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First report of Rhodnius montenegrensis (Hemiptera: Reduviidae: Triatominae) in Bolivia

ABSTRACT

Background:

The subfamily Triatominae, which comprises 157 species, carries the protozoan Trypanosoma cruzi, the etiological agent of Chagas disease. This short communication reports for the first time the occurrence of Rhodnius montenegrensis in Bolivia.

Methods:

Active searches were carried out on palm trees of the genus Oenocarpus in Beni district, Bolivia.

Results:

Fifteen R. montenegrensis specimens were collected from a rural area of the Beni district, Bolivia, and tested positive for T. cruzi.

Conclusions:

This new report expands the geographic distribution of the species in Latin America. Due to their ability to transmit trypanosomatids, the species deserves the attention of vector control programs.

Keywords:
Entomological surveillance; Western Amazon; Kissing bugs; New record

The subfamily Triatominae is currently composed of 157 species with 18 genera11. Alevi KCC, Oliveira J, Rocha DS, Galvão C. Trends in Taxonomy of Chagas Disease Vectors (Hemiptera, Reduviidae, Triatominae): From Linnaean to Integrative Taxonomy. Pathogens. 2021;10(12):1627. Available from: https://doi.org/10.3390/pathogens10121627
https://doi.org/10.3390/pathogens1012162...

2. Gil-Santana HR, Chavez T, Pita S, Panzera F, Galvão C. Panstrongylus noireaui, a remarkable new species of Triatominae (Hemiptera, Reduviidae) from Bolivia. ZooKeys. 2022;1104:203-25. Available from: https://doi.org/10.3897/zookeys.1104.81879
https://doi.org/10.3897/zookeys.1104.818...
-33. OliveiraJPSC, Gil-Santana HR, Dale C, Galvão C.Triatoma guazuLent and Wygodzinsky Is a Junior Synonym ofTriatoma williamiGalvão, Souza and Lima. Insects. 2022;13(7):591. Available from: https://doi.org/10.3390/insects13070591
https://doi.org/10.3390/insects13070591...
. In Bolivia, there are 20 species of triatomines: Eratyrus mucronatus Stål, 1859; Microtriatoma trinidadensis (Lent, 1951); Panstrongylus geniculatus (Latreille, 1811); Panstrongylus guentheri Berg, 1879; Panstrongylus megistus (Burmeister, 1835); Panstrongylus noireaui Gil-Santana et al., 2022; Panstrongylus rufotuberculatus (Champion, 1899); Panstrongylus diasi Pinto & Lent, 1946; Psammolestes coreodes Bergroth, 1911;; Rhodnius micki Zhao et al., 2021; Rhodnius prolixus Stål, 1859; Rhodnius robustus Larrousse, 1927; Rhodnius stali Lent et al. 1993; Triatoma boliviana Martínez et al., 2007; Triatoma delpontei Romaña & Abalos, 1947; Triatoma garciabesi Carcavallo et al., 1967; Triatoma guasayana Wygodzinsky & Abalos, 1949; Triatoma infestans (Klug, 1834); Triatoma sordida Stål, 1859; and Triatoma venosa Stål, 187244. Galvão C, Carcavallo R, Rocha DDS, 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. Available from: https://doi.org/10.11646/zootaxa.202.1.1
https://doi.org/10.11646/zootaxa.202.1.1...

5. Martínez AE, Chávez ET, Sossa GD, Aranda AR, Vargas MB, Vidaurre PP. Triatoma boliviana sp. n. (Hemiptera: Reduviidae: Triatominae) de los valles subandinos de La Paz-Bolivia, similar a Triatoma nigromaculata Stål, 1859. Cuadernos Hospital de Clínicas. 2007;52(10):9-16.
-66. Zhao Y, Galvão C, Cai W. Rhodnius micki, a new species of Triatominae (Hemiptera, Reduviidae) from Bolivia. ZooKeys . 2021;1012:71-93. Available from: https://doi.org/10.3897/zookeys.1012.54779
https://doi.org/10.3897/zookeys.1012.547...
.

