Effects of Ocean Acidification on Marine Biodiversity and Ecosystem Function

University of Plymouth PEARL https://pearl.plymouth.ac.uk

Faculty of Science and Engineering School of Biological and Marine Sciences

2011-09-15 Effects of ocean acidification on marine biodiversity and ecosystem function

Barry, JP http://hdl.handle.net/10026.1/1314

Oxford University Press

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CHAPTER 10 Effects of ocean acidifi cation on marine biodiversity and ecosystem function

James P . B arry, S tephen W iddicombe, and Jason M . H all- S pencer

10.1 Introduction be diffi cult to detect amidst the variability associated with other human and non-human factors, and The biodiversity of the oceans, including the strik- the greatest impacts are expected to occur as acidifi - ing variation in life forms from microbes to whales cation intensifi es through this century. and ranging from surface waters to hadal trenches, In theory, large and rapid environmental changes forms a dynamic biological framework enabling the are expected to decrease the stability and produc- fl ow of energy that shapes and sustains marine eco- tivity of ecosystems due to a reduction in biodiver- systems. Society relies upon the biodiversity and sity caused by the loss of sensitive species that play function of marine systems for a wide range of serv- important roles in energy fl ow (i.e. food web func- ices as basic as producing the seafood we consume tion) or other processes (e.g. ecosystem engineers; or as essential as generating much of the oxygen we Cardinale et al. 2006 ). In practice, however, most breathe. Perhaps most obvious is the global seafood research concerning the biological effects of ocean harvest totalling over 100 Mt yr–1 (82 and 20 Mt in acidifi cation has focused on aspects of the perform- 2008 for capture and aquaculture, respectively; FAO ance and survival of individual species during 2009 ) from fi shing effort that expands more broadly short-term studies, assuming that a change in indi- and deeper each year as fi shery stocks are depleted vidual performance will infl uence ecosystem func- ( Pauly et al. 2003 ). Less apparent ecosystem services tion. By their nature, controlled experimental linked closely to biodiversity and ecosystem func- studies are limited in both space and time, and thus tion are waste processing and improved water may not capture important processes (e.g. acclima- quality, elemental cycling, shoreline protection, rec- tization and adaptation, multispecies biological reational opportunities, and aesthetic or educational interactions, chronic low-level impacts) that can experiences ( Cooley et al. 2009 ). ultimately play large roles in the response of marine There is growing concern that ocean acidifi cation systems to ocean acidifi cation. This ‘scaling up’ caused by fossil fuel emissions, in concert with the from individual- to ecosystem-level effects is the effects of other human activities, will cause signifi - most challenging goal for research on the potential cant changes in the biodiversity and function of effects of ocean acidifi cation. marine ecosystems, with important consequences To plan for the future, society needs information to for resources and services that are important to understand how ocean acidifi cation and other envi- society. Will the effects of ocean acidifi cation on eco- ronmental changes will affect fi sheries, aqua culture, systems be similar to those arising from other envi- and other services deriving from the effi cient func- ronmental perturbations observed during human tion of marine ecosystems. The infl ux of fossil fuel or earth history? Although changes in biodiversity CO 2 into the upper ocean from the atmosphere is and ecosystem function due to ocean acidifi cation altering the chemistry of ocean waters at a faster have not yet been widely observed, their onset may rate and greater magnitude than is thought to have

192 OUP CORRECTED PROOF – FINAL, 08/11/2011, SPi

EFFECTS OF ACIDIFICATION ON MARINE BIODIVERSITY AND ECOSYSTEMS 193 occurred on earth for at least a million years and per- tems in a region), or functional diversity (the number haps as much as 40 Myr (Pelejero et al. 2010 ; see of functional roles performed by the species present) Chapter 2 ). In this chapter, the infl uence of this (see Fig. 10.1 ; Petchey and Gaston 2006 ). Biodiversity important change in ocean chemistry on the biodi- is a dynamic feature of natural systems, refl ecting versity and function of marine ecosystems is consid- the continual evolutionary response of species in a ered, from basic physiological responses of individual region to selection across a broad range of environ- organisms and species, to the potential changes in mental and ecological pressures. Biodiversity can various ocean environments. expand and contract as species diversity or other elements of biological diversity are created, main- 10.2 Biodiversity and ecosystem tained, or lost to extinction. function The function of ecosystems is wholly dependent on biodiversity that allows energy to fl ow through The term biodiversity is broadly defi ned, and used trophic webs and biological networks. Moreover, to characterize aspects of the biological complexity the stability and resilience of ecosystem functions, of natural systems. Often cast simply as the number from nutrient cycling and energy fl ow, to the of species in a region (i.e. species richness ), biodiver- population dynamics of species, are thought to be sity has a far larger scope that spans the variation sensitive to the loss of biodiversity caused by per- within and among systems and organisms over turbations of both human and non-human origin. multiple scales and levels of genetic, organismal, This concept has long been considered theoreti- ecological, or ecosystem diversity. Measures of bio- cally, with more diverse and trophically complex diversity attempt to estimate the richness and even- systems expected to be more stable and resistant ness of biological characteristics at different levels, to perturbations. Species complementarity (different such as species richness and species diversity (the species have similar ecological roles) and species number and evenness of species in a region), taxo- redundancy (different species perform the same nomic diversity (not just species richness, but diver- function) are thought to provide ‘insurance’ for sity at higher taxonomic levels), genetic diversity ecosystem function in diverse systems by promot- (genetic variation in a population or species), habitat ing functional diversity and maintaining energy or ecosystem diversity (range of habitats or ecosys- fl ow among trophic levels (i.e. ecosystem function)

Figure 10.1 Species diversity does not necessarily represent functional diversity. Note that both groups have equal species richness and diversity (a single individual from each of eight molluscan species), but the group on the right has greater taxonomic distinctness and functional diversity. Photo R. M. Warwick. OUP CORRECTED PROOF – FINAL, 08/11/2011, SPi

194 OCEAN ACIDIFICATION upon a reduction or loss of species in response to ture) are intolerable. Range shifts along other environmental variation or other factors ( Loreau gradients in pH or carbonate saturation (e.g. depth- et al. 2001 ). related or horizontally in coastal regions) may also Field studies in terrestrial and marine ecosystems be possible. over the past two decades have provided both sup- Whether marine organisms, from microbes to port (e.g. Steneck et al. 2002 ) and moderate contro- long-lived megafauna, will be able to acclimatize or versy concerning the diversity–stability concept adapt to future ocean acidifi cation is an important, ( Loreau et al. 2001 ; Cardinale et al. 2006 ). The contro- but unresolved, question. Acclimatization is the versy relates, in part, to the disproportionate role of process by which individuals adjust to environmen- key species in many systems studied, without which tal changes (i.e. physiological adjustment). This stability is reduced. This issue may be important in may result in a change in energy costs (positive or several marine ecosystems where key prey species negative) associated with living. Adaptation is the (e.g. pteropods, krill, anchovies, and squid in coastal adjustment of species to environmental change systems) or taxa that play an important structural between generations, through natural selection of role (e.g. habitat-forming corals) can be critical individuals tolerant of new conditions. Tolerance or resources for other taxa. Thus, reduced biodiversity acclimatization by at least some individuals in the due to the loss of prey taxa or habitat-forming spe- population allows for adaptation, assuming that the cies may not have large effects on energy fl ow or tolerant traits are heritable and suffi cient time is ecosystem function and stability, so long as key spe- available for selection to increase the frequency of cies that maintain the functional diversity of the tolerant genotypes through multiple generations. If system are relatively unaffected (Tilman et al. 1997 ). individuals in most populations are able to acclima- Although this debate continues, a recent examina- tize to reduced ocean pH or carbonate saturation tion of experimental studies of nearshore marine through the adjustment of physiological homeosta- communities (Duffy 2009 ) and long-term studies of sis, changes in ocean biodiversity could be mild— large marine ecosystems (Worm et al. 2006 ) provides perhaps only a contraction in genetic diversity fairly strong support for the role of biodiversity in within species with minor effects on ecosystem ecosystem function and stability. For many marine functions. systems, however, the current understanding of the Although it is expected that there will be ‘win- natural history and functional roles of most species ners’ and ‘losers’ in response to ocean acidifi cation, is poor; thus it will be challenging to predict how many vulnerable species (such as corals; see Kleypas ocean acidifi cation may affect ecosystem function. and Yates 2009 ) may suffer from reduced performance and survival, and have limited scope for adap- 10.3 Acclimatization and adaptation tation due to the expected pace and magnitude of ocean acidifi cation in the future. Taxa with short Organisms and species faced with ocean acidifi ca- generation times and immense population sizes tion or other environmental changes have four such as phytoplankton and microbes (e.g. with one options—migration, acclimatization (i.e. tolerance), to three generations per day) have perhaps the adaptation, or extinction. Migration, by individu- greatest capacity to adapt, given that upwards of 35 als or by a population successively through genera- 000 to 100 000 generations are possible over the next tions, may be possible in some cases, but the global 100 years as ocean acidifi cation intensifi es. Collins nature of ocean acidifi cation coupled with range and Bell ( 2006 ), however, found little evidence of limitations imposed by other environmental adaptation to high CO2 levels in a pond alga parameters (e.g. temperature) may limit this option. ( Chlamydomonas) after 1000 generations. In contrast, For example, meridional gradients in aragonite the scope for adaptation by species with long gen- saturation (see Fig. 14.5 in Chapter 14 ) may allow eration times (e.g. 10 to 30 yr for some fi shes) and the ranges of some mid-latitude taxa to shift toward relatively small population sizes is expected to be more saturated waters of the tropics as acidifi ca- limited when selection for tolerant genotypes is tion intensifi es, unless other factors (e.g. tempera- constrained to just a few generations. OUP CORRECTED PROOF – FINAL, 08/11/2011, SPi

