• 1.

    Patz JA, Graczyk TK, Geller N, Vittor AY, 2000. Effects of environmental change on emerging parasitic diseases. Int J Parasitol 30: 13951405.

  • 2.

    Sutherst RW, 2004. Global change and human vulnerability to vector-borne diseases. Clin Microbiol Rev 17: 136173.

  • 3.

    Walsh JF, Molyneux DH, Birley HM, 1993. Deforestation: effects on vector-borne disease. Parasitology 106 (Suppl): S55S75.

  • 4.

    Gratz NG, 1999. Emerging and resurging vector-borne diseases. Annu Rev Entomol 44: 5175.

  • 5.

    Yasuoka J, Levins R, 2007. Impact of deforestation and agricultural development on anopheline ecology and malaria epidemiology. Am J Trop Med Hyg 76: 450460.

    • Search Google Scholar
    • Export Citation
  • 6.

    Vora N, 2008. Impact of anthropogenic environmental alterations on vector-borne diseases. Medscape J Med 10: 238 [Epub Oct 15, 2008].

  • 7.

    Vittor AY, Gilman RH, Tielsch J, Glass G, Shields T, Lozano WS, Pinedo-Cancino V, Patz JA, 2006. The effect of deforestation on the human biting rate of Anopheles darlingi, the primary vector of falciparum malaria in the Peruvian Amazon. Am J Trop Med Hyg 74: 311.

    • Search Google Scholar
    • Export Citation
  • 8.

    Yanoviak SP, Paredes JE, Lounibos LP, Weaver SC, 2006. Deforestation alters phytotelm habitat availability and mosquito production in the Peruvian Amazon. Ecol Appl 16: 18541864.

    • Search Google Scholar
    • Export Citation
  • 9.

    Minakawa N, Omukunda E, Zhou G, Githeko A, Yan G, 2006. Malaria vector productivity in relation to the highland environment in Kenya. Am J Trop Med Hyg 75: 448453.

    • Search Google Scholar
    • Export Citation
  • 10.

    Fahrig L, 2003. Effects of habitat fragmentation on biodiversity. Annu Rev Ecol Evol Syst 34: 487515.

  • 11.

    Allan BF, Keesing F, Ostfeld RS, 2003. Effect of forest fragmentation on Lyme disease risk. Conserv Biol 17: 267272.

  • 12.

    Brownstein JS, Skelly DK, Holford TR, Fish D, 2005. Forest fragmentation predicts local scale heterogeneity of Lyme disease risk. Oecologia 146: 469475.

    • Search Google Scholar
    • Export Citation
  • 13.

    Wasserberg G, Yarom I, Warburg A, 2003. Seasonal abundance patterns of the sandfly Phlebotomus papatasi in climatically distinct foci of cutaneous leishmaniasis in Israeli desert. Med Vet Entomol 17: 452456.

    • Search Google Scholar
    • Export Citation
  • 14.

    Forman HTT, Godron M, 1986. Landscape Ecology. New York: John Wiley and Sons, Inc.

  • 15.

    Whitlaw JT, Chaniotis BN, 1978. Palm trees and Chagas disease in Panama. Am J Trop Med Hyg 27: 873881.

  • 16.

    Christensen HA, Devasquez AM, 1981. Host feeding profiles of Rhodnius pallescens (Hemiptera, Reduviidae) in rural villages of Central Panama. Am J Trop Med Hyg 30: 278283.

    • Search Google Scholar
    • Export Citation
  • 17.

    Zeledon R, Ugalde JA, Paniagua LA, 2001. Entomological and ecological aspects of six sylvatic species of triatomines (Hemiptera, Reduviidae) from the collection of the National Biodiversity Institute of Costa Rica, Central America. Mem Inst Oswaldo Cruz 96: 757764.

    • Search Google Scholar
    • Export Citation
  • 18.

    Zeledon R, Marin F, Calvo N, Lugo E, Valle S, 2006. Distribution and ecological aspects of Rhodnius pallescens in Costa Rica and Nicaragua and their epidemiological implications. Mem Inst Oswaldo Cruz 101: 7579.

    • Search Google Scholar
    • Export Citation
  • 19.

    Zeledon R, Rabinovich JE, 1981. Chagas' disease: an ecological appraisal with special emphasis on its insect vectors. Annu Rev Entomol 26: 101133.

    • Search Google Scholar
    • Export Citation
  • 20.

    Tarleton RL, Reithinger R, Urbina JA, Kitron U, Gurtler RE, 2007. The challenges of Chagas disease – grim outlook or glimmer of hope. PLoS Med 4: e332.

