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Systematic review on the biology, ecology, genetic diversity and parasite transmission potential of Panstrongylus geniculatus (Latreille 1811) in Latin America

Abstract

Panstrongylus geniculatus (Latreille, 1811) is the triatomine with the largest geographic distribution in Latin America. It has been reported in 18 countries from southern Mexico to northern Argentina, including the Caribbean islands. Although most reports indicate that P. geniculatus has wild habitats, this species has intrusive habits regarding human dwellings mainly located in intermediate deforested areas. It is attracted by artificial light from urban and rural buildings, raising the risk of transmission of Trypanosoma cruzi. Despite the wide body of published information on P. geniculatus, many knowledge gaps exist about its biology and epidemiological potential. For this reason, we analysed the literature for P. geniculatus in Scopus, PubMed, Scielo, Google Scholar and the BibTriv3.0 databases to update existing knowledge and provide better information on its geographic distribution, life cycle, genetic diversity, evidence of intrusion and domiciliation, vector-related circulating discrete taxonomic units, possible role in oral T. cruzi transmission, and the effect of climate change on its biology and epidemiology.

Key words:
Panstrongylus geniculatus; geographic distribution; genetic diversity; oral transmission of Trypanosoma cruzi; climate change


Chagas disease affects around 7 million people in Latin America and is considered one of the 10 most important neglected diseases in the region.11. WHO - World Health Organization. Chagas disease (American trypanosomiasis). (Updated: 2020 May 23; cited 2020 Jul 15). Available from: https://www.who.int/news-room/fact-sheets/detail/chagas-disease-(american-trypanosomiasis).
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Currently, 154 species within the Triatominae subfamily (three extinct and 151 extant) have been described and are able to transmit Trypanosoma cruzi, the causative agent of Chagas disease under natural and experimental conditions.22. Justi S, Galvão C. The evolutionary origin of diversity in Chagas disease vectors. Trends Parasitol. 2016; 33(1): 42-52. http://dx.doi.org/10.1016/j.pt.2016.11.002.
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,33. Monteiro F, Weirauch C, Felix M, Lazoski C, Abad-Franch F. Evolution, systematics, and biogeography of the Triatominae, vectors of Chagas disease. Adv Parasitol. 2018; 99: 265-344. https://doi.org/10.1016/bs.apar.2017.12.002.
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,44. Dorn P, Justi S, Dale C, Stevens L, Galvão C, Lima-Cordón R, et al. Description of Triatoma mopan sp. n. from a cave in Belize (Hemiptera, Reduviidae, Triatominae). ZooKeys. 2018; 775: 69-95. http://dx.doi.org/10.3897/zookeys.775.22553.
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,66. Nascimento J, Da Rosa J, Salgado-Roa F, Hernández C, Pardo-Diaz C, Alevi K, et al. Taxonomical over splitting in the Rhodnius prolixus (Insecta: Hemiptera: Reduviidae) clade: Are R. taquarussuensis (da Rosa et al., 2017) and R. neglectus (Lent, 1954) the same species? PLoS One. 2019; 14(2): e0211285. https://doi.org/10.1371/journal.pone.0211285.
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Panstrongylus geniculatus (Latreille, 1811) is the triatomine with the greatest geographic distribution in the Americas, ranging from southern Mexico to northern Argentina and including the Caribbean islands.99. Lent H, Wygodzinsky P. Revision of the Triatominae (Hemiptera: Reduviidae), and their significance as vectors of Chagas disease. Bull Am Museum Nat Hist. 1979; 163(3): 123-520. http://hdl.handle.net/2246/1282.
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,1010. Galvão C, Carcavallo R, 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. http://dx.doi.org/10.11646/zootaxa.202.1.1.
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This vector occupies extremely variable areas across the wild landscape, being found in different ecosystems within the same country.1111. Zeledón R, Ugalde J, Paniagua L. Entomological and ecological aspects of six sylvatic species of Triatomines (Hemiptera, Reduviidae) from the collection of the National Biodiversity Institute of Costa Rica, Central América. Mem Inst Oswaldo Cruz. 2001; 96(6): 757-64. https://doi.org/10.1590/s0074-02762001000600002.
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Most records deal with the species occupying altitudes ranging from sea level to around 2,000 metres above sea level (masl); however, the species has been found at altitudes from 2,000 to 4,000 masl in some Andean countries (i.e., Colombia, Venezuela, Ecuador, Peru and Bolivia), thereby indicating the species’ great adaptive capability, probably enabling its shift in altitude as a consequence of lowland warming, regarding today’s climate changes.1212. Carcavallo RU, Curto de Casas S, Sherlock I, Galíndez I, Juberg J, Galvão C, et al. Geographical distribution and alti-latitudinal dispersión. In RU Carcavallo RU, IG Girón, J Jurberg, editors. Atlas of Chagas disease vectors in the Americas. Rio de Janeiro: Fiocruz; 1998; p. 747-92.,1313. Parra-Henao G, Suárez-Escudero L, González-Caro S. Potential distribution of Chagas disease vectors (Hemiptera, Reduviidae, Triatominae) in Colombia, based on ecological niche modeling. J Trop Med. 2016; 1439090: 1-10. http://dx.doi.org/10.1155/2016/1439090.
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,1414. Ceccarelli S, Balsalobre A, Cano ME, Vicente ME, Rabinovich JE, Medone P, et al. Datos de ocurrencia de triatominos americanos del Laboratorio de Triatominos del CEPAVE (CONICET-UNLP). Version 1.2. Centro de Estudios Parasitológicos y de Vectores (CEPAVE). 2020 [accessed via GBIF.org on 2021-01-09]. Available from: https://doi.org/10.15468/fbywtn.
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,1515. Guhl F, Aguilera G, Pinto N, Vergara D. Actualización de la distribución geográfica y ecoepidemiología de la fauna de triatominos (Reduviidae: Triatominae) en Colombia. Biomédica. 2007; 27(1): 143-62.,1616. Chávez J. Contribución al estudio de los triatominos del Perú: distribución geográfica, nomenclatura y notas taxonómicas. An Fac Med. 2006; 67(1): 65-76.

The last few decades have seen much interest in the biology, ecology and epidemiology of P. geniculatus, thereby enabling effective control strategies for this species to be designed. Therefore, this review aims to update existing knowledge about P. geniculatus and address current information gaps. A search was conducted in Scopus, PubMed, Scielo, Google Scholar, BibTriv3.0 databases with no filters of language or time and until August 2020. All relevant studies on taxonomy, morphological variability, life cycle, geographical distribution, genetic diversity, intrusion and colonisation of human dwellings, oral transmission and discrete taxonomic units of T. cruzi and possible effects of climate change on P. geniculatus were chosen.

Taxonomy, morphology and life cycle

Taxonomy - Currently, P. geniculatus (Latreille, 1811) is the accepted scientific name for this species; however, the following synonyms have also been used reviewed by Patterson et al.:1717. Patterson J, Barbosa S, Feliciangeli M. On the genus Panstrongylus Berg 1879: evolution, ecology and epidemiological significance. Acta Trop. 2009; 110(2-3): 187-99. http://dx.doi.org/10.1016/j.actatropica.2008.09.008.
http://dx.doi.org/10.1016/j.actatropica....
Reduvius geniculatus (Latreille, 1811), Conorhinus lutulentus (Erichson, 1848), Lamus geniculatus (Stal, 1859), Conorhinus corticalis (Walker, 1873), Conorhinus geniculatus (Walker, 1873), Lamus corticalis (Lethierry & Severin, 1896), Triatoma geniculata (Chagas, 1912), Triatoma tenuis (Neiva, 1914), Triatoma fluminensis (Neiva and Pinto, 1922), Mestor geniculatus (Brindley, 1931) and Panstrongylus parageniculatus (Ortiz, 1971).

Fifteen species have been described in the Panstrongylus genus: P. chinai, P. diasi, P. geniculatus, P. guentheri, P. howardi, P. hispaniolae, P. humeralis, P. lenti, P. lignarius, P. lutzi, P. megistus, P. martinezorum, P. mitarakaensis, P. rufotuberculatus, P. tupynambai.22. Justi S, Galvão C. The evolutionary origin of diversity in Chagas disease vectors. Trends Parasitol. 2016; 33(1): 42-52. http://dx.doi.org/10.1016/j.pt.2016.11.002.
http://dx.doi.org/10.1016/j.pt.2016.11.0...
,33. Monteiro F, Weirauch C, Felix M, Lazoski C, Abad-Franch F. Evolution, systematics, and biogeography of the Triatominae, vectors of Chagas disease. Adv Parasitol. 2018; 99: 265-344. https://doi.org/10.1016/bs.apar.2017.12.002.
https://doi.org/10.1016/bs.apar.2017.12....
,1717. Patterson J, Barbosa S, Feliciangeli M. On the genus Panstrongylus Berg 1879: evolution, ecology and epidemiological significance. Acta Trop. 2009; 110(2-3): 187-99. http://dx.doi.org/10.1016/j.actatropica.2008.09.008.
http://dx.doi.org/10.1016/j.actatropica....
Studies on the taxonomy of this genus and the identification of P. geniculatus have been problematic because most are based on morphometry and karyotyping, but few have employed molecular markers.1717. Patterson J, Barbosa S, Feliciangeli M. On the genus Panstrongylus Berg 1879: evolution, ecology and epidemiological significance. Acta Trop. 2009; 110(2-3): 187-99. http://dx.doi.org/10.1016/j.actatropica.2008.09.008.
http://dx.doi.org/10.1016/j.actatropica....
,1818. Crossa R, Hernández M, Caraccio M, Rose V, Valente S, Valente V, et al. Chromosomal evolution trends of the genus Panstrongylus (Hemiptera, Reduviidae), vectors of Chagas disease. Infect Genet Evol. 2002; 2(1): 47-56. https://doi.org/10.1016/S1567-1348(02)00063-1.
https://doi.org/10.1016/S1567-1348(02)00...
,1919. dos Santos C, Jurberg J, Galvão C, Rocha D. Morphometric study of the genus Panstrongylus Berg, 1879 (Hemiptera, Reduviidae. Triatominae). Mem Inst Oswaldo Cruz. 2003; 98(7): 939-44. http://dx.doi.org/10.1590/S0074-02762003000700014.
http://dx.doi.org/10.1590/S0074-02762003...
,2020. Aldana E, Heredia E, Avendaño F, Lizano E, Concepción J, Bonfante R, et al. Análisis morfométrico de Panstrongylus geniculatus de Caracas, Venezuela. Biomédica. 2011; 31(1): 108-17. https://doi.org/10.7705/biomedica.v31i1.341
https://doi.org/10.7705/biomedica.v31i1....
) The phylogenies based on morphological traits presents the Panstrongylus genus as a monophyletic group, whereas the ITS-2 (rDNA) phylogenetic trees suggest that it is polyphyletic group of Triatoma species from South, Central and North America.99. Lent H, Wygodzinsky P. Revision of the Triatominae (Hemiptera: Reduviidae), and their significance as vectors of Chagas disease. Bull Am Museum Nat Hist. 1979; 163(3): 123-520. http://hdl.handle.net/2246/1282.
http://hdl.handle.net/2246/1282...
,2121. Marcilla A, Bargues M, Abad-Franch F, Panzera F, Carcavallo R, Noireau F, et al. Nuclear rDNA ITS-2 sequences reveal polyphyly of Panstrongylus species (Hemiptera: Reduviidae: Triatominae), vectors of Trypanosoma cruzi. Infect Genet Evol. 2002; 1(3): 225-35. http://dx.doi:10.1016/s1567-1348(02)00029-1.
https://doi.org/10.1016/s1567-1348(02)00...
In another study, using four mitochondrial markers (16S, COI, COII, Cytb) and two nuclear (18S and 28S) ones, Panstrongylus fell into two groups. One of the groups contained P. tupynambai, P. lutzi and P. geniculatus as sister taxa of Nesotriatoma, whereas the other was a highly supported group that includes Triatoma tibiamaculata and P. megistus.2222. Justi S, Russo C, Mallet J, Obara M, Galvão C. Molecular phylogeny of Triatomini (Hemiptera: Reduviidae: Triatominae). Parasit Vectors. 2014; 7(149): 1-12. http://dx.doi:10.1186/1756-3305-7-149.
https://doi.org/10.1186/1756-3305-7-149...

