Passerine birds are important models in fundamental biological research, with as many as 300,000 individuals used in laboratory experiments worldwide annually. However, because the use of passerines is rare compared with that of more conventional laboratory animals, there is often a lack of information about the basic biology and husbandry requirements of these species. We aim to address this deficit by providing an overview of the most salient aspects of passerine biology and their implications for laboratory husbandry and welfare. We start by describing the characteristics that make these birds useful and interesting research subjects. Specifically, we highlight features (e.g., birdsong) of passerine biology that differentiate these birds from more common laboratory animals. Next, we consider the implications of passerine biology for husbandry in the laboratory. Many of the aspects of passerine biology that make these species valuable to scientists are also likely to be affected by environmental variables; a good knowledge of these variables is necessary in order to choose appropriate laboratory conditions for passerines. We outline how the developmental history of the birds and choices of caging, feeding, and environmental regimes might influence their physiology and behavior and thus affect both the welfare of the birds and the quality of the resulting data. We stress the importance of a sound understanding of the biology of any species to ensure good welfare and good science.

/pdf/the-use-of-passerine-bird-species-in-laboratory-research-59dulsl38b.pdf

The use of passerine bird species in laboratory research: implications of basic biology for husbandry and welfare.

Our understanding of fundamental organismal biology has been disproportionately influenced by studies of a relatively small number of ‘model’ species extensively studied in captivity. Laboratory populations of model species are commonly subject to a number of forms of past and current selection that may affect experimental outcomes. Here, we examine these processes and their outcomes in one of the most widely used vertebrate species in the laboratory – the zebra finch (Taeniopygia guttata). This important model species is used for research across a broad range of fields, partly due to the ease with which it can be bred in captivity. However despite this perceived amenability, we demonstrate extensive variation in the success with which different laboratories and studies bred their subjects, and overall only 64% of all females that were given the opportunity, bred successfully in the laboratory. We identify and review several environmental, husbandry, life-history and behavioural factors that potentially contribute to this variation. The variation in reproductive success across individuals could lead to biases in experimental outcomes and drive some of the heterogeneity in research outcomes across studies. The zebra finch remains an excellent captive animal system and our aim is to sharpen the insight that future studies of this species can provide, both to our understanding of this species and also with respect to the reproduction of captive animals more widely. We hope to improve systematic reporting methods and that further investigation of the issues we raise will lead both to advances in our fundamental understanding of avian reproduction as well as to improvements in future welfare and experimental efficiency.

/pdf/variation-in-reproductive-success-across-captive-populations-rd31j51ppw.pdf

Variation in reproductive success across captive populations: Methodological differences, potential biases and opportunities

The vertebrate stress response has been shown to suppress investment in reproductive and immune function and may also lead to a reduced investment in the production of secondary sexual traits. However, it has been difficult to model roles of stress in sexual selection due to the inconsistent results seen in empirical studies testing for the effect of stress on the expression of secondary sexual traits. We conducted a phylogenetically controlled meta-analysis of published associations between physiological correlates of stress and sexual signaling in vertebrates in order to identify any consistent patterns. Our analysis included signaling in both males and females, 4 stress measures, and 4 categories of sexually selected traits (vocalizations, traits that varied in size, traits that varied in coloration, and opposite-sex preference). Across 38 studies of 26 species, there was no significant relationship between physiological correlates of stress and the expression of sexual signals. Mean effect size, however, varied significantly across the 4 types of sexually selected trait. We propose development of a model that incorporates the nuanced effects of species ecology, trait type, ecological context, and the complex nature of the physiological stress response, on the expression of sexually selected traits.

