Skip to main content

Advertisement

SpringerLink
Log in

Conservation genetics of maned wolves in a highly impacted area of the Brazilian Cerrado biome

  • Published:
Genetica Aims and scope Submit manuscript

Abstract

Maned wolves are large canids currently considered vulnerable to extinction due to habitat loss. They are still commonly found within the urban mesh inside the Brazilian Federal District (Distrito Federal—DF), in nearby Protected Areas (PAs), and in surrounding farms. We evaluated the genetic diversity of maned wolves in three PAs of the DF, using both invasive and noninvasive techniques to obtain DNA that was later amplified for five microsatellite markers. We sampled 23 wolves: 10 with the noninvasive method, three captured in traps, six road-killed, and four rescued in urban areas. In Águas Emendadas Ecological Station (ESECAE) we also used samples from six specimens captured between 1997 and 1998 for a temporal comparison. For maned wolves, non-invasive techniques are affordable and easier to conduct in the field, while laboratory costs are much lower for invasive samples. Hence, a sampling strategy combining both techniques may provide an interesting approach for molecular ecology studies requiring comprehensive coverage of local individuals. On the basis of such integrated sampling scheme, our analyses indicated that none of the investigated populations currently present deviations from Hardy–Weinberg expectations or indication of inbreeding. Furthermore, in ESECAE there was no reduction in genetic diversity during the last 9 years. Overall, maned wolves did not present evidence of genetic structuring among the three sampled PAs. These results thus indicate that individual exchange among PAs is still occurring at sufficient rates to avoid differentiation, and/or that the recent fragmentation in the region has not yet produced measurable effects in the genetic diversity of maned wolves.

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
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Aragona M, Setz EZF (2001) Diet of the maned wolf, Chrysocyon brachyurus (Mammalia: Canidae), during wet and dry seasons at Ibitipoca State Park, Brazil. J Zool 254:131–136

    Article  Google Scholar 

  • Bonin A, Bellemain E, Eidesen PB, Pompanon F, Brochmann C, Taberlet P (2004) How to track and assess genotyping errors in population genetics studies. Mol Ecol 13(11):3261–3273

    Article  PubMed  CAS  Google Scholar 

  • Boutin-Ganache I, Raposo M, Raymond M, Deschepper CF (2001) M13-tailed primers improve the readability and usability of microsatellite analyses performed with two different allele-sizing methods. BioTechn 31:24–28

    CAS  Google Scholar 

  • Broquet T, Menard N, Petit E (2007) Noninvasive population genetics: a review of sample source, diet, fragment length and microsatellite motif effects on amplification success and genotyping error rates. Conserv Genet 8(1):249–260. doi:10.1007/s10592-006-9146-5

    Article  Google Scholar 

  • Censo agropecuário (2006) Sistema IBGE de recuperação automática—SIDRA. http://www.sidra.ibge.gov.br. Accessed 19/11/2010

  • De Barba M, Waits LP, Genovesi P, Randi E, Chirichella R, Cetto E (2010) Comparing opportunistic and systematic sampling methods for non-invasive genetic monitoring of a small translocated brown bear population. J Appl Ecol 47(1):172–181. doi:10.1111/j.1365-2664.2009.01752.x

    Article  Google Scholar 

  • de Mattos PSR, del Lama MA, Toppa RH, Arno Rudi Schwantes AR (2004) Populational genetic structure of free-living maned wolves (Chrysocyon brachyurus) determined by proteic markers. Braz J Biol 64(3B):639–644

    PubMed  Google Scholar 

  • de Melo LFB, Sábato MAL, Magni EMV, Young RJ, Coelho CM (2007) Secret lives of maned wolves (Chrysocyon brachyurus Illiger 1815): as revealed by GPS tracking collars. J Zool 271:27–36

    Article  Google Scholar 

  • Dietz J (1984) Ecology and social organization of the maned wolf (Chrysocyon brachyurus). Smithson Contrib Zool 392:1–51

    Google Scholar 

  • Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evolut Bioinforma Online 1:47–50

