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- Material and methods
- Supporting Information
Ocean acidification is considered as a global threat to marine ecosystems (Doney et al. 2009a; Fabry et al. 2009; Kleypas & Yates 2009). It is caused by rising atmospheric carbon dioxide (CO2) concentrations, which drive changes in seawater carbonate chemistry and reduce pH (Gattuso & Buddemeier 2000). This process of ocean acidification is underway (Solomon et al. 2007) and will accelerate with increasing CO2 emissions over the course of the current century (Caldeira & Wickett 2003; Meehl et al. 2007). Many marine organisms, from phytoplankton to fish, are sensitive to changes in carbonate chemistry, and their responses to the predicted changes could lead to profound ecological shifts in marine ecosystems (reviewed by Doney et al. 2009b). As such, ocean acidification has become a priority area for research, and the number of experiments examining its effects on marine organisms has grown exponentially. Marine organisms vary broadly in their responses to ocean acidification, in part due to the wide variety of processes affected (e.g., dissolution and calcification rates, growth rates, development and survival), making it challenging to predict how marine ecosystems will respond to ocean acidification.
Several hypotheses have been proposed to explain the variation in biological responses, including: (1) organisms that have a calcium carbonate (CaCO3) structure will be more sensitive to ocean acidification than organisms that do not, (2) organisms with more soluble mineral forms of CaCO3 in their structure (e.g., aragonite) will be more sensitive than organisms with less soluble mineral forms (e.g., calcite), (3) early life history stages will be more sensitive than later life history stages, (4) highly mobile organisms with high metabolic rates may be more capable of compensating for changes in carbonate chemistry than sessile organisms with low metabolic rates and (5) autotrophs with less efficient or absent carbon-concentrating mechanisms (CCMs) will be more responsive than those with efficient CCMs. Below, we briefly review the leading hypotheses for variation in sensitivity to ocean acidification.
The sensitivity of calcification to ocean acidification may vary amongst calcifying organisms. Sensitivity may depend on the mineral form of CaCO3 used by the organism, with the solubility and susceptibility increasing from low-magnesium calcite to aragonite and high-magnesium calcite (Morse et al. 2006; Ries et al. 2009). However, some species may be better able to control pH near calcification sites under differing external conditions, and thereby may be better equipped to cope with ocean acidification (Berry et al. 2002; Cohen & McConnaughey 2003; Taylor et al. 2007). Additionally, some organisms may be able to compensate for changes in carbonate chemistry by increasing calcification rates (Gutowska et al. 2008). Finally, the sensitivity of calcification processes may be buffered for calcifying algae and corals with symbiotic autotrophs due to interactions between photosynthesis and calcification. It is known that photosynthesis can stimulate calcification across numerous taxa (Borowitzka 1982; Gattuso et al. 1999, 2000; Rost & Riebesell 2004). If photosynthesis increases in these organisms under ocean acidification, it could potentially buffer the negative effects on calcification (Ries et al. 2009).
In addition, early life history stages may be more vulnerable to ocean acidification than adults. The larval and juvenile stages of marine organisms are typically more sensitive to environmental conditions (Pechenik 1987), and can suffer extremely high mortality (Gosselin & Qian 1997). Additionally, some invertebrates begin calcifying during the larval (echinoderms and molluscs) or juvenile (corals and crustaceans) phases (Kurihara 2008). During these phases of calcification, they may rely on a more soluble mineral form of CaCO3 than the mineral used as an adult (Weiss et al. 2002; Addadi et al. 2003). Indeed, some echinoderms have shown delayed development or high mortality during larval stages when exposed to ocean acidification (Dupont et al. 2008).
Organisms may also vary in their sensitivity to ocean acidification in other physiological processes. Reduced seawater pH can disrupt the acid–base status of extracellular body fluid (e.g., blood or hemolymph). Highly mobile organisms such as fish, cephalopods and some crustaceans that are capable of controlling extracellular pH through active ion transport are predicted to be more tolerant of acidification (Gutowska et al. 2008; Pörtner 2008; Melzner et al. 2009). In turn, organisms unable to compensate for the reductions in extracellular pH have shown depressed metabolism, growth and fitness (Pörtner et al. 2004; Michaelidis et al. 2005; Siikavuopio et al. 2007). Higher maintenance costs in stressful abiotic environments could cause changes in energy allocation to reproduction and somatic growth.