The use of morphological characters to classify Panstrongylus species has led to the description of ‘new species’ in the genus. This is the case for two species described in French Guiana and Venezuela; namely, P. mitarakaensis and P. martinezorum, respectively.2323. Bérenger J, Blanchet D. A new species of the genus Panstrongylus from French Guiana (Heteroptera; Reduviidae; Triatominae). Mem Inst Oswaldo Cruz. 2007; 102(6): 733-6. https://doi.org/10.1590/S0074-02762007005000088.
https://doi.org/10.1590/S0074-0276200700...
,2424. Ayala L. Una nueva especie de Panstrongylus Berg de Venezuela (Hemiptera: Reduviidae, Triatominae). Entomotropica. 2009; 24(3): 105-9. They both look quite similar to P. geniculatus but no molecular methods have been used to confirm that they are the same species.33. Monteiro F, Weirauch C, Felix M, Lazoski C, Abad-Franch F. Evolution, systematics, and biogeography of the Triatominae, vectors of Chagas disease. Adv Parasitol. 2018; 99: 265-344. https://doi.org/10.1016/bs.apar.2017.12.002.
https://doi.org/10.1016/bs.apar.2017.12....
Another species in Venezuela, P. turpiali, was synonymised with P. chinai but both were then shown to phenotypically match P. geniculatus.2525. Valderrama A, Lizano E, Cabello D, Valera M. Panstrongylus turpiali, n. sp. (Hemiptera: Reduviidae: Triatominae) from Venezuela. Caribb J Sci. 1996; 32: 142-4.,2626. Lent H. Novos sinônimos de duas espécies de Triatominae da Venezuela (Hemiptera, Reduviidae). Entomol Vect. 1997; 4: 67-70.,2727. Ayala J. Presencia de Panstrongylus Chinai (Del ponte, 1929) en Venezuela, con notas aclaratorias sobre su sinonimia con Panstrongylus Turpiali (Heteroptera: Reduviidae: Triatominae). Boletín de la SEA. 2016; 59: 233-6. Therefore, it is necessary to use molecular approaches to clarify the taxonomic status of P. geniculatus and phenotypically similar species.

Morphological variability in P. geniculatus - Several authors have reported on the morphological characteristics of P. geniculatus. Its nymph and adult stages have been described using light and scanning electron microscopy.99. Lent H, Wygodzinsky P. Revision of the Triatominae (Hemiptera: Reduviidae), and their significance as vectors of Chagas disease. Bull Am Museum Nat Hist. 1979; 163(3): 123-520. http://hdl.handle.net/2246/1282.
http://hdl.handle.net/2246/1282...
,1717. Patterson J, Barbosa S, Feliciangeli M. On the genus Panstrongylus Berg 1879: evolution, ecology and epidemiological significance. Acta Trop. 2009; 110(2-3): 187-99. http://dx.doi.org/10.1016/j.actatropica.2008.09.008.
http://dx.doi.org/10.1016/j.actatropica....
,1919. dos Santos C, Jurberg J, Galvão C, Rocha D. Morphometric study of the genus Panstrongylus Berg, 1879 (Hemiptera, Reduviidae. Triatominae). Mem Inst Oswaldo Cruz. 2003; 98(7): 939-44. http://dx.doi.org/10.1590/S0074-02762003000700014.
http://dx.doi.org/10.1590/S0074-02762003...
,2828. Lent H, Jurberg J. Estudos morfológicos comparativos de Panstrongylus geniculatus (Latreille, 1811) e Panstrongylus megistus (Burmeister, 1835) e suas genitália externas (Hemiptera, Reduviidae, Triatominae). Rev Bras Biol. 1968; 28(4): 499-520.,2929. Galíndez I, Carcavallo R, Valderrama A. Erwinilas o cerdas interomatidiales en la subfamilia Triatominae (Hemiptera: Reduviidae). Entomol Vect. 1994; 1(3): 93-6.,3030. Carcavallo RU, Galíndez Girón I, Catalá S, Jurberg J, Lent H, Galvão C, et al. Some anatomic structures studied with scanning electronic microscopy (SEM). In RU Carcavallo, I Galíndez Girón, J Jurberg, H Lent, editors. Atlas of Chagas disease vectors in the Americas. Rio de Janeiro: Fiocruz; 1998. p. 299-393.,3131. Galíndez Girón I, Carcavallo RU, Jurberg J, Galvão C, Lent H, Barata J, et al. External morphology and anatomy. In RU Carcavallo, I Galíndez Girón, J Jurberg, H Lent, editors. Atlas of Chagas disease vectors in the Americas. Rio de Janeiro: Fiocruz; 1998. p. 53-84.,3232. Wolff M, González C. Ciclo de vida de Panstrongylus geniculatus (Hemiptera: Reduviidae) en condiciones de laboratorio. Caldasia. 1998; 20(1): 75-7. https://revistas.unal.edu.co/index.php/cal/article/view/17471.
https://revistas.unal.edu.co/index.php/c...
,3333. Soto-Vivas A. Clave pictórica de triatominos (Hemiptera: Triatominae) de Venezuela. Bol Malariol Salud Amb. 2009; 49(2): 259-74.,3434. Avendaño-Rangel F, Sandoval C, Aldana E. Descripción de setas cuticulares externas de cabeza, tórax, patas, abdomen y genitales en cuatro especies de Triatominae. Biomédica. 2016; 36(3): 354-8. http://dx.doi.org/10.7705/biomedica.v36i3.3122.
http://dx.doi.org/10.7705/biomedica.v36i...
,3535. Jaramillo N, Castillo D, Wolff M. Geometric morphometric differences between Panstrongylus geniculatus from field and laboratory. Mem Inst Oswaldo Cruz. 2002; 97(5): 667-73. http://dx.doi.org/10.1590/S0074-02762002000500015.
http://dx.doi.org/10.1590/S0074-02762002...
,3636. Jurberg J, Galvão C, Noireau F, Carcavallo R, Rocha D, Lent H. Uma iconográfica dos triatomíneos (Hemiptera: Reduviidae). Entomol Vect. 2004; 11(3): 457-94. Elsewhere, the geometric morphometric techniques applied to a sylvatic population and its laboratory descendants over five generations revealed size differences in P. geniculatus but not in its shape. Essentially, head size and wing size were both reduced from sylvatic and laboratory populations.3535. Jaramillo N, Castillo D, Wolff M. Geometric morphometric differences between Panstrongylus geniculatus from field and laboratory. Mem Inst Oswaldo Cruz. 2002; 97(5): 667-73. http://dx.doi.org/10.1590/S0074-02762002000500015.
http://dx.doi.org/10.1590/S0074-02762002...
Another morphometric study on P. geniculatus showed a reduction in the size of its populations in Caracas city, when compared with sylvatic populations from other Venezuelan regions.2020. Aldana E, Heredia E, Avendaño F, Lizano E, Concepción J, Bonfante R, et al. Análisis morfométrico de Panstrongylus geniculatus de Caracas, Venezuela. Biomédica. 2011; 31(1): 108-17. https://doi.org/10.7705/biomedica.v31i1.341
https://doi.org/10.7705/biomedica.v31i1....
In this review we have included unpublished photographs representing the known morphological characteristics of the species, which we believe will help to a primary identification of individuals captured in sylvatic, peridomestic or domestic environments (Fig. 1A-G).

Fig. 1:
(A) dorsal view of a female Panstrongylus geniculatus: (i) clipeus, (ii) antenna, (iii) compound eye, (iv) leg, (v) pronotum, (vi) scutellum, (vii) connexivum, (viii) wings (hemielytrons); (B) head; (C) pronotum and scutellum; (D) legs; (E) coxa and trochanter; (F) spicules; (G) connexivum. Source: authors.

Adult P. geniculatus insects display sexual dimorphism. The total length of the male is 22-28 mm and the larger-bodied female is 22.5-29.5 mm. The posterior end of the male’s abdomen is rounded in shape, whereas it is tip-shaped in the female (Fig. 2I-J). Its colouration is light brown to orange brown and is interspersed with dark patches on various parts of the body, which do not follow a defined pattern in that the connexivum has two intercalated regions of colour: a flat black-coloured one and another coloured orange to ochre (yellow-orange) in the interior (Fig. 1A).3636. Jurberg J, Galvão C, Noireau F, Carcavallo R, Rocha D, Lent H. Uma iconográfica dos triatomíneos (Hemiptera: Reduviidae). Entomol Vect. 2004; 11(3): 457-94.

The head is sub-conical-shaped, narrow at eye level, and shorter than the pronotum; the anteocular region is approximately twice as long as the postocular region. The dorsal surface is slightly rough. The general colouration is ochre, but in some individuals two dark stripes extending from the base of the jugae to the space between the ocelli are observed in the dorsal region. Anteniferous tubers are located near the anterior edges of the eyes, and the antennas vary from reddish brown to black. The first segment of the antenna subtly exceeds the apex level of the clypeus (Fig. 1A-B).

Behind the head is the orange-brown pronotum whose anterior lobe is slightly convex and rough. The pronotum features a central four-leaf clover-shaped mark and “1 + 1” side marks. The posterior lobe is irregularly rough, with a black band along the posterior margin, except in the humeral area (Fig. 1C). The femurs and tibiae are dark brown or black (Fig. 1A, D). The legs have light yellow or orange-yellow coxas and trochanters (Fig. 1E). The front and middle femurs have two to six (usually four) small subapical denticles arranged in two rows (Fig. 1F). The hemielytrons are light brown or light yellowish brown, with dark veins in the membranes (Fig. 1G).

Life cycle of P. geniculatus under laboratory conditions - P. geniculatus eggs do not adhere to the substrate; rather, they are oviposited free on a surface. They are oblong and symmetrically shaped, without lateral flattening or collar, and at one end is a prominent and convex operculum through which hatching is performed. The eggs are bright white for the first days after oviposition, and six-eight days later they turn pinkish yellow, pink, or pearl, becoming translucent after hatching (Fig. 2A-C). The nymphal and adult stages are shown in Fig. 2D-J.

Fig. 2:
stages of the life cycle of Panstrongylus geniculatus: (A) freshly oviposited eggs; (B) eggs near hatching; (C) hatching; (D) nymph stage N1; (E) nymph stage N2; (F) nymph stage N3; (G) nymph stage N4; (H) nymph stage N5; (I) adult (female); (J) adult (male). Source: authors.

