Predicting The Impact of Ocean Acidification On Benthic Biodiversity: What Can Animal Physiology Tell Us?

JEMBE-48664; No of Pages 11
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Journal of Experimental Marine Biology and Ecology

j o u r n a l h o m e p a g e : w w w. e l s e v i e r. c o m / l o c a t e / j e m b e
Predicting the impact of ocean acidication on benthic biodiversity: What can animal physiology tell us?
Stephen Widdicombe a,, John I. Spicer b
a b
Plymouth Marine Laboratory, Prospect Place, West Hoe, Plymouth, PL1 3DH, UK Marine Biology and Ecology Research Centre, School of Biological Sciences, University of Plymouth, Plymouth PL4 8AA, UK
a r t i c l e
Available online xxxx Keywords: Biodiversity Ocean acidication Organism physiology
i n f o
a b s t r a c t
For the past 200 years, the oceans have been absorbing carbon dioxide at an unprecidented rate. It is now evident that this ongoing process has already signicantly altered seawater carbon chemistry at a global scale and will continue to do so for hundreds of years to come; a phenomenon termed ocean acidication. The challenge currently facing scientists is to predict the long term implications of ocean acidication for the diversity of marine organisms and for the ecosystem functions this diversity sustains. This challenge is all the more difcult considering that empirical data which specically address the impact of ocean acidication on marine biodiversity are currently lacking. In the face of growing political and public pressure to provide answers, what predictions can be made and how reliable are the assumptions on which those predictions depend? Here we review the extent to which the few existing data, and understanding gained from previous physiological studies, can be used to make predictions for marine biodiversity. In doing so we also scrutinise some established paradigms concerning the impact of hypercapnia, resulting from seawater acidication, on marine organisms. 2008 Elsevier B.V. All rights reserved.
1. Ocean acidication Since the start of the industrial revolution (circa 1750) the atmospheric concentration of carbon dioxide (CO2) has risen from a pre-industrial level of around 280 ppm to a concentration of approximately 380 ppm seen today (Feely et al., 2004). This rise is even more dramatic considering that almost 50% of all the anthropogenic CO2 emitted over the last 250 years has been taken up by the world's oceans (Sabine et al., 2004). As atmospheric CO2 diffuses passively into ocean surface waters it forms carbonic acid (H2CO3). This weak acid rapidly dissociates to produce hydrogen (H+) and + bicarbonate (HCO3) ions. The production of the H ions would cause seawater pH to fall (i.e. acidity increases) were it not for the saturation of surface waters with carbonate ions (CO23 ) which react with the excess H+ ions to form more HCO3. This reaction (CO2 + H2O H2CO3 + + 2HCO3 + H CO3 + 2H ) is referred to as the carbonate buffering system and is the process by which surface ocean pH has remained between 8.0 and 8.3 pH units for the last 25 million years, despite periods of high atmospheric CO2 concentrations. As current concentrations of atmospheric CO2 are not particularly unusual in Earth's history, it was initially thought that the carbonate buffering system would continue to maintain seawater pH at normal levels despite rising emissions. However, in 2003 this assumption was challenged.
Corresponding author. E-mail address: swi@pml.ac.uk (S. Widdicombe). 0022-0981/$ see front matter 2008 Elsevier B.V. All rights reserved. doi:10.1016/j.jembe.2008.07.024
Caldeira and Wickett (2003) used model predictions to show that, compared to pre-industrial times ocean surface water pH had fallen by 0.1 pH unit, indicating a 30% increase in the concentration of H+ ions. In addition when using estimates of future levels of CO2 emissions, their model showed the pH of surface waters could fall by up to 0.4 units before 2100 and a reduction of 0.7 units was also possible by 2250. This phenomenon is now widely recognised and referred to as ocean acidication. It is now also understood that ocean acidication does not result from the total amount of CO2 entering the oceans but instead is a consequence of the unprecedentedly high rate of increase. The current anthropogenically induced increase in atmospheric CO2, caused primarily by the burning of fossil fuels and the manufacture of cement, is nearly 100 times greater than previous naturally induced increases (Blackford and Gilbert, 2007). As the carbonate buffering system relies on the availability of CO23 ions, the supply of which is primarily from geological erosion and consequently a relatively slow process, the Earth's oceans are rapidly becoming more acidic and experiencing increasing hypercapnia (elevated levels of dissolved CO2). In addition, large areas, particularly cold polar regions where CO2 dissolution is greatest, will soon become undersaturated with respect to aragonite, a highly soluble form of calcium carbonate (Orr et al., 2005). It has been suggested that these predicted changes in seawater carbon chemistry will have an enormous impact on the health and function of many marine organisms (Raven et al., 2005) and in particular there is great concern that ocean acidication will reduce marine biodiversity.
