Skip to main content
SpringerLink
Log in

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)

  • Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

An Erratum to this article was published on 13 September 2007

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Abrahamsohn IA, Coffman RL (1996) Trypanosoma cruzi. : IL-10, TNF, IFN-gamma, and IL-12 regulate innate and acquired immunity to infection. Exp Parasitol 84:231–244

    Article  PubMed  CAS  Google Scholar 

  • Amin OM (1985) Classification. In: Crompton DWT, Nickol BB (eds) Biology of the Acanthocephala. Cambridge Univ. Press, Cambridge, pp 22–71

    Google Scholar 

  • Baker AJ, Dietz JM (1996) Immigration in wild groups of golden lion tamarins (Leontopithecus rosalia). Am J Primatol 38:47–56

    Article  Google Scholar 

  • Bales KL, French JA, McWilliams J, Lake RA, Dietz JM (2006) Effects of social status, age, and season on androgen and cortisol levels in wild male golden lion tamarins (Leontopithecus rosalia). Horm Behav 49:88–95

    Article  PubMed  CAS  Google Scholar 

  • Bar ME, Alvarez BM, Oscherov EB, Damborsky MP, Jörg ME (1999) Contribution to knowledge of reservoirs of Trypanosoma cruzi (Chagas 1909) in Corrientes Province, Argentina. Rev Soc Bras Med Trop 32:271–276

    Article  PubMed  CAS  Google Scholar 

  • Barbosa PRB (2006) The oral transmission of Chagas’ disease: an acute form of infection responsible for regional outbreaks. Int J Cardiol 112:132–133

    Article  Google Scholar 

  • Basquiera AL, Sembaj A, Aguerri AM, Omelianiuk M, Guzmán S, Barral JM, Caeiro TF, Madoery RJ, Salomone OA (2003) Risk progression to chronic Chagas cardiomyopathy: influence of male sex and of parasitaemia detected by polymerase chain reaction. Heart 89:1186–1190

    Article  PubMed  CAS  Google Scholar 

  • Beck B, Castro MI, Stoinski TS, Ballou J (2002) The effects of prerelease environments and postrelease management on survivorship in reintroduced golden lion tamarins. In: Kleiman DG, Rylands AB (eds) Lion tamarins: biology and conservation. Smithsonian Institution, Washington, DC, pp 283–300

    Google Scholar 

  • Bouman A, Heineman MJ, Faas MM (2005) Sex hormones and the immune response in humans. Hum Reprod Update 11:411–423

    Article  PubMed  CAS  Google Scholar 

  • Bustamante JM, Rivarola HW, Fernández AR, Enders JE, Fretes R, Palma JA, Paglini-Oliva PA (2003) Indeterminate Chagas’ disease: Trypanosoma cruzi strain and re-infection are factors involved in the progression of cardiopathy. Clin Sci 104:415–420

    Article  PubMed  Google Scholar 

  • Camargo EP (1964) Growth and differentiation in Trypanosoma cruzi. Origin of metacyclic trypanosomes in liquid media. Rev Inst Med Trop São Paulo 6:93–100

    CAS  PubMed  Google Scholar 

  • Camargo ME (1966) Fluorescent antibody test for the serodiagnosis of American trypanosomiasis. Technical modification employing preserved culture forms of Trypanosoma cruzi in a slide test. Rev Inst Med Trop Sao Paulo 8:227–235

    PubMed  CAS  Google Scholar 

  • Coimbra-Filho AF (1969) Mico-Leão, Leontideus rosalia (Linnaeus 1766), situação atual da espécie no Brasil (Callitrichidae–Callitrichids). An Acad Bras Cienc 41(Suppl):29–52

    Google Scholar 

  • Coimbra-Filho AF (1970) Considerações gerais e a situação atual dos micos-leões escuros, Leontideus chrysomelas (Kuhl 1820) e Leontideus chrysopygus (Mikan 1823) (Callitrichidae, Callitrichids). Rev Bras Biol 30:249–268

    Google Scholar 

  • Corrêa-Oliveira R, Gomes JAS, Lemos EM, Cardoso GM, Reis DD, Adad S, Crema E, Martins-Filho OA, Costa MOR, Gazzinelli G, Bahia-Oliveira LMG (1999) The role of the immune response on the development of severe clinical forms of human Chagas’ disease. Mem Inst Oswaldo Cruz 94(Suppl 1):253–255

    PubMed  Google Scholar 

  • de Thoisy B, Michel J-C, Vogel I, Vié J-C (2000) A survey of hemoparasite infections in free-ranging mammals and reptiles in French Guiana. J Parasitol 86:1035–1040

