Predicting consequences of POP-induced disruption of blubber glucose uptake, mass gain rate and thyroid hormone levels for weaning mass in grey seal pups

Kimberley A Bennett,Kelly J Robinson,Holly C Armstrong,Simon E.W Moss,Georges Scholl,Alexandra Tranganida,Gauthier Eppe,Jean-Pierre Thomé,Cathy Debier,Ailsa J Hall

doi:10.1016/j.envint.2021.106506

Kimberley A Bennett, Kelly J Robinson + Show 8 more

Open Access

https://doi.org/10.1016/j.envint.2021.106506

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Abstract

Persistent organic pollutants (POPs) are endocrine disruptors that alter adipose tissue development, regulation and function. Top marine predators are particularly vulnerable because they possess large fat stores that accumulate POPs. However, links between endocrine or adipose tissue function disruption and whole animal energetics have rarely been investigated. We predicted the impact of alterations to blubber metabolic characteristics and circulating thyroid hormone (TH) levels associated with polychlorinated biphenyls (PCBs), polybrominated diphenyl ethers (PBDEs), and organochlorine pesticides (OCPs) on suckling mass gain and weaning mass in wild grey seal pups. Glucose uptake by inner blubber was a strong predictor of whole animal mass gain rate, which in turn, resulted in heavier weaning mass. Weaning mass was predicted to increase by 3.7 ± 1.59 (sem) %, through increased mass gain rate, in the absence of the previously reported suppressive effect of dioxin-like PCB (DL-PCBs) on blubber glucose uptake. PBDEs were, conversely, associated with faster mass gain. Alleviation of this effect was predicted to reduce weaning mass by 6.02 ± 1.86% (sem). To better predict POPs effects on energy balance, it is crucial to determine if and how PBDEs promote mass gain in grey seal pups. Weaning mass was negatively related to total T3 (TT3) levels. A 20% (range = 9.3–31.7%) reduction in TT3 by DL-PCBs partially overcame the effect of DL-PCB -mediated reduction in blubber glucose uptake. Overall, DL-PCBs were thus predicted to reduce weaning mass by 1.86 ± 1.60%. Organohalogen impacts on whole-animal energy balance in grey seal pups appear to partially offset each other through opposing effects on different mechanisms. POP effects were generally minor, but the largest POP-induced reductions in weaning mass were predicted to occur in pups that were already small. Since weaning mass is positively related to first-year survival, POPs may disproportionately affect smaller individuals, and could continue to have population-level impacts even when levels are relatively low compared to historical values. Our findings show how in vitro experiments combined with measurements in vivo can help elucidate mechanisms that underpin energy balance regulation and help to quantify the magnitude of disruptive effects by contaminants and other stressors in wildlife.

Highlights

Central place foragers are expected to offset travel costs between a central place and foraging areas by targeting productive feeding zones
Some individuals target resources closer to the haul-out[6,8,9], raising the question: why do some individuals accept the extra travel costs associated with foraging further offshore? it has been suggested that some populations, such as the Wadden Sea harbour seals, feed almost exclusively at offshore sites suggesting that these sites provide a resource which is not available closer to the haul-out[6,8,10,11]
Optimal foraging models predict that animals travelling further should forage longer to recoup travel costs, but trip length is likely constrained by other factors e.g., the need for sleep, digestion and/or social interaction

Summary

Introduction

Central place foragers are expected to offset travel costs between a central place and foraging areas by targeting productive feeding zones. Harbour seals (Phoca vitulina) make multi-day foraging trips away from coastal haul-out sites presumably to target rich food resources, but periodic track points from telemetry tags may be insufficient to infer reliably where, and how often, foraging takes place. It has been suggested that some populations, such as the Wadden Sea harbour seals, feed almost exclusively at offshore sites suggesting that these sites provide a resource which is not available closer to the haul-out[6,8,10,11]. Increased predation close to haul-out sites may reduce prey abundance around coastal sites Such zones of depletion, known as Ashmole’s halo[18], have been observed around seabird colonies and drive predators further offshore to forage. Despite the ubiquity of harbour seals around populated northern European coastlines, relatively little is known about what drives and constrains their offshore foraging

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