Gastrointestinal parasites of Leontopithecus chrysomelas in the Atlantic Forest, Brazil.

We performed coproparasitological testing of free-living golden-headed lion tamarins, Leontopithecus chrysomelas, using the Hoffmann-Pons-Janner method. In total, we collected 118 samples from ten groups: four living in Federal Protected Area and six living in Non-Protected Areas of cocoa farms. Eggs from parasites of the Acanthocephala phylum and Spiruridae, Ancylostomatidae, Ascarididae and Oxyuridae families were identified, as well as the genus Strongyloides (Nematode: Strongyloididae) and phylum Apicomplexa. This is the first description of infection with coccidian, Trichuridae family and Strongyloides spp. in L. chrysomelas. A total of 48% (n= 57) of the animals were infected and the highest prevalence (37.2±SD 8.72, n = 44) was for Acanthocephalidae, followed by Spiruridae (8.5±SD 5.03, n = 10). There was no difference in parasite prevalence by age classes or sex. However, we found higher diversity and prevalence of parasites in animals living in the Federal Protected Area. These results suggest that intestinal parasites may be influenced by environmental factors, such as the management of the areas where the animals live, in addition to the feeding behavior of L. chrysomelas and distinct transmission strategies of parasites. The combination of ecological and demographic data combined with parasitological studies may contribute to conservation programs for this species.

Gastrointestinal parasites of Leontopithecus chrysomelas in the Atlantic Forest, Brazil / Parasitas gastrintestinais de Leontopithecus chrysomelas na Floresta Atlântica, Brasil

Abstract We performed coproparasitological testing of free-living golden-headed lion tamarins, Leontopithecus chrysomelas, using the Hoffmann-Pons-Janner method. In total, we collected 118 samples from ten groups: four living in Federal Protected Area and six living in Non-Protected Areas of cocoa farms. Eggs from parasites of the Acanthocephala phylum and Spiruridae, Ancylostomatidae, Ascarididae and Oxyuridae families were identified, as well as the genus Strongyloides (Nematode: Strongyloididae) and phylum Apicomplexa. This is the first description of infection with coccidian, Trichuridae family and Strongyloides spp. in L. chrysomelas. A total of 48% (n= 57) of the animals were infected and the highest prevalence (37.2±SD 8.72, n = 44) was for Acanthocephalidae, followed by Spiruridae (8.5±SD 5.03, n = 10). There was no difference in parasite prevalence by age classes or sex. However, we found higher diversity and prevalence of parasites in animals living in the Federal Protected Area. These results suggest that intestinal parasites may be influenced by environmental factors, such as the management of the areas where the animals live, in addition to the feeding behavior of L. chrysomelas and distinct transmission strategies of parasites. The combination of ecological and demographic data combined with parasitological studies may contribute to conservation programs for this species.

Resumo Foram realizados testes coproparasitológicos de micos-leões-dourados de vida livre, Leontopithecus chrysomelas, usando-se o método de Hoffmann-Pons-Janner. No total, foram coletadas 118 amostras de dez grupos: quatro grupos residentes em Área de Conservação Federal e seis grupos em Área não protegida de fazendas de cacau. Ovos de parasitas do filo Acantocephala e das famílias Spiruridae, Ancylostomatidae, Ascarididae, Oxyuridae foram identificados, bem como o gênero Strongyloides (Nematoda: Strongyloididae) e o filo Apicomplexa. Esta é a primeira descrição de infecção de coccídeos, família Trichuridae e Strongyloides spp. em L. chrysomelas. Um total de 48% (n = 57) dos animais estavam parasitados e a maior prevalência (37,2 ±DP 8,72, n = 44) foi para Acanthocephalan, seguido por Spiruridae (8,5±DP 5,03, n = 10). Não houve diferença na prevalência do táxon de parasita por idade ou sexo. No entanto, foi encontrada maior diversidade e prevalência de parasitas em animais que vivem na Unidade de Conservação Federal. Esses resultados sugerem que os parasitas intestinais podem ser influenciados por fatores ambientais, como o manejo das áreas, além do comportamento alimentar de L. chrysomelas e distintas estratégias de transmissão dos parasitas. A combinação de dados ecológicos e demográficos com estudos parasitológicos podem contribuir para programas de conservação dessa espécie.

