Abstract
Feeding is fundamental for all heterotrophic organisms, providing the means to acquire energy for basic life processes. Recent studies have suggested that experimental ocean acidification (OA) can alter the feeding performance of marine calcifying invertebrates, but results have been inconsistent. While several reviews pertaining to the biological effects of OA exist, none provide a synthesis of OA effects on feeding performance. Here, we provide a quantitative analysis of published experiments testing for effects of elevated CO2 on feeding rates of marine calcifying invertebrates. Results revealed that suspension-feeding molluscs and predatory and grazing echinoderms experienced depressed feeding rates under elevated CO2, while arthropods appeared unaffected; larval and juvenile animals were more susceptible to CO2 effects than adults. Feeding strategy did not appear to influence the overall taxonomic trend, nor did habitat, although exposure time did have an effect. AIC model selection revealed that Phylum best predicted effect size; life stage and exposure time were also included in candidate models. Based on these results, we synthesize potential physiological attributes of different taxa that may drive OA sensitivities in feeding rates, which could potentially result in community-level impacts. We also discuss CO2 effects on calcifier feeding in the context of elevated temperature and other global marine change stressors, and highlight other areas for future research.
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Introduction
Maintaining energy balance in the face of environmental stressors is fundamental to life. The amount of food an animal consumes, when balanced with energetic losses (due to various functions such as metabolic processes, growth, development, repair, activity, reproduction, homeostatic maintenance, thermal regulation), can dictate the animal’s energy reserves. Since basic biological functions are sustained by available food reserves during periods of depressed food supply (Kooijman, 2009), animals that are unable to gather and process food efficiently may inevitably exhaust these reserves faster than animals that can feed and process food more effectively. An inability to feed effectively may therefore negatively impact the above-mentioned core functions, in turn impacting organism survival (Pepin et al., 2014). Thus, although several other processes are involved, examining animals’ feeding responses to stressors is one way to estimate energy acquisition.
Given the important link between feeding and fitness (survival and reproduction), it is important to understand the environmental factors that can influence feeding for marine organisms. These can include (but are not limited to) food availability (Wong & Cheung, 2001), temperature (Sanford, 2002; Norman, 2012), salinity (Lankford Jr. & Targett 1994; Chaparro et al., 2008), and oxygen concentrations (Pihl et al., 1992; Breitburg et al., 1994). In addition, ocean acidification (OA) is recognized as one of the greatest threats to marine biodiversity (Secretariat of the Convention on Biological Diversity, 2009; Hendriks et al., 2010, Howes et al., 2015). OA describes the reduction in oceanic pH and associated alterations to the marine carbonate system resulting from the absorption of excess anthropogenic CO2 by the oceans (Caldeira & Wickett, 2003; Orr et al., 2005). Since the onset of the Industrial Revolution, surface ocean pH has dropped by ~ 0.1 units and is expected to decline by further 0.2–0.3 units by the end of this century (RCP8.5 scenario; Hoegh-Guldberg et al., 2014). In estuarine and coastal environments where high productivity, terrestrial (nutrient) and freshwater input, and upwelling can lead to large diurnal and seasonal fluctuations in pH, the effects of OA are more variable and can be locally altered (Cai et al., 2011; Duarte et al., 2013). Given the intrinsic link between an organism’s physiology and its environment, it is thus important to consider the potential effects of OA on the feeding rates of marine organisms.
While OA is likely to have impacts on many marine organisms (Kroeker et al., 2013), the energetic costs of calcification and reliance on a calcium carbonate shell or skeleton make calcifying taxa some of the most vulnerable to OA effects (Orr et al., 2005; Ries et al., 2009; Hofmann et al., 2010; Howes et al., 2015). Resistant taxa are likely to be those that can offset effects of adverse water chemistry by maximizing feeding and energy use efficiency. The energetic costs of calcification are generally suggested to increase under elevated pCO2 conditions (but see e.g. Schoepf et al., 2013 for exceptions); however, at present, insufficient empirical evidence exists to successfully decouple the costs of calcium carbonate precipitation from perturbations of homeostatic maintenance, metabolic processes, and acid–base perturbations to the costs of each of these processes independently (Fernández-Rieriz et al., 2011). Recent evidence has suggested that if enough food is available, some marine calcifiers may be able to overcome these energetic constraints and succeed under conditions of elevated pCO2 (Thomsen et al., 2013; Pan et al., 2015; Towle et al., 2015; Ramajo et al., 2016a, b). However, food availability is highly variable in marine systems, and it is unknown how future climate change may impact a populations’ food sources. Consequently, species in which feeding rates are depressed under elevated pCO2 are likely to be negatively impacted. In contrast, species exhibiting increased feeding efficiency under elevated pCO2 may be able to tolerate OA. The limits of such physiological tolerances can select “winners” and “losers” on an ecosystem scale under future OA scenarios.
Studies assessing the impact of OA on marine calcifier feeding have been increasing recently. However, while numerous reviews pertaining to the biological effects of OA exist (Gazeau et al., 2013; Harvey et al., 2013; Kroeker et al., 2013; Wittman & Pörtner, 2013; Clements & Hunt, 2015; Lefevre, 2016), none provide a quantitative analysis of OA effects on feeding rates. Here, we provide a quantitative synthesis of OA effects on the feeding rates of calcifying marine invertebrates by reviewing published experiments. We identified groups of marine organisms that may be differentially impacted by OA with respect to their feeding rates, propose mechanisms to explain these differences, and discuss knowledge gaps and prospects for future research.
