Correction: 'The welfare problems of wide-ranging Carnivora reflect naturally itinerant lifestyles' (2023), by Bandeli et al.

[This corrects the article DOI: 10.1098/rsos.230437.][This corrects the article DOI: 10.1098/rsos.230437.].

The welfare problems of wide-ranging Carnivora reflect naturally itinerant lifestyles.

Carnivora with naturally small home ranges readily adjust to the evolutionarily new environment of captivity, but wider-ranging species seem prone to stress. Understanding why would advance both collection planning and enclosure design. We therefore investigated which aspects of wide-ranging lifestyles are key. We identified eight correlates of home range size (reflecting energetic needs, movement, intra-specific interactions, and itinerant lifestyles). We systematically assessed whether these correlates predict welfare better than range size per se, using data on captive juvenile mortality (from 13 518 individuals across 42 species) and stereotypic route-tracing (456 individuals, 27 species). Naturally itinerant lifestyles (quantified via ratios of daily to annual travel distances) were found to confer risk, predicting greater captive juvenile losses and stereotypic time-budgets. This finding advances our understanding of the evolutionary basis for welfare problems in captive Carnivora, helping explain why naturally sedentary species (e.g. American mink) may breed even in intensive farm conditions, while others (e.g. polar bears, giant pandas) can struggle even in modern zoos and conservation breeding centres. Naturally itinerant lifestyles involve decision-making, and strategic shifts between locations, suggesting that supplying more novelty, cognitive challenge and/or opportunities for control will be effective ways to meet these animals' welfare needs in captivity.

Don't use it? Don't lose it! Why active use is not required for stimuli, resources or "enrichments" to have welfare value.

Current frameworks for designing and evaluating good enclosures and "enrichments" typically focus on animals' active interactions with these features. This has undoubtedly improved the welfare of zoo-housed animals over the last 30 years or more. However, literature reviews from this same period identify persistent gaps in how such frameworks are applied: experiences and behaviors that do not rely on active interaction with stimuli or resources are largely ignored, when evaluating the welfare value of enclosures and enrichments within them. Here, we review research evidence demonstrating that active interaction is not always a reliable measure of welfare value, showing that items that elicit little or no interaction can nevertheless still reduce stress and improve well-being. This evidence largely comes from research on humans, lab animals and farm animals, but also from some zoo studies too. We then investigate why. We review psychology and ethology literatures to show that such welfare benefits can arise from five, non-mutually exclusive, processes or mechanisms that are well-understood in humans and domestic animals: (1) some motivations are sated quickly by interaction with resources, yet still have large welfare benefits; (2) active interaction may just be a way to achieve a goal or solve a problem, without being beneficial for welfare in itself; (3) having opportunities for choice and control may be inherently beneficial, even when not acted on; (4) some enclosure features meet social needs for structure, landmarks, and blocked sightlines; and (5) some stimuli may be preferred because they signaled good environments to an animal's ancestors. We use this information to identify  improved ways of enhancing and assessing zoo animal welfare. Incorporating these concepts should expand the scope of behaviors and subjective experiences that are targeted, to now include those that involve little active interaction and yet still are important for good welfare.

Conventional laboratory housing increases morbidity and mortality in research rodents: results of a meta-analysis.

