,since the 1980s average pH measurements at HOT ,the Bermuda Atlantic Time-Series Study,and European Station for Time-Series in the Ocean in the eastern Atlantic have decreased approximately 0.02units per decade (Solomon et al.2007).Since preindustrial times,the average ocean surface water pH has fallen by approximately 0.1units,from approximately 8.21to 8.10(Royal Society 2005),and is expected to decrease a further 0.3–0.4pH units (Orr et al.2005)if atmospheric CO 2concentrations reach 800ppmv [the projected end-of-century concentration according to the Intergovernmental Panel on Climate Change (IPCC)business-as-usual emission scenario].

Fossil fuel combustion and agriculture also produce increased atmospheric inputs of dissocia-tion products of strong acids (HNO 3and H 2SO 4)and bases (NH 3)to the coastal and open ocean.These inputs are particularly important close to major source regions,primarily in the north-ern hemisphere,and cause decreases in surface seawater alkalinity,pH,and DIC (Doney et al.2007).On a global scale,these anthropogenic inputs (0.8Tmol/yr reactive sulfur and 2.7Tmol/yr reactive nitrogen)contribute only a small fraction of the acidi?cation caused by anthropogenic CO 2,but they are more concentrated in coastal waters where the ecosystem responses to ocean acidi?cation could be more serious for humankind.

Seawater carbon dioxide measurements have been conducted since the beginning of the nine-teenth century (Krogh 1904)but were sparse until the middle of the twentieth century (Keeling et al.1965,T akahashi 1961)and particularly until the Geochemical Sections (GEOSECS)(1973–1979)(Craig &T urekian 1976,1980)and T ransient T racers in the Ocean (TTO)(1981–1983)(Brewer et al.1985)programs.Even so,the GEOSECS and TTO measurements were signi?cantly less precise than those of today.Although researchers recognized that the concentration of carbon dioxide in the surface ocean was more or less in equilibrium with overlying atmosphere CO 2,they largely dismissed the potential impact on the ocean biota because calcite (the assumed CaCO 3mineralogy of most calcifying organisms)would remain supersaturated in the surface ocean.

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Time series of:(a )atmospheric CO 2at Mauna Loa (in parts per million volume,ppmv)(red ),surface ocean pH (cyan ),and pCO 2(μatm)(tan )at Ocean Station ALOHA in the subtropical North Paci?c Ocean;and (b )aragonite saturation (dark blue )and (c )calcite saturation (gray )at Station ALOHA.Note that the increase in oceanic CO 2over the past 17years is consistent with the atmospheric increase within the statistical limits of the measurements.Mauna Loa data courtesy of Dr.Pieter T ans,National Oceanic and Atmospheric

Administration/Earth System Research Laboratory (https://www.wendangku.net/doc/723199691.html,/gmd/ccgg/trends );Hawaii Ocean Time-Series (HOT)/ALOHA data courtesy of Dr.David Karl,University of Hawaii (https://www.wendangku.net/doc/723199691.html, ).Geochemical Ocean Section Study (GEOSECS)data are from a station near Station ALOHA collected in 1973;GEOSECS data from T akahashi et al.(1980).

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Calci?cation:a

biological process that uses dissolved ions to form calcium

carbonate minerals for shells and skeletal components

Aragonite:

a relatively soluble mineral form of calcium carbonate found in corals,

pteropods and other molluscs,and a variety of other invertebrates and algae

Total alkalinity:a conserved thermodynamic measure of seawater acid-base chemistry that is equal to the charge difference between conservative cations and anions

Since then,multiple studies revealed several issues that elevate ocean acidi?cation as a threat to marine biota:(a )the calci?cation rates of many shell-forming organisms respond to the degree of supersaturation (e.g.,Smith &Buddemeier 1992,Kleypas et al.1999);(b )aragonite,a more soluble CaCO 3mineral equally important in calcifying organisms,may become undersaturated in the surface ocean within the early 21st century (Feely &Chen 1982,Feely et al.1988,Orr et al.2005);and (c )the biological effects of decreasing ocean pH reach far beyond limiting calci?cation.

OCEAN CARBONATE SYSTEM

Seawater carbonate chemistry is governed by a series of chemical reactions:

CO 2(atmos)→←CO 2(aq)+H 2O →←H 2CO 3→←H ++HCO ?3→←2H +

+CO 2?3.

(1)

Air-sea gas exchange equilibrates surface water CO 2to atmospheric levels with a timescale of approximately one year.Once dissolved in seawater,CO 2gas reacts with water to form carbonic acid (H 2CO 3),which can then dissociate by losing hydrogen ions to form bicarbonate (HCO 3?)and carbonate (CO 32?)ions.The seawater reactions are reversible and near equilibrium (Millero et al.2002);for surface seawater with pH of ～8.1,approximately 90%of the inorganic carbon is bicarbonate ion,9%is carbonate ion,and only 1%is dissolved CO 2.Adding CO 2to seawater in-creases aqueous CO 2,bicarbonate,and hydrogen ion concentrations;the latter lowers pH because pH =–log 10[H +].Carbonate ion concentration declines,however,because of the increasing H +concentrations.The projected 0.3–0.4pH drop for the 21st century is equivalent to approximately a 150%increase in H +and 50%decrease in CO 32?concentrations (Orr et al.2005).