Please cite this article as: Widdicombe, S., Spicer, J.I., Predicting the impact of ocean acidication on benthic biodiversity: What can animal physiology tell us? Journal of Experimental Marine Biology and Ecology (2008), doi:10.1016/j.jembe.2008.07.024
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2. Impact of ocean acidication on benthic biodiversity The oceans harbour tremendous biological diversity (May, 1994; Reaka-Kudla, 1997). The majority of this marine biodiversity is made up of invertebrates either residing in (infauna) or on (epifauna) sediments (Snelgrove, 1999) with the benthos containing 98% of all marine species and harboring living representatives of all but one of the 29 non-symbiont animal phyla so far described. Such incredible diversity results from complex interactions between the underlying physical and environmental conditions (e.g. depth, temperature, organic supply and granulometry) and the biological interactions operating between and within benthic organisms (e.g. predation and competition) (May, 1994). Essentially the physical environment will determine the suite of species that can potentially exist in an area, whilst biological interactions will ultimately determine which species full their potential and in what densities, a process known as selfstructuring (see review by Reise, 2002). Given the importance of the benthic environment as a reservoir for biodiversity, there has been much speculation as to whether ocean acidication has the potential to reduce benthic biodiversity by impacting on key biological processes such as growth, respiration, calcication, metabolic rate and activity. A further concern is that any decrease in biodiversity could lead to a reduction in a number of key ecosystem functions, in particular the cycling of carbon and nitrogen, especially as shelf seas are known to host a disproportionately large fraction of productivity (Field et al., 1998). Currently there is a lack of empirical data specically determining the impact of ocean acidication on benthic biodiversity. Obviously this must limit our understanding of, and response to, the perceived threat. While government bodies are busy constructing much needed research programmes to address the issue of ocean acidication, any resultant data base is still someway off. In the meanwhile there is another way into this area of investigation. This complimentary approach is predicated on the premise that the responses observed at a community level are a product of the multitude of impacts and responses that occur at the level of the individual. At this level of impact, some data are available on the effects of high CO2. So is it possible to predict the response of benthic biodiversity to ocean acidication based on our current understanding of how organisms respond physiologically to high CO2 and/or low pH? Ocean acidication could potentially reduce marine biodiversity in a number of ways. Firstly through a loss of those species which are sensitive to changes in CO2 and pH. Secondly, if sensitivity to acidication is a function of an organism's taxonomic group, acidication may also reduce taxonomic diversity. Thirdly, the loss of keystone / critical species, or a reduction in their activity (e.g. predation, grazing, bioturbation), could reduce habitat complexity and also reduce the biological regulation of competition. We will tackle each of these points in turn, bringing to bear our current knowledge of responses to acidied sea water, mainly at the level of the individual. 2.1. Could ocean acidication reduce the species richness of a community? To accept that ocean acidication could reduce species richness it rst needs to be demonstrated that acidication will have a detrimental effect on the survival of individuals and the long term sustainability of populations. There is some geological evidence that this has been the case in the past. Around 55.8mya the Earth experienced a period of rapid greenhouse warming where ocean temperatures rose by as much as 9 C (Kennett and Stott 1991; Slujis et al., 2006; Zachos et al., 2003, 2006), having a profound effect on marine biota (Harrington and Jaramillo, 2007). This period, known as the Palaeocene-Eocene Thermal Maximum (PETM), lasted between 100 and 200 thousand years. Whilst there is still much debate as to the precise cause of the PETM and the exact magnitude of change in
seawater pH, there is agreement that during this period the oceans did become more acidic and saline with increased periods of anoxia (Zachos et al., 2005). It is widely considered that the PETM represents the most useful historical analogue for the ocean acidication event we are experiencing at present (e.g. Zachos et al., 2005). Benthic foraminifera assemblages are well preserved in the fossil record and are considered indicative of environmental change at the seaoor (Ernst et al., 2006). Analysis of these fossilised assemblages provides strong evidence that, during the PETM, a benthonic extinction event occurred in both deep-sea and shallow-water environments (Aref and Youssef, 2004) highlighting the potential negative impacts of ocean acidication on benthic biodiversity. So what are the key physiological responses that could underlie the perceived inability of some marine organisms to cope with the changes in seawater chemistry predicted to occur in the near future? The theoretical impacts of high levels of CO2 on the physiology and function of benthic species have been highlighted (e.g., Seibel and Walsh, 2001, 2003; Prtner et al., 2004, 2005; Prtner et al., 2005; Knoll et al., 2007) but, as yet, evidence from direct relevant experimental observations is limited. By the end of 2007, less than 30 papers had been published that described the response of benthic (non-coral) species to elevated CO2. Of these, many have concentrated on impacts associated with the deep ocean storage of CO2 and the relevance of these studies to the more subtle yet longer term impacts of ocean acidication is limited. What is clear, however, from the limited information currently available, is that elevated CO2 in the marine environment has the potential to impact on the health, function and activity of many benthic invertebrates across a range of taxonomic groups: echinoderms (Kurihara and Shiriayama, 2004; Kurihara et al., 2004; Miles et al., 2007; Wood et al., 2008), molluscs (Michaelidis et al., 2005; Berge et al., 2006; Bibby et al., 2007, 2008; Gazeau et al., 2007; Kurihara et al., 2007; Beesley et al., in press), crustaceans (Metzger et al., 2007; Pane and Barry, 2007; Spicer et al., 2007) and sipunculids (Langenbuch and Prtner, 2002, 2004; Langenbuch et al., 2006). In addition to the few studies described above, a considerable body of data also exists on the effect of hypercapnia on marine animals. These data have been generated by comparative animal physiologists who have used exposure to usually very high values of pCO2 as a way of eliciting responses, in an attempt to unravel mechanisms of respiratory control and acid-base compensation (e.g., Cameron, 1978a, 1986, 1989; Truchot, 1987; Heisler, 1989; Wheatly and Henry, 1992). Whilst the validity of using data from such short (often 224 h) studies to extrapolate to more long term ocean acidication effects is as yet unclear, if used cautiously these data may help provide predictions of sensitivity and underlying response mechanisms. A number of ocean acidication studies have discussed mortality as a measure of organism sensitivity to acidied sea water. However, even if exposure to hypercapnia does not cause the death of an individual during an experimental exposure, that does not mean that populations of that species are not ultimately vulnerable to extinction. Trade-offs between maintenance activities (e.g. respiration) and growth and/or reproduction might be expected and so negative effects of ocean acidication may be detectable by studying such trade-offs (cf. Wood et al., 2008 for a very recent example of such a trade-off). It has been shown that growth, and components of growth such as protein synthesis, can be negatively affected by medium to long-term exposure to hypercapnia in bivalve molluscs (e.g. Michaelidis et al., 2005), crustaceans (e.g. Wickens, 1984), Antarctic sh (e.g. Langenbuch and Prtner, 2003), even if such effects are difcult to detect (e.g. Langenbuch et al., 2006). It is also not uncommon to nd that abiotic factors well within the environmental tolerances of adult organisms totally negate reproductive capacity (Spicer and Gaston, 1999). Hypercapnia, resulting in a seawater pH of 6.8, decreased egg production in the copepod Acartia steueri (Kurihara et al., 2004). For two rocky shore sea urchins, exposure to a CO2 concentration
