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Trypanosoma cruzi–Trypanosoma rangeli co-infection ameliorates negative effects of single trypanosome infections in experimentally infected Rhodnius prolixus

Published online by Cambridge University Press:  13 May 2016

JENNIFER K. PETERSON ,
ANDREA L. GRAHAM ,
RYAN J. ELLIOTT ,
ANDREW P. DOBSON  and
OMAR TRIANA CHÁVEZ
JENNIFER K. PETERSON*
Affiliation:
Department of Ecology and Evolutionary Biology, Princeton University, Princeton, New Jersey 08544, USA
ANDREA L. GRAHAM
Affiliation:
Department of Ecology and Evolutionary Biology, Princeton University, Princeton, New Jersey 08544, USA
RYAN J. ELLIOTT
Affiliation:
Department of Ecology and Evolutionary Biology, Princeton University, Princeton, New Jersey 08544, USA
ANDREW P. DOBSON
Affiliation:
Department of Ecology and Evolutionary Biology, Princeton University, Princeton, New Jersey 08544, USA
OMAR TRIANA CHÁVEZ
Affiliation:
Grupo BCEI, Universidad de Antioquia, Calle 70 No. 52-21, Medellín, Colombia
*
*Corresponding author: Department of Ecology and Evolutionary Biology, Princeton University, Princeton, New Jersey 08544, USA. E-mail: [email protected]
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Summary

Trypanosoma cruzi, causative agent of Chagas disease, co-infects its triatomine vector with its sister species Trypanosoma rangeli, which shares 60% of its antigens with T. cruzi. Additionally, T. rangeli has been observed to be pathogenic in some of its vector species. Although T. cruzi–T. rangeli co-infections are common, their effect on the vector has rarely been investigated. Therefore, we measured the fitness (survival and reproduction) of triatomine species Rhodnius prolixus infected with just T. cruzi, just T. rangeli, or both T. cruzi and T. rangeli. We found that survival (as estimated by survival probability and hazard ratios) was significantly different between treatments, with the T. cruzi treatment group having lower survival than the co-infected treatment. Reproduction and total fitness estimates in the T. cruzi and T. rangeli treatments were significantly lower than in the co-infected and control groups. The T. cruzi and T. rangeli treatment group fitness estimates were not significantly different from each other. Additionally, co-infected insects appeared to tolerate higher doses of parasites than insects with single-species infections. Our results suggest that T. cruzi–T. rangeli co-infection could ameliorate negative effects of single infections of either parasite on R. prolixus and potentially help it to tolerate higher parasite doses.

Keywords

Trypanosoma cruziTrypanosoma rangeliRhodnius prolixusT. cruzi–T. rangeli co-infectionChagas diseaseinfected-vector fitness
Type
Research Article
Information
Parasitology , Volume 143 , Issue 9 , August 2016 , pp. 1157 - 1167
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Copyright © Cambridge University Press 2016 

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References

REFERENCES

Añez, N. (1984). Studies on Trypanosoma rangeli Tejera 1920. VII – Its effect on the survival of infected triatomine bugs. Memorias do Instituto Oswaldo Cruz Inst Oswaldo Cruz 79, 249–255.Google Scholar
Añez, N., Nieves, E. and Cazorla, D. (1987). Studies on Trypanosoma rangeli Tejera, 1920. IX. Course of infection in different stages of Rhodnius prolixus. Memorias do Instituto Oswaldo Cruz 82, 1–6.Google Scholar
Añez, N., Molero, M., Valderrama, E., Nieves, D., Cazorla, M. and Márquez, V. (1992). Studies on Trypanosoma rangeli Tejera, 1920 X- Its comparison with Trypanosoma cruzi Chagas, 1909. Infection in different stages of Rhodnius prolixus Stal, 1859. KASMERA 20, 35–51.Google Scholar