BACKGROUND: Over 120 million mice and rats are used annually in research, conventionally housed in shoebox-sized cages that restrict natural behaviours (e.g. nesting and burrowing). This can reduce physical fitness, impair thermoregulation and reduce welfare (e.g. inducing abnormal stereotypic behaviours). In humans, chronic stress has biological costs, increasing disease risks and potentially shortening life. Using a pre-registered protocol ( https://atrium.lib.uoguelph.ca/xmlui/handle/10214/17955 ), this meta-analysis therefore tested the hypothesis that, compared to rodents in 'enriched' housing that better meets their needs, conventional housing increases stress-related morbidity and all-cause mortality. RESULTS: Comprehensive searches (via Ovid, CABI, Web of Science, Proquest and SCOPUS on May 24 2020) yielded 10,094 publications. Screening for inclusion criteria (published in English, using mice or rats and providing 'enrichments' in long-term housing) yielded 214 studies (within 165 articles, using 6495 animals: 59.1% mice; 68.2% male; 31.8% isolation-housed), and data on all-cause mortality plus five experimentally induced stress-sensitive diseases: anxiety, cancer, cardiovascular disease, depression and stroke. The Systematic Review Center for Laboratory animal Experimentation (SYRCLE) tool assessed individual studies' risks of bias. Random-effects meta-analyses supported the hypothesis: conventional housing significantly exacerbated disease severity with medium to large effect sizes: cancer (SMD = 0.71, 95% CI = 0.54-0.88); cardiovascular disease (SMD = 0.72, 95% CI = 0.35-1.09); stroke (SMD = 0.87, 95% CI = 0.59-1.15); signs of anxiety (SMD = 0.91, 95% CI = 0.56-1.25); signs of depression (SMD = 1.24, 95% CI = 0.98-1.49). It also increased mortality rates (hazard ratio = 1.48, 95% CI = 1.25-1.74; relative median survival = 0.91, 95% CI = 0.89-0.94). Meta-regressions indicated that such housing effects were ubiquitous across species and sexes, but could not identify the most impactful improvements to conventional housing. Data variability (assessed via coefficient of variation) was also not increased by 'enriched' housing. CONCLUSIONS: Conventional housing appears sufficiently distressing to compromise rodent health, raising ethical concerns. Results also add to previous work to show that research rodents are typically CRAMPED (cold, rotund, abnormal, male-biased, poorly surviving, enclosed and distressed), raising questions about the validity and generalisability of the data they generate. This research was funded by NSERC, Canada.

Social Buffering as a Tool for Improving Rodent Welfare.

The presence of a conspecific can be calming to some species of animal during stress, a phenomenon known as social buffering. For rodents, social buffering can reduce the perception of and reaction to aversive experiences. With a companion, animals may be less frightened in conditioned fear paradigms, experience faster wound healing, show reduced corticosterone responses to novelty, and become more resilient to everyday stressors like cage-cleaning. Social buffering works in diverse ways across species and life stages. For example, social buffering may rely on specific bonds and interactions between individuals, whereas in other cases, the mere presence of conspecific cues may reduce isolation stress. Social buffering has diverse practical applications for enhancing rodent wellbeing (some of which can be immediately applied, while others need further development via welfare-oriented research). Appropriate social housing will generally increase rodents' abilities to cope with challenges, with affiliative cage mates being the most effective buffers. Thus, when rodents are scheduled to experience distressing research procedures, ensuring that their home lives supply high degrees of affiliative, low stress social contact can be an effective refinement. Furthermore, social buffering research illustrates the stress of acute isolation: stressors experienced outside the cage may thus be less impactful if a companion is present. If a companion cannot be provided for subjects exposed to out-of-cage stressors, odors from unstressed animals can help ameliorate stress, as can proxies such as pieces of synthetic fur. Finally, in cases involving conditioned fear (the learned expectation of harm), newly providing social contact during exposure to negative conditioned stimuli (CS) can modify the CS such that for research rodents repeatedly exposed to aversive stimuli, adding conspecific contact can reduce their conditioned fear. Ultimately, these benefits of social buffering should inspire the use of creative techniques to reduce the impact of stressful procedures on laboratory rodents, so enhancing their welfare.

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.

Large Lemurs: Ecological, Demographic and Environmental Risk Factors for Weight Gain in Captivity.