    CAS  Google Scholar 

  • Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587

    PubMed  CAS  Google Scholar 

  • Fletchall NB, Rodden M, Taylor S (eds) (1995) Husbandry manual for the maned wolf, Chrysocyon brachyurus. AAZV, Washington

    Google Scholar 

  • Fontoura-Rodrigues ML, Lima-Rosa CAV, Tchaicka L, Valdez FP, Rodrigues FHG, de Paula RC, Gough MP, Johnson WE, Bonatto SL, Eizirik E (2008) Cross-amplification and characterization of 13 tetranucleotide microsatellites in multiple species of Neotropical canids. Mol Ecol Resour 8(4):898–900

    Article  Google Scholar 

  • Francisco LV, Langston AA, Mellersh CS, Neal CL (1996) A class of highly polymorphic tetranucleotide repeats for canine genetic mapping. Mamm Genome 7(5):359–362

    Article  PubMed  CAS  Google Scholar 

  • Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics. Cambridge University Press, Cambridge

    Google Scholar 

  • Frantz AC, Pope LC, Carpenter PJ, Roper TJ, Wilson GJ, Delahay RJ, Burke T (2003) Reliable microsatellite genotyping of the Eurasian Badger (Meles meles) using faecal DNA. Mol Ecol 12:1649–1661

    Article  PubMed  CAS  Google Scholar 

  • Gittleman JL, Funk SM, Macdonald D, Wayne RK (eds) (2001) Carnivore conservation, vol 5. Conservation biology. Cambridge University Press, Cambridge

    Google Scholar 

  • Gonzalez S, Maldonado JE, Ortega J, Talarico AC, Bidegaray-Batista L, Garcia JE, Duarte JMB (2009) Identification of the endangered small red brocket deer (Mazama bororo) using noninvasive genetic techniques (Mammalia; Cervidae). Mol Ecol Resour 9(3):754–758

    Article  CAS  Google Scholar 

  • Goossens B, Chikhi L, Utami SS, Ruiter J, Bruford MW (2000) A multi-samples, multi-extracts approach for microsatellite analysis of faecal samples in an arboreal ape. Conserv Genet 1:157–162

    Article  CAS  Google Scholar 

  • Goudet J, Raymond M, Demeeus T, Rousset F (1996) Testing differentiation in diploid populations. Genetics 144:1933–1940

    PubMed  CAS  Google Scholar 

  • Haag T, Santos AS, De Angelo C, Srbek-Araujo AC, Sana DA, Morato RG, Salzano FM, Eizirik E (2009) Development and testing of an optimized method for DNA-based identification of jaguar (Panthera onca) and puma (Puma concolor) faecal samples for use in ecological and genetic studies. Genetica 136(3):505–512

    Article  PubMed  CAS  Google Scholar 

  • IBAMA (2003) Lista de espécies da fauna brasileira ameaçadas de extinção. Ministério do Meio Ambiente, IBAMA—Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis, Brasília

  • IUCN red list of threatened species, version 2009.1 (2009) www.redlist.org

  • Jacomo ATA, Silveira L, Diniz JAF (2004) Niche separation between the maned wolf (Chrysocyon brachyurus), the crab-eating fox (Dusicyon thous) and the hoary fox (Dusicyon vetulus) in central Brazil. J Zool 262:99–106

    Article  Google Scholar 

  • Jacomo ATA, Kashivakura CK, Ferro C, Furtado MM, Astete SP, Torres NM, Sollmann R, Silveira L (2009) Home range and spatial organization of maned wolves in the Brazilian grasslands. J Mammal 90(1):150–157

    Article  Google Scholar 

  • Juarez KM, Marinho-Filho J (2002) Diet, habitat use, and home ranges of sympatric canids in central Brazil. J Mammal 83(4):925–933

    Article  Google Scholar 

  • Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program cervus accommodates genotyping error increases success in paternity assignment. Mol Ecol 16(5):1099–1106

    Article  PubMed  Google Scholar 

  • Klink CA, Machado RB (2005) Conservation of the Brazilian Cerrado. Conserv Biol 19(3):707–713

