Behavioural diversity as a potential welfare indicator for professionally managed chimpanzees (Pan troglodytes): Exploring variations in calculating diversity using species-specific behaviours

Behavioural diversity may serve as a positive indicator of animal welfare that can be applied in long-term monitoring schemes in managed settings (eg zoos, laboratories, farms). Behavioural diversity is often higher when animals live in stimulating environments and experience positive events. Unfortunately, welfare researchers have not adopted consistent, standardised approaches to measuring behavioural diversity. The goal of this exploratory study was to utilise data from 41 adult chimpanzees (Pan troglodytes) housed across 16 zoological institutions to examine various models of Shannon's Diversity Index. Specifically, we investigated the impact of: combining versus splitting behaviours, including only positive behaviours, including human interaction, and considering recipient behaviours. We evaluate how the inclusion or exclusion of different behaviours impacts the relationship of behavioural diversity with: (i) concentrations of faecal glucocorticoid metabolites (GCM), a common indicator of adrenal activity; (ii) concentrations of immunoglobulin-A (IgA), an indicator of immune function and potential indicator of positive welfare; and (iii) stereotypic behaviour, a validated indicator of poor welfare. Most indices had significant negative relationships with faecal GCM. Animals that express a variety of behaviours from their species-typical repertoire have lower average faecal GCM concentrations and are likely experiencing better welfare. We did not find significant relationships between the behavioural diversity indices and IgA concentrations. Two indices were inversely associated with stereotypic behaviour. Our findings provide additional support for using Shannon's Diversity Index to calculate behavioural diversity as a robust, valid measure of positive welfare. However, future publications must justify the process for including or excluding behaviours from calculations.

The influence of the stereotypic forms of activity in mice behaviour in standard behavioural tests

Laboratory animals often develop abnormal repetitive (stereotypic) behaviour that can influence both physiology and behavioural test results. Such abnormal behaviours usually develop in suboptimal environment and increase over time. To explore the development of stereotypic forms of activity night home-cage behaviour of laboratory mice was analysed and collated with the behaviour in open field (OFT), hole-board (HBT) and tail suspension (TST) tests twice within 16 weeks. Mice expressed few stereotypies and their duration lessened over time from median 8.2 to 1.0 %. In contrast, grooming behaviour increased significantly from 29.5 to 49.6 %. Home-cage grooming correlated with the latency of locomotion start in OFT and with the immobility time in TST. Intensity and stability of stereotypic activity and grooming inf­luenced the duration of grooming in OFT: the mice with unstable stereotypies groomed more than others, and mice with the lowes home-cage grooming level also groomed in OFT the most. Intensity and stability of night grooming influenced the behaviour in TST: the mice with unstable level of grooming were the most mobile in this test. Abnormal home-cage activity may indicate impaired welfare, and that, in turn, may affect test activity, so researchers need to keep it in mind when planning animal behaviour experiments.

Nature calls: intelligence and natural foraging style predict poor welfare in captive parrots

Understanding why some species thrive in captivity, while others struggle to adjust, can suggest new ways to improve animal care. Approximately half of all Psittaciformes, a highly threatened order, live in zoos, breeding centres and private homes. Here, some species are prone to behavioural and reproductive problems that raise conservation and ethical concerns. To identify risk factors, we analysed data on hatching rates in breeding centres (115 species, 10 255 pairs) and stereotypic behaviour (SB) in private homes (50 species, 1378 individuals), using phylogenetic comparative methods (PCMs). Small captive population sizes predicted low hatch rates, potentially due to genetic bottlenecks, inbreeding and low availability of compatible mates. Species naturally reliant on diets requiring substantial handling were most prone to feather-damaging behaviours (e.g. self-plucking), indicating inadequacies in the composition or presentation of feed (often highly processed). Parrot species with relatively large brains were most prone to oral and whole-body SB: the first empirical evidence that intelligence can confer poor captive welfare. Together, results suggest that more naturalistic diets would improve welfare, and that intelligent psittacines need increased cognitive stimulation. These findings should help improve captive parrot care and inspire further PCM research to understand species differences in responses to captivity.