Methods
Literature search and data collection
Articles were searched for via Web of Science and Google Scholar (up until March, 2017) using the keywords ‘ocean acidification’ or ‘carbon dioxide’ plus ‘feeding rate’ and/or ‘ingestion rate’ and/or ‘consumption rate’ and/or ‘clearance rate’ anywhere in article (all raw data in Table S1). We then conducted a cited literature search of each article obtained from the online literature search to collect any articles that may have been missed in the online search. This provided us with a reasonable number of publications to test hypotheses regarding OA effects on calcifier feeding rates (n = 55; see Results). While studies exist testing effects of OA-exposed food (i.e. active prey or passive food particles) on feeding of consumer organisms reared under ambient conditions (e.g. Amaral et al., 2012; Rossoll et al., 2012; Dupont et al., 2015; Benítez et al., 2016; Duarte et al., 2016; Isari et al., 2016), we only included studies that reared the target consumer organism under elevated pCO2 to describe the direct effects of OA on feeding. Consumer organisms were either predators, grazers, or suspension feeders. For data comparability, feeding rates, grazing rates, ingestion rates, clearance rates, and filtration rates were included as comparable measures of feeding.
To control for local adaptation, we assumed that each study chose control pCO2 conditions appropriate for their target species. The highest pH level (or lowest pCO2 level) employed in each experiment from each study was considered the control treatment and we considered all pCO2 levels > 600 µatm (low-end prediction for 2050) as OA treatments; intermediate pCO2 levels < 600 µatm were discarded. For studies reporting different acclimation periods or experimental durations, we considered all acclimation times in our analyses. We considered each experimental treatment as an individual data point (as per Harvey et al., 2013; Kroeker et al., 2013). Thus, if studies used > 1 experimental assay, species, size, relevant pCO2 level, or food supply, we treated each as an individual observation. For experiments that tested the combined effects of acidification and other environmental stressors (i.e. warming and hypoxia) on feeding rates, we only assessed differences between acidification groups for the control/ambient levels of the other factors.
From each study, we collected general information for each species tested, including Phylum, life history stage (larval, juvenile, or adult), feeding strategy at the life stage assessed (suspension, grazer, deposit, predator, or scavenger), and whether the life stage tested was a benthic or pelagic consumer. We also collected general study information, including units used to measure feeding performance, geographic location from which the animals were collected, pH and/or pCO2 conditions of each relevant OA treatment, and duration that individuals were reared under experimental or control conditions prior to feeding measurements (hereafter referred to as ‘acclimation duration’, measured in days). Each of these parameters was then divided into categories (Table 1). Acclimation duration categories were chosen to represent a range of exposure times (see Table 1). The pCO2 categories were based on upper-end projections for various time periods, including before year 2100 (i.e. end-of-century; < 1000 μatm), 2100–2200 (1000–1500 μatm), 2200–2300 (1501–2000 μatm), and beyond 2300 (> 2000 μatm); it is important to note that these categories all fall within the range of currently observed pCO2 values in many nearshore coastal systems.
Effect size analysis
To determine individual and mean effect sizes, we recorded the mean feeding rate, variance (standardized as standard deviation), and sample size for each OA treatment and control treatment for each observation in each study. These values were obtained from published tables, were digitally estimated from published graphs using Image J or PlotDigitizer, were obtained from online databases, or directly from corresponding authors. Means, variances, and sample sizes were used to calculate natural log response ratios (effect size, LnRR) for each experimental group. LnRR is the ratio of the experimental effect to the control effect (natural log transformed). An LnRR value of 0 signifies no effect of the experimental treatment on the response variable, while negative and positive LnRR values signify negative and positive effects, respectively (Hedges et al., 1999). We used LnRR as an effect size because this metric has a high capacity to detect true effects and is robust to low sample sizes (Lajeunesse & Forbes, 2003).
Weighted random effects models were used to derive mean effect sizes (LnRR) for each level in each of the 6 a priori factors outlined in Table 1; mean effect sizes were only calculated for taxa and/or life history stages containing 3 or more observations (n ≥ 3; corals were excluded from the effect size analysis for failing to meet this criterion [n = 2]). Bootstrapped (10,000 replicates) bias corrected and accelerated (BCa) 95% confidence intervals were used to determine statistical significance (significance occurs when 95% confidence interval does not cross 0). Q tests (α ≤ 0.05) were used to test for heterogeneity in effect sizes among studies. All analyses were conducted using R v. 3.3.0 (R Development Core Team, 2016); effect size calculations and analyses were conducted using the Metafor package (Viechtbauer, 2010).
