Effects of captivity,diet, and relocation on the gut bacterial communities of white‐footed mice

Microbes can have important impacts on their host's survival. Captive breeding programs for endangered species include periods of captivity that can ultimately have an impact on reintroduction success. No study to date has investigated the impacts of captive diet on the gut microbiota during the relocation process of generalist species. This study simulated a captive breeding program with white‐footed mice (Peromyscus leucopus) to describe the variability in gut microbial community structure and composition during captivity and relocation in their natural habitat, and compared it to wild individuals. Mice born in captivity were fed two different diets, a control with dry standardized pellets and a treatment with nonprocessed components that reflect a version of their wild diet that could be provided in captivity. The mice from the two groups were then relocated to their natural habitat. Relocated mice that had the treatment diet had more phylotypes in common with the wild‐host microbiota than mice under the control diet or mice kept in captivity. These results have broad implications for our understanding of microbial community dynamics and the effects of captivity on reintroduced animals, including the potential impact on the survival of endangered species. This study demonstrates that ex situ conservation actions should consider a more holistic perspective of an animal's biology including its microbes.     

Analysis of the hydrogenotrophic microbiota of wild and captive black howler monkeys (Alouatta pigra) in palenque national park, Mexico

Intestinal methanogenesis is one of the major pathways for consumption of hydrogen produced by bacterial fermentation and is considered to affect the efficiency of host energy harvest; however, little information is available regarding the hydrogenotrophic pathways of nonhuman primates in the wild, in general, and of howler monkeys, in particular. Microbial fermentation of plant structural carbohydrates is an important feature in wild howlers owing to the high fiber and low available energy content of leaves, which make up the primary component of their diet. In contrast, captive howlers may consume greater quantities of fruits and vegetables that are higher in water, lower in fiber, and, along with commercial monkey chow commonly added to captive monkey diets, more readily digestible than the natural diet. In this study, we analyzed the composition of methanogens and sulfate-reducing bacteria (SRB) from fecal samples of black howler monkeys (Alouatta pigra) in the wild and in captivity. The hydrogenotrophic microbiota of three groups of monkeys was evaluated by PCR-denaturing gradient gel electrophoresis (DGGE) fingerprinting, small clone library construction, and quantitative real-time PCR. Abundance of methanogens was lower than SRB in all howler monkey groups studied. DGGE banding patterns were highly similar within each wild and captive group but distinct among groups. Desulfovibrionales-enriched DGGE showed reduced microbial diversity in the captive animals compared with their wild counterparts. Taken together, the data demonstrate that environmental or dietary changes of the host imposed by captivity likely influence the composition of intestinal hydrogenotrophs in black howler monkeys.     

Differences in dietary and plasma fatty acids between wild and captive populations of a rare reptile, the tuatara (Sphenodon punctatus)

Tuatara (Sphenodon) are rare reptiles endemic to New Zealand. Wild tuatara on Stephens Island (study population) prey on insects as well as the eggs and chicks of a small nesting seabird, the fairy prion (Pachyptila turtur). Tuatara in captivity (zoos) are fed diets containing different insects and lacking seabirds. We compared the fatty acid composition of major dietary items and plasma of wild and captive tuatara. Fairy prions (eaten by tuatara in the wild) were rich in C20 and C22 polyunsaturated fatty acids (PUFA), especially the n-3 fatty acids eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA). In contrast, items from the diet of captive tuatara contained no C20 and C22 PUFA and were higher in medium-chain and less unsaturated fatty acids. Plasma from wild tuatara was higher in n-3 PUFA [including alpha-linoleic acid (C18:3n-3), EPA and DHA], and generally lower in oleic acid (C18:1) and palmitic acid (C16:0), than plasma from captive tuatara in the various fractions (phospholipid, triacylglycerol, cholesterol ester and free fatty acids). Plasma from wild adult tuatara showed strong seasonal variation in fatty acid composition, reflecting seasonal consumption of fairy prions. Differences in the composition of diets and plasma between wild and captive tuatara may have consequences for growth and reproduction in captivity. Accepted: 3 August 1998     