Pterygodermatites nycticebi infections in golden lion tamarins (Leontopithecus rosalia rosalia) and aye-ayes (Daubentonia madagascariensis) from a German zoo.

In a golden lion tamarin (Leontopithecus rosalia rosalia) colony kept indoors in a German zoo, two animals presented a sudden onset of reduced general condition, lethargy, and diarrhea. At animal capture for clinical examination, adult nematode stages were observed after stress-induced defecation. Despite treatment, two golden lion tamarins died in the following 2 days. At necropsy, spirurid stages were found in the lungs and intestine. Additionally, adult Pterygodermatites spp. were identified in histopathological samples of intestine and pancreas, confirming the previous diagnosis. Upon diagnosis, all animals were treated with ivermectin (0.2 mg/kg; SC). Thereafter, the general condition of the golden lion tamarins improved, whereby some of them excreted spirurid nematodes over 3 days. Four weeks after treatment, 20 fecal samples from the colony were examined and proved negative for parasitic stages. Given that common German cockroaches (Blattella germanica) are suitable intermediate hosts of Pterygodermatites nycticebi, 30 specimens were collected from seven different locations around the golden lion tamarins housing. Third-stage larvae of Pterygodermatites spp. were recovered from those cockroaches. Regular anthelmintic treatments, coprological screenings, and controls for intermediate hosts were recommended. More than 2 years later, P. nycticebi infection was diagnosed again histopathologically in an aye-aye (Daubentonia madagascariensis) which suddenly died. Coprological analysis confirmed the presence of spirurid eggs. Due to prosimian primates' cockroach-eating habits and given that total cockroach eradication proved impossible, continuous cockroach control strategies and regular treatments of primates are currently performed to prevent further P. nycticebi infections.

Individual behavioral differences and health of golden-headed lion tamarins (Leontopithecus chrysomelas).

Individual behavioral differences may influence how animals cope with altered environments. Depending on their behavioral traits, individuals may thus vary in how their health is affected by environmental conditions. We investigated the relationship between individual behavior of free-living golden-headed lion tamarins (Leontopithecus chrysomelas) responding to a novel object (to assess exploration-avoidance), and their habitat use and health status (endoparasitism; clinical measures: biometric data, heart rate, respiratory frequency, and temperature; fecal glucocorticoid metabolites). As parasite transmission can be affected by individual variation in social contact and social grooming, we also evaluated whether more sociable individuals show higher endoparasite loads compared with less sociable animals. Four groups living in landscapes with different levels of human disturbance were investigated: two in degraded forest fragments in an agricultural matrix (DFAM-higher disturbance), and two in a cocoa agroforestry system (cabruca-lower disturbance) in the Atlantic forest of South Bahia, Brazil. Using a subjective ratings approach, highly correlated adjective descriptors were combined to produce z-score ratings of one derived variable ("confidence"), which was selected to characterize the tamarins' exploration/avoidance responses during a novel object test. The higher the confidence score, the longer female tamarins spent foraging for prey independent of landscape, and the greater their body mass independent of sex and landscape. Only DFAM individuals showed intestinal parasite infection. Endoparasite loads were positively correlated with the number of grooming partners, suggesting an association between social grooming and transmission (more groomers = more endoparasites). Individual behavior, including in a test situation, may thus have some predictive value for behavior in a free-living context, and for its health consequences.

Lineage-specific serology confirms Brazilian Atlantic forest lion tamarins, Leontopithecus chrysomelas and Leontopithecus rosalia, as reservoir hosts of Trypanosoma cruzi II (TcII).