    • Search Google Scholar
    • Export Citation
  • 21.

    Gurtler RE, Diotaiuti L, Kitron U, 2008. Commentary: Chagas disease: 100 years since discovery and lessons for the future. Int J Epidemiol 37: 698701.

    • Search Google Scholar
    • Export Citation
  • 22.

    Dias Fernando BS, Bezerra CM, Machado EMM, Casanova C, Diotaiuti L, 2008. Ecological aspects of Rhodnius nasutus Stal, 1859 (Hemiptera: Reduviidae: Triatominae) in palms of the Chapada do Araripe in Ceara, Brazil. Mem Inst Oswaldo Cruz 103: 824830.

    • Search Google Scholar
    • Export Citation
  • 23.

    Fitzpatrick S, Feliciangeli MD, Sanchez-Martin MJ, Monteiro FA, Miles MA, 2008. Molecular genetics reveal that sylvatic Rhodnius prolixus do colonise rural houses. PLoS Negl Trop Dis 2: e210.

    • Search Google Scholar
    • Export Citation
  • 24.

    Medina M, Martínez C, Hernandez M, Duque N, Toyo J, Rangel R, 2007. Risk factors for Trypanosoma cruzi human infection in Barinas State, Venezuela. Am J Trop Med Hyg 76: 915921.

    • Search Google Scholar
    • Export Citation
  • 25.

    Sanchez-Martin MJ, Feliciangeli MD, Campbell-Lendrum D, Davies CR, 2006. Could the Chagas disease elimination programme in Venezuela be compromised by reinvasion of houses by sylvatic Rhodnius prolixus bug populations? Trop Med Int Health 11: 15851593.

    • Search Google Scholar
    • Export Citation
  • 26.

    Abad-Franch F, Palomeque FS, Aguilar HM IV, Miles MA, 2005. Field ecology of sylvatic Rhodnius populations (Heteroptera, Triatominae): risk factors for palm tree infestation in western Ecuador. Trop Med Int Health 10: 12581266.

    • Search Google Scholar
    • Export Citation
  • 27.

    Vasquez AM, Samudio FE, Saldaña A, Paz HM, Calzada JE, 2004. Eco- epidemiological aspects of Trypanosoma cruzi, Trypanosoma rangeli and their vector (Rhodnius pallescens) in Panama. Rev Inst Med Trop Sao Paulo 46: 217222.

    • Search Google Scholar
    • Export Citation
  • 28.

    Wright SJ, Duber HC, 2001. Poachers and forest fragmentation alter seed dispersal, seed survival, and seedling recruitment in the palm Attalea butyracea, with implications for tropical tree diversity. Biotropica 33: 583595.

    • Search Google Scholar
    • Export Citation
  • 29.

    Condit RW, Robinson D, Ibez R, Aguilar S, Sanjur A, Martínez R, Stallard RF, García T, Angehr GR, Petit L, Wright SJ, Robinson T, Heckadon MS, 2001. The status of the Panama Canal watershed and its biodiversity at the beginning of the 21st century. Bioscience 51: 389398.

    • Search Google Scholar
    • Export Citation
  • 30.

    Ibanez R, Condit R, Angehr G, Aguilar S, Garcia T, Martinez R, Sanjur A, Stallard RF, Wright SJ, Stanley A, Heckadon-Moreno S, 2002. An ecosystem report on the Panama Canal: monitoring the status of the forest communities and the watershed. Environ Monit Assess 80: 6595.

    • Search Google Scholar
    • Export Citation
  • 31.

    Calzada JE, Pineda V, Montalvo E, Alvarez D, Santamaria AM, Samudio F, Bayard V, Cáceres L, Saldaña A, 2006. Human trypanosome infection and the presence of intradomicile Rhodnius pallescens in the western border of the Panama Canal, Panama. Am J Trop Med Hyg 74: 762765.

    • Search Google Scholar
    • Export Citation
  • 32.

    Abad-Franch F, Monteiro FA, Jaramillo ON, Gurgel-Goncalves R, Dias FB, Diotaiuti L, 2009. Ecology, evolution, and the long-term surveillance of vector-borne Chagas disease: a multi-scale appraisal of the tribe Rhodniini (Triatominae). Acta Trop 110: 159177.

    • Search Google Scholar
    • Export Citation
  • 33.

    Holdridge LR, 1967. Life Zone Ecology. San Jose, Costa Rica: Tropical Science Center.

  • 34.