Araújo, C. A. C., Cabello, P. H. and Jansen, A. M. (2007). Growth behaviour of two Trypanosoma cruzi strains in single and mixed infections: in vitro and in the intestinal tract of the blood-sucking bug, Triatoma brasiliensis . Acta tropica 101, 225–231.CrossRefGoogle ScholarPubMed
Araújo, C. a C., Waniek, P. J. and Jansen, A. M. (2014). TcI/TcII co-infection can enhance Trypanosoma cruzi growth in Rhodnius prolixus. Parasites & Vectors 7, 94.Google Scholar
Asin, S. and Catalá, S. (1995). Development of Trypanosoma cruzi in Triatoma infestans: influence of temperature and blood consumption. Journal of Parasitology 81, 1–7.CrossRefGoogle ScholarPubMed
Azambuja, P., Feder, D. and Garcia, E. S. (2004). Isolation of Serratia marcescens in the midgut of Rhodnius prolixus: impact on the establishment of the parasite Trypanosoma cruzi in the vector. Experimental Parasitology 107, 89–96.CrossRefGoogle ScholarPubMed
Azambuja, P., Garcia, E. S. and Ratcliffe, N. a. (2005). Gut microbiota and parasite transmission by insect vectors. Trends in Parasitology 21, 568–572.Google Scholar
Basso, B. (2013). Modulation of immune response in experimental Chagas disease. World Journal of Experimental Medicine 3, 1–10.CrossRefGoogle ScholarPubMed
Basso, B., Moretti, E. and Votrero-cima, E. (1991). Immune response and Trypanosoma cruzi infection in Trypanosoma rangeli-immunized mice. American Journal of Tropical Medicine and Hygiene 44, 413–419.CrossRefGoogle ScholarPubMed
Basso, B., Castro, I., Introini, V., Gil, P., Truyens, C. and Moretti, E. (2007). Vaccination with Trypanosoma rangeli reduces the infectiousness of dogs experimentally infected with Trypanosoma cruzi . Vaccine 25, 3855–3858.CrossRefGoogle ScholarPubMed
Basso, B., Moretti, E. and Fretes, R. (2008). Vaccination with epimastigotes of different strains of Trypanosoma rangeli protects mice against Trypanosoma cruzi infection. Memórias do Instituto Oswaldo Cruz 103, 370–374.Google Scholar
Basso, B., Moretti, E. and Fretes, R. (2014). Vaccination with Trypanosoma rangeli induces resistance of guinea pigs to virulent Trypanosoma cruzi . Veterinary Immunology and Immunopathology 157, 119–123.CrossRefGoogle ScholarPubMed
Bice, D. E. and Zeledon, R. (1970). Comparison of Infectivity of Strains of Trypanosoma cruzi (Chagas, 1909). The Journal of Parasitology 56, 663–670.Google Scholar
Borges, E. C., Machado, E. M. M., Garcia, E. S. and Azambuja, P. (2006). Trypanosoma cruzi: effects of infection on cathepsin D activity in the midgut of Rhodnius prolixus . Experimental Parasitology 112, 130–133.Google Scholar
Botto-Mahan, C. (2009). Trypanosoma cruzi induces life-history trait changes in the wild kissing bug Mepraia spinolai: implications for parasite transmission. Vector Borne and Zoonotic Diseases (Larchmont, N.Y.) 9, 505–510.CrossRefGoogle ScholarPubMed
Buxton, P. (1930). The biology of a blood-sucking bug, Rhodnius prolixus . The Transactions of the Entomological Society of London 78, 227–256.Google Scholar
Calzada, J. E., Pineda, V., Garisto, J. D., Samudio, F., Santamaria, A. M. and Saldaña, A. (2010). Human trypanosomiasis in the eastern region of the Panama Province: new endemic areas for Chagas disease. The American Journal of Tropical Medicine and Hygiene 82, 580–582.CrossRefGoogle ScholarPubMed
Carcavallo, R. U., Martinez Silva, R., Otero, A.M.A. and Tonn, R. J. (1975). Infeccion natural de Rhodnius robustus Larrouse y Rhodnius pictipes Stal por T. cruzi y T. rangeli en Venezuela. Boletin de la Dirrecion de Malaiologia y Saneamiento Ambiental 15, 117–120.Google Scholar
Castro, D. P., Moraes, C. S., Garcia, E. S. and Azambuja, P. (2007). Inhibitory effects of d-mannose on trypanosomatid lysis induced by Serratia marcescens . Experimental Parasitology 115, 200–204.Google Scholar