EFFECTS OF ACIDIFICATION ON MARINE BIODIVERSITY AND ECOSYSTEMS 195

10.4 Effects of environmental change 2006 ), may also infl uence biodiversity and ecosystem function due to the loss of critical habitat for Environmental variation over space or time can various coral-associated taxa. have positive and negative effects on biodiversity Evidence for shifts in biodiversity during periods and ecosystem function related to the rate, magni- of environmental change is common in the fossil tude, duration, and spatial scale of environmental record. Mayhew et al. ( 2008 ) report signifi cant posi- change (Knoll et al. 2007 ). Habitats with greater spa- tive correlations between variation in global tem- tial heterogeneity provide variable environmental perature and the rates of origination and extinction conditions that typically support higher biodiver- of families and genera through the Phanerozoic. sity than relatively homogeneous habitats. Temporal Correlations were higher for originations, but not environmental variation also plays a key role in for extinctions, when diversity lagged behind tem- regulating local diversity. Some level of change in perature by 10 Myr, suggesting that diversifi cation environmental factors (e.g. physical disturbance or occurs mainly after a period of extinction driven by variability in temperature, oxygen, or other para- global warming. For marine genera, the effect of meters) or biological factors (e.g. variation in the variation in CO2 levels on extinction rates was abundance of predators or competitors) can lead to stronger than that of temperature, suggesting that enhanced local diversity (Connell 1978 ). Moreover, ocean carbon levels have infl uenced marine species environmental variability can promote genetic diversity throughout the Phanerozoic. Five major diversity by selecting for a broad range of geno- mass extinction events that caused the loss of 75% types to match environmental patterns, or allowing or more of all species ( Jablonski and Chaloner 1994 ; for adaptive radiation as species emerge to fi ll new see also Chapter 4 ) are the most striking features of ecological space. Species, populations, or genotypes the fossil record. For many (if not all) of these events, originate through evolutionary divergence to rapid change in environmental parameters, such as exploit novel habitats, or through specialization in temperature, oxygen levels, and ocean pH, coupled response to environmental variation (temperature, with ecological factors, appear to have played a habitat complexity, oxygen concentration, light, large role in the high extinction rates (Knoll et al. etc.) and biological interactions (trophic, competi- 2007 ; Chapter 4 ). Marine life recovered following tive, or mutualistic). each extinction event, but required millions of years, Coral reef ecosystems, typifi ed by high topo- potentially due to slow rates of evolutionary diver- graphic complexity that promotes species-packing, sifi cation or persistently unfavourable environmen- have been shown to have been cradles of diversifi - tal conditions, or both ( Knoll et al. 2007 ). cation throughout the Phanerozoic, with high rates Is it likely that ocean acidifi cation will reduce the of species origination that are often exported to off- biodiversity of marine ecosystems and drive signifi - shore and deeper regions ( Kiessling et al. 2010 ; see cant shifts in their function? The response of marine Chapter 4 ). For example, habitat complexity gener- ecosystems will be linked to the rate and magnitude ated by highly branched scleractinian corals such as of changes in ocean chemistry in relation to the Acropora spp. provide habitat for a remarkably potential rates of acclimatization, adaptation, and diverse array of fi shes and invertebrates. Such evolution of marine organisms, from microbes to branching corals are keystone functional groups, vertebrates. The ongoing large and rapid changes and are threatened by ocean acidifi cation and other in ocean pH and carbonate saturation are expected environmental changes (Bellwood et al. 2004 ). to drive environmental changes unseen in the Reduced coral growth and weaker carbonate recent evolutionary history of marine organisms, cementation will increase the probability of damage posing an evolutionary challenge to acclimatize or to most structurally complex corals during storms, adapt. At a minimum, the genetic diversity of vari- probably leading to reef fl attening and reduced reef ous marine taxa is likely to change. It remains biodiversity (Hofmann et al. 2010 ). Similar impacts unknown whether ocean acidifi cation will drive on scleractinian corals, and perhaps other structure- species to extinction, but it is possible, based on forming groups in deep-sea systems (Guinotte et al. the growing literature concerning the sensitivity OUP CORRECTED PROOF – FINAL, 08/11/2011, SPi

196 OCEAN ACIDIFICATION and performance of marine organisms under structure of phytoplankton populations (Hall- future, high-CO 2 conditions (e.g. Fabry et al. 2008 ; Spencer et al. 2008 ; Doney et al. 2009 ; see Chapters 6 Widdicombe and Spicer 2008 ; Doney et al. 2009 ). and 7). Taxa that are currently carbon-limited (e.g. Extinction is not required for ocean acidifi cation some cyanobacteria) may be among the ‘winners’ in to affect the function of marine ecosystems, since a high-CO2 ocean. For other autotrophs (e.g. coccol- changes in the relative abundance and activities of ithophores), photosynthesis and growth, as well as species can affect biological interactions (e.g. food calcifi cation, may be affected, with complex web function) and habitat quality. If calcifying taxa responses among species. A suite of experiments on are indeed the most vulnerable to decreasing ocean marine phytoplankton have shown that the pH and carbonate saturation (Orr et al. 2005 ; responses of coccolithophorids (calcitic phytoplank-

Hofmann et al. 2010 ), then potential impacts of ton) to elevated CO2 levels vary, but generally ocean acidifi cation on the abundance and produc- exhibit reduced rates of calcifi cation (Ridgwell et al. tivity of calcifying species that play key roles in 2009 ; Hendriks et al. 2010 ). Reduced calcifi cation marine food webs or other elements of ecosystem has been measured in a variety of taxa, particularly function are likely to have broad cascading effects corals and molluscs ( Michaelidis et al. 2005 ; Gazeau within the ecosystem. For example, pteropod mol- et al. 2007 ; Kuffner et al. 2008 ; Doney et al. 2009 ), and luscs sensitive to reduced aragonite saturation con- is the most widely observed and consistent effect of ditions ( Feely et al. 2004 ; Orr et al. 2005 ; Comeau ocean acidifi cation ( Hendriks et al. 2010 ; Kroeker et al. 2009 ) may be less abundant under future ocean et al. 2010 ). Exposure times have typically been conditions, leading to reduced availability for their short for most calcifi cation studies, and may often current predators, which must then fi nd alternative be too short to detect acclimatization, which has prey. Likewise, species that may depend on ptero- been shown to require about 6 weeks for a marine pods in other ways (e.g. Pteropagurus sp., a hermit fi sh (Deigweiher et al. 2008 ). In contrast, coccolitho- crab that depends upon pteropod shells as habitat; phores may acclimatize to high CO2 levels within McLaughlin and Rahayu 2008 ), may suffer from hours ( Barcelos e Ramos et al. 2010 ). Increased rates reduced pteropod abundance. Simultaneously, of calcifi cation in low-pH waters have been observed pteropod prey (e.g. copepods, diatoms) and poten- for a few taxa (e.g. crustaceans, Ries et al. 2009 ), but tial competitors (e.g. krill, salps) are likely to experi- it appears that, at least for some species, higher cal- ence reduced predation and competition, cifi cation in low-pH waters may require energetic respectively, and thus, may increase in abundance. trade-offs that reduce overall performance ( Wood Consequently, a signifi cant reshuffl ing of the struc- et al. 2008 ). ture of marine communities and ecosystem func- Even for taxa tolerant of low-pH waters, the tion in response to ocean acidifi cation is possible if physiological ‘cost of living’ is expected to change there are marked shifts in the abundance of ‘losers’ the energy required for basic biological functions and ‘winners’, particularly if key species are ( Pörtner et al. 2000 ). Immersion in high-CO2 waters affected. can disrupt the acid–base status of many marine animals, leading to reduced respiratory effi ciency, 10.5 The effects of ocean acidifi cation reduced enzyme activity, and metabolic depression, on organisms with potentially large effects on overall metabolic performance ( Seibel and Walsh 2003 ; see Chapter Several physiological processes, such as photosyn- 8 ). Assuming a constant total energy budget, a thesis, calcifi cation, acid–base homeostasis, respira- change in the ‘cost of living’ is expected to result in tion and gas exchange, and metabolic rate, can be a reallocation of energy for growth and reproduc- infl uenced by changes in ocean carbonate chemis- tion (Fig. 10.2 ). For taxa affected by ocean acidifi ca- try ( Gattuso et al. 1999 ; Seibel and Walsh 2003 ; tion, individual physiological stress can lead to Melzner et al. 2009b ; Chapter 8 ). High ocean carbon reduced growth, size, reproductive output, and sur- levels are expected to affect primary producers in vival. On a population level, impaired individual different ways, perhaps leading to a shift in the performance and survival have consequences for OUP CORRECTED PROOF – FINAL, 08/11/2011, SPi

