Effects of ocean acidification on marine ecosystems

By Richard Belshaw on 27 August 2010 - 12:20pm

I couldn't attach the pdf, so heres most of the file,

for the full article with graphs, go to www.scirus.com and search

this article appears to be state of the art, however it admits a great ignorance about how acidity or pH affects marine animal reproduction especially fish. I think we can apply common sense and say that beyond a certain point of lowering pH, increasing acidity due to pCO2, it would affect fish reproduction external to their bodies in the breeding grounds, and this point will be different for different species. Similarly because of evolution and punctuated equilibrium and niches, some fish may adapt faster than others, but the change may be too quick for them to successfully adapt to the changing environment. It just tells us that in order to absolutely prevent a crash of marine ecosystems and fish reproduction, we need to reduce pCO2, with the methods outlined in previous posts, and by circumscribing coal use and mining, and getting more efficient transportation methods, and going for locally grown organic food, and refertilizing with minerals the soils of all regions using seaweed or algae, rather than chemical fertilizers.

a google search

pH acidity affecting fish fertilization australia

reveals a japanese pdf about NOx and SOx affects of acid rain on fish fertilization

also it reveals some australian papers

There have also been some tv shows about it in australia.

The news is not good, and likely , for different species, critical thresholds will occur beyond which fertilization is impossible, about pH 6, until then, most species continue to decline in fertilization rate until the tipping point is reached.

Effects of ocean acidification on marine ecosystems Idea: Howard I. Browman
Coordination: Alain F. Vézina, Ove Hoegh-Guldberg
CONTENTS Vézina AF, Hoegh-Guldberg O
Introduction ......................................................
Pörtner HO
Ecosystem effects of ocean acidification in times of ocean warming: a physiologist’s view ......
Hofmann GE, O’Donnell MJ, Todgham AE
Using functional genomics to explore the effects of ocean acidification on calcifying marine organisms .............................................
Rost B, Zondervan I, Wolf-Gladrow D
Sensitivity of phytoplankton to future changes in ocean carbonate chemistry: current knowledge, contradictions and research directions ..................
Balch WM, Fabry VJ
Ocean acidification: documenting its impact on calcifying phytoplankton at basin scales ............
Atkinson MJ, Cuet P
Possible effects of ocean acidification on coral reef biogeochemistry: topics for research ..............199–201
203–217
219–225
227–237
239–247
249–256
Lough JM
Coral calcification from skeletal records revisited............................................................
Andersson AJ, Mackenzie FT, Bates NR
Life on the margin: implications of ocean acidification on Mg-calcite, high latitude and cold-water marine calcifiers ...........................
Kurihara H
Effects of CO2-driven ocean acidification on the early developmental stages of invertebrates ...
Dupont S, Havenhand J, Thorndyke W, Peck L, Thorndyke M Near-future level of CO2-driven ocean acid- ification radically affects larval survival and development in the brittlestar Ophiothrix fragilis ...
Ishimatsu A, Hayashi M, Kikkawa T
Fishes in high-CO2, acidified oceans .....................
Gutowska MA, Pörtner HO, Melzner F
Growth and calcification in the cephalopod Sepia officinalis under elevated seawater pCO2 .....257–264
265–273
275–284
285–294 295 – 302
303 – 309
Resale or republication not permitted without written consent of the publisher
Introduction
Alain F. Vézina1,*, Ove Hoegh-Guldberg2
1Bedford Institute of Oceanography, 1 Challenger Drive, Dartmouth, Nova Scotia B2Y 4A2, Canada 2Centre for Marine Studies, The University of Queensland, St. Lucia, Queensland 4067, Australia
Although the potential for increased atmospheric CO2 concentrations to affect ocean pH and marine calcifica- tion rates has been known for decades, the issue came to the fore following the Ocean in a High CO2 World sym- posium (Orr et al. 2005a). Ocean acidification has recently been the subject of several high-profile publications (Caldeira & Wickett 2003, Orr et al. 2005b), comprehen- sive priority-setting assessments (Royal Society 2005,
Kleypas et al. 2006), and numerous articles in the mass media. Despite the serious implications of ocean acid- ification for marine ecosystems, thorough scientific investigation of this problem is only just beginning.
It is accepted that average global ocean pH has declined over the 20th century and will continue to do so within the near future (Caldeira & Wickett 2005). It is also generally accepted that the pH in the global
*Email: alain.vezina@dfo-mpo.gc.ca
© Inter-Research 2008 · www.int-res.com
200   Mar Ecol Prog Ser 373: 199–201, 2008
ocean has already fallen by 0.1 units and is likely to fall a further 0.3 units by 2050 and 0.5 units by 2100 (Caldeira & Wickett 2005). These predictions are rela- tively certain, in part because the geological feedbacks that could affect the decline in pH are too slow to have any real effect on a century timescale. The potential effects of this decline in pH, however, on marine organisms and ecosystems are poorly understood. We felt that it was worthwhile at this early stage to assem- ble articles that critically evaluate the current state of knowledge on this topic and make constructive sug- gestions for future research.
Past work on the biological effects of change in ocean pH has focused on acute exposure, rather than on slow and continuous decline in pH levels such as those expected under global climate change. Without an understanding of how such a slow and continuous decline in pH is likely to affect ocean ecosystems, we may miss important aspects of this global ocean pH change. To compound this uncertainty, recent research (Iglesias-Rodriguez et al. 2008, Gutowska et al. 2008, this Theme Section [TS]) reveals counter-intuitive, pos- itive/neutral effects of acidification on some organisms and processes. These studies highlight a near uni- versal issue arising in studies of broad environmental problems: that is, the diversity and complexity of re- sponses by organisms make it difficult to form general predictions.
Faced with this complexity, the first article in this TS proposes a bold program which focuses on unraveling the fundamental physiological processes that underpin the diversity of observed responses (Pörtner 2008, this TS). The proposal for a focus on physiology will not necessarily meet with universal agreement; neverthe- less, a deeper understanding of ocean acidification at a physiological level is essential for progress in under- standing impacts that extend beyond the effects on calcification. It is also stimulating to reflect on potential unifying principles that may underlie organisms’ re- sponses to temperature, CO2 and oxygen, and thus affect community structure. This approach already leads to the inference that higher invertebrates and other organisms with high metabolism and well-devel- oped acid/base regulation may withstand acidification better than the lower invertebrates (see Ishimatsu et al. 2008, this TS, Gutowska et al. 2008).
Using functional genomics is another way to derive an increased mechanistic understanding of responses to acidification. This in turn can lead to more general understandings as outlined by Hofmann et al. (2008, this TS). Although the focus of their paper is on labora- tory studies of biomineralization, the approach could be applied to other potential physiological responses and could lead to diagnostic tools that can be used in the field (DeLong & Karl 2005).
Rost et al. (2008, this TS) review the methodologies that have been used to date to investigate effects of pH on phytoplankton. They report that differences in experimental design and methods may underlie the sometimes contradictory results. Importantly, these authors provide a framework for future experimental studies that may help eliminate these problems. Shift- ing from the laboratory to the field, Balch & Fabry (2008, this TS) review current approaches to estimate changes in pelagic calcification in situ and propose a program to quantify the effects of acidification on cal- cification on the global scale.
Most of the research to date on the effects of ocean acidification has focused on calcifying organisms, in particular structure-forming organisms such as corals. The rise of CO2 in ocean waters leads to more corrosive conditions for calcifying organisms, making it more difficult for them to build and maintain their carbonate skeletons. Also, the threatened status and ecological importance of coral reefs inevitably brings attention to their responses to acidification. It is widely recognized that the saturation state of carbonates has a major in- fluence on calcification at species and community lev- els (Kleypas & Langdon 2006). Atkinson & Cuet (2008, this TS), however, point out a number of biological and ecological factors that can influence this relationship and propose a research program to address the uncer- tainties. Lough (2008, this TS) discusses the recent shift from growth-based indicators towards geochemical indicators of coral response to environmental condi- tions, and makes the point that growth records remain a rich source of information and should not be forgot- ten in the continuing investigation of coral response to acidification and temperature changes. Andersson et al. (2008, this TS) combine a review of extant knowl- edge and model calculations to predict faster than expected changes in community structure, particularly at high latitudes, linked mainly to the differences in solubility among different forms of carbonate skele- tons. These papers together illustrate that much re- mains to be done, even in the best-studied part of the acidification puzzle.
