SEROLOGIC EVIDENCE OF TOXOPLASMA GONDII INFECTION IN WILD BIRDS AND MAMMALS FROM SOUTHEAST BRAZIL Author(s): Sérgio Netto Vitaliano, D.V.M., Ph.D., Herbert Sousa Soares, D.V.M., Hilda Fátima de Jesus Pena, D.V.M., Ph.D., Jitender Prakash Dubey, M.V.Sc., Ph.D. and Solange Maria Gennari, D.V.M., Ph.D. Source: Journal of Zoo and Wildlife Medicine, 45(1):197-199. 2014. Published By: American Association of Zoo Veterinarians DOI: http://dx.doi.org/10.1638/2013-0179R.1 URL: http://www.bioone.org/doi/full/10.1638/2013-0179R.1
BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/ terms_of_use. Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder.
BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research.
Journal of Zoo and Wildlife Medicine 45(1): 197–199, 2014 Copyright 2014 by American Association of Zoo Veterinarians
SEROLOGIC EVIDENCE OF TOXOPLASMA GONDII INFECTION IN WILD BIRDS AND MAMMALS FROM SOUTHEAST BRAZIL Se´rgio Netto Vitaliano, D.V.M., Ph.D., Herbert Sousa Soares, D.V.M., Hilda Fa´tima de Jesus Pena, D.V.M., Ph.D., Jitender Prakash Dubey, M.V.Sc., Ph.D., and Solange Maria Gennari, D.V.M., Ph.D.
Abstract: In this study, serum samples of 53 wild animals from two different states from the southeast region of Brazil were analyzed for the presence of anti–Toxoplasma gondii antibodies by the modified agglutination test (MAT), with a cut-off of 1 : 5 for birds and of 1 : 25 for mammals. Out of the sampled animals, 27 were birds and 26 were mammals, and from this total, 83% (n ¼ 44) were free-living animals. Antibodies were found in 13 mammals, from which 11 were free-living animals, and in five birds, all of which were free-living. In this study, T. gondii antibodies were detected in four bird species (crested seriema, Cariama cristata; buff-necked ibis, Theristicus caudatus; picazuro pigeon, Patagioenas picazuro; and burrowing owl, Athene cunicularia) and in a giant anteater (Myrmecophaga tridactyla) for the first time. Key words: Antibodies, Brazil, modified agglutination test, Toxoplasma gondii, wild birds, wild mammals.
BRIEF COMMUNICATION Toxoplasma gondii is an intracellular protozoan parasite capable of infecting several species of warm-blooded animals, including humans. Its infection is widely prevalent worldwide, particularly in Brazil, where up to 90% of humans have been exposed to this parasite, and it is transmitted by the ingestion of oocysts present in the environment, by the consumption of bradyzoites present in tissue of infected intermediate hosts, and by the transplacental transmission of tachyzoites.4 In animals, the interest in the evaluation of toxoplasmosis occurrence is greater in species that cohabitate with humans or in species that can serve as a food source as a result of the possibility of human infection.10 The pathogenicity of T. gondii can display great variation within various animal species.3 In the most susceptible species, such as Australian marsupials, New World monkeys, and penguins, the acute disease is normally fatal,8 while in the most resistant species the infection is normally mild and unspecific, with From Faculdade de Medicina Veterina´ria e Zootecnia da Universidade de Sao ˜ Paulo, Avenida Professor Doutor Orlando Marques de Paiva, 87, 05508-270, Cidade Universita´ria, Sao ˜ Paulo/SP, Brazil (Vitaliano, Soares, Pena, Gennari); Curso de Medicina Veterina´ria das Faculdades Metropolitanas Unidas (UniFMU), Rua Ministro Nelson Hungria, 541, 05690-050 Real Parque/ Morumbi, Sao ˜ Paulo/SP, Brazil (Vitaliano); and the U.S. Department of Agriculture, Agricultural Research Service, Beltsville Agricultural Research Center, Animal Parasitic Diseases Laboratory, Beltsville, Maryland 20705, USA (Dubey). Correspondence should be directed to Dr. Gennari ([email protected]).