EFFECTS OF ACIDIFICATION ON MARINE BIODIVERSITY AND ECOSYSTEMS 197 populations and species that may include reduced acidifi cation. Many taxa in habitats with variable or abundance, productivity, and resilience to distur- low pH (e.g. vesicomyid clams, vestimentiferan bance, as well as increased likelihood of extinction. tubeworms, mussels in vent or seep environments) For taxa benefi ting either directly or indirectly from also have adaptations that allow them to thrive in high CO2 levels, the opposite may be true. It is also naturally hypoxic and low-pH waters (Goffredi and important to consider the cumulative effects of Barry 2002 ; Tunnicliffe et al. 2009 ). Mobile crusta- environmental stressors on the demography and ceans and fi shes may benefi t somewhat in a high- productivity of populations. Effects on different life CO2 ocean, based on their generally higher rates of stages can sum to signifi cant impacts on population growth and calcifi cation in low-pH waters (Ries success. For example, during periods of low sea- et al. 2009 ; Kroeker et al. 2010 ). However, even taxa surface temperature (<13.1°C), exposure to low-pH with the capacity to cope with activity-related waters reduces the survival of early life stage barna- hypercapnia can experience impaired physiological cles along the coast of the south-west United performance in high-CO2 waters. Rosa and Seibel Kingdom by 25%, potentially leading to reduced ( 2008 ) found that activity levels in jumbo squid local population abundance ( Findlay et al. 2010 ). declined by 45% under a 0.3 unit reduction in pH. Sensitivity to ocean acidifi cation is expected to be In contrast, cod exposed to a large pH perturbation coupled primarily to fundamental physiological (–1 pH unit) for several months displayed no evi- adaptations linked closely to phylogeny. Marine dence of impaired maximal swimming speed organisms with a natural capacity for gas exchange ( Melzner et al. 2009a ). (i.e. organisms with well-developed respiratory and Taxa with weaker control over internal fl uid circulatory systems, as well as respiratory proteins chemistry may be at greater risk from ocean acidifi - allowing high O2 and CO2 fl uxes) that support high cation. For example, echinoderms, brachiopods, and metabolic rates and high aerobic scope (e.g. fi shes, lower invertebrates (e.g. sponges, cnidarians, and decapod crustaceans, and cephalopods) are pre- ctenophores) lack respiratory organs and exchange adapted for many of the stresses related to ocean gases with seawater by molecular diffusion across acidifi cation ( Melzner et al. 2009b ; see Chapter 8 ). various body tissues. Although physiological toler- This is due in part to the overlapping physiological ance to ocean acidifi cation has not been examined challenges posed by metabolic CO2 generation dur- closely in most of these groups (other than rates of ing intense aerobic activity (e.g. coping with inter- calcifi cation, see below), their postulated weak con- nal acid–base disruption) and the effects of ocean trol of internal fl uid chemistry (e.g. sea urchins, Miles et al. 2007 ) is expected to increase their sensitivity to changing ocean chemistry. Echinoderms Normal Stressed appear less tolerant of low-pH waters than many groups, as indicated by their conspicuous absence

from habitats with naturally high CO2 levels such as R R hydrothermal vents ( Grassle 1986 ) and low-pH

M areas near shallow CO2 vents off Italy (Hall-Spencer M G et al. 2008 ). Notably, various taxa with limited physi- G ological capabilities (many cnidarians and sponges) appear to tolerate low or variable pH, due to their occurrence in low-pH habitats such as hydrothermal

Figure 10.2 Hypothetical energy budget for normal and stressed vents and other natural CO2 venting sites. Moreover, organisms. Under normal conditions, the energetic cost of maintenance generalities based on short-term studies of organism (M) is a signifi cant portion of the total energy budget. If ocean acidifi cation physiology or survival, as are most common in the or other environmental changes are stressful, maintenance costs (e.g. ion literature, may differ from the eventual long-term regulation) can increase, leaving less energy available for growth (G) or reproduction (R). In addition, if metabolic depression is induced by ocean consequences of ocean acidifi cation. acidifi cation, the total energy budget may decrease, hence the smaller pie For calcifying taxa, the type of carbonate miner- size for the energy budget of the stressed organism. als formed can infl uence their vulnerability to ocean OUP CORRECTED PROOF – FINAL, 08/11/2011, SPi

198 OCEAN ACIDIFICATION acidifi cation. Carbonate skeletal structures of waters ( Fine and Tchernov 2007 ). Upon immersion marine taxa vary considerably both in terms of how in ambient pH waters (pHT = 8.3) the corals recalci- much calcium carbonate (CaCO 3 ) is included, from fi ed. This type of recovery is unlikely for many nearly 100% CaCO 3 to mixtures of chitin and CaCO 3 other coral taxa with modes of life linked strongly

(e.g. many crustacean shells). The form of CaCO3 to their structural framework. also varies, with most taxa precipitating aragonite Calcifi ed shells and skeletons can play important or calcite, the latter which may include some per- roles for organisms coping with environmental var- centage of magnesium. Of these, high-Mg calcite is iability. In some cases, more robust calcifi cation may the most soluble in seawater, and thus most suscep- increase the survival (and presumably the fi tness) tible to dissolution by ocean acidifi cation, followed of organisms, which can affect the biodiversity and by aragonite and calcite (see Box 1.1 in Chapter 1 ). function of marine communities. For example, the Although calcifi cation rates by organisms are intertidal snail Littorina littorea thickens its shell generally impaired under low-pH conditions, there after exposure to chemical cues produced by its is considerable variation among the responses of main predator, the green shore crab, Carcinus mae- major taxonomic groups (Hendriks et al. 2010 ; nas , in effect increasing its defence against preda- Kroeker et al. 2010 ). Scleractinian corals (aragonite) tion ( Bibby et al. 2007 ). Such shell thickening does exhibit the largest reduction in calcifi cation and not occur under high-CO2 conditions, presumably most consistent response to low-pH waters. due to the increased energetic cost of calcifi cation at Coccolithophores (calcite) and molluscs (mostly lower-pH, less saturated conditions, thereby calcitic) had somewhat weaker, variable, and non- increasing their risk of predation. Very few studies signifi cant changes in calcifi cation. Individual stud- have examined the effects of ocean acidifi cation on ies have reported generally reduced rates of behavioural responses that mediate interactions calcifi cation for bivalve and gastropod molluscs between interacting species and populations. under high-CO2 conditions (Gazeau et al. 2007 ; Doney et al. 2009 ; Ries et al. 2009 ; Hendriks et al. 10.6 Habitats 2010 ). In contrast, echinoderms (calcite) are highly variable in response, mainly due to the great varia- The risk of changes in the biodiversity and function bility in degree of calcifi cation within the phylum of marine ecosystems due to ocean acidifi cation is (e.g. Wood et al. 2008 ). Crustaceans (chitin, calcite, likely to vary considerably among habitats. Seawater amorphous carbonate) are the single group show- carbonate chemistry is affected by temperature and ing a signifi cant increase in calcifi cation rate under biological processes, leading to signifi cant patterns high-CO2 conditions ( Kroeker et al . 2010 ). in carbonate chemistry across zonal and meridional Reef-building corals in particular, due to their gradients (Kleypas et al. 1999 ; Feely et al. 2004 ), with aragonitic skeletons, are perceived to be at high depth, and in relation to biological productivity. risk from ocean acidifi cation, based on the pro- Colder high-latitude regions have naturally lower jected future reduction in aragonite saturation saturation states for aragonite and calcite due to the throughout the world’s oceans (Kleypas et al. 1999 ). higher solubility of CO2 at low temperatures, and These projections are consistent with the existing will be the fi rst surface waters to be persistently global distribution of deep-sea aragonitic corals, undersaturated with respect to aragonite ( Orr et al. which are most abundant in the Atlantic and rela- 2005 ; see Chapter 2 ), with potentially signifi cant tively rare in habitats with low aragonite satura- effects on marine calcifi ers. The infl uence of ocean tion, such as the Pacifi c Basin (Guinotte et al. 2006 ; acidifi cation on sediment ecosystems is considered Manzello 2010 ). Surprisingly, some corals may sur- in Chapter 9 . vive acidic conditions without carbonate skeletons. Two Mediterranean species (Oculina patagonica and 10.6.1 Upper ocean Madracis pharencis ) survived a 12-month exposure to acidic (pHT = 7.3–7.6) waters but lost their car- Changes in environmental conditions through this bonate skeletons, which dissolved in the corrosive century, including ocean acidifi cation and warming, OUP CORRECTED PROOF – FINAL, 08/11/2011, SPi

EFFECTS OF ACIDIFICATION ON MARINE BIODIVERSITY AND ECOSYSTEMS 199 could lead to a restructuring of phytoplankton ballasting of organic aggregates (Fabry et al. 2008 ; assemblages with consequences that would rever- Ridgwell et al. 2009 ). berate throughout marine communities. For exam- Holoplankton can also be affected by changing ple, the composition of phytoplankton assemblages ocean chemistry, perhaps especially in weakly sat- in the north-east Atlantic changed as waters urated waters of high-latitude systems. Euphausiids warmed during the latter half of the last century, and thecosomatous pteropods, two key planktonic with a poleward expansion of warm-temperate groups thought to be critical linkages in global food plankton and recession of colder forms (Hays et al. webs, may be affected differently by ocean acidifi - 2005 ). In the English Channel, coccolithophores cation. Pteropods (e.g. Limacina sp. and Clio sp.) are and dinofl agellates have become more abundant important planktonic calcifi ers in open-ocean food and dominant over the past ~20 yr, while diatoms webs and represent major prey taxa for higher and Phaeocystis have decreased (Widdicombe et al. predators (e.g. many salmon species), and thus are 2010 ). The expansion of dinofl agellates may be a key link in open-ocean food webs and energy expected based on the emergence of these groups fl ow ( Fabry et al. 2009 ). Immersion of shelled ptero- 2– during warmer, high-CO 2 periods in earth’s history pods in high-CO2 , low-CO3 waters is known to (Beardall and Raven 2004 ). Cyanobacteria, which weaken their aragonitic shells (Orr et al. 2005 ) and thrived under high CO2 levels earlier during earth’s is expected to reduce their survival and productiv- history, are also expected to benefi t from ocean ity (Comeau et al. 2009 , 2010 ). To date, only minor acidifi cation. Photosynthetic rates of two dominant decadal-scale changes have been observed globally oceanic cyanobacterial genera (Synechococcus and in these groups. In the California Current ecosys- Trichodesmium ) were observed to increase markedly tem, pteropod abundance has not declined, and under expected future climate conditions, so long may have increased over the past 50 yr ( Ohman as nutrient levels were suffi ciently high, while et al. 2009 ). In the Southern Ocean, where aragonite other closely related taxa (Prochlorococcous and undersaturation is predicted to begin as early at Nodularia) showed little change or even lower rates 2030 (McNeil and Matear 2008 ), ocean acidifi cation ( Fu et al. 2007 ). An increase in the diversity, abun- may already be affecting pteropod populations. dance, or productivity of cyanobacteria could Roberts et al. ( 2008 ) reported that the shell weights increase rates of global nitrogen fi xation (Hutchins of pteropods collected in sediment traps deployed et al. 2009 ), which would be likely to drive responses in sub-Antarctic waters (47°S) have decreased over in primary production by other groups. High CO 2 the past decade. This decrease was not correlated levels have also been shown to cause enhanced with chlorophyll abundance or temperature, but production of dimethyl sulphide by natural phyto- was consistent with changes in aragonite satura- plankton assemblages, which could promote cli- tion, and thus the potential infl uence of ocean acid- mate homeostasis by stimulating cloud formation ifi cation cannot be rejected. The loss of Limacina or (see Chapter 11 ). other key pteropod taxa in undersaturated waters

