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Temperature and parasite life-history are important modulators of the outcome of Trypanosoma rangeli–Rhodnius prolixus interactions

Published online by Cambridge University Press:  17 June 2016

JULIANA DE O. RODRIGUES ,
MARCELO G. LORENZO ,
OLINDO A. MARTINS-FILHO ,
SIMON L. ELLIOT  and
ALESSANDRA A. GUARNERI Open the ORCID record for ALESSANDRA A. GUARNERI [Opens in a new window]
JULIANA DE O. RODRIGUES
Affiliation:
Centro de Pesquisas René Rachou, Avenida Augusto de Lima, 1715, CEP 30190-002, Belo Horizonte, MG, Brazil
MARCELO G. LORENZO
Affiliation:
Centro de Pesquisas René Rachou, Avenida Augusto de Lima, 1715, CEP 30190-002, Belo Horizonte, MG, Brazil
OLINDO A. MARTINS-FILHO
Affiliation:
Centro de Pesquisas René Rachou, Avenida Augusto de Lima, 1715, CEP 30190-002, Belo Horizonte, MG, Brazil
SIMON L. ELLIOT
Affiliation:
Department of Entomology, Universidade Federal de Viçosa, Campus Universitário, CEP 36570-900, Viçosa, MG, Brazil
ALESSANDRA A. GUARNERI*
Affiliation:
Centro de Pesquisas René Rachou, Avenida Augusto de Lima, 1715, CEP 30190-002, Belo Horizonte, MG, Brazil
*
*Corresponding author: Vector Behaviour and Pathogen Interaction Group, Centro de Pesquisas René Rachou, Avenida Augusto de Lima, 1715, CEP 30190-002, Belo Horizonte, MG, Brazil. E-mail: guarneri@cpqrr.fiocruz.br
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Summary

Trypanosoma rangeli is a protozoan parasite, which does not cause disease in humans, although it can produce different levels of pathogenicity to triatomines, their invertebrate hosts. We tested whether infection imposed a temperature-dependent cost on triatomine fitness using T. rangeli with different life histories. Parasites cultured only in liver infusion tryptose medium (cultured) and parasites exposed to cyclical passages through mice and triatomines (passaged) were used. We held infected insects at four temperatures between 21 and 30 °C and measured T. rangeli growth in vitro at the same temperatures in parallel. Overall, T. rangeli infection induced negative effects on insect fitness. In the case of cultured infection, parasite effects were temperature-dependent. Intermoult period, mortality rates and ecdysis success were affected in those insects exposed to lower temperatures (21 and 24 °C). For passaged-infected insects, the effects were independent of temperature, intermoult period being prolonged in all infected groups. Trypanosoma rangeli seem to be less tolerant to higher temperatures since cultured-infected insects showed a reduction in the infection rates and passaged-infected insects decreased the salivary gland infection rates in those insects submitted to 30 °C. In vitro growth of T. rangeli was consistent with these results.

Keywords

Trypanosoma rangeliRhodnius prolixusinteractiontemperatureparasite growthvirulence
Type
Research Article
Information
Parasitology , Volume 143 , Issue 11 , September 2016 , pp. 1459 - 1468
Copyright
Copyright © Cambridge University Press 2016 

