Keywords
Triatominae
feeding
hemolymph
hemocytes
immune system
Chagas disease
feeding
hemolymph
hemocytes
immune system
Chagas disease
How to Cite
Avendaño, F., Aldana, E., & Mendoza, R. (2017). Study of hemolymphatic components of Rhodnius prolixus and Triatoma maculata fed on different blood sources. Salud UIS, 49(4), 519–533. https://doi.org/10.18273/revsal.v49n4-2017001
Abstract
Introduction: Traditionally Rhodnius prolixus has been considered the main vector and Triatoma maculata as a secondary vector of Trypanosoma cruzi in the Venezuelan rural habitat. In this work, we show interesting information about the biochemical components and the immune system, humoral and cellular, of the hemolymph of R. prolixus and T. maculata feeding on hen and rat. Methodology: Hemolymph was extracted from adults insects, maintained at 27-29 °C, 50% relative humidity and 8/16 (Light/Dark) hours, and fed on hen and rat. Hemocytes were observed by optical microscopy and transmission electron microscopy. Results: Biochemical parameters such as glucose, lipids and proteins varied in both species according to the food source. T. maculata presented higher levels of lysozyme lytic activity. Four hemocytes populations were observed by optical and transmission electron microscopy, prohemocytes, plasmocytes, granulocytes and oenocytes, their characteristics and measures are in accordance with previous reports by other authors in the subfamily Triatominae. T. maculata presented more prohemocytes and oenocytes than R. prolixus. Conclusions: R. prolixus and T. maculata are distinctly affected in their biochemical hemolymphatic components (glucose, lipids and proteins) as well as humoral (lysozyme) and cellular (prohemocytes, oenocytes) inmune components, depending on whether they were fed on hens or rats. Our results show that the food source affects the immune system of triatomines, thus their vectorial capacity might affected as well.
References
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2. Tonn R, Otero M, Mora E, Espinola H, Carcavallo R. Aspectos biológicos, ecológicos y distribución geográfica de Triatoma maculata (Erichson 1948), (Hemiptera: Reduviidae), en Venezuela. Bol Dir Malariol Saneam Amb. 1978; 18: 16-24.
3. Feliciangeli MD, Dujardin JP, Bastrenta B, Mazzarri M, Villegas J, Flores M et al. Is Rhodnius robustus (Hemiptera: Reduviidae) responsible for Chagas disease transmission in Western Venezuela?. Trop Med Int Health. 2002; 17: 280-287.
4. Rojas M, Várquez P, Villarreal M, Velandia C, Vergara L, Morán Y et al. Estudio seroepidemiológico y entomológico sobre la enfermedad de Chagas en un área infestada
por Triatoma maculata (Erichson 1848) en el centro-occidente de Venezuela. Cad Saude Publ. 2008; 24: 2323-2333. DOI: http://dx.doi.org/10.1590/S0102-311X2008001000013.
5. Lent H, Wygodzinsky P. Revision of the Triatominae (Hemiptera, Reduviidae) and their significance as vectors of Chagas’ disease. Bull Am Museum Nat Hist. 1979; 163: 123-520.
6. Farfán AE, Gutierrez R, Angulo VM. ELISA para la identificación de los patrones alimentarios de Triatominae en Colombia. Rev. Salud Pública. 2007; 9: 602-608. DOI: http://dx.doi.org/10.1590/S0124-00642007000400013.
7. Carcavallo RU, Curto de Casas SI, Sherlock IA, Galíndez Girón I, Jurberg J, Galvao C, et al. Geographic distribution and alti-latitudinal dispersion. En: Carcavallo R.U., Galindez Girón I., Jurberg J., Lent, H. (Eds.), Atlas of Chagas Disease Vectors in the Americas, Vol. II. Fiocruz, Rio de Janeiro, Brazil. 1999; 747-792.
8. Soto A, Rodríguez C, Bonfante-Cabarca R, Aldana E. Morfometría geométrica de Triatoma maculata (Erichson, 1848) de ambientes doméstico y peridoméstico, estado Lara, Venezuela. Bol Dir Malariol San Amb. 2007; 47: 231-235.
