Lisa M. Angeloni

A synthesis of two decades of research documenting the effects of noise on wildlife

Global increases in environmental noise levels – arising from expansion of human populations, transportation networks, and resource extraction – have catalysed a recent surge of research into the effects of noise on wildlife. Synthesising a coherent understanding of the biological consequences of noise from this literature is challenging. Taxonomic groups vary in auditory capabilities. A wide range of noise sources and exposure levels occur, and many kinds of biological responses have been observed, ranging from individual behaviours to changes in ecological communities. Also, noise is one of several environmental effects generated by human activities, so researchers must contend with potentially confounding explanations for biological responses. Nonetheless, it is clear that noise presents diverse threats to species and ecosystems and salient patterns are emerging to help inform future natural resource‐management decisions. We conducted a systematic and standardised review of the scientific literature published from 1990 to 2013 on the effects of anthropogenic noise on wildlife, including both terrestrial and aquatic studies. Research to date has concentrated predominantly on European and North American species that rely on vocal communication, with approximately two‐thirds of the data set focussing on songbirds and marine mammals. The majority of studies documented effects from noise, including altered vocal behaviour to mitigate masking, reduced abundance in noisy habitats, changes in vigilance and foraging behaviour, and impacts on individual fitness and the structure of ecological communities. This literature survey shows that terrestrial wildlife responses begin at noise levels of approximately 40 dBA, and 20% of papers documented impacts below 50 dBA. Our analysis highlights the utility of existing scientific information concerning the effects of anthropogenic noise on wildlife for predicting potential outcomes of noise exposure and implementing meaningful mitigation measures. Future research directions that would support more comprehensive predictions regarding the magnitude and severity of noise impacts include: broadening taxonomic and geographical scope, exploring interacting stressors, conducting larger‐scale studies, testing mitigation approaches, standardising reporting of acoustic metrics, and assessing the biological response to noise‐source removal or mitigation. The broad volume of existing information concerning the effects of anthropogenic noise on wildlife offers a valuable resource to assist scientists, industry, and natural‐resource managers in predicting potential outcomes of noise exposure.

Sexual selection in a simultaneous hermaphrodite with hypodermic insemination: body size, allocation to sexual roles and paternity

Theory predicts that variation in body size within a population of simultaneous hermaphrodites should affect sex allocation, leading to individual differences in mating strategies and increased investment in female function with size. Small animals with fewer resources should invest proportionally more of their resources in male function than large animals, resulting in sperm displacement and paternity patterns that are independent of body size. This study investigated the effect of body size on mating patterns, egg production (an indirect measure of sperm transfer) and paternity in Alderia modesta, a sperm-storing, hermaphroditic sea slug with hypodermic insemination. The relative sizes of two hermaphrodites affected the probability and duration of inseminations; smaller animals inseminated larger mates for longer than vice versa. Sperm transfer began at a smaller size and age than egg production, and estimates of both sperm transfer and egg production increased with body size. Paternity patterns varied widely; in this species, unpredictable sperm precedence patterns may be a consequence of hypodermic insemination and the lack of a well-defined sperm storage organ. Hypodermic injections across all sections of the body successfully transferred sperm and fertilized eggs. The function and consequences of hypodermic insemination are discussed. Copyright 2003 Published by Elsevier Ltd on behalf of The Association for the Study of Animal Behaviour.

Body size influences mating strategies in a simultaneously hermaphroditic sea slug, Aplysia vaccaria

The relationship between body size and hermaphroditic mating strategies was studied by following a population of the sea slug, Aplysia vaccaria, for one year. Fourteen individuals were tagged with internal microchips, and all mating pairs were weighed. Tagged individuals mated repeatedly both as sperm recipients and sperm donors. There was a trend toward size-assortative mating and size-assortative spatial clustering, and animals acting as females were larger than the average mass for the population. These findings support prior studies showing an association between larger relative size and sperm recipient roles in hermaphroditic gastropods, and highlight the need for critical experiments to determine the mechanisms of role choice and mate choice.

