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Ocean Acidification (Effects on Marine Animals: Crustaceans) -- Summary

As the air's CO2 content rises in response to ever-increasing anthropogenic CO2 emissions, and as more and more carbon dioxide therefore dissolves in the surface waters of the world's oceans, theoretical reasoning suggests the pH values of the planet's oceanic waters should be gradually dropping. The IPCC and others postulate that this chain of events, commonly referred to as ocean acidification, will cause great harm -- and possibly death -- to marine life in the decades and centuries to come. However, as ever more pertinent evidence accumulates, a much more optimistic viewpoint is emerging. Such optimism is the focus of this summary examining the effects of ocean acidification on crustaceans.

Most of the research to date has been conducted on copepods, and the balance of this summary focuses on those findings. But a number of other crustaceans have also been examined. Small et al. (2010), for example, investigated the potential effects of ocean acidification on the velvet swimming or "devil" crab (Necora puber). Working with adult individuals collected from the lower intertidal zone of Mount Batten Beach, Plymouth, UK, the authors tested the effect of 30 days' exposure of the crabs to seawater maintained in 4-L aquaria at pH values of 8.0 (control), 7.3, and 6.7, while they simultaneously measured various types of crab responses.

Results indicated "Necora puber was able to buffer changes to extra-cellular pH over 30 days exposure," and to do it "with no evidence of net shell dissolution." In addition, they found "tolerance to heat, carapace mineralization, and aspects of immune response were not affected by hypercapnic conditions," i.e., conditions that lead to more than the normal level of carbon dioxide in an organism's blood. About the only negative finding was a decline in whole-animal oxygen consumption, which they described as being "marginal" between the control and medium hypercapnic conditions, but as "significant" at a completely unrealistic future pH value of 6.7. Small et al. concluded their report by saying their results "confirm that most physiological functions in N. puber are resistant to low pH/hypercapnia over a longer period than previously investigated."

Noting "there is a particular need to study effects of OA [ocean acidification] on organisms living in cold-water environments due to the higher solubility of CO2 at lower temperatures," Bechmann et al. (2011) maintained shrimp (Pandalus borealis) larvae, from day 1 through day 36 post-hatching, under the OA scenario predicted for the year 2100 (pH 7.6) and compared them against batches of larvae held under the current oceanic pH of 8.1 (the control treatment), while water temperature was kept at a constant 5°C. Under such conditions, Bechmann et al. report survival of the larvae was not reduced at any time during the experiment, but that there was "a significant delay in zoeal progression (development time)," which "may increase the chance of loss by predation." However, they note "a multi-generation experiment with the copepod Acartia tonsa showed that effects of OA observed in the first generation were no longer present in the second and third generation (Dupont and Thorndyke, 2009)," implying that such could also prove to be the case in the situation they were investigating. The eight Norwegian researchers conclude their paper by saying "there are different opinions about how to extrapolate the effects of OA from a single species examined in relatively short-term experiments to the population and ecosystem level," while noting "all agree that more data from relevant long-term experiments are needed to better predict effects at higher levels of biological organization," citing the work of Dupont et al. (2010a,b), Hendriks and Duarte (2010) and Hendricks et al. (2010).

In another non-copepod study, Appelhans et al. (2012) examined the impacts of three different seawater pCO2 levels (650, 1250 and an extreme case of 3500 ppm) on the predator-prey relationship between the shore crab Carcinus maenas and the blue mussel Mytilus edulis, as well as on a second predator-prey relationship between the common sea star Asterias rubens and M. edulis. The experimental set up for ocean acidification at the three pCO2 levels resulted in aragonite saturation state (Ωarag) values of 0.96, 0.53 and 0.20, respectively, and calcite saturation state (Ωcalc) values of 1.64, 0.91 and 0.34, respectively, which conditions were maintained on the animals for a period of ten weeks, after which the authors performed a number of different feeding experiments (of the mussel to the crab and sea star).