The life cycle period under laboratory conditions has been shown to be dependent on the experimental conditions employed, such as temperature, relative humidity and food source in the colonies. Depending on the management of these variables, very heterogeneous records have been observed from 149.5 to 531 days, and even up to two years. When the experimental conditions are 21-26ºC and 90-100% for temperature and relative humidity, respectively, life cycle durations of 269, 297, 275.8, 273, 275.4 days have been reported (average, 278 days).3232. Wolff M, González C. Ciclo de vida de Panstrongylus geniculatus (Hemiptera: Reduviidae) en condiciones de laboratorio. Caldasia. 1998; 20(1): 75-7. https://revistas.unal.edu.co/index.php/cal/article/view/17471.
https://revistas.unal.edu.co/index.php/c...
,3737. Lent H, Jurberg J. Observacões sobre o ciclo evolutivo, em laboratorio, do Panstrongylus geniculatus (Latreille, 1811) (Hemiptera: Reduviidae: Triatominae). An Acad Brasil Ciênc. 1969; 41: 125-31.,3838. Galíndez I. Colonización y ciclo de vida de Panstrongylus geniculatus (Latreille, 1811) (Hemiptera: Reduviidae: Triatominae). Universidad de Los Andes, Núcleo Rafael Rangel, Trujillo: 1990; 34 pp.,3939. Galíndez Girón I, Torres A, Márquez J, Carcavallo R. Colonización y ciclo de vida de Panstrongylus geniculatus (Latreille, 1811) (Hemiptera, Reduviidae, Triatominae). Entomol Vector. 1997; 4(3): 83-94.,4040. Wolff M, Castillo D. Evidencias de domesticación y aspectos biológicos de Panstrongylus geniculatus (Latreille, 1811) (Hemiptera: Reduviidae). Acta Entomol Chile. 2000; 24: 77-83.,4141. Cabello D, Galíndez Girón I. Vital Statistics of Panstrongylus geniculatus (Latreille 1811) (Hemiptera: Reduviidae) under experimental conditions. Mem Inst Oswaldo Cruz. 1998; 93(2): 257-62. http://dx.doi.org/10.1590/S0074-02761998000200024.
http://dx.doi.org/10.1590/S0074-02761998...
,4242. Esteban L, Angulo V. Estudio comparativo de la ovipostura de una cepa de laboratorio y una de campo de Panstrongylus geniculatus alimentadas con Gallus domesticus y Mus musculus BALB/c en condiciones de laboratorio. XX Congreso Latinoamericano de Parasitología. Biomédica. 2011a; 31(3): 253.,4343. Esteban L, Angulo V. Estandarización de las condiciones de ayuno y peso en ninfas de V instar de Panstrongylus geniculatus para su utilización en pruebas biológicas. XX Congreso Latinoamericano de Parasitología. Biomédica. 2011; 31(3): 252-3.,4444. Rabinovich J, Feliciangeli M. Vital statistics of Triatominae (Hemiptera: Reduviidae) under laboratory conditions: IV. Panstrongylus geniculatus. J Med Entomol. 2015; 52(5): 797-805. https://doi.org/10.1093/jme/tjv112.
https://doi.org/10.1093/jme/tjv112...
One of the first studies to investigate the life cycle of P. geniculatus reported that the total development time is approximately 2 years.4545. Mayer M, Pifano C, Medina R. Aspectos epidemiológicos de la enfermedad de Chagas en Venezuela: bases para una campaña de saneamiento aplicable a zonas endémicas del medio rural venezolano. XII Conferencia Sanitaria Panamericana. 1946. Available from: http://iris.paho.org/xmlui/bitstream/handle/123456789/28807/CSP12_C30.pdf?sequence=1.
http://iris.paho.org/xmlui/bitstream/han...
Another study reported on the difficulties of establishing the species as a colony and observed that the time taken for the life cycle is 531 days (75.8 weeks).3737. Lent H, Jurberg J. Observacões sobre o ciclo evolutivo, em laboratorio, do Panstrongylus geniculatus (Latreille, 1811) (Hemiptera: Reduviidae: Triatominae). An Acad Brasil Ciênc. 1969; 41: 125-31.

The 1990s brought advances in biological knowledge. The life cycle was studied under controlled laboratory conditions and reported that the average development time was 269 days (38.4 weeks) and 297 days (42.4 weeks) for nymphs fed on chickens (Gallus gallus) and opossums (Didelphis marsupialis), respectively.3838. Galíndez I. Colonización y ciclo de vida de Panstrongylus geniculatus (Latreille, 1811) (Hemiptera: Reduviidae: Triatominae). Universidad de Los Andes, Núcleo Rafael Rangel, Trujillo: 1990; 34 pp. In a life-cycle study using uncontrolled conditions, the insects were subjected to temperatures of 21-25ºC, relative humidities of 90-100%, and were fed ad libitum weekly on chickens (G. gallus). An N1 nymph stage to adulthood duration of 275.8 days (39.4 weeks) was reported.3939. Galíndez Girón I, Torres A, Márquez J, Carcavallo R. Colonización y ciclo de vida de Panstrongylus geniculatus (Latreille, 1811) (Hemiptera, Reduviidae, Triatominae). Entomol Vector. 1997; 4(3): 83-94. The duration of the life cycle for specimens from the municipality of Amalfi in Antioquia, Colombia, which were subject to controlled temperature (29 ± 1ºC) and relative humidity (95 ± 1ºC) conditions, was 149.5 days (21.4 weeks).3232. Wolff M, González C. Ciclo de vida de Panstrongylus geniculatus (Hemiptera: Reduviidae) en condiciones de laboratorio. Caldasia. 1998; 20(1): 75-7. https://revistas.unal.edu.co/index.php/cal/article/view/17471.
https://revistas.unal.edu.co/index.php/c...
Later on, evidence of the colonisation processes in Amalfi in Antioquia, Colombia, and estimated transmission risk indicator values were obtained. They also reported on the time required for blood intake by adults (mean, 67.8 minutes for males and 80.27 minutes for females). Blood consumption was on average 0.12 g for males and 0.26 g for females, with defecation times post-feeding of 55 minutes for females and 60 minutes for males.4040. Wolff M, Castillo D. Evidencias de domesticación y aspectos biológicos de Panstrongylus geniculatus (Latreille, 1811) (Hemiptera: Reduviidae). Acta Entomol Chile. 2000; 24: 77-83. Sylvatic intrusive insects captured in domestic environments have had high T. cruzi infection prevalence (see Table III in this review). In addition, a post-feeding time close to one hour for both males and females could be a determining factor for this species regarding the oral transmission of Chagas’ disease due to food contamination. As P. geniculatus has been repeatedly associated with orally transmitted outbreaks, this hypothesis could be ascertained by comparing this species’ post-feeding time characteristics and natural infection frequencies to those for other species invading human dwellings.

The first statistical evaluation of the population dynamics of P. geniculatus under controlled laboratory conditions studied a cohort of 60 eggs placed at constant temperature (26 ± 3ºC) and relative humidity (90 ± 10%) that were fed every 15 days on chickens (G. gallus). The researchers observed that the hatching percentage was 88.9%, the average nymph development time was 273 days (39 weeks), and the longevity of the adults was 504 days (72 weeks).4141. Cabello D, Galíndez Girón I. Vital Statistics of Panstrongylus geniculatus (Latreille 1811) (Hemiptera: Reduviidae) under experimental conditions. Mem Inst Oswaldo Cruz. 1998; 93(2): 257-62. http://dx.doi.org/10.1590/S0074-02761998000200024.
http://dx.doi.org/10.1590/S0074-02761998...

In contrast, the need of optimising the ovipositors of female P. geniculatus to enable massive breeding of this species in the laboratory and for use in bioassays, compared the ovipositors of laboratory and field populations fed on chickens (G. gallus) and mice (Mus musculus, strain BALB/c). The authors found that the fertility of the first-generation laboratory population was twice that of the wild population when both were fed on chickens.4242. Esteban L, Angulo V. Estudio comparativo de la ovipostura de una cepa de laboratorio y una de campo de Panstrongylus geniculatus alimentadas con Gallus domesticus y Mus musculus BALB/c en condiciones de laboratorio. XX Congreso Latinoamericano de Parasitología. Biomédica. 2011a; 31(3): 253.,4343. Esteban L, Angulo V. Estandarización de las condiciones de ayuno y peso en ninfas de V instar de Panstrongylus geniculatus para su utilización en pruebas biológicas. XX Congreso Latinoamericano de Parasitología. Biomédica. 2011; 31(3): 252-3.

The most recent and detailed study on the vital statistics of P. geniculatus, estimated its development times by stages, vital statistics (mortality and fertility), and population growth parameters (intrinsic natural growth rate, finite population growth rate, net reproduction rate, and generational time). In a cohort of 100 eggs kept under constant temperature (26 ± 1ºC) and relative humidity (60 ± 10%) and fed every eight days with chicken blood, it was observed that the total development time by stage was 275.4 days (39.4 weeks), and mortality reached 58% in the initial stages (I, II, and III), which represents 60% of the total mortality.4444. Rabinovich J, Feliciangeli M. Vital statistics of Triatominae (Hemiptera: Reduviidae) under laboratory conditions: IV. Panstrongylus geniculatus. J Med Entomol. 2015; 52(5): 797-805. https://doi.org/10.1093/jme/tjv112.
https://doi.org/10.1093/jme/tjv112...

Geographical distribution, ecotopes and genetic variability

Geographical distribution and ecotopes - P. geniculatus has the greatest geographical distribution of species belonging to this genus. It is found exclusively in Latin America between 21.1ºN, 30.3ºS, 38.8ºE, and 94.9ºW, covering an estimated 12 million km2. To date, its presence has been reported in 18 countries (Table I, Fig. 3), from southern Mexico to northern Argentina, including the Caribbean islands.99. Lent H, Wygodzinsky P. Revision of the Triatominae (Hemiptera: Reduviidae), and their significance as vectors of Chagas disease. Bull Am Museum Nat Hist. 1979; 163(3): 123-520. http://hdl.handle.net/2246/1282.
http://hdl.handle.net/2246/1282...
,1212. Carcavallo RU, Curto de Casas S, Sherlock I, Galíndez I, Juberg J, Galvão C, et al. Geographical distribution and alti-latitudinal dispersión. In RU Carcavallo RU, IG Girón, J Jurberg, editors. Atlas of Chagas disease vectors in the Americas. Rio de Janeiro: Fiocruz; 1998; p. 747-92.,4545. Mayer M, Pifano C, Medina R. Aspectos epidemiológicos de la enfermedad de Chagas en Venezuela: bases para una campaña de saneamiento aplicable a zonas endémicas del medio rural venezolano. XII Conferencia Sanitaria Panamericana. 1946. Available from: http://iris.paho.org/xmlui/bitstream/handle/123456789/28807/CSP12_C30.pdf?sequence=1.
http://iris.paho.org/xmlui/bitstream/han...
,4646. Leite G, dos Santos C, Falqueto A. Insecta, Hemiptera, Reduviidae, Panstrongylus geniculatus: geographic distribution map. Checklist. 2007; 3(2): 147-52.,4747. Ceccarelli S, Balsalobre A, Medone P, Cano M, Gonçalves R, Gurgel R, et al. DataTri, a database of American triatomine species occurrence. Scientific Data. 2018; 5: 180071. https://dx.doi.org/10.1038/sdata.2018.71.
https://dx.doi.org/10.1038/sdata.2018.71...

TABLE I
Geographic distribution of Panstrongylus geniculatus in Latin America

Fig. 3:
continental distribution of Panstrongylus geniculatus. Maps were made with the database reported by Ceccarelli et al.4747. Ceccarelli S, Balsalobre A, Medone P, Cano M, Gonçalves R, Gurgel R, et al. DataTri, a database of American triatomine species occurrence. Scientific Data. 2018; 5: 180071. https://dx.doi.org/10.1038/sdata.2018.71.
https://dx.doi.org/10.1038/sdata.2018.71...