Identifying predictors of calcifier feeding responses to elevated CO2
Once effect sizes were derived for all experimental observations, we used model selection to determine which variables (Phylum, Feeding Strategy, Habitat, Life Stage, Acclimation Time, and pCO2) best predicted effect size. Because “experiment” was used as our unit of replication, we built additive linear mixed effects models (using the “nlme” package in R; Pinheiro et al., 2017) for all possible combinations of predictor variables with “experiment” included as a random variable; we also included a null model (i.e. model without any fixed predictor variables; random factor of “experiment” only). Prior to model construction, we determined the correlation between each of the predictor variables—if two variables had a correlation ≥ 0.80 , then any models incorporating those factors together were discarded (see Table S2). This resulted in a total of 59 models. We then used Akaike’s Information Criterion (AIC; using the “AICcmodavg” package in R [Mazerolle, 2017]) to determine which predictor variables contributed most to explaining effect size variance (Burnham & Anderson, 2002; Anderson, 2007). Models were selected based on AIC and log likelihood values, whereby best models are indicated by the lowest AIC and highest log likelihood values (Burnham & Anderson, 2002). We considered all models with a delta AIC (∆ AIC) ≤ 2 as top candidate models, as those with a ∆ AIC ≤ 2 cannot be confidently identified as inadequate models and thus eliminated (Burnham & Anderson, 2002). All analyses were conducted using R v. 3.3.0 (R Development Core Team, 2016).
Results
Literature search
Our literature search revealed a total of 55 studies assessing the effects of OA on feeding rates in marine calcifying invertebrates, published between 2008 and March, 2017 (Table 2) and spanning across 46 different geographic locations (Fig. 1). Most studies occurred in Europe (n = 20), North America (n = 10), Asia (n = 10), Australia (n = 7), and South America (n = 5) (Nlocation = 53 due to the lack of location information from one study [Houlbrèque et al., 2015] and the utilization of pre-existing data in another study [Jager et al., 2016]). Studies from the eastern coast of South America and the whole of Africa were completely absent, as well as from Greenland, northern Canada and Alaska, central America, western Australia, and northeastern Asia; there was a single study from Antarctica (Fig. 1).
a Map of approximate geographic locations of studies testing the effects of elevated pCO2 on marine calcifier feeding rates. b Cumulative (n = 55) and annual publication counts for studies assessing the effects of elevated pCO2 on marine calcifier feeding rates found in our literature search. c The total number of studies assessing feeding rates in each of four calcifying Phyla. Pie slices represent the relative proportion of each Phyla to the total number of studies found in our literature search. d–f The total number of studies assessing pCO2 effects on feeding rates across different feeding strategies (c), habitats (d), and life stages (e), for each of four calcifying Phyla. Note: The total number of studies across the four Phyla does not necessarily equal 55, as some studies may have employed > 1 divisive unit (i.e. Phyla, feeding strategy, habitat, or life stage)
There was a substantial increase in OA-invertebrate feeding rate studies over the past 3 years (2014–2016; Fig. 1). Most studies assessed the effect of OA on feeding rates in molluscs and arthropods (41 and 38%, respectively), with fewer studies focusing on echinoderms (18%) and corals (4.0%). With respect to mode of feeding, studies equally focused on suspension feeders, grazers, and predators (34.5, 34.5, and 30.9%, respectively). Based on our literature review, no studies have tested the effects of OA on feeding rates in deposit feeders or scavengers (although Zhang et al. (2015) assessed energy absorption in a benthic scavenging mollusc, Nassarius conoidalis (Deshayes, 1832)). Studies have focused more on benthic (67.3%) than pelagic (34.5%) organisms and have put more of an emphasis on adults (50.9%) and juveniles (36.4%) compared to larvae (16.4%) (life stage percentages total > 100% because one study tested both larval and juvenile individuals; Vargas et al., 2015). Across all studies, control pCO2 conditions ranged from 191 to 963 μatm, while elevated pCO2 conditions spanned from 593 to 9274 μatm. Control pCO2 ranged from 191 to 963, 325 to 871, and 380 to 654 for molluscs, arthropods, and echinoderms, respectively (respective means = 457, 519, and 469). Elevated pCO2 conditions were similarly broad for molluscs and echinoderms, while the two coral studies employed a narrower range of pCO2 conditions and the arthropods encompassed a far broader range; the average elevated pCO2 treatment was similar across taxa (Fig. 2). Experiments testing for effects on adult and juvenile calcifier feeding encompassed a similarly broad range of pCO2 conditions, while the range was narrower for larval experiments (Fig. 2). Within studies, the magnitude of difference between control and elevated pCO2 was typically less than 1000 μatm, which is in line with near-future projections.
Ranges of experimental pCO2 conditions (i.e. ocean acidification treatments) encompassed by a each Phylum and b each life stage across the 55 studies assessing ocean acidification effects on marine calcifier feeding. Plots are means and error bars are minimum and maximum values
Of the 55 studies identified in our literature search, 21 (38.2%) assessed OA effects on feeding rates alongside ocean warming (i.e. ≤ + 5°C warming; Table 2). While this sample size is too low to include in a meta-analysis, a comparison of statistical outcomes between OA only treatments and OA + warming treatments in those studies revealed that OA + warming treatments resulted in a far higher percentage of increased feeding rates than of null responses, while the percentage of decreased feeding responses remained about the same (Fig. 3).