9. García-Alzate R, Lozano-Arias D, Reyes-Lugo RM, Morocoima A, Herrera L, Mendoza-León A. Triatoma maculata, the vector of Trypanosoma cruzi, in Venezuela. Phenotypic and genotypic variability as potential indicator of vector displacement into the domestic habitat. Front Public Health. 2014; 2: 1-9. DOI: https://doi.org/10.3389/fpubh.2014.00170.
10. González-Brítez N, Morocoima A, Martínez C, Carrasco HJ. Infección por Trypanosoma cruzi y polimorfismo del citocromo B del ADN mitocondrial en Triatoma maculata de Anzoátegui y Portuguesa, Venezuela. Bol Mal Salud Amb. 2010; 50: 85-93.
11. Berrizbeitia M, Concepción J, Carzola V, Rodríguez J, Cáceres A, Quiñones W. Seroprevalencia de la infección por Trypanosoma cruzi en Canis familiaris del estado Sucre, Venezuela. Biomédica. 2013; 33: 214-225. DOI: http://dx.doi.org/10.7705/biomedica.v33i2.7.
12. García-Jordán N, Berrizbeitia M, Concepción JL, Aldana E, Cáceres A, Quiñones W. Estudio entomológico de vectores transmisores de la infección por Trypanosoma cruzi en la población rural del estado Sucre, Venezuela. Biomédica. 2015; 35: 247-257. DOI: https://doi.org/10.7705/biomedica.v35i2.2390.
13. Reyes-Lugo M, Reyes-Contreras M, Salvi I, Gelves W, Avilán A, Llavaneras D, et al. The association of Triatoma maculata (Ericsson 1848) with the gecko Thecadactylus rapicauda (Houttuyn 1782) (Reptilia: Squamata: Gekkonidae): a strategy of domiciliation of the Chagas disease peridomestic vector in Venezuela?. Asian Pac J Trop Biomed. 2011; 1: 279-284. DOI: 10.1016/S2221-1691(11)60043-9.
14. Morocoima A, Sotillo E, Salaverría C, Maniscalchi M, Pacheco F, Chique D. Domiciliación del vector peridomiciliario de la enfermedad de Chagas, Triatoma maculata (Erichson, 1848) en caserío rural del norte del estado Anzoátegui. Acta Cient Venezolana. 2005; 55: 215.
15. Luitgards-Moura J, Vargas A, Almeida C, Magno-Esperanca G, Agapito-Souza R, Folly-Ramos E, et al. A Triatoma maculata (Hemiptera, Reduviidae, Triatominae) population from Roraima, Amazon region, Brazil, has some bionomic characteristics of a potential Chagas disease vector. Rev Inst Med Trop São Paulo. 2005; 47: 131-137. DOI: http://dx.doi.org/10.1590/S0036-46652005000300003.
16. Ricardo-Silva A, Gonçalves Teresa CM, Luitgards-Moura JF, Lopes CM, Silva S, Bastos AQueiroz et al. Triatoma maculata colonises urban domicilies in Boa Vista, Roraima, Brazil. Mem Inst Oswaldo Cruz. 2016; 111: 703-706. DOI: 10.1590/0074-02760160026.
17. Corté LA, Suárez HA. Triatominos (Reduviidae: Triatominae) en un foco de enfermedad de Chagas en Talaigua Nuevo (Bolívar, Colombia). Rev Biomédica. 2005; 25: 568-574. DOI: https://doi.org/10.7705/issn.0120-4157.
18. Cantillo-Barraza O, Garces E, Gomez-Palacio A, Cortes LA, Pereira A, Marcet PL, et al. Ecoepidemiological study of an endemic Chagas disease region in northern Colombia reveals the importance of Triatoma maculata (Hemiptera: Reduviidae), dogs, and Didelphis marsupialis in Trypanosoma cruzi maintenance. Parasit Vectors. 2015; 8: 482. DOI: https://parasitesandvectors.biomedcentral.com/articles/10.1186/s13071-015-1100-2.
19. Azambuja P, Mello CB, Feder D, Garcia ES. Influence of cellular and humoral Triatominae defense system on the development of Trypanosomatides. En: Carcavallo RU, Galíndez Girón I, Juberg J, Lent H (eds). Atlas of Chagas Disease Vectors in the Americas, Vol. II. Fiocruz, Rio de Janeiro, Brazil. 1998; 709-733.
