Factors modulating the behavioral and physiological stress responses: Do they modify the relationship between flight initiation distance and corticosterone reactivity?

Understanding how vulnerable species are to new stressors, such as anthropogenic changes, is crucial for mitigating their potential negative consequences. Many studies have investigated species sensitivity to human disturbance by focusing on single behavioral or physiological parameters, such as flight initiation distance and glucocorticoid levels. However, little is known about the differential effect that modulating factors might have on behavioral versus physiological stress responses across species. This lack of knowledge make difficult to understand the relationship between both types of reactions, and thus to assess to what extent a behavioral reaction is representative of an internal physiological stress response or vice versa. We collected published data on bird flight initiation distances (FID) and corticosterone (CORT) responses, the two most frequently used indicators of stress reaction. We then investigated how spatio-temporal factors or species-specific characteristics relate to these behavioral and physiological stress responses, and potentially modify the relationship between them. Additionally, we evaluated the strength of the correlation between the two stress responses (behavioral and physiological). Our findings showed that FID and CORT responses were poorly correlated across species, and the lack of correlation was attributable to modulating factors (e.g. latitude and body mass) which influence behavior and physiology differently. These modulating factors, therefore, should be taken into consideration to better interpret FID and CORT responses in the context of species vulnerability to stress.

Human recreation decreases antibody titre in bird nestlings: an overlooked transgenerational effect of disturbance.

Outdoor recreational activities are booming and most animals perceive humans as predators, which triggers behavioural and/or physiological reactions [e.g. heart rate increase, activation of the hypothalamic-pituitary-adrenal (HPA) axis]. Physiological stress reactions have been shown to affect the immune system of an animal and therefore may also affect the amount of maternal antibodies a female transmits to her offspring. A few studies have revealed that the presence of predators affects the amount of maternal antibodies deposited into eggs of birds. In this study, using Eurasian blue and great tit offspring (Cyanistes caeruleus and Parus major) as model species, we experimentally tested whether human recreation induces changes in the amount of circulating antibodies in young nestlings and whether this effect is modulated by habitat and competition. Moreover, we investigated whether these variations in antibody titre in turn have an impact on hatching success and offspring growth. Nestlings of great tit females that had been disturbed by experimental human recreation during egg laying had lower antibody titres compared with control nestlings. Antibody titre of nestling blue tits showed a negative correlation with the presence of great tits, rather than with human disturbance. The hatching success was positively correlated with the average amount of antibodies in great tit nestlings, independent of the treatment. Antibody titre in the first days of life in both species was positively correlated with body mass, but this relationship disappeared at fledging and was independent of treatment. We suggest that human recreation may have caused a stress-driven activation of the HPA axis in breeding females, chronically increasing their circulating corticosterone, which is known to have an immunosuppressive function. Either, lower amounts of antibodies are transmitted to nestlings or impaired transfer mechanisms lead to lower amounts of immunoglobulins in the eggs. Human disturbance could, therefore, have negative effects on nestling survival at early life-stages, when nestlings are heavily reliant on maternal antibodies, and in turn lead to lower breeding success and parental fitness. This is a so far overlooked effect of disturbance on early life in birds.

Effect of human recreation on bird anti-predatory response.

Wildlife perceive humans as predators, and therefore normally flushes. Flight initiation distance (FID) is the distance a human can approach an animal at a steady pace until it flushes. Recently, several studies showed differences in within-species FID according to human presence by comparing urban and rural habitats, with urban birds showing reduced FIDs. However, urban and rural habitats also differ in structure, which might affect FID. Therefore, in order to understand the real effect of human presence, we investigated whether differences in FID are also present in natural habitats (forests), differing only in the intensity of human use for recreation. We found that human frequentation had a distinct effect on bird escape responses, with shorter FIDs in forests more-heavily frequented by humans than in forests rarely visited by humans. Whether this finding is driven by non-random spatial distribution of personalities (shy vs. bold) or phenotypic plasticity (habituation to humans) cannot be assessed with our data. Studies relying on FIDs should also incorporate human recreation intensity, as this affects the measurements strongly.

Experimental evidence of human recreational disturbance effects on bird-territory establishment.

The worldwide increase in human outdoor activities raises concerns for wildlife. Human disturbances, even at low levels, are likely to impact species during sensitive periods of the annual cycle. However, experimental studies during the putative sensitive period of territory establishment of birds which not only investigate low disturbance levels, but which also exclude the effect of habitat modification (e.g. walking trails) are lacking. Here, we experimentally disturbed birds in forest plots by walking through twice a day during territory establishment. Later we compared the breeding bird community of experimentally disturbed plots with that of undisturbed control plots. We discovered that the number of territories (-15.0%) and species richness (-15.2%) in disturbed plots were substantially reduced compared with control plots. Species most affected included those sensitive to human presence (assessed by flight-initiation distances), open-cup nesters and above-ground foragers. Long-distance migrants, however, were unaffected due to their arrival after experimental disturbance took place. These findings highlight how territory establishment is a sensitive period for birds, when even low levels of human recreation may be perceived as threatening, and alter settlement decisions. This can have important implications for the conservation of species, which might go unnoticed when focusing only on already established birds.