    Article  Google Scholar 

  • Klink CA, Moreira AG (2002) Past and current human occupation, and land use. In: Oliveira PS, Marquis RJ (eds) The cerrados of Brazil. Columbia University Press, New York

    Google Scholar 

  • Leberg PL (2002) Estimating allelic richness: effects of sample size and bottlenecks. Mol Ecol 11(11):2445–2449

    Article  PubMed  CAS  Google Scholar 

  • Lucarelli HZ, Innocencio NR, Fredrich OMBL (1989) Impactos da construção de Brasília na organização do espaço. Revista Brasileira de Geografia 51(2):99–138

    Google Scholar 

  • Mantovani JE (2001) Telemetria convencional e via satélite na determinação da área de vida de três espécies de carnívoros da região nordeste do estado de São Paulo. Universidade Federal de São Carlos, São Carlos, SP

    Google Scholar 

  • McKelvey KS, Schwartz MK (2004) Providing reliable and accurate genetic capture-mark-recapture estimates in a cost-effective way. J Wildl Manag 68(3):453–456

    Article  Google Scholar 

  • Miranda EE, Gomes EG, Guimarães M (2005) Mapeamento e estimativa da área urbanizada do Brasil com base em imagens orbitais e modelos estatísticos. EMBRAPA monitoramento por satélite Ministério da Agricultura, Pecuária e Abastecimento. http://www.urbanizacao.cnpm.embrapa.br

  • Monteiro L, Gras N, Vidal R, Cabrita J, Mégraud F (2001) Detection of Helicobacter pylori DNA in human feces by PCR: DNA stability and removal of inhibitors. J Microbiol Methods 45:89–94

    Article  PubMed  CAS  Google Scholar 

  • Moreira JR, Klautau-Guimarães N, Contel EPB, Bem AR (1998) Estudo preliminar da variabilidade genética do lobo guará (Chrysocyon brachyurus). In: Relatório técnico CENARGEN, vol 30. EMBRAPA/CENARGEN, Brasília

    Google Scholar 

  • Murphy MA, Waits LP, Kendall KC (2003) The influence of diet on faecal DNA amplification and sex identification in brown bears (Ursus arctos). Mol Ecol 12(8):2261–2265. doi:10.1046/j.1365-294X.2003.01863.x

    Article  PubMed  CAS  Google Scholar 

  • Murphy MA, Kendall KC, Robinson A, Waits LP (2007) The impact of time and field conditions on brown bear (Ursus arctos) faecal DNA amplification. Conserv Genet 8(5):1219–1224. doi:10.1007/s10592-006-9264-0

    Article  Google Scholar 

  • Napolitano C, Bennett M, Johnson WE, O’Brien SJ, Marquet PA, Barria I, Poulin E, Iriarte A (2008) Ecological and biogeographical inferences on two sympatric and enigmatic Andean cat species using genetic identification of faecal samples. Mol Ecol 17(2):678–690

    Article  PubMed  CAS  Google Scholar 

  • Netto PB, Mecenas VV, Cardoso ES (eds) (2006) APA de Cafuringa a Última Fronteira Natural do DF. SEMARH, Brasília

    Google Scholar 

  • Paetkau D, Waits LP, Clarkson PL, Vyse E, Ward R, Strobeck C (1998) Variation in genetic diversity across the range of North American brown bears. Conserv Biol 12(2):418–429

    Article  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    PubMed  CAS  Google Scholar 

  • Proença LM (2007) Soroprevalência de doenças infecciosas caninas em populações de lobos guará (Chrysocyon brachyurus) e cachorros do mato (Cerdocyon thous) na Estação Ecológica de Águas Emendadas, DF. Universidade de Brasília, Brasília

    Google Scholar 

  • Prugh LR, Ritland CE, Arthur SM, Krebs CJ (2005) Monitoring coyote population dynamics by genotyping faeces. Mol Ecol 14:1585–1596

    Article  PubMed  CAS  Google Scholar 

  • Raymond M, Rousset F (1995) GENEPOP (Vesion 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249

    Google Scholar 

  • Reed JZ, Tollit DJ, Thompsom PM, Amos W (1997) Molecular scatology: the use of molecular genetic analysis to assign species, sex and individual identity to seal faeces. Mol Ecol 6(3):225–234