Discussing their findings, Appelhans et al. report that "even though the seawater was under-saturated in aragonite in all treatment levels and in calcite in the two higher pCO2 levels, both predator organisms were able to survive under acidified conditions." And they state that "these observations are in line with recent acidification studies on crabs and echinoderms (Dupont and Thorndyke, 2008; Wood et al., 2008; Gooding et al., 2009; Dupont et al., 2010b, 2010c; Whiteley, 2011)." In addition, they indicate that "no significant responses of feeding rate and/or growth were observed under moderate (1250 ppm) seawater acidification scenarios."

At the highest and outright extreme level of acidification [3500 ppm], however, the five researchers report that "all three species show a shift in certain traits," noting that "mussel shells become more brittle, sea stars grow slower, and both sea stars and crabs feed less under strong acidification." And as a result, they state in the conclusion of their paper that "the enhanced vulnerability of mussels seems to be neutralized by the decreased consumption of the predators under high acidification," which allowed them to conclude that "when stress effects are similar on interacting species, biotic interactions may remain unaffected," providing, thereby, a real-world example of ocean acidification-induced trophic non-mismatches.

In two separate experiments conducted over two successive years, Pansch et al. (2013) first assessed larval survival and development of the bay barnacle Amphibalanus improvisus while rearing nauplius larvae in 6-well plates over ten days in response to three different pH treatments (8.02, 7.80 and 7.59), while in the second experiment larval stage and size were assessed by rearing nauplius larvae in 5-l glass bottles over 6 days in response to two different pH treatments (8.09 and 7.80). The three scientists report the "larval development of the barnacle was not significantly affected by the level of reduced pH that has been projected for the next 150 years," for "after 3 and 6 days of incubation, we found no consistent effects of reduced pH on developmental speed or larval size at pH 7.8 compared with the control pH of 8.1." Likewise, they say "after 10 days of incubation, there were no net changes in survival or overall development of larvae raised at pH 7.8 or 7.6 compared with the control pH of 8.0." In all of their many individual trials, however, they determined "there was significant variation in responses between replicate batches (parental genotypes) of some larvae," with some batches actually responding positively to reduced pH."

Pansch et al. say their results suggest "the non-calcifying larval stages of A. improvisus are generally tolerant to near-future levels of ocean acidification," and "this result is in line with findings for other barnacle species and suggests that barnacles do not show the greater sensitivity to ocean acidification in early life history reported for other invertebrate species," while adding that the barnacle's "substantial genetic variability in response to low pH may confer adaptive benefits under future ocean acidification."

In a related study, Pansch et al. (2014) investigated the effects of food availability and elevated pCO2 (ca. 400, 1000 and 3000 µatm) on the growth of newly settled barnacles of the same species (Amphibalanus improvisus) all the way to reproduction, and on their offspring. However, their work focused on "two different populations, which were presumed to differ in their sensitivity to pCO2 due to differing habitat conditions," one from the Western Baltic Sea's Kiel Fjord (an area of rapidly fluctuating seawater pH that often exceeds average projections for the end of this century), and the other from the Tjarno Archipelago, Sweden (Skagerrak) (an area of far lower fluctuations in seawater pH).

In discussing their findings, Pansch et al. report that over a period of 20 weeks, the survival, growth, reproduction and shell strength of Kiel barnacles "were all unaffected by pCO2, regardless of food availability," and that "larval development and juvenile growth of the F1 generation were tolerant to increased pCO2, irrespective of parental treatment." In contrast, they report that "elevated pCO2 had a strong negative impact on survival of Tjarno barnacles," with specimens from this population being "able to withstand moderate levels of elevated pCO2 over five weeks when food was plentiful," but which "showed reduced growth under food limitation." In addition, they found that "severe levels of elevated pCO2 negatively impacted the growth of Tjarno barnacles in both food treatments." Such findings, in the words of Pansch et al., indicate that "populations from fluctuating pCO2 environments are more tolerant to elevated pCO2 than populations from more stable pCO2 habitats." And so they conclude that "considering the high tolerance of Kiel specimens and the possibility to adapt over many generations, near future OA alone does not seem to present a major threat for A. improvisus."