Castro, D. P., Moraes, C. S., Gonzalez, M. S., Ratcliffe, N. a., Azambuja, P. and Garcia, E. S. (2012). Trypanosoma cruzi immune response modulation decreases microbiota in Rhodnius prolixus gut and is crucial for parasite survival and development. PLoS ONE 7, e36591.Google Scholar
Castro, L. A., Peterson, J. K., Saldaña, A., Perea, M. Y., Calzada, J. E., Pineda, V., Dobson, A. P. and Gottdenker, N. L. (2014). Flight behavior and performance of Rhodnius pallescens (Hemiptera: Reduviidae) on a tethered flight mill. Journal of Medical Entomology 51, 1010–1018.CrossRefGoogle ScholarPubMed
Chiang, R. G., Chiang, J. A., Hoogendoorn, H. and Lima, M. M. (2013). Exploring the role of rhodtestolin, a cardio-inhibitor from the testes of Rhodnius prolixus, in relation to the structure and function of reproductive organs in insect vectors of Chagas disease. Insects 4, 593–608.Google Scholar
Chowdury, M. and Fistein, B. (1986). Excretion of Trypanosoma cruzi by various stages of Rhodnius prolixus . International Journal for Parasitology 16, 353–359.Google Scholar
Cox, D. R. (1972). Regression models and life-tables. Journal of the Royal Statistical Society B, 34, 187–220.Google Scholar
Cox, F. E. (2001). Concomitant infections, parasites and immune responses. Parasitology 122 (Suppl.), S23–S38.CrossRefGoogle ScholarPubMed
Cummings, K. L. and Tarleton, R. L. (2003). Rapid quantitation of Trypanosoma cruzi in host tissue by real-time PCR. Molecular and Biochemical Parasitology 129, 53–59.Google Scholar
D'Alessandro, A. and Mandel, S. (1969). Natural infections and behavior of Trypanosoma rangeli and Trypanosoma cruzi in the vector Rhodnius prolixus in Colombia. Journal of Parasitology 55, 846–852.CrossRefGoogle ScholarPubMed
Davey, K. (1965). Copulation and egg-production in Rhodnius prolixus: the role of the spermathecae. Journal of Experimental Biology 42, 373–378.Google Scholar
De Moraes, A. M. L., Reis-de-Figueiredo, A., Vieira-Junqueira, a. C., Lara-da-Costa, G., Aguiar, R. K. and Cunha-de-Oliveira, P. (2001). Fungal flora of the digestive tract of Panstrongylus megistus (Reduviidae) used for experimental xenodiagnosis of Trypanosoma (Schizotripanum) cruzi Chagas, 1909. Revista iberoamericana de micología 18, 79–82.Google Scholar
De Moraes, A. M. L., Junqueira, A. C. V., Celano, V., Da Costa, G. L. and Coura, J. R. (2004). Fungal flora of the digestive tract of Rhodnius prolixus, Rhodnius neglectus, Diptelanogaster maximus and Panstrongylus megistus, vectors of Trypanosoma cruzi, Chagas, 1909. Brazilian Journal of Microbiology 35, 288–291.CrossRefGoogle Scholar
Dobson, A. (1985). The population dynamics of competition between parasites. Parasitology 91, 317–347.Google Scholar
Eichler, S. and Schaub, G. A. (2002). Development of symbionts in triatomine bugs and the effects of infections with trypanosomatids. Experimental Parasitology 100, 17–27.Google Scholar
Elliot, S. L., Rodrigues, J. D. O., Lorenzo, M. G., Martins-Filho, O. a. and Guarneri, A. a. (2015). Trypanosoma cruzi, Etiological agent of chagas disease, is virulent to its Triatomine vector Rhodnius prolixus in a temperature-dependent manner. PLoS Neglected Tropical Diseases 9, e0003646.Google Scholar
Espino, C. I., Gómez, T., González, G., do Santos, M. F. B., Solano, J., Sousa, O., Moreno, N., Windsor, D., Ying, A., Vilchez, S. and Osuna, A. (2009). Detection of Wolbachia bacteria in multiple organs and feces of the triatomine insect Rhodnius pallescens (Hemiptera, Reduviidae). Applied and Environmental Microbiology 75, 547–550.CrossRefGoogle ScholarPubMed
