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New report of Eratyrus cuspidatus Stål, 1859 (Hemiptera: Reduviidae: Triatominae) in the State of Campeche, Mexico

Abstract

INTRODUCTION:

Triatomine bugs are vectors of Trypanosoma cruzi, the etiological agent of Chagas disease.

METHODS:

Triatomine bugs were collected and identified following established protocols. In addition, infection with T. cruzi was detected by microscopic and molecular analysis.

RESULTS:

We captured an adult male specimen of the Eratyrus cuspidatus species that has not been reported in the state of Campeche.

CONCLUSIONS:

This finding provides new information on the distribution of E. cuspidatus in Mexico. However, more studies are needed to determine their epidemiological significance.

Keywords:
Triatominae; Eratyrus cuspidatus; Sylvatic vectors

Triatomine bugs are important vectors of Trypanosoma cruzi (Chagas, 1909), the etiological agent of Chagas disease, which is endemic across much of the Americas. According to the Pan American Health Organization, approximately 6 million people are infected and 65 million are at risk of contracting the infection11. Organización Panamericana de la Salud (OPS). Guía para el diagnóstico y el tratamiento de la enfermedad de Chagas. Washington, D.C.: OPS; 2018.. Currently, 150 extant and 2 extinct species of triatomines are known, and grouped into 16 genera22. Monteiro FA, Weirauch C, Felix M, Lazoski C, Abad-Franch F. Evolution, Systematics, and Biogeography of the Triatominae, Vectors of Chagas Disease. Advances in Parasitology. 2018;99:265-344.. In Mexico, approximately 33 triatomine (Hemiptera: Reduviidae: Triatominae) species have been reported, so far. It is therefore, one of the countries with the greatest diversity of triatomines. Two genera namely, Triatoma (20 species) and Meccus (6 species) are the most abundant and widely distributed33. Galvão C, Carcavallo R, Da Silva-Rocha D, Jurberg J. A checklist of the current valid species of the subfamily Triatominae Jeannel, 1919 (Hemiptera, Reduviidae) and their geographical distribution, with nomenclatural and taxonomic notes. Zootaxa. 2003;202(1):1-36.. However, other species, that until recently, had not been considered epidemiologically significant have also been reported33. Galvão C, Carcavallo R, Da Silva-Rocha D, Jurberg J. A checklist of the current valid species of the subfamily Triatominae Jeannel, 1919 (Hemiptera, Reduviidae) and their geographical distribution, with nomenclatural and taxonomic notes. Zootaxa. 2003;202(1):1-36.: Dipetalogaster maxima (Uhler, 1894), Eratyrus cuspidatus (Stål, 1859), Paratriatoma hirsuta (Barber, 1938), Panstrongylus rufotuberculatus (Champion, 1899), Triatoma nitida (Usinger, 1939), and Rhodnius prolixus (Stål, 1859). E. cuspidatus was found to be naturally infected with T. cruzi44. Lent H, Wygodzinsky P. Revision of the Triatominae (Hemiptera, Reduviidae), and their significance as vectors of Chagas disease. Bull Am Mus Nat Hist 1979;163(3):123-520.,55. Ayala CJ, Hernández CM, Escalante ME, Romero LR, Álvarez RA, Blanco P. Detección de Infección Natural por Trypanosoma cruzi (Trypanosomatidae) en Triatominos del Municipio de Colosó, Colombia. Acta Biol Colomb. 2019;24(1):180-4.,66. Dib J, Barnabe C, Tibayrenc M, Triana O. Incrimination of Eratyrus cuspidatus (Stål) in the transmission of Chagas' disease by molecular epidemiology analysis of Trypanosoma cruzi isolates from a geographically restricted area in the north of Colombia. Acta Trop. 2009;111(3):237-42.. They have begun to invade and colonize human dwellings. Since they transmit the etiologic agent of Chagas disease, more knowledge is needed about their distribution and ecology, to improve control strategies.

