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Modelling the influence of host community composition in a sylvatic Trypanosoma cruzi system

Published online by Cambridge University Press:  13 July 2017

DIANA ERAZO
Affiliation:
BIOMAC-Mathematical and Computational Biology, Universidad de los Andes, Cra 1 este # 19 a-40, Bogota, Colombia
JUAN CORDOVEZ
Affiliation:
BIOMAC-Mathematical and Computational Biology, Universidad de los Andes, Cra 1 este # 19 a-40, Bogota, Colombia
CAROLINA CABRERA
Affiliation:
Department of Pathology, School of Veterinary Medicine, The University of Georgia, 501 DW Brooks Drive, Athens, GA 30602, USA
JOSE E. CALZADA
Affiliation:
Department of Parasitology, Instituto Conmemorativo Gorgas de Estudios de la Salud, Apartado Postal 0816-02593, Panama City, Panama
AZAEL SALDAÑA
Affiliation:
Department of Parasitology, Instituto Conmemorativo Gorgas de Estudios de la Salud, Apartado Postal 0816-02593, Panama City, Panama
NICOLE L. GOTTDENKER*
Affiliation:
Department of Pathology, School of Veterinary Medicine, The University of Georgia, 501 DW Brooks Drive, Athens, GA 30602, USA
*
*Corresponding author: Department of Pathology, School of Veterinary Medicine, The University of Georgia, 501 DW Brooks Drive, Athens, GA 30602, USA. E-mail: gottdenk@gmail.com

Summary

Species composition of wild reservoir hosts can influence the transmission and maintenance of multi-host vector borne pathogens. The ‘pace of life’ hypothesis proposes that the life history strategy of reservoir hosts can influence pathogen transmission of vector borne generalist pathogens. We use empirical data to parameterize a mathematical model that investigates the impacts of host life history traits on vector transmission dynamics of the vector-borne multi-host parasite Trypanosoma cruzi in habitats characterized by different degrees of deforestation and varying host community structure. The model considers susceptible and infected vector and host populations. When comparing the proportion of vectors infected with T. cruzi predicted by the model with empirical data, we found a trend of increasing vector infection as anthropogenic landscape disturbance increases for both data and model output. The model's vector infection rates were significantly lower than empirical results, but when incorporating host congenital transmission in the model, vector infection approaches field data. We conclude that intervened habitats associated with r-selected host species communities predict higher proportions of infected vectors.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2017 