With its wide geographical distribution, P. geniculatus is found from sea level to 2,000-4,000 m above sea level in the Andean countries (Colombia, Venezuela, Ecuador, Peru and Bolivia)1414. Ceccarelli S, Balsalobre A, Cano ME, Vicente ME, Rabinovich JE, Medone P, et al. Datos de ocurrencia de triatominos americanos del Laboratorio de Triatominos del CEPAVE (CONICET-UNLP). Version 1.2. Centro de Estudios Parasitológicos y de Vectores (CEPAVE). 2020 [accessed via GBIF.org on 2021-01-09]. Available from: https://doi.org/10.15468/fbywtn.
https://doi.org/10.15468/fbywtn....
,1515. Guhl F, Aguilera G, Pinto N, Vergara D. Actualización de la distribución geográfica y ecoepidemiología de la fauna de triatominos (Reduviidae: Triatominae) en Colombia. Biomédica. 2007; 27(1): 143-62.,1616. Chávez J. Contribución al estudio de los triatominos del Perú: distribución geográfica, nomenclatura y notas taxonómicas. An Fac Med. 2006; 67(1): 65-76. and in places where the average annual temperature (minimum and maximum) ranges between -3.9 and 34.3ºC and precipitation reaches up to 4,000 mm/year.99. Lent H, Wygodzinsky P. Revision of the Triatominae (Hemiptera: Reduviidae), and their significance as vectors of Chagas disease. Bull Am Museum Nat Hist. 1979; 163(3): 123-520. http://hdl.handle.net/2246/1282.
http://hdl.handle.net/2246/1282...
Some authors have suggested that the morphological variations found among P. geniculatus populations result from the demands of the different environments.1818. Crossa R, Hernández M, Caraccio M, Rose V, Valente S, Valente V, et al. Chromosomal evolution trends of the genus Panstrongylus (Hemiptera, Reduviidae), vectors of Chagas disease. Infect Genet Evol. 2002; 2(1): 47-56. https://doi.org/10.1016/S1567-1348(02)00063-1.
https://doi.org/10.1016/S1567-1348(02)00...
Table II shows the presence of P. geniculatus above 2,000 masl in Colombia and Peru.

TABLE II
Records of Panstrongylus geniculatus presence above 2,000 masl in Colombia and Peru

Natural ecotopes vary from dry or very dry tropical forests to savanna and humid tropical forests, and P. geniculatus can be found in caverns, caves, and burrows in these environments where it is mainly associated with armadillos (Dasypodidae), anteaters (Myrmecophagidae), bats (Chiroptera), and a wide variety of other vertebrates. It is also found under bark, tree trunks and fallen trees and near bird nests in palm trees (Acrocomia aculeata, Syagrus romanzoffiana, Elaeis oleifera, and Leopoldinia piassaba) and in epiphytes.99. Lent H, Wygodzinsky P. Revision of the Triatominae (Hemiptera: Reduviidae), and their significance as vectors of Chagas disease. Bull Am Museum Nat Hist. 1979; 163(3): 123-520. http://hdl.handle.net/2246/1282.
http://hdl.handle.net/2246/1282...
,1717. Patterson J, Barbosa S, Feliciangeli M. On the genus Panstrongylus Berg 1879: evolution, ecology and epidemiological significance. Acta Trop. 2009; 110(2-3): 187-99. http://dx.doi.org/10.1016/j.actatropica.2008.09.008.
http://dx.doi.org/10.1016/j.actatropica....
,8282. Carcavallo RU, Rodríguez M, Salvatella R, Curto de Casas S, Rocha D, Sherlock I, et al. Habitats and related fauna. In RU Carcavallo, I Galíndez Girón, J Jurberg, H Lent, editors. Atlas of Chagas disease vectors in the Americas. Rio de Janeiro: Fiocruz; 1998. p. 561-620.,8383. Carcavallo RU, Rocha D, Galíndez Girón I, Sherlock I, Galvão C, Lent H, et al. Feeding sources and patterns. In RU Carcavallo, I Galíndez Girón, J Jurberg, H Lent, editors. Atlas of Chagas disease vectors in the Americas. Rio de Janeiro: Fiocruz; 1998. p. 537-60.,8484. Reyes M. Panstrongylus geniculatus Latreille 1811 (Hemiptera: Reduviidae: Triatominae), vector de la enfermedad de Chagas en el ambiente domiciliario del centro-norte de Venezuela. Rev Biomed. 2009; 20: 180-205.,8585. Abad-Franch F, Lima M, Sarquis O, Gurgel R, Sánchez M, Calzada J, et al. On palms, bugs, and Chagas disease in the Americas. Acta Trop. 2015; 151: 126-41. http://dx.doi.org/10.1016/j.actatropica.2015.07.005.
http://dx.doi.org/10.1016/j.actatropica....
Interestingly, it was reported that the species displays entomophagic behavior towards moths (Eacles spp.) in the forests of French Guyana for the first time, which confirms its versatility for survival in environments with low food availability.8686. Garrouste R. La première observation in natura de l'entomophagie de Panstrongylus geniculatus (Latreille 1811) hématophage vecteur de la maladie de Chagas (Hemiptera: Reduviidae). Ann Soc Entomol Fr (NS). 2009; 45(3): 302-4. https://doi.org/10.1080/00379271.2009.10697614.
https://doi.org/10.1080/00379271.2009.10...

Although the presence of P. geniculatus has been recorded in 18 countries, the recent availability of predictive maps can produce a robust summary of its distribution and show its spatial variation so that regions with a high probable risk of vector transmission and transmission through food contamination can be identified.8787. Bender A, Python A, Lindsay S, Golding N, Moyes C. Modelling geospatial distributions of the triatomine vectors of Trypanosoma cruzi in Latin America. PLoS Negl Trop Dis. 2020; 14(8): e0008411. http://dx.doi.org/10.1371/journal.pntd.0008411.
http://dx.doi.org/10.1371/journal.pntd.0...

Genetic diversity in P. geniculatus - The Panstrongylus genus is classified as belonging to the Triatomini, a monophyletic tribe. However, the phylogenetic relationships inside this group are far to be cleared because current knowledge is limited and messy.33. Monteiro F, Weirauch C, Felix M, Lazoski C, Abad-Franch F. Evolution, systematics, and biogeography of the Triatominae, vectors of Chagas disease. Adv Parasitol. 2018; 99: 265-344. https://doi.org/10.1016/bs.apar.2017.12.002.
https://doi.org/10.1016/bs.apar.2017.12....
The Triatomini tribe is divided into three lineages: T. dispar, North American, and South American lineages. Panstrongylus is included in the Antillean Triatoma + Panstrongylus clade within the North American lineage. Three groups were tentatively distinguished in the Panstrongylus subclade, but only one of them includes P. geniculatus and its closest relatives P. mitarakaensis, P. martinezorum;33. Monteiro F, Weirauch C, Felix M, Lazoski C, Abad-Franch F. Evolution, systematics, and biogeography of the Triatominae, vectors of Chagas disease. Adv Parasitol. 2018; 99: 265-344. https://doi.org/10.1016/bs.apar.2017.12.002.
https://doi.org/10.1016/bs.apar.2017.12....
it also includes a set of south Amazonian species as P. lutzi (and its synonym P. sherlocki), P. lenti, P. diasi, P. guentheri and P. tupynambai.99. Lent H, Wygodzinsky P. Revision of the Triatominae (Hemiptera: Reduviidae), and their significance as vectors of Chagas disease. Bull Am Museum Nat Hist. 1979; 163(3): 123-520. http://hdl.handle.net/2246/1282.
http://hdl.handle.net/2246/1282...
,1717. Patterson J, Barbosa S, Feliciangeli M. On the genus Panstrongylus Berg 1879: evolution, ecology and epidemiological significance. Acta Trop. 2009; 110(2-3): 187-99. http://dx.doi.org/10.1016/j.actatropica.2008.09.008.
http://dx.doi.org/10.1016/j.actatropica....
,2323. Bérenger J, Blanchet D. A new species of the genus Panstrongylus from French Guiana (Heteroptera; Reduviidae; Triatominae). Mem Inst Oswaldo Cruz. 2007; 102(6): 733-6. https://doi.org/10.1590/S0074-02762007005000088.
https://doi.org/10.1590/S0074-0276200700...
,2424. Ayala L. Una nueva especie de Panstrongylus Berg de Venezuela (Hemiptera: Reduviidae, Triatominae). Entomotropica. 2009; 24(3): 105-9.,8888. Barrett T. Advances in triatomine bug ecology in relation to Chagas disease. In K Harris, org. Advances in disease vector research. New York: Springer-Verlag; 1991. p. 143-76.,8989. Jurberg J, Carcavallo R, Lent H. Panstrongylus sherlocki sp. n. do estado da Bahia, Brasil (Hemiptera, Reduviidae, Triatominae). Entomol Vect. 2001; 8(2): 261-74.

Regarding karyotype variations in Panstrongylus species, it has been established that the species (P. chinai, P. geniculatus, P. lignarius, P. rufotuberculatus, P. tupynambai, P. herreri) have 20 autosomes (except P. megistus that has 18 autosomes), and X1X2Y chromosomes for males and X1X1X2X2 for females. In a study, three clusters were defined based on the C-band pattern and meiotic chromosomal behavior where P. geniculatus was not located in any of the groupings because it shares characteristics with each group. Consequently, the authors proposed that P. geniculatus should be considered as a complex of species comprising at least two different species because of its high chromosomal variability, wide distribution, and high phenotypic variation;1818. Crossa R, Hernández M, Caraccio M, Rose V, Valente S, Valente V, et al. Chromosomal evolution trends of the genus Panstrongylus (Hemiptera, Reduviidae), vectors of Chagas disease. Infect Genet Evol. 2002; 2(1): 47-56. https://doi.org/10.1016/S1567-1348(02)00063-1.
https://doi.org/10.1016/S1567-1348(02)00...
molecular evidence, however, is needed to confirm this hypothesis.

A Venezuelan study conducted a genetic variability analysis on P. geniculatus using Cytb as the molecular marker because it is extensively used to determine genetic polymorphisms in triatomines. The results showed that this marker is useful for describing genetic heterogeneity in P. geniculatus and revealed spatial and genetic patterns that agree with domiciliation processes for this species, but it could not resolve the evolutionary relationships. Even though this marker is informative about the population structure, other genes must be evaluated to study the genetic variability.9090. Nakad-Bechara C, Londoño J, Segovia M, León M, Martínez P, Rodríguez R, et al. Genetic variability of Panstrongylus geniculatus (Reduviidae: Triatominae) in the Metropolitan District of Caracas, Venezuela. Infect Genet Evol. 2018; 66: 236-44. http://dx.doi.org/10.1016/j.meegid.2018.09.011.
http://dx.doi.org/10.1016/j.meegid.2018....

A very recent study used DNA markers and molecular data to study genetic diversity in P. geniculatus with the aim obtaining information about the processes that have shaped genetic diversity in this species.9191. Caicedo-Garzón V, Salgado-Roa F, Sánchez-Herrera M, Hernández C, Arias-Giraldo L, García L, et al. Genetic diversification of Panstrongylus geniculatus (Reduviidae: Triatominae) in northern South America. PLoS One. 2019; 14(10): e0223963. https://doi.org/10.1371/journal.pone.0223963.
https://doi.org/10.1371/journal.pone.022...
Using mitochondrial DNA (mtDNA) fragments, 16S rRNA and Cytb, the authors reconstructed a phylogenetic tree that showed that P. geniculatus from Colombia and Venezuela form a monophyletic species with four clades concordant with its geographic distribution, which is partly explained by the Andes uplift (Fig. 4). However, other factors, including anthropogenic and eco-epidemiological effects must also be investigated to explain the existence of recent geographic P. geniculatus lineages. The authors also reconstructed the relationships within the Panstrongylus genus using various genetic markers. Using mtDNA markers (16S, ND4 and Cytb), they detected two clades: one includes P. lutzi and P. tupynambai, which is the sister clade of P. geniculatus (geniculatus group), and the other one includes P. lignarius and P. megistus, which represent the sister clade of P. rufotuberculatus, P. howardi and P. chinai (megistus group).

