Nasal, oral and rectal microbiota of Black lion tamarins (Leontopithecus chrysopygus)

RESEARCH PAPER

Nasal, oral and rectal microbiota of Black lion tamarins (Leontopithecus chrysopygus)

Vania M. Carvalho^I; Ralph E.T. Vanstreels^II; Cátia D. Paula^II; Cristiane K.M. Kolesnikovas^III; Maria Christina C. Ramos^IV; Selene D. Coutinho^I; Cristiana S. Martins^V; Alcides Pissinatti^{VI, VII, VIII}; José L. Catão-Dias^II

^ILaboratório de Biologia Molecular e Celular, Faculdade de Medicina Veterinária, Universidade Paulista, São Paulo, SP, Brazil

^IIDepartamento de Patologia, Faculdade de Medicina Veterinária e Zootecnia, Universidade de São Paulo, São Paulo, SP, Brazil

^IIIAssociação R3 Animal, Florianópolis, SC, Brazil

^IVLab&Vet Diagnóstico e Consultoria Veterinária Ltda, São Paulo, SP, Brazil

^VInstituto de Pesquisas Ecológicas, Nazaré Paulista, SP, Brazil.

^VICentro de Primatologia do Rio de Janeiro, Guapimirim, RJ, Brazil

^VIICentro Universitário Serra dos Órgãos, Teresópolis, RJ, Brazil

^VIIICentro Universitário Plínio Leite, Niterói, RJ, Brazil

^{Correspondence}

ABSTRACT

Black lion tamarins (Leontopithecus chrysopygus) are endangered callithrichids. Their conservation may require future translocations or reintroductions; however these approaches involve risks of pathogen introduction in the environment and stress-related opportunistic infections in these animals. In order to screen for opportunistic and potential pathogenic bacterial and fungal microbiota, ten free-ranging and ten captive Black lion tamarins were studied and the results compared. Nasal, oral and rectal swabs were collected and cultured for aerobic and facultative anaerobic bacteria and fungi, and a total 203 bacterial and 84 fungal isolates were obtained. Overall, the most frequent organisms were Staphylococcus spp., Bacillus spp., Candida spp. and Aspergillus spp. Microbiota of free-ranging and captive animals were similar in composition. A number of potentially pathogenic organisms were identified, emphasizing the importance of microbiological screening in future translocation or reintroduction conservation management programs.

Key words: microbiota, bacteria, fungi, black lion tamarins, Leontopithecus chrysopygus.

Introduction

Black lion tamarins (Leontopithecus chrysopygus) are small Neotropical and endangered callithrichids (Kierulff, 2008). This species originally occurred in large Atlantic forest areas of the São Paulo State, Brazil; however, due to factors such as deforestation and fragmentation, the remaining free-ranging animals are now limited to a few forest fragments scattered throughout the state (Coimbra-Filho, 1970, 1976, Valladares-Pádua and Cullen Jr, 1994, Kierulff, 2008, Kleiman & Rylands, 2008).

The total wild population is estimated at about 1000 animals spread through 11 isolated forests, only one population of which is clearly viable, the Morro do Diabo State Park. The remaining 10 isolated populations are too small to be viable in the mid- to long-term, but if managed as a metapopulation they could represent a significant genetic stock for the species conservation (Holst et al., 2006). In parallel, captive propagation is a possibility to establish breeding programs followed by reintroduction in the wild, similarly to the successful reintroduction program developed for the Golden lion tamarin, Leontopithecus rosalia (Beck et al., 1991).

These approaches of population management, however, pose the dilemma of moving individuals among wild populations and from the wild to captivity. The distress from such events has been shown to result in stress-induced immunosupression that may predispose the animals to infectious and parasitic diseases (Beck et al., 1993, Acevedo-Whitehouse and Duffus, 2009). In addition, moving animals among multiple environments increases the possibility of introducing pathogens in new areas adding risks to the population management process (Cunningham, 1996, Daszak et al., 2000).