    PubMed  Google Scholar 

  • Dereure J, Barnabé C, Vié J-C, Madélenat F, Raccurt C (2001) Trypanosomatidae from wild mammals in the neotropical rainforest of French Guiana. Ann Trop Med Parasitol 95:157–166

    Article  PubMed  CAS  Google Scholar 

  • Dias JCP, Coura JR (1997) Clínica e Terapêutica da doença de Chagas. Fiocruz, Rio de Janeiro, Brazil

    Google Scholar 

  • Dietz JM, Baker AJ (1993) Polygyny and female reproductive success in golden lion tamarins, Leontopithecus rosalia. Anim Behav 46:1067–1078

    Article  Google Scholar 

  • Dietz JM, Baker AJ, Miglioretti D (1994) Seasonal variation in reproduction, juvenile growth, and adult body mass in golden lion tamarins (Leontopithecus rosalia). Am J Primatol 34:115–132

    Article  Google Scholar 

  • Dietz JM, Peres CA, Pinder L (1997) Foraging ecology and use of space in wild golden lion tamarins (Leontopithecus rosalia). Am J Primatol 41:289–305

    Article  PubMed  CAS  Google Scholar 

  • do Prado JC, Leal MP, Anselmo-Franci JA, de Andrade HF Jr, Kloetzel JK (1998) Influence of female gonadal hormones on the parasitemia of female Calomys callosus infected with the “Y” strain of Trypanosoma cruzi. Parasitol Res 84:100–105

    Article  Google Scholar 

  • do Prado JC, Levy AM, Leal MP, Bernard E, Kloetzel JK (1999) Influence of male gonadal hormones on the parasitemia and humoral response of male Calomys callosus infected with the Y strain of Trypanosoma cruzi. Parasitol Res 85:826–829

    Article  PubMed  Google Scholar 

  • French JA, Bales KL, Baker AJ, Dietz JM (2003) Endocrine monitoring of wild dominant and subordinate female Leontopithecus rosalia. Int J Primatol 24:1281–1300

    Article  Google Scholar 

  • Grativol AD, Ballou J, Fleischer R (2001) Microsatellite variation within and among recently isolated populations of golden lion tamarins. Conserv Genet 2:1–9

    Article  CAS  Google Scholar 

  • Grijalva MJ, Escalante L, Paredes RA, Costales JA, Padilla A, Rowland EC, Aguilar HM, Racines J (2003) Seroprevalence and risk factors for Trypanosoma cruzi infection in the Amazon region of Ecuador. Am J Trop Med Hyg 69:380–385

    PubMed  Google Scholar 

  • Gulland FMD (1995) The impact of infectious diseases on wild animal populations: a review. In: Grenfell BT, Dobson AP (eds) Ecology of infectious diseases in natural populations. Cambridge Univ. Press, Cambridge, pp 20–51

    Google Scholar 

  • Harnett W, Harnett MM (2006) Molecular basis of worm-induced immunomodulation. Parasite Immunol 28:535–543

    Article  PubMed  CAS  Google Scholar 

  • Helmby H, Bickle Q (2006) Immune modulation by helminth infections. Parasite Immunol 28:479–481

    Article  PubMed  CAS  Google Scholar 

  • Horwitz P, Wilcox BA (2005) Parasites, ecosystems and sustainability: an ecological and complex systems perspective. Int J Parasitol 35:725–732

    Article  PubMed  Google Scholar 

  • Hudson PJ, Dobson AP, Newborn D (1998) Prevention of population cycles by parasite removal. Science 282:2256–2258

    Article  PubMed  CAS  Google Scholar 

  • IUCN (2004) 2004 IUCN Red List of Threatened Species. www.redlist.org. Downloaded on 20 May 2005

  • Jenkins SJ, Hewitson JP, Jenkins GR, Mountford AP (2005) Modulation of the host’s immune response by schistosome larvae. Parasite Immunol 27:385–393

    Article  PubMed  CAS  Google Scholar 

  • Kierulff MC, Rylands AB (2003) Census and distribution of the golden lion tamarin (Leontopithecus rosalia). Am J Primatol 59:29–44

    Article  PubMed  Google Scholar 

  • Klein SL (2004) Hormonal and immunological mechanisms mediating sex differences in parasite infection. Parasite Immunol 26:247–264

    Article  PubMed  CAS  Google Scholar 

  • Krasnov BR, Mouillot D, Khokhlova IS, Shenbrot GI, Poulin R (2005) Covariance in species diversity and facilitation among non-interactive parasite taxa: all against the host. Parasitology 131:557–568

    Article  PubMed  CAS  Google Scholar 

  • Lisboa CV, Dietz J, Baker AJ, Russel NN, Jansen AM (2000) Trypanosoma cruzi. infection in Leontopithecus rosalia at the reserva biológica de Poço das Antas, Rio de Janeiro, Brazil. Mem Inst Oswaldo Cruz 95:445–452