Excessive body mass, i.e., being overweight or obese, is a health concern associated with issues such as reduced fertility and lifespan. Some lemur species are prone to extreme weight gain in captivity, yet others are not. To better understand species- and individual-level effects on susceptibility to captive weight gain, we use two complementary methods: phylogenetic comparative methods to examine ecological explanations for susceptibility to weight gain across species, and epidemiological approaches to examine demographic and environment effects within species. Data on body masses and living conditions were collected using a survey, yielding useable data on 675 lemurs representing 13 species from 96 collections worldwide. Data on species-typical wild ecology for comparative analyses came from published literature and climate databases. We uncovered one potential ecological risk factor: species adapted to greater wild food resource unpredictability tended to be more prone to weight gain. Our epidemiological analyses on the four best-sampled species revealed four demographic and one environmental risk factors, e.g., for males, being housed with only fixed climbing structures. We make practical recommendations to help address weight concerns, and describe future research including ways to validate the proxy we used to infer body condition.

Getting a grip: cats respond negatively to scruffing and clips.

Use of scruffing and scruffing tools (eg, clipnosis clips) to immobilise cats is contentious, and cat handling guidelines vary in recommendations regarding these techniques. The current study examined whether cats show negative responses to the following restraint methods: (1) scruff (n=17), (2) clip application to the dorsal neck skin (n=16) and (3) full body (a known negative; n=19). Each cat was also handled with passive restraint (control) for comparison. During handling, cats were examined for behavioural (side/back ear positions, vocalisations, lip licking) and physiological (pupil dilation ratio, respiratory rate) responses. Full-body restrained cats showed more negative responses than passively restrained cats (respiratory rate: p=0.006, F3,37=4.31, p=0.01; ear p=0.002, F3,49=6.70, p=0.0007; pupil: p=0.007, F3,95=14.24, p=0.004; vocalisations: p=0.009, F3,49=4.85, p=0.005) and scruff-restrained cats (pupil: p=0.009; vocalisations: p=0.04). Clip restraint resulted in more negative responses than passive (pupil: p=0.01; vocalisations: p=0.007, ear p=0.02) and scruff restraint (pupil p=0.01; vocalisations: p=0.02). No differences were detected between full-body restraint, known to be aversive, and clip restraint. Full-body restraint and clip restraint resulted in the greatest number of negative responses, scruffing resulted in fewer negative responses and passive restraint showed the least number of responses. We therefore recommend against the use of full-body and clip restraint, and suggest that scruff restraint should be avoided when possible.

The effects of preferred natural stimuli on humans' affective states, physiological stress and mental health, and the potential implications for well-being in captive animals.

Exposure to certain natural stimuli improves people's moods, reduces stress, enhances stress resilience, and promotes mental and physical health. Laboratory studies and real estate prices also reveal that humans prefer environments containing a broad range of natural stimuli. Potential mediators of these outcomes include: 1) therapeutic effects of specific natural products; 2) positive affective responses to stimuli that signalled safety and resources to our evolutionary ancestors; 3) attraction to environments that satisfy innate needs to explore and understand; and 4) ease of sensory processing, due to the stimuli's "evolutionary familiarity" and/or their fractal, self-repeating properties. These processes, and the benefits humans gain from natural stimuli, seem to be largely innate. They thus have strong implications for other species (including laboratory, farm and zoo animals living in environments devoid of natural stimuli), suggesting that they too may have nature-related "sensory needs". By promoting positive affect and stress resilience, preferred natural stimuli (including views, sounds and odours) could therefore potentially provide effective and efficient ways to improve captive animal well-being.

The Days and Nights of Zoo Elephants: Using Epidemiology to Better Understand Stereotypic Behavior of African Elephants (Loxodonta africana) and Asian Elephants (Elephas maximus) in North American Zoos.