Comparatively little attention has been devoted to the impact of acidification on other ecosystem compo- nents and processes. A critical question here is the potential effect of acidification on early life stages of marine invertebrates. These larval and juvenile stages may be particularly sensitive, in part because they form their internal skeletons out of amorphous calcite which is more soluble than other forms of carbonate. Kurihara (2008, this TS) reviews the current state of knowledge on the effects of acidification on the repro- duction and early life stages of marine invertebrates, to reveal just how little we know about this crucial issue, and to sketch a way forward. Dupont et al. (2008,
Vézina & Hoegh-Guldberg: Introduction to Theme Section on ocean acidification   201
this TS) offer disquieting evidence that populations of a major keystone species of the North Atlantic may be severely disrupted through the effects of probable future acidification levels on its larval stages. The im- pact of ocean acidification on marine fish is reviewed by Ishimatsu et al. (2008) who identify the scarcity of studies using realistic pH levels under conditions of prolonged exposure, and urge new research along these lines. The TS closes with a paper by Gutowska et al. (2008) which reports counter-intuitive responses of a cephalopod species to very high CO2 levels, neatly illustrating the deep uncertainties within this major environmental issue.
This TS covers a broad range of issues, approaches and taxonomic groups, but there were certainly areas we were not able to cover. Many authors discuss the potential for genetic adaptation to rapid ocean acid- ification, and this remains a topic of great importance; however, little progress has been made in this path of research. There are few analyses based on evolution- ary thinking (although the study of Collins & Bell 2004 is often cited). Another gap is the integration of the information into models that can help us apprehend higher levels (community, ecosystem) responses to acidification. There is still uncertainty as to what types of models and modeling studies are needed to inte- grate extant knowledge and extrapolate possible future states of the ecosystem; whether it is just a ques- tion of adding incrementally to the existing ecological- biogeochemical models used extensively for global change research (Hood et al. 2006), or whether we need new approaches or different model structures. Interestingly, these are also gaps that were identified in the recent reports to the Royal Society and US fund- ing agencies (Royal Society 2005, Kleypas et al. 2006). Hopefully, the next reviews and syntheses of this rapidly evolving field will include more work in these critical areas.
Acknowledgements. Special thanks are due to Howard Brow- man who came up with the original idea for this TS, helped launch the process and participated actively in the coordina- tion and editing in the early phases. This would not have hap- pened without his foresight and leadership. We thank the authors and over 45 reviewers who were willing to participate and made this TS possible.
LITERATURE CITED
Andersson AJ, Mackenzie FT, Bates NR (2008) Life on the margin: implications of ocean acidification on Mg-calcite, high latitude and cold-water marine calcifiers. Mar Ecol Prog Ser 373:265–273
Atkinson MJ, Cuet P (2008) Possible effects of ocean acidifica- tion on coral reef biogeochemistry: topics for research. Mar Ecol Prog Ser 373:249–256
Balch WM, Fabry VJ (2008) Ocean acidification: documenting its impact on calcifying phytoplankton at basin scales. Mar Ecol Prog Ser 373:239–247
Caldeira K, Wickett ME (2003) Anthropogenic carbon and ocean pH. Nature 425:365–365
Caldeira K, Wickett ME (2005) Ocean model predictions of chemistry changes from carbon dioxide emissions to the atmosphere and ocean. J Geophys Res 110, C09S04, doi: 10.1029/JC002671
Collins S, Bell G (2004) Phenotypic consequences of 1,000 generations of selection at elevated CO2 in a green alga. Nature 431:566–569
DeLong EF, Karl DM (2005) Genomic perspectives in micro- bial oceanography. Nature 437:336–342
Dupont S, Havenhand J, Thorndyke W, Peck L, Thorndyke M (2008) Near-future level of CO2-driven ocean acidification radically affects larval survival and development in the brittlestar Ophiothrix fragilis. Mar Ecol Prog Ser 373: 285–294
Gutowska MA, Pörtner HO, Melzner F (2008) Growth and calcification in the cephalopod Sepia officinalis under ele- vated seawater pCO2. Mar Ecol Prog Ser 373:303–309
Hofmann GE, O’Donnell MJ, Todgham AE (2008) Using func- tional genomics to explore the effects of ocean acidifica- tion on calcifying marine organisms. Mar Ecol Prog Ser 373:219 – 225
Hood RR, Laws EA, Armstrong RA, Bates NR and others (2006) Pelagic functional group modeling: progress, chal- lenges and prospects. Deep-Sea Res II 53:459–512
Iglesias-Rodriguez MD, Halloran PR, Rickaby REM, Hall IR and others (2008) Phytoplankton calcification in a high- CO2 world. Science 320:336–340
Ishimatsu A, Hayashi M, Kikkawa T (2008) Fishes in high- CO2, acidified oceans. Mar Ecol Prog Ser 373:295–302 Kleypas JA, Langdon C (2006) Coral reefs and changing
seawater chemistry. In: Phinney JT, Hoegh-Guldberg O, Kleypas J, Skirving W, Strong A (eds) Coral reefs and cli- mate change: science and management. AGU Monograph Series, Coast Estuar Stud 61:73–110
Kleypas JA, Feely RA, Fabry VJ, Langdon C, Sabine CL, Rob- bins LL (2006) Impacts of ocean acidification on coral reefs and other marine calcifiers: a guide for future research. Report of a workshop held 18–20 April 2005, St. Peters- burg, FL, sponsored by NSF, NOAA, and the US Geo- logical Survey
Kurihara H (2008) Effects of CO2-driven ocean acidification on the early developmental stages of invertebrates. Mar Ecol Prog Ser 373:275–284
Lough JM (2008) Coral calcification from skeletal records revisited. Mar Ecol Prog Ser 373:257–264
Orr JC, Pantoja S, Pörtner HO (2005a) Introduction to special section: The ocean in a high-CO2 world. J Geophys Res 110, C09S01, doi:10.1029/2005JC003086
Orr JC, Fabry VJ, Aumont O, Bopp L and others (2005b) Anthropogenic ocean acidification over the twenty-first century and its impacts on calcifying organisms. Nature 437:681 – 686
Pörtner HO (2008) Ecosystem effects of ocean acidification in times of ocean warming: a physiologist’s view. Mar Ecol Prog Ser 373:203–217
Rost B, Zondervan I, Wolf-Gladrow D (2008) Sensitivity of phytoplankton to future changes in ocean carbonate chemistry: current knowledge, contradictions and research directions. Mar Ecol Prog Ser 373:227–237
Royal Society (2005) Ocean acidification due to increasing atmospheric carbon dioxide. Policy Document 12/05. The Clyvedon Press, Cardiff
MARINE ECOLOGY PROGRESS SERIES Mar Ecol Prog Ser
Vol. 373: 203–217, 2008
doi: 10.3354/meps07768
Contribution to the Theme Section ‘Effects of ocean acidification on marine ecosystems’
Ecosystem effects of ocean acidification in times of ocean warming: a physiologist’s view
Hans-O. Pörtner*
Alfred Wegener Institute for Polar and Marine Research, Marine Animal Physiology, Postfach 12 01 61, 27515 Bremerhaven, Germany
ABSTRACT: Ocean warming and acidification occur at global scales and, in the case of temperature, have already caused shifts in marine ecosystem composition and function. In the case of CO2-induced ocean hypercapnia and acidification, however, effects may still be so small that evidence for changes in the field is largely lacking. Future scenarios indicate that marine life forms are threatened by the specific or synergistic effects of factors involved in these processes. The present paper builds on the view that development of a cause and effect understanding is required beyond empirical observa- tions, for a more accurate projection of ecosystem effects and for quantitative scenarios. Identification of the mechanisms through which temperature- and CO2-related ocean physicochemistry affect organism fitness, survival and success, is crucial with this research strategy. I suggest operation of unifying physiological principles, not only of temperature but also CO2 effects, across animal groups and phyla. Thermal windows of optimized performance emerge as a basic character defining species fitness and survival, including their capacity to interact with other species. Through effects on perfor- mance at the level of reproduction, behaviour and growth, ocean acidification acts especially on lower marine invertebrates, which are characterized by a low capacity to compensate for distur- bances in extracellular ion and acid–base status and sensitivity of metabolism to such disturbances. Available data suggest that one key consequence of these features is a narrowing of thermal toler- ance windows, as well as a reduced scope for performance at ecosystem level. These changes in bioenvelopes may have major implications for the ranges of geographical distribution of these organ- isms and in species interactions.