Information on the microbiota of callithrichids is scarce and limited to captive animals. To our knowledge the only report on this topic for the genus Leontopithecus was made by Moraes et al. (2004) who investigated the fungal vaginal microbiota of captive lion tamarins (L. chrysomelas, L. chrysopygus and L. rosalia). Considering the lack of information on the Leontopithecus microbiota, the aim of this study was to screen for opportunistic and potential pathogenic aerobic and facultative anaerobic bacterial and fungal microbiota from the oral and nasal cavities and rectum of asymptomatic free-ranging and captive Black lion tamarins.

Materials and Methods

Twenty Black lion tamarins were studied in Brazil between 1997 and 1998, of which ten individuals were free-ranging (FRT) in two different governmental conservation areas (three from Fazenda Rio Claro, Lençóis Paulista; seven from Morro do Diabo State Park) and ten individuals were captive (CPT) at the Rio de Janeiro Primate Center (CPRJ). Morro do Diabo State Park is an area with limited human activity or tourism whereas Fazenda Rio Claro is a private reserve. In both areas there is extensive human and farming activity in the surroundings, and it is likely these animals had direct or indirect contact with humans and/or anthropogenic products.

The FRT were regularly monitored by radiotelemetry by the Instituto de Pesquisas Ecológicas (IPÊ - Institute for Ecological Research) as part of an on-going ecological research program. After their localization the tamarins were followed until sunset, when the group chose a tree hollow in which to spend the night. In the following morning before dawn, the tree hollow entrance was blocked and the animals were captured by sawing holes laterally to the resting chamber. The CPT were caught within their enclosure using nets, according to routine procedures established at the institution. All animals showed no evident clinical signs at physical exam and received no medications in the months prior to the study.

Once physically restrained, the tamarins were transferred to individual cages and submitted to an intramuscular association of ketamine 11mg/kg and atropine sulphate 0.044mg/kg. For nasal and oral cavities, sterile urethral swabs were introduced in the nostrils or rubbed in the gum, palate, teeth and tongue. For rectal swabs, the perianal area was cleaned with gauze and sterile saline and a sterile urethral swab was delicately introduced about one centimeter into the rectum through rotation movements. Immediately after sampling, the swab was placed in Stuart transport medium and kept under refrigeration. All procedures were approved by the Brazilian Institute of the Environment and Natural Renewable Resources.

Samples were first cultivated in BHI broth, Blood agar and Mac Conkey agar plates, which were incubated under aerobic conditions at 37 °C. After 24 h, the broths were seeded again in Blood agar and Mac Conkey agar plates. The plates were observed after 24, 48 and 72 h, and disposed after one week of observation. The swabs were also seeded into Sabouraud agar with cloramphenicol 100mg/mL, kept at room temperature and analyzed daily for 30 days. Imprints of isolated bacteria and yeast were Gram-stained and morphologically characterized. Gram positive cocci and Gram negative bacteria were submitted to the catalase and oxidase production tests, respectively. Thereafter, bacteria and yeast were identified biochemically through the use of API®System (Biomerieux). The yeasts also had their filamentation capability tested (Koneman and Roberts, 1990). The identification of mycelian fungi were based on macro and microscopic morphology achieved through Hiddel method, and according to Barnett and Hunter (1998).

Fisher's exact test was used to compare the distribution of bacterial groups (Gram positive or Gram negative) and fungal groups (yeast or mycelian fungi) between CPT vs. FRT, as well as between free-ranging tamarins sampled at Fazenda Rio Claro vs. Morro do Diabo State Park. The Kruskal-Wallis test was used to compare the bacterial and fungal recovery rates (isolates retrieved / individuals examined) between different anatomical sites (nasal, oral or rectal; df = 2). Significance level was 0.05 for all tests. It should be clear that whenever the term prevalence is used, it refers to apparent prevalence (total isolates of bacteria or fungi / total individuals examined).

