Captive Callitrichids Research Articles

Cryptococcus Infection in Captive Callitrichids in the United Kingdom

Cryptococcosis is widely reported in North America and Australia but considered rare in the UK. Disease is mainly caused by Cryptococcus neoformans and Cryptococcus gattii and affects animals and humans. Cases of cryptococcosis have been described in non-human primates, including a few in the Callitrichidae family. Six captive callitrichids from five zoological facilities in the UK were diagnosed with cryptococcosis on post-mortem examination over a 13-year period. Histological examination revealed intralesional yeast bodies consistent with Cryptococcus spp in lung, brain, lymph nodes, larynx, salivary gland and ears. C. neoformans was confirmed in two cases by culture and by culture and polymerase chain reaction (28S rRNA gene), respectively. This case series is the first report of Cryptococcus spp in captive callitrichids in the UK and reinforces the need to include this fungal disease in the differential diagnosis of sick callitrichids in zoo settings.

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.

Environmental complexity and feeding enrichment can mitigate effects of space constraints in captive callitrichids.

Non-human primates housed in zoos and laboratories often exhibit reduced activity and this poses welfare concerns. We examined the effects of enclosure types of differing size and environmental complexity on the activities of two species of callitrichids. We found that cotton-top tamarins housed in an enclosure of larger size and more environmental complexity showed higher activity levels, which was mainly contributed by more feeding/foraging activity. By contrast, Goeldi's monkeys housed in an enclosure of larger size and more environmental complexity showed lower activity levels, which was mainly contributed by less locomotory activity. In both species, off-exhibit groups housed in smaller enclosures did not show significantly less locomotory activity which would have been expected, as larger availability spaces should allow more opportunities for locomotion. Furthermore, the feeding enrichment had significant effects on increased feeding/foraging activity for both cotton-top tamarins and Goeldi's monkeys, irrespective of enclosure type. These results suggested that environmental complexity (or application of feeding enrichment) that provided more opportunities for natural foraging could have a larger effect on overall activity levels compared with larger enclosure sizes that should provide more locomotion opportunities. More importantly, it showed that even when enclosure space and complexity were limited, increased opportunities for foraging through the application of enrichment could increase species-typical behaviours. Such inexpensive, easy to implement enrichment methods should be applied to provide more complex environments for captive non-human primates, particularly in situations where there are logistical and/or cost constraints to the modification of physical exhibits.

Fatal Parastrongylus dujardini infection in captive callitrichids.

Intravascular nematodes were considered the cause of death of 14 captive callitrichids. All animals were captive born at zoos in France and died with little or no premonitory signs of disease. No consistent gross lesions were observed at necropsy, although in certain cases intracardiac adult parasites were noted. The most significant histologic findings were verminous pneumonia and pulmonary endarteritis. In all cases except one, intravascular adult nematodes were observed with eggs and larvae in the lungs. Adult nematodes were obtained from 8 animals and in all cases were identified as Parastrongylus dujardini. To the authors' knowledge, this is the first report of intravascular angiostrongylosis with primary cardiopulmonary location in callitrichids in France.

Callitrichid nutrition and food sensitivity.

Captive callitrichids are prone to developing intestinal problems. Their captive and natural diets differ enormously, and diet has been suggested to play a major role in wasting marmoset syndrome. Proteins in wheat, soy and milk are included in callitrichid diets of most colonies and have been linked to an immune reaction in Saguinus oedipus and Callithrix jacchus. In the present study of 23 males and females of the two species, wheat protein was tested but soy and milk products were excluded. One group had wheat and the other had rice in their diet. Blood samples and biopsies from the colon were taken. Results showed changes in the colon and an immune reaction to gliadin, a wheat protein related to coeliac disease in humans. A further immune reaction was also observed. Suggestions for further study and exclusion of cereal in the diet of these small, New World primates are discussed.

Vitamin D intakes by cotton-top tamarins (Saguinus oedipus)and associated serum 25-hydroxyvitamin D concentrations

Rickets and osteomalacia have been reported frequently in captive callitrichids. Some have assumed that these conditions are a consequence of unmet, unusually high requirements for vitamin D and that these high requirements are characteristic of all New World primates. As a consequence, certain commercial diets formulated for New World primates contain such high concentrations of vitamin D that their consumption by other species has resulted in signs of vitamin D toxicity. This study was conducted to assess the vitamin D status of captive cotton-top tamarins consuming diets providing either 2,500 or 26,000 IU of vitamin D3/kg dry matter. These diets had been consumed for at least 2 years before the study, with the lower vitamin D intakes by six tamarins (0.5 to 9 years old) in a zoo colony and the higher vitamin D intakes by 24 tamarins (2 to 12 years old) in a pharmaceutical research laboratory. Although not measured in this study, none of the dietary ingredients has been shown to contain vitamin D2. Serum 25-hydroxyvitamin D (25(OH)D) concentrations in the captive tamarins were compared with serum 25(OH)D concentrations (range, 25.5–120 ng/mL; 64–300 nmol/L) reported by others in healthy wild tamarins in Colombia, South America. Concentrations of 25(OH)D in serum from zoo tamarins consuming 2,500 IU vitamin D3/kg dietary dry matter ranged from 48 to 236 ng/mL (120–590 nmol/L), whereas those in serum from laboratory tamarins fed 26,000 IU vitamin D3/kg dietary dry matter ranged from 11 to 560 ng/mL (28–1,400 nmol/L), with no significant (P > 0.05) association between serum 25(OH)D concentration and sex or age. However, in the laboratory tamarins, serum 25(OH)D concentrations ranged from 46 to 60 ng/mL (115–150 nmol/L) in one 8-year-old male and four 12-year-old females that had four to nine pregnancies each. Younger females (2–5 years old) that had zero or one pregnancy and the other males (3–12 years old) generally had serum 25(OH)D concentrations above 126 ng/mL (315 nmol/L). None of the individuals in the zoo colony showed signs of colitis. Of the two tamarins in the laboratory group with 25(OH)D levels below 50 ng/mL (125 nmol/L), one was a 4-year-old male with anorexia and cachexia associated with severe colitis. The second was a 7-year-old clinically normal, multiparous (five) female with normal hematology and clinical chemistry but histologic evidence of severe colitis. Because all other individuals in this group had histologic evidence of moderate to severe colitis but were normal in other respects, an unequivocal association between low serum 25(OH)D concentrations and colitis was not apparent. A dietary vitamin D3 concentration of 2,500 IU/kg dry matter was more than sufficient to support serum 25(OH)D concentrations equivalent to those found in the wild and, although the number of observations was small, supported apparently normal growth and adult weights, reproduction through five parities, and general health in a zoo colony showing no evidence of colitis. Zoo Biol 18:473–480, 1999. © 1999 Wiley-Liss, Inc.