20. Wigglesworth VB. The physiology of the cuticle and of ecdysis in, with special reference to the function of the oenocytes and of the dermal glands. Quart J Micr Sci. 1933; 76: 269-318.
21. Wigglesworth VB. The role of haemocytes in the growth and moulting of an insect (Hemiptera). J Exp Biol. 1955; 32: 649-663.
22. Jones JC. The hemocytes of Rhodnius prolixus. Biol Bull Woods Hole. 1965; 129: 282-294.
23. Lai-Fook J. The fine structure of wound repair in an insect Rhodnius prolixus. J Morphol. 1968; 124: 7-78.
24. Lai- Fook J. Haemocytes in the repair of wouns in an insect Rhodnius prolixus. J Morphol. 1970; 130: 297-314.
25. Barracco MA, Oliveira R, Schlemper JR. The hemocytes of Panstrongylus megistus (Hemiptera: Reduviidae). Mem Inst Oswaldo Cruz. 1987; 82: 431-438. DOI: http://dx.doi.org/10.1590/S0074-02761987000300017.
26. Barracco MA, Loch C. Ultraestructural studies of the hemocytes of Panstrongylus megistus (Hemiptera: Reduviidae). Mem Inst Oswaldo Cruz. 1989; 84: 171-188. DOI: http://dx.doi.org/10.1590/S0074-02761989000200005.
27. Azambuja P, Garcia ES, Ratcliffe NA. Aspects of classification of hemipteran hemocytes from six triatomine species. Mem Inst Oswaldo Cruz. 1991; 86: 1-10. DOI: http://dx.doi.org/10.1590/S0074-02761991000100002.
28. Hypsa V, Grubhoffer L. Two hemocyte populations in Triatoma infestans: ultrastructural and lectin-binding characterization. Folia Parasitol. 1997; 44: 62-70.
29. Mello CB, Garcia ES, Ratcliffe NA, Azambuja P. Trypanosoma cruzi and Trypanosoma rangeli: interplay with hemolymph components of Rhodnius prolixus. J Invertebr Pathol. 1995; 65: 261-268.
30. Canavoso LE, Rubiolo ER. Hemolymphatic components in vectors of Trypanosoma cruzi: Study in several species of the subfamily Triatominae (Hemiptera: Reduviidae). Rev Inst Med Trop. 1993; 35: 123-128. DOI: http://dx.doi.org/10.1590/S0036-46651993000200003.
31. Canavoso LE, Rubiolo ER. Metabolic postfeeding changes in fat body and hemolymph of Dipetalogaster maximus (Hemiptera: Reduviidae). Mem Inst Oswaldo Cruz. 1998; 93: 225-230. DOI: http://dx.doi.org/10.1590/S0074-
02761998000200018.
32. Reyes-Lugo M, Girón ME, Kamiya H, Rodríguez Acosta A. A preliminary study of haemolymph from four Venezuelan populations of Panstrongylus geniculatus Latreille, 1811 (Hemiptera: Reduviidae) and its epidemiological significance. Rev Cubana Med. Trop. 2006; 58: 134-138.
33. Trinder P. Determination of glucose in blood using glucose oxidase with an alternative oxygen acceptor. Ann Clin Biochem 1969; 6: 24-27.
34. Layne E. Spectrophotometric and Turbidimetric Methods for Measuring Proteins. Methods in Enzymology. 1957; 10: 447-455.
35. 35. Frings CS, Fendley TW, Dunn RT, Queen CA. Improved determination of total serum lipids by the sulfo-phospho-vanillin reaction. Clin Chem. 1972; 18: 673-674.
36. Gupta AP. Hemocyte types: their structures, synonymies, interrelationships, and taxonomic significance. In Insect Hemocytes, ed. A.P. Gupta, Cambridge: Cambridge University Press. 1979: 85-127.
37. Palacios-Prü E, Palacios L, Mendoza RV. Synaptogenetic mechanisms during chick cerebellar cortex development. J Submicrosc Cytol. 1981; 13: 145-167.
38. Reynolds ES. The use of lead citrate at high pH as an electron-opaque satín in electron microscopy. J Cell Biol. 1963; 17: 208-212.
