On the need to incorporate carbonate variability parameters in predicting the biological impacts of ocean acidification
This post is published as an excerpt of a “Quo Vadimus” essay to be submitted to a special issue of the ICES Journal of Marine Science. I highly appreciate any criticisms and/or feedback on the article.
Ocean acidification is expected to yield negative implications for a wide array of marine organisms in the near future, as average oceanic pH levels are projected to drop by 0.3-0.4 units by the end of the century (e.g. Orr et al. 2005, IPCC 2014). However, as with other processes affected by global climate change, variability in oceanic carbonate chemistry can also be expected to increase. For example, precipitation and temperature are expected to become more variable in the future, while the frequency and magnitude of extreme weather is expected to increase (Easterling et al. 2007, IPCC 2014). Consequently, environmental conditions within marine habitats may become more variable, including more pronounced fluctuations in marine carbonate chemistry.
Although we can expect the variability of marine carbonate chemistry to increase in the future, oceanic pH is already highly variable both spatially and temporally, with coastal areas being the most dynamic of these systems. This variability can be primarily attributed to differences in ecosystem processes across systems. Although some studies suggest that interannual and seasonal surface ocean [CO32-] variability is negligible, except in higher latitudes (temporal and arctic regions) (Orr et al. 2005), others report fairly substantial variability. For example, a study by Dore et al. (2009) utilizing 20 years of time-series measurements suggested substantial interannual and seasonal variability, coupled with a long-term decrease in pH in the north Pacific, with seasonal trends driven primarily by changes in temperature, mixing, and the net assimilation of photosynthetic CO2. Biological processes have also been suggested to drive seasonal variation in CaCO3 saturation states in the Arctic Ocean (Bates et al. 2009), while highly variable carbonate parameters have been recorded in California current systems (Hauri et al. 2009, Lienweber & Gruber 2013). The degree of variability in marine carbonate chemistry also varies within and among systems. For example, in the North Sea, it has been reported that a low degree of pH variability exists in biologically inactive areas (< 0.2), but a high degree of variability exists in coastal areas, particularly those around the mouths of rivers (Hinga 2002, Blackford & Gilbert 2005). Likewise, in Australia, degrees of pH variability have been shown to vary temporally and spatially, but specific trends are not always evident (Gagliano et al. 2010), while substantial variation in carbonate saturation has been reported from a Great Barrier Reef flat, although the impacts of such variability on coral calcification are unknown (Shaw et al. 2012). Sediments are also known to be highly variable with respect to carbonate geochemistry, varying by different degrees both spatially and temporally (Figure 1, Wenzhöfer 1999, Yates & Halley 2006). Annual patterns in carbonate geochemical variability have also been documented to correlate with cyclical trends in the abundance of benthic organisms (i.e., foraminiferans; Green et al. 1993). Rainfall can also impose drastic changes and substantial variability in sediments (Figure 1) and coastal systems (Doney et al. 2007), with negative relationships observed between rainfall and pH (i.e., increased rainfall, lower pH).
Studies have provided a solid basis for understanding the complexities of marine carbonate variability. However, the ways in which these temporal and spatial trends (or lack thereof in some areas) will impact marine organisms at the various levels of biological organization are still unknown. Some studies have started to incorporate variability parameters into assessing the biological impacts of ocean acidification, suggesting that the effects of fluctuating carbonate chemistry are species specific, allowing organisms to adapt and persist or become more vulnerable in an acidifying ocean. A study conducted by Alenius & Munguia (2012) suggested that the intertidal isopod, Paradella dianae, although adapted to a high degree of variability because it lives in the intertidal zone, experiences behavioural and physiological changes under variable pH conditions compared to a stable, low pH environment, with variable conditions (low pH) yielding negative impacts on survival, oxygen consumption, and behaviour (significantly depressed swimming time and increased resting time). Cornwall et al. (2013) also observed significantly lower growth rates of coralline macroalgae under variable pH conditions relative to static conditions. On the positive side, Default et al. (2012) have reported beneficial effects of fluctuating pCO2, reporting increases in growth and survival of coral recruits under naturally-fluctuating levels of pCO2. Similarly, when assessing the impacts of static and variable pH (O2 was also assessed, but ignored here), Frieder et al. (2014) reported that low pH treatments incorporating variability resulted in quicker transitions from trochophore to veliger larvae and larger (and less variable) larval shells compared to static low pH conditions for two species of mussels (Mytilus galloprovincialis and M. californianus). Although they did not directly test the impacts of variability on animals, Shaw et al (2013b) have outlined to importance of carbonate variability on the exposure time of marine organisms to conditions either above or below current and projected means.
The vast majority of studies assessing the biological consequences of ocean acidification focus their efforts on organisms raised under or exposed to static conditions based on mean predicted near-future acidification scenarios (Figure 2). Furthermore, although research has started to shift toward assessing the biological impacts of near-future OA conditions in the context of other environmental factors (e.g., multiple factors; temperature, salinity, oxygen, etc.), they have yet to focus on understanding the impact of acidification on marine fauna in the context of current and future marine carbonate variability. Because carbonate variability can modulate an organism’s duration of exposure to carbonate conditions above, at, or below current and projected means, as well as increase the extremes that the organism experiences, variability may offset the negative effects of ocean acidification, or amplify them. Since the time spent in conditions yielding biological effects is likely increase over time, along with the extremes of these conditions (Figure 3, Shaw et al. 2013a), it would be expected that future marine carbonate variability would result in more pronounced biological effects. Of the four studies directly relating carbonate variability to biological effects, two suggested that variability will act to modulate the impacts of ocean acidification (Default et al. 2012, Frieder et al. 2014). However, it is important to recognize these studies use current degrees of variability as the basis for future variability, which may be inaccurate. As such, the duration and extremes of the conditions that the animals in those two studies were exposed to could have confounded their results, as the tested duration and extremes of conditions may not have accurately depicted those of actual future scenarios (Figure 3). As such, an accurate understanding of how carbonate variability will transpire in the future, along with how marine organisms will respond to current and near-future acidification is of utmost importance for understanding the true biological impacts of ocean acidification.
Although the current data on how variability around current and future carbonate geochemical means suggest that marine carbonate variability will have differential effects on different species (Figure 4) and that the magnitude of the effects of ocean acidification may be more or less pronounced under variable conditions (in comparison to static conditions), the number of studies that have attempted to address variability parameters in biological ocean acidification studies is negligible and insufficient to draw any generalizations. As such, it is critical that ocean acidification research, in the context of biological impacts, begins to understand current and projected localized and broad-scale variability in marine carbonate systems to accurately predict how organisms will respond under future acidification scenarios. It is also apparent that studies focusing on the biological impacts of ocean acidification need to begin understanding how the degree of marine carbonate variability is going to change with an increasingly acidifying ocean in the myriad of systems that will be impacted by ocean acidification. Understanding whether or not the variability in the marine carbonate system is going to increase, decrease, or remain the same under future climate change scenarios is imperative for predicting how marine organisms will respond to an acidifying and warming ocean. Ultimately, because ocean acidification studies focus on stable conditions under near-future predictions, our current understanding of how acidification will impact marine organisms is very limited, rendering it critical to begin understanding how acidification will affect these organisms in the context of variability around the projected means, as well as in the context of other environmental factors and their associated variabilities.
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