Triatominae): First Report in the State of Acre, Brazil, and Updated

n Eratyrus mucronatus Triatominae): First report in the State of Acre, Brazil, and

istributio updated geographic distribution Stål, 1859 (Hemiptera: in South America Reduviidae: D

1 2 3

raphic Marcos Takashi Obara

g 4 5 6* eo , Acigelda da Silva Cardoso , Maria Carmelinda Gonçalves Pinto , Cláudio G n

o Rodrigues de Souza , Rafaella Albuquerque e Silva and Rodrigo Gurgel-Gonçalves

1 Universidade de Brasília, Faculdade de Ceilândia. QNN 14, Área Especial, Ceilândia Sul. CEP 72220-140. Brasília, DF, Brasil. otes Brasil.

N 2 Secretaria Municipal de Saúde, Área Técnica de Entomologia Municipal. Av. Ceará, Nº 3188, Bairro Abraão Alab. CEP 69960-160. Rio Branco, AC, AC, Brasil. 3 Secretaria de Estado de Saúde, Área Técnica de Doença de Chagas. Rua Benjamin Constant, 830- 1º Andar, Centro. CEP 69908-420. Rio Branco,

4 Secretaria de Estado de Saúde, Área Técnica de Entomologia Estadual. Av. Antônio da Rocha Viana, Nº 1584, Bairro Vila Ivonete. CEP: 69980-560. Rio Branco, AC, Brasil. 5 Ministério da Saúde, Secretaria de Vigilância em Saúde, Unidade Técnica de Vigilância das Doenças de Transmissão Vetorial. Setor Comercial Sul, Quadra 4, Bloco A, 2º andar, Edifício Principal. CEP 70304-000. Brasília, DF, Brasil. 6 Universidade de Brasília, [email protected] de Medicina, Área de Patologia, Laboratório de Parasitologia Médica e Biologia de Vetores. Campus Universitário Darcy Ribeiro, Asa Norte. CEP 70904-970. Brasília, DF, Brasil. * Corresponding author. E-mail: Abstract: A new occurrence record of Eratyrus mucronatus Branco, Acre, Brazil. The distribution of this triatomine species was updated and a potential geographic distribution map in South America was presented based on ecological niche modeling.(Hemiptera, Reduviidae, Triatominae) is reported from Rio

Currently, 145 species are recognized in the subfamily et al. 2011). Furthermore, detection of infected colonies Triatominae (Costa et al. 2006; Costa and Felix 2007; of E. mucronatus in houses and peridomiciles has been et al. et al et al. et al. 2013; Jurberg et al. 2013) of which Schofield and Galvão 2009; Frías-Lasserreet al 2010; Rosa et observed in Bolivia (Noireau et al. . 1995; 2008) Depickère indicating the al2012;. 2012). Gonçalves The genus Eratyrus potential2012), Colombia risk of transmission (Guhl 2007), of Peru T. cruzi (Torres to humans. and Cabrera Thus, 63two occurs species: in BrazilEratyrus (Gurgel-Gonçalves cuspidatus . 2012;Eratyrus Rosa it2010) is important and Venezuela to record (Rojas the locations where E. mucronatus mucronatus Stål, 1859 is represented by has been detected in domiciles, as well as update the Eratyrus mucronatus Stål, 1859 and geographic distribution of this species and predict areas Stål, 1859. of potential occurrence. In this study we registered a occurs in Bolivia, Colombia, new occurrence of E. mucronatus in Brazil, updated etEcuador, al Guatemala,In Brazil, Guyana, this species French was Guyana, registered Panama, in the its distribution and analyzed its potential geographic Peru, Suriname, Trinidad, Venezuela and Brazil (Carcavallo distribution in South America. . 1999). states of Amazonas, Tocantins, Maranhão, Matoet al . Grosso,2012). RondôniaTree holes, and palmPará, trees in humid and rocks forest are ecoregions known habitats (Abad- of Acre,In November Brazil. This 2011, state a triatomine is located in was northern detected Brazil, in a Franchof E. mucronatus and Monteiro 2007; Gurgel-Gonçalveset al house located in the Vila Irineu Serra, Rio Branco, state nature, nymphs can feed on the haemolymph of arachnids (Amblypygi) inside in hollow forests trees (Carcavallo and adults . are 1998b). usually In totalbordering area of the the states country. of The Amazonas climate andis hot Rondônia. and humid It with has associated with mammals, such as Coendou prehensilis, an area of 152,581.4 km² equivalent to about 2% of the Didelphis marsupialis et al average monthly temperatures ranging between 24°C and and bats (Carcavallo . 1998a; 27°C.The The residence annual wasrainfall located is 2.100 in a periurbanmm, with areaa dry with season the Gaunt and Miles 2000). during the months of June, July and August (IBGE 2012). transmissionIn the Amazon, of Trypanosoma invasion of cruzi houses to humans by triatomines, either by directapparently contact related or by tofood artificial contamination, light sources, especially should through favor presence of secondary forests, palmE. treesmucronatus and livestock. (Figure açai fruit (Coura et al et al et The insect was sent to the Laboratory of Entomology of al et al Rio Branco, Acre, and identified as According to Morocoima. 1999; Valente et al. (2010). 1999; E. mucronatus Nobrega 1). The identification was confirmed by the Laboratory . 2009; Pereira . 2009). of Medical the Ministry Entomology of Health. of General The specimen Coordination is deposited of Public at In Brazil, E. mucronatus has been registered in houses in Health Laboratories of the Health Surveillance Secretariat Manausspecimens (Castro are highly et al attracted to artificial light sources. the Laboratory of Entomology of the Municipal Health . 2010) and Rondônia (Meneguetti Secretariat of Rio Branco, Acre, Brazil. 851 Obara et al. | Eratyrus mucronatus distribution in South America

