New kissing bug ( Hemiptera : Reduviidae : Triatominae ) records from Napo and Morona-Santiago provinces with distribution updates in Ecuador

Four species of Triatominae (Hemiptera: Reduviidae) are reported in four localities in Ecuadorian Amazonia. Eratyrus mucronatus Stål, 1859, Rhodnius pictipes Stål, 1872 & Panstrongylus geniculatus (Latreille, 1811) in Napo Province, and Rhodnius robustus Larrousse, 1927 in Morona-Santiago Province. Two specimens of R. pictipes were found in an urban area of Tena City (capital province). These findings can indicate a risk of Chagas disease transmission in urban and peri-urban areas of the Amazonia.


INTRODUCTION
The triatomine bugs are characterized by the hematophagous habit and morphological adaptations associated with the blood feeding.These insects are the main vectors of Chagas Disease or American Trypanosomiasis (Lent & Wygodzinski 1979;World Bank 1993).The Triatominae subfamily comprises five tribes, 17 genera, and 150 species, where Triatoma Laporte, 1832 and Rhodnius Stål 1859, are the most important vectors.
Triatoma dimidiata is the main vector in Ecuador associated with the Chagas disease transmission in Guayas and Manabí provinces; this species is distributed in Los Ríos, El Oro, Pichincha and Bolivar provinces.On the other hand, R. ecuadoriensis is associated with the transmission in Loja and El Oro provinces and is reported in Manabí, Guayas and Los Ríos too.Finally, T. carrioni is reported in Azuay, Cañar, Loja, El Oro, Zamora Chinchipe, and recently in Pichincha (Grijalva et al. 2003).Other species with less importance are P. rufotuberculatus, P. chinai, P. geniculatus, P. lignarius, P. howardi, T. venosa, T. dispar, E. mucronatus, E. cuspidatus and C. pilosa; however in the Amazonia R. pictipes and R. robustus are sylvatic vectors (Aguilar et al. 1999;Abad-Franch et al. 2001;Galvão et al. 2003;Vaca-Moncayo et al. 2017).Due to this, we reported new triatomine records in two Ecuadorian Amazonia Provinces with update distribution in Ecuador.

MATERIAL AND METHODS
This study is based on, one male specimen of E. mucronatus, three males specimens of R. pictipes and one female specimen of P. geniculatus, found dead in the main entrance of the Universidad Regional Amazónica Ikiam (0.954 0 S & 77.862 0 W); more recently, two dead female specimens of R. robustus were found in the Universidad Regional Amazónica Ikiam (same coordinates).Later, two additional dead female specimens of R. pictipes were found in two houses of the urban area of Tena City (0.989 0 S & 77.827 0 W and 0.987 0 S & 77.812 0 W).The first specimen was found inside the house in the living room close to the kitchen, and the second specimen was found outside the house on the third floor in the department entrance.Houses are surrounded by secondary forest patches at 20-125 m and 200-278 m to the Tena River.All the insects were pinned, mounted and the identification was determined using taxonomic keys of Lent & Wygodzinsky (1979), Carcavallo et al. (1998a) andSoto-Vivas (2009).In R. pictipes, the male genitalia were dissected following the morphological description of Bérenger & Pluot-Sigwalt (2002).The triatomine specimens were deposited at the entomological collection of Instituto de Investigación en Salud Pública y Zoonosis in the Universidad Central del Ecuador: "Colección Nacional de Referencia de Artrópodos de Importancia en Zoonosis (CONRAZ)".Finally, the four specimens of R. robustus collected in Yuwientza (2.067 0 S & 77.883 0 W), a Shuar community located in Morona Santiago Province was verified by CONRAZ.

RESULTS AND DISCUSION
The list of species with diagnostic characters, distribution and medical importance are given below:

Family Reduviidae Subfamily Triatominae Tribe Triatomini
Eratyrus mucronatus Stål, 1859 (Image 1) Diagnostic characters: Rostrum with first and second segments larger (subequal in length), third segment short; anterior process of scutellum form a sharply pointed spine (the spine as long as the entire scutellum); fore lobe of pronotum with 1+1 strong discal spines; humeral angles distinctly spinose; subapical reddish spot of corium comparatively small, anteriorly not attaining level of m-cu cross-vein; free portion of vesica flattened apically in side view; abdomen dorsally with five prominent tubercles along each uroterguites (Lent & Wygodzinsky 1979;Soto-Vivas 2009).