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References

REFERENCES

Abad-Franch, F., Palomeque, F., Aguilar, H. T. and Miles, M. (2005). Field ecology of sylvatic Rhodnius populations (Heteroptera, Triatominae): risk factors for palm tree infestation in western Ecuador. Tropical Medicine & International Health 10, 1258–1266.Google Scholar
Anez, 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
Bale, J. and Hayward, S. (2010). Insect overwintering in a changing climate. Journal of Experimental Biology 213, 980–994.Google Scholar
Blanford, S. and Thomas, M. (1999). Role of thermal biology in disease dynamics. Aspects of Applied Biology 53, 73–82.Google Scholar
Blanford, S., Thomas, M. B. and Langewald, J. (2000). Thermal ecology of Zonocerus variegatus and its effects on biocontrol using pathogens. Agricultural and Forest Entomology 2, 3–10.Google Scholar
Brecher, G. and Wigglesworth, V. (1944). The transmission of Actinomyces rhodnii Erikson in Rhodnius prolixus stål (Hemiptera) and its influence on the growth of the host. Parasitology 35, 220–224.CrossRefGoogle Scholar
Chapman, R. F. and Page, W. W. (1979). Factors affecting the mortality of the grasshopper, Zonocerus variegatus, in southern Nigeria. Journal of Animal Ecology 48, 271–288.CrossRefGoogle Scholar
Clark, N. (1935). The effect of temperature and humidity upon the eggs of the bug, Rhodnius prolixus (Heteroptera, Reduviidae). Journal of Animal Ecology 4, 82–87.CrossRefGoogle Scholar
D'Alessandro, A. (1976). Biology of Trypanosoma (Herpetosoma) rangeli Tejera, 1920. In Biology of Kinetoplastida (ed. Lumsden, W. H. R. and Evans, D. A.), pp. 328–403. Academic Press, London.Google Scholar
Deutsch, C. A., Tewksbury, J. J., Huey, R. B., Sheldon, K. S., Ghalambor, C. K., Haak, D. C. and Martin, P. R. (2008). Impacts of climate warming on terrestrial ectotherms across latitude. Proceedings of the National Academy of Sciences 105, 6668–6672.Google Scholar
Dias, F. B. S., Bezerra, C. M., Machado, E. M. M., Casanova, C., Diotaiuti, L. (2008). Ecological aspects of Rhodnius nasutus Stål, 1859 (Hemiptera: Reduviidae: Triatominae) in palms of the Chapada do Araripe in Ceará, Brazil. Memorias do Instituto Oswaldo Cruz 103, 824–830.Google Scholar
Dias, F. B. S., de Paula, A. S., Belisario, C. J., Lorenzo, M. G., Bezerra, C. M., Harry, M. and Diotaiuti, L. (2011). Influence of the palm tree species on the variability of Rhodnius nasutus Stål, 1859 (Hemiptera, Reduviidae, Triatominae). Infection, Genetics and Evolution 11, 869–877.CrossRefGoogle ScholarPubMed
Di Luciano, V. S. (1983). Orientation of Triatoma infestans (Hemiptera: Reduviidae) to environmental temperatures. Journal of Medical Entomology 20, 446–454.CrossRefGoogle Scholar
Ehrenfeld, M. J., Canals, M. and Cattan, P. E. (1998). Population parameters of Triatoma spinolai (Heteroptera: Reduviidae) under different environmental conditions and densities. Journal of Medical Entomology 35, 740–744.Google Scholar
Elliot, S. L., Blanford, S. and Thomas, M. B. (2002). Host–pathogen interactions in a varying environment: temperature, behavioural fever and fitness. Proceedings of the Royal Society of London Series B – Biological Sciences 269, 1599–1607.CrossRefGoogle Scholar
Elliot, S. L., Rodrigues, J. 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
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.CrossRefGoogle ScholarPubMed
Figueiredo, M. B., Genta, F. A., Garcia, E. S. and Azambuja, P. (2008). Lipid mediators and vector infection: Trypanosoma rangeli inhibits Rhodnius prolixus hemocyte phagocytosis by modulation of phospholipase A2 and PAF-acetylhydrolase activities. Journal of Insect Physiology 54, 1528–1537.CrossRefGoogle ScholarPubMed
