Occurrence of Domestic and Intrusive Triatomines

Acta Tropica 196 (2019) 37–41

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Acta Tropica

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Occurrence of domestic and intrusive triatomines (Hemiptera: Reduviidae) in sylvatic habitats of the temperate Monte Desert ecoregion of Argentina T ⁎ Ana Laura Carbajal-de-la-Fuentea,b, , María del Pilar Fernándeza,b,c, Romina Valeria Piccinalia,b, Lucía Inés Rodríguez-Planesa,b,d, Rosemere Duartee, Ricardo Esteban Gürtlera,b a Universidad de Buenos Aires, Facultad de Ciencias Exactas y Naturales, Departamento de Ecología, Genética y Evolución, Laboratorio de Eco-Epidemiología, Ciudad Autónoma de Buenos Aires, Buenos Aires, Argentina b CONICET - Universidad de Buenos Aires, Instituto de Ecología, Genética y Evolución de Buenos Aires (IEGEBA), Ciudad Autónoma de Buenos Aires, Buenos Aires, Argentina c Earth Institute, Columbia University, New York, NY, 10025, United States d Instituto de Ciencias Polares, Ambiente y Recursos Naturales (ICPA), Universidad Nacional de Tierra del Fuego (UNTDF), Usuhaia, Argentina e Laboratório de Imunodiagnóstico/Departamento de Ciências Biológicas, Escola Nacional de Saúde Pública, Fundação Oswaldo Cruz, Rio de Janeiro, Brasil

ARTICLE INFO ABSTRACT

Keywords: The eco-epidemiology of Triatominae and Trypanosoma cruzi transmission has been little studied in the Sylvatic triatomines Argentinean Monte ecoregion. Herein, we provide a comprehensive description of domestic and intrusive tria- Monte ecoregion tomines to evaluate the risk of reinfestation of rural dwellings. Triatoma infestans, T. patagonica, T. garciabesi and Argentina T. eratyrusiformis were collected by active searches or light traps. None were infected with T. cruzi. One T. infestans male was collected at 1.3 km from the nearest infested house. The ﬁnding of intrusive and domestic triatomines in sylvatic foci emphasizes the need of implementing an eﬀective vector surveillance system.

1. Introduction human-modified habitats, although it has also been reported in sylvatic areas from Argentina, Bolivia, Chile and Paraguay (Waleckx et al., Chagas disease, caused by Trypanosoma cruzi, is mostly transmitted 2015). The triatomines dispersion from sylvatic to domestic habitats by blood-sucking bugs of the Triatominae subfamily (Pan American was one of the causes related to the vector control failures and re- Health Organization, 2018). Triatomine species have been traditionally infestation of human dwellings after spraying with insecticides. Several classified according to their adaptation to human dwellings into four studies have determined the occurrence of sylvatic T. infestans or other categories: sylvatic, intrusive, domiciliary and domestic (Waleckx et al., intrusive triatomines in sylvatic habitats in Argentina (e.g., Ceballos 2015). Sylvatic species are restricted to sylvatic habitats whereas in- et al., 2009; Abrahan et al., 2016; Cavallo et al., 2016), with a total of trusive species are mostly sylvatic, with occasional reports of adult 16 triatomine species with different degrees of adaptation to human specimens invading human dwellings but leaving no evidence of colo- dwellings (Ceccarelli et al., 2018). Seven triatomine species occur in nization (presence of eggs, nymphs or exuviae). The occurrence of in- west-central Argentina: T. infestans (domestic); T. garciabesi, T. gua- trusive species inside human dwellings is probably the result of active sayana, T. platensis, T. patagonica and T. eratyrusiformis (intrusive, all dispersal (attracted by artificial lights) or passive transport (for ex- occurring in peridomestic and sylvatic habitats) and Panstrongylus ample, firewood). Domiciliary species are characterized by the presence guentheri (sylvatic) (Carcavallo et al., 1998). of adults, nymphs, eggs and exuviae (i.e., the complete life cycle of the The eco-epidemiology of triatomine bugs and T. cruzi transmission insect) inside the domicile or in peridomestic structures, but coloniza- has been little studied, particularly beyond the SW extreme of the Gran tion may be transient. Domestic species include domiciliary species but Chaco and its transition into the Monte ecoregion in Argentina. Lavalle the former are widely extended geographically. Domestic species may Department, located in northern Mendoza province, is an endemic area also display sylvatic populations or foci that may eventually invade for Chagas disease with high house infestation rates and abundance of human habitations (Noireau and Dujardin, 2010; Waleckx et al., 2015). T. infestans, and high T. cruzi infection prevalence in domestic and Triatoma infestans, a domestic species and the main vector of T. cruzi peridomestic habitats (Carbajal-de-la-Fuente et al., 2017a,b). As part of in South America, is characterized by a high level of adaptation to a broader study conducted in the area, here we describe the occurrence