KEY WORDS: Ocean acidification · Global change · Temperature effects · Calcification · Metabolic performance · Acclimation · Ecosystems · Hypoxia
Resale or republication not permitted without written consent of the publisher
Published December 23
OPEN ACCESS
TTEMPERATURE AND CO2 SHAPING MARINE ECOSYSTEMS
The oceans cover 70% of the earth’s surface. Due to their large volume and the ability of seawater to buffer CO2, oceans have absorbed approximately half of all anthropogenic CO2 emissions to the atmosphere, which amounts to more than 120 Gt C in total or 440 Gt CO2 (Sabine et al. 2004) within the last 200 yr. CO2 produced by human activities penetrates into the surface layers of the ocean and is transported by ocean currents to deeper waters. At present, the oceans take up about 2 of the 6 Gt C per annum from human activity. In this context, the contribution of ocean biology to CO2 up-
take is similarly large as that of the terrestrial bios- phere. However, the ability of the ocean to take up CO2 decreases with increasing atmospheric CO2 concentra- tions due to the reduced buffering ability of seawater as CO2 accumulates. The present increase in CO2 levels in the atmosphere is approximately 100-fold faster than at the end of the last ice ages when CO2 levels rose by about 80 ppm over 6000 yr (IPCC 2001, 2007). Now ex- ceeding 380 ppm, the present CO2 content is the high- est in the atmosphere for the last 420 000 and possibly more than 10 million yr (IPCC 2001, 2007).
Ecosystem effects of CO2 accumulation and their interaction with effects of warming, eutrophication, and hypoxia are attracting increasing international at-
*Email: hans.poertner@awi.de
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204   Mar Ecol Prog Ser 373: 203–217, 2008
tention (Cicerone et al. 2004a,b, Orr et al. 2005, based on the UNESCO symposium ‘Oceans in a High CO2 World’, http://ioc.unesco.org/iocweb/co2panel/ HighOceanCO2.htm, or a corresponding discussion in the context of OSPAR, www.ospar.org/documents/ dbase/publications/p00285_Ocean acidification.pdf, see also www.ocean-acidification.net). Once atmo- spheric CO2 levels increase, the amount of CO2 physi- cally dissolved in the water follows in accordance with Henry’s Law. Distribution kinetics and equilibria are modified by biological processes such as respiration and photosynthesis. In physical equilibrium CO2 reaches concentrations which are similar in the 2 media due to the similar ‘solubilities’ in water and air. Incre- ments in aquatic CO2 levels cause associated changes in   water   physicochemistry   or   acid – base   status,   which have been detectable in upper ocean layers for some decades (Chen & Millero 1979, Brewer et al. 1997, IPCC 2007). The CO2 budget of the ocean comprises about 1% physically dissolved CO2, including H2CO3, as well as   about   91 %   bicarbonate   (HCO3–)   and   about   8 %   car- bonate (CO32–). Model calculations revealed that in comparison with pre-industrial times, the accumulation of CO2 in 1996 had already caused a pH decrease be- yond 0.1 units equivalent to an increase of H+ ion activ- ity by 30% in the surface ocean (Haugan & Drange 1996). With the continued use of fossil fuels, atmos- pheric CO2 concentrations are expected to rise from current 380 ppm (pCO2 = 380 μatm) to more than 750 ppm (IPCC scenario IS92a; Houghton et al. 2001) or even more than 1000 ppm (Royal Society 2005) in 2100 and will climb to more than 1500 ppm (pCO2 = 1500 μatm) between 2100 and 2200 (e.g. Wigley et al. 1996). This will lead to a pH reduction in the upper ocean layers by 0.3 to 0.5 units up to 2100 (Zeebe & Wolf- Gladrow 2001, Caldeira & Wickett 2005). Acidification of the surface water by up to 0.77 pH units is finally expected if values of atmospheric CO2 achieve levels of 1900 ppm by 2300 (Caldeira & Wickett 2003).
Due to this high storage capacity, the ocean at first appeared to be a suitable place for the disposal of CO2, either directly, via diffusive entry or industrial scale deep-sea release, or indirectly, via iron fertilization, consecutive net particle export and CO2 release during deep-sea respiration. However, CO2 develops specific effects on marine life which exclude or at least limit the ocean’s use as a solution to rising atmospheric CO2 concentrations. This impact is exacerbated when com- bined with temperature extremes, potential problems of oxygen deficiency that arise from global warming, eutrophication, or potential CO2 disposal strategies through iron fertilization (Pörtner et al. 2005). Effects go beyond the potential changes in the fluxes of car- bon or nutrients which still require investigation (Riebesell et al. 2007).
The current trend of increasing atmospheric CO2 is accompanied by regional changes in other climatic factors, primarily temperature and its variability (IPCC 2001, 2007). Global warming alone has already affected the geographical distribution of aquatic and terrestrial animals with enhanced risk of local extinc- tion of species or even ecosystems, in the case of coral reefs (Parmesan & Yohe 2003, Thomas et al. 2004, Perry et al. 2005, Hoegh-Guldberg 2005). Within con- ditions set by geomorphology, ocean currents, water depth and stratification or salinity, large scale geo- graphical distribution of marine animals is shaped decisively by temperature. Depending on the level of mobility and tolerance windows for physical factors, organisms can achieve particular geographical ranges. Mode of life (e.g. passive versus active) in relation to living conditions, food supply or competition for food, are additional factors shaping the final biogeography of individual species and the functional structure of communities in open water (pelagic) and on the bottom (benthic). These considerations also apply for repro- ductive stages (eggs or sperm) as well as adult phases of the life cycle. It is clear, however, that the tolerances to climate-related factors might be very different between larvae and adult organisms (e.g. pelagic lar- vae versus benthic adults) as well as between species, thereby influencing species interactions within ecosys- tems. It is also important to point out that the future distribution of organisms also depends on how fast required habitats are being changed by climate change and how fast a species can spread and follow a changing climate. In some cases organisms may migrate, or be dispersed through reproductive stages. At this point geographical barriers such as deep-sea trenches or currents (e.g. the circum-Antarctic current) may become important (Thatje et al. 2005). Overall, the physiological principles setting performance, on the one hand, and climate dependent ecological patterns, on the other hand, may be more intertwined than tra- ditionally thought (Pörtner & Farrell 2008).
The importance of combined temperature and CO2 effects, and the limited capacities of marine organisms (from microbes to phytoplankton to animals) to accli- matize or adapt to elevated CO2 concentrations, is illustrated through current discussions of a pivotal role played by CO2 and temperature oscillations in mass extinction   events,   e.g.   during   the   Permian – Triassic (Knoll et al. 1996, 2007, Bambach et al. 2002, Berner 2002, Pörtner 2004, Pörtner et al. 2005). The course of evolutionary history might thus have been decisively influenced by atmospheric and aquatic CO2 concentra- tions. It is conceivable that the evolution of very mobile marine life-forms became possible in geological his- tory only with the decrease in atmospheric CO2 levels. CO2 levels in the Cambrian atmosphere ranged up to
about 0.5% (i.e. a pCO2 of 0.5 kPa or 5000 μatm). Aver- age atmospheric levels fell more or less continuously in the following phases of earth history (cf. Dudley 1998, Berner 2002). Cornette et al. (2002) suggested that the level of atmospheric CO2 concentrations influenced the rate of speciation in the sea, however, mechanisms and time scales involved are unclear.
Currently, CO2 is an abiotic factor which can vary strongly in some marine habitats. It remains constant in large stretches of the open ocean but will oscillate considerably where excessive metabolic or photosyn- thetic activities occur and where gas exchange with the atmosphere or open sea is at least periodically con- strained. CO2 absorption is increased by increasing solubility at low water temperatures, whereas warm- ing favours CO2 release. Variable values of pH and CO2 partial pressure in the seawater are therefore linked with water temperatures, ocean currents, CO2 consumption due to photosynthetic activity at the sea surface or by oxygen demand arising from high con- tents of organic materials in deeper layers. The latter is also causal in the formation of hypoxic layers in the oceans. Correspondingly, CO2 partial pressure rises and water pH falls progressively in seawater in the course of large-scale deep-ocean currents (‘conveyor belt’) from the North Atlantic to the North Pacific. In the oxygen minimum zones of the North Pacific, CO2 partial pressures of 1200 μatm result and contrast with corresponding values of 500 μatm in the North Atlantic (Millero 1996). CO2 partial pressures are increased and pH values reduced at the surface of upwelling zones (e.g. Feely et al. 2008). This trend is exacerbated when the water is warming. Starting out from a slightly alka- line pH of 8.2 at the surface, a pH variability of more than ±0.3 pH units can result depending on region, season and phytoplankton activity (Hinga 2002).
