Journal of
Threatened Taxa | www.threatenedtaxa.org | 26 October 2018 | 10(11):
12515–12522
New kissing bug (Hemiptera: Reduviidae: Triatominae) records from Napo and Morona-Santiago
provinces with distribution updates in Ecuador
Ana Soto-Vivas
1, Sandra Enríquez 2, Ernesto Villacrés 3, Jazzmin Arrivillaga 4, Martín Hinojosa 5 & Jonathan Liria
6
1 Carrera de Biología,
Facultad de Ciencias Biológicas, Universidad Central del Ecuador, Quito 170129,
Ecuador
2,3 Instituto de Investigación
en Salud Pública y Zoonosis
(CIZ), Universidad Central del Ecuador, Quito 170129, Ecuador
4 Área de Ambiente, Turismo Histórico Cultural, Facultad de Comunicación Social,
Universidad Central del Ecuador, Quito 170129, Ecuador
5 Carrera Ingeniería
en Ecosistemas, Universidad Regional Amazónica Ikiam, Vía Tena, Muyuna
Kilómetro 7, Napo, Ecuador
6 Grupo de Investigación
en Población y Ambiente,
Universidad Regional Amazónica Ikiam,
Vía Tena, Muyuna Kilómetro 7, Napo, Ecuador
1 aysoto@uce.edu.ec, 2 sandrabycid@gmail.com,
3 ernestovillacresguevara@yahoo.es, 4 jcarrivillaga@uce.edu.ec,
5 martin.hinojosa@ikiam.edu.ec, 6 jonathan.liria@gmail.com
(corresponding author)
Abstract: 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.
Keywords: Chagas
disease, new records, Rhodniini, Triatomini.
Spanish Abstract: Se reportan cuatro especies de Triatominae (Hemiptera: Reduviidae) en cuatro localidades en la Amazonía ecuatoriana. Eratyrus mucronatus
Stål, 1859, Rhodnius
pictipes Stål, 1872 y Panstrongylus geniculatus
(Latreille, 1811) en la provincia
de Napo, y Rhodnius robustus
Larrousse, 1927 en la Provincia
de Morona-Santiago. Dos especímenes de R. pictipes se encontraron en el
área urbana
de la ciudad de Tena (provincia
capital). Estos hallazgos pueden indicar un
riesgo de transmisión de la
enfermedad de Chagas en áreas urbanas y periurbanas de la Amazonía.
doi: https://doi.org/10.11609/jott.4345.10.11.12515-12522 | ZooBank: urn:lsid:zoobank.org:pub:0B7A9E1F-0043-4D56-925A-9A1F9D188BBC
Editor: Anonymity
requested. Date of publication: 26
October 2018 (online & print)
Manuscript details: Ms
# 4345 | Received 27 June 2018 | Final received 20 September 2018 | Finally
accepted 01 October 2018
Citation: Soto-Vivas, A., S. Enriquez,
E. Villacres, J. Arrivillaga,
M. Hinojosa & J. Liria (2018). New kissing bug (Hemiptera:
Reduviidae: Triatominae) records from Napo and Morona-Santiago provinces with distribution
updates in Ecuador. Journal of Threatened Taxa 10(11): 12515–12522; https://doi.org/10.11609/jott.4345.10.11.12515-12522
Copyright: © Soto-Vivas et al. 2018.
Creative Commons Attribution 4.0 International License.
JoTT allows unrestricted use of this article in any
medium, reproduction and distribution by providing adequate credit to the
authors and the source of publication.
Funding: Facultad de Ciencias Biológicas - Universidad Central del Ecuador, Centro Internacional de Zoonosis - Universidad Central del
Ecuador, Universidad Regional Amazónica Ikiam.
Competing interests: The authors declare no competing interests.
Author Details: Ana Soto-Vivas PhD, is a Lecturer-Researcher at the Central
University of Ecuador. Her research interests are medical entomology, geometric
morphometrics, and Triatominae
systematics and biogeography. Sandra Enríquez MSc Biology, is a
researcher at the Public Health and Zoonoses Research
Institute (CIZ) of the Central University of Ecuador, Quito. Biologist
and Entomologist. Her research interest is the taxonomy of arthropod
vectors, biodiversity, taxonomy of aquatic insects and environmental impact. Ernesto Villacres Biologist, is a researcher at CIZ. His research interests
are Triatominae and others arthropod vectors. Jazzmin Arrivillaga PhD, is a
Lecturer-Researcher at the Central University of Ecuador. Her research
interests are medical entomology and Sand-flies
systematics and biogeography. Mr. Martín
Hinojosa is an undergraduate student of Ecosystem Engineering program of
Ikiam. Jonathan
Liria PhD, is a
Lecturer-Researcher at the Ikiam University. His
research interests are medical entomology, geometric morphometrics,
and Culicidae systematics and biogeography.
