First report of <i>Microtriatoma borbai</i> Lent &amp; Wygodzinsky, 1979 (Hemiptera, Reduviidae, Triatominae) in the state of Espírito Santo, Brazil: would <i>M. borbai</i> be living in eucalyptus crops?

Gil-Santana, Hélcio Reinaldo; Martins, David dos Santos; Silva, João Bosco da; Oliveira, Jader de

doi:10.1590/0037-8682-0147-2021

Abstract

INTRODUCTION: The occurrence of Microtriatoma borbai in the state of Espírito Santo, Brazil is reported by the first time.

METHODS: A triatomine specimen collected in a hybrid eucalyptus crop in the municipality of Aracruz, Espírito Santo state was found to be a male M. borbai.

RESULTS: This finding expands the geographical distribution of M. borbai from four to five Brazilian states. It is the first report of M. borbai occurrence inside a eucalyptus crop.

CONCLUSIONS: The occurrence of M. borbai in the state of Espírito Santo broadens the geographical distribution of this species in southeastern Brazil.

Keywords: Biogeography; Bolboderini; Kissing bugs

All species included in the subfamily Triatominae are blood-sucking bugs; they are either proven or potential vectors of Chagas disease caused by the protozoan Trypanosoma cruzi (Chagas, 1909) (Kinetoplastida, Trypanosomatidae). Chagas disease is a major public health issue in Latin America¹^,².

Currently, the subfamily Triatominae includes 156 species, grouped into five tribes³^,⁴^,⁵^,⁶. The tribe Bolboderini comprises four genera; among them, Microtriatoma Prosen & Martínez, 1952 has two species: M. borbai Lent & Wygodzinsky, 1979 and M. trinidadensis (Lent, 1951)¹^,². Microtriatoma trinidadensis is very widely distributed and has been found in nine countries and several Brazilian states, whereas M. borbai has been reported only in a few states in Brazil so far¹^,⁷^,⁸^,⁹^,¹⁰^,¹¹^,¹².

Microtriatoma borbai was described based on seven male and one female specimens collected in Curitiba, Paraná state, southern Brazil. These belonged to a small population found in clusters of bromeliads, where opossums of the genus Didelphis Linnaeus, 1758 (Didelphimorphia, Didelphidae) and rodents were also present. One of these specimens of M. borbai was found to be infected with Trypanosoma cruzi¹. Rodrigues et al.⁷ found three specimens of M. borbai in a shelter of opossums in Campinas, São Paulo state, Brazil. Among them, one was positive for T. cruzi and marsupial blood. Carcavallo et al.⁸ summarized these previous occurrences of M. borbai and included a doubtful occurrence of the species in Goiás state, Brazil although they did not cite the source or the exact locality in this state. Alencar et al.⁹ reported the occurrence of M. borbai based on a male and a female specimen collected in the city and state of Rio de Janeiro, Brazil in 1963. The specimens were pinned together and deposited in the National Museum in Rio de Janeiro, without any further information about how or in which environment (e.g. a shelter) they were collected. Among 2,154 triatomine specimens collected in Mauritia flexuosa L.f. (Arecales, Arecaceae), a palm tree, in several locations by Gurgel-Gonçalves et al.¹⁰, a female specimen of M. borbai was found in Alto Garça, Mato Grosso state, Brazil. They hypothesized that the occurrence of M. borbai in M. flexuosa could be associated with the presence of the white-eared opossum, Didelphis albiventris Lund, 1840, in these palm trees.

Only eight species belonging to other three tribes of Triatominae have been reported in Espírito Santo state, Brazil so far: Cavernicola pilosa Barber, 1937 belonging to the tribe Cavernicolini; Panstrongylus diasi Pinto & Lent, 1946; Panstrongylus geniculatus (Latreille, 1811); Panstrongylus megistus (Burmeister, 1835); Triatoma infestans (Klug, 1834); Triatoma tibiamaculata (Pinto, 1926); and Triatoma vitticeps (Stål, 1859) belonging to the tribe Triatomini; and Rhodnius domesticus Neiva & Pinto, 1923 belonging to the tribe Rhodniini¹¹^,¹³^,¹⁴.

When examining the private insect collection of Suzano S.A., Unidade Aracruz, the second author (DSM) asked for a loan of some specimens, one of which was identified by the first author (HRG-S) as a male specimen of M. borbai (Figure 1). The specimen was collected from a light trap inside a crop of Eucalyptus urograndis in Aracruz, Espírito Santo state, Brazil, situated at 20°27ʹ02,38ʹʹS 40°23ʹ26,17ʹʹW, by João Bosco da Silva on December 23, 1997. Considering the importance of preserving the specimen in a public scientific collection, Suzano S.A., Unidade Aracruz donated it to the Herman Lent Collection of the Coleção de Triatomíneos do Instituto Oswaldo Cruz (CTIOC), do Laboratório Nacional e Internacional de Referência em Taxonomia de Triatomíneos (LNIRTT) in Oswaldo Cruz Institute, Rio de Janeiro, Brazil; the specimen was deposited under the number 3459.