Differences in fecal particle size between free‐ranging and captive individuals of two browser species

Data from captive animals indicated that browsing (BR) ruminants have larger fecal particles—indicative of lesser chewing efficiency—than grazers (GR). To answer whether this reflects fundamental differences between the animal groups, or different reactions of basically similar organisms to diets fed in captivity, we compared mean fecal particle size (MPS) in a GR and a BR ruminant (aurox Bos primigenius taurus, giraffe Giraffa camelopardalis) and a GR and a BR hindgut fermenter (Przewalski's horse Equus ferus przewalskii, lowland tapir Tapirus terrestris), both from captivity and from the wild. As would be expected owing to a proportion of finely ground, pelleted feeds in captive diets, MPS was smaller in captive than free‐ranging GR. In contrast, MPS was drastically higher in captive than in free‐ranging BR of either digestion type. Thus, the difference in MPS between GR and BR was much more pronounced among captive than free‐ranging animals. The results indicate that BR teeth have adapted to their natural diet so that in the wild, they achieve a particle size reduction similar to that of GR. However, although GR teeth seem equally adapted to food ingested in captivity, the BR teeth seem less well suited to efficiently chew captive diets. In the case of ruminants, less efficient particle size reduction could contribute to potential clinical problems like “rumen blockage” and bezoar formation. Comparisons of MPS between free‐ranging and captive animals might offer indications for the physical suitability of zoo diets. Zoo Biol 27:70–77, 2008. © 2007 Wiley‐Liss, Inc.     

Parental Nutrition and Chick Production in Captive Willow Ptarmigan (Lagopus L. Lagopus)

The breeding performance of captive willow ptarmigan on different diets has been studied. The nutritional factors tested were protein concentration, natural feed supplement and grass meal and flavonoid admixture, and effects on egg numbers, fertility, hatchability, chick weights at hatching and 0–14 days mortality have been recorded. The breeding performance of ptarmigan hen in captivity showed great individual variations. Egg numbers were not statistically different in groups fed the different diets. Hens fed a 15 % crude protein died tended to produce smaller chicks with significantly lower viability than chicks from hens fed a 20 % crude protein diet. Supplement of natural feed tended to increase the number of chicks hatched through a combination of tendency to higher egg numbers and improved fertility. These tendencies were, however, statistically nonsignificant. Inclusion of 34 % grass meal to the diet also tended (non-significantly) to improve fertility and hatchability, while inclusion of flavonoids had no positive effect on reproduction. Eggs from captive hens showed significantly lower fertility, and a tendency to lower hatchability than eggs from wild hens. The former difference was probably caused by the close cage confinements for the captive ptarmigan, while the latter condition probably was due to different start of incubation, most of the eggs from wild hens being started naturally.     

Ex situ Diet Influences the Bacterial Community Associated with the Skin of Red-Eyed Tree Frogs (Agalychnis callidryas)

Amphibians support symbiotic bacterial communities on their skin that protect against a range of infectious pathogens, including the amphibian chytrid fungus. The conditions under which amphibians are maintained in captivity (e.g. diet, substrate, enrichment) in ex situ conservation programmes may affect the composition of the bacterial community. In addition, ex situ amphibian populations may support different bacterial communities in comparison to in situ populations of the same species. This could have implications for the suitability of populations intended for reintroduction, as well as the success of probiotic bacterial inoculations intended to provide amphibians with a bacterial community that resists invasion by the chytrid fungus. We aimed to investigate the effect of a carotenoid-enriched diet on the culturable bacterial community associated with captive red-eyed tree frogs (Agalychnis callidryas) and make comparisons to bacteria isolated from a wild population from the Chiquibul Rainforest in Belize. We successfully showed carotenoid availability influences the overall community composition, species richness and abundance of the bacterial community associated with the skin of captive frogs, with A. callidryas fed a carotenoid-enriched diet supporting a greater species richness and abundance of bacteria than those fed a carotenoid-free diet. Our results suggest that availability of carotenoids in the diet of captive frogs is likely to be beneficial for the bacterial community associated with the skin. We also found wild A. callidryas hosted more than double the number of different bacterial species than captive frogs with very little commonality between species. This suggests frogs in captivity may support a reduced and diverged bacterial community in comparison to wild populations of the same species, which could have particular relevance for ex situ conservation projects.     