The total number of experimental treatments (n = 59) exhibiting increased (light grey bars), decreased (dark grey bars), and unaltered (i.e. null response; black bars) feeding rates in response to elevated pCO2 only (OA only) and elevated pCO2 + elevated temperature (OA + OW) from the 21 studies testing the combined effects of OA and OW on calcifier feeding rates
Effect size analysis
CO2-induced acidification significantly reduced feeding rates for marine calcifiers (Fig. 4a), but these effects varied by taxon, life history stage, and feeding mechanism. Most Q tests for heterogeneity of effect sizes within a priori groups were significant, indicating that effect sizes varied significantly among studies (Table S4). The only groups with significant effect tests with non-significant Q tests were larval echinoderms, pelagic echinoderms, and grazing molluscs, indicating consistent negative effects for these groups across studies.
Summary of effect size analysis (n = 183) for data organized by a taxa, b life stage within taxa (adult = black, juvenile = grey, larvae = white), c feeding strategy within taxa (grazers = black, predators = grey, suspension feeders = white), d habitat within taxa (benthic = black, pelagic = white), and e habitat within feeding strategy (benthic = black, pelagic = white). Numbers on left of each panel indicate the number of treatments used to derive the mean effect size. Error bars are upper and lower bootstrapped 95% confidence intervals. Asterisks indicate statistical significance (i.e. where 95% CI does not overlap with 0). Sample sizes do not match those of Table 1 because coral studies (Houlbrèque et al., 2015; Towle et al., 2015) were excluded, as well as two other studies—one that did not report variances (Watson et al., 2017) and one that contained negative means (Cooper et al., 2016)
Feeding rates of molluscs and echinoderms were the most sensitive to elevated CO2 (Fig. 4a). With all Phyla pooled, larvae and juveniles showed significantly reduced feeding responses to pCO2, but these responses varied by taxon. All molluscan life stages were negatively affected, but on average, arthropod feeding rates were unaltered across life stages; echinoderm larvae and juveniles showed significantly reduced feeding, but adults did not (Fig. 4b). With all Phyla pooled, only suspension feeders had a significantly negative feeding response to OA; grazers and predators did not (Fig. 4c). Molluscs were the only Phylum occupying the suspension-feeding category; grazing molluscs also had a negative response to elevated CO2. Both predatory and grazing echinoderms displayed significantly reduced feeding rates under elevated CO2. No arthropod feeding strategies were affected (Fig. 4c). Data were lacking for suspension-feeding arthropods and echinoderms, as well as predatory molluscs (Fig. 4c); deposit feeders and scavengers were not found in our literature search. Habitat did not consistently affect feeding response to pCO2: benthic and pelagic molluscs and echinoderms displayed significantly reduced feeding rates under elevated CO2 (Fig. 4d). Reduced feeding rate under elevated CO2 was also observed for benthic and pelagic suspension feeders (Fig. 4e). With respect to acclimation time, significantly decreased feeding rates only occurred at pCO2 levels < 1000 µatm, and for acclimation periods of 6–100 days (Fig. 5a, b). Interestingly, there was no significant positive effect of pCO2 on feeding rate (Fig. 4a–e).
Summary of effect size analysis for data organized by a pCO2 level, and b acclimation duration. Numbers on left of each panel indicate the number of treatments used to derive the mean effect size. Error bars are upper and lower bootstrapped 95% confidence intervals. Asterisks indicate statistical significance (i.e. where 95% CI does not overlap with 0)
Differential effect sizes among a priori groups may have been impacted by varying pCO2 levels if the pCO2 ranges differed greatly among groups. For example, predators had significantly higher pCO2 levels for elevated treatments than grazers and suspension feeders (ANOVA: F2,150 = 7.96, p < 0.0005), but their control pCO2 levels were also higher. Two experiments were conducted on arthropods at extremely high pCO2 levels (~ 9000 μatm; Dodd et al., 2015; Glandon & Miller, 2016). Although experimental pCO2 levels in many of these studies were higher than the mean concentrations predicted by the IPCC for the year 2100, it is important to note that low pH and high pCO2 are already experienced daily and seasonally by invertebrates living in estuaries, coasts, upwelling zones, and intertidal areas, and, thus, were within reasonable ranges expected to be experienced by these animals in the next century. Another potentially confounding factor across studies was temperature. For example, many studies on arthropods were conducted at high latitudes, while studies on molluscs were conducted at a range of latitudes. Furthermore, temperature conditions in the experiments varied substantially. Since temperature has a large effect on metabolism, this could be an important interaction with OA impacts on feeding responses.
Predictors of calcifier feeding responses to elevated CO2
AIC model selection revealed that of the 59 predictive models, “Phylum” best predicted effect size (Tables 3, S5). Based on delta AIC values, “life stage”, “exposure time”, and the null model (i.e. the model including experiment only) also served as top candidate models (Tables 3, S5).
Discussion
Ocean acidification effects on calcifying invertebrate feeding rates
Our analysis of the literature indicates that ocean acidification effects on calcifier feeding are largely dependent on taxon (Phylum), life history stage, and duration of acclimation. Mollusc and echinoderm feeding appear to be sensitive to elevated pCO2, particularly during early life history, while arthropod feeding appears more robust to elevated pCO2 effects. These results are in line with those of previous meta-analyses quantifying sensitivity in other biological endpoints (e.g. Kroeker et al., 2013; Wittman & Pörtner, 2013). Calcifying invertebrate feeding in response to elevated pCO2 also appears to be affected by acclimation duration, such that on average, acute acidification (< 10 days) had no effect, but longer-term exposure (> 10 days) did. Our meta-analysis also showed that exposure for more than 100 days did not significantly affect calcifier feeding, suggesting that exposure times beyond this may allow calcifiers to acclimate to elevated pCO2 conditions. Ultimately, our results suggest that feeding in molluscs and echinoderms may be more impacted by elevated pCO2 than arthropods, and that larvae and juveniles are more vulnerable than adults. Life stage was elucidated as the best predictor of effect size out of all fixed predictor variables, suggesting that larval and juvenile calcifiers are more susceptible to the effects of OA on feeding than adults. Analysis of interactive effects of life history stage and exposure duration was not possible, since early life history stages are short.