The classic example of short term CO2 oscillations is seen in the rock pools of the intertidal zone where res- piration dominates by night and the consumed oxygen is replaced by accumulating CO2 (Truchot & Duhamel- Jouve 1980, Morris & Taylor 1983). In the same pools, low tide in the middle of the day is characterised by excessive photosynthetic activity relative to respira- tion, and the precipitous drop in CO2 concentrations and increase in pH.
Water CO2 content also fluctuates in marine sedi- ments (e.g. at low tide) or in hypoxic bottom waters if high levels of organic material elicit increased oxygen consumption and finally anaerobic metabolism of bac- teria, meio- and macrofauna in surroundings where the exchange with surface waters is low. CO2 partial pressures of 1.60 kPa (16 000 μatm) are conceivable in anoxic environments (Knoll et al. 1996.). Deep-sea areas are anoxic in the Black Sea because no lateral oxygen import by ocean currents takes place. In other
oceans where the deep sea is oxygenated and supports animal life, special habitats have developed at hydro- thermal vents where the water is enriched with CO2 due to volcanic activity. High CO2 partial pressures of 8.00 kPa have been measured (80000 μatm) and are exploited by hydrothermal fauna like the Vestimen- tifera (giant tube worms) during CO2 fixation by their symbiotic bacteria (Childress et al. 1993).
Overall, marine animal life has adapted and possibly specialized in a range of ambient CO2 conditions, from the high concentrations found at deep sea vents to the widely fluctuating levels typical of the intertidal zone. Certain life forms have also specialised to live in the permanently low CO2 levels in the open ocean. These adaptive responses likely partially define the extent to which a species reacts sensitively to the progressively higher CO2 levels of the future.
There are few field observations of specific CO2 effects associated with climate dependent phenomena in marine ecosystems. Such phenomena have fre- quently been related to temperature effects. Even the decreasing calcification rates over the last decades in coral reefs have not been clearly explained and may be caused by combined temperature and CO2 effects (Cooper et al. 2008). Oscillating calcification rates in phytoplankton during the anthropocene (Iglesias- Rodriguez et al. 2008), palaeo-records during glacial to interglacial periods (Barker & Elderfield 2002) or mass extinction   events,   such   as   during   the   Permian – Triassic period (Knoll et al. 1996, 2007) are being discussed as related to specific CO2 effects. In all of these phenom- ena temperature is again a crucial factor. Current statements concerning the effects of CO2 on marine organisms and ecosystems are therefore largely based on experimental studies in the laboratory or in meso- cosms. Moreover, experiments at volcanic sites or after experimental release of CO2 into the deep sea have investigated specific CO2 effects. Experimental studies that explore the effect of CO2 at ecosystem level are also few, except for recent studies in mesocosms which focus on primary production and the export of organic material (Riebesell et al. 2007) or on nutrient flux in sediments (Widdicombe & Needham 2007) and on cal- cification as well as community changes in coral reefs (Jokiel et al. 2008).
The current situation is also characterized by a large uncertainty in assessing the role of ocean hypercapnia and acidification in the context of climate change effects on marine ecosystems. This uncertainty mirrors the insufficient consideration of a mechanistic cause and effect understanding which has also been empha- sized in the context of interpreting climate-induced ecosystem change in general (cf. Jensen 2003). The present paper is intended to provide a perspective on the physiological mechanisms involved in effects of
Pörtner: Ecosystem effects of ocean acidification   205
206   Mar Ecol Prog Ser 373: 203–217, 2008
ocean acidification, in the context of rising tempera- tures and higher frequencies of hypoxia events. Such research may benefit from recent progress in the field of thermal biology, where organismal limitations in response to temperature could recently be identified as being responsible for warming-induced ecosystem level changes in the abundance and well-being of a species (Pörtner & Knust 2007).
PHYSIOLOGICAL PRINCIPLES OF CO2 VS. TEMPERATURE EFFECTS ON MARINE ANIMALS
Similar to thermal effects (Pörtner 2002), CO2 effects may extend from the highest level of sensitivity seen in whole organism functioning, down to cellular and mol- ecular levels, reflecting a systemic to molecular hier- archy of tolerance limits. This emphasizes that complex macro-organisms specialize more on environmental parameters and thus respond more sensitively to envi- ronmental extremes than unicellular eukaryotes and much more so than prokaryotes (Pörtner 2002).
The integration of molecular and biochemical mech- anisms into whole organism functional networks and their performance capacity is thus a crucial element in understanding cause and effect visible at an ecosystem level. This requires knowledge of the molecular and cellular mechanisms of CO2 effects and their whole organism consequences, and in this context, know- ledge of the mechanistic links between CO2-depen- dent functional levels from molecule to ecosystem.
As for other environmental factors, unifying princi- ples of CO2 effects across groups of organisms (e.g. animal phyla, phytoplankton species) need to be dis- tinguished from those possibly specific and typical for certain groups. This applies particularly to the different physiological strategies (e.g. extracellular versus intracellular blood pigments, open versus closed circulatory systems) displayed by various ani- mal phyla. Such physiological studies of CO2 effects, via development of a cause-and-effect understand- ing, will support the development and assessment of predictive scenarios of ecosystem changes (Cicerone et al. 2004a,b, Orr et al. 2005, Royal Society 2005, Pörtner & Farrell 2008).
Realistic scenarios also require integrated analyses of effects of CO2, temperature and oxygen deficiency since all of these factors change concomitantly in the real world and their effects influence each other (Rey- naud et al. 2003, Hoegh-Guldberg 2005, Pörtner et al. 2005, Hoegh-Guldberg et al. 2007, Pörtner & Farrell 2008). According to the postulated central role of phys- iology, the principles of CO2 effects thus have to be evaluated in the light of interacting temperature (and hypoxia) effects.
Future scenarios of CO2 effects require consideration that on macro-ecological scales, the distribution of marine fish and invertebrates is strongly defined by temperature gradients (Murawski 1993, Jacob et al. 1998). These observations reflect that complex macro- organisms are specialized for a certain window of bio- climate. They also emphasize the fact that the thermal windows of species in an ecosystem differ despite the fact that they overlap at those temperatures where species coexist. The loss or replacement of a species in a community may therefore relate to the climate- driven change in its geographical distribution since species would follow their preferred thermal niches. Changes in occurrence then become predictable from the temperature regime (Pearson & Dawson 2003). The respective ‘climate envelope models’ were successfully applied in the terrestrial realm and are currently con- sidered to be the best approach in determining the effects of climate change on biodiversity (Huntley et al. 2004).
In this context, mechanistic knowledge is needed to explain the specialization of organisms on limited and specific thermal windows. Considerable progress has been made in the field of thermal biology, where rele- vant physiological mechanisms defining thermal win- dows and linking climate to ecosystem change have been identified (Pörtner 2001, 2002, Pörtner & Knust 2007). The principles involved even lead to explana- tions of regime shifts, changes in species interaction and food web structure (Pörtner & Farrell 2008). Although it is currently unclear whether windows of CO2 tolerance exist in similar ways to thermal win- dows, conventional physiological knowledge has many examples of such specialization. Defence mech- anisms against hypo- or hypercapnia effects on acid – base   status   exist   within   groups   from   different CO2 environments (see previous section). Circumstan- tial observations indicate higher sensitivity to hypo- capnia of fauna living in marine sediments as com- pared to epibenthic or pelagic fauna. This line of thought is also supported by shifting CO2 windows during evolution of air breathing ectotherms from water breathers (Ultsch 1987) and furthermore of endotherms from ectotherms.