The effect of captivity on the primate gut microbiome varies with host dietary niche

Despite careful attention to animal nutrition and wellbeing, gastrointestinal distress remains relatively common in captive non‐human primates (NHPs), particularly dietary specialists such as folivores. These patterns may be a result of marked dietary differences between captive and wild settings and associated impacts on the gut microbiome. However, given that most existing studies target NHP dietary specialists, it is unclear if captive environments have distinct impacts on the gut microbiome of NHPs with different dietary niches. To begin to examine this question, we used 16S ribosomal RNA gene amplicon sequences to compare the gut microbiomes of five NHP genera categorized either as folivores (Alouatta, Colobus) or non‐folivores (Cercopithecus, Gorilla, Pan) sampled both in captivity and in the wild. Though captivity affected the gut microbiomes of all NHPs in this study, the effects were largest in folivorous NHPs. Shifts in gut microbial diversity and in the relative abundances of fiber‐degrading microbial taxa suggest that these findings are driven by marked dietary shifts for folivorous NHPs in captive settings. We propose that zoos and other captive care institutions consider including more natural browse in folivorous NHP diets and regularly bank fecal samples to further explore the relationship between NHP diet, the gut microbiome, and health outcomes.     

Nutritional and Health Status of Woolly Monkeys

Woolly monkeys (Lagothrix lagotricha and L. flavicauda) are threatened species in the wild and in captivity. Numerous zoological institutions have historically kept Lagothrix lagotricha spp., but only a few of them have succeeded in breeding populations. Therefore the majority of institutions that formerly kept Lagothrix lagotricha are no longer able or willing to do so. Captive populations of the species have frequent health problems, most significantly hypertension and related disorders. Researchers have conducted free-ranging dietary and behavior studies with respect to woolly monkeys, but have established no concrete link between diet or nutrients and captive health problems. The available literature we discuss indicates that researchers need to examine the link further. In addition, it is critical to the survival of the primates to be able to keep breeding populations in captivity owing to increasing natural pressures such as deforestation and hunting. Therefore, better understanding of the captive and free-ranging behavior and health parameters of the species is vital to ensure their survival and to maintain forest health and diversity. Researchers need to conduct large-scale research studies comparing the health and complete diet of individuals in the wild and captivity to resolve health problems facing the species in captivity.     

Dental eruption schedules of wild and captive baboons

Dental eruption schedules previously used to age wild baboons have in the past derived from studies of captive animals housed under standard conditions and fed standard laboratory diets. This paper reports for the first time eruption schedules derived from wild baboons, the yellow baboons (Papio hamadryas cynocephalus) of Mikumi National Park, Tanzania, and compares these schedules with those of other baboon subspecies inhabiting both similar and dissimilar environments. Eighteen males and twelve females from the Viramba groups, ranging in age from 21 to 103 months, were trapped, and dental impressions and notes were made of the state of eruption of each tooth. Eruption of all teeth were delayed at Mikumi relative to the baboon standards derived from the captive animals at the Southwest Foundation for Biomedical Research, San Antonio, Texas. Teeth of the canine-premolar 3 complex and third molars were most delayed, erupting up to a year and a half later than their counterparts from captive animals. Comparison with data on hamadryas baboons from Erer-Gota in Ethiopia revealed that both the hamadryas and yellow subspecies of baboons, with different genetic backgrounds and living under markedly different environmental conditions, followed the same schedule. This constancy of developmental schedules suggests that these Mikumi data may reasonably be used as standards for other wild baboon populations and that acceleration of dental maturation, as well us maturation of other somatic systems in captivity, is another manifestation of the short-term adaptive plasticity of the baboon species as a whole.     