E. cuspidatus is distributed throughout Colombia, Ecuador, Guatemala, Mexico, Panama, Peru, and Venezuela33. Galvão C, Carcavallo R, Da Silva-Rocha D, Jurberg J. A checklist of the current valid species of the subfamily Triatominae Jeannel, 1919 (Hemiptera, Reduviidae) and their geographical distribution, with nomenclatural and taxonomic notes. Zootaxa. 2003;202(1):1-36.. In Mexico, it has been observed only in the three states: Chiapas, Veracruz, and Yucatan33. Galvão C, Carcavallo R, Da Silva-Rocha D, Jurberg J. A checklist of the current valid species of the subfamily Triatominae Jeannel, 1919 (Hemiptera, Reduviidae) and their geographical distribution, with nomenclatural and taxonomic notes. Zootaxa. 2003;202(1):1-36.,77. Zarate LG, Zarate RJ. A checklist of the Triatominae (Hemiptera: Reduviidae) of Mexico. Int J Entomol. 1985;27:102-27.,88. Ibañez-Bernal S, Paz-Rodríguez R, Alonzo-Parra D. Nuevo registro geográfico de Eratyrus cuspidatus Stål (Hemiptera: Reduviidae, Triatominae) de México. Fol Entomol Mex. 1995;94:63-4.,99. Reyes-Novelo E, Ruiz-Piña HA. New finding of Eratyrus cuspidatus Stål (Hemiptera: Reduviidae) in Yucatan. Dugesiana. 2012;18:143-5.. In the state of Campeche, Triatoma dimidiata (Latreille, 1811) is the only species associated with T. cruzi transmission, since the last 70 years44. Lent H, Wygodzinsky P. Revision of the Triatominae (Hemiptera, Reduviidae), and their significance as vectors of Chagas disease. Bull Am Mus Nat Hist 1979;163(3):123-520.. However other vector species have been identified in neighboring states. It is therefore, likely that more than one vector is present in Campeche33. Galvão C, Carcavallo R, Da Silva-Rocha D, Jurberg J. A checklist of the current valid species of the subfamily Triatominae Jeannel, 1919 (Hemiptera, Reduviidae) and their geographical distribution, with nomenclatural and taxonomic notes. Zootaxa. 2003;202(1):1-36.,77. Zarate LG, Zarate RJ. A checklist of the Triatominae (Hemiptera: Reduviidae) of Mexico. Int J Entomol. 1985;27:102-27..

Reports of sylvatic species of triatomines, contribute to the knowledge about current and new species distributions, and describe their role as existing or possible vectors of T. cruzi.

The state of Campeche is located within the following geographic coordinates: 17°48’46” N to 20°50’53” N and 92°28’7” W to 89°07’16” W. It is bordered to the north by the Gulf of Mexico and Yucatan, to the east by Quintana Roo and Belize, to the south by the Republic of Guatemala and the state of Tabasco, and to the west by the state of Tabasco and the Gulf of Mexico. The average annual temperature throughout the state is 26 °C while that along the coast is 28 °C1010. Instituto Nacional de Estadística Geografía e Informática. Marco Geoestadístico. INEGI; 2018 [updated 2018 june; cite 2019 june 17]. Available from: Available from: http:// www.inegi.org.mx/app/areasgeograficas/?ag=04
http:// www.inegi.org.mx/app/areasgeogra...
.

In March 2010, a study was conducted in Calakmul, a protected, natural, rainforest reserve, located in the Calakmul municipality, approximately 179.5 km from the capital city (Campeche). Triatomine bugs were collected manually, during the day, and with a lamp at night, according to the method described by Schofield1111. Schofield CJ. Triatominae. Biología y control. London UK: Eurocomunica; 1994.47-8p.. During the search, we examined all possible ecotopes (including hollow trees and cracks, holes in the ground, and stone piles). Captured specimens were placed in labeled flasks, containing folded cardboard sheets, and transported to the laboratory for morphological identification according to the key described by Lent and Wygodzinsky44. Lent H, Wygodzinsky P. Revision of the Triatominae (Hemiptera, Reduviidae), and their significance as vectors of Chagas disease. Bull Am Mus Nat Hist 1979;163(3):123-520.. Infection with flagellates was determined by microscopic observation of feces, obtained after abdominal compression, and dilution in phosphate buffered saline (PBS). Presence of T. cruzi was determined by PCR1212. Wincker P, Telleria J, Bosseno MF, Cardoso MA, Marques P, Yaksic N, et al. PCR based diagnosis for Chagas’ disease in Bolivian children living in an active transmission area: comparison with conventional serological and parasitological diagnosis. Parasitology. 1997;114(Pt 4):367-73..