    Article  PubMed  CAS  Google Scholar 

  • Lisboa CV, Mangia RH, Lima NRC, Martins A, Dietz J, Baker AJ, Ramon-Miranda CR, Ferreira LF, Fernandes O, Jansen AM (2004) Distinct patterns of Trypanosoma cruzi infection in Leontopithecus rosalia in distinct Atlantic Coastal Rainforest fragments in Rio de Janeiro—Brazil. Parasitology 129:703–711

    Article  PubMed  CAS  Google Scholar 

  • Lourenço-de-Oliveira R (1990) Natural infection of golden lion tamarin, Leontopithecus rosalia with Trypanosoma cruzi in the state of Rio de Janeiro, Brasil. Mem Inst Oswaldo Cruz 85:15

    Google Scholar 

  • Mallinson JJC (2001) Saving Brazil’s Atlantic rainforest: using the golden-headed lion tamarin Leontopithecus chrysomelas as a flagship for a biodiversity hotspot. Dodo 37:9–20

    Google Scholar 

  • McCallum H, Dobson A (2002) Disease, habitat fragmentation and conservation. Proc R Soc Lond B Biol Sci 269:2041–2049

    Article  Google Scholar 

  • Monteiro RV, Jansen AM, Pinto RM (2003) Coprological helminth screening in Brazilian free ranging golden lion tamarins, Leontopithecus rosalia (L. 1766) (Callitrichidae). Braz J Biol 63:727–729

    Article  PubMed  CAS  Google Scholar 

  • Monteiro RV, Baldez J, Dietz J, Baker A, Lisboa CV, Jansen AM (2006) Clinical, biochemical, and electrocardiographic aspects of Trypanosoma cruzi infection in free-ranging golden lion tamarins (Leontopithecus rosalia). J Med Primatol 35:48–55

    Article  PubMed  Google Scholar 

  • Monteiro RV, Dietz JM, Beck BB, Baker AJ, Martins A, Jansen AM (2007) Prevalence and intensity of intestinal helminths found in free-ranging golden lion tamarins (Leontopithecus rosalia, Primates, Callitrichidae) from Brazilian Atlantic forest. Vet Parasitol 145:77–85

    Article  PubMed  Google Scholar 

  • Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858

    Article  PubMed  CAS  Google Scholar 

  • Patz JA, Daszak P, Tabor GM, Aguirre AA, Pearl M, Epstein J, Wolfe ND, Kilpatrick AM, Foufopoulos J, Molyneux D, Bradley DJ (2004) Unhealthy landscapes: policy recommendations on land use change and infectious disease emergence. Environ Health Perspect 112:1092–1098

    Article  PubMed  Google Scholar 

  • Raboy BE, Dietz JM (2004) Diet, foraging, and use of space in wild golden-headed lion tamarins. Am J Primatol 63:1–15

    Article  PubMed  Google Scholar 

  • Rey L (2001) Métodos e técnicas usuais em parasitologia. In: Rey L (ed) Parasitologia. Guanabara Koogan, Rio de Janeiro, pp 787–801

    Google Scholar 

  • Rodriguez M, Terrazas LI, Marquez R, Bojalil R (1999) Susceptibility to Trypanosoma cruzi is modified by a previous non-related infection. Parasite Immunol 21:177–185

    Article  PubMed  CAS  Google Scholar 

  • Romaña CA, Pizarro NJC, Rodas E, Guilbert E (1999) Palm trees as ecological indicators of risk areas for Chagas disease. Trans R Soc Trop Med Hyg 93:594–595

    Article  PubMed  Google Scholar 

  • Ryland AB (2002) A history of lion tamarin research and conservation. In: Kleiman DG, Rylands AB (eds) Lion tamarins: biology and conservation. Smithsonian Institution, Washington, DC, pp 3–41

    Google Scholar 

  • Santos CD, Levy AM, Toldo MP, Azevedo AP, Prado JC (2007) Haematological and histopathological findings after ovariectomy in Trypanosoma cruzi infected mice. Vet Parasitol 143:222–228

    Article  PubMed  CAS  Google Scholar 

  • Schuster JP, Schaub GA (2001a) Trypanosoma. cruzi: the development of estrus cycle and parasitemia in female mice maintained with or without male pheromones. Parasitol Res 87:985–993

    CAS  Google Scholar 

  • Schuster JP, Schaub GA (2001b) Experimental Chagas disease: the influence of sex and psychoneuroimmunological factors. Parasitol Res 87:994–1000