BACKGROUND: Trypanosoma cruzi, the agent of Chagas disease in humans, has a vast reservoir of mammalian hosts in the Americas, and is classified into six genetic lineages, TcI-TcVI, with a possible seventh, TcBat. Elucidating enzootic cycles of the different lineages is important for understanding the ecology of this parasite, the emergence of new outbreaks of Chagas disease and for guiding control strategies. Direct lineage identification by genotyping is hampered by limitations of parasite isolation and culture. An indirect method is to identify lineage-specific serological reactions in infected individuals; here we describe its application with sylvatic Brazilian primates. METHODS: Synthetic peptides representing lineage-specific epitopes of the T. cruzi surface protein TSSA were used in ELISA with sera from Atlantic Forest Leontopithecus chrysomelas (golden-headed lion tamarin), L. rosalia (golden lion tamarin), Amazonian Sapajus libidinosus (black-striped capuchin) and Alouatta belzebul (red-handed howler monkey). RESULTS: The epitope common to lineages TcII, TcV and TcVI was recognised by sera from 15 of 26 L. chrysomelas and 8 of 13 L. rosalia. For 12 of these serologically identified TcII infections, the identity of the lineage infection was confirmed by genotyping T. cruzi isolates. Of the TcII/TcV/TcVI positive sera 12 of the 15 L. chrysomelas and 2 of the 8 L. rosalia also reacted with the specific epitope restricted to TcV and TcVI. Sera from one of six S. libidinous recognised the TcIV/TcIII epitopes. CONCLUSIONS: This lineage-specific serological surveillance has verified that Atlantic Forest primates are reservoir hosts of at least TcII, and probably TcV and TcVI, commonly associated with severe Chagas disease in the southern cone region of South America. With appropriate reagents, this novel methodology is readily applicable to a wide range of mammal species and reservoir host discovery.

Occurrence of Prosthenorchis elegans in Free-living Primates from the Atlantic Forest of Southern Bahia, Brazil.

Parasite prevalence and abundance are important factors affecting species' conservation. During necropsies on a free-living golden-headed lion tamarin ( Leontopithecus chrysomelas ) and two Wied's marmosets ( Callithrix kuhlii ) in the Atlantic Forest of southern Bahia, Brazil, we collected a large number of adult intestinal parasites that we identified as Prosthenorchis elegans. This parasite is pathogenic for neotropical primates. Prosthenorchis spp. infestation is influenced by diet with increased risk of exposure from ingesting invertebrate intermediate hosts. The biological similarities and sympatric nature of these two nonhuman primates support that they may harbor similar infectious and parasitic agents.

Survey of Plasmodium in the golden-headed lion tamarin (Leontopithecus chrysomelas) living in urban Atlantic forest in Rio de Janeiro, Brazil.

BACKGROUND: Communicating the presence of potential zoonotic pathogens such as Plasmodium spp. in wild animals is important for developing both animal and human health policies. METHODS: The translocation of an exotic and invasive population of Leontopithecus chrysomelas (golden-headed lion tamarins) required the screening of these animals for specific pathogens. This studies objective was to investigate Plasmodium spp. infection in the L. chrysomelas, both to know its prevalence in these animals in the local area and to minimize the risk of pathogens being translocated to the destination site. To investigate Plasmodium spp. infection, blood samples from 268 animals were assessed for the presence of Plasmodium spp. by genus-specific PCR and stained thick and thin blood smears were examined by light microscopy. Data of human malaria infection in the studied region was also assembled from SINAN (Diseases Information System Notification-Ministry of Health of Brazil). RESULTS: Results from the PCR and microscopy were all negative and suggested that no L. chrysomelas was infected with Plasmodium spp. Analysis of SINAN data showed that malaria transmission is present among the human population in the studied region. CONCLUSIONS: This study is the first to provide information on Plasmodium spp. infection in L. chrysomelas. Plasmodium spp. infection of this species is rare or absent though malaria parasites circulate in the region. In addition, there is minimal risk of translocating Plasmodium spp. infected animals to the destination site.

Infection with Trypanosoma cruzi TcII and TcI in free-ranging population of lion tamarins (Leontopithecus spp): an 11-year follow-up.

Here, we present a review of the dataset resulting from the 11-years follow-up of Trypanosoma cruzi infection in free-ranging populations of Leontopithecus rosalia (golden lion tamarin) and Leontopithecus chrysomelas (golden-headed lion tamarin) from distinct forest fragments in Atlantic Coastal Rainforest. Additionally, we present new data regarding T. cruzi infection of small mammals (rodents and marsupials) that live in the same areas as golden lion tamarins and characterisation at discrete typing unit (DTU) level of 77 of these isolates. DTU TcII was found to exclusively infect primates, while TcI infected Didelphis aurita and lion tamarins. The majority of T. cruzi isolates derived from L. rosalia were shown to be TcII (33 out 42) Nine T. cruzi isolates displayed a TcI profile. Golden-headed lion tamarins demonstrated to be excellent reservoirs of TcII, as 24 of 26 T. cruzi isolates exhibited the TcII profile. We concluded the following: (i) the transmission cycle of T. cruzi in a same host species and forest fragment is modified over time, (ii) the infectivity competence of the golden lion tamarin population fluctuates in waves that peak every other year and (iii) both golden and golden-headed lion tamarins are able to maintain long-lasting infections by TcII and TcI.