Elevated p CO 2 can also affect phytoplankton due to reduced calcifi cation (e.g. Comeau et al. communities and the entire water column commu- 2009 , 2010 ) could have signifi cant implications for nity through changes in elemental uptake or calcifi - their predators and energy fl ow through open- cation by major groups. Increased C:N and C:P ocean food webs. ratios have been measured in mixed phytoplankton Euphausiids, copepods, and other planktonic assemblages in response to high CO2 levels crustaceans are dominant elements of food webs ( Riebesell et al. 2007 ; see Chapter 6 ), potentially worldwide, and are often suitable alternative prey changing their nutritional value to consumers and for many oceanic pteropod predators (Cooley et al. leading to changes in growth and reproduction of 2009 ). In contrast to pteropods, krill and other crus- zooplankton. Reduced rates of calcifi cation for coc- taceans may not be strongly affected by ocean acid- colithophores and foraminifera, two major plank- ifi cation, and some taxa may even benefi t, but few tonic calcifying groups, may also affect the fl ux of studies have examined this topic. Kroeker et al. organic debris to deeper waters, due to changes in ( 2010 ) report that the literature available to date OUP CORRECTED PROOF – FINAL, 08/11/2011, SPi

200 OCEAN ACIDIFICATION indicates signifi cantly higher calcifi cation rates and 10.6.2 Deep-sea ecosystems marginally higher growth for crustaceans in Deep-sea ecosystems may experience some of the low-pH waters, though survival was somewhat most profound changes in biodiversity and ecosys- reduced. Kurihara (2008 ) found lower hatching tem function in response to ocean acidifi cation. success for krill exposed to low-pH waters and Dramatic shoaling of the aragonite and calcite satu- mixed effects on other crustacean taxa. It remains ration boundaries (see Chapter 2 ) will cause very questionable how krill populations will be affected large shifts in habitat quality for deep-sea calcifi ers. by ocean acidifi cation, and how the effects, if any, Aragonite and calcite undersaturation of deep-sea will infl uence marine biodiversity and food web waters is likely to restrict deep-sea aragonitic corals function. (and perhaps many calcitic forms) from much of Sparingly few studies are available to assess the their existing bathymetric ranges (Tittensor et al. effects of ocean acidifi cation on gelatinous taxa. 2010 ). As the saturation states for aragonite (Ω ) and Jellyfi sh outbreaks have been reported more com- a calcite (Ω ) drop, it becomes energetically more monly over the past decades, with several factors c costly to precipitate CaCO ( Cohen and Holcomb (warming, overfi shing, habitat modifi cation, eutro- 3 2009 ), and where Ω drops below 1, exposed CaCO phication, species introductions) being implicated 3 is subject to dissolution ( Hall-Spencer et al. 2008 ; ( Richardson et al. 2009 ). Several gelatinous groups Manzello et al. 2008 ). Recent surveys of the global are important elements of open-ocean food webs distributions of aragonitic scleractinian corals indi- from the tropics to the poles, including larvaceans, cate that few taxa are currently found below the chaetognaths, salps, and siphonophores. It remains saturation depth for aragonite (Guinotte et al. 2006 ). unclear how these taxa will respond to ocean Lophelia sp., a common aragonitic deep-sea coral, acidifi cation. has been shown to calcify 30 to 56% more slowly in Meroplankton, taxa that live only part of their waters with pH perturbations 0.15 to 0.3 units lower lives (often early life-history phases) in open than ambient ( Maier et al. 2009 ). Although calcifi ca- waters, are expected to be particularly sensitive to tion proceeds even when Ω drops below 1, contin- ocean acidifi cation. Recent reviews have shown a ued reductions in CaCO saturation appear very generally negative or mixed results concerning the 3 likely to have an effect on deep-sea corals in the effects of ocean acidifi cation on early life stages future. Many other deep-sea corals (e.g. gorgoni- (Dupont et al. 2010 ; Kroeker et al. 2010 ). Kurihara ans) precipitate less soluble calcite, but could be (2008 ) reports generally negative effects on eggs, affected as the calcite saturation depth rises with larvae, and other early phases for a variety of increasing ocean CO . marine calcifi ers. The vulnerability of early life- 2 Changes in the biodiversity of deep-sea corals history stages can have large effects on population are likely to affect the function of deep-sea ecosys- survival and demography, even though adults are tems. Deep-sea coral communities are often con- somewhat unaffected. For some taxa, the develop- sidered to be hot spots for biodiversity, with high ment and survival of early life stages are impaired, species diversity of structure-forming corals (often and in others delayed, but the larvae develop fully dominated by octocorals) as well as many other in low-pH waters, albeit more slowly than in con- taxa associated with the heterogeneous habitat trol treatments (Dupont et al. 2010 ). Slow develop- structure ( Roberts et al. 2006 ). Such communities ment can put early life-history phases at prolonged are common on many seamounts, which number risk to predators. Although the literature remains upwards of 50 000 worldwide. Impacts on deep- sparse concerning the impacts of ocean acidifi ca- sea corals could also require long periods for tion or climate-related environmental change on recovery, even in suitable habitats, considering the survival and development of meroplankton in the slow growth rates and high longevity of many general, changing ocean conditions could drive species, with ages reaching from decades to centu- important changes in the population dynamics of ries (Roberts et al. 2006 ) or longer ( Roark et al. various species, with indirect effects throughout 2009 ). marine food webs. OUP CORRECTED PROOF – FINAL, 08/11/2011, SPi

EFFECTS OF ACIDIFICATION ON MARINE BIODIVERSITY AND ECOSYSTEMS 201

Abyssal sedimentary habitats are not immune to in sinking organic fl ux, in addition to altered pH the potential effects of ocean acidifi cation. and carbonate saturation, may drive important Echinoderms, including a diverse assemblage of changes in ecosystem function. ophiuroids, echinoids, and holothurians, commonly form a dominant guild of abyssal benthic inverte- 10.6.3 Coastal ecosystems brates, along with decapod crustaceans and fi shes. The weakly calcifi ed tests of deep-sea urchins sug- Coastal ecosystems, including coastal upwelling gest that calcifi cation is either unimportant as a pro- zones, coral reefs, mangroves, kelp forests, seagrass tection against predators, or is energetically costly, beds, estuaries, and other nearshore systems, are by or both. Some taxa, such as Tromikosoma sp. in the far the most important ecosystems that humans North Pacifi c, have little or no carbonate in their depend upon for fi nfi sh and shellfi sh fi sheries and test, which is proteinaceous. As anthropogenic CO2 aquaculture, as well as recreation, and thus are criti- penetrates to the abyss in the future, seawater will cally important with respect to future impacts from become corrosive to aragonite and calcite, presum- ocean acidifi cation and other environmental ably making it even more diffi cult for many echi- changes (Cooley et al. 2009 ). Coastal systems span a noids and other carbonate-bearing taxa to form wide range of physical and oceanographic regimes their skeletons. The absence of echinoderms from from high to low latitudes, upwelling systems to areas in the Okinawa Trough exposed continuously western boundary currents, and both benthic and to high-CO2 vent fl uids (A. Boetius, pers. comm.), pelagic assemblages. The seawater chemistry and suggests that ocean acidifi cation could act selec- biological processes in these disparate environ- tively against this often dominant abyssal phylum. ments vary greatly, and thus their sensitivity to Weaker calcifi cation under more acidic conditions ocean acidifi cation is also expected to vary. could affect the survival of a variety of taxa. Mussels Anthropogenic changes in oceanographic and eco- ( Bathymodiolus brevior ) inhabiting low-pH hydro- logical processes in coastal systems related to fossil thermal vent systems in the western Pacifi c survive fuel emissions and other human activities (e.g. and grow, but have poorly calcifi ed shells, making coastal nutrient loading) are not fully understood them more vulnerable to predation by decapod (e.g. Feely et al. 2010 ), but will probably also differ crabs (Paralomus sp.) than are conspecifi cs with among ecosystems. Considering the diversity of thickly calcifi ed shells that inhabit less corrosive coastal ecosystems, it is beyond the scope of this sites ( Tunnicliffe et al. 2009 ). chapter to provide a comprehensive treatment of The strong link between communities at the sur- their vulnerability to ocean acidifi cation. Instead, face and in the deep sea suggests that changes in we touch on several features of ocean acidifi cation biodiversity in the upper ocean due to ocean acidi- in coastal systems, using upwelling systems and fi cation could initiate shifts in biodiversity and eco- coral reefs as examples. system function in the deep sea. Changes in the export of organic debris from surface waters due to 10.6.3.1 Upwelling zones ocean acidifi cation, perhaps in combination with Upwelling zones off the western US coast, along other environmental changes, could affect bathype- most eastern boundary currents, and several other lagic, abyssal, and benthic ecosystems in the deep regions worldwide typically have a wider range in sea. Recycling of organic material in the upper oxygen, pH, and other carbonate system parame- water column may increase due to increased disso- ters than most open-ocean systems, due largely to lution of coccolithophores and foraminifera, lead- the boom and bust productivity of surface waters ing to a reduction in carbonate ballast within organic and remineralization of organic material at depth. aggregates and reduced export of organic carbon to Surface pH and carbonate saturation vary through deep waters. These potential effects of ocean acidifi - these cycles, and waters in the oxygen minimum cation on the rate of carbonate rain and the biologi- zone (OMZ) several hundred metres below the sur- cal pump are not yet well understood (see Chapter face can be suboxic and corrosive to CaCO 3 . 6 ). For the food-limited deep sea, however, changes Estuaries can also have quite strong gradients in OUP CORRECTED PROOF – FINAL, 08/11/2011, SPi