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of N 500 ppm resulted in a small decrease in fertilization rate, falling to 7.644% success at N 10 000 ppm (pH = 6.8). Still, the level of hypercapnia employed (not necessarily required) to compromise reproduction in these experiments is very high, and in the same range as employed for studies of the adult tolerances. However, much remains to be achieved in this area. For example exposure of Sturgeon Acipenser transmontanus to pCO2 = 1kPa [approx. 10 400 ppm. Note: In order to provide some comparability when CO2 values are expressed by authors as partial pressures and not concentrations, we have converted the partial pressures using an appropriate solubility coefcient and, as much as possible, taking account of temperature, salinity etc. Thus values in squared brackets presented after partial pressures are very rough approximations of CO2 concentrations in ppm] resulted in a signicant reduction in semen pH (Ingermann et al., 2002). At pH less than 7.5 sperm motility was signicantly affected. This said, sperm motility was relatively insensitive to low pH in A. baeri (Gallis et al., 1991, cited in Ingermann et al., 2002) and in salmon (Bencic et al., 2000; Ingermann et al., 2002). Whilst the potential for ocean acidication to result in species extinctions via impacts on organism growth and reproduction is clear, there is little good empirical evidence (other than that from the paleolontological record) so far to demonstrate that this potential will be realised and that extinctions will denitely occur. We suggest this lack of evidence could be largely due to the fact that: (1) our database is poor; (2) many of the data were generated to answer different questions from the ones we pose here; (3) synergism with other environmental factors is rarely taken into account; (4) the species used in laboratory experiments must, by denition be common, labhardy forms, when the majority of marine species are rare and relatively sensitive; (5) we do not have enough long term studies employing realistic future pH scenarios. Another potential mechanism for biodiversity loss is that organisms at their range edges may be impacted as acidication could reduce an organism's tolerances to environmental drivers such as temperature, salinity, pollution and disease. Therefore, the potential pool of species from which any assemblage is drawn will be reduced. Much of the current data on hypercapnia-related mortality are for exposure to a single environmental factor; CO2. However, we do have some good evidence that synergistic effects can dramatically alter the sensitivity and response of an individual's physiology to hypercapnia. Ocean acidication will inevitably be accompanied by warming, therefore it is of considerable interest that Metzger et al. (2007), investigating the synergistic effects of hypercapnia (1% CO2) [approx. 7 200 ppm @ 10 C and 10 000 ppm @ 22 C) and progressive warming (10 to 22 C) on the edible crab Cancer pagurus, found that there was a hypercapnic-related reduction in the thermal tolerance range of this species. In marine environments such as tidepools and estuaries, naturally occurring hypercapnia is often accompanied by hypoxia (low oxygen) (Truchot and Duhamel-Jouve, 1980; Truchot, 1988; Zebe and Schnieder, 1996; Burnett, 1997; Lin et al., 2004; Zhai et al., 2005). There is good evidence that these two stressors act synergistically on the respiratory responses of various marine invertebrates found in these environments (Jouve Duhamel and Truchot, 1983; Truchot, 1984, 1986, 1988; Conti and Toulmond, 1986; Zebe and Schnieder, 1996; Cochran and Burnett, 1996; Burnett, 1997). For example, in a recent study the deep sea Tanner crab showed only partial compensation of an extracellular acidosis when exposed to hypercapnia, but when this hypercapnia was compounded by hypoxia no compensation was detected (Pane and Barry, 2007). More recently the effect of combined hypercapnia and hypoxia on suborganismal function, such as immune function has received attention. The combined effects of hypercapnia and hypoxia on the oyster Crassostrea virginica, and the sh Fundulus heteroclitus was shown to depress cellular defence mechanisms (Burnett and Burnett, 2000). Hypoxic hypercapnia can also increase the rate of lethal infection of shrimps from pathogens (e.g., Mikulski et al., 2000) and the ability of the
shrimp Litopenaeus vannamei (Burgents et al., 2005) and the blue crab Callinectes sapidus (Holman et al., 2004; Tanner et al., 2006) to combat Vibrio infection. Bibby et al. (2008) also showed a reduction in immune response of Mytilus edulis when exposed to elevated levels of CO2. Although not part of the questions posed by the researchers using hypercapnic hypoxia to stress the immune system of these marine invertebrates, it would have suited our present purposes better if we were able to disentangle the effects of hypoxia and hypercapnia. Given this synergism of environmental factors, marginal populations may well be more at risk than populations nearer the centre of a species geographic range. However, much depends on the extent to which there is physiological differentiation within a species and the extent to which range edge populations are open to input from more central populations (see Spicer and Gaston, 1999 for discussion). For it may also be the case that it is at range edges that physiological evolution occurs, enabling in some cases range extension, and not necessarily range contraction (see Lewontin and Birch, 1966). It is evident that we need a better understanding of the physiological differentiation across a species range generally before we can begin to understand the effect of superimposing ocean acidication as a stress on the physiology of organisms (see Prtner et al., 2005 for further discussion of synergy between hypercapnia, hypoxia and temperature). A current area of enthusiastic debate is the extent to which organisms will able to adapt or evolve in response to changes in seawater chemistry. The assumption being that if species are able to adapt sufciently quickly to keep pace with the underlying environmental change, no impact on biodiversity would be expected. However, one important issue within these debates has been a lack of consistency in dening what constitutes adaptation. Physiologists and ecologists have both been guilty of a careless or confusing use of the word adapt (Garland and Adolph, 1994). In some cases how animals adapt is used to mean simply the present ability of an individual to respond plastically to changes in its environment (e.g. Precht's resistance and capacity adaptations are used in this way with respect to plastic responses in tolerance to, and performance in, a new environment (Precht et al., 1955)). This is more properly referred to as acclimatisation (or acclimation if only one environmental factor has been altered) (see Spicer and Gaston, 1999 for further discussion and references) and there is some evidence of this when organisms are exposed to hypercapnia. Certainly short-term experiments on the effect of hypercapnia on mortality of juvenile sillago Sillago japonica showed that a sudden increase from normocapnia to 7-9% CO2 [approx. 46 10059 300 ppm] resulted in complete mortality within 15 min whereas after stepwise exposure (still relatively short term) individuals were still alive after 18 h (Kikkawa et al., 2006). Alternatively, step-wise exposure to hypercapnia made no difference to mortality rates of the copepod Metamphiascopsis hirsutus (Sato et al., 2005). In common with other more long term experiments investigating the effects of environmental challenges during long-term exposure to hypercapnia, an initial set of acute physiological responses may be replaced by a set of different more long term changes and discounting the possibility of acclimatisation in these cases may lead to erroneous conclusions. A recent study of the acute effects of hypercapnia on bivalve calcication (Mytilus edulis), made some predictions concerning critical environmental values for shell dissolution (Gazeau et al., 2007). However, more long term studies on this same species (Berge et al., 2006), and a closely-related species Mytilus galloprovincialis (Michaelidis et al., 2005) showed good (if incomplete) acclimation to hypercapnia in a way which, arguably, makes the long term predictions of Gazeau et al. (2007) less reliable. To take a sh example, initial exposure to hypercapnia results in changes in rates of ion exchange but, in the medium to long term, key structural components of sh acid-base regulation (gill chloride cells and Na+/K+ ATPase activity) are known to alter (Hayashi et al., 2004b).