some cases having no sign of clinical infection despite the seroconversion and the presence of the parasite in those animal tissues.11 Although studies indicate that wild animals are frequently positive for T. gondii antibodies,1,9,12 the role of wildlife in the epidemiology of this parasite is not well understood, nor is the susceptibility of different wild species.7 In the present article, free-living and captive wild animals from Minas Gerais and Sao ˜ Paulo states in the southeast region of Brazil were assayed for the presence of T. gondii antibodies. The animals originated from 10 different municipalities, and partners in two different public institutions gathered the samples. In Minas Gerais state, samples were obtained from the Faculdade de Medicina Veterina´ria da Universidade ˆ Federal de Uberlandia, and all samples originated ˆ from the Uberlandia municipality (1885494199S, 4881594499W). In Sao ˜ Paulo state, samples were ˆ obtained from the Faculdade de Ciencias Agra´rias e Veterina´rias, Unesp Jaboticabal, and the samples originated from nine different municipalities: Araraquara (2184794199S, 4881093699W), Barretos (2083393399S, 488349899W), Jaborandi (208549099S, 478169099W), Jaboticabal (2181591999S, 4881992199W), Matao ˜ (2183691299S, 4882195999W), Monte Alto (2181594299S, 4882994899W), Ribeirao ˜ Preto (2181093699S, 4784991599W), Sao ˜ Simao ˜ (2182894199S, 478339399W), and Taquaritinga (2182492399S, 4883092099W). In both cases, animals were kept as patients in the veterinary hospital of the respective institutions, and blood was collected. Serum samples from 53 wild animals were assayed for the presence of antibodies to T. gondii by the modified agglutination test (MAT), as described by Dubey and Desmonts,5 with a cutoff
197
198
JOURNAL OF ZOO AND WILDLIFE MEDICINE
Table 1. Presence of Toxoplasma gondii antibodies (modified agglutination test [MAT] 5) in free-living wild birds from the southeast region of Brazil. Species
No. tested/No. positive
Location
MAT titers
Cariameformes Cariama cristata (crested seriema)
1/1
Jaboticabal
100
2/2
ˆ Jaboticabal, Uberlandia
3/1
Jaboticabal
20
2/1
Monte Alto
10
5/1
Jaboticabal
40
Ciiconiformes Theristicus caudatus (buff-necked ibis)
20, 160
Columbiformes Patagioenas picazuro (picazuro pigeon) Falconiformes Caracara plancus (crested caracara) Strigiformes Athene cunicularia (burrowing Owl)
of 1 : 5 for birds and of 1 : 25 for mammals.9 Association between animal species (bird or mammal) and presence of antibodies against T. gondii were analyzed using a chi-square test. Pvalues of ,0.05 were considered statistically significant. Out of the sampled animals, 27 were birds and 26 were mammals, and from this total, 83% (n ¼ 44) were free-living animals. Antibodies were found in 6 of 27 (22.2%) birds, including one crested seriema (Cariama cristata), two buffnecked ibis (Theristicus caudatus), one picazuro pigeon (Patagioenas picazuro), one crested caracara (Caracara plancus), and one burrowing owl (Athene cunicularia), all of which are free-living animals (Table 1). In mammals, 13 of 26 (50%) were seropositive, including two gray brockets (Mazama gouazoubira), one marsh deer (Blastocerus dichotomus), two maned wolves (Chrysocyon brachyurus), one hoary fox (Pseudalopex vetulus), one white-eared opossum (Didelphis albiventris), one capuchin monkey (Sapajus apella), two collared anteaters (Tamandua tetradactyla), two giant anteaters (Myrmecophaga tridactyla), one six-banded armadillo (Euphractus sexcinctus), and one ninebanded armadillo (Dasypus novemcinctus), from which all were free-living animals except the marsh deer and the capuchin monkey (Table 2). The results of the present study corroborate previous studies that reported the widespread presence of T. gondii in wildlife, mostly in captivity.1,2,9,12 However, serologic data are only a tool with which to assess the epidemiology of the parasite. Whenever possible, it is helpful to isolate viable parasites from host tissues. Toxoplasma gondii antibodies were detected in crested seriemas, in buff-necked ibis, in picazuro