Medical importance: Eratyrus mucronatus
has been found naturally infected with Trypanosoma cruzi (Chagas 1909); It was reported in small domestic colonies attracted to light in Andean areas of Bolivia.Also, it was recorded in domiciliation process, invading urban and rural areas near fragmented forests (Soto-Vivas et al. 2001;Abad-Franch et al. 2009).

Medical importance:
Panstrongylus geniculatus is a widely distributed species occupying natural habitats like burrows; this species shows association with Dasypus novemcinctus Linnaeus, 1758 and Didelphis marsupialis Linnaeus, 1758 (Abad-Franch et al. 2001) and rodents.It is believed that it is responsible for maintaining the enzootic cycle of T. cruzi.

Rhodnius robustus Larrousse, 1927 (Image 4)
Diagnostic characters: Head laterally behind the eyes with callosities setiferous tubercles; antenna inserted proximal to the head apex; anteocular region about four times as long as postocular; distance between eyes dorsally smaller than, or equal to, width of eye; head distinctly longer than pronotum (1:0.65-0.80);median process of pygophore narrow, pointed apically and with narrow triangular base; larger species, length of males Image 2. Dorsal view of Panstrongylus geniculatus (female) collected at Campus Universidad Regional Amazónica Ikiam, Napo.

5mm © Pablo Araujo & Sandra Enríquez
Medical importance: This species is closely related to R. prolixus, and has been associated to sylvatic habits and infected with T. cruzi.In northern South America, they were found migrating from palms to the houses, occurring where R. prolixus was eliminated by Chagas disease control programs (Monteiro et al. 2003;Guhl et al. 2007;Longa & Scorza 2007).

Epidemiological significance
The Amazonian Chagas disease transmission has increased in recent years; the first reports were in Brazil by Coura et al. (1994Coura et al. ( , 1995Coura et al. ( , 2002) ) and Albajar et al. (2003); recently Santalla et al. (2011), stated a case from Bolivian Amazonia.In Ecuador, the first records were registered by Aguilar & Yépez (1995) in three Amazonian Provinces: Sucumbíos, Napo, and Pastaza.
Eratyrus mucronatus is a sylvatic species responsible for the enzootic Chagas transmission (Morocoima et al. 2010) and reported occasionally in the peridomicile with a synanthropic trend (Noireau et al. 1995;Carcavallo et Image 3. Dorsal view of Rhodnius pictipes (male) collected at Campus Universidad Regional Amazónica Ikiam, Napo.Panstrongylus geniculatus is a sylvatic species associated with animal burrows and trees that provide microclimate conditions for their survival (Herrera & Urdaneta-Morales 1992;1997).In the last decade, this species has been associated with domiciliated environments, frequently found in chicken coops and invading homes attracted by light or in search of food (Feliciangeli et al. 2004b).Also, it has been found colonizing Rattus rattus Linnaeus, 1758 burrows in precarious dwellings (Reyes-Lugo 2009).Although it is true that in urban environments this species prefers to feed on chickens, dogs, cats, and synanthropic rodents, it is important to keep the entomological vigilance and its possible implication in the transmission of T. cruzi.(Herrera et al. 2003).
Sylvatic Rhodnius species distribution is related to the Arecaceae (Palms), and their feeding habits are associated with birds; this triatomine species are specialized to explore the Palm microhabitats (Lent & Wygodzinsky 1979;Abad-Franch et al. 2009).Also, several authors stated the association between Rhodnius and birds nest of Phacellodomus rufifrons (Wied-Neuwied, 1821) and other Furnariidae species (Lent & Jurberg 1975;Abad-Franch & Monteiro 2007).Abad-Franch et al. (2001) studied the biogeography of Ecuadorian triatomine based on distribution maps for each species.We georeferenced all Orellana/Napo records for E. mucronatus, R. pictipes and P. geniculatus, and the entire records correspond only to Orellana based on the Provinces boundaries (Fig. 1 A,B); also, we checked all triatomine records found in the Zoology Museum (QCAZ) on-line data base at the Pontificia Universidad Católica del Ecuador (QCAZ 2018).Due to this it was recorded for the first time that three species in Napo, and also the R. robustus distribution has spread out to Morona Santiago Province.
Finally, the land use changes, the wild source feed availability and triatomine species competence, can be a risk of disease transmission in urban and peri-urban areas of the Ecuadorian Amazonia.Due to this it is relevant to implement programs for entomological vigilance for the Chagas disease.