FIGURE 1:
Dorsal view of the male specimen of Microtriatoma borbai Lent & Wygodzinsky, 1979 collected in Aracruz, Espírito Santo state, Brazil in 1997. Scale bar: 1.0 mm.

Eucalyptus urograndis S. T. Blake (Myrtales, Myrtaceae) is a hybrid between Eucalyptus grandis W. Hill ex Maiden and Eucalyptus urophylla S. T. Blake and is of major economic importance to the Brazilian pulp and paper industry¹⁵.

The specimen of Triatominae was identified as M. borbai following a consultation with keys, diagnosis and descriptions available in the literature¹^,¹³ as well as a comparison with type specimens of M. borbai, which were previously deposited in the CTIOC and were examined by the first author (HRG-S). The characteristics of the specimen (Figure 1) showed complete concordance with those of M. borbai according to all sources of information. In short, the identification was based on the following characteristics: a small triatomine (total length of 6.5 mm) with a dorsoventrally compressed body; integument rugose covered by short setae; maxillary plates (=genae, auct.) salient, large, projecting beyond apex of clypeus; inconspicuous ocelli; short legs with thickened femora (corresponding to the tribe Bolboderini), which do not have spines (corresponding to the genus Microtriatoma); visible proximal and distal labial segments of the same length; and membrane of hemelytra uniformly dark, but not speckled with light and dark (corresponding to M. borbai).

Notably, most previous records of M. borbai were based on one to three specimens only⁷^,⁹^,¹⁰, indicating that the species is somewhat rare or its populations are composed by few individuals. Therefore, although the present report of M. borbai in the state of Espírito Santo is based on only one specimen, it fairly supports the inclusion of this state in the geographical distribution of M. borbai (Figure 2).

FIGURE 2:
A general map of South America showing the geographical distribution of Microtriatoma borbai. Brazil is shown in green, and other countries are shown in gray. Locations of the previous occurrences of M. borbai are marked as yellow circles. The new record is indicated by the red asterisk (*). Abbreviations of Brazilian states: ES: Espírito Santo; MT: Mato Grosso; PR: Paraná; RJ: Rio de Janeiro; SP: São Paulo.

On the other hand, previous occurrences of M. borbai were associated with the shelters of opossums and rodents, clusters of bromeliads and M. flexuosa¹^,⁷^,¹⁰. Therefore, the collection of a M. borbai specimen inside a eucalyptus crop, which is a remarkably different environment than those reported previously, is striking. In fact, exotic tree monocultures, such as eucalyptus monocultures, are considered an important factor in reducing the composition of native species in the cultivation area¹⁶^,¹⁷. Therefore, future studies with more intensive and diversified methods of collecting triatomine specimens should be carried out in the region to ascertain if the occurrence of M. borbai in a eucalyptus crop was an isolated event or if M. borbai, endemic to Brazil, has eventually adapted to this crop.

ACKNOWLEDGMENTS

The authors are grateful to the Suzano S.A., Unidade Aracruz, for the donation of the specimen of Microtriatoma borbai studied here; to Dr. Cleber Galvão (CTIOC) for allowing the deposit of the specimen in his institution, and Dr. Ruy José Válka Alves (Federal University of Rio de Janeiro) for the information on botanical nomenclature. The second author (DSM) thanks the Confederação da Agricultura e Pecuária do Brasil (CNA), Empresa Brasileira de Pesquisa Agropecuária (Embrapa), and Instituto Capixaba de Pesquisa Assistência Técnica e Extensão Rural (Incaper) for the financial support to the Biomes of Brazil/Atlantic Forest Biome Project (Subproject MA 25).

