Update on the distribution of Triatoma bolivari and Triatoma brailovskyi (Hemiptera: Reduviidae: Triatominae) in western Mexico

Authors

  • José Alejandro Martínez-Ibarra,

    1. Área de Entomología Médica, Centro Universitario del Sur, Universidad de Guadalajara, Ciudad Guzmán, Jalisco, México
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  • Fernando Martínez-Hernández,

    1. Laboratorio de Epidemiología Molecular, Hospital General Doctor Manuel Gea González, México, D. F., México
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  • Guiehdani Villalobos,

    1. Laboratorio de Entomología, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, México, D. F., México
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  • Mauro Omar Vences-Blanco,

    1. Laboratorio de Biología de Parásitos, Facultad de Medicina, Universidad Nacional Autónoma de México, México, D. F., México
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  • Paz María Salazar-Schettino

    1. Laboratorio de Biología de Parásitos, Facultad de Medicina, Universidad Nacional Autónoma de México, México, D. F., México
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Biological and epidemiological information is readily available for the most common 13 domestic triatomines (Hemiptera: Reduviidae: Triatominae) of the 30 species described in Mexico (Martínez-Ibarra et al. 2008, Rebollar-Téllez et al. 2009). Information about the remainder is scarce, mainly because they have rarely been collected and examined for Trypanosoma cruzi (Chagas) infection. Two examples of them are Mexican endemic species, Triatoma bolivari (Carcavallo, Martínez and Peláez) and T. brailovskyi (Martínez, Carcavallo and Peláez), each of which have only been collected once (Magallón-Gastélum et al. 1998, Ramsey et al. 2000) after their descriptions. Even though both species are considered to be of low epidemiological importance, both have been reported inside human dwellings (Magallón-Gastélum et al. 1998, Ramsey et al. 2000), with T. bolivari having T. cruzi-like flagellates in its feces. Both are also attracted by lights (Martínez et al. 1984, Carcavallo et al. 1987). Light attraction by triatomines is considered an infestation risk factor for human dwellings (Zeledón 1983, Rebollar-Téllez et al. 2009). As a consequence, a survey for T. bolivari and T. brailovskyi was carried out in western Mexico.

This study was conducted in three states (Colima, Nayarit, and Jalisco) in western Mexico in which both species were initially described (Martínez et al. 1984, Carcavallo et al. 1987) and in the state of Jalisco where they were recently collected (Magallón-Gastélum et al. 1998). In the state of Colima, the first collection place of both species was ambiguously described by Martínez et al. (1984) and Carcavallo et al. (1987) in these terms: “on the route from Minotitlan to Santiago, in the intersection with the San Jose River.” Triatomines were searched for in the town of Camotlan (N 19°12′, W 104°08′), where the route from Minatitlan (N 19°19′, W 104° 01′) to Santiago (N 19o08′, W 104o17′) crosses the San Jose River, and in its surrounding area, as well as in two nearby small towns on the same route, Veladero de Camotlan (N 19°13′, W 104°07′) and Punta de Agua (N 19°11′, W 104°09). Searches were also carried out in sylvatic environments every two km along the route from Santiago to Camotlan. The weather in this region is classified as sub-humid and hot, with mean annual temperatures between 26° C and 28° C. The main crops include various kinds of vegetables and fruits.

In the state of Nayarit, the first collection site was also ambiguously described by Martínez et al. (1984) and Carcavallo et al. (1987) as “…collected 15 km south of Compostela city, on the downhills of Zapotan Sierra.” In this area, Carrillo Puerto (N 21°08′, W 104°50′), its surroundings regions, and ten sylvatic locations along a 15 km stretch of route south of Compostela were searched. The weather in this region is classified as semi-arid, with a dry season between October and June and mean annual temperatures of 20.4° C. The vegetation is deciduous seasonal forest and the main crop is corn (Zea mays L.) (SEGOB 2005).