Assessing vitamin D status of callitrichids: Baseline data from wild cotton-top tamarins (Saguinus oedipus) in Colombia

Bone disease related to vitamin D deficiency is an insidious problem in captive colonies of callitrichids. Currently a diagnosis of vitamin D deficiency may be made after the appearance of clinical pathology, usually bone deformities or fractures. The development of assays for vitamin D metabolites suggests it may be possible to detect incipient vitamin D deficiency before animals are adversely affected. However, there are few data on normative levels of these metabolites in any nonhuman primates. We collected blood samples from 18 wild cotton-top tamarins (Saguinus oedipus) from Colombia and assayed them for 25-hydroxy vitamin D(25-OH-D), the major circulating form of the vitamin, which is believed to be a good indicator of status. Serum concentrations of 25-OH-D averaged 76.4 ng/ml (range 25.5–120 ng/ml). This is high compared with human norms (10–55 ng/ml), but the range is lower than that reported in the literature for captive callitrichids. Juveniles had higher serum concentrations than did adults, and pregnant females had lower concentrations than did nonpregnant females. These data confirm that healthy callitrichids have higher circulating levels of 25-OH-D than do humans, but they suggest that the extremely high levels found in some captive animals (300–600 ng/ml) may be above normal. We propose that serum concentrations of 25-OH-D of 50–120 ng/ml can be considered normal for cotton-top tamarins and perhaps other callitrichids. If serum values much below 50 ng/ml are found during clinical evaluation, the possibility of incipient vitamin D deficiency should be considered. Zoo Biol 16:39–46, 1997. © 1997 Wiley-Liss, Inc.

Differences among captive callitrichids in the digestive responses to dietary gum

Differences among captive callitrichids in the digestive responses to dietary gum

Differences among captive callitrichids in the digestive responses to dietary gum

Although many members of the Callitrichidae, a monophyletic family of small, New World monkeys, have been observed to feed on plant exudates, available field data support the generalization that pygmy and common marmosets (Cebuella pygmaea and Callithrix jacchus) feed on gums to a greater extent than most other callitrichids. Because microbial fermentation is required for vertebrates to digest gums, gum-feeding primates may react differently to dietary gum from their relatives that eat little gum. To test this hypothesis, digestion trials were conducted on animals from the two marmoset species, two tamarin species (Saguinus fuscicollis and S. oedipus), and a species of lion tamarin (Leontopithecus rosalia). These species span the range of body sizes within the Callitrichidae. All animals were fed two variations of a homogeneous diet, which differed only in that gum arabic was added to one. Transit time of digesta (TFA) and digestive efficiency (as measured by the coefficients of apparent digestibility of dry matter and energy [ADDM and ADE, respectively]) were compared between diets for each individual. As predicted, the digestive responses of marmosets differed from the responses of the other study species. In marmosets, TFA tended to be longer when gum was added to the diet, while TFA did not change in the other three species. Digestive efficiency decreased in tamarins and lion tamarins with the addition of gum to the diet; marmoset digestive efficiency was unaffected by diet. The results of this research are consistent with the hypothesis that marmosets have digestive adaptations that aid in the digestion of gum that other callitrichids lack. © 1996 Wiley-Liss, Inc.

Diseases of the Callitrichidae: A review

The Callitrichidae contains four genera that embrace up to 50 species and subspecies found in neotropical habitats. Certain members have either naturally occurring or induced conditions that serve as important models of human disease. They include viral, bacterial, and parasitic infections, nutritional deficiencies, neoplasia, and various other conditions. The spontaneous diseases of captive callitrichids and those to which these species are experimentally susceptible were reviewed.

Susceptibility of tamarin (Saguinus labiatus) red blood cell membrane lipids to oxidative stress: implications for wasting marmoset syndrome.

Captive Callitrichids frequently suffer a fatal wasting disease, wasting marmoset syndrome (WMS), of unexplained cause. This paper describes studies on the erythrocytes from animals in a breeding colony of tamarins (Saguinus labiatus), in which deaths from anaemia and wasting were occurring, to seek evidence for biochemical changes which could lead to oxidative damage and premature cell lysis. In only one animal of 33 studied did the red blood cell lipids show an increased susceptibility to oxidative damage. This animal, with some degree of certainty, could be diagnosed as having WMS. It was concluded that evidence for a primary deficiency of antioxidants as a cause of unexplained deaths, or WMS, in the colony could not at present be substantiated.