202 OCEAN ACIDIFICATION oxygen, pH, and carbonate saturation (Miller et al. Changes in the biodiversity and function of 2009 ). Along the Californian coast (and eastern Pacifi c coastal ecosystems due to ocean acidifi cation are margin) the concentration of oxygen can approach likely to be linked to the vulnerability of key inter- anoxia (less than 5% saturation, ~10 μmol kg–1 ) in the mediate prey taxa, with broader effects driven indi- core of the OMZ near a depth of 700 m. Wind-driven rectly through trophic dependences. Top predators coastal upwelling and other processes can transport in these systems, including fi shes, cephalopods, hypoxic, low-pH waters from the upper OMZ toward birds, and mammals, are expected to have greater the surface, creating conditions of undersaturation physiological capacities (at least as adults) to cope with respect to CaCO3 for surface organisms and with elevated CO2 levels, than many of their prey. coastal benthic communities ( Feely et al. 2008 , 2010 ). Large, active cephalopods, especially those inhabit- The highly variable conditions found in coastal ing suboxic habitats, may experience respiratory upwelling zones act as a physiological fi lter, allowing problems with future acidifi cation (e.g. Rosa and species to thrive only if all of their life stages can toler- Seibel 2008), but most vertebrates, especially air- ate the variable local conditions. Natural environ- breathing birds and mammals, are not expected to mental variability has been shown to have large be affected directly by ocean acidifi cation. However, effects on the structure and function of the California the indirect effects of ocean acidifi cation for these Current ecosystem (e.g. Chavez et al. 2003 ), which higher predators could be substantial. Impacts on may mask or interact with the effects of ocean acidifi - highly sensitive taxa (e.g. thecosomatous ptero- cation or other anthropogenic changes. Increasing pods) could cascade through food webs, as has been acidifi cation of coastal environments through this observed in relation to other environmental changes century due to elevated CO2 emissions or other fac- (warming). For example, the breeding success of tors is likely to pose new physiological challenges for planktivorous and piscivorous seabirds along the coastal taxa. central California coast varies among warm and The response of coastal species to future ocean cold periods, but is linked directly to the availabil- chemistry has been examined in various recent ity of key prey taxa rather than specifi c physical studies indicating mixed, but generally negative, parameters ( Sydeman et al. 2001 ). It remains responses ( Kroeker et al. 2010 ). As noted above, unknown whether the potentially negative effects some photosynthetic taxa may benefi t from ocean of ocean acidifi cation on some groups (e.g. ptero- acidifi cation (e.g. some seagrasses; Hall-Spencer pods) will be balanced by positive responses in et al. 2008 ; Hendriks et al. 2010 ). However, even other groups with similar functional roles (e.g. though they thrive in highly variable environments, krill). In coastal systems with generally reduced coastal heterotrophs have generally responded to functional redundancy among species ( Micheli and low-pH or low-carbonate-saturation waters with Halpern 2005 ), the likelihood of indirect food web impaired performance (e.g. acid–base balance, cal- effects due to ocean acidifi cation and other environ- cifi cation, growth, or survival), including adults mental changes may be high. (e.g. barnacles, Findlay et al. 2010 ; bivalves, Gazeau Benthic communities in coastal systems and sea- et al. 2007 ; ophiuroids, Wood et al. 2008 ; urchins, bed habitats throughout the world’s oceans are cen- Miles et al. 2007 ) and early life-history phases (bar- tres of biodiversity where much of the species nacles, Findlay et al. 2010 ; echinoderms, Dupont richness of the oceans is found. These communities et al. 2010 ; molluscs, Kurihara 2008 ). Not all coastal include a wide range of organisms that play key fauna respond strongly or negatively to ocean acidi- roles as ecosystem engineers, providing habitat for fi cation. Adults of some higher taxa have shown lit- other taxa (e.g. corals, kelp, seagrasses, burrowing tle sensitivity to acidifi cation (e.g. Dungeness crab, taxa, and oyster beds), and play important roles in Pane and Barry 2007 ; cod, Melzner et al. 2009a ), and elemental fl uxes of carbon and nitrogen through Ries et al. ( 2009 ) observed mixed responses to ocean bioturbation and other effects of burrowing acidifi cation for juveniles of various taxa, including ( Widdicombe and Spicer 2008 ). Benthic systems in enhanced calcifi cation and growth for a lobster and coastal zones may be more vulnerable to ocean a shrimp. acidifi cation than some more offshore sites because OUP CORRECTED PROOF – FINAL, 08/11/2011, SPi

EFFECTS OF ACIDIFICATION ON MARINE BIODIVERSITY AND ECOSYSTEMS 203 they are likely to contain waters that are corrosive ment of corals can be affected by low-pH waters to CaCO3 (at least along coastal areas with strong ( Cohen and Holcomb 2009 ). Reduced calcifi cation oxygen minimum zones) earlier than many surface coupled with poor cementation can promote ero- communities (e.g. Feely et al. 2008 ), with potentially sion and reef fl attening, which severely reduces the important impacts for calcifi cation and survival. structural heterogeneity of reefs and lowers its Other chapters in this volume give a more thorough potential to support biodiversity (Alvarez-Filip discussion of benthic (Chapter 7 ) and sedimentary et al. 2009 ). Reefs experiencing a loss of structural ( Chapter 9 ) habitats. complexity also experience a loss or change in fi sh assemblages, lower densities of commercially 10.6.3.2 Coral reefs important species, and lower rates of larval fi sh Coral reefs are perhaps the ecosystems understood recruitment ( Feary et al. 2007 ). Weaker reef cemen- the best in terms of potential impacts of ocean acidi- tation also increases the potential for reef damage as fi cation for marine biodiversity. Precipitation of storm frequency and intensity increases with con-

CaCO 3 by corals and calcifying algae forms the tinued global warming, leading to further reef deg- physical structure and much of the habitat complex- radation. Eventually, erosion of poorly cemented ity of coral reefs upon which additional biodiversity (and non-accreting) forereef habitats will open develops. Tropical reef systems have also been lagoon and backreef areas to erosion and provide shown to be ‘cradles of evolution’, where more spe- less effective shoreline protection for coastal cies have originated during earth’s history than any communities. other region ( Kiessling et al. 2010 ). Likewise, tropi- The effect of ocean acidifi cation on the function of cal reefs have been shown to disappear from the entire communities has been addressed only rarely. fossil record during several mass extinctions ( Veron In a mesocosm-based study of a temperate rocky 2008 ), indicating that they are also vulnerable to shore community in the UK, Hale et al. (2011) environmental change (see Chapter 4 ). observed a reduction in the species diversity and Ocean acidifi cation, coupled with ocean warm- evenness of the faunal assemblage with reduced ing, can pose important risks for the biodiversity pH, with a general ranking of vulnerability from and function of coral reef systems in several ways, echinoderms (most sensitive), to molluscs, crusta- ranging from basic changes in the biomineraliza- ceans, and polychaetes (least sensitive). Nematode tion and erosion of the physical foundation of reefs, abundance increased as pH was reduced, most to less understood changes in biological interac- likely due to a release from biological disturbance tions among species. Numerous studies have docu- (predation and competition) rather than a direct mented a reduction in calcifi cation by corals and benefi t from ocean acidifi cation. The effects of ele- coralline algae in response to ocean acidifi cation vated temperature differed among pH treatments, ( Doney et al. 2009 ). De’ath et al. ( 2009 ) documented highlighting the diffi culty of extrapolating from a recent decline in calcifi cation rates on the Great studies involving single species or single environ- Barrier Reef attributable to warming, ocean acidifi - mental factors, to predict the effects of future envi- cation, or both. In addition to reduced calcifi cation ronmental changes on natural communities. rates, the strength of cementation may also be Natural CO2 venting sites offer perhaps the reduced in waters with a lower pH, promoting strongest evidence of shifts in the biodiversity of higher rates of physical and bio-erosion ( Manzello entire communities in response to high ocean CO2 et al. 2008 ). Processes other than calcifi cation are levels. Benthic communities along a persistent gra- also affected by ocean acidifi cation. Competition dient in pH and carbonate saturation near CO2 between corals and other taxa, particularly non- vents in intertidal to shallow subtidal depths adja- calcifying macroalgae, may also be mediated by cent to the island of Ischia off the southern coast of reduced rates of calcifi cation or other physiological Italy show dramatic faunal and fl oral patterns that processes linked to ocean acidifi cation, which are are apparently a result of differential tolerance to likely to reduce the ability of corals to compete for ocean acidity ( Hall-Spencer et al. 2008 ). Continuous space ( Kuffner et al. 2008 ). Reproduction and recruit- seafl oor venting of nearly pure CO2 alters seawater OUP CORRECTED PROOF – FINAL, 08/11/2011, SPi

204 OCEAN ACIDIFICATION

100 but 62% of 39 taxa were still present in the mildly 560

1000 3200 acidic sites (reduction of 0.27 pH units). In contrast, the pattern of diversity loss with pH was similar for 80 non-calcifying fauna and algae. Although this sys-

tem and other natural CO2 venting sites do not com- pletely mimic the scale and effects of global ocean 60 acidifi cation, they are strong indicators of its potential effects on biodiversity and ecosystem function, as well as natural laboratories that complement 40 other efforts to understand the effects of a changing Taxa remaining (%) remaining Taxa ocean.