Primarily, adults of T. dimidiata infected with T. cruzi were collected. Although this species was the most abundant, one adult of another triatominae species was collected. This specimen was probably attracted to the lights and consequently, captured near the bedroom, of the home of forest guards (18°21'54'' N and 089°53'32'' W) and visitors. It was identified as a male of E. cuspidatus44. Lent H, Wygodzinsky P. Revision of the Triatominae (Hemiptera, Reduviidae), and their significance as vectors of Chagas disease. Bull Am Mus Nat Hist 1979;163(3):123-520., which presents rounded discal tubercles, humeral angles angular or pointed but not spinose, and the process of the scutellum bent slightly upward (Figure 1). In contrast E. mucronatus presents discal tubercles in the form of strong spines, humeral angles distinctly spinose, and the scutellum upward in variable angle. The authors also compared the specimen with T. dimidiata, the more abundant vector in the area. T. dimidiata presents discal tubercles that are not pointed and not elevated, humeral angles rounded, a scutellum with a central area that is not depressed, and an apical process that is subcylindrical and bent slightly downward at the apex (Figure 2B). Identification of E. cuspidatus was confirmed by the entomologist, Alejandre-Aguilar, expert in triatomines, at the Laboratory of Entomology of the Escuela Nacional de Ciencias Biologicas del Instituto Politecnico Nacional.

FIGURE 1:
Lateral view of a male specimen of Eratyrus cuspidatus, length 23mm.

FIGURE 2:
Dorsal view of two male triatomine specimens: (A) Eratyrus cuspidatus, length 23mm. and (B) Triatoma dimidiata, 26mm.

The most important epidemiological species are those that live among humans and have a strong preference for human blood1111. Schofield CJ. Triatominae. Biología y control. London UK: Eurocomunica; 1994.47-8p.. However, sylvatic species are a source of infestation and re-infestation; in some cases, they even replace domestic species that had been controlled with chemical products (insecticides). When they adapt to the type of habitat and fauna, they can establish an ecological chain of epidemiologically important vector species1313. Peterson JK, Hashimoto K, Yoshioka K, Dorn PL, Gottdenker NL, Caranci A, et al. Chagas Disease in Central America: Recent Findings and Current Challenges in Vector Ecology and Control. Curr Trop Med Rep. 2019;6(2):76-91.. Thus, E. cuspidatus could contribute to the transmission of T. cruzi in humans, as reported in other countries1414. Ayala Hoyos CJ, Hernández Mendoza CM, Eyes Escalante M, Romero Ricardo LR, Álvarez Rodríguez RA, Blanco Tuirán P. Detección de infección natural por Trypanosoma cruzi (Trypanosomatidae) en triatominos del municipio de Colosó, Colombia. Acta biol. Colomb. 2019;24(1):180-4. DOI: http://dx.doi.org/10.15446/abc.v24n1.72306
https://doi.org/http://dx.doi.org/10.154...
.

In addition to T. dimidiata reported by Valdez-Tah et al.1515. Valdez-Tah A, Huicochea-Gómez L, Ortega-Canto J, Nazar-Beutelspacher A, Ramsey JM. Social Representations and Practices Towards Triatomines and Chagas Disease in Calakmul, México. Plos One. 2015;10(7):1-28., the occurrence of E. cuspidatus in proximity to a human dwelling suggests, that it may eventually become a part of the transmission cycle of T. cruzi among the human communities established in these areas.

This study reports the occurrence of a particular species that had not been previously reported in the state. It also reports the recent proximity of this species to human environments, possibly as a consequence of human movement into sylvatic areas.

We examined E. cuspidatus for T. cruzi infection. However, no flagellates were detected. Similarly, the result of PCR was also negative for the presence of T. cruzi. Thus, our findings concur with other reports of E. cuspidatus in Mexico. However, it is yet unknown, whether they are limited to sylvan areas, with occasional intrusion into human dwellings, or if they could possibly invade domestic areas. Therefore, more studies are needed to further investigate and determine the importance of these species as vectors of T. cruzi.

ACKNOWLEDGEMENTS

To Carlos Jesús Maas Nolasco for the photographs that appear in this work.

