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The International Journal of Comparative Psychology is sponsored by the International Society for Comparative Psychology. It is a peer-reviewed open-access digital journal that publishes studies on the evolution and development of behavior in all animal species. It accepts research articles and reviews, letters and audiovisual submissions.

Volume 20, Issue 2, 2007

Articles

Endocrinology of Stress

When an animal detects a stressor, it initiates a stress response. The physiological aspects of this stress response are mediated through two endocrine systems. The catecholamine hormones epinephrine and norepinephrine are released from the adrenal medulla very rapidly and have numerous effects on behavior, metabolism, and the cardiovascular system. This is commonly termed the Fight-or-Flight response. On a longer time scale, the glucocorticoid hormones are released from the adrenal cortex. They interact with intracellular receptors and initiate gene transcription. This production of new proteins means that glucocorticoids have a delayed, but more sustained, effect than the catecholamines. The glucocorticoids orchestrate a wide array of responses to the stressor. They have direct effects on behavior, metabolism and energy trafficking, reproduction, growth, and the immune system. The sum total of these responses is designed to help the animal survive a short-term stressful stimulus. However, under conditions of long-term stress, the glucocorticoid-mediated effects become maladaptive and can lead to disease.

From Classic Aspects of the Stress Response to Neuroinflammation and Sickness: Implications for Individuals and Offspring

Accumulating evidence suggests that exposure to psychological stressors leads to increased expression of pro-inflammatory cytokines and activation of inflammatory-related pathways in the central nervous system. Several logical predictions arise from these findings: (1) stressor exposure should produce changes in behavior that are reminiscent of acute illness; (2) administration of antiinflammatory agents should ameliorate some behavioral consequences of stressor exposure; and (3) there should be convergence between anatomical and neurochemical pathways activated by stressor exposure and those involved in mitigating sickness behaviors. Importantly, these predictions have been tested in our laboratory across multiple stressor paradigms (footshock, maternal separation, and during acute alcohol withdrawal) using two species (rats and guinea pigs), suggesting that sickness may represent a more general motivational state that can be elicited by a diverse range of psychological challenges. Implications of these findings for understanding stress-related changes in behavior, mood and neuroinflammatory processes will be discussed with special reference to implications for the individual and reproductive fitness.

The Behavioral Ecology of Disturbance Responses

Measuring the impacts of anthropogenic activities on wildlife is crucial for ensuring effective management. Animal behavior is often considered a sensitive index of impact, but its use requires detailed understanding of the context dependent decisions animals make. In this manuscript I identify a number of areas where insights from the field of animal behavior are relevant to studies of human disturbance and activity. In particular, I differentiate between disturbance effects and disturbance impacts and show how context-dependent decision-making often makes animal behavior an unreliable index of impact. I show the areas where animal behavior can be useful in quantifying minimum disturbance impact when additional information is available, and identify a number of areas where further research may help improve the management of anthropogenic activities within wildlife areas.

A Brief Review of Anthropogenic Sound in the Oceans

Sound in the oceans is generated by a variety of natural sources, such as breaking waves, rain, and marine animals, as well as a variety of human-produced sources, such as ships, sonars and seismic signals. This overview will begin with a quick review of some basic properties of sound waves with particular reference to differences between the behaviours of these waves underwater versus in air. A basic understanding of the physics of underwater sound is critical to understanding how marine animal acoustic signals have evolved relative to their different functions and how changes in the marine acoustic environment due to increasing anthropogenic sound in the oceans may impact these species. We will then review common sources of anthropogenic sound in the oceans. The frequency contributions of three major sources of underwater anthropogenic sound and their relative intensities will be discussed: naval exercises, seismic surveys and commercial shipping. Finally, a case study examining relative inputs to a regional noise budget, that of the Gerry E. Studds Stellwagen Bank National Marine Sanctuary, will be presented to introduce the audience to methodologies for characterizing and managing sound on an ecosystem level.