Infection with Trypanosoma cruzi TcII and TcI in free-ranging population of lion tamarins (Leontopithecus spp): an 11-year follow-up

Here, we present a review of the dataset resulting from the 11-years follow-up of Trypanosoma cruzi infection in free-ranging populations of Leontopithecus rosalia (golden lion tamarin) and Leontopithecus chrysomelas (golden-headed lion tamarin) from distinct forest fragments in Atlantic Coastal Rainforest. Additionally, we present new data regarding T. cruzi infection of small mammals (rodents and marsupials) that live in the same areas as golden lion tamarins and characterisation at discrete typing unit (DTU) level of 77 of these isolates. DTU TcII was found to exclusively infect primates, while TcI infected Didelphis aurita and lion tamarins. The majority of T. cruzi isolates derived from L. rosalia were shown to be TcII (33 out 42) Nine T. cruzi isolates displayed a TcI profile. Golden-headed lion tamarins demonstrated to be excellent reservoirs of TcII, as 24 of 26 T. cruzi isolates exhibited the TcII profile. We concluded the following: (i) the transmission cycle of T. cruzi in a same host species and forest fragment is modified over time, (ii) the infectivity competence of the golden lion tamarin population fluctuates in waves that peak every other year and (iii) both golden and golden-headed lion tamarins are able to maintain long-lasting infections by TcII and TcI.

Genotype variation of Trypanosoma cruzi isolates from different Brazilian biomes.

Chagas disease is an enzootic disease, in which the flagellate Trypanosoma cruzi infects a large variety of animals. Humans are accidentally infected due to the migration into wild environments. To identify T. cruzi discrete typing units (DTUs), 19 Brazilian isolates from different biomes and hosts were analyzed by PCR amplification of 24Sα rRNA, 18S rRNA and mini-exon gene sequences. The majority of the isolates was classified as TcIIb (TcII) but subtypes TcIIc (TcIII) and TcIId (TcV) were also identified. In addition, in monkeys TcI was detected.

Ocorrência de Acanthocephala em Leontopithecus (Lesson, 1840), cativos: aspectos clínico-patológicos. Callitrichidae-Primates / Acanthocephala infections in captives lion tamarins Leontopithecus (Lesson, 1840): clinical pathologic aspects. Callitrichidae-Primates

Estudaram-se achados de necropsia de 454 espécimens de Leontopithecus. Quatorze (3,1 por cento) apresentaram-se infectados por acantocéfalos intestinais identificados como Prosthenorchis elegans (Diesing, 1861). Não foram observadas diferenças na ocorrência do parasito quanto à espécie, origem - cativos ou selvagens - e sexo. Clinicamente os animais apresentaram-se com o pelame eriçado, apatia, inapetência, dores abdominais e diarréia. Em dois animais parasitados (14,2 por cento), observou-se perfuração da parede intestinal. As lesões encontradas caracterizaram-se por uma grave enterite ulcerativa. A ocorrência desses parasitos reforça a necessidade do estabelecimento de protocolos sanitários rígidos no manejo das espécies de primatas do neotrópico

This study assessed the autopsy findings of 454 Leontopithecus specimens, 14 of which (3.1 percent) were infected by intestinal Acanthocephala identified as Prosthenorchis elegans (Diesing, 1861). No difference in the occurrence of the parasite was observed regarding the species, origin (captive or wild) and sex of the lion tamarins. Clinically, the animals had spiked coat, apathy, inappetence, abdominal pain and diarrhea. Two of the parasitized animals (14.2 percent) had perforation of the intestinal wall. The lesions found were characterized as a severe ulcerative enteritis. The occurrence of such parasites highlights the need for establishing strict sanitary protocols for the management of the neotropical primate species

Parasite community interactions: Trypanosoma cruzi and intestinal helminths infecting wild golden lion tamarins Leontopithecus rosalia and golden-headed lion tamarins L. chrysomelas (Callitrichidae, L., 1766).