⁎ Corresponding author at: Intendente Güiraldes 2160, Ciudad Universitaria, C1428EGA, Ciudad Autónoma de Buenos Aires, Argentina. E-mail address: [email protected] (A.L. Carbajal-de-la-Fuente). https://doi.org/10.1016/j.actatropica.2019.04.028 Received 25 February 2019; Received in revised form 26 April 2019; Accepted 26 April 2019 Available online 28 April 2019 0001-706X/ © 2019 Elsevier B.V. All rights reserved. A.L. Carbajal-de-la-Fuente, et al. Acta Tropica 196 (2019) 37–41

Fig. 1. a) Ecoregions of western Argentina and the location of the study area in the Monte ecoregion (black circle), in Mendoza province. b) Location of sylvatic sampling sites in 2015 and neighboring houses inspected in 2013–2014. of sylvatic and intrusive triatomines in sylvatic habitats of the Monte daylight and the lights were turned on between 20 h (30 min before ecoregion, including T. infestans. This information is key to the eva- sunset) and 0 h. On average, the sampling sites (n = 16) were located at luation of the risk of house reinfestation. We report the occurrence and 10.5 km (range 0.5–12.1 km) from the nearest inhabited house. In ad- abundance of sylvatic foci for five triatomine species, their infection dition, the light trap was placed in a sylvatic area near a house where with T. cruzi, host-feeding patterns and nutritional status. the inhabitants reported the presence of triatomines inside the house in 2015. Third- to fifth-instar nymphs and adults of T. infestans were de- 2. Material and methods tected in the bedroom. The house was sprayed with 2.5% suspension concentrate deltamethrin (K-Othrina, Bayer, Munro, Argentina) by 2.1. Study area vector control personnel following standard procedures. The collected bugs were stored in plastic bags labeled with the Fieldwork was conducted in sylvatic areas of Telteca Natural and collection site and transported to the laboratory. Triatomines were Cultural Reserve (32°22′55.3″S, 68°03′17.7″W), Lavalle Department in morphologically identified following Lent and Wygodzinsky (1979) and Mendoza Province, Argentina (Fig. 1a). During 2013–2014 we assessed counted according to species, stage and sex. the local domiciliary and peridomiciliary infestation with T. infestans in When the morphological identification of adults and nymphs (third 76 houses at 0, 1, 4 and 12 months postintervention with pyrethroid to fifth instars only) was uncertain, DNA was extracted from two legs insecticide (Carbajal-de-la-Fuente et al., 2017a,b). The area comprises following Piccinali et al. (2009), and a fragment of the mitochondrial 38,500 ha of NNW–SSE oriented dunes separated by discontinuous gene COI was PCR-amplified using primers described in Piccinali et al. valleys. Dunes have a low vegetation cover dominated by shrubs co- (2009) and/or Calleros et al. (2010). Both strands of the fragments were existing with woodlands of Prosopis flexuosa. The area preserves most of Sanger sequenced in Macrogen Inc. (Seoul, Korea) and aligned manu- its original fauna. The climate is semiarid with a mean temperature of ally or using MEGA 5.1 software (Tamura et al., 2011). Sequences were 18.5 °C, a mean annual precipitation of 150 mm, and an elevation of considered true COI open reading frames because no stop codons or 500–550 masl (http://bosquestelteca.wixsite.com/telteca/info). gaps were found. The triatomine sequences (645–1084 bp fragments depending on the success of amplifications) were used as queries to find 2.2. Vector survey highly similar COI sequences in GenBank with BLAST (Altschul et al., 1990) under the nucleotide blast option (blastn) and the megablast Searches for triatomines were conducted at selected P. flexuosa algorithm. New sequences are available at GenBank under accession patches, which represent suitable habitats for triatomines in the area, numbers MK239065-MK239072. by a team of two people during 14 days in March (summer) and days in November (spring) of 2015 (Fig. 1b). The sampled area approximately 2.3. Bloodmeal sources, nutritional status and diagnosis of T. cruzi covered 11 km2. Two triatomine collection methods were used: active searches and light traps. Active searches consisted of meticulous habitat All collected third- to fifth-instar nymphs and adults were dissected dissection of potential sites where triatomines may take refuge, in- and midgut bloodmeal contents were extracted into a previously cluding branches and trunks lying on the ground and the bark of P. weighted labeled vial. The vial was weighted again with the midgut flexuosa trees (n = 84 habitats). These searches were conducted by two content, and the size of the bloodmeal (i.e., weight in mg) was esti- persons during 8 h a day between 8 a.m. and 4 p.m., with a total search mated as a proxy of its nutritional status (Gürtler et al., 2014). Blood effort of 112 person-h. meals were tested with a direct ELISA assay against human, dog, cat, One light trap was deployed one night in each of the 16 different chicken, pig, goat, rabbit, horse, murid rodent (rat or mouse) and Ca- selected sites in the sylvatic area, for a total search effort of 16 trap- viidae rodent (cavies) antisera having high sensitivity and specificity as nights. The trap consisted of two pieces of white cloth (3 m × 2 m) il- described (Gürtler et al., 2014). In addition, we tested the bloodmeal luminated by a lighting led device (Sica, Argentina) set 1 m away from content against turtle, opossum (Didelphis albiventris) and armadillo the cloth and 1 m above the ground. The whole device was mounted in (Dasypus novemcinctus) antisera with an indirect ELISA essay (Sandoval