Development of an evidence-based welfare approach for cheetahs (Acinonyx jubatus) under human care

Societal concern for animals under human care has influenced our approaches to advance animal welfare in a variety of contexts. The Animal Programs Department at the Columbus Zoo and Aquarium sought partnership with the Center for Human-Animal Interactions Research & Education (CHAIRE) at The Ohio State University to develop a holistic welfare approach for the animals within their department using a focal species, the cheetah (Acinonyx jubatus). A one-year project using the Five Domains Animal Welfare Model collected data over six 60-day periods to evaluate long-term cortisol production and behavioural observations of cheetahs under changing environmental factors. Species and individual histories were incorporated with behavioural observations and hair cortisol production, giving a holistic view of welfare. Cortisol and behavioural data were analysed using linear models to compare cheetahs at population and individual levels. Participation in a cheetah run activity, housing occupancy, and 60-day period were found to influence all behaviours within the population and stereotypic behaviour also differed within individual cheetahs. No differences in hair cortisol concentrations were found for the group, but further analysis revealed differences within individuals throughout the study. No correlation of stereotypic behaviour and cortisol levels were found. This study created a welfare assessment protocol that can be used within zoological institutes and was the first to measure cortisol concentrations in hair in cheetahs.

Apathy

‘Auto-activation’ deficit, the most severe form of apathy, is a model to approach apathy. Auto-activation deficit consists of a severe reduction in self-initiated actions contrasting with the sparing of externally driven ones under strong solicitations and the presence of automatic (stereotypic) behaviour. This severe apathy can be viewed as the consequence of a quantitative reduction of goal-directed behaviour. Auto-activation deficit is due to lesions in the prefrontal cortex (PFC)–basal ganglia circuitry, the brain system that generates and controls goal-directed behaviour. In this chapter it is proposed that several different mechanisms may be responsible for apathy. Damage to three PFC–basal ganglia circuits may explain most of the cases of apathy: (i) lesions in the orbital and ventromedial PFC–basal ganglia circuit lead to apathy through difficulties in evaluating the affective value of a given behavioural context (‘amotivation’); (ii) lesions in the lateral PFC–basal ganglia circuit contribute to apathy via an inability to generate or activate strategies required to successfully complete a given programme of actions (‘cognitive inertia’); (iii) lesions to the anterior cingulate cortex–basal ganglia circuit (located in an intermediary anatomical position between the ventral and lateral circuit) may lead to apathy via an inability to transfer the affective value of a given context (‘invigoration deficit’); (iv) the summation or the synergy of damage to these three circuits within the basal ganglia may lead to a frank decrease in the amplification of signals representing goal-directed behaviour that reach the PFC (‘empty mind’); and (v) if all three circuits are structurally intact, apathy may nevertheless occur via alterations of neurotransmission systems that modulate the activity of these circuits (i.e. dopamine, serotonin, and acetylcholine).

Stereotypies in the Autism Spectrum Disorder: Can We Rely on an Ethological Model?

Background: Stereotypic behaviour can be defined as a clear behavioural pattern where a specific function or target cannot be identified, although it delays on time. Nonetheless, repetitive and stereotypical behaviours play a key role in both animal and human behaviour. Similar behaviours are observed across species, in typical human developmental phases, and in some neuropsychiatric conditions, such as Autism Spectrum Disorder (ASD) and Intellectual Disability. This evidence led to the spread of animal models of repetitive behaviours to better understand the neurobiological mechanisms underlying these dysfunctional behaviours and to gain better insight into their role and origin within ASD and other disorders. This, in turn, could lead to new treatments of those disorders in humans. Method: This paper maps the literature on repetitive behaviours in animal models of ASD, in order to improve understanding of stereotypies in persons with ASD in terms of characterization, pathophysiology, genomic and anatomical factors. Results: Literature mapping confirmed that phylogenic approach and animal models may help to improve understanding and differentiation of stereotypies in ASD. Some repetitive behaviours appear to be interconnected and mediated by common genomic and anatomical factors across species, mainly by alterations of basal ganglia circuitry. A new distinction between stereotypies and autotypies should be considered. Conclusions: Phylogenic approach and studies on animal models may support clinical issues related to stereotypies in persons with ASD and provide new insights in classification, pathogenesis, and management.