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While we desperately need more studies on hypercapnic acclimatisation and acclimation, and such studies are of huge importance, perhaps even more importantly we would like to know how species will adapt, evolve, when challenged with exposure to a progressively more acidied, CO2 rich environment. From the fossil record there is the indication that rates of speciation of marine animals coincided with changes in environmental CO2 (Cornette et al., 2002), although the timescale is quite different from the one we are interested in today. In particular we would like to know about rates of, and the capacity for, physiological evolution in the face of increasing ocean acidication over periods of 10100's of years. While we know of no such investigations yet taking place, we do have some studies of evolution in response to global climate warming, which may throw some light on rates of evolution. Two examples should sufce. The assumption that the thermal sensitivity of species was incapable of adapting to rapidly changing temperatures (global climate warming) was tested using selection experiments involving bacteria E. coli (Bennett et al., 1990) and fruit ies Drosophila melanogaster (Huey et al., 1991). In the fruit ies evolutionary differences in tolerance to heat shock and developmental time appeared in less than four and a half years (66 generations in low temperature, 110 generations in high temperature). But these are both relatively small short-lived organisms and Huey et al. (1991) note that Small organisms with short generation times clearly have the capacity to respond genetically and rapidly to shifts in their thermal environmentlarge organisms which have long generation times are unlikely to make sufciently rapid genetic adjustments [to global climate warming] and may thus experience stress and extinction. Any hope in the possibility of marine organisms adapting to acidication engendered by these data should be tempered with the realisation that one of the main ndings to emerge from the experiments on laboratory selection for physiological features is that rarely can the outcome of selection be predicted, and frequently the results are surprising. The whole area of evolvability (an organism's ability to generate heritable phenotypic variation; Kirschner and Gerhart, 1998) and the timescales of, and scope for, physiological differentiation deserves attention generally (Garland and Carter, 1994; Feder et al., 2000), but particularly with regards to ocean acidication. So, it seems that our current understanding would suggest there is potential for ocean acidication to have a considerable negative impact on many marine organisms; however, the extent to which this potential will be realised is far from resolved. Before the scale of any reduction in species richness can be condently predicted a number of major issues need to be tackled. Most notably research is needed to assess the interactive effects of elevated CO2 and other environmental stressors. In addition, the potential of marine organisms to adapt to environmental change must be explored. 2.2. Could Ocean Acidication Reduce The Taxonomic Distinctness Of Species Within A Community? Whilst a reduction in the total number of species in an area would constitute an important impact of ocean acidication, it should be remembered that species richness does not necessarily reect phylogenetic diversity. It is possible to envisage a situation where two areas contain the same number of species and therefore could be considered equally diverse. However, if all the species in the rst area are from the same genus but the second area contains species from different families, orders or even phyla, notwithstanding problems of equivalency between taxonomic levels of different groups, there is a good case to be made that the second area should be considered more diverse than the rst. If ocean acidication were to selectively remove species from particular taxonomic groups only for them to be replaced by species from more tolerant groups already represented within an area, e.g. remove echinoderms and replace them with polychaetes, species diversity could remain high whilst taxonomic diversity would
be reduced. Another important consideration is that species richness may not necessarily respond to ocean acidication in a monotonic way. It is now a well established paradigm that the highest values of species richness can occur in response to intermediate levels of environmental disturbance (see Wilkinson, 1999 and references therein). However, a number of studies using measures of diversity based on taxonomic distances (see Warwick and Clarke, 1995) have shown a more predictable decline in response to increasing disturbance (e.g., Warwick and Clarke, 1998). To predict whether ocean acidication is likely to affect taxonomic diversity we must rst determine whether an organism's level of sensitivity to ocean acidication is in any way related to its phylogeny. As already alluded to above hypercapnia has been used by physiologists for many decades as an experimental tool to help elucidate the controls of respiratory gas exchange and the mechanisms responsible for the maintenance of acid-base balance in marine invertebrates and sh. Thus our understanding of acute physiological responses to hypercapnia by different species is reasonably good. There is broad agreement across many of the different model species investigated in detail. Aquatic animals that possess gills regulate the degree to which those gills are ventilated in response to differences in environmental O2 and not CO2 (Cameron 1986, 1989; Sundin et al., 2007). This means that alterations in blood/haemolymph pCO2 are a consequence of altered ventilation in response to pO2. So, is insensitivity to CO2 ubiquitous in aquatic gill-breathers? Differences in hypercapnic-sensitivity of acute respiratory movements of a number of marine species are relatively well documented, so reviewing the impacts of high CO2 on respiratory function may allow us to look for a link between phylogeny and vulnerability to ocean acidication. Hypercapnia increases the beating of the pleopods (increasing gill irrigation) in the stomatopod Squilla (Matula, 1912; Johnson, 1936) and the amphipod Gammarus locusta (Munro Fox and Johnson 1934), the beating of the scaphognathites in the prawn Pandalus borealis and the respiratory movements of Octopus (Winterstein, 1925). However, it did not inuence irrigation of the gills of the barnacle Balanus balanoides (Roaf, 1912; Munro Fox and Johnson, 1934). In the case of the shore crab Carcinus maenas the response tocarbon dioxide was as variable as the rate of scaphognathite beat itself (1936) although Arudpragasam and Naylor (1964) did nd a consistent (although small) response of ventilation to CO2 in the same species. There was no effect of hypercapnia (pCO2 = 7.5 or 15 mmHg [approx. 7 500 or 15 000 ppm]) on ventilation by the blue crab Callinectes sapidus (Batterton and Camerson, 1978). For the polychaetes Hyalinoecia tubicola and Diopatra cuprea, which inhabit tubes in soft sediments, exposure to hypercapnia (pH = 7.5) caused no signicant differences in the frequency or duration of respiratory irrigation (Dales et al., 1970). More pronounced hypercapnia (resulting in a seawater pH = 7.07.2) resulted initially in an irregular rhythm although the normocapnic pattern was restored after 10h continued exposure. Ventilation in some marine sh species is also sensitive to CO2 (McKendry et al., 2001) although in the dogsh Scyliorhinus stellaris gill ventilation increased only briey (breathing frequency remained constant) to 140% of control levels in the rst hour exposure (Randall et al., 1976). Clearly from this evidence we can conclude that there are obvious differences in the sensitivity of species physiologies to hypercapnia, although it is difcult to detect any clear phylogenetic signal. Perhaps in retrospect taking cognizance of the fact that ventilatory changes of aquatic gill-breathers are driven primarily by pO2, the absence of a phylogenetic pattern in ventilator response to pCO2 is not suprising (cf. Sundin et al., 2007). But still there are differences and they do not seem to correlate with other candidates such as the ecology of the different species investigated. It has long been known that the way in which extracellular spaces respond to hypercapnia is broadly similar across a wide variety of marine animals. There is initially an extracellular acidosis (blood or haemolymph pH falls) accompanied by an increase in bicarbonate,