The ability of marine autotrophs to increase photosynthetic rates under ocean acidification could also contribute to variation in organismal responses. Marine autotrophs rely on CO2(aq) or the bicarbonte ion (HCO3−) for photosynthesis, which will both increase in concentration with ocean acidification. However, many marine autotrophs utilize CCMs and do not appear carbon limited under current conditions (Raven & Beardall 2003). Yet there is variation in the efficiency of CCMs, and marine phytoplankton with less efficient CCMs have shown the capacity to increase photosynthetic rates in carbon and nutrient replete conditions (Rost & Riebesell 2004; Engel et al. 2005; Riebesell et al. 2007). In addition, seagrasses primarily rely on CO2(aq) and have shown increased photosynthesis and growth under conditions of ocean acidification (Zimmerman et al. 1997; Palacios & Zimmerman 2007; Hall-Spencer et al. 2008).
A recent quantitative review concluded that most biological processes are not significantly affected by near-future ocean acidification (Hendriks et al. 2010). However, that review did not use the standard methods for meta-analyses – quantitative methods for combining the results of several studies into an overall mean effect – which standardize studies for precision, account for variation between studies, and test for heterogeneity in effect sizes. Significant heterogeneity suggests there may be differences in responses between groups of studies, which can have ecologically important implications and guide the interpretation of the overall results of the meta-analyses (Hedges & Olkin 1985; Gurevitch & Hedges 1999; Rosenberg et al. 2000). For these reasons, heterogeneity is of primary interest when trying to quantify the variability or draw general conclusions, and we focus our current analysis on describing the variation in responses to ocean acidification.
A better understanding of the variability or generality of the biological responses is necessary to provide support for emerging hypotheses and highlight areas where further research is necessary. We quantified variation in biological responses to ocean acidification using meta-analyses. Specifically, we tested whether ocean acidification had a negative effect on survival, calcification, growth and reproduction, and a positive effect on photosynthesis. Within these categories, we tested the following hypotheses: Ocean acidification has a larger effect on (1) calcifying organisms vs. non-calcifying organisms, (2) highly soluble mineral forms of CaCO3 vs. less soluble forms and (3) early vs. later life history stages. To examine variability associated with other life history characteristics (e.g., mobility, metabolism and photosynthesis), we tested for differences between broad taxonomic groups. Finally, we tested whether the experimental methods (carbonate chemistry manipulation, magnitude of pH manipulation, duration of experiment) caused systematic biases in the results. As predicted, we found ocean acidification had negative effects across numerous processes, and that organisms with calcified structures were generally more sensitive. Results of this synthesis indicate that responses differ amongst taxonomic groups, regardless of the methodology used in experiments, and that some organisms appeared more resilient to acidification changes than others.
- Top of page
- Material and methods
- Supporting Information
The meta-analyses revealed significant negative effects on survival, growth, calcification and reproduction, suggesting predicted ocean acidification conditions will have negative consequences for many marine organisms by the end of this century. Calcification was the most sensitive process, and our analyses suggest calcifying organisms are more susceptible to ocean acidification across other response variables. This pattern was also highlighted in the differences in taxonomic groups, where survival and growth were negatively affected across most calcifiers. Our analyses also revealed additional variation in responses to ocean acidification that was driven by differences amongst taxonomic groups, with organisms such as crustaceans, fish and fleshy algae responding positively to changes in carbonate chemistry. In addition, we found that the differences in effect sizes between developmental stages were specific to taxonomic groups. With the exception of crustaceans, these results suggest the effects of ocean acidification will be negative for most calcifying organisms, but that variation in life history characteristics will prove some organisms more resilient than others.