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References

REFERENCES

Abad-Franch, F., Lima, M. M., Sarquis, O., Gurgel-Gonçalves, R., Sánchez-Martín, M., Calzada, J., Saldaña, A., Monteiro, F. A., Palomeque, F. S., Santos, W. S., Angulo, V. M., Esteban, L., Dias, F. B. S., Diotaiuti, L., Bar, M. E. and Gottdenker, N. L. (2015). On palms, bugs, and Chagas disease in the Americas. Acta Tropica 151, 126141.Google Scholar
Alkmim-Oliveira, S. M., Costa-Martins, A. G., Kappel, H. B., Correia, D., Ramirez, L. E. and Lages-Silva, E. (2013). Trypanosoma cruzi experimental congenital transmission associated with TcV and TcI subpatent maternal parasitemia. Parasitology Research 112, 671678.Google Scholar
Añez, N. (1982). Studies on Trypanosoma rangeli Tejera, 1920. III – Direct transmission of Trypanosoma rangeli between triatomine bugs. Memorias do Instituto Oswaldo Cruz 76, 641647.Google Scholar
Añez, N., Crisante, G. and Soriano, P. J. (2009). Trypanosoma cruzi congenital transmission in wild bats. Acta Tropica 109, 7880.CrossRefGoogle ScholarPubMed
Añez, N., Martens, M., Romero, M. and Crisante, G. (2011). Primoinfección por Trypanosoma cruzi previene re-infecciones severas en ratones. Boletín de Malariología y Salud Ambiental 51, 177186.Google Scholar
Basombrío, M. A., Gorla, D., Catalá, S., Segura, M. A., Mora, M. C., Gómez, L. and Nasser, J. (1996). Number of vector bites determining the infection of guinea pigs with Trypanosoma cruzi . Memórias do Instituto Oswaldo Cruz 91, 421423.Google Scholar
Bern, C., Kjos, S., Yabsley, M. J. and Montgomery, S. P. (2011). Trypanosoma cruzi and Chagas’ Disease in the United States. Clinical Microbiology Reviews 24, 655681.Google Scholar
Blackwell, A. D., Snodgrass, J. J., Madimenos, F. C. and Sugiyama, L. S. (2010). Life history, immune function, and intestinal helminths: trade-offs among immunoglobulin E, C-reactive protein, and growth in an Amazonian population. American Journal of Human Biology 22, 836848.CrossRefGoogle Scholar
Carey, J. R. and Judge, D. S. (2002). Longevity Records: Life Spans of Mammals, Birds, Amphibians, Reptiles, and Fish. Odense, Odense University Press.Google Scholar
Carlier, Y., Sosa-Estani, S., Luquetti, A. O. and Buekens, P. (2015). Congenital Chagas disease: an update. Memórias do Instituto Oswaldo Cruz 110, 363368.Google Scholar
Catala, S. S., Gorla, D. E. and Basombrio, M. A. (1992). Vectorial transmission of Trypanosoma cruzi: an experimental field study with susceptible and immunized hosts. American Journal of Tropical Medicine and Hygiene 47, 2026.Google Scholar
Coffield, D. J., Spagnuolo, A. M., Shillor, M., Mema, E., Pell, B., Pruzinsky, A. and Zetye, A. (2013). A Model for Chagas Disease with Oral and Congenital Transmission. PLoS ONE 8, e67267.CrossRefGoogle Scholar
Deane, M. P., Lenzi, H. L. and Jansen, A. (1984). Trypanosoma cruzi: vertebrate and invertebrate cycles in the same mammal host, the opossum Didelphis marsupialis . Memorias do Instituto Oswaldo Cruz. 79, 513515.Google Scholar
De Vasquez, A. M., Samudio, F. E., Saldaña, A., Paz, H. M. and Calzada, J. E. (2004). Eco-epidemiological aspects of Trypanosoma cruzi, Trypanosoma rangeli and their vector (Rhodnius pallescens) in Panama. Revista do Instituto de Medicina Tropical de Sao Paulo 46, 217222.Google Scholar
Diekmann, O., Heesterbeek, J. A. P. and Metz, J. A. J. (1990). On the definition and the computation of the basic reproduction ratio R0 in models for infectious diseases in heterogeneous populations. Journal of Mathematical Biology 28, 365382.Google Scholar
Diekmann, O., Heesterbeek, J. A. P. and Roberts, M. G. (2010). The construction of next-generation matrices for compartmental epidemic models. Journal of the Royal Society, Interface / the Royal Society 7, 873885.Google Scholar
Ernest, S. K. M. (2003). Life history characteristics of placental nonvolant mammals. Ecology 84, 34023402.Google Scholar
Fabrizio, M. C., Schweigmann, N. J. and Bartolini, N. J. (2016). Analysis of the transmission of Trypanosoma cruzi infection through hosts and vectors. Parasitology 143, 111.Google Scholar