The parasite prevalence and infection intensity in primate wild populations can be affected by many variables linked to host and/or parasite ecology or either to interparasite competition/mutualism. In this study, we tested how host sex, age, and place of origin, as well parasitic concomitant infections affect the structure of golden lion and golden-headed lion tamarins parasite community, considering Trypanosoma cruzi and intestinal helminths infection in these primates. A total of 206 tamarins from two Atlantic Coastal rain forest areas in Brazil were tested during 4 years for prevalence of T. cruzi infection and helminth prevalence. Three intestinal helminth groups showed high prevalences in both tamarin species: Prosthenorchis sp., Spiruridae, and Trichostrongylidae. An association between presence of T. cruzi infection and higher intestinal helminth prevalence was found in both tamarin species. Two explanations for this association seem to be plausible: (1) lower helminth-linked mortality rates in T. cruzi-infected tamarins and (2) lower elimination rates of helminths in such tamarins. A higher frequency of T. cruzi-positive blood cultures was significantly correlated to female tamarins and to the presence of Trichostrongylidae infection. The possibility of an increase in the transmissibility of T. cruzi and the three analyzed helminths in lion tamarins with concomitant infections is discussed.

Prevalence and intensity of intestinal helminths found in free-ranging golden lion tamarins (Leontopithecus rosalia, Primates, Callitrichidae) from Brazilian Atlantic forest.

Helminth identification and egg counts were performed in 316 fecal samples during 4 years in 199 golden lion tamarins (GLTs), Leontopithecus rosalia, from two Brazilian conservation units. Tamarin sex and age, area of occurrence and helminth co-infection were tested as potential factors that could affect helminth prevalence and egg shedding in host individuals. Three nematodes species were found at low prevalences but not in both conservation units: Ancylostomatidae (12%), Ascarididae (1%) and Tripanoxyuris minutus, an Oxyuridae (4%). Three other species had high prevalences and were found in both conservation units: one acanthocephalan, Oncicola sp. (30%), and two nematodes, Spiruridae (24%), and Trichostrongylidae (31%). These three latter helminths had distinct prevalences between the conservation units, probably due to differences in availability of helminth infective stages in each area. Prevalences were greater in females for all helminth species; this was especially the case for Oncicola sp. Sex and age differences in helminth prevalence may be associated with changes in sexual steroid levels that accompany age and reproductive status. Frequency of simultaneous infections by the two helminths considered most pathogenic (Oncicola and Trichostrongylidae) were statistically lower than expected; this may be related to: (i) higher tamarin death rate caused by the association; (ii) differences in exposure to helminth infective stages in the various areas of occurrence; (iii) and competition between these helminth species. All helminth species followed a negative binomial distribution, with stronger clumping occurring in Trichostrongylidae and in female GLTs. Distinct transmission strategies of Oncicola sp. and Spiruridae, in contrast with Trichostrongylidae, may partially explain the different clumping levels of these helminths in GLTs. Mean fecal egg counts of all helminths were not different between GLT sexes, ages or areas of occurrence. The three most common helminth species may be a threat to isolated or dense GLT populations.

Clinical, biochemical, and electrocardiographic aspects of Trypanosoma cruzi infection in free-ranging golden lion tamarins (Leontopithecus rosalia).

BACKGROUND: Wild golden lion tamarins from the Biological Reserve of Poço das Antas, Rio de Janeiro, Brazil, have high prevalence of Trypanosoma cruzi infection leading us to clinically assess the disease in this endangered species. METHODS: 34 tamarins were sampled for the presence of T. cruzi infection (through serology) and clinical evaluation (electrocardiography, blood counts and biochemical analysis). RESULTS: 32% of the sampled tamarins were T. cruzi positive, 45% of these displayed cardiac abnormalities. Main cardiac abnormality in infected tamarins was T wave low voltage; R wave low voltage and V3S wave high voltage were also found. The tamarins displaying T wave low voltage had high proportion of seric cardiac creatine kinase. Seric mean total protein was significantly higher in infected tamarins. CONCLUSIONS: Sampled tamarins displayed typical signs of T. cruzi infection, similar to experimentally infected primates and human natural infection. Potential risk of T. cruzi infection to this endangered species is discussed.