    Article  PubMed  CAS  Google Scholar 

  • Rodden M, Rodrigues F, Bestelmeyer SV (2004) Maned wolf Chrysocyon brachyurus (Illiger, 1815). In: Sillero-Zubiri C, Hoffmann M, Macdonald DW (eds) Canids: foxes, wolves, jackals and dogs. Status survey and conservation action plan IUCN/SSC—canid specialist group. Gland and Cambridge, Oxford, pp 38–43

    Google Scholar 

  • Rodden M, Rodrigues F, Bestelmeyer S (2008) Chrysocyon brachyurus. IUCN 2010: IUCN red list of threatened species version 2010-4 <www.iucnredlist.org>

  • Rodrigues FHG (2002) Biologia e conservação do lobo guará na Estação Ecológica de Águas Emendadas, DF. PhD thesis, Universidade Estadual de Campinas, Campinas, SP

  • Rodrigues FM (2005) Genética da conservação em duas espécies de canídeos no Parque Nacional das Emas—GO. PhD thesis, Universidade Federal de Goiás, Goiânia, GO

  • Rutledge LY, Holloway JJ, Patterson BR, White BN (2009) An improved field method to obtain DNA for individual identification from wolf scat. J Wildl Manag 73(8):1430–1435. doi:10.2193/2008-492

    Article  Google Scholar 

  • Salim DC, Akimoto AA, Carvalho CB, Oliveira SF, Grisolia CK, Moreira JR, Klautau-Guimaraes MN (2007) Genetic variability in maned wolf based on heterologous short-tandem repeat markers from domestic dog. Genet Mol Res 6(2):348–357

    PubMed  CAS  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning—a laboratory manual, 2nd edn. Cold Spring Habour Laboratory Press, New York

    Google Scholar 

  • Sano EE, Rosa R, Brito JLS, Ferreira LG (2008) Mapeamento semidetalhado do uso da terra do Bioma Cerrado. Pesqu Agropecu Bras 43(1):153–156

    Google Scholar 

  • Santos AS (2005) Subsídios à implantação da gestão ambiental em áreas militares do exército brasileiro, tendo como estudo de caso o campo de instrução de Formosa—GO. Ms thesis, Universidade Católica de Brasília, Brasília, DF

  • Silveira L (1999) Ecologia e conservação dos mamíferos carnívoros do Parque Nacional das Emas, Goiás. Universidade Federal de Goiás, Goiânia

    Google Scholar 

  • Silveira L, Furtado MM, Torres NM, Sollmann R, Uhl G, Jacomo ATA (2009) Maned wolf density in a central Brazilian grassland reserve. J Wildl Manag 73(1):68–71

    Article  Google Scholar 

  • Smith DA, Ralls K, Hurt A, Adams B, Parker M, Maldonado JE (2006) Assessing reliability of microsatellite genotypes from kit fox faecal samples using genetic and GIS analyses. Mol Ecol 15(2):387–406

    Article  PubMed  CAS  Google Scholar 

  • Steinke ET (2004) Considerações sobre variabilidade e mudança climática no Distrito Federal, suas repercussões nos recursos hídricos e informações ao grande público. PhD thesis, Universidade de Brasília, Brasília, DF

  • Stenglein JL, De Barba M, Ausband DE, Waits LP (2010) Impacts of sampling location within a faeces on DNA quality in two carnivore species. Mol Ecol Resour 10(1):109–114. doi:10.1111/j.1755-0998.2009.02670.x

    Article  CAS  Google Scholar 

  • Taberlet P, Griffin S, Goossens B, Questiau S, Manceau V, Escaravage N, Waits LP, Bouvet J (1996) Reliable genotyping of samples with very low DNA quantities using PCR. Nucleic Acids Res 24(16):3189–3194. doi:10.1093/nar/24.16.3189

    Article  PubMed  CAS  Google Scholar 

  • Trolle M, Noss AJ, Lima EDS, Dalponte JC (2007) Camera-trap studies of maned wolf density in the Cerrado and the Pantanal of Brazil. Biodivers Conserv 16(4):1197–1204. doi:10.1007/s10531-006-9105-y