While our results suggest sensitivity of some taxa and life stages to OA, it is important to assess the variability of effect sizes among the a priori groups that we defined to determine if significant mean effects are meaningful. After evaluation of experimental conditions, variation in effect size (defined by a significant Q-statistic) can be a secondary indicator of whether experimental results among studies are similar enough to justify combination (Hedges et al., 1999). We found that among-study variation in effect size was high for most groups and categories we chose (Phylum, Feeding Strategy, Habitat, Life Stage, Acclimation Time, Table S4). Adding a moderator such as “life stage” to the “Phylum” model decreased residual heterogeneity (fewer groups with significant Q tests, Table S4), indicating that life stage is likely an important moderator for the influence of Phylum on OA response. However, adding multiple moderators to the mixed effects models decreased the sample size of each category, over-parameterizing the models. We believe that for groups with a large sample size, a significant mean effect size, despite significant variability among its component studies, is robust. Ultimately, more experimental evidence testing for elevated CO2 effects on poorly represented groups is necessary.
Mechanistic underpinnings of feeding rate responses to elevated pCO2
Where possible, we qualitatively examined feeding rates in context of accompanying physiological rates, such as respiration, excretion, and growth, to allow for a more comprehensive understanding of the impacts of elevated pCO2 on energetics. It was assumed that elevated pCO2 would be energetically costly to marine calcifying invertebrates, due to a combination of higher energy costs of biomineralization—especially when CaCO3 is corroded in acidic seawater (Palmer, 1992; Wood et al., 2008)—and higher energy allocation to homeostasis (Beniash et al., 2010). Homeostatic costs include ion and acid–base regulation, and maintenance costs for protein synthesis (Pörtner, 2008). Remaining energy after homeostasis and maintenance may be used for growth and/or reproduction. A few feeding studies analysed the entire energy budget of calcifying marine invertebrates or measured enough pieces to make a few generalizations.
Animals could respond to increasing energy demands for homeostasis and/or biomineralization using a variety of generalized strategies, all of which have been noted in molluscs: (1) increasing aerobic respiration rates, increasing feeding rates to support increased metabolism, and increasing NH4+ excretion rates as a result of increased metabolism (Pinctada fucata (Gould, 1850), Liu & He, 2012; Argopecten purpuratus (Lamarck, 1819), Ramajo et al., 2016a; Stapp et al., 2017); (2) increasing aerobic respiration rates, maintaining or decreasing feeding rates, and using catabolism to support increased energy demands, as evidenced by increased NH4+ excretion rates (“tolerant” Mytilus edulis Linnaeus, 1758, Stapp et al., 2017); (3) maintaining respiration rates, maintaining or decreasing feeding rates, and using catabolism to support increased energy demands, as evidenced by increased excretion rates (Mytilus galloprovincialis Lamarck, 1819, Fernández-Reiriz et al., 2012; Littorina littorea (Linnaeus, 1758), Russell et al., 2013; Ruditapes philippinarum (Adams & Reeve, 1850), Xu et al., 2016); or (4) decreasing respiration and feeding rates, which often resulted in decreased growth/survival (Ruditapes decussatus (Linnaeus, 1758), Fernández-Rieriz et al., 2011; Chlamys nobilis (Reeve, 1852), Liu & He, 2012; Perna viridis (Linnaeus, 1758), Liu & He, 2012; Mytilus chilensis Hupé, 1854, Navarro et al., 2016; Mytilus coruscus Gould, 1861, Sui et al., 2016). Marine animals may use one of these strategies, or switch between them, depending on their physiological plasticity and length of acclimation. Thus, the strategies employed by calcifying marine invertebrates at different times may help to explain why feeding rates are depressed under elevated pCO2 in some cases, and not in others. Below, we use this framework to highlight potential Phyla-specific mechanisms for pCO2 effects on calcifier feeding rates, and provide additional hypotheses regarding mechanistic effects.
Molluscs
Since bivalves are osmoconformers (Shumway, 1977), they have reduced capacity for acid–base regulation compared to other species, which may explain their increased sensitivity to elevated pCO2 (Gazeau et al., 2013). Bivalve and echinoderm growth, respiration, and other physiological processes are more sensitive to elevated pCO2 than more metabolically active teleost fishes and decapod crustaceans, due to their lack of respiratory pigments (Melzner et al., 2009). Bivalves compensate for acidosis by increasing bicarbonate through dissolution of shell CaCO3 and through amino acid catabolism (Michaelidis et al., 2005); thus, loss of shell mass and excretion of NH4+ can be indicators of acidosis. Early shell formation may not be energy-limited, due to maternal-derived energy reserves (Frieder et al., 2017), and shell and soft tissue development may be uncoupled (Waldbusser et al., 2015), or shell dissolution in larval stages could result in mechanical alterations to the shell that eventually affect feeding and energy input (Talmage & Gobler, 2010). Elevated pCO2 increased ADP:ATP levels in one study on juvenile oysters (Beniash et al., 2010), but did not affect overall ATP levels in another study; however, lipid and glycogen stores were reduced to maintain cellular energy status (Dickinson et al., 2012).