Fig. 4:
genetic differentiation of Panstrongylus geniculatus in Colombia and Venezuela reported by Caicedo-Garzón et al.9191. Caicedo-Garzón V, Salgado-Roa F, Sánchez-Herrera M, Hernández C, Arias-Giraldo L, García L, et al. Genetic diversification of Panstrongylus geniculatus (Reduviidae: Triatominae) in northern South America. PLoS One. 2019; 14(10): e0223963. https://doi.org/10.1371/journal.pone.0223963.
https://doi.org/10.1371/journal.pone.022...

To conclude, further studies using more genetic markers and genomic approaches, along with widespread sampling from different geographic locations are needed to unravel the inter- and intra-specific relationships of the Panstrongylus genus, and specially for P. geniculatus considering its domiciliation reports, high infection rates with T. cruzi and incrimination in oral outbreaks of Chagas disease in Colombia and Venezuela. All this knowledge is relevant for the development of control and surveillance strategies for Chagas disease vectors.

Epidemiology, intrusion, colonisation of human habits and possible role in the oral transmission of T. cruzi

Evidence of dwelling intrusion by P. geniculatus in Latin America - Although P. geniculatus is considered a species of wild habits, several cases of intrusion into homes have been reported in different Latin American countries in recent decades. This new scenario implies an increased risk of transmission in endemic and non-endemic areas of Chagas disease, either by direct contact or via food contamination.9292. Tovar C, Negrete J, González C, León C, Ortiz M, Chacón J, et al. New scenarios of Chagas disease transmission in northern Colombia. J Parasitol Res. 2017; 3943215. https://doi.org/10.1155/2017/3943215.
https://doi.org/10.1155/2017/3943215...
,9393. Hernández C, Salazar C, Brochero H, Teherán A, Buitrago L, Vera M, et al. Untangling the transmission dynamics of primary and secondary vectors of Trypanosoma cruzi in Colombia: parasite infection, feeding sources and discrete typing units. Parasit Vectors. 2016; 9(1): 620. https://doi.org/10.1186/s13071-016-1907-5
https://doi.org/10.1186/s13071-016-1907-...
Table III shows 45 registered reports of intrusion by adult P. geniculatus in Bolivia, Brazil, Colombia, Peru, Surinam and Venezuela. Despite growing awareness of the relevance of the transmission dynamics of P. geniculatus, the drivers of house invasion remain poorly understood. However, it was observed that invasion by this species decreased with higher landscape disturbance levels and in hotter-day municipalities and increased somewhat in more places with intermediate disturbance, peaking in municipalities with average rainfall.9494. Brito R, Gorla D, Diotaiuti L, Gomes A, Souza R, Abad-Franch F. Drivers of house invasion by sylvatic Chagas disease vectors in the Amazon-Cerrado transition: A multi-year, state-wide assessment of municipality-aggregated surveillance data. PLoS Negl Trop Dis. 2017; 11(11): e0006035. https://doi.org/10.1371/journal.
https://doi.org/10.1371/journal...

TABLE III
Panstrongylus geniculatus adult specimens reported inside human dwellings in Latin American countries, without evidence of colonization (eggs, nymphs and exuviae)

It is accepted that the increased interactions occurring between triatomines and humans are mainly related to losses in vegetation cover and increases in urban and rural populations invading natural ecotopes. Most of these intrusions occur at night when P. geniculatus fly in from wild environments to inhabited areas under the attraction of artificial lighting in search of food.8484. Reyes M. Panstrongylus geniculatus Latreille 1811 (Hemiptera: Reduviidae: Triatominae), vector de la enfermedad de Chagas en el ambiente domiciliario del centro-norte de Venezuela. Rev Biomed. 2009; 20: 180-205. The author concluded that this occurred regardless of the type of housing, and that the invasion increased when high numbers of domestic animals were present and the distance to the forest was small.8484. Reyes M. Panstrongylus geniculatus Latreille 1811 (Hemiptera: Reduviidae: Triatominae), vector de la enfermedad de Chagas en el ambiente domiciliario del centro-norte de Venezuela. Rev Biomed. 2009; 20: 180-205. Recently, 11 P. geniculatus specimens were captured in the city of Bucaramanga, a Colombian neighborhood, of which five out of nine tested were positive for T. cruzi (56%), which drew attention to the risk of infection by this vector settling in the periphery of homes and adjacent to the natural ecotopes where its life cycle in the wild occurs.117117. Reyes M, Torres A, Esteban L, Flórez M, Angulo V. Riesgo de transmisión de la enfermedad de Chagas por intrusión de triatominos y mamíferos silvestres en Bucaramanga, Santander, Colombia. Biomédica. 2017; 37(1): 68-78. http://dx.doi.org/10.7705/biomedica.v37i1.3051.
http://dx.doi.org/10.7705/biomedica.v37i...

The ability of P. geniculatus to fly up to 2 km away has been verified.125125. Pifano F. El potencial enzoótico silvestre del complejo ecológico Schizotrypanum cruzi - Didelphis marsupialis - Panstrongylus geniculatus y sus incursiones a la vivienda humana del valle de Caracas - Venezuela. Bol Acad Cienc Fis Mat Nat. 1986; 46: 143-4. In other study, was reported that P. geniculatus is attracted to artificial light sources. These researchers installed a light trap positioned 45 m above sea level in a wild area of Manaus in the Amazonas State of Brazil, and they operated it monthly for three consecutive nights over the course of a year. They found that the most commonly captured triatomine was P. geniculatus (38 individuals) in addition to six other species.132132. Castro M, Barrett T, Santos W, Abad-Franch F, Rafael J. Attraction of Chagas disease vectors (Triatominae) to artificial light sources in the canopy of primary Amazon rainforest. Mem Inst Oswaldo Cruz. 2010; 105(8): 1061-4. http://dx.doi.org/10.1590/s0074-02762010000800019.
http://dx.doi.org/10.1590/s0074-02762010...
Likewise, Jacome et al., determined the risk associated with the dispersive nocturnal flights of sylvatic triatomines by installing artificial lights in a model house in the northeastern plains of Colombia and concluded that this nocturnal dynamic poses a risk for the domestic introduction of discrete typing units (DTUs) of T. cruzi associated with sylvatic transmission foci.133133. Jácome-Pinilla D, Hincapié-Peñaloza E, Ortiz M, Ramírez J, Guhl F, Molina J. Risks associated with dispersive nocturnal flights of sylvatic Triatominae to artificial lights in a model house in the northeastern plains of Colombia. Parasit Vectors. 2015; 8: 600. https://dx.doi.org/10.1186/s13071-015-1209-3.
https://dx.doi.org/10.1186/s13071-015-12...

Evidence of intradomiciliary and peridomiciliary colonisation of P. geniculatus in Latin America

Although P. geniculatus is registered as an intrusive wild species in some regions of the Americas, in other regions it is registered as a species capable of colonising human dwellings. These differences in the behavior of P. geniculatus probably reflect the genetic differences in this species across Latin American populations. Generally, the reported number of P. geniculatus nymphs associated with human dwellings varies, and Table IV lists nine publications that have reported on the presence of P. geniculatus eggs and nymphs. Furthermore, two intradomiciled adults and three peridomiciled nymphs in Muñecas, La Paz (Bolivia) were recorded.4848. Depickère S, Durán P, López R, Chávez T. Presence of intradomicile colonies of the triatomine bug Panstrongylus rufotuberculatus in Muñecas, La Paz, Bolivia. Acta Trop. 2011; 117(2): 97-100. https://doi.org/10.1016/j.actatropica.2010.10.005.
https://doi.org/10.1016/j.actatropica.20...

TABLE IV
Registration of Panstrongylus geniculatus adults, nymphs and eggs inside houses or peridomiciles in Latin American countries

Fifteen pigsties were examined in Muana, Pará State, Brazil, contained 207 females, 168 males, 2 N5, 7 NIII, 16 NII, 28 NI stages and 385 unhatched eggs, thereby evidencing a domiciliation process for P. geniculatus. In 10 of the 15 houses located up to a 10 m distant from the pigsties, 21 adults were collected in total.134134. Valente V, Valente S, Noireau F, Carrasco H, Miles M. Chagas disease in the Amazon Basin: Association of Panstrongylus geniculatus (Hemiptera: Reduviidae) with domestic pigs. J Med Entomol. 1998; 35(2): 99-103. https://doi.org/10.1093/jmedent/35.2.99.
https://doi.org/10.1093/jmedent/35.2.99...

The presence of P. geniculatus adults in 80 homes in Amalfi, Antioquia, Colombia, but only in one of the homes did they find nymphal stages of the insect was recorded.4040. Wolff M, Castillo D. Evidencias de domesticación y aspectos biológicos de Panstrongylus geniculatus (Latreille, 1811) (Hemiptera: Reduviidae). Acta Entomol Chile. 2000; 24: 77-83. Thirty-seven adults and a nymph of P. geniculatus in the intra-domicile of the studied dwellings in Atlántico, Colombia were reported.135135. Maestre-Serrano R, Eyes-Escalante M. Actualización de la presencia y distribución de triatominos en el departamento del Atlántico-Colombia: 2003-2010. Bol Malariol Salud Amb. 2012; 52(1): 125-8. The presence of adults and nymphs in development stages IV and V of P. geniculatus in the intra-domiciles in six of seven villages in the municipality of Tamara in Casanare Department (Colombia) was recorded.136136. Montenegro D, Vera M, Zuleta L, Llanos I, Junqueira A. Estrategia para determinar la línea base en áreas de interrupción vectorial de la enfermedad de Chagas. Rev Panam Salud Publica. 2016; 39(6): 341-51.

Two males and one female P. geniculatus, 5NV, 8NIV, 3NIII, and 1NII stages, and seven eggs were captured in the tunnel of a rat (Rattus rattus) inside a house in Miranda, Venezuela. All the triatomines were abundantly blood-fed, with the exception of one recently molted male and one female, whose emergences were confirmed by the presence of NV-stage exuviae. Fecal examination of the three NV-stages and an adult male revealed the presence of T. cruzi.137137. Reyes M, Rodríguez A. Domiciliation of selvatic Chagas disease vector Panstrongylus geniculatus (Latreille, 1811) (Triatominae: Reduviidae) in Venezuela. Trans R Soc Trop Med Hyg. 2000; 94(5): 508. https://doi.org/10.1016/s0035-9203(00)90068-3.
https://doi.org/10.1016/s0035-9203(00)90...
In three houses examined in El Guamito, Lara State, Venezuela, were found one female, six N5-, two NIII- and two N2-stages and an overall T. cruzi infection rate of 9%.138138. Feliciangeli M, Carrasco H, Patterson J, Suárez B, Martínez C, Medina M. Mixed domestic infestation by Rhodnius prolixus Stal, 1859 and Panstrongylus geniculatus (Latreille, 1811), vector incrimination, and seroprevalence for Trypanosoma cruzi among inhabitants in El Guamito, Lara state, Venezuela. Am J Trop Med Hyg. 2004; 71(4): 501-5. https://doi.org/10.4269/ajtmh.2004.71.501.
https://doi.org/10.4269/ajtmh.2004.71.50...
In another study in the same state, P. geniculatus was found in 11 homes, registering 136 adults and two NIII stages, with a colonisation index of 18.18% and a 5.07% infection rate for T. cruzi.139139. Rodríguez-Bonfante C, Amaro A, García M, Wohlert L, Guillén P, García R, et al. Epidemiología de la enfermedad de Chagas en el municipio Andrés Eloy Blanco, Lara, Venezuela: infestación triatomínica y seroprevalencia en humanos. Cad Saude Publica. 2007; 23(5): 1133-40. https://doi.org/10.1590/S0102-311X2007000500015.
https://doi.org/10.1590/S0102-311X200700...
3390 adult P. geniculatus specimens, 26 NV, 71 NIV and 27 NIII stages were captured in the Metropolitan District of Caracas between 2007 and 2013, of which 59,5% carried T. cruzi. The authors warned that dramatic modifications to the surrounding natural habitats had led to the establishment of a T. cruzi urban enzootic cycle, resulting in a high risk of transmission of Chagas disease in this capital city.140140. Carrasco H, Segovia M, Londoño J, Ortegoza J, Rodríguez M, Martínez C. Panstrongylus geniculatus and four other species of triatomine bug involved in the Trypanosoma cruzi enzootic cycle: high risk factors for Chagas disease transmission in the Metropolitan District of Caracas, Venezuela. Parasit Vectors. 2014; 7(602): 1-5. https://doi.org/10.1186/s13071-014-0602-7.
https://doi.org/10.1186/s13071-014-0602-...