REFERENCES

  • 1
    Organización Panamericana de la Salud (OPS). Guía para el diagnóstico y el tratamiento de la enfermedad de Chagas. Washington, D.C.: OPS; 2018.
  • 2
    Monteiro FA, Weirauch C, Felix M, Lazoski C, Abad-Franch F. Evolution, Systematics, and Biogeography of the Triatominae, Vectors of Chagas Disease. Advances in Parasitology. 2018;99:265-344.
  • 3
    Galvão C, Carcavallo R, Da Silva-Rocha D, Jurberg J. A checklist of the current valid species of the subfamily Triatominae Jeannel, 1919 (Hemiptera, Reduviidae) and their geographical distribution, with nomenclatural and taxonomic notes. Zootaxa. 2003;202(1):1-36.
  • 4
    Lent H, Wygodzinsky P. Revision of the Triatominae (Hemiptera, Reduviidae), and their significance as vectors of Chagas disease. Bull Am Mus Nat Hist 1979;163(3):123-520.
  • 5
    Ayala CJ, Hernández CM, Escalante ME, Romero LR, Álvarez RA, Blanco P. Detección de Infección Natural por Trypanosoma cruzi (Trypanosomatidae) en Triatominos del Municipio de Colosó, Colombia. Acta Biol Colomb. 2019;24(1):180-4.
  • 6
    Dib J, Barnabe C, Tibayrenc M, Triana O. Incrimination of Eratyrus cuspidatus (Stål) in the transmission of Chagas' disease by molecular epidemiology analysis of Trypanosoma cruzi isolates from a geographically restricted area in the north of Colombia. Acta Trop. 2009;111(3):237-42.
  • 7
    Zarate LG, Zarate RJ. A checklist of the Triatominae (Hemiptera: Reduviidae) of Mexico. Int J Entomol. 1985;27:102-27.
  • 8
    Ibañez-Bernal S, Paz-Rodríguez R, Alonzo-Parra D. Nuevo registro geográfico de Eratyrus cuspidatus Stål (Hemiptera: Reduviidae, Triatominae) de México. Fol Entomol Mex. 1995;94:63-4.
  • 9
    Reyes-Novelo E, Ruiz-Piña HA. New finding of Eratyrus cuspidatus Stål (Hemiptera: Reduviidae) in Yucatan. Dugesiana. 2012;18:143-5.
  • 10
    Instituto Nacional de Estadística Geografía e Informática. Marco Geoestadístico. INEGI; 2018 [updated 2018 june; cite 2019 june 17]. Available from: Available from: http:// www.inegi.org.mx/app/areasgeograficas/?ag=04
    » http:// www.inegi.org.mx/app/areasgeograficas/?ag=04
  • 11
    Schofield CJ. Triatominae. Biología y control. London UK: Eurocomunica; 1994.47-8p.
  • 12
    Wincker P, Telleria J, Bosseno MF, Cardoso MA, Marques P, Yaksic N, et al. PCR based diagnosis for Chagas’ disease in Bolivian children living in an active transmission area: comparison with conventional serological and parasitological diagnosis. Parasitology. 1997;114(Pt 4):367-73.
  • 13
    Peterson JK, Hashimoto K, Yoshioka K, Dorn PL, Gottdenker NL, Caranci A, et al. Chagas Disease in Central America: Recent Findings and Current Challenges in Vector Ecology and Control. Curr Trop Med Rep. 2019;6(2):76-91.
  • 14
    Ayala Hoyos CJ, Hernández Mendoza CM, Eyes Escalante M, Romero Ricardo LR, Álvarez Rodríguez RA, Blanco Tuirán P. Detección de infección natural por Trypanosoma cruzi (Trypanosomatidae) en triatominos del municipio de Colosó, Colombia. Acta biol. Colomb. 2019;24(1):180-4. DOI: http://dx.doi.org/10.15446/abc.v24n1.72306
    » https://doi.org/http://dx.doi.org/10.15446/abc.v24n1.72306
  • 15
    Valdez-Tah A, Huicochea-Gómez L, Ortega-Canto J, Nazar-Beutelspacher A, Ramsey JM. Social Representations and Practices Towards Triatomines and Chagas Disease in Calakmul, México. Plos One. 2015;10(7):1-28.
  • Financial Support: This study was funded by the Autonomous University of Campeche Project number UACAM-EXB-065-2009.

Publication Dates

  • Publication in this collection
    27 Jan 2020
  • Date of issue
    2020

History

  • Received
    17 June 2019
  • Accepted
    30 Oct 2019
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