Onset rate and intensity of signs of organophosphate poisoning related to paraoxon dose and survival in rats

Introduction: Oganophosphorus compounds (OP) bind to acetylcholinesterase (AChE) and inactivate it. In the synaptic cleft, undestroyed and accumulated acetylcholine produce the acute cholinergic effects. The aim of this study was to determine the frequency, speed of onset and intensity of certain signs of paraoxon poisoning depending on dose and outcome of poisoning. Methods: The study was conducted in adult Wistar rats. The median lethal dose (LD50) of paraoxon as well as protective ratio (PR) of atropine (10 mg/kg intramuscularly) was determined. Clinical signs of poisoning were observed: fasciculations, tremor, seizures, ataxia, piloerection, lacrimation, exophthalmos, bizzare/stereotypic behaviour and dyspnoea. The time from paraoxon injection to the first appearance of the sign of poisoning was recorded as well as the intensity of poisoning with evaluation at 10 time intervals throughout the 4 h observational period. Results: The LD50 of paraoxon was 0.33 mg/kg (subcutaneously) and PR of atropine was 2.73. Dose-dependent, piloerection occurred more often (p = 0.009) and at higher intensity (p = 0.016) at higher doses. Fasciculations, tremor, seizures and ataxia occurred significantly earlier at higher doses of paraoxon (p = 0.015, 0.002, 0.021 and 0.016, respectively), as well as the intensity of seizure, tremor and fasciculation. Piloerection (p = 0.002) and seizures occurred more frequently (p = 0.009) in non-survivors. Fasciculations, tremor, seizures and ataxia occurred significantly earlier and at higher intensity in non-survivors (p < 0.001, for all parameters), as well as dyspnoea (p = 0.009 and p = 0.048). In atropine-protected rats, nicotinic effects persevered, so they were the prognostic parameter of the severity of the poisoning. Conclusion: Seizures and fasciculations followed by tremor were strong prognostic parameters of the probability of lethal outcome of paraoxon poisoning. Also, the mentioned poisoning signs were with their intensity and speed of occurrence in a clear positive correlation with the administered dose of paraoxon. Even at high doses of paraoxon, atropine blocked the muscarinic (but not nicotinic) effects and somewhat mitigated the CNS toxic effects.

Longitudinal Improvements in Zoo-Housed Elephant Welfare: A Case Study at ZSL Whipsnade Zoo

Over the last two decades, criticisms were raised regarding the welfare experienced by elephants in European and North American zoos. Concerns regarding the welfare of zoo-housed elephants in the UK and Europe were consolidated in the publication of several key reports, and media interest peaked. Throughout this study we aim to outline the behavioural measures of welfare observed in the current group of Asian elephants (Elephas maximus) at Zoological Society of London (ZSL) Whipsnade Zoo, using key welfare indicators for this species and comparing them to previous published work. Following the instigation of a species-specific research programme, empirical behavioural data were available to quantify any developments in care and welfare. The collection of behavioural information revealed that individuals in our study group engage in low levels of stereotypic behaviour, have formed and maintain strong associations with one another and display a high proportion of engagement in lying rest. We outline that by applying simple, low-cost methods of behavioural data collection and analysis, it is possible to collect evidence that allows us to evaluate individual level welfare. This facilitates the adoption of an evidence-based approach to zoo management as well as demonstrating compliance with updated legislation for this species.