20 10.7 Implications of biodiversity loss

0 Although studies available to date do not provide a 0.0 0.5 1.0 1.5 clear picture of future changes in ecosystem func- pH reduction (units) tion due to ocean acidifi cation, much evidence suggests that ocean acidifi cation could have increasingly Figure 10.3 Change in diversity as a function of pH reduction for profound effects in several marine ecosystems (coral organisms living near the Ischia CO2 vents. The biodiversity remaining (per cent of taxa that occur in areas with no pH reduction, open square) is reefs, deep-sea systems, high-latitude systems), shown for calcifying taxa (51 taxa total, white circles) and non-calcifying particularly in combination with other anthropo- taxa (71 taxa total, black circles). Atmospheric p CO levels (ppmv CO ) that 2 2 genic environmental changes. Some reshuffl ing of would be required to cause pH changes in ocean surface waters equivalent dominance in phytoplankton communities appears to those observed at three locations along the pH gradient at Ischia are indicated by dotted vertical lines. For calcifi ers (short dashed curve), likely, but it is still not known if the long-term effects non-calcifi ers (long dashed curve), and all taxa combined (solid curve, data of higher ocean CO2 levels will cause a decrease or not shown), exponential regressions explained 99%, 90%, and 88% of the increase in primary production (see Chapter 6 ). If variance, respectively. Fitted regressions indicate a loss of biodiversity of key species in intermediate trophic levels (e.g. the- ~40% for non-calcifi ers and all taxa, and ~70% for calcifi ers, for a pH cosomatous pteropods) are affected either posi- reduction corresponding to the atmospheric p CO2 level expected by 2100. Data from Hall-Spencer et al . ( 2008 ). tively or negatively by ocean acidifi cation, food webs may be destabilized to some extent, perhaps altering the path and effi ciency of energy transfer to chemistry at this site. CO2 mixes as it is advected upper trophic levels. If biodiversity is reduced downstream to produce a spatial gradient in ocean within food webs, it is expected that the productiv- pH from normal (pHT ~8.2) to acidic (pHT ~6.6). ity and predictability of fi sheries will be reduced Hall-Spencer et al. ( 2008 ) documented patterns of ( Worm et al. 2006 ). It is also possible, however, that species richness at sites along the pH gradient cre- a simpler food web structure and potentially higher ated by the venting CO2 , fi nding a general decrease primary production will enable greater trophic in biodiversity with pH for all fl oral and faunal taxa transfer from the base to the top of food webs, examined. Over all taxa, biodiversity declined thereby increasing fi sheries yields. exponentially with pH ( R2 = 0.88; P < 0.001), with a Changes in biodiversity could have important slope indicating a 65% loss in taxa richness for a 1 effects on ecosystem services for society, with the unit decrease in pH (Fig. 10.3 ). Taxa richness for cal- greatest impacts being on island nations which rely cifi ers declined more rapidly with pH than non- heavily on seafood harvests and have less opportu- calcifying taxa with a ~60% loss of species under a nity for agriculture ( Cooley et al. 2009 ). Expected ~0.5 unit pH reduction. Of 12 calcifying algal taxa, declines in coral reefs will affect coastal fi sheries 10 were lost with just a 0.27 unit pH reduction, and as well as tourism, an economic base for many tropi- none were present in the lower-pH sites. Calcifying cal island nations. Reduced calcifi cation, growth, and animals were also less diverse in lower-pH areas, survival of calcifying organisms, especially molluscs, OUP CORRECTED PROOF – FINAL, 08/11/2011, SPi

EFFECTS OF ACIDIFICATION ON MARINE BIODIVERSITY AND ECOSYSTEMS 205 could compromise aquaculture efforts around the Ecologists are now developing innovative methods world, reducing production as demand for seafood to move forward from short-term, single-species rises with population. In addition, negative impacts studies that have provided important information on on larvae could place a greater reliance on cultured species’ responses to ocean acidifi cation, to experi- larvae rather than natural seeding. For example, mental approaches that capture longer-term, ecosys- recent failures of oyster reproduction for both natu- tem-level effects and provide predictions of future ral and cultured larvae in the Pacifi c Northwest ecosystem responses useful for resource managers appear to be linked strongly to low-pH waters ( Feely and other stakeholders (Fig. 10.4 ). The design of et al. 2010 ). Chapter 13 gives a broader discussion of experiments that integrate the effects of multiple the societal impacts of ocean acidifi cation. environmental factors (e.g. warming, ocean acidifi - Will the effects of ocean acidifi cation on ecosys- cation, eutrophication) on population and ecosystem tem function be comparable to those of other anthro- performance is challenging, but is essential to gain pogenic environmental changes? Overfi shing has an understanding of the real-world effects of ocean had very large effects on the distribution and abun- acidifi cation. Multispecies responses to ocean acidifi - dance of marine fi sh communities across the globe cation, in combination with other stressors, may be ( Pauly et al. 2003 ) and, at least at present, is exerting considerably different from results extrapolated from greater infl uence on the function of marine ecosys- single-species, single-factor studies. For example, tems than ocean acidifi cation. In terrestrial systems, experimental approaches that examine linkages the effects of climate change are expected to be sec- between physiological responses to ocean acidifi ca- ond only to land-use changes in the projected rapid tion and long-term organism performance and decline in terrestrial biodiversity by 2100, with activity, particularly in the context of multispecies somewhat smaller effects of elevated CO2 levels interactions would move beyond simpler mechanis- ( Sala et al. 2000 ). Anthropogenic activities including tic studies of physiological performance. A greater fossil fuel emissions, pollutants, and nutrient addi- understanding of the potential for adaptation by tions to coastal and open-ocean waters are all individual species and entire communities are also expected to increase through much of this century important elements of future research programmes. and drive increasingly negative impacts on the Longer-term experiments, preferably including mul- function of ocean ecosystems ( Doney 2010 ). tiple factors and encompassing multispecies com-

High CO2 (Ocean acidification / Warming)

Biogeo- Organism EXPERIMENTS & Behaviour Communities OBSERVATIONS chemistry physiology

Ecosystem PREDICTIONS Populations Biodiversity function

END USERS Ecosystem value Policy Society

Figure 10.4 Integration of ocean acidifi cation research activities. Experimental studies concerning the effects of ocean acidifi cation andwarming, or other environmental changes, on individuals to communities will provide input for understanding and modelling the effects on population processes and ecosystem function. Ultimately, integrated research and outreach will provide information for various stakeholders and society. OUP CORRECTED PROOF – FINAL, 08/11/2011, SPi

206 OCEAN ACIDIFICATION munities, will be essential for examining the effects function of marine ecosystems than other anthropo- of chronic ocean acidifi cation. One important goal of genic activities, but its infl uence in various commu- such studies will be to understand if and how ocean nities is expected to increase as ocean acidifi cation acidifi cation and other anthropogenic environmental intensifi es through this century. In some ecosystems, changes will ultimately affect the function of marine it is possible that ocean acidifi cation, along with communities. Will ocean acidifi cation drive commu- other anthropogenic environmental changes, may nities past ‘tipping points’ with dramatic shifts in alter ecosystem function by reducing biodiversity ecosystem function and ecosystem services, as has and either approaching or potentially crossing eco- been proposed for coral reef systems ( Hoegh- logical tipping points, with unpredictable effects on Guldberg et al. 2007 )? New experimental approaches ecosystem function and services for society. to evaluate the response of organisms to ocean acidifi cation and other concurrent environmental changes and human infl uences, including (1) the potential for 10.9 Acknowledgements acclimatization and adaptation by key taxa, (2) scal- J.P.B. is grateful for support from the David and ing up from individuals to populations, multispecies Lucille Packard Foundation, and to F. Melzner and assemblages, and communities over long timescales W. Fischer who provided important and very help- and in various ecosystems, and (3) effects on energy ful comments on the manuscript. fl ow through marine food webs and the eventual consequences for top predators, including marine fi sheries, will provide society with new tools and References understanding concerning how the resources and Alvarez-Filip, L., Dulvy, N.K., Gill, J.A., Côté, I.M., and services society depends upon may be affected in a Watkinson, A.R. (2009). Flattening of Caribbean coral changing ocean. reefs: region-wide declines in architectural complexity. Proceedings of the Royal Society B: Biological Sciences , 276 , 10.8 Conclusion 3019–25. Barcelos e Ramos, J., Müller, M.N., and Riebesell, U. (2010). Ocean acidifi cation represents a large and very rapid Short-term response of the coccolithophore Emiliania change in the chemistry of the ocean, with the poten- huxleyi to abrupt changes in seawater carbon dioxide tial to affect the biodiversity and function of a vari- concentrations. Biogeosciences , 6 , 177–86. ety of marine ecosystems. Although broad effects of Beardall, J. and Raven, J.A. (2004). The potential effects of global climate change on microalgal photosynthesis, anthropogenic ocean acidifi cation have not yet been growth and ecology. Phycologia , 43 , 26–40. observed, they may be diffi cult to detect amid the Bellwood, D.R., Hughes, T.P., Folke, C., and Nyström, M. infl uence of other factors, and are expected to emerge (2004). Confronting the coral reef crisis. Nature , 429 , and increase through this century. Ocean acidifi ca- 827–33. tion is considered a threat mainly due to the expected Bibby, R., Cleall-Harding, P., Rundle, S., Widdicombe, S., reduction in calcifi cation in various species as the and Spicer, J. (2007). Ocean acidifi cation disrupts pH of ocean waters decreases. Reduced calcifi cation, induced defences in the intertidal gastropod Littorina growth, and survival by corals in coral reef habitats littorea . Biology Letters , 3 , 699–701. and deep-sea coral-dominated communities are Cardinale, B.J., Srivastava, D.S., Duffy, J.E. et al. (2006). expected in response to ocean acidifi cation, with Effects of biodiversity on the functioning of trophic ecosystem-wide impacts due to the indirect effects groups and ecosystems. Nature , 443 , 989–92. Chavez, F.P., Ryan, J., Lluch-Cota, S.E., and Niquen, M. on coral-associated taxa. Shifts in phytoplankton (2003). From anchovies to sardines and back: multidec- communities and intermediate prey groups due to adal change in the Pacifi c Ocean. Science , 299 , 217–21. differential responses to ocean acidifi cation may Cohen, A.L. and Holcomb, M. (2009). Why corals care drive changes in energy fl ow through marine food about ocean acidifi cation: uncovering the mechanism. webs, ultimately infl uencing the productivity and Oceanography , 22 , 117–27. stability of marine fi sheries. Ocean acidifi cation is Collins, S. and Bell, G. (2006). Evolution of natural algal currently considered to have lesser impacts on the populations at elevated CO2 . Ecology Letters, 9 , 129–35. OUP CORRECTED PROOF – FINAL, 08/11/2011, SPi