Garcia, E. S., Machado, E. M. and Azambuja, P. (2004). Effects of eicosanoid biosynthesis inhibitors on the prophenoloxidase-activating system and microaggregation reactions in the hemolymph of Rhodnius prolixus infected with Trypanosoma rangeli . Journal of Insect Physiology 50, 157–165.Google Scholar
Garcia, E. S., Castro, D. P., Figueiredo, M. B., Genta, F. A. and Azambuja, P. (2009). Trypanosoma rangeli: a new perspective for studying the modulation of immune reactions of Rhodnius prolixus . Parasites & Vectors 2, 1–10.Google Scholar
Gazos-Lopes, F., Mesquita, R. D., Silva-Cardoso, L., Senna, R., Silveira, A. B., Jablonka, W., Cudischevitch, C. O., Carneiro, A. B., Machado, E. A., Lima, L. G., Monteiro, R. Q., Nussenzveig, R. H., Follu, E., Romeiro, A., Vanbeselaere, J., Mendonça-Previato, L., Previato, J. O., Valenzuela, J. G., Ribeiro, J. M. C., Atella, G. C. and Silva-Neto, M. A. C. (2012). Glycoinositolphospholipids from trypanosomatids subvert nitric oxide production in Rhodnius prolixus salivary glands. PloS ONE 7, e47285.Google Scholar
Gregório, E. A. and Ratcliffe, N. A. (1991). The prophenoloxidase system and in vitro interaction of Trypanosoma rangeli with Rhodnius prolixus and Triatoma infestans haemolymph. Parasite Immunology 13, 551–564.Google Scholar
Grewal, M. S. (1957). Pathogenicity of Trypanosoma rangeli Tejera, 1920 in the invertebrate host. Experimental Parasitology 6, 123–130.Google Scholar
Guarneri, A. A., Diotaiuti, L., Gontijo, N. F., Gontijo, A. F. and Pereira, M. H. (2000). Comparison of feeding behaviour of Triatoma infestans, Triatoma brasiliensis and Triatoma pseudomaculata in different hosts by electronic monitoring of the cibarial pump. Journal of Insect Physiology 46, 1121–1127.Google Scholar
Guarneri, A. A., Lazzari, C., Xavier, A. A. P., Diotaiuti, L. and Lorenzo, M. G. (2003). The effect of temperature on the behaviour and development of Triatoma brasiliensis . Physiological Entomology 28, 185–191.Google Scholar
Hecker, H., Schwarzenbach, M. and Rudin, W. (1990). Development and interactions of Trypanosoma rangeli in and with the reduviid bug Rhodnius prolixus . Parasitology Research 76, 311–318.Google Scholar
Heger, T. J., Guerin, P. M. and Eugster, W. (2006). Microclimatic factors influencing refugium suitability for Rhodnius prolixus . Physiological Entomology 31, 248–256.Google Scholar
Joerg, M. (1962). Influencia de temperaturas fijas en periodos anuales sobre metamorfosis y fertilidad de Triatoma infestans . Boletín Chileno de Parasitología 17, 17–19.Google Scholar
Lake, P. and Friend, W. (1967). A monoxenic relationship, Nocardia rhodnii Erikson in the gut of Rhodnius prolixus Stal (Hemiptera: Reduviidae). Proceedings of the Entomological Society of Ontario 98, 53–57.Google Scholar
Lazzari, C. (1991). Circadian rhythm of egg hatching in Triatoma infestans (Hemiptera: Reduviidae). Journal of Medical Entomology 28, 740–741.Google Scholar
Lazzari, C. R. and Nunez, J. A. (1989). The response to radiant-heat and the estimation of the temperature of distant sources in Triatoma infestans . Journal of Insect Physiology 35, 525–529.Google Scholar
Lehane, M., McEwen, P., Whitaker, C. and Schofield, C. (1992). The role of temperature and nutritional status in flight initiation by Triatoma infestans . Acta Tropica 52, 27–38.Google Scholar
Lorenzo, M. G. and Lazzari, C. R. (1998). Activity pattern in relation to refuge exploitation and feeding in Triatoma infestans (Hemiptera: Reduviidae). Acta Tropica 70, 163–170.Google Scholar
Lorenzo, M. G., Guarneri, A. A., Pires, H. H. R., Diotaiuti, L. and Lazzari, C. R. (2000). Aspectos microclimáticos del hábitat de Triatoma brasiliensis . Cadernos de Saude Publica 16, S69–S74.Google Scholar