    CAS  Google Scholar 

  • Sloss MW, Zajac AM, Kemp RL (1999) Parasitologia clínica veterinária. Manole, São Paulo, Brazil

    Google Scholar 

  • Starling JA (1985) Feeding, nutrition and metabolism. In: Crompton DWT, Nickol BB (eds) Biology of the Acanthocephala. Cambridge Univ. Press, Cambridge, pp 125–212

    Google Scholar 

  • Teixeira AR, Monteiro PS, Rebelo JM, Arganaraz ER, Vieira D, Lauria-Pires L, Nascimento R, Vexenat CA, Silva AR, Ault SK, Costa JM (2001) Emerging Chagas disease: trophic network and cycle of transmission of Trypanosoma cruzi from palm trees in the Amazon. Emerg Infect Dis 7:100–112

    Article  PubMed  CAS  Google Scholar 

  • Toft JD 2nd (1982) The pathoparasitology of the alimentary tract and pancreas of nonhuman primates: a review. Vet Pathol Suppl 7:44–92

    Article  PubMed  Google Scholar 

  • Travis DA, Hungerford L, Engel GA, Jones-Engel L (2006) Disease risk analysis: a tool for primate conservation planning and decision making. Am J Primatol 68:855–867

    Article  PubMed  CAS  Google Scholar 

  • Vicente JJ, Rodrigues HO, Gomes DC, Pinto RM, Faria Z (1997) Nematóides do Brasil, parte V: nematóides de mamíferos. Rev Bras Zool 14(Suppl 1):1–452

    Google Scholar 

  • Wilson K, Bjørnstad ON, Dobson AP, Merler S, Poglayen G, Randolph SE, Read AF, Skorping A (2002) Heterogeneities in macroparasite infections: patterns and processes. In: Hudson PJ, Rizzoli A, Grenfell BT, Heesterbeek H, Dobson AP (eds) The ecology of wildlife diseases. Oxford, New York, pp 6–44

    Google Scholar 

  • Woolhouse MEJ (1998) Patterns in parasite epidemiology: the peak shift. Parasitol Today 14:428–434

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank the director and staff of IBAMA in REBIO Poço das Antas and in REBIO Una for logistic support, the owners of Reintroduction farms for access to their properties, and the director and staff of the Associação Mico Leão Dourado for logistic and technical support. This work was conducted under authorizations from IBAMA, CNPq and the Animal Care and Use Committee of FIOCRUZ and the University of Maryland. This work was supported by grants from the Brazilian Conselho Nacional de Pesquisa e Desenvolvimento—CNPq, Edital Universal no. 472777/2003 and the US National Science Foundation.

Author information

Authors and Affiliations

  1. Lab. Biologia de Tripanosomatídeos, Instituto Oswaldo Cruz, FIOCRUZ, Av. Brasil 4365, Rio de Janeiro, RJ, 21040-360, Brazil

    Rafael V. Monteiro & Ana Maria Jansen

  2. Department of Biology, University of Maryland, College Park, MD, 20742, USA

    James M. Dietz

  3. Species Conservation Center, Smithsonian National Zoological Park, 3001 Connecticut Ave NW, Washington, DC, 20008, USA

    Becky Raboy

  4. Great Ape Trust of Iowa, 4200 SE 44th Avenue, Des Moines, IA, 50320, USA

    Benjamin Beck

  5. Center for Research and Conservation, Universiteit Antwerpen, Koningin Astridplein 26, B-2018, Antwerpen, Belgium

    Kristel D. Vleeschower

  6. Philadelphia Zoological Gardens, 3400 West Girard Avenue, Philadelphia, PA, 19104-1196, USA

    Andrew Baker

  7. Associação Mico Leão Dourado, P.O. Box 109968, Casimiro de Abreu, RJ, 28960-970, Brazil

    Andréia Martins

  8. Lab. Biologia de Tripanosomatídeos, Pavilhão Carlos Chagas, 3º andar, Av. Brasil, 4365, Rio de Janeiro, RJ, 21040-360, Brazil

    Rafael V. Monteiro

Authors
  1. Rafael V. Monteiro
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. James M. Dietz
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Becky Raboy
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Benjamin Beck
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Kristel D. Vleeschower
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Andrew Baker
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Andréia Martins
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Ana Maria Jansen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rafael V. Monteiro.

Additional information

An erratum to this article can be found at http://dx.doi.org/10.1007/s00436-007-0730-5

Rights and permissions

Reprints and permissions

About this article

Cite this article

Monteiro, R.V., Dietz, J.M., Raboy, B. et al. 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). Parasitol Res 101, 1689–1698 (2007). https://doi.org/10.1007/s00436-007-0652-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-007-0652-2

Keywords

Search

Navigation