Assessing the impact of preventative measures to limit the spread of Toxoplasma gondii in wild carnivores of Madagascar.

Novel multihost pathogens can threaten endangered wildlife species, as well as humans and domestic animals. The zoonotic protozoan parasite Toxoplasma gondii is transmitted by members of Felidae and can infect a large number of animal species, including humans. This parasite can have significant health consequences for infected intermediate hosts and could further endanger wild carnivore populations of Madagascar. Building on an empirical characterization of the prevalence of the pathogen in local mammals, we used mathematical models of pathogen transmission in a multihost community to compare preventative measures that aim to limit the spread of this parasite in wild carnivores. Specifically, we examined the effect of hypothetical cat vaccination and population control campaigns on reducing the risk of infection by T. gondii in wild Eupleridae. Our model predicted that the prevalence of exposure to T. gondii in cats would be around 72% and that seroprevalence would reach 2% and 43% in rodents and wild carnivores, respectively. Reducing the rodent population in the landscape by half may only decrease the prevalence of T. gondii in carnivores by 10%. Similarly, cat vaccination and reducing the population of definitive hosts had limited impact on the prevalence of T. gondii in wild carnivorans of Madagascar. A significant reduction in prevalence would require extremely high vaccination, low turnover, or both in the cat population. Other potential control methods of T. gondii in endangered Eupleridae include targeted vaccination of wild animals but would require further investigation. Eliminating the threat entirely will be difficult because of the ubiquity of cats and the persistence of the parasite in the environment.

Evaluación del impacto de las medidas preventivas para limitar el contagio de Toxoplasma gondii en los carnívoros silvestres de Madagascar Resumen Los patógenos novedosos con múltiples hospederos pueden amenazar tanto a las especies silvestres como a los humanos y a los animales domésticos. Los miembros de la familia Felidae transmiten el protozoario parásito Toxoplasma gondii, el cual puede infectar a un gran número de especies animales, incluyendo al humano. Este parásito puede generar consecuencias importantes para la salud en los hospederos intermediarios infectados y podría poner más en peligro a las poblaciones de carnívoros silvestres de Madagascar. Usamos modelos matemáticos de la transmisión de patógenos en una comunidad con múltiples hospederos a partir de una caracterización empírica de la prevalencia del patógeno en los mamíferos locales para comparar las medidas preventivas que buscan limitar la transmisión de este parásito en los carnívoros silvestres. En específico, examinamos el efecto de la vacunación hipotética de felinos y las campañas de control poblacional sobre la reducción del riesgo de infección de T. gondii en los Eupleridae silvestres. Nuestro modelo predijo que la prevalencia de la exposición a T. gondii en los felinos sería de un 72% y que la seroprevalencia llegaría al 2% y al 43% en los roedores y carnívoros silvestres, respectivamente. La reducción a la mitad de la población de roedores en el paisaje podría disminuir sólo en un 10% la prevalencia del protozoario en los carnívoros. De forma similar, la vacunación y la reducción de la población de hospederos definitivos tuvieron un impacto limitado sobre la prevalencia de T. gondii en los carnívoros silvestres de Madagascar. Una reducción significativa en la prevalencia requeriría que la población de felinos tuviera una vacunación extremadamente elevada, baja rotación, o ambas. Otros métodos potenciales de control de T. gondii en los Eupleridae incluyen la vacunación de animales silvestres, pero requieren de mayor investigación. La eliminación completa de la amenaza será difícil por la ubicuidad de los felinos y la persistencia del parásito en el ambiente.

Pathogenic enterobacteria in lemurs associated with anthropogenic disturbance.