    Gomez-Nunez JC, 1969. Resting places, dispersal and survival of CO60-tagged adult Rhodnius prolixus. J Med Entomol 6: 8386.

  • 35.

    Noireau F, Flores R, Vargas F, 1999. Trapping sylvatic Triatominae (Reduviidae) in hollow trees. Trans R Soc Trop Med Hyg 93: 1314.

  • 36.

    Abad-Franch F, Noireau F, Paucar A, Aguilar HM, Carpio C, Racines J, 2000. The use of live-bait traps for the study of sylvatic Rhodnius populations (Hemiptera: Reduviidae) in palm trees. Trans R Soc Trop Med Hyg 94: 629630.

    • Search Google Scholar
    • Export Citation
  • 37.

    Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Stevens MH, White JS, 2009. Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 24: 127135.

    • Search Google Scholar
    • Export Citation
  • 38.

    Laird NM, Ware JH, 1982. Random-effects models for longitudinal data. Biometrics 38: 963974.

  • 39.

    Romana CA, Pizarro JC, Rodas E, Guilbert E, 1999. Palm trees as ecological indicators of risk areas for Chagas disease. Trans R Soc Trop Med Hyg 93: 594595.

    • Search Google Scholar
    • Export Citation
  • 40.

    Teixeira AR, Monteiro PS, Rebelo JM, Rebelo JM, Argañaraz 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: 100112.

    • Search Google Scholar
    • Export Citation
  • 41.

    Abad-Franch F, Ferraz G, Campos C, Palomeque FS, Grijalva MJ, Aguilar HM, Miles MA, 2010. Modeling disease vector occurrence when detection is imperfect: infestation of Amazonian palm trees by Triatomine bugs at three spatial scales. PLoS Negl Trop Dis 4: e620.

    • Search Google Scholar
    • Export Citation
  • 42.

    Bar ME, Wisnivesky-Colli C, 2001. Triatoma sordida Stal 1859 (Hemiptera, Reduviidae: Triatominae) in palms of northeastern Argentina. Mem Inst Oswaldo Cruz 96: 895899.

    • Search Google Scholar
    • Export Citation
  • 43.

    Gurgel-Goncalves R, Palma AR, Menezes MN, Leite RN, Cuba CA, 2003. Sampling Rhodnius neglectus in Mauritia flexuosa palm trees: a field study in the Brazilian savanna. Med Vet Entomol 17: 347350.

    • Search Google Scholar
    • Export Citation
  • 44.

    Jabin D, 2001. Le Palmier Attalea butyracea comme Indicateur du Risque Ecologique de la Trypanosomose Americaine dans la Province de Panama. Report to the Laboratory. Paris: IRD-CEREG.

    • Search Google Scholar
    • Export Citation
  • 45.

    D'Alessandro A, Barreto P, Saravia N, Barreto M, 1984. Epidemiology of Trypanosoma cruzi in the oriental plains of Colombia. Am J Trop Med Hyg 33: 10841095.

    • Search Google Scholar
    • Export Citation
  • 46.

    Gurgel-Goncalves R, Duarte MA, Ramalho ED, Palma AR, Romana CA, Cuba-Cuba CA, 2004. Spatial distribution of Triatominae populations (Hemiptera: Reduviidae) in Mauritia flexuosa palm trees in Federal District of Brazil. Rev Soc Bras Med Trop 37: 241247.

    • Search Google Scholar
    • Export Citation
  • 47.

    Terborgh J, Lopez L, Nuñez P, Rao M, Shahabuddin G, Orihuela G, Riveros M, Ascanio R, Adler GH, Lambert TD, Balbas L, 2001. Ecological meltdown in predator-free forest fragments. Science 294: 19231926.

    • Search Google Scholar
    • Export Citation
  • 48.

    Gascon C, Lovejoy TE, Bierregaard RO, Malcolm JR, Stouffer PC, Vasconcelos HL, Laurance WF, Zimmerman B, Tocher M, Borges S, 1999. Matrix habitat and species richness in tropical forest remnants. Biol Conserv 91: 223229.

    • Search Google Scholar
    • Export Citation
  • 49.

    Goodrich JM, Buskirk SW, 1995. Control of abundant native vertebrates for conservation of endangered species. Conserv Biol 9: 13571364.

  • 50.

    Laurance WF, Laurance SG, Hilbert DW, 2008. Long-term dynamics of a fragmented rainforest mammal assemblage. Conserv Biol 22: 11541164.

  • 51.