Over century and longer timescales,the ocean’s ability to absorb atmospheric CO 2depends on the extent of CaCO 3dissolution in the water column or sediments:

CaCO 3→←CO 2?3+Ca 2+

(2)

The mineral CaCO 3derives from shells and skeletons of marine organisms,including plankton,

corals and coralline algae,and many other invertebrates.In pelagic environments,carbonates fall through the water column and are either dissolved or deposited in shallow or deep-sea sediments (Berelson et al.2007,Feely et al.2004).CaCO 3formation and dissolution rates vary with saturation state ( ),de?ned as the ion product of calcium and carbonate ion concentrations:

=[Ca 2+] CO 2?3

sp .(3)The apparent solubility product K

sp depends on temperature,salinity,pressure,and the particular mineral phase;aragonite is approximately 50%more soluble than calcite (Mucci 1983).Because [Ca 2+]is closely proportional to salinity, is largely determined by variations in [CO 32?],which can be calculated from DIC and total alkalinity data.Shell and skeleton formation generally occurs where >1.0and dissolution occurs where <1.0(unless the shells or skeletons are protected,for example,by organic coatings).

Saturation states are highest in shallow,warm tropical waters and lowest in cold high-latitude regions and at depth,which re?ects the increase in CaCO 3solubility with decreasing temperature and increasing pressure (Feely et al.2004)(Figure 2).The aragonite and calcite saturation horizons ( =1)are shallower in the Indian and Paci?c Oceans than in the Atlantic Ocean because of the longer deep-water circulation pathways and thus accumulation of more DIC from respired CO 2(Broecker 2003).Anthropogenic CO 2penetration into the ocean is concentrated in the upper thermocline (Sabine et al.2004),and over time this has contributed to the shoaling of saturation horizons by 30–200m from the preindustrial period to the present;evidence of aragonite undersaturation in thermocline waters in the North Paci?c and Indian Oceans (Feely et al.2002,

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Vertical distributions of anthropogenic CO 2concentrations in μmol kg ?1and the saturation state =1.0horizons for aragonite (red )and calcite (white )for present (solid line )and preindustrial (dashed line )conditions along north-south transects in the (a )Atlantic,(b )Paci?c,and (c )Indian Oceans as in Feely et al.(2004).Adapted with permission from AAAS.

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Sabine et al.2002);seasonal upwelling of seawater corrosive to aragonite ( arag <1.0)onto the western continental shelf of North America,approximately 40years earlier than predicted by models (Feely et al.2008);and an increase in areal extent of shallow undersaturated regions in the eastern tropical Atlantic (Chung et al.2003,2004).

BIOLOGICAL RESPONSES TO ACIDIFICATION

Early studies investigated responses of calcifying organisms to altered seawater carbonate chem-istry (Agegian 1985,Borowitzka 1981,Fabry 1990,Smith &Roth 1979),but usually for reasons unrelated to anthropogenic CO 2.Several ground-breaking studies,speci?cally designed to test atmospheric CO 2impacts,revealed potentially dramatic responses in corals (Gattuso et al.1998,Langdon et al.2000,Marubini &Atkinson 1999,Marubini &Davies 1996),coral reef commu-nities (Langdon et al.2000,2003;Leclercq et al.2000),and planktonic organisms (Bijma 1991,Riebesell et al.2000).Numerous other studies mostly veri?ed these results but also revealed the complicated nature of calci?cation responses,for example to Mg/Ca ratios (Ries 2005,Ries et al.2006,Stanley et al.2005)or CO 2in combination with changing temperature (Reynaud et al.2003)or nutrients (Langdon &Atkinson 2005,Sciandra et al.2003).

Calcifying organisms exert a variable degree of control over biomineralization,which generally involves passive and active ion movement in and out of a calci?cation compartment isolated from ambient seawater (Weiner &Dove 2003).Reduced calci?cation rates are observed following acidi?cation for a variety of calcareous organisms even when aragonite or calcite >1.0(Royal Society 2005,Kleypas et al.2006,Fabry et al.2008).The degree of sensitivity varies among species,however,and some taxa may show enhanced calci?cation at CO 2levels projected to occur over the 21st century (Iglesias-Rodr ′?guez et al.2008,Ries et al.2008).However,calci?cation-CO 2response studies exist for a limited number of species in many calcifying groups,and we currently lack suf?cient understanding of calci?cation mechanisms to explain species-speci?c differences observed in manipulative experiments.

Thus far,most of the elevated CO 2response studies on marine biota,whether for calci?cation,photosynthesis,or some other physiological measure,have been short-term experiments that range from hours to weeks.Chronic exposure to increased pCO 2may have complex effects on the growth and reproductive success of calcareous plankton and could induce possible adaptations that are not observed in short-term experiments.Nevertheless,such laboratory experiments enable testing of single or multiple environmental variables in highly controlled settings and are critically needed to identify species’preadapted sensitivities to increasing CO 2.

Shallow-Water Tropical Corals and Coral Reefs

Scleractinian (stony)corals evolved in the T riassic period more than 200million years ago (Mya),and their ability to produce large quantities of CaCO 3has undoubtedly contributed to their evolutionary success (Wood 2001).Scleractinian corals are an important group of hypercalci?ers,organisms with the capacity to produce massive quantities of CaCO 3but in which calci?cation rates vary under different environmental conditions (Stanley &Hardie 1998).

A dramatic example is the work by Fine &T chernov (2007)in which two species of corals grown in highly acidi?ed water completely lost their skeletons (Figure 3),then regrew them after being returned to seawater of normal pH.The study highlights three points:(a )coral calci?cation rates can vary greatly in response to changes in pH and aragonite saturation state,(b )the naked,anemone-like coral polyps remained healthy,but (c )the ?tness of organisms overall would change because of the loss of the protective skeleton.These results also support the paleontologically

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2 mm

Figure 3

Photos of scleractinian coral Oculina patagonica after being maintained for 12months in (a )normal seawater (pH =8.2)and (b )acidi?ed seawater (pH =7.4).From Fine &T chernov (2007).Reprinted with permission from AAAS.

sudden appearance of scleractinian corals some 14million years (Ma)after the Permian extinction event;that is,corals may have continued to exist as “naked corals”until ocean chemistry became favorable for skeletal formation (Stanley &Fautin 2001).