Suspension feeding is an energy-demanding process controlled by ciliary activity on the gill (Galtsoff, 1964; Jorgensen, 1990), and is commonly used as an indicator of environmental stress (Axiak & George, 1987; Stevens, 1987). Ciliary activity requires a large amount of energy (Mytilus edulis ATP hydrolysis 58-87% of ATP synthesized; Clemmesen & Jorgensen 1987), and is mechanically linked to respiration. In bivalves, the GABAA (or GABAA-like) neuroreceptor can underlie behavioural responses to elevated concentrations of pCO2 in sediments (Clements et al., 2017). GABA has been suggested to play an inhibitory role in regulating the actions of serotonin on ciliary beating (Mathieu et al., 2014). In gastropods, GABAA (or GABAA-like) functioning is also linked to prey escape responses to predators, and could thus be important in predator feeding rates (Watson et al., 2014). While GABAA receptors appear sensitive to pCO2 elevation in molluscs, the same receptors in larval crustaceans appear robust to elevated pCO2 (Charpentier & Cohen, 2016). Consequently, altered ion gradients at GABAA (or GABAA-like) receptors resulting from elevated CO2 may act to drive many of the effects on calcifier feeding.
Echinoderms
Biological responses of echinoderms to OA are class- and species-specific (Dupont et al., 2010). In our study, differences appeared to depend on local adaptation and the relative need for calcification. For example, among sea stars, feeding rates in Asterias rubens Linneaus, 1758 appeared to be more sensitive to pCO2 than those of Pisaster ochraceus (Brandt, 1835), but P. ochraceus may be better adapted to high pCO2 since it lives in the intertidal in an upwelling zone (Keppel et al., 2015). Mechanistically, some echinoderms can resist the effect of OA on calcification due to a protective organic layer around their spines (Ries et al., 2009), or by buffering using their magnesium-calcite test (Miles et al., 2007), which may invoke physiological trade-offs that reduce feeding rates and other physiological rates such as respiration. Elevated pCO2 can also affect the feeding structures of grazing echinoderms (e.g. sea urchins’ Aristotle’s lantern), although it appears that OA effects on these structures may be dependent on diet (Asnaghi et al., 2013). Furthermore, olfactory changes under elevated pCO2 may also be responsible for the observed negative effects on echinoderm predation rates, given that olfaction is particularly susceptible to changes in pCO2 (Clements & Hunt, 2015; Ashur et al., 2017; Tresguerres & Hamilton, 2017). Fewer feeding studies were conducted on echinoderms compared to molluscs, and fewer still included respiration measurements, precluding associations between feeding and respiration. A distinct mechanism(s) for pCO2 effects on echinoderm feeding rates requires more detailed investigation.
Arthropods
In contrast to molluscs and echinoderms, arthropod feeding appeared less affected by elevated pCO2. This observation may be due to differences in metabolic rates, the use of respiratory pigments in arthropods, and/or acid–base regulation (Melzner et al., 2009). Regulation of extracellular pH in arthropods such as Carcinus maenas (Linneaus, 1758) may allow these crabs to feed at normal rates during short-term assays (Appelhans et al., 2012), but may increase energy demands during longer-term exposure. Likewise, a variety of copepod species can strongly regulate internal pH without requiring additional energy via feeding (e.g. Hildebrandt et al., 2016). However, while arthropods can regulate extracellular pH, effects of acidification on feeding rates and, thus, energy balance appear to be mixed. For example, most copepod feeding was unaffected by pCO2, while feeding of crabs, lobsters, and shrimp was most often negatively affected. Growth rates are complicated to measure in arthropods, due to moulting, but where lower growth was noted, respiration rates were also often negatively affected (e.g. Euphausia pacifica Hansen, 1911, Cooper et al., 2016; Homarus gammarus (Linneaus, 1758), Small et al., 2016). Respiration rates of copepods under elevated pCO2 appeared to be sex-specific (Cripps et al., 2016) and respond to food concentrations (Thor & Oliva, 2015), and thus may lend to the variable responses observed in arthropods. A direct mechanism for pCO2 effects on the feeding rates of arthropod species requires more research.
Corals
Unlike the other taxa included in our meta-analysis, there exists a relative paucity of information on feeding rate responses of corals to OA, precluding any meaningful conclusions. The two studies measuring coral feeding rates under elevated pCO2 identified in this review found contrasting effects of OA on coral feeding rates. Houlbrèque et al. (2015) reported reduced feeding rates under elevated pCO2 in Stylophora pistillata Esper, 1797. Interestingly, however, these authors found that depressed feeding did not impact physiology or calcification, so long as the corals were consuming food at any rate. In contrast, Towle et al. (2015) reported increased feeding rates for Acropora cervicornis (Lamarck, 1816), which likely mitigated OA effects on calcification. Together, these studies suggest that food consumption in corals, despite potentially being reduced under elevated pCO2, can mitigate OA effects on calcification for these two species, and that reduced feeding may not necessarily result in negative physiological effects. This idea is further supported by Edmunds (2011), who reported that food consumption partially alleviated OA effects on growth in Porites spp. Link, 1807. More research is necessary to draw more confident conclusions, however, given that only two studies measuring coral feeding rates were found in our literature search.