Stereotypic behavior is an important indicator of compromised welfare. Zoo elephants are documented to perform stereotypic behavior, but the factors that contribute to performance have not been systematically assessed. We collected behavioral data on 89 elephants (47 African [Loxodonta africana], 42 Asian [Elephas maximus]) at 39 North American zoos during the summer and winter. Elephants were videoed for a median of 12 daytime hours per season. A subset of 32 elephants (19 African, 13 Asian) was also observed live for a median of 10.5 nighttime hours. Percentages of visible behavior scans were calculated from five minute instantaneous samples. Stereotypic behavior was the second most commonly performed behavior (after feeding), making up 15.5% of observations during the daytime and 24.8% at nighttime. Negative binomial regression models fitted with generalized estimating equations were used to determine which social, housing, management, life history, and demographic variables were associated with daytime and nighttime stereotypic behavior rates. Species was a significant risk factor in both models, with Asian elephants at greater risk (daytime: p<0.001, Risk Ratio = 4.087; nighttime: p<0.001, Risk Ratio = 8.015). For both species, spending time housed separately (p<0.001, Risk Ratio = 1.009), and having experienced inter-zoo transfers (p<0.001, Risk Ratio = 1.175), increased the risk of performing higher rates of stereotypy during the day, while spending more time with juvenile elephants (p<0.001, Risk Ratio = 0.985), and engaging with zoo staff reduced this risk (p = 0.018, Risk Ratio = 0.988). At night, spending more time in environments with both indoor and outdoor areas (p = 0.013, Risk Ratio = 0.987) and in larger social groups (p = 0.039, Risk Ratio = 0.752) corresponded with reduced risk of performing higher rates of stereotypy, while having experienced inter-zoo transfers (p = 0.033, Risk Ratio = 1.115) increased this risk. Overall, our results indicate that factors related to the social environment are most influential in predicting elephant stereotypic behavior rates.

Play in juvenile mink: litter effects, stability over time, and motivational heterogeneity.

Mink are potentially ideal for investigating the functions of play: deleterious effects of early social isolation suggest a crucial developmental role for play; and huge numbers of highly playful juvenile subjects can be studied on farms. We collected descriptive data on 186 pairs from 93 litters, half provided with play-eliciting environmental enrichment objects in their home cages, to test three hypotheses: (1) play frequency is subject to litter effects; (2) relative playfulness is stable over time; (3) play sub-types share a single, common motivational basis. We found weak litter effects that were driven by stronger litter effects on general activity, and weakly stable individual differences in both total and rough-and-tumble play. Experimentally increasing object play did not inhibit rough-and-tumble play, showing these sub-types are not motivational substitutes. Frequencies of these sub-types were also uncorrelated, and changed differently with time of day and age, further supporting this conclusion.

Cage-induced stereotypic behaviour in laboratory mice covaries with nucleus accumbens FosB/ΔFosB expression.

Stereotypic behaviour (SB) occurs in certain human disorders (e.g. autism), and animals treated with stimulants or raised in impoverished conditions, including laboratory mice in standard cages. Dysfunctional cortico-basal ganglia pathways have been implicated in these examples, but for cage-induced forms of SB, the relative roles of ventral versus dorsal striatum had not been fully ascertained. Here, we used immunohistochemical staining of FosB and ΔFosB to assess long-term activation within the nucleus accumbens and caudate-putamen of C57BL/6 mice. Housed in typical laboratory cages, these mice spontaneously developed different degrees of route-tracing, bar-mouthing and other forms of SB (spending 0% to over 50% of their active time budgets in this behaviour). The most highly stereotypic mice showed the most elevated FosB/ΔFosB activity in the nucleus accumbens. No such patterns occurred in the caudate-putamen. The cage-induced SB common in standard-housed mice thus involves elevated activity within the ventral striatum, suggesting an aetiology closer to compulsive gambling, eating and drug-seeking than to classic amphetamine stereotypies and other behaviours induced by motor loop over-activation.

Benefits of a ball and chain: simple environmental enrichments improve welfare and reproductive success in farmed American mink (Neovison vison).