Falla, A., Herrera, C., Fajardo, A., Montilla, M., Vallejo, G. A. and Guhl, F. (2009). Haplotype identification within Trypanosoma cruzi I in Colombian isolates from several reservoirs, vectors and humans. Acta Tropica 110, 15–21.CrossRefGoogle ScholarPubMed
Fellet, M. R., Lorenzo, M. G., Elliot, S. L., Carrasco, D. and Guarneri, A. A. (2014). Effects of infection by Trypanosoma cruzi and Trypanosoma rangeli on the reproductive performance of the vector Rhodnius prolixus . PLoS ONE 9, e105255.Google Scholar
Ferreira, L. L., Lorenzo, M. G., Elliot, S. L. and Guarneri, A. a. (2010). A standardizable protocol for infection of Rhodnius prolixus with Trypanosoma rangeli, which mimics natural infections and reveals physiological effects of infection upon the insect. Journal of Invertebrate Pathology 105, 91–97.Google Scholar
Fisher, R. (1930). The Genetical Theory of Natural Selection. Clarendon Press, Oxford.Google Scholar
Friend, W. G., Choy, C. and Cartwright, E. (1965). The effect of nutrient intake on the development and the egg production of Rhodnius prolixus Stahl (Hemiptera: Reduviidae). Canadian Journal of Zoology 43, 891–904.CrossRefGoogle ScholarPubMed
Garcia, E. S., Mello, C. B., Azambuja, P. and Ribeiro, J. M. C. (1994). Rhodnius prolixus: salivary antihemostatic components decrease with Trypanosoma rangeli infection. Experimental Parasitology 78, 287–293.Google Scholar
Garcia, E. S., Machado, E. M. M. and Azambuja, P. (2004). Inhibition of hemocyte microaggregation reactions in Rhodnius prolixus larvae orally infected with Trypanosoma rangeli . Experimental Parasitology 107, 31–38.CrossRefGoogle ScholarPubMed
Gillet, J. (1935). The genital sterna of the imature stages of Rhodnius prolixus (Hemiptera). Transactions of the Royal Entomological Society of London 83, 1–5.CrossRefGoogle Scholar
Giraudoux, P. (2013). pgirmess: Data analysis in ecology. R package version 1.5.8. http://CRAN.R-project.org/package=pgirmess Google Scholar
Gómez, I. (1967). Nuevas observaciones acerca de la acción patógena del Trypanosoma rangeli Tejera, 1920 sobre Rhodnius prolixus Stal, 1859. Revista do Instituto de Medicina Tropical de São Paulo 9, 5–10.Google Scholar
Gorla, D. E. and Noireau, F. (2010). Geographic distribution of Triatomine vectors in America. In American Trypanosomiasis Chagas Disease (ed. Telleria, J. and Tibayrenc, M.), pp. 209–231. Elsevier, Amsterdam.CrossRefGoogle Scholar
Gottdenker, N. L., Chaves, L. F., Calzada, J. E., Peterson, J. K., Santamaría, A. M., Pineda, V. and Saldaña, A. (2016). Trypanosoma cruzi and Trypanosoma rangeli Co-infection patterns in insect vectors vary across habitat types in a fragmented forest landscape. Parasitology Open Submitted .Google Scholar
Grewal, M. S. (1957). Pathogenicity of Trypanosoma rangeli in the Invertebrate Host. Experimental Parasitology 6, 123–130.CrossRefGoogle ScholarPubMed
Grijalva, M. J., Suarez-Davalos, V., Villacis, A. G., Ocana-Mayorga, S. and Dangles, O. (2012). Ecological factors related to the widespread distribution of sylvatic Rhodnius ecuadoriensis populations in southern Ecuador. Parasites & Vectors 5, 17.Google Scholar
Grisard, E. C., Campbell, D. a. and Romanha, a. J. (1999). Mini-exon gene sequence polymorphism among Trypanosoma rangeli strains isolated from distinct geographical regions. Parasitology 118 (Pt 4), 375–382.Google Scholar
Groot, H. (1951). Nuevo foco de trypanosomiasis humana en Colombia. Anales de la Sociedad de Biologia de Bogotá 4, 220–221.Google Scholar
Guhl, F. and Marinkelle, C. J. (1982). Antibodies against Trypansoma cruzi in mice infected with T. rangeli . Annals of Tropical Medicine and Parasitology 76, 361.Google Scholar
