Leslie New

Modelling the biological significance of behavioural change in coastal bottlenose dolphins in response to disturbance

Summary 1. Behavioural change in response to anthropogenic activities is often assumed to indicate a biologically significant effect on a population of concern. Disturbances can affect individual health through lost foraging time or other behaviours, which will impact vital rates and thus the population dynamics. However, individuals may be able to compensate for the observed shifts in behaviour, leaving their health and thus their vital rates and population dynamics, unchanged. 2. We developed a mathematical model simulating the complex social, spatial, behavioural and motivational interactions of coastal bottlenose dolphins (Tursiops truncatus) in the Moray Firth, Scotland, to assess the biological significance of increased rate of behavioural disruptions caused by vessel traffic. 3. We explored a scenario in which vessel traffic increased from 70 to 470 vessels a year in response to the construction of a proposed offshore renewables’ facility. Despite the more than sixfold increase in vessel traffic, the dolphins’ behavioural time budget, spatial distribution, motivations and social structure remain unchanged. 4. We found that the dolphins are able to compensate for their immediate behavioural response to disturbances by commercial vessels. If the increased commercial vessel traffic is the only escalation in anthropogenic activity, then the dolphins’ response to disturbance is not biologically significant, because the dolphins’ health is unaffected, leaving the vital rates and population dynamics unchanged. 5. Our results highlight that behavioural change should not automatically be correlated with biological significance when assessing the conservation and management needs of species of interest. This strengthens the argument to use population dynamics targets to manage human activities likely to disturb wildlife.

Using Energetic Models to Investigate the Survival and Reproduction of Beaked Whales (family Ziphiidae)

Mass stranding of several species of beaked whales (family Ziphiidae) associated with exposure to anthropogenic sounds has raised concern for the conservation of these species. However, little is known about the species’ life histories, prey or habitat requirements. Without this knowledge, it becomes difficult to assess the effects of anthropogenic sound, since there is no way to determine whether the disturbance is impacting the species’ physical or environmental requirements. Here we take a bioenergetics approach to address this gap in our knowledge, as the elusive, deep-diving nature of beaked whales has made it hard to study these effects directly. We develop a model for Ziphiidae linking feeding energetics to the species’ requirements for survival and reproduction, since these life history traits would be the most likely to be impacted by non-lethal disturbances. Our models suggest that beaked whale reproduction requires energy dense prey, and that poor resource availability would lead to an extension of the inter-calving interval. Further, given current information, it seems that some beaked whale species require relatively high quality habitat in order to meet their requirements for survival and reproduction. As a result, even a small non-lethal disturbance that results in displacement of whales from preferred habitats could potentially impact a population if a significant proportion of that population was affected. We explored the impact of varying ecological parameters and model assumptions on survival and reproduction, and find that calf and fetus survival appear more readily affected than the survival of adult females.

Estimating resource acquisition and at-sea body condition of a marine predator

Body condition plays a fundamental role in many ecological and evolutionary processes at a variety of scales and across a broad range of animal taxa. An understanding of how body condition changes at fine spatial and temporal scales as a result of interaction with the environment provides necessary information about how animals acquire resources. However, comparatively little is known about intra- and interindividual variation of condition in marine systems. Where condition has been studied, changes typically are recorded at relatively coarse time-scales. By quantifying how fine-scale interaction with the environment influences condition, we can broaden our understanding of how animals acquire resources and allocate them to body stores. Here we used a hierarchical Bayesian state-space model to estimate the body condition as measured by the size of an animals lipid store in two closely related species of marine predator that occupy different hemispheres: northern elephant seals (Mirounga angustirostris) and southern elephant seals (Mirounga leonina). The observation model linked drift dives to lipid stores. The process model quantified daily changes in lipid stores as a function of the physiological condition of the seal (lipid:lean tissue ratio, departure lipid and departure mass), its foraging location, two measures of behaviour and environmental covariates. We found that physiological condition significantly impacted lipid gain at two time-scales – daily and at departure from the colony – that foraging location was significantly associated with lipid gain in both species of elephant seals and that long-term behavioural phase was associated with positive lipid gain in northern and southern elephant seals. In northern elephant seals, the occurrence of short-term behavioural states assumed to represent foraging were correlated with lipid gain. Lipid gain was a function of covariates in both species. Southern elephant seals performed fewer drift dives than northern elephant seals and gained lipids at a lower rate. We have demonstrated a new way to obtain time series of body condition estimates for a marine predator at fine spatial and temporal scales. This modelling approach accounts for uncertainty at many levels and has the potential to integrate physiological and movement ecology of top predators. The observation model we used was specific to elephant seals, but the process model can readily be applied to other species, providing an opportunity to understand how animals respond to their environment at a fine spatial scale.

A Risk Function for Behavioral Disruption of Blainville's Beaked Whales (Mesoplodon densirostris) from Mid- Frequency Active Sonar

There is increasing concern about the potential effects of noise pollution on marine life in the world’s oceans. For marine mammals, anthropogenic sounds may cause behavioral disruption, and this can be quantified using a risk function that relates sound exposure to a measured behavioral response. Beaked whales are a taxon of deep diving whales that may be particularly susceptible to naval sonar as the species has been associated with sonar-related mass stranding events. Here we derive the first empirical risk function for Blainville’s beaked whales (Mesoplodon densirostris) by combining in situ data from passive acoustic monitoring of animal vocalizations and navy sonar operations with precise ship tracks and sound field modeling. The hydrophone array at the Atlantic Undersea Test and Evaluation Center, Bahamas, was used to locate vocalizing groups of Blainville’s beaked whales and identify sonar transmissions before, during, and after Mid-Frequency Active (MFA) sonar operations. Sonar transmission times and source levels were combined with ship tracks using a sound propagation model to estimate the received level (RL) at each hydrophone. A generalized additive model was fitted to data to model the presence or absence of the start of foraging dives in 30-minute periods as a function of the corresponding sonar RL at the hydrophone closest to the center of each group. This model was then used to construct a risk function that can be used to estimate the probability of a behavioral change (cessation of foraging) the individual members of a Blainville’s beaked whale population might experience as a function of sonar RL. The function predicts a 0.5 probability of disturbance at a RL of 150dBrms re µPa (CI: 144 to 155) This is 15dB lower than the level used historically by the US Navy in their risk assessments but 10 dB higher than the current 140 dB step-function.