E. mucronatus were obtained et al. Dataet on al the occurrence of et al from etLent al. and(2007), Wygodzinsky Cortez et al(1979), Silveira et al. (1984),(2008), RebeloSerrano et . al (1998),. (2008), Soto Castro Vivas et al. (2001),(2010), Chávez Morocoima (2006), et Guhlal. (2010), Torres and Cabrera. (2007), (2010), Rojas Meneguetti et al. et al E. mucronatus

(2011), Depickère . (2012). Records of onin collections Triatomine of Taxonomy Rodolfo at Carcavallo the Oswaldo and Cruz Herman Institute, Lent at the National and International Reference LaboratoryE. mucronatus FIOCRUZ, were analyzed. The distributional data for available in other museums provided by the Global Biodiversity Information Facility - GBIF (http:// data.gbif.org), species link (http://splink.cria.org.br/) andE. mucronatusVertNet (http://vertnet.org/index.php), data on climate were obtainedwere also fromanalyzed. the In order to develop ecological niche models for

WorldClim project (http://www.worldclim.org). The environmental data used in the analyses cover South America, at a spatial resolution of 2.5’ (5 km). To avoid the confounding effects of calibrating models in an overly temperature,dimensional environmentalmean diurnal rangespace, (meanonly a ofsubset monthly of the (max 19 variables in the climatic data were chosen: annual mean Figure 1. Eratyrus mucronatus specimen (male) from municipality of month, minimum temperature of coldest month, annual Attalea temp - min temp), maximum temperature of warmest palm trees found in the peridomicile of the house where the specimen precipitation, precipitation of wettest month, and wasRio Branco, detected, state probably of Acre, the Brazil. natural A. ecotopedorsal view. of E. B.mucronatus lateral view.. C. et al. 2012).

precipitation of driest month (Gurgel-Gonçalves

Figure 2. Eratyrus mucronatus

Geographic distribution of in South America. The squares represent the known records for this species in Venezuela, darkColombia, red (high Ecuador, suitability). Peru, Bolivia and Brazil. The triangle represents the new record from the state of Acre, Brazil described in the present article. Areas identified as suitable based on climatic variables using ecological niche modeling (Maxent method) are shown in redscale: light red (low suitability) to