Author
Contribution: ASV conducted
the Triatominae identification and wrote the first
manuscript draft. JL, EV and MH conducted the specimens
collections. ASV, JA, SE and JL wrote the final manuscript. SE prepared the
specimen photographs. JL elaborated the distribution maps.
Acknowledgements: The authors thank Pablo Araujo for the triatomine
specimens photographs.
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. Ecuador
currently contains about 17 species such as the following: Triatoma
dimidiata (Latreille,
1811), Triatoma carrioni
Larrousse, 1926, Triatoma
venosa (Stål, 1872), Triatoma dispar
Lent, 1950, Eratyrus mucronatus
Stål, 1859, Eratyrus
cuspidatus Stål, 1859, Cavernicola pilosa
Barber, 1937, Panstrongylus geniculatus (Latreille,
1811), Panstrongylus rufotuberculatus
(Champion, 1899), Panstrongylus howardi (Neiva, 1911), Panstrongylus
chinai (Del Ponte, 1929), Panstrongylus
lignarius (Walker, 1873), Pastrongylus
herreri (Wygodzinsky,
1948), Rhodnius ecuadoriensis
Lent & León, 1958, Rhodnius pictipes Stål, 1872, Rhodnius robustus Larrousse, 1927, and was recently described Rhodnius barretti
Abad-Franch et al. 2013 (Abad-Franch
et al. 2001; Galvão et al. 2003; Abad-Franch et al. 2013; Vaca-Moncayo
et al. 2017).
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 (0.9540S & 77.8620W);
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 (0.9890S & 77.8270W and 0.9870S &
77.8120W). 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) and Soto-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
(2.0670S & 77.8830W), 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).
Material
examined: EC-N-M-T25, 01.ix.2016,
1 male, Campus Universidad Regional Amazónica Ikiam (7km to Muyuna), Napo,
0.9540S & 77.8620W, 600m, coll. Conraz.
Distribution (Carcavallo et
al. 1999; Galvão et al. 2003; Chávez 2006; Guhl et al. 2007; Bérenger et al.
2009; Morocoima et al. 2010; Meneguetti
et al. 2011; Obara et al. 2013; Hiwat
2014; Galvão 2014; Ceccarelli
et al. 2018): Bolivia (Beni, La Paz, Chuquisaca,
Oruro, Potosí); Brazil (Acre, Amazonas, Goiás, Maranhão, Mato Grosso, Pará, Rondonia,
Tocantins); Colombia (Antioquia, Boyacá, Casanare, Cundinamarca, Meta, Norte
Santander, Vaupés); Ecuador (Esmeraldas, Loja, Napo, Orellana,
Sucumbíos), Guatemala, Guiana, French Guiana (Cayenne, Grand Santi, Montsinéry-Tonnegrande, Mana, Régina, Roura,
Saul, Kourou, Sinnamary);
Panama, Perú (Junín, Madre de Dios, Loreto, Ucayali,
San Martín), Suriname (Brokopondo, Paramaribo, Para, Sipaliwini); Trinidad (Tunapuna-Piarco,
San Juan-Laventille); Venezuela (Anzoátegui, Aragua,
Amazonas, Barinas, Carabobo, Cojedes, Guárico, Falcón, Lara, Mérida, Monagas,
Portuguesa, Sucre, Táchira, Trujillo, Yaracuy, Zulia).
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).
Panstrongylus geniculatus (Latreille, 1811)
(Image 2)
Diagnostic
characters: Length more than 20mm;
head comparatively short and stout, in lateral view; posterior process of scutellum elongate subcylindrical,
narrowly tapering apically; pronotum with extensive,
conspicuous black markings; all connexival segments
with light and dark marking; abdomen light colored ventrally, with longitudinal
series of black spots (Lent & Wygodzinsky 1979;
Soto-Vivas 2009).