Rhodnius Stål, 1859 species are present in wild areas and consequently maintain the enzootic cycle, with the main ecotopes being palm trees of the genus Attalea. However, they have been reported to be present in and around homes (intradomiciliary and peridomiciliary), posing an epidemiological risk of transmission of Chagas disease, since they act as significant transmitters of natural infection with Trypanosoma cruzi (Chagas, 1909) (Kinetoplastida: Trypanosomatidae)77. Abad-Franch F, Monteiro FA, Jaramillo ON, Dias FBS, Gurgel-Gonçalves R, Diotaiuti L. Ecologia, evolução e da vigilância a longo prazo da doença de Chagas transmitidas por vetores: uma avaliação multi-escala da tribo Rhodniini (Triatominae). Acta Trop. 2009;110:159-77. Available from: https://doi.org/10.1016/j.actatropica.2008.06.005
https://doi.org/10.1016/j.actatropica.20...
-88. Dias FBS, Quartier M, Diotaiuti L, Mejía G, Harry M, Lima ACL, et al. Ecology of Rhodnius robustus Larrousse, 1927 (Hemiptera, Reduviidae, Triatominae) in Attalea palm trees of the Tapajós River Region (Pará State, Brazilian Amazon). Parasit Vectors. 2014;7(154):1-11. Available from: https://doi.org/10.1186/1756-3305-7-154
https://doi.org/10.1186/1756-3305-7-154...
.

The species Rhodnius montenegrensis has been registered only in Brazil, occurring in the states of Acre99. Meneguetti DUO, Tojal SD, Miranda PRM, Rosa JA, Camargo LMA. First report of Rhodnius montenegrensis (Hemiptera, Reduviidae, Triatominae) in the State of Acre, Brazil. Rev Soc Bras Med Trop. 2015;48(4):471-(3). Available from: https://doi.org/10.1590/0037-8682-0029-2015
https://doi.org/10.1590/0037-8682-0029-2...
, Amazonas1010. Madeira FP, Menezes LRM, Jesus AC, Moraes MHS, Oliveira J, Rosa JA, et al. First report of Rhodnius montenegrensis (Hemiptera, Reduviidae, Triatominae) in Amazonas, Brazil. Rev Soc Bras Med Trop . 2020;53:e20190436. Available from: https://doi.org/10.1590/0037-8682-0436-2019
https://doi.org/10.1590/0037-8682-0436-2...
, Rondônia1111. Rosa JA, Rocha CS, Gardim S, Pinto MC, Mendonça VJ, Ferreira Filho JCR, et al. Description of Rhodnius montenegrensis n. sp. (Hemiptera: Reduviidae: Triatominae) from the state of Rondônia, Brazil. Zootaxa. 2012;3478:62-76. Available from: https://doi.org/10.11646/zootaxa.3478.1.8.
https://doi.org/10.11646/zootaxa.3478.1....
, and Roraima1212. Gama Neto JL, Oliveira J, Rosa JA, Santos FM, Machado VA, Silva W. Two new records of Triatominae (Hemiptera: Reduviidae) from Roraima state, Brazil. Rev Chil de Entomol.2020;46(2):321-327. Available from: https://doi.org/10.35249/rche.46.2.20.23
https://doi.org/10.35249/rche.46.2.20.23...
. This distribution has been expanded with the present study, which aims to describe the first report of the occurrence of R. montenegrensis in Bolivia. Between 2019 and 2020, 15 specimens of R. montenegrensis were collected from rural areas in the municipality of Guayaramerin, Beni, and Bolivia (Figure 1).

FIGURE 1:
Location of R. montenegrensis collection in Bolivia in 2019.

Guajará-Mirim, in Brazil, borders Guayaramerin, located in Bolivia, and is considered a twin city separated by the Mamoré River1313. Márquez ME, Concepción JL, González-Marcano E, Mondolfi AP. Detection of Trypanosoma cruzi by polymerase chain reaction. In: Clinical Applications of PCR. Humana Press, New York, NY, 2016;125-141. Available from: https://doi.org/10.1007/978-1-4939-3360-0_12
https://doi.org/10.1007/978-1-4939-3360-...
. The first record of the species R. montenegrensis in 2012 was made in the municipality of Monte Negro1111. Rosa JA, Rocha CS, Gardim S, Pinto MC, Mendonça VJ, Ferreira Filho JCR, et al. Description of Rhodnius montenegrensis n. sp. (Hemiptera: Reduviidae: Triatominae) from the state of Rondônia, Brazil. Zootaxa. 2012;3478:62-76. Available from: https://doi.org/10.11646/zootaxa.3478.1.8.
https://doi.org/10.11646/zootaxa.3478.1....
, Rondônia, a city close to Guajará-Mirim; thus, we may justify the presence of this specimen in Bolivia due to the surroundings of these municipalities.