STRATEGIES FOR PHYSIOLOGICAL RESEARCH
How should one go about studying specific CO2 effects and then integrate these findings with studies of temperature and hypoxia effects? In physiology, lab- oratory studies apply defined scenarios of environmen- tal parameters and are used to identify the mecha- nisms causing changes at molecular to organismic levels of biological organization. For a clear elabora-
Pörtner: Ecosystem effects of ocean acidification   207
Fig. 1. Mortality in animals corresponding to exposure time and concentration of ambient CO2 (conceptual considera- tions, after Pörtner et al. 2005). Priorities among effective mechanisms in causing mortality likely shift between short- term exposure to high concentrations (hampering oxygen supply) versus long-term exposure to low concentrations (hampering growth and reproduction). Acclimation and evo- lutionary adaptation cause a shift in steepness and position of the sensitivity curve (broken arrows). Sensitivity likely differs between species such that ecosystem shifts may develop progressively rather than suddenly beyond thresholds
tion of effects and mechanisms involved, extreme con- ditions are applied first, before intermediate values of environmental parameters are tested. For example, this strategy was used to characterize the effects of anoxia and hypoxia effects on marine animals, such as invertebrates dwelling in the intertidal zone (for re- view see Grieshaber et al. 1994). Although full, long- term anoxia is experienced by few of these facultative anaerobes, anoxia exposure was used to identify the biochemical mechanisms, their capacities and the ATP yield of anaerobic energy production. Consecutive studies then explored the relevance and use of these mechanisms in more moderate and more realistic levels of hypoxia under field conditions.
In the case of CO2, earlier physiological work used levels of 10 000 ppm and higher in aquatic (including marine) animals as a tool to challenge and investigate the mechanisms of acid–base regulation, as well as their capacity to compensate for acid–base distur- bances (e.g. Heisler 1986a,b). In this context, the ques- tion arose as to what extent CO2 is effective as a vari- able natural factor in various aquatic environments (see above) and whether it has ecologically relevant effects, such as in metabolic depression (e.g. during low tide) (Reipschläger & Pörtner 1996, Burnett 1997, Pörtner et al. 1998). A perspective emerged of how CO2 oscillations on longer time scales might have been involved in mass extinction events in earth history (Pörtner et al. 2004, 2005, Knoll et al. 2007). These studies also became relevant from an applied point of view, namely as a guideline for assessment of environ- mental impact of projected ocean storage scenarios, as compiled in the IPCC special report on carbon capture and storage (Caldeira et al. 2006). Such scenarios of ocean disposal involve local effects of CO2 on marine organisms and ecosystems at levels similar to those used in earlier physiological work. Present knowledge of such effects contributed to the recent banning by OSPAR (Oslo-Paris Commission, www.ospar.org) in 2007 of CO2 placement strategies in the water column or on the sea bed.
In contrast, scenarios of anthropogenic ocean acidifi- cation from atmospheric CO2 release involve much lower CO2 levels and, therefore, long term rather than acute effects (cf. Pörtner et al. 2005) (Fig. 1). Nonethe- less, for a clear and comprehensive identification of the mechanisms and of the detailed regulatory pathways involved in responding to CO2, the use of high concen- trations is still required, especially given the limited time frame of experimental studies. Consecutively, various CO2 levels need to be applied including, but also beyond, those expected from CO2 accumulation scenarios, in order to find out when effects set in and why and to what extent such mechanisms respond to the relatively low concentrations involved. It is also
important to consider whether such effects occur over short or long time scales and also, whether they can be compensated for during acclimation or adaptation processes.
These considerations put into perspective claims that previous investigations are invalid because they have used high CO2 levels that are beyond expected scenar- ios of ocean acidification. This criticism would imply that a completely different picture might develop once effects of ‘realistic’ values are being studied. From an empirical point of view the exclusive study of expected CO2 accumulation scenarios appears sufficient, how- ever, the identification of some mechanisms above noise levels will rely on the use of higher concentra- tions. While some processes such as calcification may well begin to show clear early effects even under low levels, others such as protein synthesis may also be affected, but significant changes may not yet be detectable during limited experimental periods or for methodological reasons (cf. Langenbuch et al. 2006). Since protein synthesis is involved in growth, demon- stration of this effect (e.g. Michaelidis et al. 2005) and identification of the mechanisms causing reduced pro- tein synthesis are crucial for an understanding of CO2 effects. For any mechanism, clear-cut and significant effects should develop on relatively short time scales under a high CO2 regime.
208   Mar Ecol Prog Ser 373: 203–217, 2008
Mechanisms responsive to low CO2 levels will also respond to high levels, albeit to different degrees and on different time scales (Pörtner et al. 2005). At present there is no evidence of mechanisms which exclusively respond to low CO2 levels and thus escape identifica- tion in experiments that use these elevated levels. However, mechanisms responding to high levels might not yet do so to low levels, such that fewer mechanisms might be affected by low than high CO2 levels. Some mechanisms effective during long-term moderate exposures, like reductions in protein synthesis, will also be involved during short-term exposures but the period may be too short for them to become detrimen- tal, even under extreme conditions. Other mecha- nisms, such as those involved in oxygen supply, respond strongly in this case and thereby take priority (Fig. 2). Apparently different patterns at various CO2 concentrations may result from a change in the priori- ties of CO2 effects. Studies at high levels are thus im- portant for a comprehensive identification of affected
mechanisms and should not be dismissed based on premature paradigms. Conceptually, it is important to study the extreme and then ‘titrate’ responses and mechanisms at various intermediate levels of physico- chemical parameters including the range of expected values.
The scale and magnitude of CO2 effects depend on both concentration and time scale. Acute effects are usually only observed under very high CO2 levels. In animals, oxygen supply is affected, e.g. via fast distur- bance of blood oxygen transport through oxygen bind- ing proteins as in squid (Pörtner et al. 2004) or via the onset of cardiocirculatory collapse as in fish (Ishimatsu et al. 2005). These processes may be only minimally affected under long-term moderate CO2 exposures with no significant harm seen under laboratory condi- tions. Recent insight into thermal effects and their eco- logical consequences in the field indicates, however, that full performance capacity and aerobic scope is crucial for successful competition and survival in the
Low water pH   and high CO2 and reduced HCO3–
Ionequilibria –   Na+/H+-exchangeetc.
Calcification
–
H+ Ω
Chemosensory neurons H+i
Adenosine
accumulation and release
H+i
+
Functional capacity
–
Calcification site
Epithelia (gill, gut, kidney) Brain
CO2 HCO3–   H2O
H2O
–
3 Na+ H+
Cl– H+
ATP- ase
+ 2K
Na+– HCO3–
H+ e
Heart
Muscle
––
Gene expression ( + or – )
Intracellular space
Na+
Blood pigment
Extracellular space   Tissues
Fig. 2. Overview of processes and mechanisms affected by CO2 in a generalized water-breathing animal, emphasizing a key role for extracellular pH in defining sensitivity to ocean hypercapnia and acidification (after Pörtner et al. 2005). As with thermal sensitivity, the first line of hypercapnia tolerance is set at the level of functional capacity of whole animals defined e.g. by tissues in- volved in oxygen supply (cf. Fig. 4). Dark shaded areas indicate processes involved in changing energy budget. Grey arrows indi- cate signalling through water or body fluid physicochemistry, with a key role for intra- and extracellular H+ (H+i and H+e) or other factors like adenosine, K+, Na+, or Cl–. Ω quantifies the saturation of carbonates, e.g. aragonite, where K*sp is the solubility product
Ωaragonite = [Ca2+][CO23−]
K* sp, aragonite
Ventilation rate   (some groups)   Operculum
Metabolic equilibria Protein synthesis rate
membrane
field (Pörtner & Knust 2007). Therefore, minor distur- bances of oxygen transport pathways may significantly depress performance and affect the capacity of organ- isms to forage and compete for resources, to repro- duce, display various behaviours or just avoid predators (Pörtner & Farrell 2008).
Similar concerns argue for a consideration of time scale in studies of CO2 effects, especially during mild exposures (Fig. 1). A recent example of this is the study by Gazeau et al. (2007) which focussed on changes in calcification upon acute exposure (2 h) to various CO2 levels in marine bivalves (mussels Mytilus edulis and oysters Crassostrea edule). Calcification was progres- sively reduced with rising CO2 levels. Assuming the unlikely, namely that no acclimation occurs, the authors projected a decrease in calcification rates by 25 and 10% upon exposure to year 2100 CO2 accumulation scenarios. A threshold value of 1800 ppm was elabo- rated for M. edulis where shell dissolution would ex- ceed calcification. However, the data from Michaelidis et al. (2005) on Mytilus galloprovincialis and those from Berge et al. (2006) on Mytilus edulis rather suggest that acclimation sets in within days and supports net (in- cluding shell) growth and calcification even beyond that threshold. Studies of acute responses (e.g. Gazeau et al. 2007) thus do not yet provide a realistic picture of how animals respond over weeks or months to various CO2 levels, and need to be complemented by long-term investigations that allow acclimation to occur.