Our results are in contrast to a previous meta-analysis, which concluded there was no consistent evidence for negative impacts on biological rates (with the exception of calcification rates for bivalves) under near-future ocean acidification scenarios (Hendriks et al. 2010). The differences in our conclusions can be explained by several factors. First, there was little overlap in the studies included in both analyses (i.e., 17 studies were shared by both analyses, and we included the results from 56 additional studies). Thus, the results from our meta-analyses represented a different dataset. Next, Hendriks et al. (2010) included multiple responses from the same experiments in the meta-analyses, which weighted the experiments reporting multiple responses more heavily than others. Additionally, Hendriks et al. (2010) included the response(s) of Zostera marina reported by Zimmerman et al. (1997), which was excluded from our analyses because of its disproportionate influence on the significance of our results, as indicated by the sensitivity analyses. There are also methodological differences between the studies, including our choice of an effect size metric, LnRR, and the model used for meta-analysis (i.e., random effects), and use of resampling statistics for determination of significance. Finally, our interpretation of the overall effects of ocean acidification differs from the previous analysis due to the significant heterogeneity highlighted in the categorical and continuous analyses.
The magnitude of the effect of ocean acidification on calcification was similar amongst calcifiers, with the exception of crustaceans and calcifying algae. This is somewhat surprising given the different calcification strategies (i.e., intracellular vesicles in coccolithophores vs. extracellular compartments in scleractinian corals). The negative responses of corals and coccolithophores to ocean acidification could have profound repercussions for marine ecosystems, with scleractinian corals serving as habitat for coral reef ecosystems and coccolithophores serving as the foundation of its food web. Crustaceans, however, appeared unaffected under conditions of ocean acidification, and the responses of calcifying algae were highly variable. These results are in contrast to the hypothesis that organisms utilizing high-Mg calcite will be more sensitive to ocean acidification because both crustaceans and coralline algae (which made up most of the calcifying algae category) utilize high-Mg calcite for calcified structures. This hypothesis, based on the solubility of the pure mineral forms in seawater, may fail to predict the sensitivity of marine organisms to ocean acidification because it does not account for biogenic calcification processes (Pörtner 2008). Crustaceans maintain a high control of their intracellular pH through ion-transport regulation (Wheatly & Henry 1992), suggesting they may have the ability to optimize environmental conditions at the calcification site. Additionally, the exoskeleton of most crustaceans is covered by an extensive biogenic covering, which can buffer their CaCO3 structures from direct dissolution in acidified seawater (Ries et al. 2009). Finally, unlike the other calcifiers included in our analysis, crustaceans moult their shells regularly and have less CaCO3 in their structures. As such, our results do not support the hypothesis that more soluble forms of CaCO3 will be more sensitive to ocean acidification, and the resilience of crustaceans and coralline algae requires further experimentation to understand the mechanisms for their responses.
Our results do not support the hypothesis that increased photosynthetic carbon assimilation amongst photosynthesis utilizing organisms in response to ocean acidification can buffer its effects on calcification. Coccolithophores have less efficient CCMs than many marine autotrophs, and can increase carbon assimilation under conditions of ocean acidification (Rost & Riebesell 2004). Despite this experimental evidence, we found an overall reduction in calcification. In addition, we did not detect an effect of ocean acidification on symbiotic coral zooxanthellae photosynthesis, and calcification in the host corals was reduced. For coral symbionts, photosynthesis is limited by inorganic nutrient supply, and experimental work suggests that calcification rates can be maintained under conditions of ocean acidification if the nutrient supply and consequently the primary and secondary production are increased (Langdon & Atkinson 2005; Cohen & Holcomb 2009; Ries et al. 2009).
Our results support the hypothesis that highly mobile organisms with developed intracellular/extracellular pH regulatory mechanisms may be more resilient to ocean acidification. Both fish and brachyuran crustaceans have well-developed pH regulation and were not negatively affected by the changes in carbonate chemistry. Interestingly, even though we detected significant increases in calcification amongst crustaceans, we were not able to detect significant effects on their growth. The decoupling of calcification and growth for these organisms may be explained by energy allocation strategies. If crustaceans use more energy to maintain calcification, this could result in reduced energy allocation to growth. This hypothesis is in contrast to the results of Arnold et al. (2009) where the European lobster Homarus gammarus (L.) larvae developed less calcified exoskeletons but maintained their growth rates under high CO2/low pH conditions. In this instance, decreased calcification paired with increased growth could signal an opposing energy allocation strategy. However, these hypotheses assume that calcification processes are growth limiting, which may not be true for organisms that do not have extensive calcified structures or fast growth rates.