Can simple enrichments enhance caged mink welfare? Pilot data from 756 sub-adults spanning three colour-types (strains) identified potentially practical enrichments, and suggested beneficial effects on temperament and fur-chewing. Our main experiment started with 2032 Black mink on three farms: from each of 508 families, one juvenile male-female pair was enriched (E) with two balls and a hanging plastic chain or length of hose, while a second pair was left as a non-enriched (NE) control. At 8 months, more than half the subjects were killed for pelts, and 302 new females were recruited (half enriched: 'late E'). Several signs of improved welfare or productivity emerged. Access to enrichment increased play in juveniles. E mink were calmer (less aggressive in temperament tests; quieter when handled; less fearful, if male), and less likely to fur-chew, although other stereotypic behaviours were not reduced. On one farm, E females had lower cortisol (inferred from faecal metabolites). E males tended to copulate for longer. E females also weaned more offspring: about 10% more juveniles per E female, primarily caused by reduced rates of barrenness ('late E' females also giving birth to bigger litters on one farm), effects that our data cautiously suggest were partly mediated by reduced inactivity and changes in temperament. Pelt quality seemed unaffected, but E animals had cleaner cages. In a subsidiary side-study using 368 mink of a second colour-type ('Demis'), similar temperament effects emerged, and while E did not reduce fur-chewing or improve reproductive success in this colour-type, E animals were judged to have better pelts. Overall, simple enrichments were thus beneficial. These findings should encourage welfare improvements on fur farms (which house 60-70 million mink p.a.) and in breeding centres where endangered mustelids (e.g. black-footed ferrets) often reproduce poorly. They should also stimulate future research into more effective practical enrichments.

Winning the genetic lottery: biasing birth sex ratio results in more grandchildren.

Population dynamics predicts that on average parents should invest equally in male and female offspring; similarly, the physiology of mammalian sex determination is supposedly stochastic, producing equal numbers of sons and daughters. However, a high quality parent can maximize fitness by biasing their birth sex ratio (SR) to the sex with the greatest potential to disproportionately outperform peers. All SR manipulation theories share a fundamental prediction: grandparents who bias birth SR should produce more grandoffspring via the favored sex. The celebrated examples of biased birth SRs in nature consistent with SR manipulation theories provide compelling circumstantial evidence. However, this prediction has never been directly tested in mammals, primarily because the complete three-generation pedigrees needed to test whether individual favored offspring produce more grandoffspring for the biasing grandparent are essentially impossible to obtain in nature. Three-generation pedigrees were constructed using 90 years of captive breeding records from 198 mammalian species. Male and female grandparents consistently biased their birth SR toward the sex that maximized second-generation success. The most strongly male-biased granddams and grandsires produced respectively 29% and 25% more grandoffspring than non-skewing conspecifics. The sons of the most male-biasing granddams were 2.7 times as fecund as those of granddams with a 50∶50 bias (similar results are seen in grandsires). Daughters of the strongest female-biasing granddams were 1.2 times as fecund as those of non-biasing females (this effect is not seen in grandsires). To our knowledge, these results are the first formal test of the hypothesis that birth SR manipulation is adaptive in mammals in terms of grandchildren produced, showing that SR manipulation can explain biased birth SR in general across mammalian species. These findings also have practical implications: parental control of birth SR has the potential to accelerate genetic loss and risk of extinction within captive populations of endangered species.

Environmentally enriched rearing environments reduce repetitive perseveration in caged mink, but increase spontaneous alternation.

Studies spanning 15 species (including American mink, Neovison vison) demonstrate that within similarly-housed populations, individuals displaying high levels of stereotypic behaviour (SB) typically show perseverative responding (e.g. during set-shifting, or reversal/extinction learning). Similar correlations in autism and schizophrenia suggest this indicates captivity-induced cortico-striatal circuit dysfunction. However, this pattern does not prove developmental impairment: SB, perseveration and their inter-correlations also occur in normal humans. We therefore differentially-reared enriched versus non-enriched mink to investigate whether treatments that exacerbate SB correspondingly increase perseveration (Study 1). Enriched-rearing did reduce SB and perseverative response repetition (in two-choice guessing tasks), while increasing spontaneous alternation: a strategy yielding more rewards, and suggesting enhanced hippocampal development. This complements previous research demonstrating cortical/hippocampal impairments and reduced behavioural flexibility in non-enriched animals, with implications for research animals and wild animals captive-raised for reintroduction into nature. Consistent with previous data, highly stereotypic subjects repeated guessing task responses most rapidly, suggesting disinhibition during repetition. However, unexpectedly, SB and perseveration did not co-vary across individuals. We therefore suggest that behavioural changes manifest as increased perseveration are important but do not fully explain captive animals' SBs, possible reasons including the contributory role of differential motivations for underlying source behaviours. Re-analyses of old data (Study 2) confirmed that spontaneous alternation is profitable; and demonstrated that the precise methods used for quantifying perseveration and SB can modify the strength of apparent relationships between them, as can statistically controlling for feeding motivation: as predicted, partialling out motivational effects increased the variance in SB predicted by perseveration.