39. Watson ML. Staining of tissue sections for electron microscopy with heavy metals. J Biophys Biochem Cytol. 1958; 4: 475-478.
40. Pacheco MA, Concepción JL, Rangel JD, Ruiz MC, Michelangeli F, Domínguez-Bello MG. Stomach lysozymes of the three-toed sloth (Bradypusvariegatus), an arboreal folivore from the Neotropics. Comp Bioch Physiol. 2007; 147: 808–819. DOI: http://doi.org/10.1016/j.cbpa.2006.07.010.
41. Moreno J. Physiological mechanisms underlaying reproductive trade-off. Etologia. 1993; 3: 41-56.
42. Roff D. Life history evolution. Sinauer associates, Inc. USA. 2002; 132.
43. Ryan RO. Dynamics of insect lipophorin metabolism. J Lipids Res. 1990; 31: 1725-1739.
44. Flores-Villegas AL, Salazar-Schettino PM, Córdoba-Aguilar A, Gutiérrez-Cabrera AE, Rojas-Wastavino GE, Bucio-Torres MI, et al. Immune defence mechanisms of triatomines against bacteria, viruses, fungi and parasites. Bulletin of Entomological Research. 2015; 105, 523–532.
45. Otálora-Luna F, Pérez-Sánchez AJ, Sandoval C, Aldana E. Evolution of hematophagous habit in Triatominae (Heteroptera: Reduviidae). Rev Chil Hist Nat. 2015; 88: 4.
46. Justi SA, Russo CAM, Mallet JR dos S, Obara MT, Galvão C. Molecular phylogeny of Triatomini (Hemiptera: Reduviidae: Triatominae). Parasit Vectors. 2014; 7: 149.
47. Rabinovich JE, Kitron UD, Obed Y, Yoshioka M, Gottdenker N, Chaves LF. Ecological patterns of blood-feeding by kissing-bugs (Hemiptera: Reduviidae: Triatominae). Mem Inst Oswaldo Cruz. 2011; 106: 479-494.
48. Gupta AP. Cellular elements in hemolymph. In: Kerkut, G.A., Gilbert, L.I. (Eds.), Comprehensive Insect Physiology, Biochemistry, and Pharmacology. Pergamon Press, Oxford. 1985: 401-451.
49. Caselín-Castro S, Llanderal-Cázares C, Ramírez-Cruz A, Soto Hernández M, Méndez-Montiel JT. Caracterización morfológica de hemocitos de la hembra de Dactylopius coccus Costa (Hemiptera: Coccoidea: Dactylopiidae). Agrociencia. 2008; 42; 349-355.
50. Russo J, Allo MR, Nenon JP, Brehélin M. The hemocytes of the mealybugs Phenacoccus manihoti and Planococcus citri (Insecta: Homoptera) and their role in capsule formation. Can J Zool. 1994; 72(2): 252-258. DOI: https://doi.org/10.1139/z94-034.
51. Azambuja P, Garcia ES. Characterization of inducible lysozyme activity in the hemolymph of Rhodnius prolixus. Braz J Med Biol Res. 1987; 20: 539-548.
52. Mello CB, Garcia ES, Ratcliffe NA, Azambuja P. Trypanosoma cruzi and Trypanosoma rangeli: interplay with hemolymph components of Rhodnius prolixus. J Invertebr Pathol. 1995; 65: 261-268.
2. Tonn R, Otero M, Mora E, Espinola H, Carcavallo R. Aspectos biológicos, ecológicos y distribución geográfica de Triatoma maculata (Erichson 1948), (Hemiptera: Reduviidae), en Venezuela. Bol Dir Malariol Saneam Amb. 1978; 18: 16-24.
3. Feliciangeli MD, Dujardin JP, Bastrenta B, Mazzarri M, Villegas J, Flores M et al. Is Rhodnius robustus (Hemiptera: Reduviidae) responsible for Chagas disease transmission in Western Venezuela?. Trop Med Int Health. 2002; 17: 280-287.