Recommendations for future research
This quantitative review has identified knowledge gaps and opportunities for research in key areas that would aid in development of broader understanding of physiological causes, and widespread ecological effects, of OA on the feeding rates of marine calcifying invertebrates.
Population effects
Global marine change research has recently started to focus on the potential for organisms to acclimate and/or adapt to global change stressors across multiple generations (Harvey et al., 2014; Sunday et al., 2014; Calosi et al., 2016). While such studies have been implemented for many biological endpoints, we did not find studies testing for acclamatory or adaptive responses of marine calcifier feeding rates to elevated CO2. These studies are needed to realistically predict effects of global marine change stressors on the population scale.
Community effects
Our results indicate that elevated pCO2 can impact the feeding performance of certain marine calcifiers; next steps would be to examine interactive effects of pCO2 on both the prey and the consumer. Many studies consider the effects of prey exposure (e.g. Amaral et al., 2012; Rossoll et al., 2012; Benítez et al., 2016; Duarte et al., 2016; Dupont et al., 2015; Isari et al., 2016) and consumer exposure (studies included in this review) in isolation; however, combined effects on predator–prey and herbivore–plant interactions can have major implications for predicting community-level responses to elevated pCO2. For example, while elevated CO2 appeared to affect individual attributes of a crab predator (Carcinus maenas) and its gastropod prey (Littorina littorea), the predator–prey interactions between these two species were unaltered (Landes & Zimmer, 2012). In contrast, elevated CO2 reduced growth in the barnacle Semibalanus balanoides (Linneaus, 1767), but alterations in the feeding behaviour of its gastropod predator, Nucella lapillus (Linneaus, 1758), dominated the relationship and snails reduced feeding rates to the point of starvation (Harvey & Moore, 2017). It is thus evident that considering elevated pCO2 effects to both the consumer and its food are important when testing for relative effects of OA on marine calcifier feeding performance.
Functional and ecological consequences of altered feeding rates
Taxon- and life stage-specific effects of elevated pCO2 on feeding rates of calcifying marine invertebrates may lead to functional changes in populations, communities, and ecosystems. Where feeding rates are depressed under elevated pCO2, organisms may not be able acquire the necessary energy to overcome the negative physiological consequences of OA. As such, population declines might be expected in organisms suffering depressed feeding rates from elevated pCO2. Population-level changes can also accompany elevated feeding rates under OA, as increased feeding may enhance populations of certain organisms, or lead to faster depletion of their prey or competitors. Such effects could have major implications for the carrying capacity of populations in which feeding rates increase, and shifts in community structure occur.
Additional considerations for future studies
Multiple stressor effects
Although it appears that CO2-induced OA can impact the feeding rates of some calcifying marine invertebrates, it is important to understand that OA is unlikely to occur in isolation, but will occur in the wake of numerous other stressors of global marine change such as salinity changes, ocean warming (OW), and hypoxia (Breitburg et al., 2015). The complex interactions between these multiple drivers can thus elicit different biological responses than the responses observed in single-stressor experiments (Kroeker et al., 2013; Harvey et al., 2013; Gobler & Baumann, 2016). Our literature search identified a total of 21 studies assessing the effects of elevated pCO2 on feeding rates in the context of elevated temperature consistent with OW predictions (i.e. ≤ + 5°C warming; Table 2). While this sample size is too low to assess meta-analytically, a comparison of statistical outcomes between OA only treatments and OA + OW treatments in those 21 studies revealed that OA + OW treatments resulted in a far higher percentage of increased feeding rates than of null responses, while the percentage of decreased feeding responses remained the same (Fig. 3). Thus, it appears that OW may act to predominantly increase calcifier feeding rates in an antagonistic fashion with OA, although this effect may not be sufficient to overcome feeding rate decreases associated with OA. Other anthropogenic changes such as eutrophication and food availability are important to consider in the context of OA (Thomsen et al., 2013; Wallace et al., 2014; Pan et al., 2015; Ramajo et al., 2016a, b), particularly given the high degree of temporal variability of such conditions in coastal and estuarine waters. In a multiple stressor study on feeding rates, Cole et al. (2016) tested for the combined effects of OA, OW, hyposalinity, and food availability on the feeding rates of the oyster Ostrea angasi Sowerby II, 1871, reporting that oysters were unable to compensate for increases in metabolic demand by feeding more under stressed conditions. Testing a similar number of stressors, Burnell et al. (2013) assessed the effect of elevated pCO2 on the feeding rate of the sea urchin, Amblypneustes pallidus (Lamarck, 1816), in the context of OW and eutrophication, reporting that eutrophication offset increased feeding (grazing) rates imposed by OA and OW. Campanati et al. (2016) reported that barnacles, Balanus amphitrite Darwin, 1854, increased feeding rates under elevated pCO2 and reduced O2. In contrast, Sui et al. (2016) reported that elevated pCO2 reduced feeding rates in the mussel Mytilus coruscus under ambient (but not reduced) O2 levels, and that low O2 alone elicited an even more severe decrease in mussel feeding rate than elevated pCO2 alone. Ultimately, the number of studies assessing the effects of OA on marine calcifier feeding rates in the context of other global change stressors in the marine realm is low, especially for stressors such as salinity, oxygen and food availability that are common stressors in coastal and estuarine areas.