Many laboratory studies on a variety of coral species,indeed almost every study published to date (Figure 4),con?rm that coral calci?cation rates decrease in response to decreasing aragonite saturation state.Analyses of cores from massive coral colonies of the Great Barrier Reef show that calci?cation rates declined 21%between 1988and 2003,although this decrease exceeds that expected from lowered saturation state alone and probably re?ects the composite effects of a suite of changing environmental conditions (e.g.,saturation state,temperature,nutrients)(Cooper et al.2008).

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Species studied

Response to increasing CO 2

a d

c b Calci?cation

Photosynthesis 2

Nitrogen Fixation

Reproduction

Major group

Coccolithophores 1

Planktonic Foraminifera

Molluscs Echinoderms 1Tropical corals

Coralline red algae

Coccolithophores 3

Prokaryotes Seagrasses

Cyanobacteria

Molluscs Echinoderms

Physiological response

4243111

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1–––––

bility, light, and

temperature; 3) Under nutrient replete conditions.

225

–––

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–––

141

–41

1––

–––

–

––

Figure 4

Representative examples of impacts of ocean acidi?cation on major groups of marine biota derived from experimental manipulation studies.The response curves on the right indicate four cases:(a)linear negative,(b)linear positive,(c)level,and (d)nonlinear parabolic responses to increasing levels of seawater pCO 2for each of the groups.Note that in some cases strains of the same species exhibited different behavior in different experiments (cf.Fabry et al.2008;Guinotte &Fabry 2008).

Many other benthic calcifying taxa are also both biogeochemically and ecologically important,including calcifying green algae and coralline red algae in particular.The contribution of calcifying green algae in the genus Halimeda to the global net CaCO 3production may rival that of coral reefs (Milliman &Droxler 1996,Rees et al.2007).Coralline red algae are widespread,globally signi?cant,but often overlooked benthic marine calci?ers (Foster 2001).A recent study on a common crustose coralline alga in Hawaii showed that both calci?cation rates and recruitment rates decline at lower carbonate saturation state (Kuffner et al.2008),but relatively few studies have been conducted on either green or red algae.

Field measurements of reef calci?cation at the community scale (Bates 2002,Broecker &T akahashi 1966,Gattuso et al.1995,Kawahata et al.1999,Kayanne et al.2005)consistently show that calci?cation rates are correlated with changes in a variety of components of the carbonate system in seawater (alkalinity,pCO 2,saturation state).A recent study suggests that inorganic precipitation of calcium carbonate cements,an important binding component in coral reefs,is

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correlated with saturation state and that the abundance of such cements may increase reef resistance to erosion (Manzello et al.2008).

Coral reef ecosystems are de?ned by their ability to produce a net surplus of CaCO 3that pro-duces the reef structure (Kleypas et al.2001).Reef structures typically span only 10–30m in depth,but are structurally complex and support high marine biodiversity.During the repeated glacial to interglacial sea level transgressions from 3Mya to the present,reef ecosystems thrived because their rapid accretion rates migrated the coral community upward and maintained the community within the minimum light levels for continued growth.Under increasing ocean acidi?cation,not only will coral community calci?cation decrease,but also dissolution rates will increase (Langdon et al.2000,Yates &Halley 2006),particularly for those reefs that are already near the limit for reef growth (e.g.,higher latitude reefs).Interestingly,even though global warming may allow corals to migrate to higher latitudes (Precht &Aronson 2004),the decrease in reef CaCO 3production may restrict reef development to lower latitudes where aragonite saturation levels can support calcium carbonate accumulation (Guinotte et al.2003,Kleypas et al.2001).

Deep-Water Corals and Carbonate Mounds

Deep-water scleractinian corals thrive in the subphotic waters of continental slopes,usually in depths of 200–1000m.They are slow growing and often long lived,up to 1500years old,and form habitat that supports high biodiversity and ?sheries.The maximum depth of these commu-nities,particularly of the aragonitic scleractinian corals,appears to coincide with the depth of the aragonite saturation horizon (Guinotte et al.2006),which reaches an average depth of >2000m in the North Atlantic,but can be as shallow as 200m in the North Paci?c Ocean (Figure 2).As in the case of their tropical counterparts,deep-water corals can produce large mounds of cal-cium carbonate,albeit much more slowly (Roberts et al.2006).In contrast to the equatorward contraction of tropical coral reefs,it is the depth distribution of deep-water coral communities that will contract;the deepest communities will be the ?rst to experience a shift from saturated to undersaturated conditions (Figure 2).