Gottdenker, N. L., Chaves, L. F., Calzada, J. E., Saldaña, A. and Carroll, C. R. (2012). Host life history strategy, species diversity, and habitat influence Trypanosoma cruzi vector infection in changing landscapes. PLoS Neglected Tropical Diseases 6, e1884.Google Scholar
Gurtler, R. E., Cecere, M. C., Castanera, M. B., Canale, D., Lauricella, M. A., Chuit, R., Cohen, J. E. and Segura, E. L. (1996). Probability of infection with Trypanosoma cruzi of the vector Triatoma infestans fed on infected humans and dogs in Northwest Argentina. American Journal of Tropical Medicine and Hygiene 55, 2431.Google Scholar
Han, B. A., Schmidt, J. P., Bowden, S. E. and Drake, J. M. (2015). Rodent reservoirs of future zoonotic diseases. Proceedings of the National Academy of Sciences of the United States of America 112, 70397044.Google Scholar
Jansen, A. M., Leon, L., Machado, G. M., da Silva, M. H., Souza-Leão, S. M. and Deane, M. P. (1991). Trypanosoma cruzi in the opossum Didelphis marsupialis: parasitological and serological follow-up of the acute infection. Experimental Parasitology 73, 249259.Google Scholar
Jansen, A. M., Xavier, S. C. C. and Roque, A. L. R. (2015). The multiple and complex and changeable scenarios of the Trypanosoma cruzi transmission cycle in the sylvatic environment. Acta Tropica 151, 115.CrossRefGoogle ScholarPubMed
Johnson, P. T. J., Rohr, J. R., Hoverman, J. T., Kellermanns, E., Bowerman, J., Lunde, K. B., DiAngelo, J. R., Bland, M. L., Bambina, S., Cherry, S. and Birnbaum, M. J. (2012). Living fast and dying of infection: host life history drives interspecific variation in infection and disease risk. Ecology Letters 15, 235242.Google Scholar
Johnson, P. T. J., Preston, D. L., Hoverman, J. T. and Richgels, K. L. D. (2013). Biodiversity decreases disease through predictable changes in host community competence. Nature 494, 230233.Google Scholar
Kribs-Zaleta, C. (2010). Estimating contact process saturation in sylvatic transmission of Trypanosoma cruzi in the United States. PLoS Neglected Tropical Diseases 4, e656.Google Scholar
Lee, K. A., Wikelski, M., Robinson, W. D., Robinson, T. R. and Klasing, K. C. (2008). Constitutive immune defences correlate with life-history variables in tropical birds. Journal of Animal Ecology 77, 356363.Google Scholar
Lochmiller, R. L. and Deerenberg, C. (2000). Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 88, 8798.Google Scholar
Marinkelle, C. (1965). Direct transmission between individuals of Rhodnius prolixus Stal. Revista Biología Tropical 13, 5558.Google Scholar
Martin, L. B., Weil, Z. M., Kuhlman, J. R. and Nelson, R. J. (2006). Trade-offs within the immune systems of female white-footed mice, Peromyscus leucopus . Functional Ecology 20, 630636.CrossRefGoogle Scholar
Miller, B. L. W. and Sinervo, B. (2007). Heritable body size mediates apparent life-history trade-offs in a simultaneous hermaphrodite. Journal of Evolutionary Biology 20, 15541562.CrossRefGoogle Scholar
Monteiro, F. A., Wesson, D. M., Dotson, E. M., Schofield, C. J. and Beard, C. B. (2000). Phylogeny and molecular taxonomy of the rhodniini derived from mitochondrial and nuclear DNA sequences. American Journal of Tropical Medicine and Hygiene 62, 460465.CrossRefGoogle ScholarPubMed
Nouvellet, P., Dumonteil, E. and Gourbière, S. (2013). The improbable transmission of Trypanosoma cruzi to human: the missing link in the dynamics and control of Chagas disease. PLoS Neglected Tropical Diseases 7, e2505.Google Scholar
Orozco, M. M., Enriquez, G. F., Cardinal, M. V., Piccinali, R. V. and Gürtler, R. E. (2016). A comparative study of Trypanosoma cruzi infection in sylvatic mammals from a protected and a disturbed area in the Argentine Chaco. Acta Tropica 155, 3442.CrossRefGoogle Scholar
Ostfeld, R. S., Levi, T., Jolles, A. E., Martin, L. B., Hosseini, P. R. and Keesing, F. (2014). Life history and demographic drivers of reservoir competence for three tick-borne zoonotic pathogens. PLoS ONE 9, e107387.Google Scholar
Perlowagora-Szumlewicz, A., Muller, C. A. and Moreira, C. J. (1990). Studies in search of a suitable experimental insect model for xenodiagnosis of hosts with Chagas’ disease. 4 – the reflection of parasite stock in the responsiveness of different vector species to chronic infection with different Trypanosoma cruzi stocks. Revista de Saude Publica 24, 165177.CrossRefGoogle ScholarPubMed