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with near full or partial pH compensation as a result of predominantly active ion transport processes in the gills (Cameron, 1978a, 1986, 1989; Toews et al., 1983; Heisler, 1980, 1989, 1993; Cameron and Iwama, 1987; Truchot, 1987; Ahearn et al., 1999; Whiteley, 1999; Clairborne et al., 2002; Freire et al., 2007). Maintenance of intracellular pH is essential for countless cellular functions and regulations (Putnam and Roos, 1997) and, broadly speaking, extracellular pH is regulated 0.5 0.8 pH units above intracellular pH (Prtner et al., 2004). Therefore, the extent to which an organism can achieve pH compensation in the face of increasing levels of CO2 could offer another method of identifying differences in sensitivity to hypercapnia between taxonomic groups. Hypercapnia-related decreases in intracellular pH appear to be almost fully compensated after 2448 h exposure in a wide range of marine invertebrates (Lindinger et al., 1984) and sh (Heisler, 1980; Claiborne and Evans, 1992; Larsen et al., 1997; McKenzie et al., 2003), including one of the best studied benthic organisms, the sipunculid worm Sipunculus nudis (Prtner et al., 1998, 2000). However, in some invertebrates, such as Mytilus edulis (Zange et al., 1990), Callinectes sapidus (Wood and Cameron, 1985), Chionoecetes tanneri (Pane and Barry, 2007), Psammechinus miliaris (Miles et al., 2007) (and including S. nudis) there is only partial, or no, compensation in hypercapnia-induced disturbance of extracellular acid-base balance. This can be contrasted with a number of marine sh species (teleost and elasmobranch) which show almost complete compensation of extracellular acid-base balance during acute and even more long-term exposure to hypercapnia (Cross et al., 1969; Toews et al., 1983; Randall et al., 1976; Heisler et al., 1976; Wright et al., 1988; Hayashi et al., 2004a). Atypical of many other invertebrates, the cuttlesh Sepia ofcinalis (and to some extent the velvet ddler crab Necora puber (Spicer et al., 2007) like the sh, is capable of maintaining its extracellular pH under conditions of hypercapnia showing near complete compensation (via an increase in extracellular bicarbonate) (Gutowska et al., 2007). So when we ask the question is there a phylogenetic signal, this time in the acute response of extracellular acid-base balance to hypercapnia, we get a rather complicated answer. The sh (both teleost and elasmobranchs), the cephalopod molluscs, and, to a lesser extent the crustaceans, show near complete extracellular acid base compensation when exposed to hypercapnia. However, compensation is poor or incomplete in the bivalve molluscs, the echinoderms and the sipunculid worms. More than any of the features we have discussed up until now, poor regulation of extracellular acid-base balance may hold the key to species or taxonomic specic vulnerability to elevated CO2. However, the extent to which this pattern is phylogenetic, and the extent to which it is linked with differences in metabolism (sh, cephalopods and crustaceans are much more active than the other groups, have higher metabolism and show less reliance on long term anaerobiosis mechanisms) or iono-regulation (many intertidal or estuarine species show well developed osmo-/ionoregulatory ability), needs much more investigation (cf. Truchot, 1987; Cameron, 1989; Heisler, 1989; Prtner, 1989; Whiteley, 1999; Whiteley et al., 2001; Freire et al., 2007). Certainly any explanation of such a pattern must take into account the fact that iono-regulation is tightly coupled to the maintenance of acid-base balance, as common ion exchange mechanisms (gills, renal systems) are used to achieve both. Thus species that show poorly developed ion regulation should be less likely to possess the physiological machinery required for effective regulation of extracellular acid-base. This seems to be true for the echinoderms and the molluscs. Similarly differences in extracellular acid-base regulation between shallow water and deep sea species, could have been predicted on the basis that deep sea species often show reduced rates of ion exchange across their gills (e.g. Goffredi and Childress, 2001). Maintenance of extracellular pH is not only linked to intracellular pH but is seen as important for the function of respiratory proteins. Both pCO2 (i.e. a specic CO2 effect; Mangum and Burnett, 1986) and
acidity can have pronounced effects on O2 binding by respiratory pigments; hemoglobins (Weber, 1980), hemocyanins (Mangum, 1997), but particularly the annelid pigments erythrocruorin and chlorocruorin (Weber, 1980). Could it be that vulnerability to high CO2 is related to the type of respiratory protein an organism possess? In vertebrate hemoglobins and in the annelid and crustacean respiratory proteins referred to above, increasing pCO2 and/or decreasing pH reduces O2 afnity. However, this is not invariant as in the lugworm Arenicola marina, CO2 increases, not decreases the afnity of eryrthrocruorin for O2 (Weber, 1980). The Bohr effect is the specic effect of pH on O2 afnity and has been interpreted as an adaptive feature in many species, enhancing O2 unloading to acidic tissues. However, it could equally be a maladaptive feature (see discussion in Wells, 1990) as, by reducing the O2 afnity of the pigment it could compromise O2 loading at the gas exchange surfaces. Bohr effects vary greatly from species to species and may be correlated more with ecology than with phylogeny. For example, polychaete species with respiratory pigments which show pronounced Bohr effects inhabit permanent and semi-permanent burrows, e.g. Diopatra cuprea (Weber et al., 1978) whereas those with little or no Bohr effect inhabit transient or restricted burrows, e.g. Marphysa sanginea, Nephtys homergii and Travisia pupa (Manwell, 1960; Weber, 1971; Weber et al., 1978). The squid Illex illecebrosus, appears to have a very nely tuned internal O2 transport system, to supply its high metabolism (Prtner & Zielinski, 1998), but the high sensitivity of its haemocyanin to CO2 is thought to compromise respiratory gas transport while actively swimming in hypercapnic conditions (Prtner et al., 2004). However, it should be noted that respiratory pigments from many infaunal (minor phyla) worm species such as the echiuroids, Lissomyema mellita and Urechis caupa (Mangum, 1992a), the priapulid Priapulus caudatus and the sipunculids Phascolopsis gouldi, Siphonosoma ingens and Thermiste zostericola (Mangum, 1992b) invariably exhibit no Bohr effect, so while ecology may predominate over phylogeny in terms of the CO2 sensitivity of respiratory pigments, still we should not be too hasty in dispensing with the idea of a phylogenetic component in this area. There is also the possibility that increasing extracellular pCO2 can decrease the amount of oxygen bound by a respiratory pigment (the Root effect) (Weber, 1980). The Root effect is predominantly a feature of some haemoglobins and is not ubiquitous, and as such its occurrence and the sensitivity of different groups deserves future attention. Whilst there is a wide range in an organism's sensitivity to hypercapnia across the different marine species, there is currently some tentative physiological evidence to suggest that this sensitivity could be dependant on an organism's phylogeny. If there is a phylogenetic element to sensitivity it seems most likely to be found with respect to extracellular acid-base balance and/or respiratory pigments. So, in light of these weak phylogenetic factors, is there also any evidence to suggest that sensitivity could be a function of other biological / ecological divisions, e.g. habitat or life stage? For example, is there a difference between deep-sea and shallow-water species, infauna and epifauna, benthic and pelagic or between adults and juveniles? Pane and Barry (2007) reported a marked difference in the acidbase responses to acute hypercapnia (24 h, 1% CO2 [approx. 