Effects of Noise on Rodent Physiology

Experiments are described in which Sprague Dawley rats were deliberately subjected to a daily 15- min white noise regime (90 dB) for 3 or 6 weeks, to determine its effects on the cardiovascular system and intestinal mucosa. In one set of experiments cardiovascular responses were monitored by radiotelemetry. Exposure to noise increased heart rate and mean arterial pressure and reduced stimulation of the parasympathetic nervous system. In the second set of experiments, one group of rats was exposed to the noise protocol for 3 weeks and a second group was not. All the rats were then anaesthetized and the small intestines of half the animals were fixed for microscopy. The remaining rats had their mesenteric microvasculature perfused for one minute with fluorescent albumin before fixing for microscopy. The rats exposed to noise showed significantly more eosinophils and degranulated mast cells in the intestinal villi than the quiet rats. In addition, the villi were swollen and the epithelial cells had widened junctions. The noise group also showed significantly more leakage of fluorescent albumin from the mesenteric microvessels. These experiments demonstrate that 90 dB white noise reduces stimulation the parasympathetic nervous system and also induces an inflammatory response in the intestinal mucosa, resulting in structural damage. These results are consistent with a stress response.

The Effect of Transportation Noise on Health and Cognitive Development:A Review of Recent Evidence

Noise from transport is an increasingly prominent feature of the urban environment. Whilst the auditory effects of noise on humans are established, non-auditory effects - the effects of noise exposure on human health, well-being and cognitive development - are less well established. This narrative review evaluates recent studies of aircraft and road traffic noise that have advanced or synthesized knowledge about several aspects of adult and child health and cognition. Studies have demonstrated a moderate effect of transport noise on hypertension, cardiovascular disease and catecholamine secretion: there is also evidence for an effect on psychological symptoms but not for the onset of more serious clinically defined psychiatric disorder. One way noise may affect health is through annoyance: noise causes annoyance responses in both children and adults and annoyance may cause stress-responses and subsequent illness. Another possible mechanism is sleep disturbance: transport noise has been found to disturb sleep in laboratory and field studies, although there is evidence for adaptation to noise exposure. For children effects of aircraft and road traffic noise have been observed for impaired reading comprehension and memory skills: there is equivocal evidence for an association with blood pressure. To date most health effects have been very little researched and studies have yet to examine in detail how noise exposure interacts with other environmental stressors. In conclusion, noise is a main cause of environmental annoyance and it negatively affects the quality of life of a large proportion of the population. In addition, health and cognitive effects, although modest, may be of importance given the number of people increasingly exposed to environmental noise and the chronic nature of exposure.

A Brief Review of Known Effects of Noise on Marine Mammals

Marine mammals, especially cetaceans, are highly vocal and dependent on sound for almost all aspects of their lives, e.g. food-finding, reproduction, communication, detection of predators/hazards, and navigation. They are thus likely sensitive to anthropogenic noise. Sound has a large potential area of impact, sometimes covering millions of square kilometers of ocean with levels high enough to cause possible disturbance in marine mammals. There can be great variation in the reaction of marine mammals to noise, depending on such factors as species, individual, age, sex, prior experience with noise, and behavioral state. Species with similar hearing capabilities can respond differently to the same noise. Observed effects of noise on marine mammals include: changes in vocalizations, respiration, swim speed, diving, and foraging behavior; displacement, avoidance, shifts in migration path, stress, hearing damage, and strandings. Responses of marine mammals to noise can often be subtle and barely detectable, and there are many documented cases of apparent tolerance of noise. However, marine mammals showing no obvious avoidance or changes in activities may still suffer important, even lethal, consequences. Acoustically-induced strandings may displace a local beaked whale ( Ziphiidae ) population (for an extended period if not permanently) or even possibly eliminate most of its members. As beaked whales seem to be found in small, possibly genetically isolated, resident populations, even a transient and localized acoustic impact could have prolonged population consequences. Observed reactions to noise in marine mammals could theoretically result in impacts such as decreased foraging efficiency, higher energetic demands, less group cohesion, higher predation, decreased reproduction, and thus seriously impact the population. Alternatively, they may be harmless. However, noise is thought to contribute to at least some species’ declines or lack of recovery (Southern resident killer whales ( Orcinus orca ) , western gray whales ( Eschrichtius robustus ) off Sakhalin).