T. cruzi isolates from P. geniculatus, R. rattus and from humans infected during an orally-acquired Chagas disease outbreak in a non-endemic region of Venezuela belong to a same T. cruzi I genotype (TcId). The similarity in the parasite isolates from the three patients affected by the urban oral outbreak, the triatomine, and the rat captured at the guava juice preparation site allowed the authors to suggest that the source of infection was common among these persons and the vector, providing indirect evidence of P. geniculatus domiciliation in this region.141141. Díaz-Bello Z, Thomas M, López M, Zavala-Jasper R, Noya O, Alarcón de Noya B, et al. Trypanosoma cruzi genotyping supports a common source of infection in a school-related oral outbreak of acute Chagas disease in Venezuela. Epidemiol Infect. 2014; 142(1): 156-62. https://doi.org/10.1017/S0950268813000757.
https://doi.org/10.1017/S095026881300075...

The colonisation capacity of P. geniculatus has been studied under laboratory conditions. One such study reported a ro/b index of 0.77, but concluded that as a “K” strategist with a low reproduction rate and a prolonged generational time, it was unlikely that P. geniculatus was an important disease vector at the household level, a finding that does not presently reflect the epidemiological importance of the species.4141. Cabello D, Galíndez Girón I. Vital Statistics of Panstrongylus geniculatus (Latreille 1811) (Hemiptera: Reduviidae) under experimental conditions. Mem Inst Oswaldo Cruz. 1998; 93(2): 257-62. http://dx.doi.org/10.1590/S0074-02761998000200024.
http://dx.doi.org/10.1590/S0074-02761998...
Nevertheless, another study compared the results they obtained from P. geniculatus (ro/b = 0.74) with two species known for their high colonising capacity, Rhodnius prolixus (0.74) and Triatoma infestans (0.65), and concluded that P. geniculatus has a remarkable colonising capacity, which should alert the relevant institutions to the risk presented by this species and the need to design new control strategies aimed at the wild species that in recent decades have been increasingly reported as having home intrusion and colonisation behavior.4444. Rabinovich J, Feliciangeli M. Vital statistics of Triatominae (Hemiptera: Reduviidae) under laboratory conditions: IV. Panstrongylus geniculatus. J Med Entomol. 2015; 52(5): 797-805. https://doi.org/10.1093/jme/tjv112.
https://doi.org/10.1093/jme/tjv112...

The presence of sexual dimorphism was an indicator of home adaptation and the authors concluded that populations of P. geniculatus from Caracas, Venezuela, are morphologically adapted to home environments.2020. Aldana E, Heredia E, Avendaño F, Lizano E, Concepción J, Bonfante R, et al. Análisis morfométrico de Panstrongylus geniculatus de Caracas, Venezuela. Biomédica. 2011; 31(1): 108-17. https://doi.org/10.7705/biomedica.v31i1.341
https://doi.org/10.7705/biomedica.v31i1....
That the ability of the species to adapt to different environments in a few generations as was recently confirmed by Nakad-Bechara et al.9090. Nakad-Bechara C, Londoño J, Segovia M, León M, Martínez P, Rodríguez R, et al. Genetic variability of Panstrongylus geniculatus (Reduviidae: Triatominae) in the Metropolitan District of Caracas, Venezuela. Infect Genet Evol. 2018; 66: 236-44. http://dx.doi.org/10.1016/j.meegid.2018.09.011.
http://dx.doi.org/10.1016/j.meegid.2018....
and poses a future risk to humans and should alert health institutions, especially taking into account the possible new scenarios of climate change and the specific anthropic processes of deforestation and landscape fragmentation.

P. geniculatus and oral transmission of T. cruzi

Over the last two decades, the oral form of disease transmission has changed from being a rare and unusual event to a public health concern after causing numerous deaths.142142. Nicholls R, Cucunubá Z, Knudson A, Flórez A, Montilla M, Puerta C, et al. Enfermedad de Chagas aguda en Colombia, una entidad poco sospechada. Informe de 10 casos presentados en el periodo 2002 a 2005. Biomédica. 2007; 27(1): 8-17. https://doi.org/10.7705/biomedica.v27i1.244.
https://doi.org/10.7705/biomedica.v27i1....
,143143. Rueda K, Trujillo J, Carranza J, Vallejo G. Transmisión oral de Trypanosoma cruzi: una nueva situación epidemiológica de la enfermedad de Chagas en Colombia y otros países suramericanos. Biomédica. 2014; 34(4): 631-41. https://doi.org/10.7705/biomedica.v34i4.2204.
https://doi.org/10.7705/biomedica.v34i4....

The difficulty in obtaining direct evidence incriminating the vector species responsible for the oral transmission of T. cruzi, is related to the fact that oral Chagas disease outbreaks occur several days after food contamination. Despite this difficulty, in some reported cases strong suspicions exist about the role of P. geniculatus in this transmission mechanism, because it has been observed as an abundant species in the area of the outbreak and it has been found invading the houses where contaminated food was prepared and, although in some cases the captured insects did not carry T. cruzi parasites, in other cases high levels of natural infection were observed. Table V lists 11 publications that report indirect evidence involving P. geniculatus in the oral transmission of T. cruzi.

TABLE V
Cases where Panstrongylus geniculatus has been reported as a highly probable transmitter of oral Trypanosoma cruzi infection in Latin America

Venezuela has experienced the most numerous and acute cases of parasite transmission by the oral route, with the source of infection generally being the intake of juices contaminated with triatomine feces. Infections have been reported in greater Caracas and the states of Falcon, Merida, Tachira, and Vargas where P. geniculatus has been the species linked with most of the outbreaks. Because it is the most abundant species in these localities, it has high T. cruzi infection rates and has been observed to defecate while returning to its shelter after feeding 128128. Carrasco H, Torrellas A, García C, Segovia M, Feliciangeli M. Risk of Trypanosoma cruzi I (Kinetoplastida: Trypanosomatidae) transmission by Panstrongylus geniculatus (Hemiptera: Reduviidae) in Caracas (Metropolitan District) and neighboring States, Venezuela. Int J Parasitol. 2005; 35(13): 1379-84. https://doi.org/10.1016/j.ijpara.2005.05.003.
https://doi.org/10.1016/j.ijpara.2005.05...
,140140. Carrasco H, Segovia M, Londoño J, Ortegoza J, Rodríguez M, Martínez C. Panstrongylus geniculatus and four other species of triatomine bug involved in the Trypanosoma cruzi enzootic cycle: high risk factors for Chagas disease transmission in the Metropolitan District of Caracas, Venezuela. Parasit Vectors. 2014; 7(602): 1-5. https://doi.org/10.1186/s13071-014-0602-7.
https://doi.org/10.1186/s13071-014-0602-...
,152152. Alarcón de Noya B, Díaz-Bello Z, Colmenares C, Ruiz-Guevara R, Mauriello L, Muñoz A, et al. Update on oral chagas disease outbreaks in Venezuela: Epidemiological, clinical and diagnostic approaches. Mem Inst Oswaldo Cruz. 2015; 110(3): 377-86. http://dx.doi.org/10.1590/0074-02760140285.
http://dx.doi.org/10.1590/0074-027601402...

In the municipality of Chacao in Caracas in 2007, 103 people from a school were infected with T. cruzi, and of those infected, 19% needed hospitalisation and one child died. The infection source was juice made in a house where T. cruzi-infected P. geniculatus insects were captured.149149. Alarcón de Noya B, Díaz-Bello Z, Colmenares C, Ruiz-Guevara R, Mauriello L, Zavala-Jaspe R, et al. Large urban outbreak of orally acquired acute Chagas disease at a school in Caracas, Venezuela. J Infect Dis. 2010; 201(9): 1308-15. http://dx.doi.org/10.1086/651608.
http://dx.doi.org/10.1086/651608...
During 2009, another outbreak occurred in a school environment that affected 82 people, from which three children and one adult died. Again, the evidence from the case indicates that the infection source was juice contaminated with the feces of P. geniculatus.150150. Suárez J, de Suárez C, Alarcón de Noya B, Espinosa R, Chiurillo M, Villaroel A, et al. Enfermedad de Chagas sistémico en fase aguda por transmisión oral: diagnóstico integral de un caso autopsiado. Gac Med Caracas. 2010; 118(3): 212-22.

In Colombia, several cases of infection by oral transmission have occurred in areas with low endemicity and presence of domiciled vectors. Thus, wild vectors such as P. geniculatus have become important in relation to this mechanism of infection and may be associated with outbreaks related to oral transmission in several Colombian municipalities.153153. Ramírez J, Montilla M, Cucunubá Z, Floréz A, Zambrano P, Guhl F. Molecular epidemiology of human oral Chagas disease outbreaks in Colombia. PLoS Negl Trop Dis. 2013; 7(2): e2041. http://dx.doi/10.1371/journal.pntd.0002041.
http://dx.doi/10.1371/journal.pntd.00020...
In Lebrija, Santander, an acute case was presented, where ten infections and two deaths were reported.145145. Hernández L, Ramírez A, Cucunubá Z, Zambrano P. Brote de Chagas agudo en Lebrija, Santander, 2008. Revista del Observatorio de Salud Pública de Santander. 2009; 4(1): 28-36. A report on a new scenario for transmission in the department of Córdoba-Colombia in an area that was not considered to be a region at risk of T. cruzi transmission. This report was based on an acute case of the disease in which the patient did not present lesions on the skin or in the periocular region that indicated the bite of the insect.9292. Tovar C, Negrete J, González C, León C, Ortiz M, Chacón J, et al. New scenarios of Chagas disease transmission in northern Colombia. J Parasitol Res. 2017; 3943215. https://doi.org/10.1155/2017/3943215.
https://doi.org/10.1155/2017/3943215...

The transmission sources for two oral outbreaks were identified, one of them in the Colombian town of Restrepo, Meta. By epidemiological analysis, genotyping and allele identification of seven T. cruzi microsatellites in the samples obtained from patients, as well as insects and reservoirs implicated in the outbreaks, they determined that this outbreak was caused by fecal contamination of arepa and pineapple juices by P. geniculatus. Their distance analysis allowed them to observe the grouping of patients with insects rather than with the reservoirs. Their findings were further explained by recent housing construction in the outbreak area, which altered the natural habitat of P. geniculatus and caused its intrusion into homes.113113. Hernández C, Vera M, Cucunubá Z, Flórez C, Cantillo O, Buitrago L, et al. High-Resolution molecular typing of Trypanosoma cruzi in 2 large outbreaks of acute Chagas disease in Colombia. J Infect Dis. 2016; 214(8): 1252-5. https://doi.org/doi:10.1093/infdis/jiw360.
https://doi.org/10.1093/infdis/jiw360...