12 800 ppm]) of the deep sea Tanner crab Chionoecetes tanneri and the shallow water Dungeness crab Cancer magister. While C. magister displayed a compensated acidosis with haemolymph pH returning close to pre-exposure levels within 24 h, the extracellular acidosis in C. tanneri was largely uncompensated. Pane and Barry (2007) conclude that deep sea animals such as C. tanneri lack the acid-base regulatory ability to cope with hypercapnic exposure and so CO2 sequestration would be more detrimental to deep-sea fauna, compared with shallow water forms. While these authors are correct when they claim that their data support the proposition of Seibel and Walsh (2001) that deep sea animals exhibit lower metabolisms, and so
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exchange ions at the gills more slowly, than shallow water forms, still great care should be taken in deducing general patterns from such a two-species comparison (Garland and Adolph, 1994; Feder et al., 2000). The shallow-water crab Necora puber also showed near complete compensation during short-term hypercapnic exposure (Spicer et al., 2007) and therefore supports the idea that shallowwater species are more tolerant. However, the response of another shallow water crab, Callinectes sapidus, when exposed to hypoxic hypercapnia in the estuarine environments it inhabits (Burnett, 1997), suggests this general assumption is less robust. Whilst showing a marked compensation to hypercapnia (2% CO2 approx. 15 000 ppm]), C. sapidus sustains a larger decrease in haemolymph pH (Cameron and Iwama, 1987; Cameron, 1978b) than was recorded for the deep sea C. tanneri (1% CO2 [approx. 12 800 ppm]) (Pane and Barry, 2007) over a similar period of time. In fact environmental hypercapnia has been recorded to reduce haemolymph pH in C. sapidus to as low as 7.2, a value 0.6 pH units below that seen in control crabs not exposed to hypercapnic conditions (Cameron, 1985). Long-term studies of the effect of hypercapnia on the extracellular acid-base of other shallow water species have also showed a permanent reduction in haemolymph pH. In the mussel Mytilus galloprovincialis (Michaelidis et al., 2005) and the sea urchin Psammechinus miliaris (Miles et al., 2007) largely uncompensated acidosis was seen when exposed to seawater with a pH of 7.3 and 7.5 respectively. The current evidence would suggest that it is premature to conclude that an organism from the deep sea will be more sensitive to ocean acidication than those from shallow coastal areas. Another major biological division is between organisms that live within the sediment (infauna) and those that live on the sediment surface (epifauna). As CO2 levels within the sediment are invariably higher, and O2 levels lower, than in the overlying water, it may seem reasonable to assume that infaunal species would have an enhanced tolerance of hypercapnia and hypoxia. However, is there any evidence to support this assumption? It has long been known that exposure to hypercapnia in laboratory experiments can be lethal to some marine organisms. Haywood (1925) found that cilia on gills isolated from the mussel Mytilus edulis stopped beating almost immediately in high CO2 (controlling for pH) environments. The lethal effects of hypercapnia have also been shown for a number of different planktonic copepods at pH values b 6.5 (Rose et al., 1977; Yamada and Ikeda, 1999), and for Acartia erythraea at pH levels b 7 (Kurihara et al., 2004). Benthic organisms have also been shown to be susceptible to hypercapnia. Bamber (1990) reported that the critical acid tolerances of marine bivalves, after 30 days exposure, could range from pH 6.6 in Mytilus edulis to pH 6.0 in the oyster Crassostrea gigas. Knutzen (1981), reviewing literature current at that time, found that for several different marine animals lethal effects were only evident at seawater pH b 7.0. This concurs with the conclusions of Michaelidis et al. (2005) that marine bivalves cannot tolerate pH b 7.0 (although they do add that deleterious effects were evident at pH = 7.5). However, the majority of previous studies have focussed on organisms that were assumed to be most sensitive; organisms that live on or above the sea oor. Consequently we still know very little of the susceptibilities of most benthic infauna. Infaunal organisms do indeed tend to inhabit naturally hypoxic and hypercapnic environments (e.g., Atkinson and Taylor, 1988), but does that really mean they will be more tolerant to high levels of CO2 than epibenthic or even pelagic species. Studies by Batten and Bamber (1996) and Widdicombe and Needham (2007), both on the burrowing polychaete worm Nereis virens, would seem to show an infaunal organism that can tolerate seawater with a pH at least as low as 6.5. It has also been claimed that the nemertean Procephalothrix simulus can survive at pH levels down to as low as 5 (Yanfang and Shichum, 2005). However, generic comparisons between infaunal and epifaunal organisms based on such limited evidence would be unwise. What we do know is that some infaunal organisms do naturally experience hypoxic and hypercapnic condi-
tions (together with variations in other affectors of acid-base balance, such as ammonia). For example, water from a burrow of the thalassinidean shrimp Callianassa californiensis has a pH which varies between 6.3 and 7.0 (Torres et al., 1977), and the deposit feeding lugworm Arenicola marina experiences a pCO2 of 3 mmHg (approx. 