4. Rojas M, Várquez P, Villarreal M, Velandia C, Vergara L, Morán Y et al. Estudio seroepidemiológico y entomológico sobre la enfermedad de Chagas en un área infestada
por Triatoma maculata (Erichson 1848) en el centro-occidente de Venezuela. Cad Saude Publ. 2008; 24: 2323-2333. DOI: http://dx.doi.org/10.1590/S0102-311X2008001000013.
5. Lent H, Wygodzinsky P. Revision of the Triatominae (Hemiptera, Reduviidae) and their significance as vectors of Chagas’ disease. Bull Am Museum Nat Hist. 1979; 163: 123-520.
6. Farfán AE, Gutierrez R, Angulo VM. ELISA para la identificación de los patrones alimentarios de Triatominae en Colombia. Rev. Salud Pública. 2007; 9: 602-608. DOI: http://dx.doi.org/10.1590/S0124-00642007000400013.
7. Carcavallo RU, Curto de Casas SI, Sherlock IA, Galíndez Girón I, Jurberg J, Galvao C, et al. Geographic distribution and alti-latitudinal dispersion. En: Carcavallo R.U., Galindez Girón I., Jurberg J., Lent, H. (Eds.), Atlas of Chagas Disease Vectors in the Americas, Vol. II. Fiocruz, Rio de Janeiro, Brazil. 1999; 747-792.
8. Soto A, Rodríguez C, Bonfante-Cabarca R, Aldana E. Morfometría geométrica de Triatoma maculata (Erichson, 1848) de ambientes doméstico y peridoméstico, estado Lara, Venezuela. Bol Dir Malariol San Amb. 2007; 47: 231-235.
9. García-Alzate R, Lozano-Arias D, Reyes-Lugo RM, Morocoima A, Herrera L, Mendoza-León A. Triatoma maculata, the vector of Trypanosoma cruzi, in Venezuela. Phenotypic and genotypic variability as potential indicator of vector displacement into the domestic habitat. Front Public Health. 2014; 2: 1-9. DOI: https://doi.org/10.3389/fpubh.2014.00170.
10. González-Brítez N, Morocoima A, Martínez C, Carrasco HJ. Infección por Trypanosoma cruzi y polimorfismo del citocromo B del ADN mitocondrial en Triatoma maculata de Anzoátegui y Portuguesa, Venezuela. Bol Mal Salud Amb. 2010; 50: 85-93.
11. Berrizbeitia M, Concepción J, Carzola V, Rodríguez J, Cáceres A, Quiñones W. Seroprevalencia de la infección por Trypanosoma cruzi en Canis familiaris del estado Sucre, Venezuela. Biomédica. 2013; 33: 214-225. DOI: http://dx.doi.org/10.7705/biomedica.v33i2.7.
12. García-Jordán N, Berrizbeitia M, Concepción JL, Aldana E, Cáceres A, Quiñones W. Estudio entomológico de vectores transmisores de la infección por Trypanosoma cruzi en la población rural del estado Sucre, Venezuela. Biomédica. 2015; 35: 247-257. DOI: https://doi.org/10.7705/biomedica.v35i2.2390.
13. Reyes-Lugo M, Reyes-Contreras M, Salvi I, Gelves W, Avilán A, Llavaneras D, et al. The association of Triatoma maculata (Ericsson 1848) with the gecko Thecadactylus rapicauda (Houttuyn 1782) (Reptilia: Squamata: Gekkonidae): a strategy of domiciliation of the Chagas disease peridomestic vector in Venezuela?. Asian Pac J Trop Biomed. 2011; 1: 279-284. DOI: 10.1016/S2221-1691(11)60043-9.
14. Morocoima A, Sotillo E, Salaverría C, Maniscalchi M, Pacheco F, Chique D. Domiciliación del vector peridomiciliario de la enfermedad de Chagas, Triatoma maculata (Erichson, 1848) en caserío rural del norte del estado Anzoátegui. Acta Cient Venezolana. 2005; 55: 215.
15. Luitgards-Moura J, Vargas A, Almeida C, Magno-Esperanca G, Agapito-Souza R, Folly-Ramos E, et al. A Triatoma maculata (Hemiptera, Reduviidae, Triatominae) population from Roraima, Amazon region, Brazil, has some bionomic characteristics of a potential Chagas disease vector. Rev Inst Med Trop São Paulo. 2005; 47: 131-137. DOI: http://dx.doi.org/10.1590/S0036-46652005000300003.