Results

A total of 203 bacterial isolates were obtained, representing 12 Gram positive and 14 Gram negative genera (Actinomicetale bacteria were not identified down to genus); 3 bacterial isolates were not identified successfully. A total 84 fungal isolates were obtained, with 4 genera of yeasts and 14 genera of mycelian fungi (Mycelia sterilia fungi were not identified down to genus); one yeast isolate could not be identified. Due to field contamination, oral swabs from 4 captive tamarins were not cultured for bacteria. Figure 1 summarizes the aerobic bacterial and fungal genera isolated from the nasal, oral and rectal swabs of free-ranging (FRT) and captive (CPT) tamarins. Figure 2 presents details on the combination of bacterial and fungal isolates found in each individual.

In none of the three anatomical sites there were significant differences (all p > 0.05) on the proportion of bacterial groups (Gram positive or Gram negative) or fungal groups (yeast or mycelian fungi) between the isolates from CPT and FRT, nor between tamarins from Fazenda Rio Claro (FRC) and from Morro do Diabo State Park (MDSP). However, a few considerations can be made: Actinomicetale bacteria were retrieved from the nasal swabs of 6/7 MDSP, but were absent in 3 FRC; Lactococcus was absent in the oral swabs of 7 MDSP, but present in 2/3 FRC; Streptococcus was absent in the oral swabs of 7 MDSP, but present in 2/3 FRC.

Bacterial recovery rates were different among anatomical sites (K = 12.88, df = 2, p = 0.002), with recovery rates of rectal samples being lower than those of oral and nasal samples (nasal = 4.10+1.37 isolates retrieved / examined individual; oral = 4.12 ± 1.41; rectal = 2.75 ± 0.97). Similarly, fungal recovery rates were also different among anatomical sites (K = 12.67, df = 2, p = 0.002), with recovery rates of nasal samples being higher than those of oral and rectal samples (nasal = 2.40 ± 1.63; oral = 1.00 ± 0.79; rectal = 0.80 ± 0.62).

In the nasal cavity, Gram positive bacteria were predominant over Gram negative bacteria (G+ 96.3% of bacterial isolates, G- 3.7%) with Staphylococcus (43.9% of bacterial isolates) and Bacillus (29.3%) recognized as the most frequent Gram positive genera. Mycelian fungi dominated the fungal microbiota of the nasal cavity (Yeast 37.5% of fungal isolates, Mycelian 62.5%).

In the oral cavity, Gram positive bacteria had an overall frequency higher than Gram negative bacteria (G+ 70.8% of bacterial isolates, G- 29.2%). Streptococcus (28.3% of bacterial isolates), Bacillus (26.1%) and Staphylococcus (19.6%) were the most frequent Gram positive genera. Mycelian fungi were more frequent than yeast in the oral fungal microbiota (Yeast 22.2% of fungal isolates, Mycelian 77.8%).

Unlike in the nasal and oral microbiota, the rectum revealed Gram negative bacteria as being more frequent than Gram positive bacteria (G+ 38.2% of bacterial isolates, G- 61.8%). Escherichia coli was the most frequent bacteria (29.1% of bacterial isolates), followed by Serratia spp. (10.9%). Yeasts were more frequent than mycelian fungi in the rectal samples (Yeast 75% of fungal isolates, Mycelian 25%).

Discussion

Investigation of clinically healthy black lion tamarins showed Gram positive bacteria as dominant in the nasal and oral microbiota, while the rectal microbiota was predominantly composed of Gram negative bacteria. Nasal, oral and rectal microbiota shared many microorganisms but in different proportions. The nasal microbiota had the highest recovery rate, being dominated by Gram positive bacteria and presenting a large variety of mycelian fungi and a high frequency of Candida yeast. The oral microbiota had intermediary recovery rate and was predominantly composed of Gram positive bacteria and mycelian fungi (note that the higher relative frequency of mycelian fungi in the oral cavity when compared to the nasal cavity was more due to a decreased recovery of yeasts than to an increased recovery of filamentous fungi). The rectal microbiota presented poor recovery rates, being composed by a majority of Gram negative bacteria and yeast fungi. These findings are consistent with those described for other primates including humans (Brown et al., 1973, Hill et al., 1978, Nordstrom et al., 1989, Bailey and Coe 2002, Moreira et al., 2003, 2004).