38 A.L. Carbajal-de-la-Fuente, et al. Acta Tropica 196 (2019) 37–41 et al., 2004). Infection with T. cruzi was identified by PCR amplification quality of the extracted DNA (Table 1). To further confirm these results, of a 330-basepair (bp) fragment from the kDNA minicircles of T. cruzi and because some fragments have low overlap with the sequences (kDNA-PCR) using the primers and cycling conditions described in available in Genbank, the sequences were compared to those from Burgos et al. (2005). Positive (i.e., contents from the rectal ampoule of a morphologically identified adults of T. patagonica and T. garciabesi from bug infected with T. cruzi as determined by optic microscopy) and ne- Telteca Reserve and T. patagonica from San Luis, a neighboring pro- gative controls (i.e., sterile water or contents of the rectal ampoule of a vince. A 99.9–100% of identity between sequences was found. bug that only fed on pigeons) were included in each round of DNA During the spring survey the light traps attracted both sexes of T. extraction as described in Carbajal-de-la-Fuente et al. (2017a). eratyrusiformis (n = 13), T. garciabesi (n = 8) and T. patagonica (n = 8). During the summer the light traps attracted one female of T. patagonica 2.4. Data analysis and one male of T. infestans. The male T. infestans was collected at 1.3 km from the nearest house (Fig. 1b), whose domicile was heavily The prevalence of infested sites (traps) was calculated as the pro- infested with T. infestans nymphs and adults (n = 15). Nearly half (9/ portion of all traps inspected where at least one triatomine (nymph or 16) of all light traps set up in the summer and spring captured adult adult) was found. We used logistic regression to assess the effect of triatomines; 6 (66%) of the 9 positive traps attracted two or three season (spring vs. summer) on the proportion of infested sites. To de- species at the same time. Although a higher proportion of light traps termine the effect of season on the number of triatomines collected per collected triatomines in spring than in summer (77.7% [7/9] vs 28.6% ff fi trap, we used a Poisson or negative binomial regression based on the [2/7]), these di erences were marginally signi cant (ORsping = 8.7, – significance of the overdispersion parameter (α) using a likelihood ratio CI = 0.9 84.8, p = 0.06). The total number of triatomines collected per fi – test (H0: α = 0). We evaluated the effect of season for the active search trap was signi cantly higher in the spring (median, 4; IQR, 2 5) com- – and light traps separately because these sampling methods target dif- pared to summer (median, 0; IQR, 0 1), (Poisson regression, ORsping – ferent stages and are subjected to different limitations. We compared IRR = 11.2, CI = 2.7 47.2, p = 0.001). the nutritional status between species and stages using a non-para- The active searches were carried out in 84 sites (56 in the summer metric test (Kruskal-Wallis) because the size of bloodmeal contents did and 28 in spring); 15.5% (13/84) of them yielded 27 nymphs of all fi not fit a normal distribution. Medians were preferred over means when stages, including the unidenti ed nymphs of Triatominae (n = 22), fl numeric variables deviated significantly from a normal distribution, which were found in dry trunks and under the bark of P. exuosa trees. and we reported the interquartile range (IQR) as a measure of varia- Only one adult female of T. patagonica was collected by active search. bility. The proportion of sites positive for triatomines was not statistically different between seasons (12.5% [7/56] vs. 21.4% [6/28]; Logistic regression, OR = 1.9, CI = 0.6–6.4, p = 0.3) (Fig. 2). The median 3. Results sping number of nymphs collected in the infested sites during both seasons was 1 nymph per site (spring: 1, IQR = 1–2; summer: 1, IQR = 1–4) 3.1. Triatomine collection and identification (binomial regression, IRR = 1.7, CI = 0.8–3.6, p = 0.1). Active searches and light traps in sylvatic environment revealed the 3.2. Host-feeding sources and nutritional status occurrence of nymphs (n = 27) and adults of both sexes (n = 32), including T. infestans, T. patagonica, T. garciabesi and T. eratyrusiformis At least one bloodmeal source was identified in three (7.1%) tria- (Table 1). Two T. patagonica females were identified by sequencing the tomines collected in sylvatic habitat. Horse was the only bloodmeal COI gene (99% of similarity with Genebank accession numbers source identified in a T. eratyrusiformis male and in a T. patagonica male. KU842349 and KU842348). DNA sequencing also identified 2 nymphs A blood meal on cavies was identified in a fifth-instar nymph of T. of T. eratyrusiformis (99% identity with sequence GQ336898) and 3 of eratyrusiformis.Differences in the nutritional status among species were T. garciabesi (99% similitude with sequence EF451041), while the re- not significant (Kruskal-Wallis, p = 0.1). However, nymphs and adults maining (n = 7) could not be amplified due to problems with the of T. eratyrusiformis showed greater bloodmeal contents than insects from other species. Adults of T. eratyrusiformis had lower bloodmeal Table 1 contents (median: 8.3 mg, IQR: 3.8–10.3 mg) than nymphs (median: Distribution of triatomines by species, stage and collection method in wild – ff habitats of Telteca Natural and Cultural Reserve, Mendoza, March (summer) 30.1 mg, IQR: 2.3 57.9 mg), but the di erences were not statistically fi and November (spring) 2015. signi cant (Kruskal-Wallis, p = 0.9). The T. infestans collected at the house nearest to the light trap had blood-fed on dog (33%), rodent Species Stage Number of triatomines (13%) and human (13%). Adults of T. infestans collected in nearby Light trap Active Summer Spring Total domestic sites had larger bloodmeal contents (median: 37.65 mg, IQR: search 16.60–43.20 mg) than sylvatic triatomines collected here.