Copepods are another group of crustaceans that appear to be highly adapted to changes in oceanic pH. Some copepods are planktonic (drifting in sea water) and others are benthic (living on the ocean floor). Additionally, some copepods migrate between the sea surface and ocean floor, during which activity they can encounter large pH differences, as has been noted by Feely et al. (2010). In addition, Wootton and Pfister (2012) have found that upwelling along coastal areas and estuaries can lead to pH values that vary by as much as 0.25 pH unit in a 24-hour period plus a much larger 1.5 units, seasonally, over a 10-year period. Also, copepods perform diel vertical migration (DVM), which in the summer exposes them to a pH change greater than one full pH unit between surface and deeper waters, as has been documented by Fabry et al. (2008) and Olafsson et al. (2009), which according to Engstrom-Ost et al. (2014), is "due to benthic respiration, limited photosynthesis and low CO2 exchange with the atmosphere."

Desiring to learn more about the abilities of copepods to cope with such rapid and large changes in oceanic pH, the latter team of three Finnish and three Swedish scientists collected a large number of them via vertical net hauls from depths of 25 meters in the western Gulf of Finland, which they brought back to their laboratory in order to study the effects of pH variability on a number of copepod bodily functions. Working with the species Acartia bifilosa, Engstrom-Ost et al. found there was actually a stimulating effect of lowered pH on their recruitment, which they said was indicative of the fact that "A. bifilosa copepods are tolerant to a significant pH gradient, similar to that experienced during DVM, upwelling episodes and changed mixing conditions in the Baltic Sea." And they thus conclude that A. bifilosa "may have considerable capacity to adapt to future pH decline, such as may occur with ocean acidification," because they say "it is already adapted to pH gradients and shifting pH environments."

Other researchers have come to a similar conclusion. Lewis et al. (2013) examined "the natural distributions of the dominant Artic copepods found under winter sea ice in relation to the current seawater carbonate chemistry conditions and compared these with their short-term responses to future high CO2 conditions." This was done at the temporary Catlin Arctic Survey Ice Base (CIB) during late winter to early spring in 2011," where "the zooplankton were dominated by adult calanoid copepods, comprising mainly the Arctic endemics Calanus glacialis and Calanus hyperboreus but also the smaller, globally occurring Oithona similis, together with the nauplii of various copepod species," after which a series of OA experiments were conducted "using these copepod species and life history stages to compare their response to future high CO2 conditions with natural under-ice pCO2 exposures."

The five researchers' data revealed "species and life stage sensitivities to manipulated conditions were correlated with their vertical migration behavior and with their natural exposures to different pCO2 ranges," and they report that "vertically migrating adult Calanus spp. crossed a pCO2 range of >140 µatm daily and showed only minor responses to manipulated high CO2," while "Oithona similis, which remained in the surface waters and experienced a pCO2 range of <75 µatm, showed significantly reduced adult and nauplii survival in high CO2 experiments."

In light of these findings, Lewis et al. conclude that "the natural range of pCO2 experienced by an organism determines its sensitivity to future OA," adding, "certainly, ubiquitous species in their adult form, living across a range of physicochemical conditions, are likely capable of surviving change." They also note the "larvae of many marine organisms are released at very specific times to coincide with favorable environmental or food conditions," and it seems logical to conclude the same would hold true in the future, making it easier for copepod larvae to survive future OA conditions as well.