As human population density continues to increase exponentially, speeding the reduction and fragmentation of primate habitat, greater human-primate contact is inevitable, making higher rates of pathogen transmission likely. Anthropogenic effects are particularly evident in Madagascar, where a diversity of endemic lemur species are threatened by rapid habitat loss. Despite these risks, knowledge of how anthropogenic activities affect lemur exposure to pathogens is limited. To improve our understanding of this interplay, we non-invasively examined six species of wild lemurs in Ranomafana National Park for enteric bacterial pathogens commonly associated with diarrheal disease in human populations in Madagascar. Patterns of infection with Enterotoxigenic Escherichia coli, Shigella spp., Salmonella enterica, Vibrio cholerae, and Yersinia spp. (enterocolitica and pseudotuberculosis) were compared between lemurs inhabiting intact forest and lemurs inhabiting degraded habitat with frequent exposure to tourism and other human activity. Fecal samples acquired from humans, livestock, and rodents living near the degraded habitat were also screened for these bacteria. Remarkably, only lemurs living in disturbed areas of the park tested positive for these pathogens. Moreover, all of these pathogens were present in the human, livestock, and/or rodent populations. These data suggest that lemurs residing in forests altered or frequented by people, livestock, or peridomestic rodents, are at risk for infection by these diarrhea-causing enterobacteria and other similarly transmitted pathogens.

Biomedical evaluation of Verreaux's sifaka (Propithecus verreauxi) from Kirindy Mitea National Park in Madagascar.

Evaluation of the health, prevalence, and incidence of diseases in wild populations is a critical component of wildlife management. In addition, the establishment of reference physiologic parameters can Verreaux's sifaka (Propithecus verreauxi) from Kirindy Mitea National Park, Madagascar, during two field captures incontribute to the assessment of population risks. Complete medical evaluations were performed on 33 wild June 2010 and June 2011. Each animal received a complete physical examination: weight, body temperature, heart rate, and respiratory rate were recorded, and ectoparasites collected. Blood samples were collected for complete blood cell count, differential white blood cell count, hemoparasite examination, serum biochemical profile, fat-soluble vitamin analysis, trace mineral analysis, and toxoplasmosis and viral serology. Fecal samples were collected for bacterial culture and endoparasite examination. Significant differences exist between age classes for neutrophil and lymphocyte count, alkaline phosphatase, and creatinine values. Parasites detected were Callistoura sp., Bertiella lemuriformis, and Dipetalonema petteri. This publication reports the first complete biomedical evaluation of the P. verreauxi and provides a basis for hematologic and biochemical comparisons of P. verreauxi in the wild.

A 12-month survey of gastrointestinal helminth infections of lemurs kept in two zoos in Madagascar.

Infections with gastrointestinal parasites may be a major threat to lemurs kept in captivity, as they are a common cause of diarrhea. In this study, fecal egg count patterns and clinical signs associated with gastrointestinal nematodes were assessed for 12 mo in 40 lemurs kept under different husbandry and climatic conditions at two sites in Madagascar. Involved species were black-and-white ruffed lemurs (Varecia variegata), eastern grey bamboo lemurs (Hapalemur griseus), greater bamboo lemurs (Prolemur simus), red-bellied lemurs (Eulemur rubriventer), common brown lemurs (Eulemurfulvus), crowned lemurs (Eulemur coronatus), and Sclater's black lemurs (Eulemur macaco flavifrons). At site 1 (Tsimbazaza Zoological Park), lemurs were kept in small enclosures with daily cleaning of the cement soiling and without routine anthelmintic program, whereas at site 2 (Ivoloina Zoological Park), lemurs received routine anthelmintic prophylaxis and were housed in small enclosure with daily cleaning of sandy soil enclosures. A total of five genera of nematode eggs from the orders Strongylida, Oxyurida, and Enoplida were recovered and identified from 198 out of 240 samples (83%) at site 1 and 79% (189 out of 240) at site 2 with the use of a modified McMaster technique. Significant differences were found for parasites from the order Strongylida between the two sites. The differences may be due to climate conditions and the presumed life cycle of these parasites. No significant differences were found for parasites from the other orders. No significant differences were noted between sexes or between seasons. No clinical signs of parasitic gastroenteritis were seen in either lemur collection.

Comparison of biomedical evaluation for white-fronted brown lemurs (Eulemur fulvus albifrons) from four sites in Madagascar.