EFFECTS OF ACIDIFICATION ON MARINE BIODIVERSITY AND ECOSYSTEMS 207

Comeau, S., Gorsky, G., Jeffree, R., Teyssié, J.-L., and sive ‘acidifi ed’ water onto the continental shelf. Science , Gattuso, J.-P. (2009). Impact of ocean acidifi cation on 320 , 1490–2. a key arctic pelagic mollusc (Limacina helicina ). Feely, R.A., Alin, S.R., Newton, J. et al. (2010). The Biogeosciences , 6 , 1877–82. combined effects of ocean acidifi cation, mixing and res- Comeau, S., Jeffree, R., Teyssié, J.-L., and Gattuso, J.-P. piration on pH and carbonate saturation in an urban- (2010). Response of the arctic pteropod Limacina helicina ized estuary. Estuarine, Coastal, and Shelf Science , 88 , to projected future environmental conditions. PLoS One , 442–9. 5 , e11362. Findlay, H.S., Burrows, M.T., Kendall, M.A., Spicer, J.I., Connell, J.H. (1978). Diversity in tropical rain forests and and Widdicombe, S. (2010). Can ocean acidifi cation coral reefs. Science , 199 , 1302–10. affect population dynamics of the barnacle Semibalanus Cooley, S.R., Kite-Powell, H.L., and Doney, S.C. (2009). balanoides at its southern range edge? Ecology , 9 , Ocean acidifi cation’s potential to alter global marine 2931–40. ecosystems services. Oceanography , 22 , 172–81. Fine, M. and Tchernov, D. (2007). Scleractinian coral spe- De’ath, G., Lough, J.M., and Fabricius, K.E. (2009). cies survive and recover from decalcifi cation. Science , Declining coral calcifi cation on the Great Barrier Reef. 315, 1811. Science , 323 , 116–19. Fu, F-X., Warner, M.E., Zhang, Y., Feng, Y., and Hutchins,

Doney, S.C. (2010). The growing human footprint on D.A. (2007). Effects of increased temperature and CO2 coastal and open-ocean biogeochemistry. Science , 328 , on photosynthesis, growth and elemental ratios in 1512–16. marine Synechococcus and Prochlorococcus (cyanobacte- Doney, S.C., Fabry, V.J., Feely, R.A., and Kleypas, J.A. ria). Journal of Phycology , 43 , 485–96.

(2009). Ocean acidifi cation: the other CO2 problem. Gattuso, J.-P., Allemand, D., and Frankignoulle, M. (1999). Annual Review of Marine Science , 1 , 169–92. Photosynthesis and calcifi cation at cellular, organismal Deigweiher, K., Koschnick, N., Pörtner, H.-O., and Lucassen, and community levels in coral reefs: a review on inter- M. (2008). Acclimation of ion regulatory capacities in gills actions and control by carbonate chemistry. American of marine fi sh under environmental hypercapnia. Zoologist , 39 , 160–83. American Journal of Physiology – Regulatory, Integrative and Gazeau, F., Quiblier, C., Jansen, J.M., Gattuso, J.-P., Comparative Physiology , 295 , R1660–R1670. Middelberg, J., and Heip, C.H.R. (2007). Impact of ele-

Duffy, J.E. (2009). Why biodiversity is important to the vated CO2 on shellfi sh calcifi cation. Geophysical Research functioning of real-world ecosystems. Frontiers in Letters , 34 , L07603, doi:10.1029/2006GL028554. Ecology and the Environment , 7 , 437–44. Goffredi, S.K. and Barry, J.P. (2002). Species-specifi c vari- Dupont, S., Ortega-Martinez, O., and Thorndike, M. ation in sulfi de physiology between closely related (2010). Impact of near-future ocean acidifi cation on vesicomyid clams. Marine Ecology Progress Series , 225 , echinoderms. Ecotoxicology , 19 , 449–62. 227–38. Fabry, V.J., Seibel, B.A., Feely, R.A., and Orr, J.C. (2008). Grassle, J.F. (1986). The ecology of deep-sea hydrother- Impacts of ocean acidifi cation on marine fauna and mal vent communities. Advances in Marine Biology , 23 , ecosystem processes. ICES Journal of Marine Science, 65 , 301–62. 414–32. Guinotte, J.M., Orr, J., Cairns, S., Freiwald, A., Morgan, L., Fabry, V.J., McClintock, J.B., Mathis, J.T., and Grebmeier, and George, R. (2006). Will human-induced changes in J.M. (2009). Ocean acidifi cation at high latitudes: the seawater chemistry alter the distribution of deep-sea bellwether. Oceanography , 22 , 160–71. scleractinian corals? Frontiers in Ecology and the FAO (2009). The state of world fi sheries and aquaculture (2008) , Environment , 4 , 141–6. 178 pp. Food and Agriculture Organization of the Hale, R., Calosi, P., McNeill, L., Mieszkowska, N., and United Nations (FAO), Rome, Italy. Widdicombe, S. (in press). Predicted levels of future Feary, D.A., Almany, G.R., McCormick, M.I., and Jones, ocean acidifi cation and temperature rise could alter G.P. (2007). Habitat choice, recruitment and the response community structure and biodiversity in marine ben- of coral reef fi shes to coral degradation. Oecologia , 153 , thic communities. Oikos , 120, 661–674. 727–37. Hall-Spencer, J.M., Rodolfo-Metalpa, R., Martin, S. et al. Feely, R.A., Sabine, C.L., Lee, K. et al. (2004). Impact of (2008). Volcanic carbon dioxide vents show ecosystem

anthropogenic CO2 on the CaCO3 system in the oceans. effects of ocean acidifi cation. Nature , 454 , 96–9. Science , 305 , 362–6. Hays, G.C., Richardson, A.J., and Robinson, C. (2005). Feely, R.A., Sabine, C.L., Hernandez-Ayon, J., Ianson, D. Climate change and marine plankton. Trends in Ecology and Hales, B. (2008). Evidence for upwelling of corro- and Evolution , 20, 337–44. OUP CORRECTED PROOF – FINAL, 08/11/2011, SPi

208 OCEAN ACIDIFICATION

Hendriks, I.E., Duarte, C.M., and Alvarez, M. (2010). Maier, C., Hegeman, J., Weinbauer, M.G., and Gattuso, J.-P. Vulnerability of marine biodiversity to ocean acidifi ca- (2009). Calcifi cation of the cold-water coral Lophelia per- tion: a meta-analysis. Estuarine, Coastal and Shelf Science , tusa under ambient and reduced pH. Biogeosciences , 6 , 86 , 157–64. 1671–80. Hoegh-Guldberg, O., Mumby, P.J., Hooten, A.J. et al. (2007). Manzello, D.P. (2010). Ocean acidifi cation hot spots: spa-

Coral reefs under rapid climate change and ocean acidi- tiotemporal dynamics of the seawater CO2 system of fi cation. Science , 318 , 1737–42. eastern Pacifi c coral reefs . Limnology and Oceanography , Hofmann, G.E., Barry, J.P., Edmunds, P.J. et al. (2010). The 55 , 239–48. effect of ocean acidifi cation on calcifying organisms in Manzello, D.P., Kleypas, J.A., Budd, D.A., Eakin, C.M., marine ecosystems: an organism to ecosystem perspec- Glynn, P.W., and Langdon, C. (2008). Poorly cemented tive. Annual Review of Ecology, Evolution and Systematics , coral reefs of the eastern tropical Pacifi c: possible

41 , 127–47. insights in reef development in a high-CO2 world. Hutchins, D.A., Mulholland, M.R., and Fu, F. (2009). Proceedings of the National Academy of Sciences USA , 105 ,