    Luz C, Fargues J, 1999. Dependence of the entomopathogenic fungus, Beauveria bassiana, on high humidity for infection of Rhodnius prolixus. Mycopathologia 146: 3341.

    • Search Google Scholar
    • Export Citation
  • 52.

    Fargues J, Luz C, 2000. Effects of fluctuating moisture and temperature regimes on the infection potential of Beauveria bassiana for Rhodnius prolixus. J Invertebr Pathol 75: 202211.

    • Search Google Scholar
    • Export Citation
  • 53.

    Ceballos LA, Vazquez-Prokopec GM, Cecere MC, Marcet PL, Gürtler RE, 2005. Feeding rates, nutritional status and flight dispersal potential of peridomestic populations of Triatoma infestans in rural northwestern Argentina. Acta Trop 95: 149159.

    • Search Google Scholar
    • Export Citation
  • 54.

    Chaves LF, Cohen JM, Pascual M, Wilson ML, 2008. Social exclusion modifies climate and deforestation impacts on a vector-borne disease. PLoS Negl Trop Dis 2: e176.

    • Search Google Scholar
    • Export Citation
  • 55.

    Vazquez-Prokopec GM, Ceballos LA, Marcet PL, Cecere MC, Cardinal MV, Kitron U, Gürtler RE, 2006. Seasonal variations in active dispersal of natural populations of Triatoma infestans in rural north-western Argentina. Med Vet Entomol 20: 273279.

    • Search Google Scholar
    • Export Citation
  • 56.

    Cardinal MV, Lauricella MA, Ceballos LA, Lanati L, Marcet PL, Levin MJ, Kitron U, Gürtler RE, Schijman AG, 2008. Molecular epidemiology of domestic and sylvatic Trypanosoma cruzi infection in rural northwestern Argentina. Int J Parasitol 38: 153315.

    • Search Google Scholar
    • Export Citation

 

 

 

 

Association of Anthropogenic Land Use Change and Increased Abundance of the Chagas Disease Vector Rhodnius pallescens in a Rural Landscape of Panama

View More View Less
  • Department of Pathology, College of Veterinary Medicine, and Odum School of Ecology, The University of Georgia, Athens, Georgia; Department of Parasitology, Instituto Conmemorativo Gorgas de Estudios de la Salud, Panama City, Panama

Anthropogenic disturbance is associated with increased vector-borne infectious disease transmission in wildlife, domestic animals, and humans. The objective of this study was to evaluate how disturbance of a tropical forest landscape impacts abundance of the triatomine bug Rhodnius pallescens, a vector of Chagas disease, in the region of the Panama Canal in Panama. Rhodnius pallescens was collected (n = 1,186) from its primary habitat, the palm Attalea butyracea, in five habitat types reflecting a gradient of anthropogenic disturbance. There was a high proportion of palms infested with R. pallescens across all habitat types (range = 77.1–91.4%). Results show that disturbed habitats are associated with increased vector abundance compared with relatively undisturbed habitats. Bugs collected in disturbed sites, although in higher abundance, tended to be in poor body condition compared with bugs captured in protected forest sites. Abundance data suggests that forest remnants may be sources for R. pallescens populations within highly disturbed areas of the landscape.

Author Notes

*Address correspondence to Nicole L. Gottdenker, Department of Pathology, School of Veterinary Medicine, The University of Georgia, 501 DW Brooks Drive, Athens, GA 30602. E-mail: gottdenk@gmail.com

Financial support: This study was supported by Environmental Protection Agency STAR Science to Achieve Results Fellowship FP-91669001, Sigma Xi Scientific Research Grant G200803150739, a University of Georgia Graduate School Dissertation Completion Award, a Dean A. Lindholm Memorial Travel Award, and a University of Georgia Center for Latin American Studies Scholarship. Scholarship support was also provided by the Wildlife Disease Association.

Disclosure: Funding sources have not officially endorsed this publication and the views expressed herein may not reflect their views.

Authors' addresses: Nicole L. Gottdenker, Department of Pathology, School of Veterinary Medicine, The University of Georgia, Athens, GA, E-mail: gottdenk@gmail.com. José E. Calzada and Azäel Saldaña, Department of Parasitology, Instituto Conmemorativo Gorgas de Estudios de la Salud, Apartado Postal 0816-02593, Panama City, Panama, E-mails: jcalzada@gorgas.gob.pa and asaldana@gorgas.gob.pa. C. Ronald Carroll, Odum School of Ecology, Ecology Building, The University of Georgia, Athens, GA, E-mail: ronecology@gmail.com.

Save