Overall, the most frequent bacteria were Staphylococcus spp. (22% of bacterial isolates) and Bacillus spp. (21%), followed by Escherichia coli, Streptococcus spp., Actinomicetale, Klebsiella pneumoniae, Corynnebacterium spp. and Citrobacter spp. Gram positive cocci as Aerococcus, Staphylococcus and Streptococcus were previously reported in the intestinal tract, skin and mucosa of healthy nonhuman primates (Daniel et al., 1976, Hill et al., 1978, Swindle et al., 1982, Lewis et al., 1987), however in some conditions have also been implied as the cause of pneumonia, nephritis and cystitis in this group of animals (Hunt et al., 1978, Boever and Wallach 1983, McClure et al., 1986). Streptococcus pneumoniae is an important pathogen leading to pneumonia in primates, but it is not usually considered as an important callitrichid pathogen (McClure et al., 1986, Chi et al., 2007); while we did not identify this specific organism in the studied animals, there were five Streptococcus isolates that could not be identified down to species. Aerococcus viridans is frequent in the reproductive tract of primates, but is also known to cause abortion and natimortality (Swindle et al., 1982). Bacillus, as a sporeforming bacteria, has the soil as its primary reservoir and is widespread in water and air (Nicholson, 2002). As a consequence it is encountered also in the microbiota of animals (Jungle et al., 2005, Lima et al., 2012, Souza et al., 2012), meantime, its role as spontaneous nonhuman primate pathogen is unknown.

Escherichia coli is known to be one of the most abundant saprophytic bacteria in the gastrointestinal tract of warm-blooded animals. However, pathogenic strains are important cause of diarrhoea and can also cause other pathologic conditions, including septicaemias, meningitis, urinary infections, abscesses and celulitis (McClure et al., 1986, Carvalho et al., 2003, Blanco et al., 2004, Carvalho et al., 2012). Indeed, E. coli seems to be a potential pathogen for callithrichids (Mansfield et al., 2001). In the present study E. coli was isolated most commonly from rectal samples being demonstrated in 80% of animals sampled. Carvalho et al. (2003), studying Neotropical monkeys (56% of which were callithrichids) from rehabilitation centres, zoos and private breeders in Brazil, found enteropathogenic Escherichia coli (EPEC) strains in 29% of the studied animals, all of which were callithrichids. Although 37% of the individual with these pathogenic strains were clinically healthy, colon's histopathological evaluation of animals submitted for necropsy and from which EPEC was isolated revealed distortion and reduction in crypt size and an inflammatory infiltrate. Furthermore, the isolates revealed a genetic relationship with human EPEC (Carvalho et al., 2007).

Klebsiellapneumoniae has been frequently implied in pulmonary disease, septicaemia, meningitis and other pathologic processes in primates (Fox and Rohovsky 1975, Hunt et al., 1978, Chalmers et al., 1983, Gozalo et al., 1991, Pisharath et al., 2005). Outbreaks in callithrichids breeding colonies have revealed K. pneumoniae infection causing severe purulent peritonitis and sepsis (Gozalo et al., 1991, Pisharath et al., 2005). It is interesting to note that in this study, although recovered from free-ranging and captive animals, Klebsiella was present more frequently in the rectum and nasal cavity of animals' kept in captivity.

Other bacteria isolated in the studied animals included Pseudomonas aeruginosa and Citrobacter freundii, which have been reported to cause diarrhoea, pneumonia, septicaemia, nephritis and cystitis in nonhuman primates (Hunt et al., 1978, Boever and Wallach 1983, Lausen et al., 1986, McClure et al., 1986, Ocholi et al., 1989). Zoonotic bacterial pathogens associated with diseases of captive nonhuman primates, as Salmonella, Shigella, Bordetella, Pasteurella and Yersinia (Baskerville et al., 1983; Taffs et al., 1983; Cooper et al., 1976) were not isolated in this study, indicating that the sanitary management is an important approach to maintaining colonies' health (Daszak et al., 2000).