Health and nutritional assessments of wildlife are important management tools and can provide a means to evaluate ecosystem health. Such examinations were performed on 37 white-fronted brown lemurs (Eulemur fulvus albifrons) from four sites in Madagascar. Comparison of health parameters between sites revealed statistically significant differences in body weight, body temperature, respiratory rate, hematology parameters (white cell count, hematocrit, segmented neutrophil count, and lymphocyte count), serum chemistry parameters (aspartate aminotransferase, alanine aminotransferase, serum alkaline phosphatase, total protein, albumin, phosphorus, calcium, sodium, chloride, and creatinine phosphokinase), and nutrition parameters (copper, zinc, ferritin, retinol, tocopherol, and 25-hydroxycholecalciferol). Two of 10 lemurs tested were positive for toxoplasmosis; none of 10 were positive for Cryptosporidium or Giardia. Enteric bacteria and endo- and ectoparasites were typical. Statistically different values in hematology and chemistry values probably do not reflect clinically significant differences, whereas nutrition parameter differences are likely related to season, soil, and forage availability.

PREVALENCE OF ANTIBODIES TO SELECTED VIRUSES AND PARASITES IN INTRODUCED AND ENDEMIC CARNIVORES IN WESTERN MADAGASCAR.

Introduced animals impact endemic populations through predation, competition, and disease transmission. Populations of endemic carnivores in Madagascar are declining, and pathogens transmitted from introduced species may further endanger these unique species. We assessed the exposure of introduced and endemic carnivores to common viral and parasitic pathogens in two national parks of Madagascar (Kirindy Mitea National Park and Ankarafantsika National Park) and their neighboring villages. We also identified variables associated with the presence of antibodies to these pathogens in fosa ( Cryptoprocta ferox ). Introduced and endemic species were exposed to canine parvovirus, canine herpesvirus, feline calicivirus, and Toxoplasma gondii . Domestic dogs ( Canis familiaris ) and cats ( Felis catus ) may be sources of infection for these pathogens. Prevalence of antibodies to Toxoplasma in captured fosa was >93%, and adults were more likely to be exposed than immature individuals. Our data provide a basis upon which to evaluate and manage risks of pathogen transmission between species.

Epidemiology of pathogenic enterobacteria in humans, livestock, and peridomestic rodents in rural Madagascar.

BACKGROUND: Among the families of enteric bacteria are globally important diarrheal agents. Despite their potential for zoonotic and environmental transmission, few studies have examined the epidemiology of these pathogens in rural systems characterized by extensive overlap among humans, domesticated and peridomestic animals. We investigated patterns of infection with Enterotoxigenic Escherichia coli, Shigella spp., Salmonella enterica, Vibrio cholerae, and Yersinia spp. (enterocolitica, and pseudotuberculosis) in Southeastern Madagascar where the potential for the aforementioned interactions is high. In this pilot project we conducted surveys to examine behaviors potentially associated with risk of infection and if infection with specific enterobacteria species was associated with diarrheal disease. METHODOLOGY/PRINCIPAL FINDINGS: PCR was conducted on DNA from human, livestock, and rodent fecal samples from three villages. Overall, human prevalence was highest (77%), followed by rodents (51%) and livestock (18%). Rodents were ∼2.8 times more likely than livestock to carry one of the bacteria. The incidence of individual species varied between villages, with the observation that, E. coli and Shigella spp. were consistently associated with co-infections. As an aggregate, there was a significant risk of infection linked to a water source in one village. Individually, different pathogens were associated with certain behaviors, including: those who had used medication, experienced diarrhea in the past four weeks, or do not use toilets. CONCLUSIONS/SIGNIFICANCE: Different bacteria were associated with an elevated risk of infection for various human activities or characteristics. Certain bacteria may also predispose people to co-infections. These data suggest that a high potential for transmission among these groups, either directly or via contaminated water sources. As these bacteria were most prevalent in humans, it is possible that they are maintained in humans and that transmission to other species is infrequent. Further studies are needed to understand bacterial persistence, transmission dynamics, and associated consequences in this and similar systems.

Survey of Giardia and Cryptosporidium in lemurs from the Ranomafana National Park, Madagascar.

We detected Cryptosporidium sp. by direct immunofluorescence in fecal samples from greater bamboo lemurs (Prolemur simus) and eastern rufous mouse lemurs (Microcebus rufus) inhabiting the Ranomafana National Park, Madagascar. This is the first report of an occurrence of these potentially zoonotic parasites in free-ranging lemurs in the rain forest of Madagascar.