pigeons, in burrowing owls, and in giant anteaters for the first time. Crested seriemas, buff-necked ibis, and burrowing owls, as well as crested caracaras, are predators and can be infected by consumption of parasite-harboring prey, such as small birds and rodents. On the other hand, picazuro pigeons, which are granivorous, can be infected as a result of their foraging habits. These species feed from the ground, behavior that is also shared by crested seriemas and buff-necked ibis when foraging for insects, and, in this case, infection may indicate soil contamination with T. gondii oocysts in the environment. In the case of mammals, gray brocket deer and marsh deer are strict herbivores, and their infection is probably due to environmental contamination with oocysts, whereas all the other studied species of mammals are omnivorous and can be infected either by environmental contamination or by consumption of parasite-harboring prey. In captive animals, the risk of infection is higher as a result of factors such as stress associated with captivity, the presence of synanthropic animals, and possible errors in health management, such as feeding carnivores with meat that was not previously frozen.1 Bird titers ranged from 10 to 160, while in mammals variation ranged from 25 to 800. Seropositivity was significantly higher (P 0.05) in mammals than in birds, but this may not be indicative of more recent infections or of greater exposure because sera from avian species may not react in serologic tests for T. gondii as mammalian sera,6 and for this reason, caution should be used when interpreting serologic data collected from birds.
VITALIANO ET AL.—T. GONDII SEROPOSITIVITY IN WILD ANIMALS
199
Table 2. Presence of Toxoplasma gondii antibodies (modified agglutination test [MAT] 25) in captive and freeliving wild mammals from the southeast region of Brazil. Species
No. tested/No. positive
Location
MAT titers
3/2 1/1
S. Simao, ˜ Rib. Preto Jaboticabal
25, 100 50
3/2 1/1
Barretos, Jaborandi Araraquara
25, 400 200
3/1
Jaboticabal
50
1/1
Jaboticabal
25
2/1 2/2 1/1 1/1
Jaboticabal Matao, ˜ Taquatiringa ˆ Uberlandia Ribeirao ˜ Preto
Artiodactyla Mazama gouazoubira (gray brocket) Blastocerus dichotomus (marsh deer)a Carnivora Chrysocyon brachyurus (maned wolf ) Pseudalopex vetulus (hoary fox) Marsupialia Didelphis albiventris (white-eared opossum) Primatas Sapajus apella (capuchin monkey)a Xenarthra Tamandua tetradactyla (collared anteater) Myrmecophaga tridactyla (giant anteater) Euphractus sexcinctus (six-banded armadillo) Dasypus novemcinctus (nine-banded armadillo) a
400 100, 800 25 800
Animals kept in captivity.
Acknowledgments: This study was supported by the Fundac ao ˜ de Amparo a` Pesquisa do Estado de Sao ˜ Paulo (FAPESP) and the Conselho Nacional de Desenvolvimento Cientı´fico e Tecnolo´gico (CNPq). S. N. Vitaliano and H. S. Soares possessed a scholarship from FAPESP. S. M. Gennari and H. F. J. Pena are in receipt of a scholarship from CNPq. The authors also thank Dr. Andre´ Luiz Quagliatto Santos and Dr. Karin Werther for kindly supplying the blood samples and Dr. Marcelo Bahia Labruna for the assistance in statistical analysis.