Mycelian fungi were the most frequently retrieved fungal organisms from nasal and oral swabs of the studied tamarins, whilst yeasts were most frequently recovered from rectal samples. Overall, the most frequent fungal genera were Candida (35% of fungal isolates) and Aspergillus (15%), followed by Penicillium and Trichoderma. Fungal infections are generally considered less common than those caused by bacteria, but also have an important role as opportunistic agents and may cause significant impairment or death (Chalmers et al., 1983, Megaki 1986, Kalter 1989, Nordstrom et al., 1989). Candida is well known to be an important inhabitant of the intestinal tract of captive primates, and has been reported to cause glossitis, esophagitis, gastritis and septicaemia (Stone et al., 1974, Chalmers et al., 1983, Nordstrom et al., 1989); it has also been identified in the vaginal microbiota of clinically healthy Black lion tamarins (Moraes et al., 2004). Mycelian fungi are known to be occasionally present in the skin, vagina and intestinal microbiota of free-ranging and captive primates without causing disease [Daniel et al., 1976, Nordstrom et al., 1989, Benno et al., 1987, Moraes et al., 2004], but Aspergillus is recognized to cause respiratory disease in immunologically impaired primates (Migaki, 1986, Haustein et al., 2008).

Little is known about the microbiotal differences among free-ranging and captive primates of the same species, but with different habitats and behaviours there could be differences between the two groups. Diet and habitat, exposure to vaccinations and antibiotics, contact with humans and other non-human primates, increased density of individuals, and poor welfare or stress are also important factors that may affect the microbiotal composition in captive animals (McClure et al., 1980, Rolland et al., 1985, Benno et al., 1987, Lewis et al., 1987, Costa et al., 1989, Bruorton et al., 1991, Bailey and Coe, 2002). In the present study relatively few differences were found in the microbiotal composition of the studied free-ranging and captive lion tamarins; it is unclear if this is occurred because there are no real differences, or if it was only due to small sampling size. The nasal, oral and rectal samples of these animals were similar in the relative proportions of the major bacterial and fungal groups, and had similar composition in terms of most prevalent genera. On the other hand, organisms that are known to be frequently pathogenic such as Aeromonas, Pseudomonas or Klebsiella were either recorded only in captive animals, or were found to be more frequent in those animals. It is not clear, however, if those potential pathogens were human-borne, and future molecular studies should attempt to clarify the phylogenetic origin of these organisms.

The small sample size, limited by the rarity of specimens in captivity and the logistic difficulties of collecting and processing samples from these free-ranging animals, may have restricted the detection of relevant differences among captive and free-ranging animals, as well as among free-ranging tamarins from different conservation areas. Translocations and reintroductions are management strategies that require intensive animal handling and movement, which are stressful conditions that might lead to stress-induced immunosupression and increased occurrence of opportunistic infectious diseases (Fox and Rohovsky, 1975, Ocholi et al., 1989, Bush et al., 1991). Because most of the organisms identified are opportunistically pathogenic under conditions of stress, minimizing stress during all steps of the translocation and reintroduction processes may be relevant. Finally, it is important that a long-term health-monitoring program is established post-release, and any deaths during or after the release process are thoroughly evaluated with pathologic and microbiologic examinations.

Acknowledgments

We are thankful to the field assistants involved in the captures, José Aparecido de Oliveira and José Maria Aragão, and to Dr. Marcos Amaku for the contributions to the manuscript. This study was supported by the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP, 1996/12176-9, 1999/09459-7), Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ, E-26/171.271/2006). We are also thankful to the Greater Los Angeles Zoo Association (GLAZA), the American Society of Primatologist (ASP) and the Instituto Brasileiro do Meio Ambiente e Recursos Naturais Renováveis (IBAMA). José Luiz Catão-Dias is a recipient of a scholarship by the CNPq (301517/2006-1) and Ralph E. T. Vanstreels has a scholarship by FAPESP (2009/53956-9).