Pyrosequencing faecal DNA to determine diet of little penguins: is what goes in what comes out?

DNA barcoding of faeces or stomach contents is an emerging approach for dietary analysis. We pyrosequenced mtDNA 16S markers amplified from faeces of captive little penguins (Eudyptula minor) to examine if recovered sequences reflect the proportions of species consumed. We also analysed wild little penguin faeces collected from 100 nests in southeast Australia. In the captive study, pilchards were the primary fish fed to the penguins and DNA sequences from pilchard were the most common sequences recovered. Sequences of three other fish fed in constant mass proportions (45:35:20) were all detected, but proportions of sequences (60:6:34) were considerably different than mass proportions in the diet. Correction factors based on relative mtDNA density in the fish did not improve diet estimates. Consistency between replicate samples suggests that the observed bias resulted from differences in prey digestibility. Detection of DNA from fish consumed before the penguins were brought into captivity indicates that a DNA signal in faeces can persist for at least 4 days after ingestion. In the wild-collected faeces, 24 distinct fish and 1 squid were identified; anchovy, barracouta and pilchard accounted for over 80% of these sequences. Our results highlight that DNA sequences recovered in dietary barcoding studies can provide semi-quantitative information on diet composition, but these data should be given wide confidence intervals.     

Differences in carotenoid accumulation among three feeder-cricket species: implications for carotenoid delivery to captive insectivores

There are a limited number of feeder-invertebrates available to feed captive insectivores, and many are deficient in certain nutrients. Gut-loading is used to increase the diversity of nutrients present in the captive insectivore diet; however, little is known about delivery of carotenoids via gut-loading. Carotenoids may influence health and reproduction due to their roles in immune and antioxidant systems. We assessed interspecific variation in carotenoid accumulation and retention in three feeder-cricket species (Gryllus bimaculatus, Gryllodes sigillatus and Acheta domesticus) fed one of three diets (wheat-bran, fish-food based formulated diet, and fresh fruit and vegetables). Out of the three species of feeder-cricket in the fish-food-based dietary treatment group, G. bimaculatus had the greatest total carotenoid concentration. All cricket species fed the wheat-bran diet had very low carotenoid concentrations. Species on the fish-food-based diet had intermediate carotenoid concentrations, and those on the fruit and vegetable diet had the highest concentrations. Carotenoid retention was poor across all species. Overall, this study shows that, by providing captive insectivores with G. bimaculatus crickets recently fed a carotenoid-rich diet, the quantity of carotenoids in the diet can be increased.     

The phenotypic costs of captivity

The breeding of threatened species in captivity for release is a central tool in conservation biology. Given gloomy predictions for biodiversity trends in the Anthropocene, captive breeding will play an increasingly important role in preventing future extinctions. Relative to the wild, captive environments drastically alter selection pressures on animals. Phenotypic change in captive animals in response to these altered selection pressures can incur fitness costs post-release, jeopardising their potential contribution to population recovery. We explore the ways in which captive environments can hinder the expression of wild phenotypes. We also stress that the phenotypes of captive-bred animals differ from their wild counterparts in multiple ways that remain poorly understood. We propose five new research questions relating to the impact of captive phenotypes on reintroduction biology. With better use of monitoring and experimental reintroductions, a more robust evidence base should help inform adaptive management and minimise the phenotypic costs of captivity, improving the success of animal reintroductions.     