Guhl, F. and Vallejo, G. A. (2003). Trypanosoma (Herpetosoma) rangeli Tejera, 1920: an updated review. Memórias do Instituto Oswaldo Cruz 98, 435–442.Google Scholar
Guhl, F., Hudson, L., Marinkelle, C. J., Jaramillo, C. a. and Bridge, D. (1987). Clinical Trypanosoma rangeli infection as a complication of Chagas’ disease. Parasitology 94 (Pt 3), 475–484.Google Scholar
Gutierrez, F. R. S., Trujillo Güiza, M. L. and Escobar Martínez, M. D. C. (2013). Prevalence of Trypanosoma cruzi infection among people aged 15 to 89 years inhabiting the department of Casanare (Colombia). PLoS Neglected Tropical Diseases 7, e2113.Google Scholar
Harrell, F. E. Jr (2014). rms: Regression Modeling Strategies. R package version 4.2-1. http://CRAN.R-project.org/package=rms Google Scholar
Harrington, D. P. and Fleming, T. R. (1982). A class of rank test procedures for censored survival data. Biometrika 69, 553–566.CrossRefGoogle Scholar
Henriques, C., Castro, D. P., Gomes, L. H. F., Garcia, E. S. and De Souza, W. (2012). Bioluminescent imaging of Trypanosoma cruzi infection in Rhodnius prolixus . Parasites & Vectors 5, 1–15.Google Scholar
Herbig-Sandreuter, A. (1957). Further studies on Trypanosoma rangeli Tejera 1920. Acta Tropica 14, 193–207.Google ScholarPubMed
Holm, S. (1979). A simple sequentially rejective multiple test procedure. Scandinavian Journal of Statistics 6, 65–70.Google Scholar
Hoyos, R., Pacheco, L., Agudelo, L. A., Zafra, G., Blanco, P. and Triana, O. (2007). Seroprevalencia de la enfermedad de Chagas y factores de riesgo asociados en una población de Morroa, Sucre. Biomédica 27, 130–136.Google Scholar
Kollien, A. and Schaub, G. (1998 a). Trypanosoma cruzi in the rectum of the bug Triatoma infestans: effects of blood ingestion by the starved vector. American Journal of Tropical Medicine and Hygiene 59, 166–170.Google Scholar
Kollien, A. and Schaub, G. (1998 b). The Development of Trypanosoma cruzi (Trypanosomatidae) in the Reduviid bug Triatoma infestans (Insecta): influence of starvation. Journal of Eukaryotic Microbiology 45, 59–63.CrossRefGoogle ScholarPubMed
Kollien, A. H., Schmidt, J. and Schaub, G. A. (1998). Modes of association of Trypanosoma cruzi with the intestinal tract of the vector Triatoma infestans . Acta Tropica 70, 127–141.CrossRefGoogle ScholarPubMed
Lima, M. M., Borges-Pereira, J., Albuquerque Dos Santos, J. A., Teixeira Pinto, Z. and Vianna Braga, M. (1992). Development and reproduction of Panstrongylus megistus (Hemiptera: Reduviidae) infected with Trypanosoma cruzi, under laboratory conditions. Annals of the Entomological Society of America 85, 458–461.Google Scholar
Luz, C., Rocha, L. F. N. and Nery, G. V. (2004). Detection of entomopathogenic fungi in peridomestic triatomine-infested areas in central Brazil and fungal activity against Triatoma infestans (Klug) (Hemiptera: Reduviidae). Neotropical Entomology 33, 783–791.Google Scholar
Mac Cord, J. R., Jurberg, P. and Lima, M. M. (1983). Marcacao individual de tratomineos para estudos comportamentais e ecologicos. Memórias do Instituto Oswaldo Cruz 78, 473–476.Google Scholar
Marini, V., Moretti, E., Bermejo, D. and Basso, B. (2011). Vaccination with Trypanosoma rangeli modulates the profiles of immunoglobulins and IL-6 at local and systemic levels in the early phase of Trypanosoma cruzi experimental infection. Memórias do Instituto Oswaldo Cruz 106, 32–37.Google Scholar
Marti, G. A., Balsalobre, A., Susevich, M. L., Rabinovich, J. E. and Echeverría, M. G. (2015). Detection of triatomine infection by Triatoma virus and horizontal transmission: protecting insectaries and prospects for biological control. Journal of Invertebrate Pathology 124, 57–60.Google Scholar
McGraw, J. B. and Caswell, H. (1996). Estimation of individual fitness from life-history data. The American Naturalist 147, 47–64.Google Scholar