As a corollary, acclimation is relevant and also affects calcification. If acclimation capabilities are to be evalu- ated properly, physiological mechanisms need to be identified which mediate the decrease in performance including calcification rates. These mechanisms need to be evaluated in how they vary between species, dur- ing acclimation and adaptation, and thereby contribute to the species-specific level of sensitivity on various time scales. In this context, calcification should not be treated as an isolated phenomenon. In other words, the drop in calcification rates is a crucial effect but, except for the different nature of the carbonates (predomi- nantly aragonite in Mytilus edulis versus calcite in Crassostrea edule), a full mechanistic explanation needs to consider the physiological (within animal) mechanisms and processes setting calcification rates.
UNIFYING MECHANISMS OF CO2 EFFECTS
Current literature emphasizes the sensitivity of calci- fiers to ocean acidification (e.g. Royal Society 2005), but this view may not be sufficient for understanding ecosystem effects. Calcification plays a role in the sta- bilization of body form and function and in the protec- tion against predators or, in the case of corals, in the
building of a reef as a specific habitat. Some forms such as corals and phytoplankton can exist (for ex- tended periods) without their calcareous shell (Fine & Tchernov 2007), whereas others such as echinoderms cannot as their skeletons support organismal function- ing. The question is whether effects on calcification are currently considered very crucial only because effects on calcified exoskeletons are so very obvious. Is calcifi- cation really a key bottleneck or simply one among several physiological processes concomitantly affected in sensitive organisms? This section builds on the view that such physiological processes are usually closely coordinated and that, in the case of a calcifier, the con- trol of calcification is integrated into the control of other processes equally relevant for survival, such as growth, neural functioning, and regulation of body fluid pH and intracellular pH in various tissues. How- ever, knowledge of the mechanisms regulating calcifi- cation is limited. Moreover, it is not clear whether the responses of calcifiers and non-calcifiers are shaped via similar mechanisms. Such knowledge is needed to answer this question and is critical for a comparative assessment of sensitivities. Previous studies using rela- tively high CO2 levels in fact provide physiological background information which indicates that unifying principles define sensitivity to CO2 in both calcifying and non-calcifying animals.
The carbonate concentration and saturation levels of calcium carbonates in seawater are widely reported to set calcification rates. Calcification, however, rarely occurs at surfaces exposed to sea water. Rather, it occurs in relatively isolated compartments where ion transport across various epithelia establishes an envi- ronment suitable for calcification. Therefore, the per- spective that water carbonate saturation directly sets calcification rates would be too simplistic physiologi- cally. The influence of aquatic physicochemistry is important but often indirect, via effects on calcium and proton equivalent ion transport through the outermost barriers (e.g. gill or equivalent epithelia). These mech- anisms do not usually transport carbonate, but rather bicarbonate; calcium channels and proton pumps may also be involved (Carre et al. 2006). Carbonate precip- itated in calcified structures is therefore not directly originating from water carbonate, but generated or modulated via several reactions from imported bicar- bonate and/or CO2 trapped in the alkaline compart- ment at calcification sites. Water carbonate levels (CO32–) and calcium carbonate saturation levels thus are useful proxies but usually not direct drivers of cal- cification. These proxies also mirror the effects on ion transport mechanisms of associated water parameters, such as pH, calcium or bicarbonate levels and thereby influence the setting of more direct effectors of calcifi- cation which comprise a range of physiological para-
Pörtner: Ecosystem effects of ocean acidification   209
210   Mar Ecol Prog Ser 373: 203–217, 2008
meters inside the organism and compartments involved. Although not directly effective at the calcifi- cation site either (Fig. 2), extracellular body fluid including blood or haemolymph in animals is the first compartment affected by water physicochemistry. The extracellular   acid – base   status,   as   reflected   in   extracel- lular pH, responds in a species-specific way and acts as a mediator of the effects of water physicochemistry on calcification in most animals.
It   is   important   to   note   that   intracorporeal   acid – base status not only comprises adjustments in compartmen- tal pH values. pH compensation occurs through the accumulation of bicarbonate in mostly extracellular, but also intracellular compartments. Extracellular bicarbonate accumulation will support compensation of intracellular acidosis through transmembrane ion exchange (Pörtner et al. 1998). Bicarbonate accumula- tion will lead to higher saturation levels of the calcium carbonates, quantified by Ω (Fig. 2). At calcification sites, this may even lead to a counter-intuitive improvement of conditions for calcification under hypercapnia. Examples exist where such upregulation of calcification is visible in marine invertebrates (e.g. cephalopod Sepia officinalis, Gutowska et al. 2008, this Theme Section [TS]; infaunal ophiurids, Wood et al. 2008) and even in marine phytoplankton (Iglesias- Rodriguez et al. 2008). In the case of ophiurids, improved calcification came at the cost of muscle wastage, indicating a disturbance of energy budget not visible in the cuttlefish. We require quantification of the levels of intracorporeal physicochemistry to be maintained   by   ion   and   acid – base   regulation   for   ade- quate calcification and for adequate coordination of calcification with whole body systemic functioning.
Extracellular   acid – base   status   thus   not   only   modu- lates calcification rates but also influences other physi- ological processes. The comparison of non-calcifying with calcifying marine invertebrates in fact supports the   view   that   extracellular   acid – base   status   and   espe- cially extracellular pH (pHe) may be a unifying para- meter which is operative in both calcifiers and non-cal- cifiers to set CO2 sensitivity. Work on a non-calcifying worm, Sipunculus nudus, has provided the most com- prehensive data set on physiological effects under hypercapnia to date. Key effects include metabolic depression and associated patterns of transepithelial acid – base   regulation   (Pörtner   et   al.   1998),   reduced rates   of   tissue   acid – base   regulation   (Pörtner   et   al. 2000), reduced rates of protein synthesis (Langenbuch et al. 2006) and enhanced levels of adenosine in ner- vous tissue and associated depression of behaviours (Reipschläger et al. 1997). These responses were asso- ciated with hypercapnia-induced acidosis which ini- tially developed in both extra- and intracellular fluid compartments (of muscle tissue) but over time,
resulted in incompletely compensated extracellular but fully compensated intracellular acidosis (Pörtner et al. 1998). More detailed study has identified extracel- lular pH as a key variable mediating metabolic depres- sion (Reipschläger & Pörtner 1996) through reduced rates of ion exchange (Pörtner et al. 2000), at main- tained rates of ammonia excretion (Pörtner et al. 1998). Modified amino-acid metabolism or reduced rates of protein synthesis are mediated via modified intracellu- lar   acid – base   variables,   especially   under   conditions   of severe extracellular acidosis (Langenbuch & Pörtner 2002, Langenbuch et al. 2006). Maintenance of extra- cellular pH thus appears as the first line of defence against hypercapnia induced disturbances of meta- bolic and tissue functioning as well as of behavioral performance. The key role of extracellular pH is emphasized by the fact that a lowering of pHe is simi- larly effective in metabolic depression regardless of hypercapnic or normocapnic conditions (Reipschläger & Pörtner 1996).
In mussels Mytilus galloprovincialis, a study by Michaelidis et al. (2005) used elevated CO2 levels to set water pH to 7.3, close to the maximum degree of acidification expected during realistic emission scenar- ios (Caldeira & Wickett 2003). Despite lower levels of ambient pCO2, compensation of the extracellular aci- dosis occurred but was even less than in Sipunculus nudus. Under these conditions shell growth was largely reduced, in line with the finding of depressed calcification in M. edulis (Gazeau et al. 2007). Most importantly, the reductions of shell and soft body growth were found closely coordinated in M. gallo- provincialis, indicating a common mechanism modula- ting the rate of both processes including the rate of calcification. Moreover, the metabolic effects of hyper- capnia were the same in S. nudus and M. galloprovin- cialis. In line with phenomena seen in the sipunculid worm, Michaelidis et al. (2005) reported a decrease in metabolic rate, associated with a rise in ammonia ex- cretion during partially compensated extracellular aci- dosis. These findings strongly suggest that as in S. nudus, the lowered extracellular pH in mussels is key to the observed metabolic depression. It is also very likely that the low capacity of sipunculids and bivalves to compensate for disturbances in extracellular pH explains the reduction in growth and calcification.