Submitted: November 22, 2013

Approved: April 17, 2014.

All the content of the journal, except where otherwise noted, is licensed under a Creative Commons License CC BY-NC.

• Acevedo-Whitehouse K, Duffus AL (2009) Effects of environmental change on wildlife health. Phil Trans R Soc B 364:3429-3438.
• Bailey MT, Coe CL (2002) Intestinal microbial patterns of the common marmoset and rhesus macaque. Comp Biochem Physiol A 133:379-388.
• Barnett JA, Hunter BB (1998) Illustrated genera of imperfect fungi. 4^th ed. Burgess Publishing, Minneapolis.
• Baskerville M, Wood M, Baskerville A (1983) An outbreak of Bordetella bronchiseptica pneumonia in a colony of common marmosets (Callithrix jacchus). Lab Anim 17:350-5.
• Beck BB, Kleiman DG, Dietz JM, Castro I, Carvalho, Martins A, Rettberg-Beck B (1991) Losses and reproduction in reintroduced golden lion tamarins Leontopithecus rosalia Dodo 27:50-61.
• Benno Y, Honjo S, Mitsuoka T (1987) Effect of two-year milk-feeding on gastrointestinal microbiota of the cynomolgus monkey (Macaca fascicularis). Microbiol Immunol 31:943-947.
• Blanco M, Blanco JE, Blanco J, Carvalho VM, Onuma DL, Castro AFP (2004) Typing of intimin (eae) genes in attaching and effacing Escherichia coli strains from monkeys. J Clin Microbiol 42:1382-1383.
• Boever WJ, Wallach JD (1983) Diseases of exotic animals: medical and surgical management. W.B. Saunders, Philadelphia.
• Brown LR, Handler S, Allen SS, Shea C, Wheatcroft MG, Frome WJ (1973). Oral microbial profile of the marmoset. J Dent Res 52:815-822.
• Bruorton MR, Davis CL, Perrin MR (1991) Gut microbiota of vervet and samango monkeys in relation to diet. Appl Environ Microbiol 57:573-578.
• Bush M, Buck BB, Montali RJ (1993). Medical considerations of reintroduction. In: Fowler ME (ed) Zoo and Wild Animals Medicine. 3^rd ed. W.S. Saunders, Denver, pp 24-26.
• Carvalho VM, Gyles CL, Ziebell K, Ribeiro MA, Catão-Dias JL, Sinhorini IL, Otman J, Keller R, Trabulsi LR, Castro AFP (2003) Characterization of monkey Enteropathogenic Escherichia coli (EPEC) and human typical and atypical EPEC serotype isolates from Neotropical nonhuman primates. J Clin Microbiol 41:1225-1234.
• Carvalho VM, Irino K, Onuma D, Castro AFP (2007). Random amplification of polymorphic DNA reveals clonal relationships among enteropathogenic Escherichia coli isolated from non-human primates and humans. Braz J Med Biol Res 40:237-241.
• Carvalho VM, Osugui L, Setzer AP, Lopez RP, Castro AFP, Irino K, Catão-Dias JL (2012) Characterization of extraintestinal pathogenic Escherichia coli isolated from captive wild felids with bacteremia. J Vet Diagn Invest 24:1014-1016.
• Chalmers DT, Murgatroyd LB, Wadsworth PF (1983) A survey of the pathology of marmosets (Callithrix jacchus) derived from a marmoset breeding unit. Lab Anim 17:270-279.
• Chi F, Leider M, Leendertz F, Bergmann C, Christophe B, Schenk S, Pauli G, Ellerbrok H, Hakenbeck R (2007) New Streptococcus pneumoniae clones in deceased wild chimpanzees. J Bacteriol 189:6085-6088.
• Coimbra-Filho AF (1970) Acerca da redescoberta de Leontideus chrysopygus (Mikan, 1823) e apontamentos sobre a sua ecologia (Callitrichidae - Primates). Revta Bras Biol 30:609-615.
