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BEHAVIOURAL ECOTOXIOCOLOGY MEETS CLIMATE CHANGE: Interactive effects of mercury pollution and climate change on behaviour, physiology and fitness in a keystone arctic seabird

Periodic Reporting for period 1 - BehavToxArc (BEHAVIOURAL ECOTOXIOCOLOGY MEETS CLIMATE CHANGE: Interactive effects of mercury pollution and climate change on behaviour, physiology and fitness in a keystone arctic seabird)

Periodo di rendicontazione: 2020-07-01 al 2022-06-30

Global climate change is exposing ecosystems to multiple environmental stressors, including altered thermal conditions, changing resource bases, and changes in pollutant cycling. Thus, a pressing research priority for ecologists and conservation biologists involves understanding how multiple stressor interactions will affect biological systems as climate change progresses. Of special note, increases in chemical contaminant exposure concurrent with climate change have the potential to affect organismal responses to other climate change-associated stressors, impairing resiliency. The Arctic marine biota is especially vulnerable to joint effects of climate change and environmental contamination, as the Arctic is warming >3 times as fast as other regions, leading to cascading ecological effects. Furthermore, anthropogenic emissions have led to accumulation of pollutants in the Arctic, and particularly to high levels of mercury (Hg) pollution. Some recent data suggest increasing Hg exposure in Arctic animals concurrent with climate change, raising the alarming possibility that climate change and increasing Hg exposure could have interactive effects on Arctic animals.
Ecotoxicological studies in the Arctic, and elsewhere, have not adequately considered how behavioural and physiological effects of Hg might impair animal resiliency to climate change. Thus, the central objective of this project (BehavToxArc) was to explore interactive effects of Hg contamination and climate change on Arctic animals from behavioural ecological and ecophysiological perspectives using a keystone Arctic seabird species, the little auk (Alle alle), as a model system. Specific aims were:
1) To determine whether Hg exposure affects the capacity for behavioural plasticity in response to changes in foraging landscapes associated with climate change by limiting time activity budgets and behavioural performance traits (e.g. dive length).
2) To determine whether Hg exposure is associated with changes in the adrenocortical stress response that might limit behavioural patterns.
3) To determine whether Hg exposure affects animal personality traits (neophobia) that are key to determining responses to multiple stressor landscapes.
The primary conclusion deriving from the project is that subtle toxicological effects of Hg have the potential to inhibit animal behavioural responses to climate change, especially in the rapidly changing Arctic. In particular, we found evidence that Hg contamination might affect little auk diving patterns, with implications for foraging efficiency given changes in prey distribution in warming oceans. Behavioural toxicological effects of Hg contamination might be even more pronounced in species feeding at higher trophic positions than little auks, due to higher bioaccumulation levels. Thus, our work calls for further work to evaluate the extent to which Hg exposure might limit animal behavioural responses to climate change across a diversity of species representing different foraging niches, and to assess downstream effects on population stability.
Through this research initiative (BehavToxArc), we leveraged state-of-the-art biologging techniques (triaxial accelerometers) coupled with individual-level blood mercury (Hg) measurements to demonstrate that subtle toxicological effects of Hg exposure on seabird (little auk) behavioural patterns might limit resiliency to climate change. Specifically, we found evidence that Hg exposure is associated with changes in dive bout patterning, with birds displaying high blood Hg levels increasing the length of inter-dive breaks when making long dives. These effects of Hg on diving behaviour might limit foraging efficiency in warming oceans, as birds are forced to dive longer to reach copepod prey at greater depth. These groundbreaking results (published in Environmental Science & Technology, https://doi.org/10.1021/acs.est.2c08893(si apre in una nuova finestra)) underscore the importance of considering how subtle behavioural and physiological effects of contamination might limit animal resiliency to changes in foraging landscapes linked to climate change, especially in the rapidly changing Arctic. We found no evidence for effects of Hg exposure on adrenocortical stress physiology (corticosterone (CORT) levels), suggesting that behavioural effects of Hg exposure must arise via other pathways. However, we did find evidence that CORT might play an important role in mediating animal responses to environmental challenges, by supporting energetically expensive behaviours under thermoregulatory challenges. Results involving CORT will soon be submitted for publication. Final analyses of the relationship between Hg exposure and neophobia, and important animal personality trait, remain outstanding, and to be completed in the near future. In addition to empirical work, we also published a review paper (in Science of the Total Environment), which develops a conceptual framework for understanding interactions between chemical contaminants and other environmental stressors from a behavioural reaction norm perspective. This review aims to stimulate future research, guided by the hypothesis that effects of contaminants on behavioural reaction norms are key to driving contaminant-by-climate change interactive effects on individuals, populations, and ultimately ecosystems. We have also presented results at international scientific conferences (Conference of the Animal Behavior Society (2022); Conference of the Society for the Study of Animal Behaviour (2021)) to reach a wide audience. Two Masters students conducted internships through BehavToxArc.
Climate change and environmental pollution are two fundamental challenges of the Anthropocene, yet very few studies have addressed the potential for these two stressors to have interactive effects on wild animal populations. Moreover, those few studies that have assessed such interactive effects have rarely adopted a behavioural ecological perspective. BehavToxArc is among the first initiatives to have thoroughly addressed whether contaminant exposure might exacerbate effects of climate change on animal populations through effects on behavioural patterns and underlying physiological control mechanisms. Through BehavToxArc, we leveraged state-of-the-art biologging technologies to assemble unique datasets regarding relationships between mercury (Hg) contamination levels and seabird behavioural patterns, including detailed time activity budgets and behavioural performance traits (dive length). By compiling these data across multiple (five) years and at two breeding colonies of a keystone Arctic seabird species, the little auk (Alle alle), we derived new insights into the potential for Hg contamination to inhibit behavioural responses to changes in environmental conditions associated with rapid Arctic climate change. This work has forwarded a neglected hypothesis, namely, that chemical contamination might inhibit animal resiliency to climate change through effects on behavioural and physiological traits. This hypothesis is critical in the context of projecting how contaminant exposure and global climate change might interact to affect the stability of animal populations, especially in the rapidly warming Arctic. Future work will follow up on these hypotheses in a broader range of species, and aim to determine implications for populations, ecosystems and societies in the context of climate change.
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