Low capacity of acid–base regulation through pro- ton equivalent ion exchange may be a general pattern explaining the elevated sensitivity of lower marine invertebrates and their life stages to CO2 (Pörtner et al. 2004, 2005, Shirayama & Thornton 2005, Dupont et al. 2008, this TS). The reduced capacity of lower marine invertebrates   to   regulate   extracellular   acid – base   sta- tus becomes explainable in the light of their hypometa- bolic   mode   of   life.   Acid – base   regulation   bears   a   signif-
Pörtner: Ecosystem effects of ocean acidification   211
icant cost (Pörtner et al. 2000) which can be reduced at the expense of capacity and of the baseline idling of ion-exchange mechanisms. At the same time these organisms   need   to   modulate   the   acid – base   status   of large volumes of extracellular fluid in open circulatory systems (more than 50% in the sipunculid). A larger degree of acidification upon acute CO2 exposure is facilitated by much lower non-bicarbonate buffer val- ues than found in vertebrate blood. As a consequence, sensitivity is enhanced as reduced capacity meets the requirement to adjust pH in large fluid compartments. Low capacity also means that the setpoint of extra- cellular pH even fluctuates passively depending on water physicochemistry as seen in Sipunculus nudus in response to fluctuating water bicarbonate levels (Fig.   3).   Comparative   work   emphasizes   that   acid – base regulation capacity in relation to the rate of energy turnover is not only dependent on phylogeny but is also influenced by mode of life and habitat. For exam- ple, reduced capacity to regulate extracellular pH was recently found in deep-sea versus shallow-water crus- taceans (Pane & Barry 2007, see also Spicer et al. 2007) where the slow and hypometabolic mode of life in deep-sea species is reflected in a reduced rate (and thus cost) for acid–base regulation.
Contrasting these data with findings in teleost fish supports the existence of a common mechanism of CO2 sensitivity in marine water-breathing animals. Teleost fish   in   vivo   do   not   display   similar   patterns   of   acid – base compensation as the invertebrates (Heisler 1986b, Larsen et al. 1997, Ishimatsu et al. 2004). The extracel- lular acidosis is rapidly and more or less fully compen- sated, and there is no metabolic depression at moderate CO2 levels around 1%. Transient metabolic stimulation may even occur instead, as seen in Antarctic eelpout
(G. Lannig pers. comm.). However, similarities between fish and marine invertebrate responses do exist. Meta- bolic depression can occur in fish and has been ob- served in European eels at CO2 levels above 2% (Cruz- Neto & Steffensen 1997). Moreover, when isolated hepatocytes of Antarctic eelpout were investigated dur- ing exposure to respiratory and non-respiratory extra- cellular acidosis (Langenbuch & Pörtner 2003), they dis- played metabolic phenomena strikingly similar to those observed in invertebrate tissues and whole animals. In fish, these cellular responses are alleviated at the whole-animal level due to the large capacity of the in- tact organism to more or less fully compensate for the   acid – base   disturbance   in   relatively   high   levels of hypercapnia. This line of evidence supports the con- clusion that while cellular responses may be similar, whole-animal responses, and thus, resulting sensitivi- ties, are largely different in the (lower) marine inverte- brates and in fish due to different capacities to compen- sate for an extracellular acidosis. Nonetheless, the sensitivity   of   tissues   to   extracellular   acid – base   dis- turbances may also be modulated and vary among species.
These considerations confirm that the capacity of these organisms to maintain extracellular pH under various CO2 conditions is crucial in mediating or allevi- ating hypercapnia effects (Fig. 2). Both acute and long term CO2 sensitivity are likely highest in those lower marine invertebrates with a poor capacity to compen- sate for deviations from control extracellular pH which then affects systemic processes such as calcification as well as cellular processes like those involved in growth. According to mode of life and energy turnover, the most heavily calcified groups such as articulates, echinoderms (cf. Miles et al. 2007), bryozoans and cnidarians may be among those with the poorest capacity to regulate acid–base status. These were also those most severely affected during the Permian– Triassic mass extinction events (Knoll et al. 1996, 2007, Pörtner et al. 2004, 2005). In contrast, sensitivity is low- est in fish with a high capacity for extracellular pH compensation. Further study of these various groups is needed to further support this hypothesis. Such a hypothesis also needs testing in the light of possibly differential capacities of various groups to acclimate long term to ocean hypercapnia. While current data emphasize steady state in acid–base status reached within hours to days after an initial CO2 disturbance, this steady-state value may well shift progressively during a long term acclimation process. Such long term analyses are not yet available and should help to eluci- date the capacity to acclimate or adapt to ocean acidification scenarios. Long-term adjustments (within weeks) occur in the gene expression of ion exchangers contributing to acid–base regulation in teleost gills
2.9 mM
[HCO3– ]w
1 mM
0.6 mM
3.4 mM
8.0 7.8 7.6 7.4 7.2 7.0
–48 –24 0 24 48 72
Time (h)
Fig. 3. Body fluid extracellular pH (pHe) in a lower marine invertebrate, the sipunculid Sipunculus nudus, depending on water bicarbonate levels ([HCO3–]w) at constant levels of gaseous CO2 (author’s unpubl. data). The data emphasize a rapid response to changing water physicochemistry and its relevance for extracellular acid–base equilibria and associ- ated physiological processes (see Fig. 2)
pHe
212   Mar Ecol Prog Ser 373: 203–217, 2008
(Deigweiher et al. 2008) and indicate significant accli- mation capacity to long term hypercapnia in fish.
Overall, while current emphasis is on the sensitivity of calcifiers to ocean hypercapnia, they are likely sen- sitive not because they are calcifiers but because at the same time, they are sessile, hypometabolic organisms that display a poor capacity to regulate their systemic acid–base status and, mainly, extracellular pH.
METHODS CRITIQUE FOR STUDIES OF CALCIFICATION AND ACID–BASE REGULATION
As outlined above, the available data indicate that acid – base   status   and   the   capacity   to   regulate   and   com- pensate   for   acid – base   disturbances   are   crucially important in setting sensitivity to ocean hypercapnia. As a consequence, studies of calcification or other pro- cesses affected by ocean acidification need to investi- gate the organism in steady state with respect to inter- nal parameters like extracellular pH which modulate those rates. Studies of calcification that do not consider steady-state   acid – base   regulation   will   not   support long term predictions of calcification rates. On long time scales, over periods of weeks or months, acclima- tion or adaptation may shift the mechanisms and set- points   (steady-state   values)   of   acid – base   regulation and may thereby compensate for the CO2-induced acid – base   disturbance   and   its   effect   on   physiological processes, including calcification.
In this context, physiological (including biomedical) sciences and oceanography have both met the chal- lenge to precisely quantify relevant physicochemical parameters   defining   acid – base   status   of   body   fluids and ocean water. Due to the parallel and independent evolution of these fields, they have developed compa- rable but different strategies to do so. It is beyond the scope of this opinion paper to review the respective methodologies. From a physiological point of view it is crucial   to   analyse   acid – base   parameters   in   water   and body fluids by use of the same techniques, for reliable estimates   of   effective   acid – base   parameters   within and outside the body and for analyses of associated ion gradients across epithelia. In the fields of medical and comparative physiology this has traditionally been done by use of glass electrodes for analyses of pH and, after adequate modification, of pCO2 (Eggin- ton et al. 1999). Quantification of proton equivalent ion exchange has been carried out through assays of titratable alkalinity in water or urine, through continu- ous pH recordings in water (glass electrodes) or ana- lyses of total CO2 in water and body fluids. Continu- ous monitoring of intracellular pH is possible by use of 31P-NMR (nuclear magnetic resonance), whereas a set of   homogenate   techniques   reliably   quantifies   acid –
base parameters in tissues (Pörtner 1990, Pörtner et al. 1990).
Calcification rates are frequently analysed from changes   in   water   acid – base   status   through   the   alkalin- ity anomaly technique (Smith & Key 1975, Gazeau et al. 2007). The consideration of interfering metabolic and   acid – base   regulation   processes   casts   some   doubt on the absolute rates determined. Metabolism and the associated net rates of proton or base production influ- ence water alkalinity and may have to be taken into account. Protein metabolism causes net proton release and thus a potential overestimation of calcification rates. Under those circumstances, and with the meth- ods used, any CO2 or pH effects on metabolism (Pört- ner 1995) including the consecutive proton-equivalent ion exchange between animals and water may thus mimic changes in calcification.