Material
examined: EC-N-M-T34,
22.viii.2018, 1 female, Campus Universidad Regional Amazónica
Ikiam (7km to Muyuna),
Napo, 0.9540S & 77.8620W, 600m, coll. Conraz.
Distribution (Carcavallo et
al., 1999; Galvão et al. 2003; Chávez 2006; Guhl et al. 2007; Leite et al.
2007; Bérenger et al. 2009; Morocoima
et al. 2010; Meneguetti et al. 2011; Obara et al. 2013; Hiwat 2014; Galvão 2014; Ceccarelli et al.
2018): Argentina (Chaco, Corrientes, Entre Ríos, Formosa, Misiones, Santa Fe,
Santiago Del Estero); Bolivia (Beni, Cochabamba,
Santa Cruz, Tarija); Brazil (Acre, Amapá, Amazonas,
Bahia, Ceará, Distrito Federal, Espírito
Santo, Goiás, Maranhão, Mato Grosso, Mato
Grosso do Sul, Minas Gerais, Pará, Paraná, Piauí, Rio de Janeiro, Rondônia, Roraima, São Paulo, Tocantins); Colombia (Antioquia,
Amazonas, Bolívar, Boyacá, Cauca, Casanare, Cesar, Cundinamarca, Magdalena, Huila,
Meta, Norte de Santander, Putumayo, Santander, Sucre, Tolima, Valle del Cauca);
Costa Rica (Alajuela, Cartago, Guanacaste, Heredia, Limón, Puntarenas, San
José); Ecuador (Esmeraldas, Imbabura, Manabí, Napo, Orellana,
Pastaza, Pichincha, Sucumbíos); French Guiana (Cayenne,
Saint-Laurent-du-Maroni); Guatemala, Guyana
(Cuyuni-Mazaruni); Mexico (Chiapas, Veracruz,
Yucatán); Nicaragua (Atlántico Norte, Atlántico Sur, Managua, Río San Juan);
Panama (Bocas del Toro, Colón, Los Santos, Panamá); Paraguay (Alto Paraná,
Boquerón, Caaguazú, Concepción, Paraguarí); Peru (Amazonas, Ayacucho,
Cajamarca, Cusco, Huánuco, Junín, Madre de Dios, Loreto, Pasco, San Martín,
Ucayali); Suriname (Brokopondo, Commewijne,
Para, Paramaribo, Saramacca, Sipaliwini,
Wanica); Trinidad & Tobago (Diego Martín, San
Juan-Laventille, Sangre Grande, Siparia,
Tunapuna-Piarco); Uruguay; Venezuela (Anzoátegui,
Amazonas, Aragua, Barinas, Bolívar, Carabobo, Delta Amacuro, Distrito Capital,
Falcón, Guárico, Lara, Mérida, Miranda, Monagas, Trujillo, Táchira, Yaracuy,
Vargas, Zulia).
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.
Tribe Rhodniini
Rhodnius pictipes Stål, 1872 (Image
3)
Diagnostic
characters: Head laterally behind
the eyes with callosities setiferous tubercles;
antenna inserted proximal to head; anteocular region
of the head at least 2.7 times as long as postocular;
pronotum very granulose, rugose;
femora yellowish, mottled with dark brown; tibiae of all pairs of legs with
dark submedian annulus; corium brownish, irregularly
spotted with black; rectangular dark spots of dorsal connexival
segments with conspicuous pointed projection posteriorly, at least on segments
3 to 5; process of pygophore bispinous
with short base (Lent & Wygodzinsky 1979; Bérenger & Pluot-Sigwalt
2002; Soto-Vivas 2009).
Material
examined: EC-N-M-T26, EC-N-M-T27,
EC-N-M-T28, 03.iii.2016, 3 males, Campus Universidad Regional Amazónica Ikiam (7km to Muyuna), Napo, 0.9540S & 77.8620W,
600m, coll. CONRAZ. EC-N-T-T29, 23.iii.2018, 1 female,
Barrio El Dorado (Tena
City), Napo, 0.9870S & 77.8120W, 500m, CONRAZ. EC-N-T-T30, 20.v.2018, 1 female Barrio San
Antonio (Tena City), Napo, 0.9890S &
77.8270W, 517m, coll. CONRAZ.