Acclimation and adaptation potential
Alongside testing the effects of multiple stressors, global marine change research has recently started to focus on the potential for organisms to acclimate and/or adapt to global change stressors across multiple generations (Harvey et al., 2014; Sunday et al., 2014; Calosi et al., 2016). While such studies have been implemented for many biological endpoints, we did not identify any studies testing for acclimatory or adaptive responses of marine calcifier feeding rates to elevated pCO2. Given that such studies are crucial to realistically predicting effects of marine global change stressors, studies assessing the adaptive and plastic capacity for marine calcifiers to adequately alter their feeding rates in response to global change stressors across multiple generations are most certainly needed.
Food exposure versus feeder exposure to elevated pCO2
While our results suggest that elevated pCO2 can impact the feeding performance of certain calcifying marine invertebrates, the studies herein often do not consider the combined effects of exposure to elevated pCO2 in both the prey and the consumer. While studies often consider the effects of prey or food exposure (e.g. Amaral et al., 2012; Rossoll et al., 2012; Dupont et al., 2015; Benítez et al., 2016; Duarte et al., 2016; Isari et al., 2016; Smith et al., 2016) and consumer exposure (studies highlighted in this review) in isolation, the combined effects of prey and consumer exposure are most often ignored. However, this consideration can have major implications for predicting feeding rate responses to elevated pCO2. Moreover, considering the effect of OA on both consumers and prey is an important consideration when attempting to predict community responses to elevated pCO2. For example, while elevated pCO2 appeared to affect individual attributes of a crab predator (Carcinus maenas) and its gastropod prey (Littorina littorea), the predator–prey interactions and outcomes between these two species were unaltered (Landes & Zimmer, 2012). In contrast, OA effects on crab (Panopeus herbstii H. Milne Edwards, 1834) foraging behaviour outweighed OA effects on its oyster prey (Crassostrea virginica (Gmelin, 1791)) in driving feeding rate responses to OA (Dodd et al., 2015). Similarly, while elevated pCO2 reduced tissue production and rostro-carinal diameter in the barnacle Semibalanus balanoides, alterations in the feeding behaviour of its gastropod predator, Nucella lapillus, dominated the relationship and snails reduced feeding rates to the point of starvation (Harvey & Moore, 2017). It is thus evident that considering effects to both the consumer and its prey are important when testing for effects of OA on marine calcifier feeding performance.
Incorporating other processes involved in energy acquisition
It is important to note that feeding rates may not always correspond directly with energy acquisition. Other processes of energy acquisition such as appetite, digestion, assimilation efficiency, and energy allocation are also at play, along with behavioural processes such as food selectivity and foraging and handling times (among others). Furthermore, effects of elevated pCO2 on energetically demanding processes also need to be accounted for. Thus, studies focusing on more direct measures of energy acquisition will be useful for determining the extent to which animals can use increased energy acquisition to overcome negative effects of CO2-induced OA. While such studies have been recently conducted (e.g. Stumpp et al., 2013; Morley et al., 2016; Yuan et al., 2016; Harvey & Moore, 2017), our knowledge to this extent is still emerging and awaits a more established body of research.
Conclusion
Our quantitative study highlights the importance of taxon and life stage when predicting OA effects on the feeding performance of calcifying marine invertebrates. Mollusc and echinoderm feeding rates—particularly at early life stages—are sensitive to elevated pCO2 conditions at exposure times of 10–100 days; arthropod feeding appears robust to elevated pCO2. Physiological, mechanical, and/or neurobiological changes induced by OA may help to mechanistically explain observed effects of elevated pCO2 on invertebrate feedng rates; however, more research is necessary in order to draw more confident conclusions. How feeding rates are impacted when both consumer and food are exposed to elevated pCO2 is a key area for future research. Knowledge of the effects of local adaptation and acclimation, multiple stressors, and functional and ecological consequences of changes in feeding rates are also needed to understand what such changes mean for future ecosystems under global change.
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Acknowledgements
We wish to thank Dr. Benjamin Harvey for his assistance and guidance with the meta-analysis component of this study. We also thank Dr. Robert Condon, Dr. Luc Comeau, Dr. Remi Sonier, and three anonymous reviewers for constructive feedback which helped improve the original manuscript. This study was funded by a NSERC Visiting Postdoctoral Fellowship to JCC (Grant #501540-2016).
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Table S2. Correlation matrix for predictor variables used to build additive linear mixed effects models in AIC model selection analysis. Supplementary material 2 (XLSX 8 kb)
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Table S4. Weighted mean effect sizes, bootstrapped 95% confidence intervals, and Q-test results from effect size analysis. Supplementary material 4 (XLSX 18 kb)
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Clements, J.C., Darrow, E.S. Eating in an acidifying ocean: a quantitative review of elevated CO2 effects on the feeding rates of calcifying marine invertebrates. Hydrobiologia 820, 1–21 (2018). https://doi.org/10.1007/s10750-018-3665-1
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DOI: https://doi.org/10.1007/s10750-018-3665-1