Peterson, J. K., Bartsch, S. M., Lee, B. Y. and Dobson, A. P. (2015). Broad patterns in domestic vector-borne Trypanosoma cruzi transmission dynamics: synanthropic animals and vector control. Parasites & vectors 8, 537.Google Scholar
Poulin, R. and Morand, S. (2004). Parasite Biodiversity. Smithsonian Books, Washington, DC.Google Scholar
Previtali, M. A., Ostfeld, R. S., Keesing, F., Jolles, A. E., Hanselmann, R. and Martin, L. B. (2012). Relationship between pace of life and immune responses in wild rodents. Oikos 121, 14831492.Google Scholar
Rabinovich, J. E. and Nieves, E. L. (2011). Vital statistics of Triatominae (Hemiptera: Reduviidae) under laboratory conditions: III. Rhodnius neglectus . Journal of Medical Entomology 48, 775787.Google Scholar
Rabinovich, J. E., Wisnivesky-Colli, C., Solarz, N. and Gürtler, R. (1990). Probability of transmission of Chagas disease by Triatoma infestans (Hemiptera: Reduviidae) in an endemic area of Santiago del Estero, Argentina. Bulletin of the WHO 68, 737746.Google Scholar
Rabinovich, J. E., Schweigmann, N., Yohai, V. and Wisnivesky-Colli, C. (2001). Probability of Trypanosoma cruzi transmission by Triatoma infestans (Hemiptera: Reduviidae) to the opossum Didelphis albiventris (Marsupialia: Didelphidae). American Journal of Tropical Medicine and Hygiene 65, 125130.Google Scholar
R Development Core Team (2016). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN: 3-900051-07-0.Google Scholar
Rocha, F. L., Roque, A. L. R., de Lima, J. S., Cheida, C. C., Lemos, F. G., de Azevedo, F. C., Arrais, R. C., Bilac, D., Herrera, H. M., Mourão, G. and Jansen, A. M. (2013). Trypanosoma cruzi infection in neotropical wild carnivores (Mammalia: Carnivora): at the top of the T. cruzi transmission chain. PLoS ONE 8, e67463.Google Scholar
Roellig, D. M., Ellis, A. E. and Yabsley, M. J. (2009). Oral transmission of Trypanosoma cruzi with opposing evidence for the theory of carnivory. Journal of parasitology 95, 360364.Google Scholar
Ryckman, R. (1951). Recent observations of cannibalism in Triatoma (Reduviidae). Journal of Parasitology 37, 433434.CrossRefGoogle ScholarPubMed
Schaub, G. (1988). Direct transmission of Trypanosoma cruzi between vectors of Chagas’ disease. Acta tropica 45, 1119.Google Scholar
Soetaert, K., Meysman, F. and Petzoldt, T. (2010). Solving differential equations in R. In AIP Conference Proceedings, pp. 31–34.Google Scholar
Spagnuolo, A. M., Shillor, M. and Stryker, G. A. (2011). A model for Chagas disease with controlled spraying. Journal of Biological Dynamics 5, 299317.Google Scholar
Suarez-Davalos, V., Dangles, O., Villacis, A. G. and Grijalva, M. J. (2010). Microdistribution of sylvatic triatomine populations in central-coastal ecuador. Journal of Medical Entomology 47, 8088.Google Scholar
Tacutu, R., Craig, T., Budovsky, A., Wuttke, D., Lehmann, G., Taranukha, D., Costa, J., Fraifeld, V. E. and De Magalhães, J. P. (2012). Human ageing genomic resources: integrated databases and tools for the biology and genetics of ageing. Nucleic Acids Research 41, gks1155.Google Scholar
Urbano, P., Poveda, C. and Molina, J. (2015). Effect of the physiognomy of Attalea butyracea (Arecoideae) on population density and age distribution of Rhodnius prolixus (Triatominae). Parasites & Vectors 8, 112.Google Scholar
Vaz, V. C., D'Andrea, P. S. and Jansen, A. M. (2007). Effects of habitat fragmentation on wild mammal infection by Trypanosoma cruzi . Parasitology 134, 17851793.Google Scholar
Weigl, R. (2005). Longevity of Mammals in Captivity; from the Living Collections of the World. A List of Mammalian Longevity in Captivity. E. Schweizerbart'sche, Stuttgart.Google Scholar
Yoshida, N. (2008). Trypanosoma cruzi infection by oral route. How the interplay between parasite and host components modulates infectivity. Parasitology International 57, 105109.Google Scholar
Yoshida, N. (2009). Molecular mechanisms of Trypanosoma cruzi infection by oral route. Memórias do Instituto Oswaldo Cruz 104(Suppl), 101107.Google Scholar
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