LITERATURE CITED 1. Andre´, M. R., C. H. Adania, R. H. F. Teixeira, K. F. Silva, M. M. G. Jusi, S. T. Z. Machado, C. P. De Bortolli, M. Falcade, L. Sousa, S. M. Alegrettii, P. A. N. Felippe, and R. Z. Machado. 2010. Antibodies to Toxoplasma gondii and Neospora caninum in captive neotropical and exotic wild canids and felids. J. Parasitol. 96: 1007–1009. 2. Costa, D. G. C., M. F. V. Marvulo, J. S. A. Silva, S. C. Santana, F. J. R. Magalhaes, ˜ C. D. F. Lima Filho, V. O. Ribeiro, L. C. Alves, R. A. Mota, J. P. Dubey, and J. C. R. Silva. 2012. Seroprevalence of Toxoplasma gondii in domestic and wild animals from the Fernando de Noronha, Brazil. J. Parasitol. 98: 679–680. 3. Cunningham, A. A., D. Buxton, and K. M. Thomson. 1992. An epidemic of toxoplasmosis in a captive colony of squirrel monkeys (Saimiri sciureus). J. Comp. Pathol. 107: 207–219. 4. Dubey, J. P. 2010. Toxoplasmosis of Animals and Humans, 2nd ed. CRC Press, Boca Raton, Florida.
5. Dubey, J. P., and G. Desmonts. 1987. Serological responses of equids fed Toxoplasma gondii oocysts. Equine Vet. J. 19: 337–339. 6. Frenkel, J. K. 1981. False-negative serologic test for Toxoplasma in birds. J. Parasitol. 76: 952–953. 7. Humphreys, J. G., R. L. Stewart, and J. P. Dubey. 1995. Prevalence of Toxoplasma gondii antibodies in sera of hunterkilled white-tailed deer in Pennsylvania. Am. J. Vet. Res. 56: 172–173. 8. Innes, E. A. 1997. Toxoplasmosis: comparative species susceptibility and host immune response. Comp. Immunol. Microb. 20: 131–138. ˆ 9. Minervino, A. H. H., H. S. Soares, R. A. BarretoJu´nior, K. A. L. Neves, H. F. J. Pena, E. L. Ortolani, J. P. Dubey, and S. M. Gennari. 2010. Seroprevalence of Toxoplasma gondii antibodies in captive wild mammals and birds in Brazil. J. Zoo Wildl. Med. 41: 572–574. 10. Sogorb, F. S., L. F. Jamra, E. C. Guimaraes, ˜ and M. P. ˆ Deane. 1972. Toxoplasmose espontanea em animais dome´sticos e silvestres, em Sao ˜ Paulo. Rev. Inst. Med. Trop. Sao ˜ Paulo 14: 314–320. 11. Vitaliano, S. N., T. W. P. Mineo, M. R. Andre´, R. Z. Machado, J. R. Mineo, and K. Werther. 2010. Experimental infection of crested caracara (Caracara plancus) with Toxoplasma gondii simulating natural conditions. Vet. Parasitol. 172: 71–75. 12. Vitaliano, S. N., D. A. O. Silva, T. W. P. Mineo, R. A. Ferreira, E. Bevilacqua, and J. R. Mineo. 2004. Seroprevalence of Toxoplasma gondii and Neospora caninum in captive maned wolves (Chrysocyon brachyurus) from southeastern and midwestern regions of Brazil. Vet. Parasitol. 122: 253– 260.
Received for publication 4 August 2013
BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/ terms_of_use. Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder.
BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research.
Journal of Zoo and Wildlife Medicine 45(1): 197–199, 2014 Copyright 2014 by American Association of Zoo Veterinarians
SEROLOGIC EVIDENCE OF TOXOPLASMA GONDII INFECTION IN WILD BIRDS AND MAMMALS FROM SOUTHEAST BRAZIL Se´rgio Netto Vitaliano, D.V.M., Ph.D., Herbert Sousa Soares, D.V.M., Hilda Fa´tima de Jesus Pena, D.V.M., Ph.D., Jitender Prakash Dubey, M.V.Sc., Ph.D., and Solange Maria Gennari, D.V.M., Ph.D.