DTUs of T. cruzi detected in P. geniculatus

Natural infections of T. cruzi in P. geniculatus have been widely reported and quantified in different Latin American countries. Despite no clear trend, high rates of natural infection occur with this parasite, reaching 44% on average. Brazilian rates are 16.5%,154154. Valente V. Potential for domestication of Panstrongylus geniculatus (Latreille, 1811) (Liemiptera, Reduviidae, Triatominae) in the municipality of Muaná, Marajó Island, State of Pará, Brazil. Mem Inst Oswaldo Cruz. 1999; 94(1): 399-400. http://dx.doi.org/10.1590/S0074-02761999000700078.
http://dx.doi.org/10.1590/S0074-02761999...
50%,155155. Dario M, Lisboa C, Costa L, Moratelli R, Nascimento M, Costa L, et al. High Trypanosoma spp. diversity is maintained by bats and triatomines in Espírito Santo state, Brazil. PLoS One. 2017; 12(11): e0188412. https://doi.org/10.1371/journal.pone.0188412.
https://doi.org/10.1371/journal.pone.018...
4.7%156156. Ferro A, Sobral-Souza T, Vancine M, Muylaert R, de Abreu A, Pelloso S, et al. Spatial prediction of risk areas for vector transmission of Trypanosoma cruzi in the State of Paraná, southern Brazil. PLoS Negl Trop Dis. 2018; 12(10): e0006907. https://doi.org/10.1371/journal.pntd.0006907.
https://doi.org/10.1371/journal.pntd.000...
and 27.3%.157157. Dario M, Andrade T, dos Santos C, Fux B, Brandão A, Falqueto A. Molecular characterization of Trypanosoma cruzi samples derived from Triatoma vitticeps and Panstrongylus geniculatus of the Atlantic rainforest, southeast Brazil. Parasite. 2018; 25: 59. https://doi.org/10.1051/parasite/2018060.
https://doi.org/10.1051/parasite/2018060...
The Trinidadian rate is 42.5%,8080. Omah-Maharaj I. Studies on vectors of Trypanosoma cruzi in Trinidad, West Indies. Med Vet Entomol. 1992; 6(2): 115-20. https://doi.org/10.1111/j.1365-2915.1992.tb00586.x.
https://doi.org/10.1111/j.1365-2915.1992...
the Colombian rates are 50%,4040. Wolff M, Castillo D. Evidencias de domesticación y aspectos biológicos de Panstrongylus geniculatus (Latreille, 1811) (Hemiptera: Reduviidae). Acta Entomol Chile. 2000; 24: 77-83. 70.6%9393. Hernández C, Salazar C, Brochero H, Teherán A, Buitrago L, Vera M, et al. Untangling the transmission dynamics of primary and secondary vectors of Trypanosoma cruzi in Colombia: parasite infection, feeding sources and discrete typing units. Parasit Vectors. 2016; 9(1): 620. https://doi.org/10.1186/s13071-016-1907-5
https://doi.org/10.1186/s13071-016-1907-...
and 58.3%,118118. Ayala C, Hernández C, Eyes M, Romero L, Álvarez R, Blanco P. Detección de infección natural por Trypanosoma cruzi (Trypanosomatidae) en triatominos del municipio de Colosó, Colombia. Acta Biol Col. 2019; 24(1): 180-4. http://dx.doi.org/10.15446/abc.v24n1.72306.
http://dx.doi.org/10.15446/abc.v24n1.723...
the Venezuelan rates are 20%138138. Feliciangeli M, Carrasco H, Patterson J, Suárez B, Martínez C, Medina M. Mixed domestic infestation by Rhodnius prolixus Stal, 1859 and Panstrongylus geniculatus (Latreille, 1811), vector incrimination, and seroprevalence for Trypanosoma cruzi among inhabitants in El Guamito, Lara state, Venezuela. Am J Trop Med Hyg. 2004; 71(4): 501-5. https://doi.org/10.4269/ajtmh.2004.71.501.
https://doi.org/10.4269/ajtmh.2004.71.50...
and 76.1%,128128. Carrasco H, Torrellas A, García C, Segovia M, Feliciangeli M. Risk of Trypanosoma cruzi I (Kinetoplastida: Trypanosomatidae) transmission by Panstrongylus geniculatus (Hemiptera: Reduviidae) in Caracas (Metropolitan District) and neighboring States, Venezuela. Int J Parasitol. 2005; 35(13): 1379-84. https://doi.org/10.1016/j.ijpara.2005.05.003.
https://doi.org/10.1016/j.ijpara.2005.05...
the Peruvian rate is 50%,120120. Padilla C, Alvarado U, Ventura G, Luna-Caipo D, Suárez M, Tuñoque J, et al. Detección de unidades discretas de tipificación de Trypanosoma cruzi en triatominos recolectados en diferentes regiones naturales de Perú. Biomédica. 2017; 37(2): 167-79. https://doi.org/10.7705/biomedica.v37i0.3559.
https://doi.org/10.7705/biomedica.v37i0....
and the Bolivian rate is 62.5%.5151. Rojas M, Pinazo M, García L, Arteaga M, Uriona L, Gamboa S, et al. Trypanosoma cruzi infected Panstrongylus geniculatus and Rhodnius robustus adults invade households in the Tropics of Cochabamba region of Bolivia. Parasit Vectors. 2016; 9(158): 1-6. https://doi.org/10.1186/s13071-016-1445-1
https://doi.org/10.1186/s13071-016-1445-...

Currently, seven DTUs, TcI to TcVI and T.c.bat, are known to circulate in the vectors in different proportions.158158. Zingales B, Andrade S, Briones M, Campbell D, Chiari E, Fernandes O, et al. A new consensus for Trypanosoma cruzi intraspecific nomenclature: second revision meeting recommends TcI to TcVI. Mem Inst Oswaldo Cruz. 2009; 104(7): 1051-4. https://doi.org/10.1590/s0074-02762009000700021.
https://doi.org/10.1590/s0074-0276200900...
,159159. Marcili A, Lima L, Cavazzana Jr, Junqueira A, Veludo H, Da Silva F, et al. A new genotype of Trypanosoma cruzi associated with bats evidenced by phylogenetic analyses using SSU rDNA, cytochrome b and Histone H2B genes and genotyping based on ITS1 rDNA. Parasitology. 2009; 136(6): 641-55. https://doi.org/10.1017/S0031182009005861.
https://doi.org/10.1017/S003118200900586...
The T. cruzi DTUs in P. geniculatus correspond to six of the seven described DTUs (TcI, TcII, TcIII, TcIV, TcV and TcVI), the geographic distributions of which in America for P. geniculatus are shown in Fig. 5. In Bolivia, insects infected with TcI and TcIII have been reported inside homes.5151. Rojas M, Pinazo M, García L, Arteaga M, Uriona L, Gamboa S, et al. Trypanosoma cruzi infected Panstrongylus geniculatus and Rhodnius robustus adults invade households in the Tropics of Cochabamba region of Bolivia. Parasit Vectors. 2016; 9(158): 1-6. https://doi.org/10.1186/s13071-016-1445-1
https://doi.org/10.1186/s13071-016-1445-...
In Brazil, insects infected with TcII and TcIII have been identified.157157. Dario M, Andrade T, dos Santos C, Fux B, Brandão A, Falqueto A. Molecular characterization of Trypanosoma cruzi samples derived from Triatoma vitticeps and Panstrongylus geniculatus of the Atlantic rainforest, southeast Brazil. Parasite. 2018; 25: 59. https://doi.org/10.1051/parasite/2018060.
https://doi.org/10.1051/parasite/2018060...
In Colombia, the transmission dynamics of the primary and secondary vectors in six departments (Antioquia, Cesar, Guajira, Huila, Meta, and Norte de Santander) were studied and, with six circulating DTUs (TcI, TcII, TcIII, TcIV, TcV and TcVI). P. geniculatus was observed to be the species with the highest number of DTUs.9393. Hernández C, Salazar C, Brochero H, Teherán A, Buitrago L, Vera M, et al. Untangling the transmission dynamics of primary and secondary vectors of Trypanosoma cruzi in Colombia: parasite infection, feeding sources and discrete typing units. Parasit Vectors. 2016; 9(1): 620. https://doi.org/10.1186/s13071-016-1907-5
https://doi.org/10.1186/s13071-016-1907-...
,160160. Messenger LA, Ramírez JD, Llewellyn MS, Guhl F, Miles MA. Importation of hybrid human-associated Trypanosoma cruzi strains of southern South American origin, Colombia. Emerg Infect Dis. 2016; 22(8): 1452-5. While TcI, TcIII and TcIV genotypes were isolated from the insects collected in the Colombian department of Casanare,133133. Jácome-Pinilla D, Hincapié-Peñaloza E, Ortiz M, Ramírez J, Guhl F, Molina J. Risks associated with dispersive nocturnal flights of sylvatic Triatominae to artificial lights in a model house in the northeastern plains of Colombia. Parasit Vectors. 2015; 8: 600. https://dx.doi.org/10.1186/s13071-015-1209-3.
https://dx.doi.org/10.1186/s13071-015-12...
insects from Peru, Ecuador and French Guyana were only infected with TcI.120120. Padilla C, Alvarado U, Ventura G, Luna-Caipo D, Suárez M, Tuñoque J, et al. Detección de unidades discretas de tipificación de Trypanosoma cruzi en triatominos recolectados en diferentes regiones naturales de Perú. Biomédica. 2017; 37(2): 167-79. https://doi.org/10.7705/biomedica.v37i0.3559.
https://doi.org/10.7705/biomedica.v37i0....
,161161. Barnabé C, Brisse S, Tibayrenc M. Population structure and genetic typing of Trypanosoma cruzi, the agent of Chagas disease: a multilocus enzyme electrophoresis approach. Parasitology. 2000; 120(5): 513-26. https://doi.org/10.1017/s0031182099005661.
https://doi.org/10.1017/s003118209900566...
Last, TcI, TcIII and TcIV DTUs were identified in P. geniculatus collected from Venezuela.140140. Carrasco H, Segovia M, Londoño J, Ortegoza J, Rodríguez M, Martínez C. Panstrongylus geniculatus and four other species of triatomine bug involved in the Trypanosoma cruzi enzootic cycle: high risk factors for Chagas disease transmission in the Metropolitan District of Caracas, Venezuela. Parasit Vectors. 2014; 7(602): 1-5. https://doi.org/10.1186/s13071-014-0602-7.
https://doi.org/10.1186/s13071-014-0602-...

Fig. 5:
geographical distribution in America of Trypanosoma cruzi discrete typing units (DTUs) detected in Panstrongylus geniculatus.

Possible effects of climate change on P. geniculatus

Although controversy persists about the consequences of climate change on vector-transmitted infectious diseases, there is full consensus that the global temperatures are closely linked with the physiological processes of arthropod vectors.162162. Liang L, Gong P. Climate change and human infectious diseases: a synthesis of research findings from global and spatio-temporal perspectives. Environ Int. 2017; 103: 99-108. https://doi.org/10.1016/j.envint.2017.03.011.
https://doi.org/10.1016/j.envint.2017.03...
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https://doi.org/10.1890/08-0079.1...
Indeed, it has been shown that temperature and relative humidity can affect a vector insect by changing its original geographical distribution, altering the duration of its life cycle, or modifying its vector capacity, all which have consequences for the prevalence of infectious diseases.164164. Gage K, Burkot T, Eisen R, Hayes E. Climate and vector-borne diseases. Am J Prev Med. 2008; 35(5): 436-50. https://doi.org/10.1016/j.amepre.2008.08.030.
https://doi.org/10.1016/j.amepre.2008.08...