Distribution (Carcavallo et al. 1999; Abad-Franch
et al. 2001; Galvão et al. 2003; Chávez 2006; Cortez et al. 2007; Guhl et al. 2007; Hiwat 2014; Galvão 2014; Ceccarelli et al. 2018): Bolivia (Cochabamba, Santa Cruz, Beni, Pando); Belize, Brazil (Amapá,
Amazonas, Goiás, Maranhão, Mato Grosso, Pará,
Piauí, Roraima, Tocantins);
Colombia (Amazonas, Boyacá, Caquetá, Cundinamarca, Guaviare, Meta, Norte
Santander, Putumayo, Vaupés); Ecuador (Azuay, Morona Santiago, Napo, Orellana, Sucumbíos); Guiana, French Guiana (Cayenne, Saint-Laurent
du Maroni); Peru (Ayacucho, Cusco, Huánuco, Madre de Dios, Loreto, Ucayali, San
Martín, Junín); Suriname (Brokopondo, Commewijne, Coronie, Marowijne, Paramaribo, Para, Saramacca,
Sipaliwini, Wanica);
Trinidad (Diego Martín, Rio Claro-Mayaro, Siparia, Tanapuma-Piarco);
Venezuela (Anzoátegui, Amazonas, Apure, Aragua, Bolívar, Carabobo, Cojedes,
Delta Amacuro, Falcón, Mérida, Miranda, Monagas, Portuguesa, Táchira, Trujillo,
Sucre, Yaracuy, Zulia).
Medical
importance: Occasionally
attracted to light in human dwellings. It has been found naturally infected
with T. cruzi. (Carcavallo et al. 1999; Feliciangeli
et al. 2004a; Abad-Franch et al. 2009).
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 20–23.5 mm, of
females 23–26 mm (Lent & Wygodzinsky 1979; Soto-Vivas 2009).
Material
examined: EC-MS-Y-T17,
EC-MS-Y-T18, EC-MS-Y-T19, EC-MS-Y-T20, 14.xi.2009, 3 males and 1 female, Yuwientza “Shuar community”,
Morona Santiago, 2.0670S & 77.8830W, 1,126m, coll. Conraz; EC-N-M-T32, 12.vii.2018, 1 female, Campus
Universidad Regional Amazónica Ikiam
(7km to Muyuna), Napo, 0.9540S &
77.8620W, 600m, coll. Conraz; EC-N-M-T33,
23.viii.2018, 1 female, Campus Universidad Regional Amazónica
Ikiam (7km to Muyuna),
Napo, 0.9540S & 77.8620W, 600m, coll. Conraz.
Distribution: (Carcavallo et
al. 1999; Abad-Franch et al. 2001; Galvão et al. 2003; Chávez 2006; Cortez et al. 2007; Guhl et al. 2007; Bérenger et al.
2009; Hiwat, 2014; Galvão
2014; Ceccarelli et al. 2018): Bolivia (Cochabamba, Beni, La Paz, Santa Cruz, Pando); Brazil (Acre, Amapá, Amazonas, Goiás, Maranhão, Mato Grosso, Pará, Rondonia,
Roraima, Tocantins); Colombia (Amazonas, Arauca,
Bolívar, Cundinamarca, Norte Santander, Santander, Tolima); Ecuador (Napo,
Morona Santiago, Sucumbíos, Orellana); French Guiana
(Cayenne, Macouria, Matoury,
Grand-Santi, Regina), Perú
(Amazonas, Cajamarca, Junín, Madre de Dios, Loreto, San Martín, Ucayali);
Suriname (Brokopondo, Marowijne,
Para, Saramacca, Sipaliwini);
Venezuela (Apure, Barinas, Bolívar, Cojedes, Falcón, Mérida, Monagas, Sucre,
Táchira, Trujillo, Yaracuy).
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. (1994,
1995, 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. More recently, Amunárriz
et al. (2010), reported a population infected by T.
cruzi located between the margins of Napo and Aguarico rivers.
These authors mentioned three triatomine
species involved: P. geniculatus, R. pictipes and R. robustus.
Abad-Franch & Monteiro
(2007) stated that all Amazonian triatomine species
comprises four tribes: Rhodniini, Bolbolderini,
Cavernicolini, and Triatomini
(with Eratyrus).
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 al. 1998b; Soto-Vivas et al. 2001).
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.
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