Nutrient cycles and marine microbes in a CO 2 -enriched 10450–5. ocean. Oceanography , 22 , 128–45. Mayhew, P.J., Jenkins, G.B., and Benton, T.G. (2008). Jablonski, D. and Chaloner, W.G. (1994). Extinctions in the A long-term association between global temperature fossil record. Philosophical Transactions of the Royal Society and biodiversity, origination and extinction in the fossil B: Biological Sciences , 344 , 11–17. record. Proceedings of the Royal Society, B, Biological Kiessling, W., Simpson, C., and Foote, M. (2010). Reefs as Sciences , 275 , 47–53. cradles of evolution and sources of biodiversity in the Melzner, F., Göbel, S., Langenbuch, M., Gutowska, M., Phanerozoic. Science , 327 , 196–8. Pörtner, H.-O., and Lucassen, M. (2009a). Swimming Kleypas, J.A., Buddemeier, R.W., Archer, D., Gattuso, J.-P., performance in Atlantic Cod (Gadus morhua ) following Langdon, C., and Opdyke, B.N. (1999). Geochemical long-term (4–12 months) acclimation to elevated seawa-

consequences of increased atmospheric carbon dioxide ter P co 2 . Aquatic Toxicology , 92 , 30–7. on coral reefs. Science , 284 , 118–20. Melzner, F., Gutowska, M.A., and Langenbuch, M.,

Kleypas, J.A. and Yates, K.K. (2009). Coral reefs and ocean (2009b). Physiological basis for high CO2 tolerance in acidifi cation. Oceanography , 22 , 108–17. marine ectothermic animals: pre-adaptation through Knoll, A.H., Bambach, R.K., Payne, J.L., Pruss, S., and lifestyle and ontogeny? Biogeosciences , 6 , 2313–31. Fischer, W.W. (2007). Paleophysiology and the end-Per- Michaelidis, B., Ouzounis, C., Paleras, A., and Pörtner, mian mass extinction. Earth Planetary Science Letters , 256 , H.O. (2005). Effects of long-term moderate hypercapnia 295–313. on acid-base balance and growth rate in marine mussels Kroeker, K.J., Kordas, R.L., Crim, R.N., and Singh, G.G. Mytilus galloprovincialis . Marine Ecology Progress Series , (2010). Meta-analysis reveals negative yet variable 293 , 109–18. effects of ocean acidifi cation on marine organisms. Micheli, F. and Halpern, B.S. (2005). Low functional redun- Ecology Letters , 13 , 1419–34. dancy in coastal marine assemblages. Ecology Letters , 8 , Kuffner, I.B., Andersson, A.J., Jokiel, P.L., Rodgers, K.S., 391–400. and Mackenzie, F.T. (2008). Decreased abundance of Miles, H., Widdicombe, S., Spicer, J.I., and Hall-Spencer, J. crustose coralline algae due to ocean acidifi cation. (2007). Effects of anthropogenic seawater acidifi cation Nature Geoscience , 1 , 114–17. on acid-base balance in the sea urchin Psammechinus mil-

Kurihara, H. (2008). Effects of CO 2 -driven ocean acidifi ca- iaris. Marine Pollution Bulletin , 54 , 89–96. tion on the early developmental stages of invertebrates. Miller, A.W., Reynolds, A.C., Sobrino, C., and Riedel, G.F.

Marine Ecology Progress Series , 373 , 275–84. (2009). Shellfi sh face uncertain future in high CO2 world: Loreau, M., Naeem, S., Inchausti, P. et al. (2001). Biodiversity infl uence of acidifi cation on oyster larvae calcifi cation and ecosystem functioning: current knowledge and and growth in estuaries. PLoS One , 4 , e5661. future challenges. Science , 294, 804–8. Ohman, M.D., Lavaniegos, B.E., and Townsend, A.W. McLaughlin, P.A. and Rahayu, D.L. (2008). Pteropagurus and (2009). Multi-decadal variation in calcareous holozoo- Catapagurus (Decapoda, Anomura, Paguidae): resource plankton in the California Current system: thecosome sharing or ‘any port in a storm’? Zoosystema , 30 , 899–916. pteropods, heteropods and foraminifera. Geophysical McNeil, B.I. and Matear, R.J. (2008). Southern ocean acidi- Research Letters , 36 , L18608, doi:10.1029/2009GL033901.

fi cation: a tipping point at 450-ppm atmospheric CO2 . Orr, J.C., Fabry, V.J., Aumont, O. et al. (2005). Anthropogenic Proceedings of the National Academy of Sciences USA , 105 , ocean acidifi cation over the twenty-fi rst century and its 18860–4. impact on calcifying organisms. Nature , 437 , 681–6. OUP CORRECTED PROOF – FINAL, 08/11/2011, SPi

EFFECTS OF ACIDIFICATION ON MARINE BIODIVERSITY AND ECOSYSTEMS 209

Pane, E.F. and Barry, J.P. (2007). Ineffi cient acid-base regu- Sala, O.E., Chapin, F.S. III, Armesto, J.J. et al . (2000). Global lation in the deep-sea decapod crab (Chionoecetes tan- biodiversity scenarios for the year 2100. Science , 287 , neri) during short-term hypercapnia. Marine Ecology 1770–4. Progress Series , 334 , 1–9. Seibel, B.A. and Walsh, P.J. (2003). Biological impacts of Pauly, D., Alder, J., Bennett, E., Christensen, V., Tyedmers, deep-sea carbon dioxide injection inferred from indices P., and Watson, R. (2003). The future of fi sheries. Science , of physiological performance. Journal of Experimental 302 , 1359–61. Biology , 206 , 641–50. Pelejero, C., Calvo, E., and Hoegh-Guldberg, O. (2010). Steneck, R.S., Graham, M.H., Bourque, B.J. et al. (2002). Paleo-perspectives on ocean acidifi cation. Trends in Kelp forest ecosystems: biodiversity, stability, resil- Ecology and Evolution , 25 , 332–44. ience and future. Environmental Conservation, 29 , Petchey, O.L. and Gaston, K.J. (2006). Functional diversity: 436–59. back to basics and looking forward. Ecology Letters, 9 , Sydeman, W.J., Hester, M.M., Thayer, J.A., Gress, F., 741–58. Martin, P., and Buffa, J. (2001). Climate change, repro- Pörtner, H-O., Bock, C., and Reipschläger, A. (2000). ductive performance and diet composition of marine Modulation of the cost of pHi regulation during meta- birds in the southern California Current system, 1969– bolic depression: a 31 P-NMR study in invertebrates 1997. Progress in Oceanography , 49 , 309–29. ( Sipunculus nudus ) isolated muscle. Journal of Experimental Tilman, D., Knops, J., Wedin, D., Reich, P., Ritchie, M., and Biology , 203 , 2417–28. Siemann, E. (1997). The infl uence of functional diversity Richardson, A.J., Bakun, A., Hays, G.C., and Gibbons, M.J. and composition on ecosystem processes. Science , 277 , (2009). The jellyfi sh joyride: causes, consequences and 1300–2. management responses to a more gelatinous future. Tittensor, D.P., Baco, A.R., Hall-Spencer, J.M., Orr, J.C., and Trends in Ecology and Evolution , 24 , 213–322. Rogers, A.D. (2010). Seamounts as refugia from ocean Ridgwell, A., Schmidt, D.N., Turley, C et al. (2009). From acidifi cation for cold-waters stony corals. Marine laboratory manipulations to earth system models: pre- Ecology , 31 (Suppl. 1), 212–25. dicting pelagic calcifi cation and its consequences. Tunnicliffe, V., Davies, K.T.A., Butterfi eld, D.A., Embley, Biogeosciences , 6 , 2611–23. R.W., Rose, J.M., and Chadwick, W.W. Jr (2009). Survival Riebesell, U., Schulz, K.G., Bellerby, R.G.J. et al. (2007). of mussels in extremely acidic waters on a submarine

Enhanced biological carbon consumption in a high CO2 volcano. Nature Geoscience , 2 , 344–8. ocean. Nature , 450 , 545–8. Veron, J.E.N. (2008). Mass extinctions and ocean acidifi ca- Ries, J.B., Cohen, A.L., and McCorkle, D.C. (2009). Marine tion: biological constraints on geological dilemmas.

calcifi ers exhibit mixed responses to CO 2 -induced ocean Coral Reefs , 27 , 459–72. acidifi cation. Geology , 37 , 1131–4. Widdicombe, C.E., Eloire, D., Harbour, D., Harris, R.P., Roark, E.B., Guilderson, T.P., Dunbar, R.B., Fallon, S.J., and and Somerfi eld, P.J. (2010). Long-term phytoplankton Mucciarone, D.A. (2009). Extreme longevity in proteina- community dynamics in the western English Channel. ceous deep-sea corals. Proceedings of the National Academy Journal of Plankton Research , 32 , 643–55. of Sciences USA , 106 , 5204–8. Widdicombe, S. and Spicer, J.I. (2008). Predicting the Roberts, D., Howard, W.R., Moy, A.D. et al. (2008). Interannual impact of ocean acidifi cation on benthic biodiversity:

variability of pteropod shell weights in the high-CO2 what can animal physiology tell us? Journal of Southern Ocean. Biogeosciences Discussions , 5 , 4453–80. Experimental Marine Biology and Ecology , 366 , 187–97. Roberts, J.M., Wheeler, A.J., and Freiwald, A. (2006). Reefs Wood, H.L., Spicer, J.I., and Widdicombe, S. (2008). Ocean of the deep: the biology and geology of cold-water coral acidifi cation may increase calcifi cation rates, but at a ecosystems. Science , 312 , 543–7. cost. Proceedings of the Royal Society B: Biological Sciences , Rosa, R. and Seibel, B.A. (2008). Synergistic effects of cli- 275 , 1767–73. mate-related variables suggest future physiological Worm, B., Barbier, E.B., Beaumont, N. et al. (2006). Impacts impairment in a top oceanic predator. Proceedings of the of biodiversity loss on ocean ecosystem services. Science , National Academy of Sciences USA , 105 , 20776–80. 314 , 787–90.