Mejía-Jaramillo, A. M., Peña, V. H. and Triana-Chávez, O. (2009). Trypanosoma cruzi: biological characterization of lineages I and II supports the predominance of lineage I in Colombia. Experimental Parasitology 121, 83–91.Google Scholar
Mello, C. B., Azambuja, P., Garcia, E. S. and Ratcliffe, N. a. (1996). Differential in vitro and in vivo behavior of three strains of Trypanosoma cruzi in the gut and hemolymph of Rhodnius prolixus . Experimental Parasitology 82, 112–121.Google Scholar
Mundall, E. (1978). Oviposition in Triatoma protracta: role of mating and relationship to egg growth. Journal of Insect Physiology 24, 321–323.Google Scholar
Neves, D. and Peres, R. (1975). Aspectos da biologia do Rhodnius prolixus quando alimentado em animais sadios ou infectados com o Trypanosoma cruzi . Revista Brasileira de Biologia 35, 317–320.Google Scholar
Nogueira, N. F. S., Gonzalez, M. S., Gomes, J. E., de Souza, W., Garcia, E., Azambuja, P., Nohara, L. L., Almeida, I. C., Zingales, B. and Colli, W. (2007). Trypanosoma cruzi: involvement of glycoinositolphospholipids in the attachment to the luminal midgut surface of Rhodnius prolixus . Experimental Parasitology 116, 120–128.Google Scholar
Paim, R. M., Pereira, M. H., Di Ponzio, R., Rodrigues, J. O., Guarneri, A. a, Gontijo, N. F. and Araújo, R. N. (2012). Validation of reference genes for expression analysis in the salivary gland and the intestine of Rhodnius prolixus (Hemiptera, Reduviidae) under different experimental conditions by quantitative real-time PCR. BMC Research Notes 5, 128.Google Scholar
Pavia, P. X., Vallejo, G. A., Montilla, M., Nicholls, R. S. and Puerta, C. J. (2007). Detection of Trypanosoma cruzi and Trypanosoma rangeli infection in triatomine vectors by amplification of the histone H2A/SIRE and the sno-RNA-C11 genes. Revista do Instituto de Medicina Tropical de São Paulo 49, 23–30.Google Scholar
Pedersen, A. B. and Fenton, A. (2007). Emphasizing the ecology in parasite community ecology. Trends in Ecology & Evolution (Personal edition) 22, 133–139.Google Scholar
Perlowagora-Szumlewicz, A. and Muller, C. A. (1982). Studies in search of a suitable experimental insect model for xenodiagnosis of hosts with Chagas disease. 1-Comparative xenodiagnosis with nine triatomine species of animals with acute infections by Trypanosoma cruzi . Memorias do Instituto Oswaldo Cruz 77, 37–53.Google Scholar
Peterson, J. K., Graham, A. L., Dobson, A. P. and Chavez, O. T. (2015). Rhodnius prolixus life history outcomes differ when infected with different Trypanosoma cruzi I strains. American Journal of Tropical Medicine and Hygiene 93, 564–572.CrossRefGoogle ScholarPubMed
Peto, R. and Peto, J. (1972). Asymptotically efficient rank invariant test procedures. Journal of the Royal Statistical Society A 135, 185–207.CrossRefGoogle Scholar
Pineda, V., Montalvo, E., Alvarez, D., Santamaría, A. M., Calzada, J. E. and Saldaña, A. (2008). Feeding sources and trypanosome infection index of Rhodnius pallescens in a Chagas disease endemic area of Amador County, Panama. Revista do Instituto de Medicina Tropical de São Paulo 50, 113–116.CrossRefGoogle Scholar
R Core Team (2014). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.Google Scholar
Ratcliffe, N. A., Nigam, Y. N., Mello, C. B., Garcia, E. S. and Azambuja, P. (1996). Trypanosoma cruzi and Erythrocyte Agglutinins: a comparative study of occurrence and properties in the Gut and Hemolymph of Rhodnius prolixus . Experimental Parasitology 83, 83–93.CrossRefGoogle ScholarPubMed
Rojas, W., Caro, M. A., Lopera, J. G., Triana, O., Dib, J. C. and Bedoya, G. (2007). Análisis de polimorfismos en los genes tripanotión reductasa y cruzipaína en cepas colombianas de Trypanosoma cruzi . Biomédica 27, 50–63.Google Scholar