Other Benthic Invertebrates

Calcareous skeletal hard parts are widespread among benthic invertebrate phyla,yet apart from corals,few studies have investigated the effects of climate-relevant CO 2increases on calci?ca-tion in these fauna.Gazeau and coworkers (2007)reported that calci?cation rates in the mussel Mytilus edulis and the Paci?c oyster Crassostrea gigas decreased by 25%and 10%,respectively,when grown at ～740ppmv CO 2.Similarly,reduced shell growth was observed in the gastropod Strombus luhuanus and two sea urchin species when grown at 560ppmv CO 2over a 6-month period (Shirayama &Thorton 2005).Moreover,mussels,sea urchins (Michaelidis et al.2005,Miles et al.2007),and to a much lesser extent the crab Necora puber (Spicer et al.2007)are sensi-tive to internal acidi?cation of body ?uids and use shell dissolution to compensate.Calci?cation in the arms of a burrowing brittle star increased when organisms were grown in low pH water (Wood et al.2008;Figure 4,case b).However,decreased muscle mass in arms was also observed,which would reduce arm movement and likely decrease respiration and feeding.Thus,the en-hanced calci?cation observed in short-term experiments would probably not be sustainable in the long-term.

The response of early developmental stages of benthic invertebrates to CO 2-induced acidi?-cation of seawater has been investigated in bivalves and sea urchins.Kurihara &Shirayama (2004)reported reduced fertilization success,developmental rates,larval size,and spicule skeletogenesis

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microatmosphere (μatm):a measure of seawater pCO 2;1μatm =10?6atm

with increasing CO 2in the sea urchins Hemicentrotus pulcherrimum and Echinodetra mathei.When gametes of the oyster C.gigas were exposed to 2268μatm pCO 2,no differences in rates of fer-tilization or embryo development were observed,relative to the control group,until 24h after fertilization,when more than 80%of the D-shaped larvae grown in high-CO 2seawater displayed malformed shells or remained unmineralized (Kurihara et al.2007).

Planktonic Calci?cation

The major calcareous plankton groups are calcite-forming coccolithophores and foraminifera and aragonite-forming euthecosomatous pteropods.Most planktonic studies have focused on coc-colithophores,although to date these studies have covered only four of approximately 250to 500living coccolithophore species (Y oung et al.2005)and revealed nonuniform calci?cation re-sponse to high-CO 2/low-pH seawater (Figure 4).Many laboratory and mesocosm studies with the bloom-forming coccolithophore species of Emiliania huxleyi and Gephyrocapsa oceanica reported decreased calci?cation (Figure 4,case a)that ranged from –25%to –66%when pCO 2was in-creased to 560–840μatm (Riebesell et al.2000;Zondervan et al.2001,2002;Sciandra et al.2003;Delille et al.2005;Engel et al.2005).Recently,Iglesias-Rodr ′?guez and colleagues (2008)found a doubling of cell-speci?c calci?ca-tion rates for laboratory E.huxleyi cultures grown at 750μatm versus 300μatm pCO 2(Figure 4,case b).Overall size increased under high-CO 2conditions,as did size and mass of individual calcitic coccoliths that surround the cell surface.However,at the same time,signi?cantly reduced growth rates at elevated pCO 2suggest that this E.huxleyi strain would be more at risk of outcompetition by other phytoplankton species under future high-CO 2conditions.

Similarly,Langer and coworkers (2006)found differing responses to elevated pCO 2for two other coccolithophore species,both important in calcite export to sediments.The coccolithophore Coccolithus pelagicus exhibited no signi?cant change in calci?cation for CO 2varying from 150to 915μatm (Figure 4,case c).Calci?cation rates decreased and coccolith malformations increased for Calcidiscus leptoporus cultures in response to pCO 2levels both above and below present-day values (Figure 4,case d).In contrast,examination of Atlantic Ocean sediments from the Last Glacial Maximum (LGM),when surface water pCO 2was approximately 200μatm,revealed no malformed coccoliths in C.leptoporus ,suggesting that this species was adapted to low CO 2during the LGM and has subsequently adjusted to elevated modern CO 2.Such resiliency is consistent with the ?ndings of Iglesias-Rodr ′?guez and colleagues (2008),who examined a high-resolution sediment core and observed a distinct increase in the average coccolith mass,domi-nated by C.leptoporous and C.pelagicus ,from 1960to 2000that follows the rise in atmospheric CO 2.

In laboratory experiments with two species of symbiont-bearing,planktonic foraminifera,shell mass decreased as carbonate ion concentration decreased (Spero et al.1997;Bijma et al.1999,2002).When grown in seawater chemistry equivalent to 560and 740ppmv CO 2,the shell mass of foraminifers Orbulina universa and Globigerinoides sacculifer declined by 4–8%and 6–14%,re-spectively,compared with preindustrial CO 2controls.

Data from a single species of euthesomatous pteropod (Clio pyramidata )indicate net shell dissolution occurs in live pteropods when the saturation state of seawater with respect to aragonite is forced to <1.0(Orr et al.2005,Fabry et al.2008).Even though the animals were actively swimming,shell dissolution occurs within 48hours when live pteropods,collected in the subarctic Paci?c,are exposed to aragonite undersaturation levels similar to those projected for Southern Ocean surface waters by year 2100.

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Primary Production and Nitrogen Fixation

Carbon-concentrating mechanisms enable most marine phytoplankton species to accumulate in-tracellular inorganic carbon either as CO 2or HCO 3?or both (Giordano et al.2005).Largely be-cause of these mechanisms,most marine phytoplankton tested in single-species laboratory studies and ?eld population experiments show little or no change in photosynthetic rates when grown under high pCO 2conditions equivalent to ～760μatm (T ortell et al.1997,Hein &Sand-Jensen 1997,Burkhardt et al.2001,T ortell &Morell 2002,Rost et al.2003,Beardall &Raven 2004,Giordano et al.2005,Martin &T ortell 2006).In contrast,the widely distributed coccolithophore E.huxleyi has low af?nity for inorganic carbon and could be carbon limited in the modern ocean (Rost &Riebesell 2004).Whether E.huxleyi will show increased rates of photosynthesis with pro-gressive oceanic uptake of atmospheric CO 2may depend on nutrient and trace metal availability,light conditions,and temperature (Zondervan 2007).