Environmental Noise and Decision Making Possible Implications of Increases in Anthropogenic Noise for Information Processing in Marine Mammals

Recent increases in anthropogenic noise in the marine environment are a source of concern for the current welfare and future fitness of many marine mammal species. In this article I explore the specific question of how environmental noise could affect information processing. I also discuss the possible changes in behavior that would result, and how these changes could negatively impact the welfare and fitness of marine mammals. I identify two ways in which environmental noise could affect decision-making. First, environmental noise could add statistical noise to the detection of auditory signals, either masking them completely or rendering them ambiguous. Animals can respond to this problem either by moving away from the source of noise, or by altering the characteristics of their signal processing to increase the signal to noise ratio. Second, environmental noise could generate emotional states of fear or anxiety that cause biases in information processing. Anxiety is an emotion that functions as an early warning of potential threats, and is associated with a suite of changes in information processing including sensitization to stimuli potentially associated with threats, and pessimistic biases in decision making resulting in increased risk aversion. Although these changes are clearly beneficial in the short term, chronic anxiety is likely to result in behavioral changes that will be detrimental to an animal’s fitness in the longer term. Thus, there are likely to be subtle effects of noise on decision-making that have not so far been considered in relation to the effects of anthropogenic noise on marine mammal behavior.

The Influence of Metal Pollution on the Immune System A Potential Stressor for Marine Mammals in the North Sea

Marine mammals of the North Sea are loaded with metal pollutants. The environmental exposure induces concentrations bioavailable to immune cells high enough to affect their function. Such an imbalance of the immune system caused by pollutants may play a significant role in the incidence of infectious diseases in marine mammals. Metals influence the function of immunocompetent cells by a variety of mechanisms. Depending on the particular metal, its speciation, concentration and bioavailability, and a number of other factors, a continuous metal exposure will result in an immunosuppression or immunoenhancement effects. Both effects were demonstrated on the cellular level in animals of the North Sea. This article reviews metal concentrations in the North and Baltic Seas particularly in tissues of marine mammals, discusses pollutants effects on health and immune functions, and underlines the still existing problem of animals living in polluted coastal areas.

Potential Synergism between Stress and Contaminants in Free-ranging Cetaceans

Noise has increased significantly over the last decades in oceans, and this trend is accelerating in large part because of oil exploration and exploitation, both of which are expanding worldwide. Considered together with recent evidence that noise disturbs the behavior, echolocation, navigation and communication of marine mammals, it is likely that noise, increasingly encountered by marine mammals, will add to their allostatic load. Glucocorticoids (GCs) are the major hormones that mediate the long term effects of stress. GCs’ effects depend, among other factors, on the intracellular concentrations of the various isoforms of the glucocorticoid receptors (GR). Tissue and cell-type specificity are also conferred by the presence in target cells of GR ligands such as chaperones, cochaperones and modulatory element binding proteins whose concentrations vary according to tissue, cell types and even to the cell cycle phase. The normal regulation of GCs production in adult life relies on the normal development of the hypothalamus-pituitary adrenal (HPA) axis in uterine and early postnatal life, which in turn depends on the absence of chronic stress imposed to both the mother and newborn during these critical periods. Worldwide, cetacean populations, such as the beluga population inhabiting the St Lawrence Estuary (SLE) in Canada, are exposed to anthropogenic stressors, and are contaminated by persistent lipophilic contaminants of which many are abundantly transferred to newborns during lactation. GCs and certain organochlorine contaminants (OCs), for instance dioxin-related polychlorinated biphenyls (DRPBs), mediate their prolonged and profound effects through nuclear receptors such as aryl hydrocarbon receptors (AhR). These effects are exerted on most organs, especially on the developing brain and lymphoid organs of fetuses and juveniles and on adrenal glands of adult mammals. Multiple interactions have been demonstrated between GCs and OCs, often through interactions between their receptors. These interactions may disturb the delicate balance required by immature and adult mammals to react optimally to stressors.

