Wild carnivores in zoos, conservation breeding centres, and farms commonly live in relatively small, unstimulating enclosures. Under these captive conditions, in a range of species including giant pandas, black-footed ferrets, and European mink, male reproductive abilities are often poor. Such problems have long been hypothesized to be caused by these animals' housing conditions. We show for the first time that rearing under welfare-improving (i.e., highly valued and stress-reducing) environmental enrichments enhances male carnivores' copulatory performance: in mate choice competitions, enriched male American mink (Neovison vison) mated more often than non-enriched males. We screened for several potential mediators of this effect. First was physiological stress and its impact on reproductive physiology; second, stress-mediated changes in morphology and variables related to immunocompetence that could influence male attractiveness; and third, behavioural changes likely to affect social competence, particularly autistic-like excessive routine and repetition (‘perseveration’) as is reflected in the stereotypies common in captive animals. Consistent with physiological stress, excreted steroid metabolites revealed that non-enriched males had higher cortisol levels and lower androgen levels than enriched conspecifics. Their os penises (bacula) also tended to be less developed. Consistent with reduced attractiveness, non-enriched males were lighter, with comparatively small spleens and a trend to greater fluctuating asymmetry. Consistent with impaired social competence, non-enriched males performed more stereotypic behaviour (e.g., pacing) in their home cages. Of all these effects, the only significant predictor of copulation number was stereotypy (a trend suggesting that low bodyweights may also be influential): highly stereotypic males gained the fewest copulations. The neurophysiological changes underlying stereotypy thus handicap males sexually. We hypothesise that such males are abnormally perseverative when interacting with females. Investigating similar problems in other taxa would be worthwhile, since many vertebrates, wild and domestic, live in conditions that cause stereotypic behaviour and/or impair neurological development.
a b s t r a c tWe 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 biascorrected 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.
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.
Effects of sub-optimal housing on inactivity vary across species and experiments, probably because inactivity is heterogeneous, reflecting both positive states (e.g. relaxation) and negative ones (e.g. fear). We therefore aimed to identify specific subtypes of inactivity that could indicate poor welfare in mink, by comparing their behaviour in enriched and non-enriched conditions (the former having been previously demonstrated to be highly preferred by mink and to enhance their welfare). We assessed this in three groups of subjects, as well as after housing conditions were reversed for the last group. During live scans, inactive animals were scored for posture, location, and whether awake or apparently asleep. Data on temperament and physiological stress indicators were also collected for one group; these confirmed that non-enriched housing increased faecal cortisol metabolites (FCM; P=0.040). Non-enriched housing also increased locomotor stereotypy in females (sex*housing: P=0.004). Inactivity in the nest-box (vs. in the open cage) was higher among females in non-enriched housing (housing*sex P<0.001), and increased by 20% of observations after enrichment removal (P=0.018) for both sexes. Furthermore, males with fearful temperaments spent the most time inactive in the nest-box (sex*temperament P=0.054), while females whose FCM decreased most when given enrichment also showed the largest decreases in this behaviour (sex*FCM change P=0.019). Together, this suggests that inactivity in the nest-box may reflect anxiety-induced hiding. Lying awake (i.e. prone with eyes open) was also higher in non-enriched housing (3.1% of observations vs. 1.7%; P=0.002); furthermore, this subtype of inactivity increased after enrichment removal (by 1.0% of observations; P=0.021), and decreased when non-enriched mink were given enrichment (by 2.4% of observations; P=0.004). This behaviour did not co-vary with fearfulness, however, nor with FCM (both P>0.05). This suggests that lying awake is not fear-related (e.g. not reflecting enhanced vigilance) but instead reflects some other negative state. Effects on inactivity subtypes as defined by posture were less consistent. For example, time spent lying belly down tended to decrease in mink moved from non-enriched to enriched cages (P=0.054), but enriched mink spent significantly less time belly down (in one of the three groups; P=0.002). Overall, two subtypes of inactivity, lying in the nestbox and lying awake seem likely to be valid indicators of housing-induced poor welfare in this species, being consistently increased by non-enriched cages. Lying in the nest-box may indicate fear or anxiety, and lying awake, a boredom-like state.
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.
Animal welfare science is a young and thriving field. Over the last two decades, the output of scientific publications on welfare has increased by c. 10-15% annually (tripling as a proportion of all science papers logged by ISI’s Web of Science), with just under half the c. 8500 total being published in the last 4 years. These papers span an incredible 500+ journals, but around three quarters have been in 80 animal science, veterinary, ethology, conservation and specialized welfare publications, and nearly 25% are published in just two: Animal Welfare and Applied Animal Behaviour Science. Farmed animals – especially mammals – have attracted by far the most research. This broadly reflects the vastness of their populations and the degree of public concern they elicit; poultry, however, are under-studied, and farmed fish ever more so: fish have only recently attracted welfare research, and are by far the least studied of all agricultural species, perhaps because of ongoing doubts about their sentience. We predict this farm animal focus will continue in the future, but embracing more farmed fish, reptiles and invertebrates, and placing its findings within broader international contexts such as environmental and food security concerns. Laboratory animals have been consistently well studied, with a shift in recent years away from primates and towards rodents. Pets, the second largest animal sector after farmed animals, have in contrast been little studied considering their huge populations (cats being especially overlooked): we anticipate research on them increasing in the future. Captive wild animals, especially mammals, have attracted a consistent level of welfare research over the last two decades. Given the many thousands of diverse species kept by zoos, this must, and we predict will, increase. Future challenges and opportunities including refining the use of preference tests, stereotypic behaviour, corticosteroid outputs and putative indicators of positive affect, to enable more valid conclusions about welfare; investigating the evolution and functions of affective states; and last but not least, identifying which taxonomic groups and stages of development are actually sentient and so worthy of welfare concern.
Ferrets (Mustela putorius furo) are kept and used in multiple sectors of society, but little is known about how they are housed and what environmental enrichment (EE) they may benefit from. We aimed to help guide caretakers about what housing and EE can be provided for ferrets. Through an online questionnaire of ferret caretakers, including pet, laboratory, zoological collection, rescue and working animal sectors internationally, we described ferret housing, opportunities for exploration, EE provision and caretaker opinions on ferrets’ preferred EE types, and problematic EE. In total, 754 valid responses from 17 countries were analysed, with most (82.4%) coming from pet owners. Most ferrets were housed socially, with housing varying across sectors from single-level cages to free-range housing in a room or outdoor enclosure; pet owners mostly used multi-level cages. The most commonly reported EE included hammocks, tunnels and tactile interaction with caretakers. Respondents reported that ferrets particularly enjoyed digging substrates, tunnels, human interaction and exploration. The most frequently reported problems were that ingestion of unsuitable chew toys and rubber items could cause internal blockages, narrow tunnels could trap ferrets, and certain fabrics that could catch claws. This suggests a need for increased awareness of the risks of these EE types and for more commercially available safety-tested ferret EE. Scent trails were relatively rarely provided but were reported to be enjoyed and harmless, so we recommend that these should be provided more commonly. Our results suggest that there is scope to improve ferret housing and EE provision to benefit ferret welfare across all sectors.
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