Marliére, N. P., Latorre-Estivalis, J. M., Lorenzo, M. G., Carrasco, D., Alves-Silva, J., Rodrigues, J. O., Ferreira, L. L., Lara, L. M., Lowenberger, C. and Guarneri, A. A. (2015). Trypanosomes modify the behavior of their insect hosts: effects on locomotion and on the expression of a related gene. PLoS Neglected Tropical Diseases 9, e0003973.Google Scholar
Schilman, P. and Lazzari, C. (2004). Temperature preference in Rhodnius prolixus, effects and possible consequences. Acta Tropica 90, 115–122.CrossRefGoogle ScholarPubMed
Schottelius, J. (1987). Neuraminidase fluorescence test for the differentiation of Trypanosoma cruzi and Trypanosoma rangeli . Tropical Medicine and Parasitology 38, 323–327.Google Scholar
Statistical Package, R. (2009). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.Google Scholar
Sternberg, E. D. and Thomas, M. B. (2014). Local adaptation to temperature and the implications for vector-borne diseases. Trends in Parasitology 30, 115–122.Google Scholar
Takle, G. B. (1988). Studies on the cellular immune responses of insects toward the insect pathogen Trypanosoma rangeli . Journal of Invertebrate Pathology 51, 64–72.Google Scholar
Teixeira, A., Monteiro, P. S., Rebelo, J. M., Argañaraz, E. R., Vieira, D., Lauria-Pires, L., Nascimento, R., Vexenat, C. A., Silva, A. R. and Ault, S. K. (2001). Emerging Chagas disease: trophic network and cycle of transmission of Trypanosoma cruzi from palm trees in the Amazon. Emerging Infectious Diseases 7, 100–112.Google Scholar
Thekisoe, O. M., Rodriguez, C. V., Rivas, F., Coronel-Servian, A. M., Fukumoto, S., Sugimoto, C., Kawazu, S. and Inoue, N. (2010). Detection of Trypanosoma cruzi and T. rangeli infections from Rhodnius pallescens bugs by loop-mediated isothermal amplification (LAMP). American Journal of Tropical Medicine and Hygiene 82, 855–860.Google Scholar
Thomas, M. B. and Blanford, S. (2003). Thermal biology in insect-parasite interactions. Trends in Ecology & Evolution 18, 344–350.Google Scholar
Tobie, E. J. (1964). Increased infectivity of a cyclically maintained strain of Trypanosoma rangeli to Rhodnius prolixus and mode of transmission by invertebrate host. Journal of Parasitology 50, 593–598.Google Scholar
Tobie, E. J. (1965). Biological factors influencing transmission of Trypanosoma rangeli by Rhodnius prolixus . Journal of Parasitology 51, 837–841.CrossRefGoogle ScholarPubMed
Tovar, D., Urdaneta-Morales, S. and Tejero, F. (1988). Trypanosoma (Herpetosoma) rangeli Tejera, 1920: study of the effects of the parasite on the vector. Acta Cientifica Venezolana 40, 208–214.Google Scholar
Vallejo, G. A., Marinkelle, C. J., Guhl, F. and de Sanchez, N. (1986). Laboratory maintenance of Trypanosoma (Herpetosoma) rangeli Tejera, 1920. Revista de Biología Tropical 34, 75–81.Google Scholar
Watkins, R. (1971). Trypanosoma rangeli: effect on excretion in Rhodnius prolixus . Journal of Invertebrate Pathology 17, 67–71.Google Scholar
Whitten, M. M. A., Mello, C. B., Gomes, S. A. O., 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
Whitten, M., Sun, F., Tew, I., Schaub, G., Soukou, C., Nappi, A. and Ratcliffe, N. (2007). Differential modulation of Rhodnius prolixus nitric oxide activities following challenge with Trypanosoma rangeli, T. cruzi and bacterial cell wall components. Insect Biochemistry and Molecular Biology 37, 440–452.Google Scholar
Wigglesworth, V. and Gillett, J. (1934). The function of the antennae in Rhodnius prolixus (Hemiptera) and the mechanism of orientation to the host. Journal of Experimental Biology 11, 120–139.Google Scholar
World Health Organization (2015). Chagas disease (American trypanosomiasis). Geneva: Fact sheet 340. http://www.who.int/mediacentre/factsheets/fs340/en/.Google Scholar