Fishery Effects on Dolphins Targeted by Tuna Purse-seiners in the Eastern Tropical Pacific Ocean

Dolphins in the eastern tropical Pacific Ocean (ETP), particularly spotted (Stenella attenuate) and spinner (Stenella longirostris) dolphins, are subject to fishery-induced stress due to chase and encirclement by tuna purse-seiners intent on capturing the large yellowfin tuna that are frequently found associated with dolphin schools in this area of the Pacific Ocean. The direct, observed mortality of dolphins in the fishing nets has decreased over the years from several hundred thousand annually during the early 1960’s when the fishing practice originated, to less than 5000 dolphins annually (thought to be a biologically insignificant level) since the early 1990s. Despite the decrease in observed mortality, the dolphin populations have not been recovering as expected. In an effort to determine whether fishery-related stress may be contributing to this lack of recovery, through unobserved effects on survival or reproduction, a variety of studies have been and continue to be conducted examining various aspects of interactions between ETP dolphins and the tuna purse-seine fishery. These studies include a review of current knowledge of stress physiology in mammals, a necropsy program to examine dolphins killed during purse-seining operations, a chase-recapture experiment, and various analyses of existing (historical) data which have led to ongoing studies of fishery effects on mother-calf pairs, ETP dolphin reproductive biology, and analyses of dolphin school composition. The effect of noise has not been addressed directly in these studies, but potentially contributes to fishery-related stress in terms of initiating the significant and prolonged evasion response typical of dolphin schools reacting to tuna purse-seiners in the ETP. Although studies completed to date have not provided a definitive answer to whether fishery-induced stress is a significant factor in the lack of dolphin stock recovery in the ETP, it is possible that at least some adults, and probably many young dolphins, are negatively affected by interactions with tuna purseseine fishing operations.

The Long-term Consequences of Short-term Responses to Disturbance Experiences from Whalewatching Impact Assessment

Studies often use behavioral responses to detect the impact of given disturbances on animals. However, the observation of these short-term responses can often lead to contradicting results. Here we describe studies focusing on the impacts of whale watching to show how the biological relevance of short-term responses can be inferred from contextual information. They showed that short-term behavioral responses could have long-term consequences for individuals and their populations using information about variation in response magnitude with exposure levels, long term population biology data, and multiple response variables. They showed that the added energetic constraints of the responses can impair life functions and lead to influences on vital rates with the potential to affect population viability. Individuals will manage disturbances as another ecological variable and will assess its costs in relation to other energetic trade-offs associated with the occupancy of the habitat in which the disturbance takes place. This can lead to rapid shift in tactics to cope with the disturbance, such as shift from short-term avoidance tactics to long-term habitat abandonment. When individuals cannot elude proximity to the disturbance, their fitness is reduced as observed through reduced reproductive success. These studies provide mechanisms to inform the US National Research Councils’ Population Consequences of Acoustic Disturbance framework in which the influence of noise impact of on marine mammal conservation can be studied.

Adaptive Management, Population Modeling and Uncertainty Analysis for Assessing the Impacts of Noise on Cetacean Populations

Population modeling is now widely used in threatened species management and for predicting the impacts and benefits of competing management options. However, some argue that the results of models must be used with caution, particularly when data are limited. This is important, as even the simplest models would generally require more data (and knowledge) than are available in order to have complete confidence in model predictions. In particular, population models often suffer from a lack of data on demographic rates, spatial distribution, dispersal, management responses, habitat correlations and the magnitude of temporal variations. A number of authors identify behavioral and physiological responses of animals to anthropogenic noise. Assessing population level impacts of noise on cetacean populations is essential to understanding how noise impacts on the future viability of marine mammal populations. This assessment will be particularly challenging due to the difficulties associated with identifying a clear link between behavioral responses of animals and physiological impacts, observing and measuring changes in cetacean population parameters and the long lag-times over which population changes manifest in long-lived species. The urgency of the conservation situation for many of these socially important species demands immediate action, despite pervasive uncertainty. Adaptive management provides a coherent framework for action and continuous improvement under uncertainty. I review the elements of adaptive management and discuss the role of population modeling in that context. I discuss Bayesian approaches to enhancing inferential power and reducing uncertainty in model parameter estimation. I then review approaches to characterizing irreducible uncertainty with Monte Carlo methods and sensitivity analysis and conclude with a brief discussion of formal decision tools available to assist with decision making under severe uncertainty. I propose that urgently needed action should not be postponed due to uncertainty and that adaptive management provides a coherent framework for instituting immediate action with a plan for learning.