T. infestans Male 1 0 1 0 1 3.3. Infection with T. cruzi T. eratyrusiformis N5 – 2* 202 Male 12 0 0 12 12 Female 1 0 0 1 1 Thirty percent (13/44) of the triatomines collected by active sear- T. patagonica Male 7 0 0 7 7 ches (including 12 nymphs and 1 adult), all adults collected by light * * Female 1 1 22 traps (n = 31), and nymphs and adults of T. infestans collected at the T. garciabesi N3 0 2* 022 house (n = 15), were examined for T. cruzi infection by kDNA-PCR. N5 0 1* 101 Male 7 0 1 6 7 None of the specimens was infected with T. cruzi. Female 2 0 0 2 2 Triatoma sp. Nymphs 0 22a 12 10 22 4. Discussion Total 31 28 17 42 59

N1, N2, N3, N4, N5: first-, second-, third-, fourth- and fifth-instar nymphs, re- Our results document the occurrence of T. infestans, T. patagonica, T. spectively. garciabesi and T. eratyrusiformis in sylvatic areas of the Monte ecoregion. * Molecular identification by COI gene. Nymphs of T. garciabesi, T. eratyrusiformis and Triatoma sp. and two a Unidentified by morphological and/or molecular methods: 10 N1, 4 N2, 3 adults of T. infestans and T. garciabesi were collected in summer, while N3, 1 N4, and 4 N5. 30 adults of T. patagonica, T. garciabesi and T. eratyrusiformis —mainly

39 A.L. Carbajal-de-la-Fuente, et al. Acta Tropica 196 (2019) 37–41

Fig. 2. Number of triatomines captured in March (summer) and November (spring) of 2015 (bars), and proportion of infested sites or positive light traps by season and collection method (dots) in sylvatic areas of Telteca Natural and Cultural Reserve, Mendoza province, Argentina. The error bars indicate the 95% conﬁdence intervals for the percentage of infested sites and the numbers above the bars indicate the number of positive sites per season and method.