The Effect of Human Activities and Their Associated Noise on Ungulate Behavior

Background The effect of anthropogenic noise on terrestrial wildlife is a relatively new area of study with broad ranging management implications. Noise has been identified as a disturbance that has the potential to induce behavioral responses in animals similar to those associated with predation risk. This study investigated potential impacts of a variety of human activities and their associated noise on the behavior of elk (Cervus elaphus) and pronghorn (Antilocapra americana) along a transportation corridor in Grand Teton National Park. Methodology/Principal Findings We conducted roadside scan surveys and focal observations of ungulate behavior while concurrently recording human activity and anthropogenic noise. Although we expected ungulates to be more responsive with greater human activity and noise, as predicted by the risk disturbance hypothesis, they were actually less responsive (less likely to perform vigilant, flight, traveling and defensive behaviors) with increasing levels of vehicle traffic, the human activity most closely associated with noise. Noise levels themselves had relatively little effect on ungulate behavior, although there was a weak negative relationship between noise and responsiveness in our scan samples. In contrast, ungulates did increase their responsiveness with other forms of anthropogenic disturbance; they reacted to the presence of pedestrians (in our scan samples) and to passing motorcycles (in our focal observations). Conclusions These findings suggest that ungulates did not consistently associate noise and human activity with an increase in predation risk or that they could not afford to maintain responsiveness to the most frequent human stimuli. Although reduced responsiveness to certain disturbances may allow for greater investment in fitness-enhancing activities, it may also decrease detections of predators and other environmental cues and increase conflict with humans.

Locally adapted traits maintained in the face of high gene flow

Gene flow between phenotypically divergent populations can disrupt local adaptation or, alternatively, may stimulate adaptive evolution by increasing genetic variation. We capitalised on historical Trinidadian guppy transplant experiments to test the phenotypic effects of increased gene flow caused by replicated introductions of adaptively divergent guppies, which were translocated from high- to low-predation environments. We sampled two native populations prior to the onset of gene flow, six historic introduction sites, introduction sources and multiple downstream points in each basin. Extensive gene flow from introductions occurred in all streams, yet adaptive phenotypic divergence across a gradient in predation level was maintained. Descendants of guppies from a high-predation source site showed high phenotypic similarity with native low-predation guppies in as few as ~12 generations after gene flow, likely through a combination of adaptive evolution and phenotypic plasticity. Our results demonstrate that locally adapted phenotypes can be maintained despite extensive gene flow from divergent populations.

Fear, food and sexual ornamentation: plasticity of colour development in Trinidadian guppies

The evolution of male ornamentation often reflects compromises between sexual and natural selection, but it may also be influenced by phenotypic plasticity. We investigated the developmental plasticity of male colour ornamentation in Trinidadian guppies in response to two environmental variables that covary in nature: predation risk and food availability. We found that exposure to chemical predator cues delayed the development of pigment-based colour elements, which are conspicuous to visual-oriented predators. Predator cues also reduced the size of colour elements at the time of maturity and caused adult males to be less colourful. To the best of our knowledge, these findings provide the first example of a plastic reduction in the development of a sexually selected male ornament in response to predator cues. The influence of predator cues on ornamentation probably affects individual fitness by reducing conspicuousness to predators, but could reduce attractiveness to females. Reduced food availability during development caused males to delay the development of colour elements and mature later, probably reflecting a physiological constraint, but their coloration at maturity and later in adulthood was largely unaffected, suggesting that variation in food quantity without variation in quality does not contribute to condition dependence of the trait.

Size-dependent mating and gender choice in a simultaneous hermaphrodite, Bulla gouldiana