REFERENCES

¹ Lent H, Wygodzinsky P. Revision of the Triatominae (Hemiptera: Reduviidae) and their significance as vectors of Chagas’ disease. Bull Am Mus Nat Hist. 1979;163:123-520.
² Monteiro FA, Weirauch C, Félix M, Lazoski C, Abad-Franch F. Evolution, systematics, and biogeography of the Triatominae, vectors of Chagas disease. Adv Parasitol. 2018;99:265-344. Available from: https://doi.org/10.1016/bs.apar.2017.12.002
» https://doi.org/10.1016/bs.apar.2017.12.002
³ Galvão C. Taxonomia dos Vetores da Doença de Chagas da Forma à Molécula, quase três séculos de história. In: Atualidades em Medicina Tropical no Brasil: Vetores (1º ed.) Oliveira J, Alevi KCC, Camargo LMA, Meneguetti DUO (eds). (2020) pp 9-37, Stricto Sensu Editora.
⁴ Justi AS, Galvão C. The Evolutionary Origin of Diversity in Chagas Disease Vectors. Trends Parasitol. 2017;33(1):42-52.
⁵ Alevi KCC, Oliveira J, Garcia ACC, Cristal DC, Delgado LMG, de Freitas Bittinelli I, et al.Triatoma rosaisp. nov. (Hemiptera, Triatominae): A New Species of Argentinian Chagas Disease Vector Described Based on Integrative Taxonomy. Insects. 2020;11(12):830. Available from: https://doi.org/10.3390/insects11120830
» https://doi.org/10.3390/insects11120830
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 Rodrigues VLCC, Ferraz Filho AN, Silva EOR, Lima VLC. Prevalência, índices de infecção e hábitos alimentares de triatomíneos capturados em uma área de vigilância epidemiológica. Rev Soc Bras Med Trop. 1992;25(3):183-90.
⁸ Carcavallo RU, Curto de Casas SI, Galíndez Girón I, Jurberg J, Mena Segura C. Geographical and altitudinal dispersion of genera species of the tribes Alberproseniini, Bolboderini and Cavernicolini. Entomol. Vect. 1995;2(6):127-44.
⁹ Alencar J, Carcavallo RU, Jurberg J, Gil-Santana H. Registro de ocorrência do Microtriatoma borbai Lent & Wygodzinsky, 1979 no Estado do Rio de Janeiro, Brasil (Hemiptera, Reduviidae, Triatominae). Entomol Vect. 2000;7(4):445-7.
¹⁰ Gurgel-Gonçalves R, Cura C, Schijman AG, Cuba Cuba CA. Infestation of Mauritia flexuosa palms by triatomines (Hemiptera: Reduviidae), vectors of Trypanosoma cruzi and Trypanosoma rangeli in the Brazilian savanna. Acta Trop. 2012;121(2):105-11.
¹¹ Galvão C, Carcavallo R, Rocha DS, 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;202:1-36.
¹² Souza ES, Monte GLS, Paiva VF, Galvão C. Microtriatoma trinidadensis (Lent, 1951) (Hemiptera, Reduviidae, Triatominae): first record in the state of Amazonas, Brazil. Check List 2019; 15(5):905-909. Available from: https://doi.org/10.15560/15.5.905
» https://doi.org/10.15560/15.5.905
¹³ Galvão C. Vetores da doença de Chagas no Brasil. Curitiba: Sociedade Brasileira de Zoologia; 2014. 289 p.
¹⁴ Oliveira J, Rosa JA, Alevi KCC. Chagas disease vectors of Espírito Santo, Brazil: first report of Triatoma infestans (Klug, 1834) (Hemiptera, Triatominae) in Brazilian state and development of an identification key based on cytogenetic date. Am J Trop Med Hyg. 2021;104(2):653-5.
¹⁵ Leonardi GA, Carlos NA, Mazzafera P, Balbuena TS. Eucalyptus urograndis stem proteome is responsive to short-term cold stress. Genet Mol Biol. 2015;38(2):191-8. Available from: http://dx.doi.org/10.1590/S1415-475738220140235
» http://dx.doi.org/10.1590/S1415-475738220140235
¹⁶ Majer JD, Recher HF. Are Eucalypts Brazil’s Friend or Foe? An Entomological Viewpoint. An Soc Entomol Brasil 1999;28(2):185-200.
¹⁷ Rocha PLB, Viana BF, Cardoso MZ, Melo AMC, Costa MGC, Vasconcelos RN, et al. What is the value of eucalyptus monocultures for the biodiversity of the Atlantic forest? A multitaxa study in southern Bahia, Brazil. J For Res. 2013;24:263-72. Available from: https://doi.org/10.1007/s11676-012-0311-z
» https://doi.org/10.1007/s11676-012-0311-z

Publication Dates

Publication in this collection
02 June 2021
Date of issue
2021

History

Received
11 Mar 2021
Accepted
14 Apr 2021

This is an open-access article distributed under the terms of the Creative Commons Attribution License

[1] ¹ Lent H, Wygodzinsky P. Revision of the Triatominae (Hemiptera: Reduviidae) and their significance as vectors of Chagas’ disease. Bull Am Mus Nat Hist. 1979;163:123-520.