In a recent mesocosm CO 2manipulation study with a phytoplankton community dominated by diatoms and coccolithophores,Riebesell and coworkers (2007)reported 27%and 39%higher CO 2uptake in experimental pCO 2treatments of 700and 1050μatm,respectively,relative to the 350μatm pCO 2treatment.Direct extrapolation of such experimental results to large-scale ocean regions may be problematic,however.The global warming that accompanies ocean acidi?cation increases thermal strati?cation of the upper ocean,thereby reducing the upwelling of nutrients,and has been linked to observed decreases in phytoplankton biomass and productivity on a global basis (Behrenfeld et al.2006).

Fu and coworkers (2007)explored in culture the physiological responses of two key marine photosynthetic cyanobacteria to warmer,more CO 2-rich conditions.They observed only minimal changes for Prochlorococcus ,whereas for Synechococcus they measured greatly elevated photosynthesis rates and a 20%increase in cellular C:P and N:P ratios.The CO 2and temperature responses were synergistic;that is,the change in photosynthesis for warm,high-CO 2conditions was much greater than the sum of the responses to either factor individually.

Although seagrasses are able to utilize HCO 3?,most species do so inef?ciently.In all species tested to date,light-saturated photosynthetic rates increase dramatically with increased dissolved CO 2(aq)concentration (Zimmerman et al.1997,Short &Neckles 1999,Invers et al.2001).In experiments with the eelgrass Zostera marina ,Palacios &Zimmerman (2007)reported an increase in biomass and reproductive output under high-CO 2conditions,suggesting potentially higher productivity of seagrasses that form a critical habitat for many ?sh and invertebrate species.The bene?ts from CO 2-enriched seawater,however,may be offset by the negative effects of increased temperature on vegetative growth (Ehlers et al.2008).

Nitrogen-?xing cyanobacteria in the genus Trichodesmium ,which support a large fraction of primary productivity in low nutrient areas of the world’s oceans,show increased rates of carbon and nitrogen ?xation and increased C/N ratios under elevated pCO 2(Hutchins et al.2007,Barcelos e Ramos et al.2007).At CO 2levels of 750ppmv,Trichodesmium CO 2?xation rates increased by 15–128%and N 2?xation rates increased by 35–100%relative to the rates in present day CO 2conditions (Hutchins et al.2007).

ECOLOGICAL AND BIOGEOCHEMICAL IMPACTS Food Webs and Ecosystems

The limited number of studies conducted at climate-relevant CO 2levels hampers predictions of the impacts of ocean acidi?cation on marine ecosystems (Fabry et al.2008).Nevertheless,many CaCO 3-secreting organisms clearly exhibit reduced calci?cation with elevated CO 2and

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decreasing pH and CO 32?.Assuming calci?ed structures provide protection from predators and/or other bene?ts to the organism,these calci?ers will either need to adapt to the changing seawater chemistry,shift their distributions to more carbonate ion–rich regions,or be adversely impacted.In an intriguing ?eld study,Hall-Spencer et al.(2008)quantify dramatic shifts in the nearshore benthic community in the vicinity of natural subsurface volcanic CO 2vents.Consistent with expectations from laboratory studies,the regions near the vents under high-CO 2,low-pH water were marked by the absence of scleractinian corals and reduced abundances in sea urchins,coralline algae,and gastropds.The vent areas were dominated instead by seagrasses with an increased frequency of non-native,invasive species.

One clear threshold that will affect marine organisms is when surface waters become undersat-urated with respect to their shell mineralogy.Surface waters of high latitude regions,for example,are projected to become undersaturated with respect to aragonite as early as 2050(Orr et al.2005),and the progressive shoaling of the aragonite saturation horizon will likely limit aragonitic organ-isms and change food web dynamics.Euthecosomatous pteropods are important components of polar and subpolar regions,where their densities can reach upward of thousands of individuals per cubic meter (Bathmann et al.1991,Pane et al.2004),and they are prey for a variety of zoo-plankton and ?sh predators.In the North Paci?c,pteropods can be important prey of juvenile pink salmon,accounting in some years for >60%by weight of their diet (Armstrong et al.2005).If pteropods cannot adapt to living continuously in seawater that is undersaturated with respect to aragonite,their ranges will contract to shallower depths and lower latitudes.Detection of such acidi?cation-driven population shifts will be dif?cult because of a lack of baseline data on their current distributions and abundances.

More subtle ecological effects are also likely to occur,but are less predictable and will be more dif?cult to detect.For one,the calci?cation thresholds of many organisms do not coincide with the chemical threshold where saturation state =1,but instead can occur at both higher and lower values.Many reef-building corals,for example,appear to cease calci?cation at aragonite saturation as high as 2.0.A slowdown in calci?cation for any organism may (a )reduce its ability to compete with noncalcifying organisms,as observed when crustose coralline algae were exposed to high-CO 2conditions (Kuffner et al.2008);(b )reduce the age at sexual maturity;(c )change its buoyancy;or (d )change light behavior in the water column (T yrrell et al.1999).Given that many taxa exhibit species-speci?c effects (Fabry 2008,Ries et al.2008),each of these changes is likely to affect community dynamics in complicated ways,similar to the projected effects of temperature increases on terrestrial communities.Even small variations in species’responses will become ampli?ed over successive generations and could drive major reorganizations of planktonic and benthic ecosystems.In the North Sea,one study has provided an interesting link between decreasing ocean pH and increasing jelly?sh frequency since 1970(Attrill et al.2007).