The specimens were collected by means of an active search in palm trees (genus Oenocarpus) distributed in areas of secondary forests and pasture lands. Using tweezers and machetes to assist in thinning, the bracts were removed (as they can lodge a large number of invertebrates and small vertebrates), and the triatomines were collected one at a time to avoid damage. We captured 15 triatomines - nine adults, three fourth-instar nymphs, and three fifth-instar nymphs of R. montenegrensis.

For identification, we used the method described by Rosa et al. (2012)1111. Rosa JA, Rocha CS, Gardim S, Pinto MC, Mendonça VJ, Ferreira Filho JCR, et al. Description of Rhodnius montenegrensis n. sp. (Hemiptera: Reduviidae: Triatominae) from the state of Rondônia, Brazil. Zootaxa. 2012;3478:62-76. Available from: https://doi.org/10.11646/zootaxa.3478.1.8.
https://doi.org/10.11646/zootaxa.3478.1....
. Fifteen triatomines were subjected to infection analysis and identification at the Parasitology Laboratory of the Department of Biological Sciences, Faculty of Pharmaceutical Sciences, Universidade Estadual Paulista, Campus de Araraquara. The specimens were added to the Triatominae collection (Figure 2) by Dr. José Maria Soares Barata (CTJMSB) at UNESP, Araraquara. The infectious capability of the triatomines was investigated by molecular analysis [conventional polymerase chain reaction (PCR)], to detect and confirm the presence of T. cruzi, the etiologic agent of Chagas disease.

FIGURE 2:
Rhodnius montenegrensis specimen captured in a palm tree in the municipality of Guayaramerin, Beni, Bolivia. Legends: R. montenegrensis. A: female: dorsal side; B: female: ventral side; C: male: dorsal side; D: male: ventral side; E: head; F: pronotum and scutellum; G: process of the I urotergite; H: male external genitalia - median process of the pygophore.

To identify T. cruzi, we first extracted the DNA with the PureLink™ Genomic DNA Mini Kit (Thermo Fisher Scientific, MA, USA), using the digestive tract of each collected triatomine suspended in absolute alcohol and stored at -20°C. For the PCR, we followed the kDNA-PCR protocol described by Márquez et al. (2016)1414. Neto TO, Nogueira RJB, Rafael CESS, Santos YY. As dinâmicas de transportes na fronteira Brasil-Bolívia: Guajará Mirim-Guayaramerín. Rev Transp y Territ. 2020; 22: 346-366. Available from: https://doi.org/10.34096/rtt.i22.6696
https://doi.org/10.34096/rtt.i22.6696...
. Among the 15 samples tested, 6 yielded positive results for T. cruzi (Figure 3).

FIGURE 3:
Caption: M - Marker (Ladder 1kb), CP - positive control (Y strain), Samples - C188, C327, C393, C580, C583 tested positive for T. cruzi. We used the forward primer 121: 5′ · AAATAATG TACGGGKGAGATGCATGA · 3′ and reverse primer 122: 5′ · GGTTCGATT GGGGTTGGTGTAATATA · 3′.