Effects of long-term captivity on thermoregulation,metabolism and ventilation of the southern brown bandicoot (Marsupialia: Peramelidae)

Thermoneutral metabolic and ventilatory parameters were measured every 3 months over 2 years for southern brown bandicoots held in captivity, and from a nearby reserve. Captive bandicoots were 130 g (9.9%) heavier than wild bandicoots. Long-term captivity had no effect on body temperature, basal metabolic rate (oxygen consumption), thermal conductance or respiratory ventilation, but there was an effect on carbon dioxide production, respiratory exchange ratio and total evaporative water loss (values were between 15 and 25% higher for captive than for wild bandicoots). Diet may be influencing these aspects of captive bandicoot physiology; the diet of captive bandicoots would be considerably different to that of wild bandicoots. Water availability seems to have a minimal effect. This study has important implications regarding physiological measurement for captive and wild mammals. For bandicoots at least, captive animals are equivalent to wild animals for some physiological parameters at thermoneutrality (body temperature, resting metabolic rate and thermal conductance), but not others.     

Digesta Passage,Digestibility and Behavior in Captive Gorillas Under Two Dietary Regimens

Gorilla adaptation has been debated in recent years given the wide variation among diets of gorillas in different habitats. Gorillas are the largest of living primates, have large colons and should be capable of processing tough foods. Preliminary captive studies have suggested that they may well have long average gut retention times relative to smaller hominoids, which should facilitate digestive efficiency in their wild counterparts. Indeed, wild gorillas consume large amounts of fibrous foods as staples or fall-back foods across their range, in response to habitat-related or seasonal changes in fruit availability. Fluctuations in diet might be matched by changes in digesta passage and digestibility, with possible selective retention of harder to digest items. We further studied digestive processes via chemical cobalt and chromium markers to track liquid and solids, as they passed through the guts of gorillas at the San Francisco Zoo (SFZ). In addition, we examined the effects of variation in captive diets on intake, digesta passage, digestion and behavior. The SFZ gorillas exhibited high digestibility coefficients, and gut passage was long relative to those of smaller-bodied hominoids. The results permit us to understand more fully the relationships of digestive processes to adaptation and dietary flexibility in the wild and to inform the development of dietary recommendations to improve the well-being of captive gorillas.     

Can Captive-Bred Varecia variegata variegata Adapt to a Natural Diet on Release to the Wild?

We compared the diets of 3 groups of released captive-bred Varecia variegata variegata (RG1, RG2, RG3) in the Betampona Reserve to that recorded for a resident wild group, between 1998 and 2001. We investigated whether the released captive-bred Varecia, from differing captive backgrounds, could cope with seasonal changes in climate and consequently food availability, finding sufficient food to meet their nutritional requirements, and dietary choices and selection. We collected data on diet, including plant part, family, genus and, if known, species. In addition, we collected data on seasonal variation in dietary composition. Dietary overlap is significant at the familial level between RG1/RG3 and the wild group. There is some dietary overlap between RG2 and the wild group, but it is not significant. In general, RG1 and RG3 more closely followed the dietary choices and seasonal changes in diet exhibited by the wild group. We conclude that Varecia raised in free-ranging environments are better adapted to meet their nutritional requirements in the wild than those raised in cages are. However, even they struggle to deal with seasonal climatic changes and consequent changes in food availability. We suggest that future re-introduction efforts for primates include attempts to integrate released individuals rapidly into wild groups so that they can learn to cope with a seasonal environment through direct observation of wild conspecifics.     

American alligator (Alligator mississippiensis) weight gain in captivity and implications for captive reptile body condition

The body condition of an animal is an indicator of health status and is dependent upon many factors, some of which can vary between wild and captive settings. Despite this, there have not been many studies on how captivity affects body condition relative to wild animal populations. This study explores the body condition of captive and wild American alligators (Alligator mississippiensis) because reptiles are frequently overlooked in studies of captive animal health and because alligators are well-represented in captivity. We collected body condition data from 209 captive alligators and 935 wild alligators throughout Florida and southeastern Georgia and compared the relationships between body condition and body length for each group. We found that captive alligators exhibited significantly higher body condition values as they aged, and that this result was driven by the difference between captive and wild males. Body condition values for captive juveniles did not differ from wild juveniles, but they differed when comparing adults. Our results suggest that factors such as diet and movement rates play major roles in determining alligator body condition and that body condition may be an important metric for monitoring captive alligator health, especially for older adult males.     

