Managing the nonlethal effects of disturbance on wildlife populations has been a long‐term goal for decision makers, managers, and ecologists, and assessment of these effects is currently required by European Union and United States legislation. However, robust assessment of these effects is challenging. The management of human activities that have nonlethal effects on wildlife is a specific example of a fundamental ecological problem: how to understand the population‐level consequences of changes in the behavior or physiology of individual animals that are caused by external stressors. In this study, we review recent applications of a conceptual framework for assessing and predicting these consequences for marine mammal populations. We explore the range of models that can be used to formalize the approach and we identify critical research gaps. We also provide a decision tree that can be used to select the most appropriate model structure given the available data. Synthesis and applications: The implementation of this framework has moved the focus of discussion of the management of nonlethal disturbances on marine mammal populations away from a rhetorical debate about defining negligible impact and toward a quantitative understanding of long‐term population‐level effects. Here we demonstrate the framework's general applicability to other marine and terrestrial systems and show how it can support integrated modeling of the proximate and ultimate mechanisms that regulate trait‐mediated, indirect interactions in ecological communities, that is, the nonconsumptive effects of a predator or stressor on a species' behavior, physiology, or life history.
While sophisticated tools are used to monitor behavioral changes of large marine vertebrates, determining whether these changes are meaningful for management and conservation is challenging. The Population Consequences of Disturbance model proposed a bioenergetics model to detect biologically meaningful population responses, where disturbance costs are linked to lost energy. The model assumes that changes in behavior, caused by disturbance, compromise maternal condition, reducing energy delivery to offspring, leading to reduced reproduction, increased offspring mortality, and eventually increased adult mortality. Given its coastal habits and past whaling history, gray whales' (Eschrichtius robustus) life history and ecology are better known than for many other baleen whales. However, their preference for coastal habitat increases their exposure to human disturbance. We created a female gray whale bioenergetics model to determine energy requirements for a two‐year reproductive cycle and determined the consequences of lost energy under three possible disturbance scenarios. An annual energetic loss of 4% during the year in which she is pregnant, would prevent a female from successfully producing/weaning a calf. For this reason, gray whale reproduction is particularly sensitive to disturbance during pregnancy. During the year in which she is lactating, she would wean her calf at a lower mass with a 37% energetic loss. A female would lack the energy to become pregnant during a year with a 30–35% energetic loss, and female mortality would likely occur at 40–42% annual energetic loss. Our model can be used for assessing disturbance costs or other effects associated with climate change and/or anthropogenic activities and can be applied to other species with similar life histories.
Integrating behavior and physiology is critical to formulating new hypotheses on the evolution of animal life-history strategies. Migratory capital breeders acquire most of the energy they need to sustain migration, gestation, and lactation before parturition. Therefore, when predicting the impact of environmental variation on such species, a mechanistic understanding of the physiology of their migratory behavior is required. Using baleen whales as a model system, we developed a dynamic state variable model that captures the interplay among behavioral decisions, energy, reproductive needs, and the environment. We applied the framework to blue whales (Balaenoptera musculus) in the eastern North Pacific Ocean and explored the effects of environmental and anthropogenic perturbations on female reproductive success. We demonstrate the emergence of migration to track prey resources, enabling us to quantify the trade-offs among capital breeding, body condition, and metabolic expenses. We predict that periodic climatic oscillations affect reproductive success less than unprecedented environmental changes do. The effect of localized, acute anthropogenic impacts depended on whales' behavioral response to the disturbance; chronic, but weaker, disturbances had little effect on reproductive success. Because we link behavior and vital rates by modeling individuals' energetic budgets, we provide a general framework to investigate the ecology of migration and assess the population consequences of disturbance, while identifying critical knowledge gaps.
Animals make behavioural and reproductive decisions that maximise their lifetime reproductive success, and thus their fitness, in light of periodic and stochastic variability of the environment. Modelling the variation of an individual's energy levels formalises this tradeoff and helps to quantify the population‐level consequences of stressors (e.g. disturbance from human activities and environmental change) that can affect behaviour or physiology. In this study, we develop a dynamic state variable model for the spatially explicit behaviour, physiology and reproduction of a female, long‐lived, migratory marine vertebrate. The model can be used to investigate the spatio‐temporal patterns of behaviour and reproduction that allow an individual to maximise its overall reproductive output. We parametrised the model for eastern North Pacific blue whales Balaenoptera musculus, and used it to predict the effects of changing environmental conditions and increasing human disturbance on the population's vital rates. In baseline conditions, the model output had high fidelity to observed energy dynamics, movement patterns and reproductive strategies. Simulated scenarios suggested that environmental changes could have severe consequences on the population's vital rates, but that individuals could tolerate high levels of anthropogenic disturbance. However, this ability depended on where, when and how often disturbance occurred. In scenarios with both environmental change and anthropogenic disturbance, synergistic interactions caused stronger effects than in isolation. In general, larger body size offered a buffer against stochasticity and disturbance, and, consequently, we predicted juveniles to be more susceptible to disturbance. We also predicted that females prioritise their own survival at the expense of the current reproductive attempt, presumably the result of their long lifespan. Our approach provides a general framework to make predictions of the cumulative and synergistic effects of human disturbance and climate change on migratory populations, which can inform effective management and conservation efforts.