Abstract: In this study, serum samples of 53 wild animals from two different states from the southeast region of Brazil were analyzed for the presence of anti–Toxoplasma gondii antibodies by the modified agglutination test (MAT), with a cut-off of 1 : 5 for birds and of 1 : 25 for mammals. Out of the sampled animals, 27 were birds and 26 were mammals, and from this total, 83% (n ¼ 44) were free-living animals. Antibodies were found in 13 mammals, from which 11 were free-living animals, and in five birds, all of which were free-living. In this study, T. gondii antibodies were detected in four bird species (crested seriema, Cariama cristata; buff-necked ibis, Theristicus caudatus; picazuro pigeon, Patagioenas picazuro; and burrowing owl, Athene cunicularia) and in a giant anteater (Myrmecophaga tridactyla) for the first time. Key words: Antibodies, Brazil, modified agglutination test, Toxoplasma gondii, wild birds, wild mammals.
BRIEF COMMUNICATION Toxoplasma gondii is an intracellular protozoan parasite capable of infecting several species of warm-blooded animals, including humans. Its infection is widely prevalent worldwide, particularly in Brazil, where up to 90% of humans have been exposed to this parasite, and it is transmitted by the ingestion of oocysts present in the environment, by the consumption of bradyzoites present in tissue of infected intermediate hosts, and by the transplacental transmission of tachyzoites.4 In animals, the interest in the evaluation of toxoplasmosis occurrence is greater in species that cohabitate with humans or in species that can serve as a food source as a result of the possibility of human infection.10 The pathogenicity of T. gondii can display great variation within various animal species.3 In the most susceptible species, such as Australian marsupials, New World monkeys, and penguins, the acute disease is normally fatal,8 while in the most resistant species the infection is normally mild and unspecific, with From Faculdade de Medicina Veterina´ria e Zootecnia da Universidade de Sao ˜ Paulo, Avenida Professor Doutor Orlando Marques de Paiva, 87, 05508-270, Cidade Universita´ria, Sao ˜ Paulo/SP, Brazil (Vitaliano, Soares, Pena, Gennari); Curso de Medicina Veterina´ria das Faculdades Metropolitanas Unidas (UniFMU), Rua Ministro Nelson Hungria, 541, 05690-050 Real Parque/ Morumbi, Sao ˜ Paulo/SP, Brazil (Vitaliano); and the U.S. Department of Agriculture, Agricultural Research Service, Beltsville Agricultural Research Center, Animal Parasitic Diseases Laboratory, Beltsville, Maryland 20705, USA (Dubey). Correspondence should be directed to Dr. Gennari ([email protected]).