Environmental enrichment reduces signs of boredom in caged mink.

Animals housed in impoverished cages are often labelled 'bored'. They have also been called 'apathetic' or 'depressed', particularly when profoundly inactive. However, these terms are rarely operationally defined and validated. As a negative state caused by under-stimulation, boredom should increase interest in stimuli of all kinds. Apathy (lack of interest), by contrast, should manifest as decreased interest in all stimuli, while anhedonia (loss of pleasure, a depressive symptom) should specifically decrease interest in normally rewarding stimuli. We tested the hypotheses that mink, a model carnivore, experience more boredom, depression-like apathy, or anhedonia in non-enriched (NE) cages than in complex, enriched (E) cages. We exposed 29 subjects (13 E, 16 NE) to ten stimuli categorized a priori as aversive (e.g. air puffs), rewarding (e.g. evoking chasing) or ambiguous/neutral (e.g. candles). Interest in stimuli was assessed via latencies to contact, contact durations, and durations oriented to stimuli. NE mink contacted all stimuli faster (P = 0.003) than E mink, and spent longer oriented to/in contact with them, albeit only significantly so for ambiguous ones (treatment*type P<0.013). With stimulus category removed from statistical models, interest in all stimuli was consistently higher among NE mink (P<0.0001 for all measures). NE mink also consumed more food rewards (P = 0.037). Finally, we investigated whether lying down while awake and stereotypic behaviour (both increased by NE housing) predicted these responses. Lying awake positively co-varied with certain measures of increased exploration. In contrast, stereotypic 'scrabbling' or locomotion (e.g. pacing) did not. Overall, NE mink showed no evidence of apathy or depression, but instead a heightened investigation of diverse stimuli consistent with boredom. This state was potentially indicated by spending much time lying still but awake (although this result requires replication). Boredom can thus be operationalized and assessed empirically in non-human animals. It can also be reduced by environmental enrichment.

Recurrent perseveration correlates with abnormal repetitive locomotion in adult mink but is not reduced by environmental enrichment.

We analysed the relationship between abnormal repetitive behaviour (ARB), the presence/absence of environmental enrichment, and two types of behavioural disinhibition in farmed American mink, Neovison vison. The first type, recurrent perseveration, the inappropriate repetition of already completed responses, was assessed using three indices of excessive response repetition and patterning in a bias-corrected serial two-choice guessing task. The second type, disinhibition of prepotent responses to reward cues, a form of impulsivity, was tested in a locomotive detour task adapted from primate reaching tasks: subjects were required to walk around, rather than directly into, a transparent barrier behind which food was visible. In older adult females, recurrent perseveration positively predicted pre-feeding abnormal repetitive locomotion (ARL) in Non-enriched housing. High-ARL subjects also performed repeated (same-choice) responses more rapidly than low-ARL animals, even when statistically controlling for alternated (different-choice) response latency. Mink performed much less ARL following transfer to Enriched housing, but there was no corresponding change in recurrent perseveration. Thus, elevated recurrent perseveration is not sufficient for frequent ARL; and while captive environments do determine ARL frequency, in mink, they do not necessarily do so by modifying levels of perseveration. Disinhibition of prepotent responses to reward cues, meanwhile, did not predict ARL. In a separate sample of differentially housed young adults, neither type of behavioural disinhibition predicted ARL, and again, whether or not housing was enriched did not affect behavioural disinhibition despite affecting ARL. Thus, the relationship between recurrent perseveration and ARB may only develop with age; longitudinal studies are now required for confirmation.