16. Ricardo-Silva A, Gonçalves Teresa CM, Luitgards-Moura JF, Lopes CM, Silva S, Bastos AQueiroz et al. Triatoma maculata colonises urban domicilies in Boa Vista, Roraima, Brazil. Mem Inst Oswaldo Cruz. 2016; 111: 703-706. DOI: 10.1590/0074-02760160026.
17. Corté LA, Suárez HA. Triatominos (Reduviidae: Triatominae) en un foco de enfermedad de Chagas en Talaigua Nuevo (Bolívar, Colombia). Rev Biomédica. 2005; 25: 568-574. DOI: https://doi.org/10.7705/issn.0120-4157.
18. Cantillo-Barraza O, Garces E, Gomez-Palacio A, Cortes LA, Pereira A, Marcet PL, et al. Ecoepidemiological study of an endemic Chagas disease region in northern Colombia reveals the importance of Triatoma maculata (Hemiptera: Reduviidae), dogs, and Didelphis marsupialis in Trypanosoma cruzi maintenance. Parasit Vectors. 2015; 8: 482. DOI: https://parasitesandvectors.biomedcentral.com/articles/10.1186/s13071-015-1100-2.
19. Azambuja P, Mello CB, Feder D, Garcia ES. Influence of cellular and humoral Triatominae defense system on the development of Trypanosomatides. En: Carcavallo RU, Galíndez Girón I, Juberg J, Lent H (eds). Atlas of Chagas Disease Vectors in the Americas, Vol. II. Fiocruz, Rio de Janeiro, Brazil. 1998; 709-733.
20. Wigglesworth VB. The physiology of the cuticle and of ecdysis in, with special reference to the function of the oenocytes and of the dermal glands. Quart J Micr Sci. 1933; 76: 269-318.
21. Wigglesworth VB. The role of haemocytes in the growth and moulting of an insect (Hemiptera). J Exp Biol. 1955; 32: 649-663.
22. Jones JC. The hemocytes of Rhodnius prolixus. Biol Bull Woods Hole. 1965; 129: 282-294.
23. Lai-Fook J. The fine structure of wound repair in an insect Rhodnius prolixus. J Morphol. 1968; 124: 7-78.
24. Lai- Fook J. Haemocytes in the repair of wouns in an insect Rhodnius prolixus. J Morphol. 1970; 130: 297-314.
25. Barracco MA, Oliveira R, Schlemper JR. The hemocytes of Panstrongylus megistus (Hemiptera: Reduviidae). Mem Inst Oswaldo Cruz. 1987; 82: 431-438. DOI: http://dx.doi.org/10.1590/S0074-02761987000300017.
26. Barracco MA, Loch C. Ultraestructural studies of the hemocytes of Panstrongylus megistus (Hemiptera: Reduviidae). Mem Inst Oswaldo Cruz. 1989; 84: 171-188. DOI: http://dx.doi.org/10.1590/S0074-02761989000200005.
27. Azambuja P, Garcia ES, Ratcliffe NA. Aspects of classification of hemipteran hemocytes from six triatomine species. Mem Inst Oswaldo Cruz. 1991; 86: 1-10. DOI: http://dx.doi.org/10.1590/S0074-02761991000100002.
28. Hypsa V, Grubhoffer L. Two hemocyte populations in Triatoma infestans: ultrastructural and lectin-binding characterization. Folia Parasitol. 1997; 44: 62-70.
29. Mello CB, Garcia ES, Ratcliffe NA, Azambuja P. Trypanosoma cruzi and Trypanosoma rangeli: interplay with hemolymph components of Rhodnius prolixus. J Invertebr Pathol. 1995; 65: 261-268.
30. Canavoso LE, Rubiolo ER. Hemolymphatic components in vectors of Trypanosoma cruzi: Study in several species of the subfamily Triatominae (Hemiptera: Reduviidae). Rev Inst Med Trop. 1993; 35: 123-128. DOI: http://dx.doi.org/10.1590/S0036-46651993000200003.