Ruegg, R. P. and Davey, K. G. (1979). The effect of C18 juvenile hormone and Altosid on the efficiency of egg production in Rhodnius prolixus . International Journal of Invertebrate Reproduction 1, 3–8.Google Scholar
Saldaña, A. and Sousa, O. (1996). Trypanosoma rangeli: Epimastigote Immunogenicity and Cross-reaction with Trypanosoma cruzi . Journal of Parasitology 82, 363–366.Google Scholar
Schaub, G. A. (1988 a). Development of isolated and group-reared first instars of Triatoma infestans infected with Trypanosoma cruzi . Parasitology Research 74, 593–594.Google Scholar
Schaub, G. A. (1988 b). Developmental time and mortality of larvae of Triatoma infestans infected with Trypanosoma cruzi . Transactions of the Royal Society of Tropical Medicine and Hygiene 82, 94–96.CrossRefGoogle ScholarPubMed
Schaub, G. A. (1989 a). Does Trypanosoma cruzi stress its vectors? Parasitology Today 5, 185–188.CrossRefGoogle ScholarPubMed
Schaub, G. A. (1989 b). Trypanosoma cruzi: quantitative studies of development of two strains in small intestine and rectum of the vector Triatoma infestans . Experimental Parasitology 68, 260–273.Google Scholar
Schaub, G. A. (1990). Membrane feeding for infection of the reduviid bug Triatoma infestans with Blastocrithidia triatomae (Trypanosomatidae) and pathogenic effects of the flagellate. Parasitology 76, 306–310.Google Scholar
Schaub, G. A. (1992). The effects of trypanosomatids on insects. Advances in Parasitology 31, 255–319.Google Scholar
Schaub, G. A. (1994). Pathogenicity of trypanosomatids on insects. Parasitology Today 10, 463–468.Google Scholar
Schaub, G. A. and Losch, P. (1989 a). Parasite/host-interrelationships of the trypanosomatids Trypanosoma cruzi and Blastocrithidia triatomae and the reduviid bug Triatoma infestans: influence of starvation of the bug. Annals of Tropical Medicine and Parasitology 83, 215–223.Google Scholar
Schaub, G. A. and Losch, P. (1989 b). Parasite/host-interrelationships of the trypanosomatids Trypanosoma cruzi and Blastocrithidia triatomae and the reduviid bug Triatoma infestans: influence of starvation on the bug. Annals of Tropical Medicine and Parasitology 83, 215–223.Google Scholar
Schaub, G. a. and Lösch, P. (1988). Trypanosoma cruzi: origin of metacyclic trypomastigotes in the urine of the vector Triatoma infestans . Experimental Parasitology 65, 174–186.Google Scholar
Schaub, G. A., Grünfelder, C. G., Zimmermann, D. and Peters, W. (1989). Binding of lectin-gold conjugates by two Trypanosoma cruzi strains in ampullae and rectum of Triatoma infestans . Acta Tropica 46, 291–301.Google Scholar
Therneau, T. (2015). A Package for Survival Analysis in S. version 2.38. http://CRAN.R-project.org/package=survival Google Scholar
Therneau, T. and Grambsch, P. (2000). Modeling Survival Data: Extending the Cox Model. Springer, New York.CrossRefGoogle Scholar
Tobie, E. J. (1965). Biological factors influencing transmission of Trypanosoma rangeli by Rhodnius prolixus . Journal of Parasitology 51, 837–841.Google Scholar
Toloza, A. C., Germano, M., Cueto, G. M., Vassena, C., Zerba, E. and Picollo, M. I. (2008). Differential patterns of insecticide resistance in eggs and first instars of Triatoma infestans (Hemiptera: Reduviidae) from Argentina and Bolivia. Journal of Medical Entomology 45, 421–426.Google Scholar
Twombly, S., Clancy, N. and Burns, C. W. (1998). Life history consequences of food quality in the freshwater copepod Boeckella triarticulata . Ecology 79, 1711–1724.Google Scholar