Rhodnius montenegrensis and R. robustus present some morphological similarities; however, morphological1515. De Carvalho DB, Congrains C, Chahad-Ehlers S, Pinotti H, Brito RA, Da Rosa JA. Differential transcriptome analysis supports Rhodnius montenegrensis and Rhodnius robustus (Hemiptera, Reduviidae, Triatominae) as distinct species. PLoS One. 2017;12(4):e0174997. Available from: https://doi.org/10.1371/journal.pone.0174997
https://doi.org/10.1371/journal.pone.017...
, morphometric1515. De Carvalho DB, Congrains C, Chahad-Ehlers S, Pinotti H, Brito RA, Da Rosa JA. Differential transcriptome analysis supports Rhodnius montenegrensis and Rhodnius robustus (Hemiptera, Reduviidae, Triatominae) as distinct species. PLoS One. 2017;12(4):e0174997. Available from: https://doi.org/10.1371/journal.pone.0174997
https://doi.org/10.1371/journal.pone.017...
, transcriptomic1515. De Carvalho DB, Congrains C, Chahad-Ehlers S, Pinotti H, Brito RA, Da Rosa JA. Differential transcriptome analysis supports Rhodnius montenegrensis and Rhodnius robustus (Hemiptera, Reduviidae, Triatominae) as distinct species. PLoS One. 2017;12(4):e0174997. Available from: https://doi.org/10.1371/journal.pone.0174997
https://doi.org/10.1371/journal.pone.017...
, and cytogenetic1616. Pita S, Lorite P, Cuadrado A, Panzera Y, Oliveira J, Alevi KCC, et al. High chromosomal mobility of ribosomal clusters in holocentric chromosomes of Triatominae, vectors of Chagas disease (Hemiptera-Reduviidae). Med Vet Entomol. 2022 Mar;36(1):66-80. Available from: 10.1111/mve.12552
https://doi.org/10.1111/mve.12552...
studies have allowed differentiation of the species and confirmed the specific status of R. montenegrensis. For this reason, there may be an erroneous description of the distribution of R. montenegrensis, both in Brazil and in other Latin American countries (with an emphasis on countries bordering Brazil).

R. montenegrensis specimens collected from palm trees and residences revealed their ability to adapt to the human environment, dispersal, and mobility1717. Jesus AC, Madeira FP, Moraes MHDS, Morais AA, Oliveira J, Rosa JA, Camargo LMA, Meneguetti DUO, Bernarde PS. Occurrence of triatomines (Hemiptera, Reduviidae) and their natural infection by Trypanosoma cruzi (Chagas, 1909) in Boca do Moa community, Cruzeiro do Sul, Acre, Brazil. Rev Soc Bras Med Trop . 2021;8(54):e0590-2020. Available from: https://doi.org/10.1590/0037-8682-0590-2020
https://doi.org/10.1590/0037-8682-0590-2...
. Studies conducted in Acre, Amazonas, and Rondônia demonstrate the predominance of this species in its natural ecotope, and intrusion into residences and the infection rate for T. cruzi in this species are significant in the localities where they were captured99. Meneguetti DUO, Tojal SD, Miranda PRM, Rosa JA, Camargo LMA. First report of Rhodnius montenegrensis (Hemiptera, Reduviidae, Triatominae) in the State of Acre, Brazil. Rev Soc Bras Med Trop. 2015;48(4):471-(3). Available from: https://doi.org/10.1590/0037-8682-0029-2015
https://doi.org/10.1590/0037-8682-0029-2...