However,ocean acidi?cation is not occurring in isolation;it is one of many stressors related to climate change and other factors.The already dif?cult challenge of predicting the ecological effects of ocean acidi?cation is magni?ed by these simultaneous changes,especially because the pace of the changes is unprecedented except for the most abrupt catastrophic events in Earth’s history (e.g.,the bolide impact that caused the Cretaceous-T ertiary extinction).

Oceanic CaCO 3Budget

Despite the increasing evidence that calci?cation in many organisms will decline in the face of in-creased CO 2levels (Figure 4),the impact on the global CaCO 3budget remains poorly constrained.Estimates of carbonate production in the water column have large uncertainties that range from 0.6–1.6±0.3Pg C yr ?1based on satellite-and sediment-trap-derived estimates of carbonate

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Table 1Summary of CaCO 3?ux estimates for the ocean updated from Berelson et al.(2007)Flux estimate

Flux estimate Flux term

mmol CaCO 3m ?2d ?1

Pg C yr ?1

Production in the euphotic zone 0.4–1.00.5–1.6Export from the surface (models)0.3–1.10.4–1.8Dissolution from 200to 1500m Atlantic 0.30.1Indian 1.10.3Paci?c 0.80.6T otal

1.0Export to sediment traps below 2000m ?0.24±0.030.4±0.05Dissolution on sea ?oor below 2000m 0.24±0.17

0.4±0.3Atlantic and Paci?c only Burial in sediments

0.08

0.1

Data from Honjo et al.(2008).

Anthropogenic carbon dioxide:

excess carbon dioxide added to ocean and atmosphere from human fossil fuel combustion and deforestation

production (Balch et al.2007,Milliman 1993)(Table 1)to 0.4–1.8Pg C yr ?1based on models of carbonate export (Moore et al.2004,Murnane et al.1999).Production rates estimated from seasonal surface-ocean alkalinity changes yield a minimum estimate of 1.4±0.3Pg C yr ?1(Lee 2001),which is consistent with the higher estimates.On the dissolution side,the estimates range from 0.5–1.0Pg C yr ?1based on sediment trap studies (Honjo et al.2008),alkalinity gradients and water mass ages (Berelson et al.2007,Feely et al.2004,Sarmiento et al.2002),and models (Gehlen et al.2007).Carbonate burial in deep marine sediments is estimated to be 0.1Pg C yr ?1(Table 1).Because ocean acidi?cation is expected to decrease CaCO 3saturation states (Figure 1b and c )and increase dissolution rates,ocean alkalinity and the ocean’s capacity to take up more CO 2from the atmosphere will presumably increase.If all carbonate production were shut down by ocean acidi?cation,the atmospheric CO 2would decline by approximately 10–20ppmv (Gruber et al.2004).In the near-term this may be observed ?rst in coastal regions where coral reef calci?ca-tion rates could decrease by as much as 40%by the end of this century (Andersson et al.2005,2007).However,over the same timeframe,the uptake rate of anthropogenic carbon dioxide from the atmosphere could completely overwhelm these natural buffering mechanisms so the ocean’s ef?ciency for taking up carbon will probably decline with time over the next two centuries.

Carbon and Nutrient Cycling

Ocean acidi?cation also has the potential to alter ocean biogeochemical dynamics for organic carbon and nutrients via several more indirect pathways.Increased carbonate dissolution in the water column could decrease the contribution of CaCO 3to the ballasting of organic carbon to the deep sea (Armstrong et al.2002,Klaas &Archer 2002,Passow 2004),causing more organic carbon to remineralize in shallow waters and decreasing the ocean’s CO 2uptake ef?https://www.wendangku.net/doc/723199691.html,boratory and mesocosm experiments suggest a shift toward organic matter with higher C/N ratios for individual phytoplankton species and plankton communities grown at high CO 2.This could degrade the food quality for heterotrophic zooplankton and microbial consumers.

Changing elemental stoichiometries is one of the few mechanisms by which biology can alter ocean carbon storage (Boyd &Doney 2003),and higher C/N ratios in export material would make the ocean biological pump more ef?cient in exporting carbon to depth.Another such lever is nitrogen ?xation because it decouples the otherwise tight connection between inorganic carbon

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and nitrogen in the water column.Higher nitrogen ?xation rates at elevated CO 2would provide additional new nitrogen in low-nutrient subtropical regions,zones where future primary pro-duction is expected otherwise to decline because of increased vertical strati?cation and reduced vertical nutrient inputs from below (Boyd &Doney 2002).The actual increase in nitrogen ?xation,however,could be limited by phosphorus and iron supplies.

Chemical Speciation in Seawater

A major but underappreciated consequence of ocean acidi?cation will be broad alterations of in-organic and organic seawater chemistry beyond the carbonate system.Analogous to the dramatic changes in the carbonate speciation,i.e.,the measurable decrease in the concentration of carbonate ion and the increase in bicarbonate and aqueous CO 2,many other so-called weak acid species that undergo acid-base reactions in seawater will undergo signi?cant speciation shifts with decreasing pH.Affected chemical species include those major elements such as boron,minor elements includ-ing phosphorus,silicon,and nitrogen,and trace elements such as iron,zinc,vanadium,arsenic,and chromium.For example,plots of chemical species concentration versus pH for phosphate,silicate,?uoride,and ammonia species as a function of pH show large changes with decreasing pH (?gure 1.2.11in Zeebe &Wolf-Gladrow 2001).These changes in speciation are important for understanding and modeling the responses of phytoplankton and other components of the marine ecosystem to changes in pH.