males— were collected mostly in the spring. Adults of T. eratyrusiformis elsewhere (Noireau and Dujardin, 2001). In our study area, light traps were the most abundant triatomines collected by light traps, followed attracted adults only, mainly males. The reason why males of several by T. patagonica and T. garciabesi. The greatest number of nymphs was triatomine species fly more often than females to light traps and houses collected by active manual searches in the bark of P. flexuosa trees, remains poorly understood. Some laboratory and field studies suggest which harbored T. patagonica, T. garciabesi and T. eratyrusiformis. Other that female triatomines are equally or more likely to start dispersive shrubs typical of this region were not a suitable refuge for triatomines. flights than males (Gurevitz et al., 2006; Minoli and Lazzari, 2006), but Prosopis flexuosa woodlands in the central Monte have a relatively high males are usually caught more often at light traps (Vazquez-Prokopec productivity, provide valuable resources (i.e. wood, forage, fruit) and et al., 2006; Carbajal-de-la-Fuente et al., 2007). generate microhabitats with particular edaphic and climatic conditions Our results indicate that the four triatomine species captured by for wildlife (Flores et al., 2004). Our study did not detect the occurrence light traps had little bloodmeal contents, which could have stimulated of triatomines infected with T. cruzi, and although the sample size is them to initiate flight. Nutritional status influences triatomine flight rather small, the sparse bloodmeal contents found in most of the bugs activity (Abrahan et al., 2016). Horses and cavies were the only compared to domestic T. infestans collected in human habitations bloodmeal sources identified in a few T. eratyrusiformis and T. patago- (Cecere et al., 2015), including those collected in domestic triatomines nica because of their low nutritional status. Cavies play a significant collected in the same area, suggests nutritional distress. eco-epidemiological role in peridomestic cycles in the Yungas ecoregion Triatoma infestans has not been reported in sylvatic areas of the (northwestern Argentina) because T. eratyrusiformis feeds on them and Monte since 1936 (Mazza et al., 1936) although intrusive species such are frequently infected with T. cruzi (Cecere et al., 2015). Our data are as T. patagonica, T. garciabesi and T. eratyrusiformis have been described insufficient to test whether the same pattern occurs in Mendoza. In this for our study area (Carcavallo et al., 1998). Local people may confound area, horses are used for transportation by rural villagers, who usually these species with T. infestans when triatomines invade domestic areas travel and spend the night in sylvatic environments. We cannot exclude (Carbajal-de-la-Fuente, unpublished data). They pose a very low that the horse blood meals registered in this study are related to the transmission risk, confirmed by the absence of T. cruzi-infected triato- intrusion of humans and horses in sylvatic habitats. mines. On the contrary, T. infestans bugs collected in local domiciles Our study had some limitations. The biophysical complexity of during 2013–2014 were found infected with T. cruzi (Carbajal-de-la- sylvatic environments may also reduce the detectability of triatomines Fuente et al., 2017a). by active searches and light traps. Detection failure becomes a key step Since sylvatic triatomines are not targeted for chemical control, in the estimation of eco-epidemiological parameters (Abad-Franch house invasion and reinfestation can persist as long as sylvatic vector et al., 2010). The low number of triatomines collected did not allow us populations occur near dwellings. However, the detection of sylvatic to perform more robust analyses of the relationship between T. cruzi triatomines in their natural habitats usually range from fairly to ex- infection and nutritional variables. Blood-feeding patterns determined tremely difficult. The only T. infestans found in this study was collected by direct ELISA may detect blood meals that occurred within the pre- in a light trap located 1.3 km from the nearest house, whose domicile vious two or three months depending on site-specific temperatures and was concurrently colonized with T. infestans (i.e., in 2015), but not in other factors. Therefore, bloodmeal results correspond to a rather un- 2013 (pre-spraying) or 2014 (post-spraying). Flight dispersal of T. in- defined time window. festans towards the sylvatic environment appears to be the most plau- Although in this study triatomines infected with T. cruzi were not sible explanation of the origin of this bug since the dwelling was within detected and searches for sylvatic triatomines were mostly undertaken the flight range of T. infestans (Schofield et al., 1992). Sylvatic habitats at > 10 km from the nearby houses, the finding of sylvatic foci of po- may provide a transient or permanent refuge after control interventions tentially intrusive vectors of T. cruzi emphasizes the importance of an with insecticides and function as sources for house reinfestation effective vector surveillance system. The occurrence of sylvatic foci of (Ceballos et al., 2011; Rojas de Arias et al., 2017). In the Argentine T. infestans may pose additional threats to ongoing vector elimination Chaco region, a sylvatic colony of T. infestans was detected 1.1 km away efforts. In the light of continuing house reinfestation events, triatomine from the nearest infested house in an isolated habitat with no signs of surveys of sylvatic habitats adjacent to infested villages should be a part current or past human use over the previous two decades (Ceballos of a locally adapted vector surveillance and control strategy. et al., 2011). Here, we report a low number of triatomines collected by light 5. Conclusions traps, unlike in a similar landscape in the High Monte where a large number of flight-dispersing adults of T. infestans and other species were In light of the degree of adaptation to human dwellings proposed by attracted to public lights (Di Iorio and Gürtler, 2017). The capture Noireau and Dujardin (2010), we report the occurrence of domestic (T. success was also lower than those of T. sordida and T. guasayana infestans), intrusive (T. patagonica, T. garciabesi) and sylvatic (T.