852 Obara et al. | Eratyrus mucronatus distribution in South America

E. mucronatus were assembled. These occurrences were referenced to In A. Martinez,(ed.) R.J. TonnAtlas of and Chagas E. Cortón. Disease 1998a. Vectors Feeding in Americas sources and Data on a total of 58 occurrences of patterns; p. 537-560 R.U. Carcavallo, I. Galíndez Girón, J, Jurberg and H. Lent. . Volume geographic coordinates with an uncertainty of ≤ 5 km and II. Rio de Janeiro: Fiocruz. In Carcavallo, R.U., M. Rodríguez, R. Salvatella, S.I. Curto de Casas, I. SherlockAtlas of Occurrenceprecision of 0.01°. data were The records separated were into georeferenced two sets: one based for Chagasand C. Galvão. Disease 1998b. Vectors Habitats in Americas and related fauna; p. 561-619 R.U. on data found at http://www.fallingrain.com/world. Carcavallo, I. Galíndez Girón, J. Jurberg and H. Lent (ed.). , Volume II. Rio de Janeiro: Fiocruz. Carcavallo, R.U., S.I. Curto de Casas, I. Sherlock, I. Galíndez Girón, ofmodel E. mucronatus calibration (75% of points) and the other for model J. Jurberg,In C. Galvão, C.A. Mena Segura and F. Noireau. 1999. evaluationet (25%al. 2006), of points). applying Maps the ofdefault potential parameters distribution with AtlasGeographical of Chagas distribution disease vectors and in alti-latitudinalAmericas dispersion; p. 747- were produced using Maxent version 3.2.1 Fiocruz.792 R.U. Carcavallo, I. Galíndez Girón, J, Jurberg and H. Lent. (ed.) 10 replicates using Bootstrap replication method. Then, , Volume III. Rio de Janeiro: (Phillips Castro,light M.C.M., sources T.V. in Barrett,the canopy W.S. of Santos, primary F. AmazonAbad-Franch rainforest. and J.A. Memórias Rafael. the averaged model was imported into ARC VIEW (version do2010. Instituto Attraction Oswaldo of Chagas Cruz disease vectors (Triatominae) to artificial 3.2) to create and edit the distribution map. Predicted 105: 1061-1064. Anales areas in semi-arid caatinga ecoregion were eliminated in Chávez,de la J. Facultad 2006. Contribución de Medicina 67(1): al estudio de los triatominos del Perú: the final edited map. Distribución geográfica, nomenclatura y notas taxonómicas. 65-76. The quality of the models was evaluated using the ROC Cortez, M.R., M. Avalos, V. Rocha and D. Gorla. 2007. Distribuición (receiver operating characteristic) curve,et alwhich. 2006). correlates Model biogeograficaIn de los triatominosTriatominos en Bolivia: de Bolivia discriminacion y la enfermedad de la accuracythe sensitivity was also and assessed specificity by examining of model the predictionsproportion distribuiciónde Chagas de las espécies en relación a variables ambientales; p. 67-137de Chagas. : Cortez, M.R. (ed.) ofacross test multiplepoints falling thresholds into regions (Phillips of predicted presence Costa, J. and M.. La Felix. Paz: 2007. Ministerio Triatoma de Salud juazeirensis y Deportes. Programa Nacional (Anderson et al. 2002). Using Maxent’s internal Jackknife Memórias do Instituto Oswaldo Cruz sp. nov. from the state of Bahia, northeastern Brazil (Hemiptera: Reduviidae: Triatominae).Triatoma melanica 102: 87-90. test,The the variables updated that geographic most influence distribution the distribution map of ofE. Costa,Triatominae). J., A.M. Argolo Zootaxa and M. Felix. 2006. Redescription of triatomine species (Figure were 2) presents identified. the known records in South Neiva & Lent, 1941, new status (Hemiptera: Reduviidae: mucronatus disease: from bush to husts1385: and 47-52. houses. Is it the case of the Brazilian America and the new record of the state of Acre, Brazil. Coura,Amazon? J.R., A.C.V. Memórias Junqueira, do Instituto M.N. Oswaldo Bóia, O. Cruz Fernandes. 