We did not detect significant effects of ocean acidification on photosynthesis in the overall weighted, random effects analysis. Although seagrasses use CO2(aq) for photosynthesis and the dominant coccolithophore species Emiliania huxleyi has a relatively inefficient CCM, neither group showed significant effects. However, these results differed in the unweighted, fixed effects analyses that included more experiments. In these analyses, all taxonomic groups responded positively to ocean acidification. The switch from non-significant to positive effects in the unweighted, fixed effects analysis was not driven by studies with especially large pH manipulations (data not shown), because most of the additional studies had experimental pH reductions < 0.5 units. Although photosynthesis was positively affected in the unweighted, fixed effects analysis, the magnitude of the effect sizes remained very small compared to other response variables, suggesting the photosynthetic responses of marine autotrophs are more subtle and less variable than the other response variables.
We did not detect variation amongst the mean effects of differing developmental stages across most response variables. However, this does not necessarily indicate differential sensitivities do not exist amongst life stages. Instead, these differences may be swamped by more pronounced causes of variation, such as taxonomic differences. While experiments examining larval responses were generally lacking, the categorical weighted meta-analyses amongst developmental stages within taxonomic groups showed significant differences amongst life stages (see also Dupont et al. 2010), but the patterns varied depending on the taxonomic group in question. These results indicate differential sensitivities amongst life stages is small compared to the degree of variation caused by differing life histories, and the most sensitive life stage may differ amongst taxonomic groups (Kurihara 2008).
Although our analyses highlighted several biological factors that explain variation in responses to ocean acidification, there are still likely to be species-specific sources of heterogeneity (Dupont et al. 2008; Fabry 2008; Kurihara 2008). Experimental work has shown that closely related species can respond very differently to the same conditions. For example, the echinoderm Echinus esculentus larvae had high mortality under ocean acidification, while the echinoderm Strongylocentrotus droebachiensis larvae showed increased developmental success (Dupont & Thorndyke 2009). These species-specific differences may be more pronounced within certain taxonomic groups, and are likely responsible for our inability to detect strong effects of ocean acidification on calcification in coccolithophores or photosynthesis in seagrasses. For example, it appears that strains of the coccolithophore species E. huxleyi have different responses to ocean acidification (Langer et al. 2009; Ridgewell et al. 2009); and some species of seagrass significantly increase photosynthesis under reduced pH, whereas other species are relatively immune to the changes due to differences in their CCMs (Invers et al. 1997). The sources of variation between closely related species (or strains) remain a fruitful area of research for examining mechanisms for resiliency. However, we were able to detect significant negative effects of ocean acidification across all response variables except photosynthesis despite differing species, life histories and developmental stages indicating the differences caused by species-specific variation are minor compared to the overall effect of ocean acidification.
It is important to note that ocean acidification will occur in concert with other environmental changes, and the biological responses we have highlighted may differ with the presence of additional stressors. Several studies have considered the combined effects of ocean acidification and increased temperature on marine organisms. Although not included in our analyses, increased temperatures both increased and decreased the severity of the effect size of ocean acidification (Reynaud et al. 2003, 2004; Hare et al. 2007; Anthony et al. 2008; Findlay et al. 2008; Byrne et al. 2009; Martin & Gattuso 2009; Munday et al. 2009). However, it is not apparent what drives the direction of the response (i.e., increasing or decreasing in severity). Organisms differ in their thermal tolerance, and within their range of tolerance, increased temperatures can increase physiological rates and may buffer negative effects of ocean acidification. Outside their range of tolerance, increased temperatures are detrimental and could compound any stress caused by acidification (Pörtner 2008). Additionally, the responses of marine autotrophs are dependent on light intensity and nutrient concentrations, with increased light and nutrient supply potentially buffering any negative impacts of ocean acidification (Zondervan et al. 2001, 2002; Rost et al. 2002). Accurate forecasting of ocean acidification’s impacts on marine organisms will require additional studies examining these interactions between multiple environmental stressors.