[2] ² Monteiro FA, Weirauch C, Félix M, Lazoski C, Abad-Franch F. Evolution, systematics, and biogeography of the Triatominae, vectors of Chagas disease. Adv Parasitol. 2018;99:265-344. Available from: https://doi.org/10.1016/bs.apar.2017.12.002
» https://doi.org/10.1016/bs.apar.2017.12.002

[3] ³ Galvão C. Taxonomia dos Vetores da Doença de Chagas da Forma à Molécula, quase três séculos de história. In: Atualidades em Medicina Tropical no Brasil: Vetores (1º ed.) Oliveira J, Alevi KCC, Camargo LMA, Meneguetti DUO (eds). (2020) pp 9-37, Stricto Sensu Editora.

[4] ⁴ Justi AS, Galvão C. The Evolutionary Origin of Diversity in Chagas Disease Vectors. Trends Parasitol. 2017;33(1):42-52.

[5] ⁵ Alevi KCC, Oliveira J, Garcia ACC, Cristal DC, Delgado LMG, de Freitas Bittinelli I, et al.Triatoma rosaisp. nov. (Hemiptera, Triatominae): A New Species of Argentinian Chagas Disease Vector Described Based on Integrative Taxonomy. Insects. 2020;11(12):830. Available from: https://doi.org/10.3390/insects11120830
» https://doi.org/10.3390/insects11120830

[6] 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] ⁷ Rodrigues VLCC, Ferraz Filho AN, Silva EOR, Lima VLC. Prevalência, índices de infecção e hábitos alimentares de triatomíneos capturados em uma área de vigilância epidemiológica. Rev Soc Bras Med Trop. 1992;25(3):183-90.

[8] ⁸ Carcavallo RU, Curto de Casas SI, Galíndez Girón I, Jurberg J, Mena Segura C. Geographical and altitudinal dispersion of genera species of the tribes Alberproseniini, Bolboderini and Cavernicolini. Entomol. Vect. 1995;2(6):127-44.

[9] ⁹ Alencar J, Carcavallo RU, Jurberg J, Gil-Santana H. Registro de ocorrência do Microtriatoma borbai Lent & Wygodzinsky, 1979 no Estado do Rio de Janeiro, Brasil (Hemiptera, Reduviidae, Triatominae). Entomol Vect. 2000;7(4):445-7.

[10] ¹⁰ Gurgel-Gonçalves R, Cura C, Schijman AG, Cuba Cuba CA. Infestation of Mauritia flexuosa palms by triatomines (Hemiptera: Reduviidae), vectors of Trypanosoma cruzi and Trypanosoma rangeli in the Brazilian savanna. Acta Trop. 2012;121(2):105-11.

[11] ¹¹ Galvão C, Carcavallo R, Rocha DS, 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;202:1-36.

[12] ¹² Souza ES, Monte GLS, Paiva VF, Galvão C. Microtriatoma trinidadensis (Lent, 1951) (Hemiptera, Reduviidae, Triatominae): first record in the state of Amazonas, Brazil. Check List 2019; 15(5):905-909. Available from: https://doi.org/10.15560/15.5.905
» https://doi.org/10.15560/15.5.905

[13] ¹³ Galvão C. Vetores da doença de Chagas no Brasil. Curitiba: Sociedade Brasileira de Zoologia; 2014. 289 p.

[14] ¹⁴ Oliveira J, Rosa JA, Alevi KCC. Chagas disease vectors of Espírito Santo, Brazil: first report of Triatoma infestans (Klug, 1834) (Hemiptera, Triatominae) in Brazilian state and development of an identification key based on cytogenetic date. Am J Trop Med Hyg. 2021;104(2):653-5.

[15] ¹⁵ Leonardi GA, Carlos NA, Mazzafera P, Balbuena TS. Eucalyptus urograndis stem proteome is responsive to short-term cold stress. Genet Mol Biol. 2015;38(2):191-8. Available from: http://dx.doi.org/10.1590/S1415-475738220140235
» http://dx.doi.org/10.1590/S1415-475738220140235

[16] ¹⁶ Majer JD, Recher HF. Are Eucalypts Brazil’s Friend or Foe? An Entomological Viewpoint. An Soc Entomol Brasil 1999;28(2):185-200.

[17] ¹⁷ Rocha PLB, Viana BF, Cardoso MZ, Melo AMC, Costa MGC, Vasconcelos RN, et al. What is the value of eucalyptus monocultures for the biodiversity of the Atlantic forest? A multitaxa study in southern Bahia, Brazil. J For Res. 2013;24:263-72. Available from: https://doi.org/10.1007/s11676-012-0311-z
» https://doi.org/10.1007/s11676-012-0311-z

First report of Microtriatoma borbai Lent & Wygodzinsky, 1979 (Hemiptera, Reduviidae, Triatominae) in the state of Espírito Santo, Brazil: would M. borbai be living in eucalyptus crops?

Abstract

ACKNOWLEDGMENTS

REFERENCES

Publication Dates

History