Another study to demonstrate the high degree of elasticity of copepods to changes in pH was conducted by Almen et al., (2014). Writing as background for their work they note that "copepods perform diel vertical migration to avoid predators," as documented by Vuorinen et al. (1983), during which they experience "highly fluctuating conditions in their physicochemical environment, i.e., pH, temperature, salinity, oxygen, light and chlorophyll a concentrations." Against this background the team of four researchers set out to examine the vertical profiles of an array of some of these environmental variables along with the vertical distribution of common copepods in a shallow coastal area of the Baltic Sea, sampling once a month (in June, July and August) every sixth hour during a 24-hour period. Their work revealed that copepods regularly experience "a change in pH of more than 0.5 units and 5°C change in temperature" in each of their daily migrations; and they thus remark that "coastal copepods are experiencing a range of variation in their physicochemical environment that is equal to or larger than the predicted climate change for the year 2100."

Pedersen et al. (2013) investigated "the impact of medium-term exposure to CO2 acidified seawater on survival, growth and development in the North Atlantic copepod Calanus finmarchicus," where using a custom-developed experimental system, "fertilized eggs and subsequent development stages were exposed to normal seawater (390 ppm CO2) or one of three different levels of CO2-induced acidification (3,300, 7,300, 9,700 ppm CO2)." The four Norwegian researchers report that "following the 28-day exposure period, survival was found to be unaffected by exposure to 3,300 ppm CO2, but significantly reduced at 7,300 and 9,700 ppm CO2," which values of course are far beyond any atmospheric concentration predicted under the most extreme of circumstances. Thus Pedersen et al. write, in the concluding paragraph of their paper, "the absence of any apparent reduction in the overall survival during the present medium-term exposure to 3,300 ppm CO2, indicates that survival of Calanus eggs and nauplii may be robust against the direct effects of the worst-case CO2 scenario predicted for year 2300."

The following year Pedersen et al. (2014) studied the effects of four different CO2-induced ocean acidification (OA) scenarios -- recent ambient (380 µatm CO2), future pessimistic (1080 µatm CO2), future medium (2080 µatm CO2) and future higher than expected (3080 µatm CO2) - on the same copepod species, but over a period of two generations under conditions of limited food availability. In so doing the eight European researchers found "a significant delay in development rate among the parental generation animals exposed to 2080 µatm CO2 but not in the following F1 generation animals under the same conditions." And they go on to state that this discovery "suggests that C. finmarchicus may have adaptive potential to withstand the direct long-term effects of even the more pessimistic future OA scenarios" -- even under conditions of limited food supply -- which observations clearly underline, as they describe it, "the importance of trans-generational experiments."

Working with the Arctic copepod Calanus glacialis, Weydmann et al. (2012) investigated "how the reduction of sea surface pH from present day levels (pH 8.2) to a realistic model-based level of pH 7.6, and to an extreme level of pH 6.9, would affect the egg production and hatching success of C. glacialis under controlled laboratory conditions." Results of their experiment indicated that "CO2-induced seawater acidification had no significant effect on C. glacialis egg production," and that a reduction in pH to 6.9 only delayed hatching at what they called that "extreme level of pH." They also report there was no significant effect "on the survival of adult females," which observation, in their words, "is in agreement with previous studies on other copepod species," citing Mayor et al. (2007) and Kurihara and Ishimatsu (2008), leading Weydmann et al. to state that "copepods, as a group, may be well equipped to deal with the chemical changes associated with ocean acidification." And in light of all of the research cited above on copepods, it would appear that wherever they are found, they should be able to withstand whatever degree of ocean acidification that might be experienced in the planet's future.

In summation, multiple analyses indicate that many crustaceans will successfully adapt to the changing pH conditions predicted to occur in the future. Out in the real-world of nature, many crustaceans cross pH gradients much larger than predicted for the next century without detriment. Others show a high degree of adaptability across generations. Taken together, these findings represent good news and suggest worries of future widespread species decline from ocean acidification are overstated, if not inaccurate.

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Appelhans, Y.S., Thomsen, J., Pansch, C., Melzner, F. and Wahl, M. 2012. Sour times: seawater acidification effects on growth, feeding behavior and acid-base status of Asterias rubens and Carcinus maenas. Marine Ecology Progress Series 459: 85-97.

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Last updated 31 March 2015