4 000 ppm) after 4 hours of tidal exposure (Toulmond, 1973). However, such data are surprisingly scant and there is an urgent need to carry out good comparative experiments on survival of hypercapnia by infaunal and epifaunal benthos, in particular concentrating on mobile deposit feeding clams and worms, sediment dwelling sea urchins and burrow dwelling thalassinidean shrimps. Another widely held assumption is that that calcifying species will be more at risk from the effects of ocean acidication than noncalcifying species (e.g., Orr et al., 2005; Raven et al., 2005; Gazeau et al., 2007). While intuitively attractive, and perhaps even correct, we still await a better understanding of the issues surrounding calcication. In particular, the mechanisms acting at the precise sites of calcication (for many animals this is a specialised extracellular space immediately adjacent to the forming exoskeleton, and not the wateranimal interface), and how environmental hypercapnia affects the acid-base balance of this space are still unclear. Consequently, the extent to which the fundamental mechanisms responsible for acidbase regulation are shared by, or are different between, calciers and non-calciers, is crucial to predicting sensitivities of the two groups (e.g. calciers are more likely to have an internal store of buffer base, although it is known that use of this source can be different from species to species). A very recent development is that, counterintuitively (cf. Riebesell et al., 2000 for example), exposure to acidied sea water appears to enhance calcication in planktonic coccolithophores (Iglesias-Rodriquez et al., 2008) and in echinoderms (Wood et al., 2008) but in the latter at least, at the expense of maintaining muscle tissue (i.e. there is a trade-off, see Wood et al., 2008 for details). In this connection it should also be noted that during the PETM (and the Ordovician period, 440500 mya, and Late Triassic, 290 mya) marine invertebrates appeared to maintain the ability to construct calcareous skeletons, even though the atmosphere at that time is thought to have CO2 concentrations, in the case of the PETM, at least an order of magnitude greater than the present day (Berner, 2006 cited in Knoll et al., 2007; Mander et al., 2008). Clearly the ecophysiology of calcifying species should be an urgent focus for those interested in future effects of ocean acidication. A number of recent reports and papers (e.g. Raven et al., 2005) have stated that larvae are a critical stage in an organism's life cycle as they are more sensitive than adults to changes in environmental conditions such as hypercapnia, temperature and salinity. If true, it would imply that organisms with short larval stages will be less affected by acidication than organisms with long planktonic larval stages. Generally speaking it is believed that sensitivity to external perturbation decreases as an organism develops, with the early developmental stages being more sensitive than the adult. There is also the assumption that small animals, or species, are just large animals writ small. There are sufcient empirical grounds to cast doubt on the generality of both of these statements (Burggren, 2005; Spicer and Gaston 1999). Current information on differences in the sensitivities of different life stages does, however, seem to indicate that early life stages are more sensitive to hypercapnia than adults, with some of our best evidence coming from sh (see Ishimatsu et al., 2004, 2005; Kikkawa et al., 2003, 2004; Fivelstad et al., 2003). There are also, however, some invertebrate examples, e.g. Hatching rate of eggs from the copepod Temora longicornis was affected at pH levels that did not affect adult survival (Grice et al., 1973). From the discussions above, concerning extracellular acid-base balance and respiratory pigments, it seems possible that the sensitivity of a species to ocean acidication may be affected by its phylogeny. However, the limited empirical data currently available would suggest that any such relationship between phylogeny and
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sensitivity is extremely weak. There does seem to be stronger evidence, however, that sensitivity could be affected by developmental stage or habitat. In the absence of new data, we should currently assume that species loss will most likely be idiosyncratic. Therefore, impacts on both species richness and taxonomic distinctness measures of diversity will be very difcult to predict without new studies providing increased understanding of the impact acidication on marine organism physiology. 2.3. Could ocean acidication reduce the impact of large organisms on the surrounding environment and associated biodiversity? In benthic systems the activities of some species can have a signicantly large effect on the surrounding biodiversity (see review by Widdicombe and Austen, 2005) primarily by reducing competitive exclusion. This impact on competition can be a result of either density dependant predation / consumption i.e. keystone species (Paine, 1966) or habitat modication and creation of environmental heterogeneity though processes such as reef building and bioturbation, i.e. ecosystem engineering (Jones et al., 1994; Lawton, 1994). Keystone species and ecosystem engineers are predominantly large organisms whose inuence within an ecosystem is proportionately larger than would be expected from their abundance. The majority of these key or critical organisms are relatively large compared to the animals which are affected by their activities (e.g. a predator is often larger than its prey). Consequently, if ocean acidication is to reduce the top-down biological control of benthic biodiversity, we would expect that an organism's sensitivity to acidication would be related to body-size with larger organisms more sensitive than smaller ones over an evolutionary time-scale (see earlier discussion on adaptation by large and small bodied species). From the discussion above, on the effect of CO2 on different developmental stages, different body sizes, and on the ability of species to adapt to high CO2, we can conclude two things. Effects of body size are almost always confounded by the fact that embryonic and larval individuals are generally smaller than the adults, making it very difcult to disentangle body size and development as different factors. If larvae of a particular species are, lets assume, more sensitive to CO2, is that because they are larvae or because they have a smaller body size than the adult stages? And can we equate differences in the effects of CO2 on different sized individuals during development with differences in CO2 effects between species when the adults have different body sizes? There are no rigorous studies of the effect of CO2 where size and development are separated out, and where intra- and inter-specic CO2 effects on body size have been explicitly investigated. Even interspecic comparisons where adults are compared (as a way for controlling for development) have no formal comparisons of large versus small body sized species. In fact even nding a meaningful metric may be difcult for some of the groups of interest, e.g. a sea urchin may occupy twice as much space as a crab, but in terms of metabolically active tissue may be a fraction of the size. So our rst conclusion is that we have no good comparison of CO2 sensitivity and body size (intraspecically, controlling for development, or interspecically). Secondly, when discussing adaptation we implied that, all other things being equal, smaller bodied species would have a greater chance of adapting than larger bodied species (see above). So the working hypothesis for the moment must be that smaller bodied species will be more vulnerable to high CO2 within a single generation but larger bodied species will be more vulnerable across generations. Alternatively, a reduction in the top-down biological control of benthic biodiversity could come about not just through the complete loss of important species but also through a reduction in that species activity (e.g. feeding rates, bioturbation, burrow irrigation). Metabolic depression (a reduction in metabolic activity) in response to high CO2 has been documented but it is not ubiquitous. Such depression is often associated with a decrease in intracellular pH, as the latter