Summary Anthropogenic disturbance is of increasing concern for wildlife populations, necessitating the development of models that link behavioural changes at the individual level with biologically meaningful changes at the population level. We developed a general framework for estimating the fitness consequences of disturbance that affects foraging behaviour using state‐dependent behavioural theory implemented by Stochastic Dynamic Programming (SDP). We illustrate this framework using generalized examples of pinnipeds, a group of marine carnivores that include both capital‐ and income‐breeding species. We examined how disturbance affected pup recruitment separately for each reproductive strategy, and the impact of foraging decisions and parameter values on model results. The effect of disturbance on pup recruitment was greater for income than capital breeders for all disturbance scenarios. Disturbance had negligible effects on pup recruitment when it occurred within less frequented foraging patches, but moderate to large effects when it occurred within an important foraging patch. Model results were sensitive to values of patch productivity (the energy gained from successful foraging), the probability of disturbance and individual behavioural choices in the face of disturbance. State‐dependent behavioural theory implemented by SDP is a powerful tool for investigating when behavioural changes in response to disturbance may be meaningful at the population level. This approach allows us to incorporate many factors that are known to influence the behavioural and physiological responses of animals to anthropogenic disturbance, and places disturbance within the context of a temporally and spatially variable environment. The general framework we have developed can be used to estimate the consequences of anthropogenic disturbance across a broad range of species.
Acoustic disturbance is a growing conservation concern for wildlife populations because it can elicit physiological and behavioral responses that can have cascading impacts on population dynamics. State‐dependent behavioral and life history models implemented via Stochastic Dynamic Programming (SDP) provide a natural framework for quantifying biologically meaningful population changes resulting from disturbance by linking environment, physiology, and metrics of fitness. We developed an SDP model using the endangered western gray whale (Eschrichtius robustus) as a case study because they experience acoustic disturbance on their summer foraging grounds. We modeled the behavior and physiological dynamics of pregnant females as they arrived on the feeding grounds and predicted the probability of female and offspring survival, with and without acoustic disturbance and in the presence/absence of high prey availability. Upon arrival in mid‐May, pregnant females initially exhibited relatively random behavior before they transitioned to intensive feeding that resulted in continual fat mass gain until departure. This shift in behavior co‐occurred with a change in spatial distribution; early in the season, whales were more equally distributed among foraging areas with moderate to high energy availability, whereas by mid‐July whales transitioned to predominate use of the location that had the highest energy availability. Exclusion from energy‐rich offshore areas led to reproductive failure and in extreme cases, mortality of adult females that had lasting impacts on population dynamics. Simulated disturbances in nearshore foraging areas had little to no impact on female survival or reproductive success at the population level. At the individual level, the impact of disturbance was unequally distributed across females of different lengths, both with respect to the number of times an individual was disturbed and the impact of disturbance on vital rates. Our results highlight the susceptibility of large capital breeders to reductions in prey availability, and indicate that who, where, and when individuals are disturbed are likely to be important considerations when assessing the impacts of acoustic activities. This model provides a framework to inform planned acoustic disturbances and assess the effectiveness of mitigation strategies for large capital breeders.
Western gray whales (WGW) Eschrichtius robustus are considered one of the world's most endangered baleen whale populations. Development of oil and gas fields in northeastern Sakhalin, Russia, is a concern, because they overlap with WGW feeding grounds. Some WGW migrate ~10 000 km from feeding grounds around Sakhalin Island (Russia), to breeding grounds in Baja California (BajaC; Mexico) and possibly ~6000 km to the South China Sea (China). We developed a WGW female bioenergetics model to examine potential consequences of energy lost from foraging cessation caused by anthropogenic disturbance, and compared it to eastern gray whales (EGW). Energy loss was then linked to potential reductions in reproduction and survival. Mean total energy requirements were 11 and 15% greater for WGW breeding in BajaC and China, respectively, compared to EGW, due to longer migration distance (25%) to BajaC and higher metabolic rates at foraging grounds. However, this difference is minimal for EGW that use the northern extent of their foraging range. On average, WGW breeding in BajaC and China need 9 and 17% more energy for survival than EGW. Our model predicts that WGW mortality would likely occur at 38 to 40% annual energetic loss. Long-term yearly energy loss of < 30% would reduce population growth due to lower reproductive rates. Ongoing yearly energy losses of > 30% would result in adult female mortality the first year, followed by lower reproductive rates of survivors. Our model suggests that energy losses of > 30% caused by disturbance should be considered a threshold for concern for this Critically Endangered population.
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