Elasmobranch Responses to Experimental Warming, Acidification, and Oxygen Loss—A Meta-Analysis

Abstract

Despite the long evolutionary history of this group, the challenges brought by the Anthropocene have been inflicting an extensive pressure over sharks and their relatives. Overexploitation has been driving a worldwide decline in elasmobranch populations, and rapid environmental change, triggered by anthropogenic activities, may further test this group's resilience. In this context, we searched the literature for peer-reviewed studies featuring a sustained (>24 h) and controlled exposure of elasmobranch species to warming, acidification, and/or deoxygenation: three of the most pressing symptoms of change in the ocean. In a standardized comparative framework, we conducted an array of mixed-model meta-analyses (based on 368 control-treatment contrasts from 53 studies) to evaluate the effects of these factors and their combination as experimental treatments. We further compared these effects across different attributes (lineages, climates, lifestyles, reproductive modes, and life stages) and assessed the direction of impact over a comprehensive set of biological responses (survival, development, growth, aerobic metabolism, anaerobic metabolism, oxygen transport, feeding, behavior, acid-base status, thermal tolerance, hypoxia tolerance, and cell stress). Based on the present findings, warming appears as the most influential factor, with clear directional effects, namely decreasing development time and increasing aerobic metabolism, feeding, and thermal tolerance. While warming influence was pervasive across attributes, acidification effects appear to be more context-specific, with no perceivable directional trends across biological responses apart from the necessary to achieve acid-base balance. Meanwhile, despite its potential for steep impacts, deoxygenation has been the most neglected factor, with data paucity ultimately precluding sound conclusions. Likewise, the implementation of multi-factor treatments has been mostly restricted to the combination of warming and acidification, with effects approximately matching those of warming. Despite considerable progress over recent years, research regarding the impact of these drivers on elasmobranchs lags behind other taxa, with more research required to disentangle many of the observed effects. Given the current levels of extinction risk and the quick pace of global change, it is further crucial that we integrate the knowledge accumulated through different scientific approaches into a holistic perspective to better understand how this group may fare in a changing ocean.

Impacts of ocean warming on echinoderms: A meta‐analysis

“…Under the end-of-century experimental conditions the effect size for metabolic rate was less positive, indicating that echinoderms may live closer to their physiological thermal limits by 2100. Interestingly, while similar positive metabolic responses to warming were found in other meta-analyses on marine invertebrates and fishes, they have generally found far lower metabolic rate increases for similar magnitudes of warming (~7%-17% increase with 3-4°C of warming on average; Hu et al, 2022;Pereira Santos et al, 2021;Sampaio et al, 2021). A comparable response could have been anticipated for development success, as this would also be expected to shift due to an increase in the rate of cell processes (Munday et al, 2008;Pörtner et al, 2017;Pörtner & Peck, 2010;Schulte, 2015).…”

Impacts of Deoxygenation and Hypoxia on Shark Embryos Anti-Predator Behavior and Oxidative Stress

“…The reduction in the freeze response duration and the increase in the tail beat rate evidenced in this study can be even more aggravated when we consider the synergistic effects of other environmental changes, such as the increase in temperature, for example. Therefore, future studies addressing the interplay between hypoxia and other climate-change-related drivers (e.g., warming and acidification) are greatly needed (see also [ 4 , 5 ]) to better understand how sharks may fare in the ocean of tomorrow.…”

“…Dissolved oxygen (DO) is one of the most critical limiting factors in the marine environment [ 1 , 2 ]. Yet, oxygen loss is the least studied among the main symptoms of climate change in the oceans [ 3 , 4 , 5 ]. In the last five decades, the amount of dissolved oxygen in the oceans has dropped by two percent, and models predict a decline of one to seven percent by the end of this century [ 6 , 7 ].…”

A Systematic Review of the Behavioural Changes and Physiological Adjustments of Elasmobranchs and Teleost’s to Ocean Acidification with a Focus on Sharks

“…Heinrich et al [19] suggested that behavioral tolerance and adaptation flexibility of sharks may help to deal with projected future CO2 levels. A recent meta-analysis [53] found a wide range of ecological dependencies that have the potential to strongly influence elasmobranch. Whether those catastrophes will happen or not depends on context and species-specific.…”

“…Behavior may act as the first indicator for changing environmental conditions [53] and can influence physiology and even on survival of the individual. Loss or reduction of learning abilities is among the topics investigated in animal behaviors under laboratory conditions.…”