To date, several studies have aimed to establish the effect of environmental variables on triatomines; however, attention has been mainly directed to T. infestans and R. prolixus.165165. Roca M, Lazzari C. Effects of relative humidity on the haematophagous bug Triatoma infestans: hygropreference and eclosion success. J Insect Phys. 1994; 40(10): 901-7. https://doi.org/10.1016/0022-1910(94)90024-8.
https://doi.org/10.1016/0022-1910(94)900...
,166166. Luz C, Fargues J, Grunewald J. Development of Rhodnius prolixus (Hemiptera: Reduviidae) under constant and cyclic conditions of temperature and humidity. Mem Inst Oswaldo Cruz. 1999; 94(3): 403-9. http://dx.doi.org/10.1590/S0074-02761999000300022.
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,167167. Tamayo L, Guhl F, Vallejo G, Ramírez J. The effect of temperature increase on the development of Rhodnius prolixus and the course of Trypanosoma cruzi metacyclogenesis. PLoS Negl Trop Dis. 2018; 12(8): e0006735. https://doi.org/10.1371/journal.pntd.0006735.
https://doi.org/10.1371/journal.pntd.000...
No studies on P. geniculatus that assess the effect of climatic conditions on its life cycle or vector capacity have been reported under controlled laboratory conditions in the available databases. Only estimates of its potential distribution based on ecological niche modeling have been reported for some Latin American countries.

In Brazil, the geographic distribution of triatomine species in the Central West region was estimated and the climatic factors that influence their occurrence were analysed. The results indicate that among the variables analysed, temperature seasonality better explains the models of occurrence. The authors also reported that almost the entire region has the climatic conditions appropriate for at least one species and, according to the distribution maps, P. geniculatus was the most widespread species with the greatest potential for occurrence.168168. Pereira J, Almeida P, Sousa A, Paula A, Machado R, Gurgel-Gonçalves R. Climatic factors influencing triatomine occurrence in Central-West Brazil. Mem Inst Oswaldo Cruz. 2013; 108(3): 335-41. http://dx.doi.org/10.1590/S0074-02762013000300012.
http://dx.doi.org/10.1590/S0074-02762013...
In Venezuela, the possible effects of climate change on the potential distribution of five species (Eratyrus mucronatus, P. geniculatus, T. maculata, R. robustus, and R. prolixus) were analysed. It was found that the variables best explaining the model were seasonal temperature (47.9%) and isometry (26.5%), and the highest relative vector competence values were those for R. prolixus (0.8) and P. geniculatus (0.1). However, they concluded that the possible future effects of climate change on the vulnerability of the Venezuelan P. geniculatus population show a slight downwards trend.169169. Ceccarelli S, Rabinovich J. Global climate change effects on Venezuela's vulnerability to Chagas disease is linked to the geographic distribution of five Triatomine species. J Med Entomol. 2015; 52(6): 1333-43. https://dx.doi.org/10.1093/jme/tjv119.
https://dx.doi.org/10.1093/jme/tjv119...

In Colombia, the geographical distribution of four species (P. geniculatus, R. pallescens, R. prolixus, and T. maculata) was estimated and identified a relationship between landscape structure and climate factors that influence their occurrence. According to the predictive maps on potential species distribution, the variables that best explain the model were altitude (26%) and precipitation seasonality (18%).1313. Parra-Henao G, Suárez-Escudero L, González-Caro S. Potential distribution of Chagas disease vectors (Hemiptera, Reduviidae, Triatominae) in Colombia, based on ecological niche modeling. J Trop Med. 2016; 1439090: 1-10. http://dx.doi.org/10.1155/2016/1439090.
http://dx.doi.org/10.1155/2016/1439090...
In light of the potential future geographical distributions, expressed as the suitability of a climate niche, several papers agree that P. geniculatus has a wide geographic distribution and has a greater distribution potential in possible climate change scenarios.1313. Parra-Henao G, Suárez-Escudero L, González-Caro S. Potential distribution of Chagas disease vectors (Hemiptera, Reduviidae, Triatominae) in Colombia, based on ecological niche modeling. J Trop Med. 2016; 1439090: 1-10. http://dx.doi.org/10.1155/2016/1439090.
http://dx.doi.org/10.1155/2016/1439090...
,168168. Pereira J, Almeida P, Sousa A, Paula A, Machado R, Gurgel-Gonçalves R. Climatic factors influencing triatomine occurrence in Central-West Brazil. Mem Inst Oswaldo Cruz. 2013; 108(3): 335-41. http://dx.doi.org/10.1590/S0074-02762013000300012.
http://dx.doi.org/10.1590/S0074-02762013...
,169169. Ceccarelli S, Rabinovich J. Global climate change effects on Venezuela's vulnerability to Chagas disease is linked to the geographic distribution of five Triatomine species. J Med Entomol. 2015; 52(6): 1333-43. https://dx.doi.org/10.1093/jme/tjv119.
https://dx.doi.org/10.1093/jme/tjv119...

We recently observed that when P. geniculatus colonies are kept at 30ºC, they have higher mortality and lower fertility than those kept at 26 and 28ºC (Unpublished observations). Thus, it seems possible that under natural conditions, this species probably moves to areas where temperatures and altitudes favor its survival.

In Conclusion

All 15 of the species in the Panstrongylus genus have been described using morphological characters. Some of them are phenotypically similar to P. geniculatus, but molecular methods have not yet been used to determine whether or not they are the same species.

Geometric morphometry studies have revealed a reduction in the size of the populations studied in the urban areas of Caracas (Venezuela), when compared with sylvatic populations. The size reduction has also been verified in laboratory-raised populations, when compared with sylvatic populations; hence, this size reduction is likely associated with domiciliation processes.

Life-cycle timing under laboratory conditions has been shown to be dependent on the experimental conditions employed, such as temperature, relative humidity and the food source for the colonies. Depending on the management of these variables, very heterogeneous data have been recorded from 149.5-531 days to even up to two years. Other studies using temperature conditions of 21-26ºC and relative humidity of 90-100% have reported life cycle durations of 269, 297, 275.8, 273 and 275.4 days (average, 278 days).

Although P. geniculatus has been found in 18 countries, the recently generated predictive maps can produce a robust summary of its distributions. They can map its spatial variation to identify regions where a high risk of vector transmission of T. cruzi and transmission through food contamination are likely.

Based on the karyotype characteristics of P. geniculatus, which has high chromosomal variability, P. geniculatus is proposed to be a complex of species containing at least two different ones. The use of Cytb as a molecular marker has revealed spatial and genetic patterns related to domiciliation processes. The phylogenetic reconstruction of P. geniculatus from Colombia and Venezuela, using 16S rRNA and Cytb, showed that it comprises four phylogenetic clades concordant with its geographical distribution and the Andes uplift. However, it will be necessary to use other molecular markers and genomic approaches to identify intraspecific variations related to domiciliation of this species, high infection rates with T. cruzi and incrimination in oral outbreaks of Chagas disease in Colombia and Venezuela.

P. geniculatus is considered to have sylvatic habits; however, in recent decades at least 45 cases of intrusion into homes by adult insects have been reported in Bolivia, Brazil, Colombia, Peru, Surinam and Venezuela. This new scenario implies an increased transmission risk of the disease in endemic and non-endemic areas, either by direct contact or by food contamination. Nevertheless, in some Latin American regions the presence of nymphs, eggs and exuviae is evidence of colonisation of human dwellings, as reported in nine publications.(40,48,134,135,136, 137,138,139,140) These differences in species behavior probably reflect genetic differences between the populations.

The difficulty in obtaining direct evidence incriminating which vector species is responsible for oral transmission of T. cruzi, is related to the fact that orally-transmitted outbreaks of Chagas disease occur several days after food contamination. Despite this difficulty, in some reported cases there are strong suspicions about the role of P. geniculatus in this transmission mechanism, because it has been abundantly observed in outbreak areas. Indeed, it has been found invading houses where contaminated food is prepared and although in some cases the captured insects did not show infection with T. cruzi, in other cases high levels of natural infection were observed. At least 10 publications present indirect evidence involving P. geniculatus in the oral transmission of T. cruzi.113113. Hernández C, Vera M, Cucunubá Z, Flórez C, Cantillo O, Buitrago L, et al. High-Resolution molecular typing of Trypanosoma cruzi in 2 large outbreaks of acute Chagas disease in Colombia. J Infect Dis. 2016; 214(8): 1252-5. https://doi.org/doi:10.1093/infdis/jiw360.
https://doi.org/10.1093/infdis/jiw360...
,143143. Rueda K, Trujillo J, Carranza J, Vallejo G. Transmisión oral de Trypanosoma cruzi: una nueva situación epidemiológica de la enfermedad de Chagas en Colombia y otros países suramericanos. Biomédica. 2014; 34(4): 631-41. https://doi.org/10.7705/biomedica.v34i4.2204.
https://doi.org/10.7705/biomedica.v34i4....
,144144. Ríos J, Arboleda M, Montoya A, Alarcón E, Parra-Henao G. Probable brote de transmisión oral de enfermedad de Chagas en Turbo, Antioquia. Biomédica. 2011; 31(2): 185-195. https://doi.org/10.7705/biomedica.v31i2.302.
https://doi.org/10.7705/biomedica.v31i2....
,145145. Hernández L, Ramírez A, Cucunubá Z, Zambrano P. Brote de Chagas agudo en Lebrija, Santander, 2008. Revista del Observatorio de Salud Pública de Santander. 2009; 4(1): 28-36.,146146. Zambrano P, Cucunubá Z, Montilla M, Flórez C, Parra E, Cortés L. Brotes de síndrome febril asociado a miocarditis aguda chagásica de posible transmisión oral en el departamento de Santander, diciembre de 2008 a mayo de 2009. Inf Quinc Epidemiol Nac. 2008; 15: 17-32.,147147. Soto H, Tibaduiza T, Montilla M, Triana O, Suárez D, Torres M, et al. Investigación de vectores y reservorios en brote de Chagas agudo por posible transmisión oral en Aguachica, Cesar, Colombia. Cad Saude Publica. 2014; 30(4): 746-56. https://doi.org/10.1590/0102-311X00024013.
https://doi.org/10.1590/0102-311X0002401...
,148148. Santalla J, Oporto P, Espinoza E, Ríos T, Brutus L. Primer brote reportado de la enfermedad de Chagas en la Amazonía Boliviana: reporte de 14 casos agudos por transmisión oral de Trypanosoma cruzi en Guayaramerín, Beni-Bolivia. Biofarbo. 2011; 19(1): 52-8.,149149. Alarcón de Noya B, Díaz-Bello Z, Colmenares C, Ruiz-Guevara R, Mauriello L, Zavala-Jaspe R, et al. Large urban outbreak of orally acquired acute Chagas disease at a school in Caracas, Venezuela. J Infect Dis. 2010; 201(9): 1308-15. http://dx.doi.org/10.1086/651608.
http://dx.doi.org/10.1086/651608...
,150150. Suárez J, de Suárez C, Alarcón de Noya B, Espinosa R, Chiurillo M, Villaroel A, et al. Enfermedad de Chagas sistémico en fase aguda por transmisión oral: diagnóstico integral de un caso autopsiado. Gac Med Caracas. 2010; 118(3): 212-22.,151151. Añez N, Crisante G, Rojas A, Dávila D. Brote de enfermedad de Chagas agudo de posible transmisión oral en Mérida, Venezuela. Bol Malariol Salud Amb. 2013; 53(1): 1-10.

Although it is not completely clear what the effect of climate change will be on the biology of P. geniculatus, it is known that the species has optimal development between 26 and 28ºC and between 90-100% relative humidity. That colonies kept at 30ºC have high mortality and low fertility means that increases in temperature may affect the distribution of the species such that it could move altitudinally to find places with more favorable temperatures.

ACKNOWLEDGEMENTS

To Sandra Cheesman, PhD, from Edanz Group (https://en-author-services.edanzgroup.com/ac) and Jason Garry for editing a draft of this manuscript.

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  • Financial support: Colombian Science, Technology and Innovation Department (Colciencias) project 120465843375 contract 063-2015 (http://www.colciencias.gov.co/node/1119) to FG, GAV and JDR; University of Tolima Research Fund (project 770115).

Publication Dates

  • Publication in this collection
    26 Feb 2021
  • Date of issue
    2021

History

  • Received
    07 Oct 2020
  • Accepted
    26 Jan 2021
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