Stress and sexual signaling: a systematic review and meta-analysis

Many breeding programs managed by the Association of Zoos and Aquariums' (AZA) Species Survival Plans® (SSPs) are not meeting goals for population size and genetic diversity due to failure of recommended pairs to breed successfully. According to AZA Population Management Center analyses, as many as 80% of recommended breeding pairs fail to produce young before the next breeding and transfer plan is issued. Determining reasons for failure and ensuring that a specific pairing produces offspring can be challenging. Mate incompatibility, one possible reason for failure, might be addressed by allowing mate choice. Although many SSP® coordinators and breeding managers, who implement breeding recommendations at their institutions, recognize the potential benefits of mate choice, examples and models for presenting and assessing choice are lacking. Here we review examples from birds, rodents, lagomorphs, marsupials, carnivores, fishes, and insects where mate choice has been incorporated. These examples provide strong evidence that free mate choice and mating with preferred partners increase a variety of reproductive success measurements when compared to assigned mate pairings. We suggest innovative housing and breeding arrangements for better incorporating mate choice into the management strategies for species held ex situ. Further, we discuss the fitness consequences and welfare implications of allowing choice. We advocate for a more systematic use of behavioral research in cooperative breeding programs. Behavioral management for mating can yield more successful programs, thus ensuring SSP® genetic and demographic goals are met, while simultaneously improving welfare.

https://onlinelibrary.wiley.com/doi/pdf/10.1002/zoo.21450

Improving the sustainability of ex situ populations with mate choice.

Animals perceiving repeated aversive events can become chronically stressed. Chronic activation of the hypothalamic-pituitary-adrenal (HPA) axis can have deleterious consequences on physiological parameters (e.g. BW, blood chemistry) and behaviour (e.g. emotional reactivity, stereotypies, cognition). Environmental enrichment (EE) can be a mean to reduce animal stress and to improve welfare. The aim of this study was first, to assess the effects of EE in battery cages on the behaviour of young Japanese quail and second, to evaluate the impact of EE on quail exposed to chronic stress. The experiment involved quail housed in EE cages and submitted or not to a chronic stress procedure (CSP) (EE cages, control quail: n=16, CSP quail: n=14) and quail housed in standard cages and exposed or not to the CSP (standard non-EE cages, control quail: n=12, CSP quail: n=16). Our procedure consisted of repeated aversive events (e.g. ventilators, delaying access to food, physical restraint, noise) presented two to five times per 24 h, randomly, for 15 days. During CSP, EE improved quail's welfare as their stereotypic pacing decreased and they rested more. CSP decreased exploration in all quail. After the end of CSP, quail presented increased emotional reactivity in emergence test. However, the effect of EE varied with test. Finally, chronic stress effects on comfort behaviours in the emergence test were alleviated by EE. These results indicate that EE can alleviate some aspects of behavioural alterations induced by CSP.

Environmental enrichment reduces behavioural alterations induced by chronic stress in Japanese quail.

Much attention has been focused, quite rightly, on the welfare of laboratory rodents and farm animals but certain other groups have been less well represented in welfare research. Small birds, for example, are often kept as pets and used in a wide variety of behavioural and physiological experiments where 'best' housing conditions are based on advice from experienced keepers as opposed to being tested experimentally. We investigated the effects of two husbandry conditions on the welfare of captive zebra finches: (a) optional cover and (b) rewarded handling versus random rewards. As a correlate of welfare in the four conditions (cover+reward, cover, reward, nothing), we recorded the time to settle and perform normal behaviours after an experimenter entered the room throughout the study (ie habituation to disturbance). In addition, we measured female preference for males in the four conditions to see whether welfare situation affected attractiveness as a mate. Birds in the two conditions where a reward was provided settled most quickly; and their settling time decreased across the study. Birds provided with cover alone became more disturbed by the entry of the experimenter as the study progressed. However, the birds taking longest on average to settle were those in cages with no cover and no reward. Females preferred males in the reward conditions as mates, either due to the fact that these males settled more quickly or because less-stressed males are more attractive in some other way. Thus, rewarding birds after disturbance is an effective and simple way to improve habituation to handling and human presence. In addition, these birds are more attractive to females, implying that males more habituated to captivity may be preferred as mates. Provision of cover may help under certain circumstances, but appears paradoxically to lead to increased fearfulness over time under the conditions studied here.

J. A. Archer

Papers

Welfare and mate choice in zebra finches: effect of handling regime and presence of cover