1999. Chagas The ecological niche model indicates that E. mucronatus 2012. After should occur widely in Amazon. The species also showed 94 (1): 379-384.Eratyrus Depickère,mucronatus S., P. Durán, R. López, E. MartínezActa and Tropica T. Chávez. a potential geographic distribution in drier ecoregions five years of chemical control: colonies of the triatomine bordering distribution are still present of Mepraia in Bolivia. spinolai 123: 234-238.Mepraia Frías-Lasserre,gajardoi D. 2010. A new species and karyotype variation in the and its parapatric model of speciation. Neotropical (Porter) Entomology and outside the Amazon region, in northern Venezuela and Frías et al (Hemiptera: Reduviidae: Triatominae) in Chile Colombia, such as Maracaibo dry forests, Lara-Falcón 39: dry forests, Paraguana xeric scrub and La Costa xeric bugs572-583. (Triatominae) and their associated trypanosomes. Memórias do Gaunt,Instituto M. and Oswaldo M. Miles. Cruz 2000. The ecotopes and evolution of triatomine ecologicalshrublands. conditions All of the for models the occurrence derived fromof E. mucronatus the analysis. Allperformed test points well fell (AUC in the> 0.92), area summarizingof predicted presencethe necessary of E. 95: 557-565.Triatoma jatai . The Jackknife tests showed that precipitation Gonçalves, T.C.M., S.C. Neves-Neves, J.R.S. Mallet, A.L. Carbajal-de-la-Memórias mucronatus doFuente Instituto and OswaldoC.M. Lopes. Cruz 2013. sp. nov. in the state of Tocantins, Brazil (Hemiptera: Reduviidae: Triatominae).Memórias do Instituto the models. Oswaldo Cruz 108: 429-437. of the wettest month was the variable that best explained Guhl, F. 2007. Chagas disease in Anden countries. The importance of E. mucronatus 102(1): 29-37. of T. cruzi Guhl, F., G. Aguilera, N. Pinto and D. Vergara. Biomédica 2007. Actualización de la et al. 2008; Torres as anda potential Cabrera vector 2010; distribución geográfica y ecoepidemiología de la fauna de triatominos2012. to humans. 2012). has The been new highlighted record of in Bolivia, Peru in (Reduviidae: Triatominae) en Colombia. 27: 143-162. et al E. mucronatus Gurgel-Gonçalves,ecological niche R., modeling. C. Galvão, Journal J. Costaof Tropical and Medicine A.T Peterson. and Venezuela (Rojas Geographic distribution of Chagas disease vectors in BrazilGeografia based on e Depickèrepotential of this species. Ecological niche modeling predicts demografia do Estado do Acre. 2012: 1-15. domicile in Brazil is further evidence of the synanthropic IGBE 2012. Instituto Brasileiro de Geografia e Estatística. that E. mucronatus is widespread in Amazon, suggesting Database accessible at http://www. andibge.gov.br/. F.F.F. Moreira. Captured 2013. on Triatoma 29 October pintodiasi 2012. Jurberg, J., V. Cunha, S. Cailleaux, R. Raigorodschi, M.S. Lima,Revista D.S. Rocha Pan- that the invasion of this species in households must be Amazônica de Saúde sp. nov. do subcomplexo T. rubrovaria (Hemiptera, Reduviidae, Triatominae). veryAcknowledgments common in humid: ecoregions of South America. 4: 43-56. Lent,Chagas’disease. H and P. Wygodzinsky. Bulletin of the 1979. American Revision Museum on of the Natural Triatominae History The authors are grateful to Gilberto Gil da Silva (Hemiptera, Reduviidae) and their significance as vectors of Serato and Janis Lunier de Souza, entomology technicians from the Municipal Health of Rio Branco, for their support in identifying the report163: 123-520. Eratyrus mucronatus species. We also thank Patricia Gurgel Gonçalves for reviewing the Meneguetti, D.U.O., O. Trevisan, R.M. Rosa and L.M. Camargo.Revista da 2011. Sociedade First LiteratureEnglish version Cited of the manuscript. Brasileira de Medicina Tropical, Stal, 1859, (Hemiptera, Reduviidae, Triatominae), in the State of Rondonia, Brazil. Eratyrus mucronatus 44: 511-512. Abad-Franch, F. and F.A. Monteiro. 2007. Biogeography and Memóriasevolution doof Morocoima, A., J. Chique, L. Herrera and S.U. Morales. 2010.Boletín de AmazonianInstituto Oswaldo triatomines Cruz (Heteroptera: Reduviidae): implications for Marariologia (Stal,y Salud 1859) Ambiental (Hemiptera, 2: Reduviidae, Triatominae): Chagas disease surveillance in humid forest ecoregions. primer registro para el estado Anzoátegui (Venezuela). distributions of spiny pocket102: 57-69. mice in South America: insights from 307-310. Anderson, R.P., M. Gómez-LaverdeGlobal Ecology and and A.T. Biogeography Peterson. 2002. Geographical Nóbrega, A.A., M.H, Garcia, E. Tatto,Emerging M.T InfectiousObara, E. Costa,Diseases J. Sobel and W.N. Araujo. 2009. Oral transmission of Chagas Disease by consumption predictive models. 11: 131-141. of açai Palm Fruit, Brasil. 15: 653-655. Carcavallo, R.U., D.S. Rocha, I. Galíndez Girón, I. Sherlock, C. Galvão, Noireau, F., M.F. Bosseno, R. Carrasco, J. Telleria, F. Vargas, C. 853 Obara et al. | Eratyrus mucronatus distribution in South America