Untergasser, A., Nijveen, H., Rao, X., Bisseling, T., Geurts, R. and Leunissen, J. A. (2007). Primer3Plus, an enhanced web interface to Primer3. Nucleic Acids Research 35, W71–W74.Google Scholar
Urdaneta-Morales, S. and Rueda, I. G. (1977). A comparative study of the behavior of Venezuelan and Brazilian strains of Trypanosoma (Schizotrypanum) cruzi in the Venezuelan invertebrate host (Rhodnius prolixus). Revista do Instituto de Medicina Tropical de São Paulo 19, 241–250.Google Scholar
Urdaneta-Morales, S. and Tejero, F. (1986). Trypanosoma (herpetosoma) rangeli Tejera, 1920. Intracellular amastigote stages of reproduction in white mice. Revista do Instituto de Medicina Tropical de São Paulo 28, 166–169.Google Scholar
Urrea, D., Carranza, J. C., Cuba Cuba, C., Gurgel-Gonçalves, R., Guhl, F., Schofield, C. J., Triana, O. and Vallejo, G. a. (2005). Molecular characterisation of Trypanosoma rangeli strains isolated from Rhodnius ecuadoriensis in Peru, R. colombiensis in Colombia and R. pallescens in Panama, supports a co-evolutionary association between parasites and vectors. Infection, Genetics and Evolution 5, 123–129.Google Scholar
Urrea, D. A., Guhl, F., Herrera, C. P., Falla, A., Carranza, J. C., Cuba-Cuba, C., Triana-Chávez, O., Grisard, E. C. and Vallejo, G. A. (2011). Sequence analysis of the spliced-leader intergenic region (SL-IR) and random amplified polymorphic DNA (RAPD) of Trypanosoma rangeli strains isolated from Rhodnius ecuadoriensis, R. colombiensis, R. pallescens and R. prolixu . Acta Tropica 120, 59–66.CrossRefGoogle Scholar
Vallejo, G. A., Marinkelle, C., Guhl, F. and de Sanchez, N. (1988). Comportamiento de la infección y diferenciación morfolóica entre Trypanosoma cruzi y Trypanosoma rangeli en el intestino del vector Rhodnius prolixus . Revista Brasileira de Biologia 48, 577–587.Google Scholar
Vallejo, G. A., Guhl, F., Carranza, J. C., Lozano, L. E., Sánchez, J. L., Jamarillo, J. C., Gualtero, D., Castañeda, N., Silva, J. C. and Steindel, M. (2002). kDNA markers define two major Trypanosoma rangeli lineages in Latin-America. Acta Tropica 81, 77–82.Google Scholar
Vallejo, G. A., Guhl, F. and Schaub, G. A. (2009). Triatominae-Trypanosoma cruzi/T. rangeli: vector-parasite interactions. Acta Tropica 110, 137–147.CrossRefGoogle ScholarPubMed
Vargas, N., Souto, R. P., Carranza, J. C., Vallejo, G. a. and Zingales, B. (2000). Amplification of a specific repetitive DNA sequence for Trypanosoma rangeli identification and its potential application in epidemiological investigations. Experimental Parasitology 96, 147–159.Google Scholar
Venables, W. N. and Ripley, B. D. (2002). Modern Applied Statistics with S, 4th Edn. Springer, New York.CrossRefGoogle Scholar
Watkins, R. (1971). Trypanosoma rangeli: effect on excretion in Rhodnius prolixus . Journal of Invertebrate Pathology 17, 67–71.Google Scholar
Whitten, M. M., Mello, C. B., Gomes, S. a., Nigam, Y., Azambuja, P., Garcia, E. S. and Ratcliffe, N. a. (2001). Role of superoxide and reactive nitrogen intermediates in Rhodnius prolixus (Reduviidae)/Trypanosoma rangeli interactions. Experimental Parasitology 98, 44–57.Google Scholar
Wood, S. F. (1954). Environmental temperature as a factor in development of Trypanosoma cruzi in Triatoma protracta . Experimental Parasitology 3, 227–233.Google Scholar
Zuñiga, C., Penin, P., Gamallo, C. and de Diego, J. (1997 a). Characterization of a Trypanosoma rangeli Strain of Colombian Origin. Memórias do Instituto Oswaldo Cruz 92, 523–530.Google Scholar
Zuñiga, C., Paláu, M. T., Penin, P., Gamallo, C. and de Diego, J. A. (1997 b). Trypanosoma rangeli: increase in virulence with inocula of different origins in the experimental infection in mice. Parasitology Research 83, 797–800.Google Scholar

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