Unmanned aircraft systems as a new source of disturbance for wildlife: A systematic review.

The use of small Unmanned Aircraft Systems (UAS; also known as "drones") for professional and personal-leisure use is increasing enormously. UAS operate at low altitudes (<500 m) and in any terrain, thus they are susceptible to interact with local fauna, generating a new type of anthropogenic disturbance that has not been systematically evaluated. To address this gap, we performed a review of the existent literature about animals' responses to UAS flights and conducted a pooled analysis of the data to determine the probability and intensity of the disturbance, and to identify the factors influencing animals' reactions towards the small aircraft. We found that wildlife reactions depended on both the UAS attributes (flight pattern, engine type and size of aircraft) and the characteristics of animals themselves (type of animal, life-history stage and level of aggregation). Target-oriented flight patterns, larger UAS sizes, and fuel-powered (noisier) engines evoked the strongest reactions in wildlife. Animals during the non-breeding period and in large groups were more likely to show behavioral reactions to UAS, and birds are more prone to react than other taxa. We discuss the implications of these results in the context of wildlife disturbance and suggest guidelines for conservationists, users and manufacturers to minimize the impact of UAS. In addition, we propose that the legal framework needs to be adapted so that appropriate actions can be undertaken when wildlife is negatively affected by these emergent practices.

Happy to breed in the city? Urban food resources limit reproductive output in Western Jackdaws.

Urban areas expand worldwide, transforming landscapes and creating new challenging habitats. Some bird species, mainly omnivorous feeding on human waste and cavity nesters, commonly breed in these habitats and are, therefore, regarded as urban-adapted. Although urban areas may provide new nesting sites and abundant human waste, the low breeding success found in some of these species suggests that the poor protein content in human waste might limit breeding parameters. We investigated whether the breeding success of a cavity nester and omnivorous species commonly breeding in urban areas, the Western Jackdaw (Corvus monedula), depended on the availability of good-quality non-urban food. We approached the objective by combining a literature review and experiments in the field. With the literature review, we compared jackdaw populations in different habitats across Europe and found that clutch size and number of fledglings per pair decreased with distance to non-urban foraging grounds, even after controlling for the effect of colony size, latitude, and climate. In two experiments, we tested whether the breeding success of urban pairs could be increased by supplementing high-quality food, first only during egg formation and second also until chick fledging. Food supplementation during egg formation led to larger eggs and higher hatching success than in urban control nests, but this did not result in higher chick survival. However, when food supplementation was prolonged until fledging in the second experiment, we observed a significant increase of nestling survival. These findings highlight that research and management actions should not only focus on species displaced by urbanization, but also on "urban-adapted" species, as they might be suffering from a mismatch between availability of nesting sites in buildings and adequate non-urban food resources. In these cases, nest sites should be provided in or close to adequate food resources.

Determinants of uncertainty in wildlife responses to human disturbance.

Outdoor recreation is increasing in intensity and space. Areas previously inaccessible are now being visited by ever-growing numbers of people, which increases human-wildlife encounters across habitats. This has raised concern among researchers and conservationists as, even in non-aggressive encounters, animals often perceive humans as predators and mount physiological and behavioural responses that can have negative consequences. However, despite all the research in recent decades, not many general patterns have emerged, especially at the level of populations, and many studies have yielded seemingly contradictory or inconclusive results. We argue that this is partly due to incomplete knowledge of the number and complexity of factors that may modulate the responses of animals. Thus, we aim to provide a conceptual approach intended to highlight the reasons that make it difficult to detect general patterns. We present a comprehensive compilation of factors modulating animal responses to humans at increasing levels (from sensory detection and immediate behavioural and physiological reactions, to changes in fitness and population trends), which may help understanding the uncertainty in the patterns. We observed that there are many modulating factors, which can be categorized as reflecting characteristics of the recreational activity itself (e.g. intensity of human presence), of the animals concerned (e.g. age or antipredatory strategy), and of the spatio-temporal context (e.g. habitat or timing of the encounter). Some factors appear to have non-linear and complex effects, which, if not considered, may lead to erroneous conclusions. Finally, we conclude that the difficulty in finding general patterns will be amplified at higher levels (i.e. at the level of populations), since as we proceed from one level to the next, the number of potential modulating factors accumulates, adding noise and obscuring direct associations between recreation and wildlife. More comprehensive knowledge about which (and how) factors affect animal responses across levels will certainly improve future research design and interpretation, and thus, our understanding of human recreational impacts on wildlife.

Contrasting effects of climate change on rabbit populations through reproduction.