Fitting Models of Multiple Hypotheses to Partial Population Data: Investigating the Causes of Cycles in Red Grouse

There are two postulated causes for the observed periodic fluctuations (cycles) in red grouse (Lagopus lagopus scoticus). The first involves interaction with the parasitic nematode Trichostrongylus tenuis. The second invokes delayed regulation through the effect of male aggressiveness on territoriality. Empirical evidence exists to support both hypotheses, and each hypothesis has been modeled deterministically. However, little effort has gone into looking at the combined effects of the two mechanisms or formally fitting the corresponding models to field data. Here we present a model for red grouse dynamics that includes both parasites and territoriality. To explore the single and combined hypotheses, we specify three versions of this model and fit them to data using Bayesian state‐space modeling, a method that allows statistical inference to be performed on mechanistic models such as ours. Output from the three models is then examined to determine their goodness of fit and the biological plausibility of the parameter values required by each to fit the population data. While all three models are capable of emulating the observed cyclic dynamics, only the model including both aggression and parasites does so under consistently realistic parameter values, providing theoretical support for the idea that both mechanisms shape red grouse cycles.

A Collision Risk Model to Predict Avian Fatalities at Wind Facilities: An Example Using Golden Eagles, Aquila chrysaetos

Wind power is a major candidate in the search for clean, renewable energy. Beyond the technical and economic challenges of wind energy development are environmental issues that may restrict its growth. Avian fatalities due to collisions with rotating turbine blades are a leading concern and there is considerable uncertainty surrounding avian collision risk at wind facilities. This uncertainty is not reflected in many models currently used to predict the avian fatalities that would result from proposed wind developments. We introduce a method to predict fatalities at wind facilities, based on pre-construction monitoring. Our method can directly incorporate uncertainty into the estimates of avian fatalities and can be updated if information on the true number of fatalities becomes available from post-construction carcass monitoring. Our model considers only three parameters: hazardous footprint, bird exposure to turbines and collision probability. By using a Bayesian analytical framework we account for uncertainties in these values, which are then reflected in our predictions and can be reduced through subsequent data collection. The simplicity of our approach makes it accessible to ecologists concerned with the impact of wind development, as well as to managers, policy makers and industry interested in its implementation in real-world decision contexts. We demonstrate the utility of our method by predicting golden eagle (Aquila chrysaetos) fatalities at a wind installation in the United States. Using pre-construction data, we predicted 7.48 eagle fatalities year-1 (95% CI: (1.1, 19.81)). The U.S. Fish and Wildlife Service uses the 80th quantile (11.0 eagle fatalities year-1) in their permitting process to ensure there is only a 20% chance a wind facility exceeds the authorized fatalities. Once data were available from two-years of post-construction monitoring, we updated the fatality estimate to 4.8 eagle fatalities year-1 (95% CI: (1.76, 9.4); 80th quantile, 6.3). In this case, the increased precision in the fatality prediction lowered the level of authorized take, and thus lowered the required amount of compensatory mitigation.

Understanding the Population Consequences of Acoustic Disturbance for Marine Mammals

Loud anthropogenic underwater noise, such as that associated with sonar operations, pile driving, or seismic surveys, can cause behavioral and physiological disturbance to many animals that may affect their survival or ability to breed. However, no formal framework for assessing the population-level consequences of this disturbance is currently available. We describe an interim version of a framework developed by a working group on the population consequences of disturbance, funded by the US Office of Naval Research through the University of California, that can be used to assess the effects of offshore renewable energy developments on marine mammal populations.

A Dynamic State Model of Migratory Behavior and Physiology to Assess the Consequences of Environmental Variation and Anthropogenic Disturbance on Marine Vertebrates

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.

Indirect effects of primary prey population dynamics on alternative prey

We develop a theory of generalist predation showing how alternative prey species are affected by changes in both mean abundance and variability (coefficient of variation) of their predators primary prey. The theory is motivated by the indirect effects of cyclic rodent populations on ground-breeding birds, and developed through progressive analytic simplifications of an empirically-based model. It applies nonetheless to many other systems where primary prey have fast life-histories and can become superabundant, thus facilitating impact on alternative prey species and generating highly asymmetric interactions. Our results suggest that predator effects on alternative prey should generally decrease with mean primary prey abundance, and increase with primary prey variability (low to high CV)-unless predators have strong aggregative responses, in which case these results can be reversed. Approximations of models including predator dynamics (general numerical response with possible delays) confirm these results but further suggest that negative temporal correlation between predator and primary prey is harmful to alternative prey. Finally, we find that measurements of predator numerical responses are crucial to predict-even qualitatively-the response of ecosystems to changes in the dynamics of outbreaking prey species.

State‐space modelling of the flight behaviour of a soaring bird provides new insights to migratory strategies

U.S. Department of Energy (Grant DEEE0003538); U.S. Fish and Wildlife Service (Pennsylvania SWG grants T-12 and T47-R-1)