10. Madeira FP, Menezes LRM, Jesus AC, Moraes MHS, Oliveira J, Rosa JA, et al. First report of Rhodnius montenegrensis (Hemiptera, Reduviidae, Triatominae) in Amazonas, Brazil. Rev Soc Bras Med Trop . 2020;53:e20190436. Available from: https://doi.org/10.1590/0037-8682-0436-2019
https://doi.org/10.1590/0037-8682-0436-2...
-1111. Rosa JA, Rocha CS, Gardim S, Pinto MC, Mendonça VJ, Ferreira Filho JCR, et al. Description of Rhodnius montenegrensis n. sp. (Hemiptera: Reduviidae: Triatominae) from the state of Rondônia, Brazil. Zootaxa. 2012;3478:62-76. Available from: https://doi.org/10.11646/zootaxa.3478.1.8.
https://doi.org/10.11646/zootaxa.3478.1....
,1717. Jesus AC, Madeira FP, Moraes MHDS, Morais AA, Oliveira J, Rosa JA, Camargo LMA, Meneguetti DUO, Bernarde PS. Occurrence of triatomines (Hemiptera, Reduviidae) and their natural infection by Trypanosoma cruzi (Chagas, 1909) in Boca do Moa community, Cruzeiro do Sul, Acre, Brazil. Rev Soc Bras Med Trop . 2021;8(54):e0590-2020. Available from: https://doi.org/10.1590/0037-8682-0590-2020
https://doi.org/10.1590/0037-8682-0590-2...
. Another aspect described in these studies is the non-occurrence of domiciliation of R. montenegrensis1010. Madeira FP, Menezes LRM, Jesus AC, Moraes MHS, Oliveira J, Rosa JA, et al. First report of Rhodnius montenegrensis (Hemiptera, Reduviidae, Triatominae) in Amazonas, Brazil. Rev Soc Bras Med Trop . 2020;53:e20190436. Available from: https://doi.org/10.1590/0037-8682-0436-2019
https://doi.org/10.1590/0037-8682-0436-2...
,1717. Jesus AC, Madeira FP, Moraes MHDS, Morais AA, Oliveira J, Rosa JA, Camargo LMA, Meneguetti DUO, Bernarde PS. Occurrence of triatomines (Hemiptera, Reduviidae) and their natural infection by Trypanosoma cruzi (Chagas, 1909) in Boca do Moa community, Cruzeiro do Sul, Acre, Brazil. Rev Soc Bras Med Trop . 2021;8(54):e0590-2020. Available from: https://doi.org/10.1590/0037-8682-0590-2020
https://doi.org/10.1590/0037-8682-0590-2...
.

With the expansion of this species in Brazilian states and a neighboring country, such as Bolivia, it is pertinent to affirm the epidemiological importance of including this species in the transmission cycle of Chagas disease in the Brazilian and international Amazon.

Rhodnius montenegrensis has also been reported in domestic environments, but only in the countryside1818. Meneguetti DUO, Soares EBA, Campaner M, Camargo LMA. First report of Rhodnius montenegrensis (Hemiptera: Reduviidae: Triatominae) infection by Trypanosoma rangeli. Rev Soc Bras Med Trop . 2014;47(3):374-376. Available from: https://doi.org/10.1590/0037-8682-0179-2013
https://doi.org/10.1590/0037-8682-0179-2...
. In addition, it has been found to be naturally infected with Trypanosoma rangeli Tejera, 1920, which is of major importance because the difficulty in isolation and diagnosis may be related to a double trypanosomatid infection, which can lead to false positive or true positive results for Chagas disease1818. Meneguetti DUO, Soares EBA, Campaner M, Camargo LMA. First report of Rhodnius montenegrensis (Hemiptera: Reduviidae: Triatominae) infection by Trypanosoma rangeli. Rev Soc Bras Med Trop . 2014;47(3):374-376. Available from: https://doi.org/10.1590/0037-8682-0179-2013
https://doi.org/10.1590/0037-8682-0179-2...
,1919. Peterson JK, Graham AL, Elliott RJ, Dobson AP, Triana Chávez O. Trypanosoma cruzi-Trypanosoma rangeli co-infection ameliorates negative effects of single trypanosome infections in experimentally infected Rhodnius prolixus. Parasitology. 2016;143(9):1157-1167. Available from: https://doi.org/10.1017/S0031182016000615
https://doi.org/10.1017/S003118201600061...
. This new report on the occurrence of R. montenegrensis expands the geographic distribution of the species in Latin America, with Bolivia being the second country to register the presence of the insect and increasing the number of species described in the locality.

ACKNOWLEDGMENTS

We would like to thank the Federal Institute of Education, Science and Technology of Rondônia (IFRO), Guajará-Mirim Campus, for the technical support in carrying out the study. The second-last author (JO) thanks: São Paulo State Research Support Foundation - FAPESP for the scholarship. The last author (JAR) thanks CNPq for the productivity grant, process 317358/2021-9.