BACKGROUND: Climate change is affecting many physical and biological processes worldwide. Anticipating its effects at the level of populations and species is imperative, especially for organisms of conservation or management concern. Previous studies have focused on estimating future species distributions and extinction probabilities directly from current climatic conditions within their geographical ranges. However, relationships between climate and population parameters may be so complex that to make these high-level predictions we need first to understand the underlying biological processes driving population size, as well as their individual response to climatic alterations. Therefore, the objective of this study is to investigate the influence that climate change may have on species population dynamics through altering breeding season. METHODOLOGY/PRINCIPAL FINDINGS: We used a mechanistic model based on drivers of rabbit reproductive physiology together with demographic simulations to show how future climate-driven changes in breeding season result in contrasting rabbit population trends across Europe. In the Iberian Peninsula, where rabbits are a native species of high ecological and economic value, breeding seasons will shorten and become more variable leading to population declines, higher extinction risk, and lower resilience to perturbations. Whereas towards north-eastern countries, rabbit numbers are expected to increase through longer and more stable reproductive periods, which augment the probability of new rabbit invasions in those areas. CONCLUSIONS/SIGNIFICANCE: Our study reveals the type of mechanisms through which climate will cause alterations at the species level and emphasizes the need to focus on them in order to better foresee large-scale complex population trends. This is especially important in species like the European rabbit whose future responses may aggravate even further its dual keystone/pest problematic. Moreover, this approach allows us to predict not only distribution shifts but also future population status and growth, and to identify the demographic parameters on which to focus to mitigate global change effects.

Dying like rabbits: general determinants of spatio-temporal variability in survival.

1. Identifying general patterns of how and why survival rates vary across space and time is necessary to truly understand population dynamics of a species. However, this is not an easy task given the complexity and interactions of processes involved, and the interpopulation differences in main survival determinants. 2. Here, using European rabbits (Oryctolagus cuniculus) as a model and information from local studies, we investigated whether we could make inferences about trends and drivers of survival of a species that are generalizable to large spatio-temporal scales. To do this, we first focused on overall survival and then examined cause-specific mortalities, mainly predation and diseases, which may lead to those patterns. 3. Our results show that within the large-scale variability in rabbit survival, there exist general patterns that are explained by the integration of factors previously known to be important at the local level (i.e. age, climate, diseases, predation or density dependence). We found that both inter- and intrastudy survival rates increased in magnitude and decreased in variability as rabbits grow old, although this tendency was less pronounced in populations with epidemic diseases. Some causes leading to these higher mortalities in young rabbits could be the stronger effect of rainfall at those ages, as well as, other death sources like malnutrition or infanticide. 4. Predation is also greater for newborns and juveniles, especially in population without diseases. Apart from the effect of diseases, predation patterns also depended on factors, such as, density, season, and type and density of predators. Finally, we observed that infectious diseases also showed general relationships with climate, breeding (i.e. new susceptible rabbits) and age, although the association type varied between myxomatosis and rabbit haemorrhagic disease. 5. In conclusion, large-scale patterns of spatio-temporal variability in rabbit survival emerge from the combination of different factors that interrelate both directly and through density dependence. This highlights the importance of performing more comprehensive studies to reveal combined effects and complex relationships that help us to better understand the mechanisms underlying population dynamics.

The paradox of the long-term positive effects of a North American crayfish on a European community of predators.

Invasions of non-native species are one of the major causes of losses of native species. In some cases, however, non-natives may also have positive effects on native species. We investigated the potential facilitative effects of the North American red swamp crayfish (Procambarus clarkii) on the community of predators in southwestern Spain. To do so, we examined the diets of predators in the area and their population trends since introduction of the crayfish. Most predator species consumed red swamp crayfish, which sometimes occurred in over 50% of their diet samples. Moreover, the abundance of species preying on crayfish increased significantly in the area as opposed to the abundance of herbivores and to predator populations in other areas of Europe, where those predators are even considered threatened. Thus, we report the first case in which one non-native species is both beneficial because it provides prey for threatened species and detrimental because it can drive species at lower trophic levels to extinction. Increases in predator numbers that are associated with non-native species of prey, especially when some of these predators are also invasive non-natives, may increase levels of predation on other species and produce cascading effects that threaten native biota at longer temporal and larger spatial scales. Future management plans should include the complexity of interactions between invasive non-natives and the entire native community, the feasibility of successful removal of non-native species, and the potential social and economic interests in the area.

Testing the threat-sensitive predator avoidance hypothesis: physiological responses and predator pressure in wild rabbits.

Predation is a strong selective force with both direct and indirect effects on an animal's fitness. In order to increase the chances of survival, animals have developed different antipredator strategies. However, these strategies have associated costs, so animals should assess their actual risk of predation and shape their antipredator effort accordingly. Under a stressful situation, such as the presence of predators, animals display a physiological stress response that might be proportional to the risk perceived. We tested this hypothesis in wild European rabbits (Oryctolagus cuniculus), subjected to different predator pressures, in Doñana National Park (Spain). We measured the concentrations of fecal corticosterone metabolites (FCM) in 20 rabbit populations. By means of track censuses we obtained indexes of mammalian predator presence for each rabbit population. Other factors that could modify the physiological stress response, such as breeding status, food availability and rabbit density, were also considered. Model selection based on information theory showed that predator pressure was the main factor triggering the glucocorticoid release and that the physiological stress response was positively correlated with the indexes of the presence of mammalian carnivore predators. Other factors, such as food availability and density of rabbits, were considerably less important. We conclude that rabbits are able to assess their actual risk of predation and show a threat-sensitive physiological response.