Similarly,many trace element species that are strongly hydrolyzed in seawater (e.g.,aluminum,iron,chromium,bismuth,uranium)and form oxy-anion [MO x -(OH)n ],hydroxyl [M(OH)n ],or carbonate complexes are also strongly in?uenced by variations in both temperature and pH (Byrne et al.1988,Byrne 2002).These changes can directly affect their bioavailability to phytoplankton.For those species complexed with Cl ?ion,pH in?uences are much weaker.However,the details of the metal speciation as a function of pH,as well as the speciation impacts on bioavailability,are not as well known for the trace elements as they are for the major and minor elements.Even less well known is the in?uence of pH on metal organic complexes that are also abundant in the euphotic regions of the oceans (Bruland &Lohan 2004).

In much the same manner,dissolved organic matter that undergoes hydrolysis reactions in seawater (e.g.,organic acids,amino acids,nucleic acids,proteins,humic materials)will also be strongly in?uenced by changing pH.The overall impact of decreasing pH on the structure and function of these biologically important organic compounds is largely unknown.Consequently,more research is needed on how ocean acidi?cation will impact trace metal and organic matter speciation and biogeochemical processes in the high-CO 2oceans of the future.

GEOLOGICAL AND HISTORICAL EVIDENCE

Historical evidence for changes in ocean carbonate chemistry and calci?cation rates has been sought over three basic timescales:the recent past (decades;preindustrial through present);glacial-interglacial cycles (thousands of years);and the Phanerozoic (past 540Ma),with particular em-phasis on the Cenozoic (past 65Ma).Boron isotope measurements,for example,are often used as a proxy for ocean pH (Palmer et al.1998,Pearson &Palmer 2002,Sanyal et al.1996),whereas changes in the CaCO 3response are inferred from organism calci?cation rates or the depth of CaCO 3deposition in the deep ocean.

Several studies have examined the coral calci?cation records from the previous decades to centuries for evidence of a recent decline in calci?cation.Many of these studies found little to no evidence that ocean acidi?cation has caused a measurable decrease in calci?cation rates (Bessat &

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PETM:Paleocene-Eocene thermal maximum

Buigues 2001;Lough &Barnes 1997,2000).Analysis of coral calci?cation records is confounded by the dif?culty of detecting an acidi?cation signal within a naturally highly variable record,and ideally would include multiple cores across multiple locations (Lough 2004).As previously mentioned,one such analysis conducted on a suite of coral cores from widely spaced locations on the Great Barrier Reef showed that calci?cation rates declined by 21%between 1988and 2003,although the cause of the decrease could not be speci?cally ascribed to ocean acidi?cation (Cooper et al.2008).Boron isotopes from coral skeletons have also been used to detect changes in seawater pH on a coral reef,but the recorded pH changes did not correlate well with the calci?cation signal (Pelejero et al.2005);indeed,the use of boron isotopes in corals as a pH proxy is not uniformly accepted (Blamart et al.2007,Honisch et al.2004).

Over glacial-interglacial cycles (thousands of years),atmospheric CO 2concentrations ?uctu-ated between approximately 180and 290ppmv in concert with changes in orbital changes that affect solar forcing at the Earth’s surface.Concurrent cycles in CaCO 3deposition and dissolution occurred on the sea ?oor due to CaCO 3compensation (Broecker &T akahashi 1978).In fact,the term ocean acidi?cation was ?rst used to describe a decrease in carbonate ion concentration in the western equatorial Atlantic at the onset of the last glacial period (Broecker &Clark 2001).Various proxies (e.g.,foraminiferal Zn/Ca and Mg/Ca ratios,boron isotopes,foraminiferal test character-istics)used to estimate changes in both surface and deep-ocean carbonate ion concentration tend to reinforce the CaCO 3compensation hypothesis,but direct evidence for changes in the ocean carbonate system is lacking.

Over longer timescales (Ma),the paleontological record provides evidence for a strong cor-relation between atmospheric CO 2and global temperature (Doney &Schimel 2007),but a less-than-convincing correlation between atmospheric CO 2concentration and estimated ocean pH.Periods of high atmospheric CO 2concentrations are common throughout the geologic record and some periods (e.g.,Permian and Cretaceous)exhibit massive shallow-water CaCO 3deposits,including reef structures.Initially this appears to be a conundrum:If high atmospheric CO 2con-centration produces acidic seas,why were CaCO 3production and preservation so prevalent in these earlier high-CO 2periods?The short answer to this question is that the carbonate saturation states may have been high during those periods despite the high pCO 2levels.Fluid inclusions of seawater preserved in ancient halite deposits indicate that Ca 2+,Mg 2+and SO 42?concentrations have varied by factor of two over the past 600Ma (Mackenzie &Lerman 2006).The long an-swer is complicated and requires an understanding of the timescales over which various processes (e.g.,climate and atmospheric CO 2,continental weathering,volcanism,methane clathrates,sea ?oor spreading)affect the carbon cycle and carbonate system in seawater (Dickens et al.1995,Doney &Schimel 2007,MacKenzie &Morse 1992),as well as other long-term factors that affect calci?cation (e.g.,biological evolution).

The most salient paleo-analog to the current atmospheric CO 2increase is the strong ocean acidi?cation event at the Paleocene-Eocene thermal maximum (PETM)55Mya.The PETM is marked by the sudden and massive carbon input to the ocean/atmosphere system,a shoaling of the deep ocean’s calcite saturation horizon by at least 2km in less than 2000years that did not recover for tens of thousands of years,global warming of at least 5?C in less than 10,000years,and major shifts in marine planktonic communities (Kennett &Stott 1991;Zachos et al.1993,2003,2005).The only major extinctions occurred within the benthic foraminifera,though it is unclear whether ocean acidi?cation was the main factor or whether changes in ocean circulation led to anoxia in bottom waters (Zachos et al.2008).