REFERENCES

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    Alevi KCC, Oliveira J, Rocha DS, Galvão C. Trends in Taxonomy of Chagas Disease Vectors (Hemiptera, Reduviidae, Triatominae): From Linnaean to Integrative Taxonomy. Pathogens. 2021;10(12):1627. Available from: https://doi.org/10.3390/pathogens10121627
    » https://doi.org/10.3390/pathogens10121627
  • 2
    Gil-Santana HR, Chavez T, Pita S, Panzera F, Galvão C. Panstrongylus noireaui, a remarkable new species of Triatominae (Hemiptera, Reduviidae) from Bolivia. ZooKeys. 2022;1104:203-25. Available from: https://doi.org/10.3897/zookeys.1104.81879
    » https://doi.org/10.3897/zookeys.1104.81879
  • 3
    OliveiraJPSC, Gil-Santana HR, Dale C, Galvão C.Triatoma guazuLent and Wygodzinsky Is a Junior Synonym ofTriatoma williamiGalvão, Souza and Lima. Insects. 2022;13(7):591. Available from: https://doi.org/10.3390/insects13070591
    » https://doi.org/10.3390/insects13070591
  • 4
    Galvão C, Carcavallo R, Rocha DDS, 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. Available from: https://doi.org/10.11646/zootaxa.202.1.1
    » https://doi.org/10.11646/zootaxa.202.1.1
  • 5
    Martínez AE, Chávez ET, Sossa GD, Aranda AR, Vargas MB, Vidaurre PP. Triatoma boliviana sp. n. (Hemiptera: Reduviidae: Triatominae) de los valles subandinos de La Paz-Bolivia, similar a Triatoma nigromaculata Stål, 1859. Cuadernos Hospital de Clínicas. 2007;52(10):9-16.
  • 6
    Zhao Y, Galvão C, Cai W. Rhodnius micki, a new species of Triatominae (Hemiptera, Reduviidae) from Bolivia. ZooKeys . 2021;1012:71-93. Available from: https://doi.org/10.3897/zookeys.1012.54779
    » https://doi.org/10.3897/zookeys.1012.54779
  • 7
    Abad-Franch F, Monteiro FA, Jaramillo ON, Dias FBS, Gurgel-Gonçalves R, Diotaiuti L. Ecologia, evolução e da vigilância a longo prazo da doença de Chagas transmitidas por vetores: uma avaliação multi-escala da tribo Rhodniini (Triatominae). Acta Trop. 2009;110:159-77. Available from: https://doi.org/10.1016/j.actatropica.2008.06.005
    » https://doi.org/10.1016/j.actatropica.2008.06.005
  • 8
    Dias FBS, Quartier M, Diotaiuti L, Mejía G, Harry M, Lima ACL, et al. Ecology of Rhodnius robustus Larrousse, 1927 (Hemiptera, Reduviidae, Triatominae) in Attalea palm trees of the Tapajós River Region (Pará State, Brazilian Amazon). Parasit Vectors. 2014;7(154):1-11. Available from: https://doi.org/10.1186/1756-3305-7-154
    » https://doi.org/10.1186/1756-3305-7-154
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    Meneguetti DUO, Tojal SD, Miranda PRM, Rosa JA, Camargo LMA. First report of Rhodnius montenegrensis (Hemiptera, Reduviidae, Triatominae) in the State of Acre, Brazil. Rev Soc Bras Med Trop. 2015;48(4):471-(3). Available from: https://doi.org/10.1590/0037-8682-0029-2015
    » https://doi.org/10.1590/0037-8682-0029-2015
  • 10
    Madeira FP, Menezes LRM, Jesus AC, Moraes MHS, Oliveira J, Rosa JA, et al. First report of Rhodnius montenegrensis (Hemiptera, Reduviidae, Triatominae) in Amazonas, Brazil. Rev Soc Bras Med Trop . 2020;53:e20190436. Available from: https://doi.org/10.1590/0037-8682-0436-2019
    » https://doi.org/10.1590/0037-8682-0436-2019
  • 11
    Rosa JA, Rocha CS, Gardim S, Pinto MC, Mendonça VJ, Ferreira Filho JCR, et al. Description of Rhodnius montenegrensis n. sp. (Hemiptera: Reduviidae: Triatominae) from the state of Rondônia, Brazil. Zootaxa. 2012;3478:62-76. Available from: https://doi.org/10.11646/zootaxa.3478.1.8.