compromises the activities of numerous enzymes, including those involved in intermediate metabolism (Somero, 1985). In S. nudis there is a hypercapnia-induced metabolic depression although it appears to be correlated more with acidosis of the extracellular than the intracellular uids (Reipschlger and Prtner, 1996; Prtner et al., 1998). Where Amphiura liformis showed hypercapnic-induced metabolic depression, Hemipholis elongata did not (Christensen and Colacino, 2000). The extent to which this is related to the possession of a respiratory pigment (haemoglobin) by the latter, but not the former, is not known. It is interesting though that the O2 binding properties of the haemoglobin are insensitive to pH (Christensen et al., in prep cited by Christiensen and Colacino, 2000). Hypercapnia results in a reduction in oxygen uptake (controlling for activity) in sh, although sensitivity decreases with increasing acclimation temperature (Basu, 1959) (see also metabolic depression N 2% CO2 Cruz-Neto and Steffensen, 1997). However, oxygen uptake (as a measure of aerobic metabolism) of the shrimp Paleomonetes pugio and the sh Fundulus heteroclitus were unaffected by hypercapnia (pCO2 = 68 mmHg) (Cochran and Burnett, 1996). In fact hypercapnia instead of reducing activity could under some circumstances actually increase it (at least in the short term). For example, hypercapnic sh were hyperactive (struggling behaviour) and showed a decreased blood ow to the gut, although the results of this reaction for food assimilation are as yet unknown (Farrell et al., 2001). More tantalisingly very recent work by Wood et al. (2008) on echinoderms seems to indicate that metabolic rate may actually increase in acidied water. It is suggested that the discussion above allows us to formulate a specic prediction that larger bodied species will be more vulnerable across generations to hypercapnia than small bodied species, particularly if rates of adaptation are shown to correlate with body size. In addition, some, but not all, species may exhibit reduced metabolic activity resulting in reduced behavioural activity and growth. If there is an increase in metabolism this will be traded off against a cost elsewhere (growth, reproduction, or other maintenance activities). Both of these factors could potentially lead to a reduction in top-down biological control and a subsequent reduction in biodiversity. However, the caveat still remains that more data are needed and these predictions are just that, predictions, that require empirical testing. 3. The relationship between biodiversity and ecosystem function in a high CO2 future There are currently two major impediments to predicting the impact of ocean acidication on the biodiversityecosystem function relationship. Obviously the rst is the lack of relevant empirical data currently available which describe the response of biodiversity and ecosystem function to ocean acidication. Currently, there are no published studies that have directly measured the impact of acidication on the diversity and structure of benthic communities and only one published study which has measured the impact of ocean acidication on a relationship between a benthic organism and ecosystem function (Widdicombe and Needham, 2007). The second and perhaps the more fundamental impediment is that there is still no consensus as to the existence of predictable relationships between biodiversity and ecosystem function. This is despite the fact that the relationship between biodiversity and ecosystem functions has been a dening feature of ecology in the last decade (Chapin et al., 1998; Loreau et al., 2001), and that investigation and discussions have at last encompassed marine habitats (e.g., Gessner et al., 2004; Worm et al., 2006). The identication of any general relationship(s) as might exist have proved elusive when tested for empirically (e.g., Naeem et al., 1994, 1995; Tilman et al,. 1996; Schwartz et al., 2000; Diaz and Cabido, 2001; Reich et al., 2004; Hooper et al., 2005), as has the investigation of three of the most commonly suggested underpinning mechanisms; 1) complimentarity of species, 2) interaction(s) between species, 3) likelihood of including
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more inuential in terms of function, species (sampling effect) (Naemm, 2002). Our current broad understanding is that while an increase in species richness (as a proxy for Biodiversity) appears to lead to an increase in species redundancy, it also results in greater resilience of ecosystems to external perturbation, partly through an insurance effect (McGrady-Steed et al., 1997; Hooper et al., 2005; Reusch et al., 2005; Tilman et al., 2006). Still there is considerable practical interest in furthering that understanding (Battarbee et al., 2008). 4. Summary In science, ideas and paradigms tend to evolve over time as bodies of work gradually build to support new ideas and theories. Occasionally, however, sudden shifts in understanding leave the scientic community facing a void of knowledge that urgently needs to be lled; Ocean acidication being an example of this. In such times there is a temptation to seize on what few data exist and make broad assumptions and generalisations. Whilst it is important for scientists to erect challenging and provocative hypotheses we must always be conscious of the quantity and quality of the data that support them. In this paper we have used data from ocean acidication experiments and earlier work from physiological studies to review several of the current assumptions that are used to predict the likely impacts of ocean acidication on marine biodiversity and the services this diversity supports. We conclude that there is clear potential for the chemical changes associated with ocean acidication to impact on individuals at a physiological level particularly through disruption of extracellular acid-base balance. There is some weak evidence that the severity of this impact could be related to an organism's phylogeny suggesting that both species and taxonomic measures of biodiversity could be reduced. However, there is also evidence that potential species extinctions will be more strongly governed by factors related to an organism's lifestyle and activity (e.g. infaunal v epifaunal, deep v shallow, deposit feeder v suspension feeder, large v small) than by its phylogeny. There is also huge uncertainty as to what extent organism adaptation or acclimation will mitigate the long term effects of ocean acidication. There are clearly still many gaps in our understanding that prevent us from condently predicting the changes in biodiversity likely to result from forecast changes in seawater chemistry over the next 100 years. Ocean acidication has highlighted the fact that we still do not have a truly holistic understanding of the processes and tradeoffs that make up an organism's physiology. This must be a priority for future research. Other priorities must be studies which increase the ecological understanding of the mechanisms and interactions that structure marine communities and studies that quantify the capacity of animals to adapt and evolve. Only by investing in multidisciplinary research that brings together physiology with population, community and evolutionary biology, will we be able to predict the effects of not only ocean acidication but other, as yet unforeseen, environmental challenges faced by marine ecosystems. Acknowledgments This paper is a contribution to the Plymouth Marine Laboratory core project Oceans 2025. SW would also like to thank John Gray for his broad minded and positive attitude towards novel science. In 2003, a time when ocean acidication was relatively unknown, John reviewed a grant application which aimed to address issues associated with low pH and benthic systems. His positive comments helped the grant gain funding; money which supported much of the benthic ocean acidication research subsequently conducted at PML. We also thank Nia Whiteley for her constructive comments on the manuscript and Steve Grimes for information on the PETM. [SS]
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