We did not detect strong effects of methodological factors on effect size. The method of carbonate chemistry manipulation did not consistently explain heterogeneity in effect sizes. This is consistent with reviews of methodology that indicate the speciation of carbonate parameters is very similar between both DIC addition at constant TA and manipulation of TA at constant DIC for moderate pCO2 levels (c. 700 p.p.m.) (Ridgewell et al. 2009; Schulz et al. 2009; Shi et al. 2009; Gattuso et al. 2010). In addition, the magnitude of the unit change of pH did not predict the effect size for most of the analyses. The significant relationship between unit change in pH and the effect size in the growth analysis was driven by a few very negative effect sizes amongst echinoderms, and in combination with the other analyses, does not provide strong support for a linear relationship. This could be indicative of nonlinear relationships between pH and effect sizes, including the possibility of thresholds or tipping points (Scheffer et al. 2001; Ries et al. 2009). This also suggests the selection criteria did not have a systematic bias on the effect size (e.g., by only including studies with less than a 0.5-unit pH reduction our effect size estimates were not consistently underestimating the true effect size). More experiments that examine the relationship between unit change in pH and effect size will shed light on how the magnitude of the carbonate chemistry manipulation drives biological responses.
Additionally, we did not find strong support for a linear relationship between the duration of the experiment and the effect size. There were a few significant comparisons, however, the slopes of the fitted lines were nearly zero in all cases, and there was no trend in the direction of the slopes (Table 1). These correlations are dependent on the studies and species included in the analyses, and significant correlations could be unrelated to the methodological factors being tested. Overall, our results suggest methodological factors did not explain the variation in responses to ocean acidification.
The results of the sensitivity analyses suggest that the patterns highlighted in our meta-analyses are a robust representation of the current literature on ocean acidification. The results from the unweighted, fixed effects analyses of the larger dataset are very similar to the main results, suggesting our selection criteria for studies did not bias the results. However, the significance of the photosynthetic responses of marine autotrophs in the unweighted, fixed effects analysis suggests the power of the main photosynthesis analysis may have suffered from low sample size. Unfortunately, we did not include several studies because they did not report enough information to ensure their comparability (e.g., seawater pH or two parameters of the carbonate chemistry). The inclusion of all applicable studies is always preferable in meta-analysis (Englund et al. 1999) and this problem highlights the importance of data reporting in future ocean acidification research. Finally, it is important to consider that the published literature is probably biased towards studies that find significant effects.
Even though we included as many studies as possible to examine the biological responses to ocean acidification, the studies were limited to a few taxonomic groups and even fewer ecosystems. Although ocean acidification is predicted to be a global stressor, the literature is dominated by studies in coral reef and pelagic ecosystems. Studies are needed in other coastal environments, including variable pH environments (e.g., upwelling zones, CO2 vent systems and estuarine areas) to explore whether history of exposure to a more variable pH environment confers adaptation potential. More physiological studies are needed to understand how these individual responses combine to affect performance and fitness of marine organisms, and long-term studies are needed to address possible acclimation or adaptive responses. Additionally, studies are needed that examine the ecological consequences of reduced performance/fitness in marine communities or ecosystems.
In conclusion, our analyses revealed a strong negative effect of ocean acidification on marine organisms despite the variation in the sensitivity of taxonomic groups and developmental stages. However, differential sensitivities still have important implications for marine ecosystems where individual species often play disproportionately strong roles in structuring communities (Shurin et al. 2002; Borer et al. 2005). Additionally, differential sensitivities will influence species interactions and could drive unforeseen impacts on marine communities and ecosystems. However, this synthesis did not support all the leading hypotheses for variation in response to ocean acidification (i.e., early developmental stages and more soluble CaCO3 polymorphs are more susceptible to ocean acidification). But instead, we found the explanatory power of these hypotheses was specific to organisms within taxonomic groups. This research has important implications because a clear understanding of the magnitude and the sources of the variation in the responses to ocean acidification will allow managers and policy makers to make more accurate generalizations, and improve the accuracy of models and forecasts for ocean acidification’s impacts. Further progress in explaining the variation in biological responses to ocean acidification will require studies targeting the biological mechanisms for variation.