40 A.L. Carbajal-de-la-Fuente, et al. Acta Tropica 196 (2019) 37–41 eratyrusiformis) triatomine species collected by active searches or light Cavallo, M.J., Amelotti, I., Gorla, D.E., 2016. Invasion of rural houses by wild traps in a sylvatic environment of the Monte ecoregion. None were Triatominae in the arid Chaco. J. Vector Ecol. 41, 97–102. https://doi.org/10.1111/ jvec.12199. infected with T. cruzi. One T. infestans male was collected at 1.3 km Ceballos, L., Piccinali, R., Berkunsky, I., Kitron, U., Gürtler, R., 2009. First finding of from the nearest infested house. The finding of intrusive and domestic melanic sylvatic Triatoma infestans (Hemiptera: Reduviidae) colonies in the triatomines in sylvatic foci emphasizes the need of implementing an Argentine Chaco. J. Med. Entomol. 46, 1195–1202. https://doi.org/10.1603/033. ff 046.0530. e ective vector surveillance system. Ceballos, L.A., Piccinali, R.V., Marcet, P.L., Vazquez-Prokopec, G.M., Cardinal, M.V., Schachter-Broide, J., Dujardin, J.P., Dotson, E.M., Kitron, U., Gürtler, R.E., 2011. Authors’ contribution Hidden sylvatic foci of the main vector of chagas disease Triatoma infestans: threats to the vector elimination Campaign? PLoS Negl. Trop. Dis. 5. https://doi.org/10. 1371/journal.pntd.0001365. Conceived and designed the study ALCF, MPF and REG. Performed Ceccarelli, S., Balsalobre, A., Medone, P., Cano, M.E., Gonçalves, R.G., Feliciangeli, D., field work: ALCF. Processed the biological material: ALCF, MPF and Vezzani, D., Wisnivesky-Colli, C., Gorla, D.E., Marti, G.A., Rabinovich, J.E., 2018. RVP. Analyzed the data: ALCF, MPF, LRP, RVP and REG. Contributed DataTri, a database of American triatomine species occurrence. Sci. Data 5, 180071. https://doi.org/10.1038/sdata.2018.71. with reactives: RD. Wrote the paper: ALCF, MPF, RVP, LRP and REG. All Cecere, M.C., Cardinal, M.V., Arrabal, J.P., Moreno, C., Gürtler, R.E., 2015. Microcavia authors read and approved the final manuscript. australis (Caviidae, Rodentia), a new highly competent host of Trypanosoma cruzi I in rural communities of northwestern Argentina. Acta Trop. 142, 34–40. https://doi. org/10.1016/j.actatropica.2014.10.019. Funding Di Iorio, O., Gürtler, R.E., 2017. Seasonality and temperature-dependent flight dispersal of Triatoma infestans (Hemiptera: Reduviidae) and other vectors of Chagas disease in This study was supported by grants from the former Ministerio de Western Argentina. J. Med. Entomol. 54, 1285–1292. https://doi.org/10.1093/jme/ tjx109. Ciencia, Tecnología e Innovación Productiva (PDTS-PX03 to R.E.G. and Flores, G., Lagos, S., Roig-Juñent, S., 2004. Ground dwelling arthropods from beneath A.L.C.F.) and Agencia Nacional de Promoción Científica y Tecnológica de la Prosopis flexuosa, in Telteca Reserve (Mendoza – Argentina). Multequina 13, 71–90. 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