However,the similarity of the PETM and several comparable,but smaller,Eocene events to modern conditions is incomplete.First,whether the carbon excursion at the PETM was as rapid as the present-day excursion remains unclear.Second,the PETM and smaller events occurred

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within a background of already high CO 2and global temperature.Third,the Mg:Ca ratio,an important factor that affects the carbonate mineralogy of many organisms,was also signi?cantly different from that of today (Stanley &Hardie 2001).Finally,the marine biota during the PETM were also different.Corals and coral reefs had not yet re-established following the Cretaceous-T ertiary extinction (Wood 2001);modern coccolithophores are very different from those of the early T ertiary (Y oung 1994);and modern thecosomatous pteropod families appeared after the PETM,in the Eocene and Miocene (Lalli &Gilmer 1989).

SUMMARY POINTS

1.The surface ocean currently absorbs approximately one-third of the excess carbon dioxide (CO 2)injected into the atmosphere from human fossil fuel use and deforestation,which leads to a reduction in pH and wholesale shifts in seawater carbonate chemistry.

2.The resulting lowering of seawater carbonate ion concentrations and the saturation state for calcium carbonate are well documented in ?eld data,and the rate of change is projected to increase over the 21st century unless predicted future CO 2emissions are curbed dramatically.

3.Acidi?cation will directly impact a wide range of marine organisms that build shells from calcium carbonate,from planktonic coccolithophores and pteropods and other molluscs,to echinoderms,corals,and coralline algae.Many calcifying species exhibit reduced calci-?cation and growth rates in laboratory experiments under high-CO 2conditions,whereas some photosynthetic organisms (both calcifying and noncalcifying)have higher carbon ?xation rates under high CO 2.

4.Our present understanding of potential ocean acidi?cation impacts on marine organisms stems largely from short-term laboratory and mesocosm experiments;consequently,the response of individual organisms,populations,and communities to more realistic gradual changes is largely unknown (Boyd et al.2008).

5.The potential for marine organisms to adapt to increasing CO 2and the broader impli-cations for ocean ecosystems are not well known;an emerging body of evidence suggests that the impact of rising CO 2on marine biota will be more varied than previously thought,with both ecological winners and losers.

6.Ocean acidi?cation likely will affect the biogeochemical dynamics of calcium carbonate,organic carbon,nitrogen,and phosphorus in the ocean as well as the seawater chemical speciation of trace metals,trace elements,and dissolved organic matter.

7.Acidi?cation impacts processes so fundamental to the overall structure and function of marine ecosystems that any signi?cant changes could have far-reaching consequences for the oceans of the future and the millions of people that depend on its food and other resources for their livelihoods.

8.Geo-engineering solutions that attempt to slow global warming without reducing atmo-spheric CO 2concentration,such as injection of stratospheric aerosols (Crutzen 2006),will not reduce ocean acidi?cation.

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FUTURE ISSUES

A fully integrated program of laboratory,mesocosm,?eld monitoring,and modeling ap-proaches is required to provide policymakers with informed management strategies that address how humans might best mitigate or adapt to these long-term changes.This pro-gram should emphasize how changes in the metabolic processes at the cellular level will be manifested within the ecosystem or community structure,and how they will in?uence future climate feedbacks.A program should include the following components:

1.A systematic monitoring system with high-resolution measurements in time and space of atmospheric and surface water pCO 2,carbonate,alkalinity,and pH to validate model predictions and provide the foundations for interpreting the impacts of acidi?cation on ecosystems;

2.In regions projected to undergo substantial changes in carbonate chemistry,tracking of abundances and depth distributions of key calcifying and noncalcifying species at appropriate temporal and spatial scales to enable the detection of possible shifts and discrimination between natural variability and anthropogenic-forced changes;

3.Standardized protocols and data reporting guidelines for carbonate system perturbation and calci?cation experiments;

4.Manipulative laboratory experiments to quantify physiological responses,including cal-ci?cation and dissolution,photosynthesis,respiration,and other sensitive indices useful in predicting CO 2tolerance of ecologically and economically important species;

5.New approaches to investigate/address long-term subtle changes that more realistically simulate natural conditions;

6.Mesocosm and ?eld experiments to investigate community and ecosystem responses (i.e.,shifts in species composition,food web structure,biogeochemical cycling,and feedback mechanisms)to elevated CO 2and potential interactions with nutrients,light,and other environmental variables;

7.Integrated modeling approach to determine the likely implications of ocean acidi?cation processes on marine ecosystems and ?sheries,including nested models of biogeochemical processes and higher trophic-level responses to address ecosystem-wide dynamics such as competition,predation,reproduction,migration,and spatial population structure;and

8.Robust and cost-effective methods for measuring pH,pCO 2,and dissolved total alkalinity on moored buoys,ships of opportunity,and research vessels,?oats,and gliders.

DISCLOSURE STATEMENT

The authors are not aware of any potential biases that might be perceived as affecting the objectivity of this review.

ACKNOWLEDGMENTS

This work was jointly supported by the National Science Foundation (NSF)and the National Oceanic and Atmospheric Administration (NOAA).S.D.acknowledges support from NSF grant ATM-0628582.We also speci?cally acknowledge program managers Phil T aylor and Don Rice

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