some cases having no sign of clinical infection despite the seroconversion and the presence of the parasite in those animal tissues.11 Although studies indicate that wild animals are frequently positive for T. gondii antibodies,1,9,12 the role of wildlife in the epidemiology of this parasite is not well understood, nor is the susceptibility of different wild species.7 In the present article, free-living and captive wild animals from Minas Gerais and Sao ˜ Paulo states in the southeast region of Brazil were assayed for the presence of T. gondii antibodies. The animals originated from 10 different municipalities, and partners in two different public institutions gathered the samples. In Minas Gerais state, samples were obtained from the Faculdade de Medicina Veterina´ria da Universidade ˆ Federal de Uberlandia, and all samples originated ˆ from the Uberlandia municipality (1885494199S, 4881594499W). In Sao ˜ Paulo state, samples were ˆ obtained from the Faculdade de Ciencias Agra´rias e Veterina´rias, Unesp Jaboticabal, and the samples originated from nine different municipalities: Araraquara (2184794199S, 4881093699W), Barretos (2083393399S, 488349899W), Jaborandi (208549099S, 478169099W), Jaboticabal (2181591999S, 4881992199W), Matao ˜ (2183691299S, 4882195999W), Monte Alto (2181594299S, 4882994899W), Ribeirao ˜ Preto (2181093699S, 4784991599W), Sao ˜ Simao ˜ (2182894199S, 478339399W), and Taquaritinga (2182492399S, 4883092099W). In both cases, animals were kept as patients in the veterinary hospital of the respective institutions, and blood was collected. Serum samples from 53 wild animals were assayed for the presence of antibodies to T. gondii by the modified agglutination test (MAT), as described by Dubey and Desmonts,5 with a cutoff
197
198
JOURNAL OF ZOO AND WILDLIFE MEDICINE
Table 1. Presence of Toxoplasma gondii antibodies (modified agglutination test [MAT] 5) in free-living wild birds from the southeast region of Brazil. Species
No. tested/No. positive
Location
MAT titers
Cariameformes Cariama cristata (crested seriema)
1/1
Jaboticabal
100
2/2
ˆ Jaboticabal, Uberlandia
3/1
Jaboticabal
20
2/1
Monte Alto
10
5/1
Jaboticabal
40
Ciiconiformes Theristicus caudatus (buff-necked ibis)
20, 160
Columbiformes Patagioenas picazuro (picazuro pigeon) Falconiformes Caracara plancus (crested caracara) Strigiformes Athene cunicularia (burrowing Owl)
of 1 : 5 for birds and of 1 : 25 for mammals.9 Association between animal species (bird or mammal) and presence of antibodies against T. gondii were analyzed using a chi-square test. Pvalues of ,0.05 were considered statistically significant. Out of the sampled animals, 27 were birds and 26 were mammals, and from this total, 83% (n ¼ 44) were free-living animals. Antibodies were found in 6 of 27 (22.2%) birds, including one crested seriema (Cariama cristata), two buffnecked ibis (Theristicus caudatus), one picazuro pigeon (Patagioenas picazuro), one crested caracara (Caracara plancus), and one burrowing owl (Athene cunicularia), all of which are free-living animals (Table 1). In mammals, 13 of 26 (50%) were seropositive, including two gray brockets (Mazama gouazoubira), one marsh deer (Blastocerus dichotomus), two maned wolves (Chrysocyon brachyurus), one hoary fox (Pseudalopex vetulus), one white-eared opossum (Didelphis albiventris), one capuchin monkey (Sapajus apella), two collared anteaters (Tamandua tetradactyla), two giant anteaters (Myrmecophaga tridactyla), one six-banded armadillo (Euphractus sexcinctus), and one ninebanded armadillo (Dasypus novemcinctus), from which all were free-living animals except the marsh deer and the capuchin monkey (Table 2). The results of the present study corroborate previous studies that reported the widespread presence of T. gondii in wildlife, mostly in captivity.1,2,9,12 However, serologic data are only a tool with which to assess the epidemiology of the parasite. Whenever possible, it is helpful to isolate viable parasites from host tissues. Toxoplasma gondii antibodies were detected in crested seriemas, in buff-necked ibis, in picazuro
pigeons, in burrowing owls, and in giant anteaters for the first time. Crested seriemas, buff-necked ibis, and burrowing owls, as well as crested caracaras, are predators and can be infected by consumption of parasite-harboring prey, such as small birds and rodents. On the other hand, picazuro pigeons, which are granivorous, can be infected as a result of their foraging habits. These species feed from the ground, behavior that is also shared by crested seriemas and buff-necked ibis when foraging for insects, and, in this case, infection may indicate soil contamination with T. gondii oocysts in the environment. In the case of mammals, gray brocket deer and marsh deer are strict herbivores, and their infection is probably due to environmental contamination with oocysts, whereas all the other studied species of mammals are omnivorous and can be infected either by environmental contamination or by consumption of parasite-harboring prey. In captive animals, the risk of infection is higher as a result of factors such as stress associated with captivity, the presence of synanthropic animals, and possible errors in health management, such as feeding carnivores with meat that was not previously frozen.1 Bird titers ranged from 10 to 160, while in mammals variation ranged from 25 to 800. Seropositivity was significantly higher (P 0.05) in mammals than in birds, but this may not be indicative of more recent infections or of greater exposure because sera from avian species may not react in serologic tests for T. gondii as mammalian sera,6 and for this reason, caution should be used when interpreting serologic data collected from birds.