Anthropogenic Noise as a Stressor in Animals: A Multidisciplinary Perspective

This paper could not have been written without the financial and organizational support from Dieter Paulmann and Jo Hastie respectively. Thanks are also due to 2 anonymous reviewers, whose comments on an earlier version of the manuscript greatly improved the paper. The views expressed in this paper are those of the authors alone and do not represent those of Stellwagen Bank National Marine Sanctuary, the U.S. National Marine Sanctuary Program, Southwest Fisheries Science Center, the U.S. National Marine Fisheries Service, NOAA and/or any other institution or agency. Correspondence concerning this article should be addressed to Andrew Wright, Leviathan Sciences, U.S.A. (marinebrit@gmail.com). Consequences of extreme noise exposure are obvious and usually taken into some consideration in the management of many human activities that affect either human or animal populations. However, the more subtle effects such as masking, annoyance and changes in behavior are often overlooked, especially in animals, because these subtleties can be very difficult to detect. To better understand the possible consequences of exposure to noise, this review draws from the available information on human and animal physiology and psychology, and addresses the importance of context (including physiological and psychological state resulting from any previous stressor exposure) in assessing the true meaning of behavioral responses. The current consensus is that the physiological responses to stressors of various natures are fairly stereotyped across the range of species studied. It is thus expected that exposure to noise can also lead to a physiological stress response in other species either directly or indirectly through annoyance, a secondary stressor. In fact many consequences of exposure to noise can result in a cascade of secondary stressors such as increasing the ambiguity in received signals or causing animals to leave a resourceful area, all with potential negative if not disastrous consequences. The context in which stressors are presented was found to be important not only in affecting behavioral responses, but also in affecting the physiological and psychological responses. Young animals may be particularly sensitive to stressors for a number of reasons including the sensitivity of their still-developing brains. Additionally, short exposure to stressors may result in long-term consequences. Furthermore, physiological acclimation to noise exposure cannot be determined from apparent behavioral reactions alone due to contextual influence, and negative impacts may persist or increase as a consequence of such behavioral changes. Despite the lack of information available to managers, uncertainty analysis and modeling tools can be coupled with adaptive management strategies to support decision making and continuous improvements to managing the impacts of noise on free-ranging animals.

Do Marine Mammals Experience Stress Related to Anthropogenic Noise?

This paper could not have been written without the financial and organizational support from Dieter Paulmann and Jo Hastie respectively. Thanks are also due to two anonymous reviewers, whose comments on an earlier version of the manuscript greatly improved the paper. The views expressed in this paper are those of the authors alone and do not represent those of Stellwagen Bank National Marine Sanctuary, the U.S. National Marine Sanctuary Program, Southwest Fisheries Science Center, the U.S. National Marine Fisheries Service, NOAA and/or any other institution or agency. Correspondence concerning this article should be addressed to Andrew Wright, Leviathan Sciences, U.S.A. (marinebrit@gmail.com). Sound travels much further than light in the marine environment. As a result, marine mammals, especially cetaceans, rely heavily on sound for many important life functions, including breeding and foraging. This reliance on sound means it is quite likely that exposure to noise will have some detrimental effects on these life functions. However, there has been little application to marine mammals of the knowledge available in other species of stress responses to noise and other stressors. In this paper we begin to integrate what is known about marine mammals with the current knowledge gained in terrestrial mammals about stress physiology, specifically considering physiological and psychological context and thus also cumulative and synergistic impacts. We determined that it is reasonable to extrapolate information regarding stress responses in other species to marine mammals, because these responses are highly conserved among all species in which they have been examined to date. As a result, we determined that noise acts as a stressor to marine mammals. Furthermore, given that marine mammals will likely respond in a manner consistent with other species studied, repeated and prolonged exposures to stressors (including or induced by noise) will be problematic for marine mammals of all ages. A range of issues may arise from the extended stress response including, but not limited to, suppression of reproduction (physiologically and behaviorally), accelerated aging and sickness-like symptoms. We also determined that interpretation of a reduction in behavioral responses to noise as acclimation will be a mistake in many situations, as alternative reasons for the observed results are much more likely. We recommend that research be conducted on both stress responses and life-history consequences of noise exposure in marine mammals, while emphasizing that very careful study designs will be required. We also recommend that managers incorporate the findings presented here in decisions regarding activities that expose marine mammals to noise. In particular, the effects of cumulative and synergistic responses to stressors can be very important and should not be dismissed lightly.