Changes in the faecal microbiome of pied tamarins (Saguinus bicolor) associated with chronic, recurrent diarrhoea and weight loss.

BackgroundChronic recurrent diarrhoea and weight loss is a common problem in captive callitrichids. These symptoms are common clinical features of marmoset wasting syndrome (MWS), a chronic enteric inflammation of unknown aetiology associated with mortality in captive marmosets. The unknown aetiology of the condition presents problems for conservation projects where affected colonies present higher mortality and lower birth rates. Since a role for the microbiome has been established in chronic enteric inflammation of other species it is possible that the intestinal microbiome undergoes similar changes during MWS.ResultsThe faecal microbiome of pied tamarins (Saguinus bicolor) at Jersey Zoo was determined using 16S rRNA gene amplicon sequencing to compare the composition of the faecal microbiome of tamarins affected by chronic recurrent diarrhoea and weight loss with unaffected individuals. Affected individuals had a higher relative abundance of amplicon sequence variants assigned to Lactobacillus and Helicobacter jaachi while unaffected individuals had a higher relative abundance of some Lachnospiraceae and Ruminococcaceae.ConclusionsAlthough Helicobacter has been shown to reside in healthy wild and captive marmosets and tamarins and appears to form part of the normal microbiota, the results of this study raise the prospect that certain species of Helicobacter may be associated with chronic, recurrent diarrhoea in captive callitrichids. The presence of Lactobacillus may also play a role in the development of MWS. Since depletion of Lachnospiraceae and Ruminococcaceae have been linked to chronic gastrointestinal inflammation in humans, this feature of the microbiome of affected tamarins provides another avenue of further research in the pathogenesis of MWS

Principal Component Analysis as a Novel Method for the Assessment of the Enclosure Use Patterns of Captive Livingstone’s Fruit Bats (Pteropus livingstonii)

The Spread of Participation Index (SPI) is a standard tool for assessing the suitability of enclosure design by measuring how captive animals access space. This metric, however, lacks the precision to quantify individual-level space utilization or to determine how the distribution of resources and physical features within an enclosure might influence space use. Here we demonstrate how Principal Component Analysis (PCA) can be employed to address these aims and to therefore facilitate both individual-level welfare assessment and the fine-scale evaluation of enclosure design across a range of captive settings. We illustrate the application of this methodology by investigating enclosure use patterns of the Livingstone’s fruit bat (Pteropus livingstonii) population housed at Jersey Zoo. Focal sampling was used to estimate the time each of 44 individuals in the first data collection period and 50 individuals in the second period spent in each of 42 theoretical enclosure sections. PCA was then applied to reduce the 42 sections to five and seven ecologically relevant “enclosure dimensions” for the first and second data collection periods respectively. Individuals were then assigned to the dimension that most accurately represented their enclosure use patterns based on their highest dimensional eigenvalue. This assigned dimension is hereafter referred to as the individual’s Enclosure Use Style (EUS). Sex was found to be significantly correlated with an individual’s EUS in the second period, whilst age was found to significantly influence individual fidelity to assigned EUS. When assessing the effect of resource location on group-level preference for certain sections, the presence of feeders and proximity to public viewing areas in period one, and feeders and heaters in period two, were positively correlated with space use. Finally, individual EUS remained consistent between both data collection periods. We interpret these results for this species in the context of its observed behavioural ecology in the wild and evaluate the degree to which the current captive enclosure for this population allows for optimal individual welfare through the facilitation of spatial choice. We then explore how these methods could be applied to safeguard captive animal welfare across a range of other scenarios

Social roles influence cortisol levels in captive Livingstone's fruit bats (Pteropus livingstonii)