groups within the Triatominae. Acta Tropica andCamacho, possible N. Yaksi infection and with S.F. Breniere.Trypanosoma 1995. cruzi Sylvatic (Kinetoplastida: triatomines Schofield, C.J. and C. Galvão. 2009. Classification, evolution, and species Trypanosomastidae).(Hemiptera: Reduviidae) Journal in of Bolivia: Medical trends Entomology towards domesticity 110: 88-100. Silveira,Revista A.C., Brasileira V.R. Feitosa de and Malariologia R. Borges. e1984. Doenças Distribuição Tropicais de triatomíneos 32: 594-598.Journal capturados no ambiente domiciliar, no períodoSeroepidemiology de 1975/83, Brasil. of Pereira,Food K.S., Protection F.L. Schmidt, A.M.A. Guaraldo, R.M.B. Franco, V.L. Dias and Chagas disease in two rural populations in the municipality 39: 15-312. of Costa L.A.C. Passos. 2009. Chagas disease as a foodborne illness. Serrano, O., F. Mendoza, B. Suárez and A. Soto. 2008.Biomedica modeling of species 72: 441-446. geographic distributions. Ecological Modelling Phillips, S.J., R.P. Anderson and R.E. Schapire. 2006. Maximum entropy de Oro,Eratyrus at Aragua mucronatus State, northern Venezuela. 28: 108-15. Soto Vivas, A., H. Barazarte and D.M. Fernández.Entomotropica 2001. Primer registro 190: 231-259. Stål, 1959 (Hemiptera: Reduviidae) en el Rebelo,Brasil. J.M.M., Cadernos V.L.L. de Saúde Barros Pública and W.A. Mendes. 1998. Espécies de ambiente domiciliario en Venezuela. 16: 215-217. Triatominae (Hemiptera: Reduviidae) do Estado do Maranhão, Torres, D.B. and R. Cabrera.Revista 2010. Geographical do Instituto de distribution Medicina Tropical and intra- de 14: 187-192. Sãodomiciliary Paulo capture of sylvatic triatomines in La Convención Rojas, M.E., P. Várquez, M.F. Villarreal, C. Velandia, L. Vergara, Y.H. Province, Cusco, Peru. Considerations on the Móran-Borges, J. Ontiveros, M.Y. Calderón, M.A. Chiurillo-Siervo, epidemiology 52: 157-160. and transmission of Chagas disease in the Brazilian C.C. Rodríguez-Bonfate, E. Aldana, J.L. ConcepciónTriatoma and R.A. maculata Bonfate- Valente,Amazon. S.A.S., Memórias V.C. Valente do Instituto and H.F. Oswaldo Neto. 1999. Cruz Cabarcas. 2008. Estudio soroepidemiológico y entomológicoCadernos sobre dela Saúdeenfermedad Pública de Chagas en un área infestada por 94 (Suppl 1): 395-398. (Erichon 1848) en el centro-occidente de Venezuela. 24: 2323-2333. Rosa,and J.A., C.E. C.S. Almeida. Rocha, S. Gardim, M.C. Pinto,Rhodnius V.J. Mendonça, montenegrensis J.C.R.F. Filho, sp.n. : February 2013 E.O.C. Carvalho, L.M.A. Camargo, J. Oliveira, J.D. Nascimento, M. Cilense Received: December: September 2012 2013 Brazil. Zootaxa 2012. Description of Accepted (Hemiptera: Reduviidae: Triatominae) from the state of Rondônia, Published online 3478: 62-76. Editorial responsibility: Lívia Aguiar Coelho

854