    Article  Google Scholar 

  • Vynne C, Skalski JR, Machado RB, Groom MJ, Jácomo AT, Marinho-Filho J, Neto MBR, Pomilla C, Silveira L, Smith H, Wasser SK (2010) Effectiveness of scat-detection dogs in determining species presence in a tropical savanna landscape. Conserv Biol. doi: 10.1111/j.1523-1739.2010.01581.x

  • Waits LP, Paetkau D (2005) Noninvasive genetic sampling tools for wildlife biologists: a review of applications and recommendations for accurate data collection. J Wildl Manag 69(4):1419–1433

    Article  Google Scholar 

  • Wasser SK, Houston CS, Koehler GM, Cadd GG, Fain SR (1997) Techniques for application of faecal DNA methods to field studies of Ursids. Mol Ecol 6(11):1091–1097

    Article  PubMed  CAS  Google Scholar 

  • Wikramanayake E, McKnight M, Dinerstein E, Joshi A, Gurung B, Smith D (2004) Designing a conservation landscape for tigers in human-dominated environments. Conserv Biol 18(3):839–844

    Article  Google Scholar 

  • Young AG, Clarke GM (eds) (2000) Genetics, demography and viability of fragmented populations, vol 4. Conservation biology. Cambridge University Press, Cambridge

    Google Scholar 

Download references

Acknowledgments

We thank Gilvan de França, Ana Bruzzi-Lion and Fred Vet for field support; Valdir Steinke for the aid in Arcview®; Laila Proença for the veterinarian support; Nazaré Klautau and Daniela Salim for contributing samples; Rafael Ajuz for the help with obtaining the zoo samples; Carlos Fonseca for statistical suggestions and also for all people at PUCRS who helped with laboratory procedures. This study had financial support from Fundação o Boticário de Proteção à Natureza, Idea Wild and Fundação Universidade de Brasília. Marília Lion had a student fellowship from CAPES. Jader Marinho and Eduardo Eizirik received grants from the Brazil’s National Research Council (CNPq) that also supported this project (Process numbers 305415/2007-7 and 490594/2007-7, respectively).

Author information

Authors and Affiliations

  1. Departamento de Zoologia, PPG-Biologia Animal, Instituto de Ciências Biológicas, Universidade de Brasília, Asa Norte, Brasilia, DF, 70910900, Brazil

    Marília Bruzzi Lion & Jader Soares Marinho-Filho

  2. Laboratório de Biologia Genômica e Molecular, Faculdade de Biociências, Pontifícia Universidade Católica do Rio Grande do Sul, Partenon, Porto Alegre, RS, 90619-900, Brazil

    Marília Bruzzi Lion, Eduardo Eizirik & Manoel Ludwig da Fontoura-Rodrigues

  3. Instituto Pró-Carnívoros, Atibaia, SP, Brazil

    Eduardo Eizirik & Flávio Henrique Guimarães Rodrigues

  4. Departamento de Botânica, Ecologia e Zoologia, Centro de Biociências, Universidade Federal do Rio Grande do Norte, Lagoa Nova, Natal, RN, 59072-970, Brazil

    Marília Bruzzi Lion & Adrian Antonio Garda

  5. Departamento de Biologia Geral, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Pampulha, Belo Horizonte, MG, 31270-901, Brazil

    Flávio Henrique Guimarães Rodrigues

Authors
  1. Marília Bruzzi Lion
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Eduardo Eizirik
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Adrian Antonio Garda
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Manoel Ludwig da Fontoura-Rodrigues
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Flávio Henrique Guimarães Rodrigues
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jader Soares Marinho-Filho
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Marília Bruzzi Lion.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 38 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lion, M.B., Eizirik, E., Garda, A.A. et al. Conservation genetics of maned wolves in a highly impacted area of the Brazilian Cerrado biome. Genetica 139, 369–381 (2011). https://doi.org/10.1007/s10709-011-9555-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10709-011-9555-3

Keywords

Search

Navigation