A critical component of conserving and housing species ex situ is an explicit scientific understanding of the physiological underpinnings of their welfare. Cortisol has been repeatedly linked to stress, and therefore used as an indicator of welfare for many species. In order to measure cortisol in the Livingstone's fruit bat (Pteropus livingstonii; a critically endangered keystone species) without disturbing the captive population, we have developed and validated a non-invasive, novel hormone extraction procedure and faecal glucocorticoid assay. A total of 92 faecal samples, 73 from the P. livingstonii breeding colony at Jersey Zoo, Channel Islands and 19 samples from P. livingstonii housed at Bristol Zoological Gardens, UK, have been collected and analyzed. Mixed-effect modelling of the influence of physiological state variables on cortisol concentration revealed that lactating females had higher cortisol levels than non-lactating females, indicating that our assay is measuring biologically relevant hormone concentrations. Males and older bats also had higher cortisol than non-lactating females and younger individuals. Further analysis applied social network methodology to compare the cortisol levels of bats with different social roles. We found that individuals that linked social groups possessed higher than average cortisol levels and conversely, individuals with high-quality, positive relationships had lower cortisol levels. These results demonstrate, for the first time in a bat species, social mediation of stress hormones. Lastly, the frequency of vocalisation was found to positively correlate with cortisol concentration in males, suggesting that this behaviour may be used by animal management as a visual indicator of a bat's hormonal status. Hence, this research has provided unique insights and empirical scientific knowledge regarding the relationship between the physiology and social behaviour of P. livingstonii, therefore allowing for recommendations to be made to optimise bat welfare at the individual level

After Short Interbirth Intervals, Monkeys Have Higher Infant Mortality

Unusually short or long interbirth intervals (IBIs) are associated with increased risks of infant mortality in humans. However, further research is needed to determine the extent to which this relationship holds more broadly among primates. Using Cox proportional hazards models, we examined the effects of atypical IBI on infant survivorship using a large demographic dataset (n = 15,852) of callitrichine monkeys (marmosets, tamarins, and lion tamarins) from zoo and laboratory populations. In seven of the nine species studied, infants born after short IBIs had significantly higher risks of mortality than infants born after longer IBIs. Taken together, these results suggest that fundamental constraints may underlie the relationships between elevated infant mortality and atypical birth spacing in human and nonhuman primates

A comparative study of litter size and sex composition in a large dataset of callitrichine monkeys

In many birds and mammals, the size and sex composition of litters can have important downstream effects for individual offspring. Primates are model organisms for questions of cooperation and conflict, but the factors shaping interactions among same-age siblings have been less-studied in primates because most species bear single young. However, callitrichines (marmosets, tamarins, and lion tamarins) frequently bear litters of two or more, thereby providing the opportunity to ask whether variation in the size and sex composition of litters affects development, survival, and reproduction. To investigate these questions, we compiled a large dataset of nine species of callitrichines (n = 27,080 individuals; Callithrix geoffroyi, Callithrix jacchus, Cebuella pygmaea, Saguinus imperator, Saguinus oedipus, Leontopithecus chrysomelas, Leontopithecus chrysopygus, Leontopithecus rosalia, and Callimico goeldii) from zoo and laboratory populations spanning 80 years (1938-2018). Through this comparative approach, we found several lines of evidence that litter size and sex composition may impact fitness. Singletons have higher survivorship than litter-born peers and they significantly outperform litter-born individuals on two measures of reproductive performance. Further, for some species, individuals born in a mixed-sex litter outperform isosexually-born individuals (i.e., those born in all-male or all-female litters), suggesting that same-sex competition may limit reproductive performance. We also document several interesting demographic trends. All but one species (C. pygmaea) has a male-biased birth sex ratio with higher survivorship from birth to sexual maturity among females (although this was significant in only two species). Isosexual litters occurred at the expected frequency (with one exception: C. pygmaea), unlike other animals, where isosexual litters are typically overrepresented. Taken together, our results indicate a modest negative effect of same-age sibling competition on reproductive output in captive callitrichines. This study also serves to illustrate the value of zoo and laboratory records for biological inquiry