Simultaneous hermaphrodites are predicted to optimally divide resources between male and female function, which can result in both size-dependent mating behaviors and conflict between potential mates. Predicted strategies include size-assortative mating, conditional exchange of gametes, and mating patterns where relative size affects investment in each sexual role. This study investigated the effect of body size on the mating strategies of a hermaphroditic opisthobranch, Bulla gouldiana. Although individuals were spatially aggregated in the field with high levels of movement and size variation, there was little evidence for predictions. Laboratory experiments, however, revealed complicated effects of mass on the probability and duration of mating, as well as gender choice. Pairs were more likely to mate if they included at least one large animal, with the larger animal typically inseminating the smaller. When both individuals were large, they were more likely to each mate in both sexual roles by switching roles once. Although B. gouldiana did not usually alternate between sexual roles multiple times within mating events, paired individuals behaved similarly (neither or both mating as sperm donors) more often than expected by chance. This suggests some level of reciprocity, which is unlikely to be conditional given rates of unilateral mating. When the larger member of the mating pair inseminated the smaller, the duration of insemination increased with the size of the smaller sperm recipient. Copulations lasted longer in pairs that switched sexual roles than in those that did not switch roles. This study suggests that variation in body size can lead to size-dependent mating patterns, but only some of the patterns in B. gouldiana support theoretical predictions. We review other studies that have addressed similar issues, providing inconsistent mating patterns in sperm-storing hermaphrodites.

Behavioral responses associated with a human-mediated predator shelter

Human activities in protected areas can affect wildlife populations in a similar manner to predation risk, causing increases in movement and vigilance, shifts in habitat use and changes in group size. Nevertheless, recent evidence indicates that in certain situations ungulate species may actually utilize areas associated with higher levels of human presence as a potential refuge from disturbance-sensitive predators. We now use four-years of behavioral activity budget data collected from pronghorn (Antilocapra americana) and elk (Cervus elephus) in Grand Teton National Park, USA to test whether predictable patterns of human presence can provide a shelter from predatory risk. Daily behavioral scans were conducted along two parallel sections of road that differed in traffic volume - with the main Teton Park Road experiencing vehicle use that was approximately thirty-fold greater than the River Road. At the busier Teton Park Road, both species of ungulate engaged in higher levels of feeding (27% increase in the proportion of pronghorn feeding and 21% increase for elk), lower levels of alert behavior (18% decrease for pronghorn and 9% decrease for elk) and formed smaller groups. These responses are commonly associated with reduced predatory threat. Pronghorn also exhibited a 30% increase in the proportion of individuals moving at the River Road as would be expected under greater exposure to predation risk. Our findings concur with the ‘predator shelter hypothesis’, suggesting that ungulates in GTNP use human presence as a potential refuge from predation risk, adjusting their behavior accordingly. Human activity has the potential to alter predator-prey interactions and drive trophic-mediated effects that could ultimately impact ecosystem function and biodiversity.

Research Priorities from Animal Behaviour for Maximising Conservation Progress

Poor communication between academic researchers and wildlife managers limits conservation progress and innovation. As a result, input from overlapping fields, such as animal behaviour, is underused in conservation management despite its demonstrated utility as a conservation tool and countless papers advocating its use. Communication and collaboration across these two disciplines are unlikely to improve without clearly identified management needs and demonstrable impacts of behavioural-based conservation management. To facilitate this process, a team of wildlife managers and animal behaviour researchers conducted a research prioritisation exercise, identifying 50 key questions that have great potential to resolve critical conservation and management problems. The resulting agenda highlights the diversity and extent of advances that both fields could achieve through collaboration.

Environmental enrichment affects adrenocortical stress responses in the endangered black-footed ferret

Potential stressors of wildlife living in captivity, such as artificial living conditions and frequent human contact, may lead to a higher occurrence of disease and reduced reproductive function. One successful method used by wildlife managers to improve general well-being is the provision of environmental enrichment, which is the practice of providing animals under managed care with environmental stimuli. The black-footed ferret (Mustela nigripes) is a highly-endangered carnivore species that was rescued from extinction by removal of the last remaining individuals from the wild to begin an ex situ breeding program. Our goal was to examine the effect of environmental enrichment on adrenocortical activity in ferrets by monitoring fecal glucocorticoid metabolites (FGM). Results demonstrated that enrichment lowered FGM in juvenile male ferrets, while increasing it in adult females; enrichment had no effect on FGM in juvenile females and adult males. These results correspond with our findings that juvenile males interacted more with the enrichment items than did adult females. However, we did not detect an impact of FGM on the incidence of disease or on the ability of ferrets to become reproductive during the following breeding season. We conclude that an environmental enrichment program could benefit captive juvenile male ferrets by reducing adrenocortical activity.