• Coimbra-Filho AF (1976) Leontopithecus rosalia chrysopygus (Mikan, 1823), o mico-leão do Estado de São Paulo (Callitrichidae - Primates). Silvicultura 10:1-36.
• Cooper JE, Needham JR (1976) An outbreak of shigellosis in laboratory marmosets and tamarins (Family: Callitrichidae). J Hyg (Cambridge) 76:415-424.
• Costa MA, Mehta T, Males JR (1989) Effects of dietary cellulose, Psyllium husk and cholesterol level on fecal and colonic microbial metabolism in monkeys. J Nutr 119:986-992.
• Cunningham AA (1996) Disease risks of wildlife translocations. Conserv Biol.10:349-353.
• Daniel MD, Fraser CEO, Barahona HH, Hajema EM, Melendez LV (1976). Microbial agents of the owl monkey (Aotus trivirgatus). Lab Anim Sci 26:1073-1078.
• Daszak P, Cunningham AA, Hyatt AD (2000) Emerging infectious diseases of wildlife-threats to biodiversity and human health. Science 287:443-449.
• Fox JG, Rohovsky MW (1975) Meningitis caused by Klebsiella spp. in two rhesus monkeys. J Am Vet Med Assoc 67:634-636.
• Gozalo A, Montoya E (1991). Klebsiella pneumoniae infection in a New World nonhuman primate center. Lab Primate Newsletter 30:13-15.
• Haustein SV, Kolterman AJ, Sundblad JJ, Fechner JH, Knechtle SJ (2008). Nonhuman primate infections after organ transplantation. ILAR J 49:200-219.
• Hill AC, Turton JA, Blesby J (1978) Bacterial and mycoplasma flora of a laboratory colony of the common marmoset (Callithrix jacchus). Vet Rec 23:284-287.
• Holst B, Médici EP, Marino-Filho OJ, Kleiman D, Leus L, Pissinatti A, Vivekananda G, Ballou JD, Traylor-Holzer K, Raboy B, Passos F, Vleeschouwer K, Montenegro MM (2006) Workshop de avaliação de viabilidade populacional e de habitat dos micos-leões, relatório final. IUCN/SSC Conservation Breeding Specialist Group, Apple Valley.
• Hunt RD, Anderson JH, Chalifoux V (1978) Spontaneous infections diseases of marmosets. In: Goldsmith E.Z. (ed) Primates in Medicine. Karger, Basel, pp 245-251.
• Junge RE, Louis EE (2005) Biomedical evaluation of two sympatric lemur species (Propithecus verreauxi deckeni and Eulemur fulvus rufus) in Tsiombokibo Classified Forest, Madagascar. J Zoo Wildl Med 36:581-589.
• Kalter SS (1989) Infectious diseases of nonhuman primates in a zoo settings. Zoo Biol 8:61-76.
• Kierulff MCM, Rylands AB, Mendes SL, Oliveira MM (2008) Leontopithecus chrysopygus In: IUCN Red List of Threatened Species. Available at: www.iucnredlist.org Acessed 14 March 2013.
• Kleiman DG, Rylands AB (2002) Lion Tamarins: biology and conservation. Smithsonian Institute Press, Washington D.C.
• Koneman EW, Roberts GD (1990) Micologia: prática de laboratório. Editorial Medica Panamericana, Buenos Aires.
• Lausen NCG, Richter AG, Lage AL (1986) Pseudomonas aeruginosa infection in squirrel monkeys. J Am Vet Med Assoc 189:1216-1218.
• Lewis DH, Stein RF, McMurray DN (1987) Fecal microbiota of marmosets with wasting marmoset syndrome. Lab Anim Sci 37:103-105.
• Lima DCV, Siqueira DB, Mota RA, Rameh-de-Albuquerque LC, Souza DS, Santos AS, Silva LBG (2012) Microbiology of rectal and otologic swabs of wild carnivores from the Zoo of the Parque Estadual de Dois Irmãos, Pernambuco, Brazil. Pesq Vet Bras 32:159-164.