Modeling problems in conservation genetics using captive Drosophila populations: Rapid genetic adaptation to captivity

Long-term captive breeding programs for endangered species generally aim to preserve the option of release back into the wild. However, the success of re-release programs will be jeopardized if there is significant genetic adaptation to the captive environment. Since it is difficult to study this problem in rare and endangered species, a convenient laboratory animal model is required. The reproductive fitness of a large population of Drosophila melanogaster maintained in captivity for 12 months was compared with that of a recently caught wild population from the same locality. The competitive index measure of reproductive fitness for the captive population was twice that of the recently caught wild population, the difference being highly significant. Natural selection over approximately eight generations in captivity has caused rapid genetic adaptation. Captive breeding strategies for endangered species should minimize adaptation to captivity in populations destined for reintroduction into the wild. A framework for predicting the impact of factors on the rate of genetic adaptation to captivity is suggested. Equalization of family sizes is predicted to approximately halve the rate of genetic adaptation. Introduction of genes from the wild, increasing the generation interval, using captive environments close to those in the wild and achieving low mortality rates are all expected to slow genetic adaptation to captivity. Many of these procedures are already recommended for other reasons. © 1992 Wiley-Liss, Inc.     

Comparative study of gut microbiota from captive and confiscated-rescued wild pangolins

Pangolins are among the most critically endangered animals due to widespread poaching and worldwide trafficking. Captive breeding is considered to be one way to protect them and increase the sizes of their populations. However, comparative studies of captive and wild pangolins in the context of gut microbiota are rare. Here, the gut microbiome of captive and confiscated-rescued wild pangolins is compared, and the effects of different periods of captivity and captivity with and without antibiotic treatment are considered. We show that different diets and periods of captivity, as well as the application of antibiotic therapy, can alter gut community composition and abundance in pangolins. Compared to wild pangolins, captive pangolins have an increased capacity for chitin and cellulose/hemicellulose degradation, fatty acid metabolism, and short-chain fatty acid synthesis, but a reduced ability to metabolize exogenous substances. In addition to increasing the ability of the gut microbiota to metabolize nutrients in captivity, captive breeding imposes some risks for survival by resulting in a greater abundance of antibiotic resistance genes and virulence factors in captive pangolins than in wild pangolins. Our study is important for the development of guidelines for pangolin conservation, including health assessment, disease prevention, and rehabilitation of wild pangolin populations.     

Diet and environment shape fecal bacterial microbiota composition and enteric pathogen load of grizzly bears

Background

Diet and environment impact the composition of mammalian intestinal microbiota; dietary or health disturbances trigger alterations in intestinal microbiota composition and render the host susceptible to enteric pathogens. To date no long term monitoring data exist on the fecal microbiota and pathogen load of carnivores either in natural environments or in captivity. This study investigates fecal microbiota composition and the presence of pathogenic Escherichia coli and toxigenic clostridia in wild and captive grizzly bears (Ursus arctos) and relates these to food resources consumed by bears.

Methodology/Principal Findings

Feces were obtained from animals of two wild populations and from two captive animals during an active bear season. Wild animals consumed a diverse diet composed of plant material, animal prey and insects. Captive animals were fed a regular granulated diet with a supplement of fruits and vegetables. Bacterial populations were analyzed using quantitative PCR. Fecal microbiota composition fluctuated in wild and in captive animals. The abundance of Clostridium clusters I and XI, and of C. perfringens correlated to regular diet protein intake. Enteroaggregative E. coli were consistently present in all populations. The C. sordellii phospholipase C was identified in three samples of wild animals and for the first time in Ursids.

Conclusion

This is the first longitudinal study monitoring the fecal microbiota of wild carnivores and comparing it to that of captive individuals of the same species. Location and diet affected fecal bacterial populations as well as the presence of enteric pathogens.