    » https://doi.org/10.11646/zootaxa.3478.1.8
  • 12
    Gama Neto JL, Oliveira J, Rosa JA, Santos FM, Machado VA, Silva W. Two new records of Triatominae (Hemiptera: Reduviidae) from Roraima state, Brazil. Rev Chil de Entomol.2020;46(2):321-327. Available from: https://doi.org/10.35249/rche.46.2.20.23
    » https://doi.org/10.35249/rche.46.2.20.23
  • 13
    Márquez ME, Concepción JL, González-Marcano E, Mondolfi AP. Detection of Trypanosoma cruzi by polymerase chain reaction. In: Clinical Applications of PCR. Humana Press, New York, NY, 2016;125-141. Available from: https://doi.org/10.1007/978-1-4939-3360-0_12
    » https://doi.org/10.1007/978-1-4939-3360-0_12
  • 14
    Neto TO, Nogueira RJB, Rafael CESS, Santos YY. As dinâmicas de transportes na fronteira Brasil-Bolívia: Guajará Mirim-Guayaramerín. Rev Transp y Territ. 2020; 22: 346-366. Available from: https://doi.org/10.34096/rtt.i22.6696
    » https://doi.org/10.34096/rtt.i22.6696
  • 15
    De Carvalho DB, Congrains C, Chahad-Ehlers S, Pinotti H, Brito RA, Da Rosa JA. Differential transcriptome analysis supports Rhodnius montenegrensis and Rhodnius robustus (Hemiptera, Reduviidae, Triatominae) as distinct species. PLoS One. 2017;12(4):e0174997. Available from: https://doi.org/10.1371/journal.pone.0174997
    » https://doi.org/10.1371/journal.pone.0174997
  • 16
    Pita S, Lorite P, Cuadrado A, Panzera Y, Oliveira J, Alevi KCC, et al. High chromosomal mobility of ribosomal clusters in holocentric chromosomes of Triatominae, vectors of Chagas disease (Hemiptera-Reduviidae). Med Vet Entomol. 2022 Mar;36(1):66-80. Available from: 10.1111/mve.12552
    » https://doi.org/10.1111/mve.12552
  • 17
    Jesus AC, Madeira FP, Moraes MHDS, Morais AA, Oliveira J, Rosa JA, Camargo LMA, Meneguetti DUO, Bernarde PS. Occurrence of triatomines (Hemiptera, Reduviidae) and their natural infection by Trypanosoma cruzi (Chagas, 1909) in Boca do Moa community, Cruzeiro do Sul, Acre, Brazil. Rev Soc Bras Med Trop . 2021;8(54):e0590-2020. Available from: https://doi.org/10.1590/0037-8682-0590-2020
    » https://doi.org/10.1590/0037-8682-0590-2020
  • 18
    Meneguetti DUO, Soares EBA, Campaner M, Camargo LMA. First report of Rhodnius montenegrensis (Hemiptera: Reduviidae: Triatominae) infection by Trypanosoma rangeli Rev Soc Bras Med Trop . 2014;47(3):374-376. Available from: https://doi.org/10.1590/0037-8682-0179-2013
    » https://doi.org/10.1590/0037-8682-0179-2013
  • 19
    Peterson JK, Graham AL, Elliott RJ, Dobson AP, Triana Chávez O. Trypanosoma cruzi-Trypanosoma rangeli co-infection ameliorates negative effects of single trypanosome infections in experimentally infected Rhodnius prolixus Parasitology. 2016;143(9):1157-1167. Available from: https://doi.org/10.1017/S0031182016000615
    » https://doi.org/10.1017/S0031182016000615
  • Financial Support: This study was financed in part by the National Council for Scientific and Technological Development (CNPq), Brazil. JAR: CNPq, PQ-2, process 307 398/2018-8; Federal Institute of Education, Science and Technology of Rondônia (IFRO), Public notice No.5/2021/REITPROPESP/IFRO, DE 05 DE JULHO DE 2021.

Publication Dates

  • Publication in this collection
    24 Oct 2022
  • Date of issue
    2022

History

  • Received
    29 Apr 2022
  • Accepted
    11 Aug 2022
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