American Society of Naturalists

A membership society whose goal is to advance and to diffuse knowledge of organic evolution and other broad biological principles so as to enhance the conceptual unification of the biological sciences.

“Propensity for risk in reproductive strategy affects susceptibility to anthropogenic disturbance”

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Enrico Pirotta, Vincent Hin, Marc Mangel, Leslie New, Daniel P. Costa, André M. de Roos, and John Harwood (Oct 2020)

Risky reproductive strategies in pilot whales reduce the ability to cope with human disturbance

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A female long-finned pilot whale (<i>Globicephala melas</i>) with her calf.<br/>(Credit: Enrico Pirotta)
A female long-finned pilot whale (Globicephala melas) with her calf.
(Credit: Enrico Pirotta)

Human activities in the ocean are expanding at a fast pace. When disturbance from these activities causes animals to change their behavior (for example, interrupt feeding activity), the long-term consequences on populations are mediated by changes in the energy stores of individuals, which can affect their survival and, importantly, reproduction. When to reproduce, when to abandon an ongoing attempt, or how much energy to transfer to offspring are critical decisions for an animal, and the best strategy changes dynamically over the course of life. This is particularly true in long-lived organisms, like most cetaceans, where parents invest a lot of energy on their offspring.

Researchers from Washington State University, the University of Amsterdam, University of California Santa Cruz, and the University of St Andrews developed a model to investigate how such reproductive strategies affect susceptibility to disturbance from human activities, using long-finned pilot whales in the North Atlantic as the model species. Results show that, in undisturbed conditions, females maximize the number of calves, but, when disturbance affects feeding activity, their finely tuned strategy leads to dramatic effects on both survival and reproduction. In contrast, females develop more cautious strategies in unpredictable environments, which improve their ability to cope with disturbed conditions.

Because most animals live in variable environments, fragile reproductive strategies may be unlikely to evolve and persist. For example, the long-finned pilot whale population in the North Atlantic inhabits a seasonal environment, with large inter-annual variability in food resources. Therefore, pilot whales have likely evolved low propensity to risk, which would make them comparatively more able to cope with anthropogenic disturbance. More generally, this study shows how assumptions about risk propensity can drastically affect predictions of the population consequences of human disturbance.


Abstract

Animals initiate, interrupt or invest resources in reproduction in light of their physiology and the environment. The energetic risks entailed in an individual’s reproductive strategy can influence the ability to cope with additional stressors, such as anthropogenic climate change and disturbance. To explore the trade-offs between internal state, external resource availability and reproduction, we applied State-Dependent Life-History Theory (SDLHT) to a Dynamic Energy Budget (DEB) model for long-finned pilot whales (Globicephala melas). We investigated the reproductive strategies emerging from the interplay between fitness maximization and propensity to take energetic risks, and the resulting susceptibility of individual vital rates to disturbance. Without disturbance, facultative reproductive behavior from SDLHT and fixed rules in the DEB model led to comparable individual fitness. However, under disturbance, the reproductive strategies emerging from SDLHT increased vulnerability to energetic risks, resulting in lower fitness than fixed rules. These fragile strategies might therefore be unlikely to evolve in the first place. Heterogeneous resource availability favored more cautious, and thus more robust, strategies, particularly when knowledge of resource variation was accurate. Our results demonstrate that the assumptions regarding the dynamic trade-offs underlying an individual’s decision-making can have important consequences for predicting the effects of anthropogenic stressors on wildlife populations.