VITALIANO ET AL.—T. GONDII SEROPOSITIVITY IN WILD ANIMALS
199
Table 2. Presence of Toxoplasma gondii antibodies (modified agglutination test [MAT] 25) in captive and freeliving wild mammals from the southeast region of Brazil. Species
No. tested/No. positive
Location
MAT titers
3/2 1/1
S. Simao, ˜ Rib. Preto Jaboticabal
25, 100 50
3/2 1/1
Barretos, Jaborandi Araraquara
25, 400 200
3/1
Jaboticabal
50
1/1
Jaboticabal
25
2/1 2/2 1/1 1/1
Jaboticabal Matao, ˜ Taquatiringa ˆ Uberlandia Ribeirao ˜ Preto
Artiodactyla Mazama gouazoubira (gray brocket) Blastocerus dichotomus (marsh deer)a Carnivora Chrysocyon brachyurus (maned wolf ) Pseudalopex vetulus (hoary fox) Marsupialia Didelphis albiventris (white-eared opossum) Primatas Sapajus apella (capuchin monkey)a Xenarthra Tamandua tetradactyla (collared anteater) Myrmecophaga tridactyla (giant anteater) Euphractus sexcinctus (six-banded armadillo) Dasypus novemcinctus (nine-banded armadillo) a
400 100, 800 25 800
Animals kept in captivity.
Acknowledgments: This study was supported by the Fundac ao ˜ de Amparo a` Pesquisa do Estado de Sao ˜ Paulo (FAPESP) and the Conselho Nacional de Desenvolvimento Cientı´fico e Tecnolo´gico (CNPq). S. N. Vitaliano and H. S. Soares possessed a scholarship from FAPESP. S. M. Gennari and H. F. J. Pena are in receipt of a scholarship from CNPq. The authors also thank Dr. Andre´ Luiz Quagliatto Santos and Dr. Karin Werther for kindly supplying the blood samples and Dr. Marcelo Bahia Labruna for the assistance in statistical analysis.
LITERATURE CITED 1. Andre´, M. R., C. H. Adania, R. H. F. Teixeira, K. F. Silva, M. M. G. Jusi, S. T. Z. Machado, C. P. De Bortolli, M. Falcade, L. Sousa, S. M. Alegrettii, P. A. N. Felippe, and R. Z. Machado. 2010. Antibodies to Toxoplasma gondii and Neospora caninum in captive neotropical and exotic wild canids and felids. J. Parasitol. 96: 1007–1009. 2. Costa, D. G. C., M. F. V. Marvulo, J. S. A. Silva, S. C. Santana, F. J. R. Magalhaes, ˜ C. D. F. Lima Filho, V. O. Ribeiro, L. C. Alves, R. A. Mota, J. P. Dubey, and J. C. R. Silva. 2012. Seroprevalence of Toxoplasma gondii in domestic and wild animals from the Fernando de Noronha, Brazil. J. Parasitol. 98: 679–680. 3. Cunningham, A. A., D. Buxton, and K. M. Thomson. 1992. An epidemic of toxoplasmosis in a captive colony of squirrel monkeys (Saimiri sciureus). J. Comp. Pathol. 107: 207–219. 4. Dubey, J. P. 2010. Toxoplasmosis of Animals and Humans, 2nd ed. CRC Press, Boca Raton, Florida.
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Received for publication 4 August 2013