31. Canavoso LE, Rubiolo ER. Metabolic postfeeding changes in fat body and hemolymph of Dipetalogaster maximus (Hemiptera: Reduviidae). Mem Inst Oswaldo Cruz. 1998; 93: 225-230. DOI: http://dx.doi.org/10.1590/S0074-
02761998000200018.
32. Reyes-Lugo M, Girón ME, Kamiya H, Rodríguez Acosta A. A preliminary study of haemolymph from four Venezuelan populations of Panstrongylus geniculatus Latreille, 1811 (Hemiptera: Reduviidae) and its epidemiological significance. Rev Cubana Med. Trop. 2006; 58: 134-138.
33. Trinder P. Determination of glucose in blood using glucose oxidase with an alternative oxygen acceptor. Ann Clin Biochem 1969; 6: 24-27.
34. Layne E. Spectrophotometric and Turbidimetric Methods for Measuring Proteins. Methods in Enzymology. 1957; 10: 447-455.
35. 35. Frings CS, Fendley TW, Dunn RT, Queen CA. Improved determination of total serum lipids by the sulfo-phospho-vanillin reaction. Clin Chem. 1972; 18: 673-674.
36. Gupta AP. Hemocyte types: their structures, synonymies, interrelationships, and taxonomic significance. In Insect Hemocytes, ed. A.P. Gupta, Cambridge: Cambridge University Press. 1979: 85-127.
37. Palacios-Prü E, Palacios L, Mendoza RV. Synaptogenetic mechanisms during chick cerebellar cortex development. J Submicrosc Cytol. 1981; 13: 145-167.
38. Reynolds ES. The use of lead citrate at high pH as an electron-opaque satín in electron microscopy. J Cell Biol. 1963; 17: 208-212.
39. Watson ML. Staining of tissue sections for electron microscopy with heavy metals. J Biophys Biochem Cytol. 1958; 4: 475-478.
40. Pacheco MA, Concepción JL, Rangel JD, Ruiz MC, Michelangeli F, Domínguez-Bello MG. Stomach lysozymes of the three-toed sloth (Bradypusvariegatus), an arboreal folivore from the Neotropics. Comp Bioch Physiol. 2007; 147: 808–819. DOI: http://doi.org/10.1016/j.cbpa.2006.07.010.
41. Moreno J. Physiological mechanisms underlaying reproductive trade-off. Etologia. 1993; 3: 41-56.
42. Roff D. Life history evolution. Sinauer associates, Inc. USA. 2002; 132.
43. Ryan RO. Dynamics of insect lipophorin metabolism. J Lipids Res. 1990; 31: 1725-1739.
44. Flores-Villegas AL, Salazar-Schettino PM, Córdoba-Aguilar A, Gutiérrez-Cabrera AE, Rojas-Wastavino GE, Bucio-Torres MI, et al. Immune defence mechanisms of triatomines against bacteria, viruses, fungi and parasites. Bulletin of Entomological Research. 2015; 105, 523–532.
45. Otálora-Luna F, Pérez-Sánchez AJ, Sandoval C, Aldana E. Evolution of hematophagous habit in Triatominae (Heteroptera: Reduviidae). Rev Chil Hist Nat. 2015; 88: 4.
46. Justi SA, Russo CAM, Mallet JR dos S, Obara MT, Galvão C. Molecular phylogeny of Triatomini (Hemiptera: Reduviidae: Triatominae). Parasit Vectors. 2014; 7: 149.
47. Rabinovich JE, Kitron UD, Obed Y, Yoshioka M, Gottdenker N, Chaves LF. Ecological patterns of blood-feeding by kissing-bugs (Hemiptera: Reduviidae: Triatominae). Mem Inst Oswaldo Cruz. 2011; 106: 479-494.
48. Gupta AP. Cellular elements in hemolymph. In: Kerkut, G.A., Gilbert, L.I. (Eds.), Comprehensive Insect Physiology, Biochemistry, and Pharmacology. Pergamon Press, Oxford. 1985: 401-451.
49. Caselín-Castro S, Llanderal-Cázares C, Ramírez-Cruz A, Soto Hernández M, Méndez-Montiel JT. Caracterización morfológica de hemocitos de la hembra de Dactylopius coccus Costa (Hemiptera: Coccoidea: Dactylopiidae). Agrociencia. 2008; 42; 349-355.
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