PERSPECTIVES: INTEGRATING THERMAL, HYPOXIA AND HYPERCAPNIA RESPONSES
Ocean acidification occurs in concert with ocean warming and an increased frequency of hypoxia events. Recent work demonstrated that knowing the thermal window of performance of a species is crucial in defining sensitivity to the warming trend (Pörtner & Knust 2007). Future studies need to address effects of ocean hypercapnia and acidification within and beyond the limits of the baseline thermal window of a species, considering its capacity to thermally acclimate or adapt. The focus should be on measures of perfor- mance, metabolism and calcification in animals that have   reached   new   acid – base   equilibria   during   longer term exposures. Sensitivities to temperature and CO2 integrate in such a way that elevated CO2 levels en- hance the sensitivity of organisms to thermal extremes. This occurs through reductions in tissue functional capacities including those involved in oxygen supply (Pörtner et al. 2005, Metzger et al. 2007). Considering the mechanisms affected by CO2 (Fig. 2) it appears that a   shift   of   acid – base   status,   including   a   shift   of   extra- cellular pH, likely reduces the functional capacity of affected mechanisms and of the whole organism in due course. As a result, pO2 levels in the body fluids fall and, upon warming, reach limiting levels earlier than during normocapnia (Fig. 4). A narrowing of thermal windows results and the effect observed suggests a large sensitivity of the width of thermal windows to CO2. Such effects would be corroborated by increasing hypoxia events in the oceans. Conversely, if elevated CO2 levels or hypoxia cause a narrowing of thermal windows, this also means that exposure to thermal extremes will enhance sensitivity to elevated CO2 levels or hypoxia.
Pörtner: Ecosystem effects of ocean acidification   213
Tp
Tp
Normocapnia 10–22°C 1 % Hypercapnia 10–22°C
Tc
CO2 should include studies at a high organisational level, especially with respect to the intact organism and the mechanisms involved. This includes studying the   patterns   of   acid – base   regulation   and   hypoxemia as well as the capacity to regulate extracellular acid– base status and mainly extracellular pH, at extreme temperatures for an analysis of the background of temperature-dependent CO2 or hypoxia sensitivity and, vice versa, CO2- and oxygen-dependent thermal sensitivity.
While larval and juvenile stages may be more sensi- tive when effects of hypercapnia are studied in isola- tion (Ishimatsu et al. 2004, 2005) these relationships may become more complicated when temperature effects are considered. The temperature signal is cur- rently the strongest signal eliciting ecosystem change, due to physiological impacts and the limited thermal windows of individual species (e.g. Pörtner & Knust 2007). The available data indicate that (1) thermal extremes affect large individuals first and (2) a ther- mally variable environment favours species with smaller individuals including juveniles, due to their wider windows of thermal tolerance (e.g. Pörtner et al. 2008). If CO2 exacerbates these relationships by narrowing thermal windows this would favour smaller body sizes (and their wider thermal windows) even more and further constrain the size range of a species. Constant CO2 conditions may thus favour larger body sizes. The synergistic interactions between tempera- ture and CO2 thus have implications for how the sen- sitivity of a species to global change depends on body size (allometry). While sensitivity to CO2 per se may be highest in early life stages of many organisms, thermal stress also impacts the largest individuals of a species. With their already constrained thermal win- dows, they may then also become more sensitive to the synergistic effects of CO2. Once again, the regula- tion   of   extracellular   acid – base   status   may   be   crucial in this context as efficient pH regulation and its temperature-dependent characteristics are limited to within the thermal window of a species (e.g. Sommer et al. 1997).
As a general conclusion, these relationships and their implications at an ecosystem level need to be investigated with a wide range of organisms from various habitats. With the currently available data it is unclear whether these relationships have already started to affect species and ecosystems, for example through a narrowing of biogeographical distribution ranges. It appears most likely that such integrative effects will be the first to be observed in the field and bring with them the need to then disentangle the contribution of CO2, hypoxia and temperature as well as their synergistic interaction in causing those effects.
15
10
5
0
Tc
10 12 14 16 18 20 22 Temperature (°C)
Fig. 4. Heat tolerance of the edible crab Cancer pagurus under normo- and hypercapnia (after Metzger et al. 2007). Discontinuities in the curve depicting arterial oxygen tensions (pO2) under normocapnia were identified as indicators of thermal limits (upper pejus temperature, Tp, according to Frederich & Pörtner 2000) reflecting onset of a loss in eco- logically relevant performance and fitness (Pörtner & Knust 2007). Highly elevated CO2 levels (1% hypercapnia) cause heat tolerance to decrease dramatically by about 5°C. Similarly, the general lowering of haemolymph pO2 under hypercapnia causes a downward shift of upper critical temperatures (Tc) by about 4.5°C. Assuming a symmetric thermal window the data reflect a high sensitivity to CO2 and shrinkage of the thermal window by more than 80%. Temperature-dependent biogeographical ranges of marine animals may thus respond to even moderately elevated CO2 levels (Pörtner et al. 2005)
This paper presents a set of hypotheses for a compre- hensive mechanistic framework which brings the indi- vidual effects of the factors temperature, CO2 and hypoxia together into an integrative picture of climate sensitivity at organismal level (Fig. 5). The mechanistic scheme illustrates how virtually all mechanisms rele- vant in setting and shifting thermal windows will be affected through the exacerbation of hypoxemia (hypoxia in body fluids) under the effects of ambient hypercapnia or hypoxia. Both factors cause a decreased pH regulation capacity and setpoint of acid – base   regulation,   and   will   likely   do   so   to   the largest extent where temperature extremes are already causing hypoxemia. Thermal windows and sensitivities differ between species co-existing in the same ecosystem. Through differences in sensitivities, some of these effects will cause changes in species interactions and thereby functional shifts observed in ecosystem level processes.
Comparable to thermal limitation (Pörtner 2002), efforts to understand sensitivity of marine animals to
pO2 (kPa)
214   Mar Ecol Prog Ser 373: 203–217, 2008
Stress hormones, adenosine, Δ redox
Tc
Td
Fig. 5. Conceptual model of how ocean acidification, hypoxia and temperature extremes interact mechanistically, based on the oxygen and capacity limitation concept of thermal windows. The model indicates the hierarchies (upper panel) of functional limi- tation (beyond pejus temperatures, Tp), hypoxemia, anaerobic metabolism and protection through metabolic depression (below and beyond critical temperatures, Tc) and denaturation as well as repair (beyond denaturation temperatures, Td). Optimized oxy- gen supply to tissues between low and high pejus temperatures (upper panel), combined with the kinetic stimulation of perfor- mance rates by warming, supports a performance optimum (i.e. an optimum of aerobic scope) close to upper pejus temperature (lower panel). Systemic (e.g. stress hormones, adenosine) and cellular signals (e.g. hypoxia inducible factor HIF-1α, and redox status) associated with temperature-induced hypoxemia contribute to the acclimation response (horizontal arrows in upper panel), which leads to a shift in thermal tolerance limits and thus windows. Ambient hypoxia and elevated CO2 levels both cause lower performance optima and a narrowing of thermal windows (arrows attached to curves in both panels), through lower systemic oxygen tensions and shifted setpoints of acid–base regulation including the deviation of pH from the typical linear temperature-dependent decline (pH scale not shown) (upper panel). Details of the signalling pathways involved are not depicted.Modified from Pörtner & Knust (2007)
Acclimation in functional capacity
Δ Energy consumers / ion exchange Δ Mitochondrial functions
Acclimation in protection
+HIF-1
Anaerobic capacity
O2 supply pathways
Metabolic depression
Acclimation in repair: + HSP, + antioxidants
Loss of performance
Tp
Tp
Anaerobiosis
Tc
Hypoxemia
Denaturation
Td
0
0
pH setpoints decreased
Optimum
Hypoxia, CO2
Temperature
Acknowledgements. This work is a contribution to the ‘Euro- pean Project on Ocean Acidification’ (EPOCA) which received funding from the European Community’s Seventh Framework Programme (FP7/2007-2013) under grant agree- ment no. 211384. EPOCA is endorsed by the International Programme LOICZ. Supported by the Mar Co POL I research program of the Alfred Wegener Institute. The author thanks Magda Gutowska, Gisela Lannig and Frank Melzner for con- structive criticisms, as well as the editors (Ove Hoegh- Guldberg and Alain Vézina) and 3 anonymous referees for their stimulating comments.
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