• Mansfield KG, Lin KC, Xia D, Newman JV, Schauer DB, MacKey J, Lackner AA, Carville A (2001) Enteropathogenic Escherichia coli and ulcerative colitis in cotton-top tamarins (Saguinus oedipus). J Infect Dis 184: 803-7.
• McClure HM, Brodie AR, Anderson DC, Swenson RB (1986) Bacterial infections of nonhuman primates. In: Benirschke K. (ed) Primates: the Road to Selfsustaining Populations. Springer-Verlag, New York, pp 531-549.
• Migaki G (1986) Mycotic infections in nonhuman primates. In: Benirschke K. (ed.), Primates: the road to selfsustaining populations. Springer-Verlag. New York.
• Moraes IA, Stussi JSP, Lilenbaum W, Pissinatti A, Luz FP, Ferreira AMR (2004) Isolation and Identification of fungi from vaginal flora in three species of captive Leontopithecus Am J Primatol 64:337-343.
• Moreira ACA, Carvalho MAR, Cisalpino EO, Damasceno CA, Negrette AC (2003) Cocos gram-positivos anaeróbios estritos da cavidade oral e do trato intestinal de primatas Calitriquídeos (Callithrix jacchus e Callithrix penicillata) mantidos em cativeiro. Revta Cient Med Biol 2:94-103.
• Moreira ACA, Carvalho MAR, Negrette AC, Damasceno CA, Cisalpino EO (2004) Susceptibilidade a antimicrobianos de cocos Gram-positivos anaeróbios estritos isolados em primatas Calitriquídeos (Callithrix penicillata e Callithrix jacchus). Revta Cient Med Biol 3:53-59.
• Nicholson WL (2002) Roles of Bacillus endospores in the environment. Cell Mol Life Sci 59:410-416.
• Nordstrom KM, Belcher AM. Epple G, Greenfield KL, Leyden JJ, Smith III AB (1989) Skin surface microflora of the saddle-back tamarin monkey, Saguinus fuscicollis J. Chem Ecol 15:629-639.
• Ocholi RA, Chima JC, Spencer THI (1989) Concurrent infection of Pata monkey (Erythrocebus patas) by Citrobacter freundii and Trichuris trichura J Wildl Dis 25:124-125.
• Pisharath HR, Cooper TK, Brice AK, Cianciolo RE, Pistorio AL, Wachtman LM, Mankowski JL, Newcomer CE (2005) Septicemia and peritonitis in a colony of common marmosets (Callithrix jacchus) secondary to Klebsiella pneumoniae infection. Contemp Top Lab Anim Sci 44:35-37.
• Rolland RM, Hausfater G, Marshall B, Levy SB (1985) Antibiotic-resistant bacteria in wild primates: increased prevalence in Baboons feeding on human refuse. Appl Environ Microbiol 49:791-794.
• Souza CGV, Olinda RG, Amorim RNL, Oliveira MF, Alves ND, Amóra SSA, Bezerra FSB, Feijó, FMC (2012)Characterization of auricular natural microbiota from captive agoutis (Dasyprocta aguti). Pesq Vet Bras 32:927-930.
• Stone HH, Kolb LD, Currie CA, Geheber CE, Cuzzell JZ (1974) Candida sepsis: Pathogenesis and principles of treatment. Ann Surg 179:697-711.
• Swindle MM, Craft CF, Marriot BM, Stranberg JD (1982) Ascending intrauterine infections in rhesus monkeys. J Am Vet Med Assoc 191:1367-1370.Taffs LF, Dunn G (1983) An outbreak of Yersinia pseudotuberculosis infection in a small indoor breeding colony of red-bellied (Saguinus labiatus) tamarins. Lab Anim 17: 311-20.
• Valladares-Pádua CB, Cullen Jr L (1994) Distribution, abundance and minimum viable metapopulation of the black lion tamarin (Leontopithecus chrysopygus). Dodo 30:80-88.

Publication Dates

• Publication in this collection
  13 Feb 2015
• Date of issue
  Dec 2014

History

• Accepted
  17 Apr 2014
• Received
  22 Nov 2013