In the state of Jalisco, two areas were searched: the Biological Station of the UNAM in Chamela (N 19°30′, W 105°03′), from where some of the first specimens of T. bolivari and T. brailovskyi were collected for description (Martínez et al. 1984, Carcavallo et al. 1987), and two small nearby towns in the same area, Juan Gil Preciado (N 19°33′, W 105°02′) and Chamela (N 19°31′, W 105°01). The small towns of Cuatitlan (N 19°21′, W 104°22′), Ayotitlan (N 19°22′, W 104°09′), and Cuzalapa (N 19°24′, W 104°17′), which are located in the area from which T. brailovskyi was recently reported (Magallón-Gastélum et al. 1998), were also searched. In the Chamela area, the weather is classified as sub-humid and hot, with a marked rainy season and drought from November to June. The vegetation is deciduous low forest and deciduous tropical forest. On the other hand, in the Cuatitlan area, the weather is semi-dry, with a mean annual temperature of 23.5° C. The vegetation is characterized as perennial forest.

T. bolivari and T. brailovskyi were searched for in each studied village as well as in the Chamela Biological Station during five three-day field trips. Triatomines were sought in intradomiciliary and peridomiciliary areas, including the areas between the main constructions and the fences (about 20 to 30 m). In sylvatic areas, all potential natural ecotopes of triatomines (e.g., bird nests, hollow trees and their cracks, holes in the ground, railings, rock pile boundary walls, heaps of stone, fallen cacti, and hollows in caves and cliffs) were sampled. Triatomines were collected by hand during the day with the aid of flashlights. At night they were sampled using 30 wire-netting bait-traps, called Noireau traps (Noireau et al. 2002), as modified by Martínez-Ibarra et al. (2008). The traps were placed in 30 different sites, including domestic and natural ecotopes of triatomines, as described above. Six 22-watt Universal Black Light Traps (BioQuip™, Rancho Dominguez, CA) were also placed in sylvatic areas. They were not placed in towns to avoid competition with the lights of human dwellings. Using tweezers, the collected triatomines were transferred to plastic containers labeled with collection information (sex, place, and method of capture). Specific descriptions were used to identify the collected species (Martínez et al. 1984, Carcavallo et al. 1987). Live individuals were transported to the laboratory, fed on Swiss mice, and placed individually in Petri dishes until defecation. Infection by T. cruzi was determined through microscopic examination of feces. Parasites detected in the feces were collected and intraperitoneally inoculated into Swiss mice.

Two female and six male T. bolivari and two male T. brailovskyi were collected. All ten specimens were collected from the Chamela area. Two specimens (a male of each species) were collected from the village of Chamela, and the rest were collected inside the area of the Chamela Biological Station. Efforts to collect T. bolivari or T. brailovskyi from the states of Colima and Nayarit, or from the Cuatitlan area in the state of Jalisco, were unfruitful. The collected specimens of both species came from outside houses and buildings that were located close to white light bulbs, indicating that they had most likely been attracted to these areas by the lights. The specimen of T. bolivari collected outside houses in the village of Chamela was positive for T. cruzi.

We report the first collection of T. bolivari in western Mexico, the second collection in the country, and the first of live specimens since the initial description of this species more than 20 years ago (Carcavallo et al. 1987). This is also only the second time that females of this species have been collected in Mexico. It is also the first time this species has been collected in western Mexico; the only other collection reported was in the southern Mexican state of Oaxaca (Ramsey et al. 2000). The previous and current collection results are in agreement with those of Carcavallo et al. (1987), who proposed that T. bolivari is a sylvatic (rarely collected in human dwellings) species.

This is also only the second time that T. brailovskyi has been collected in Mexico since its initial description more than 25 years ago (Martínez et al. 1984). Similar to previous reports (Martínez et al. 1984, Magallón-Gastélum et al. 1998), only male specimens could be collected. As Martínez et al. (1984) established, the lack of collected females could indicate a higher mobility and tendency of dispersal by the males and a tendency of females to stay in their natural habitats.

One specimen of T. bolivari was infected by T. cruzi, which is the first time that this species has been found to be infected by this protozoan. This finding confirms the results of Carcavallo et al. (1987), who reported a specimen of T. bolivari with T. cruzi-like flagellates on its feces. The capture of infected specimens of T. bolivari illustrates the risk sylvatic strains of T. cruzi undergo when moving to human dwellings. These strains could be maintained in circulation in domestic and peridomestic environments by other triatomine species, such as Meccus phyllosomus longipennis (Usinger) and M. p. picturatus (Usinger), which were also detected in the study areas (Martínez-Ibarra et al. 2008).

Not a single specimen of T. bolivari or T. brailovskyi was collected in the states of Colima or Nayarit, or in Cuatitlan in the state of Jalisco. In the states of Colima and Nayarit, a possible explanation for the lack of specimens is that the study areas have been highly disturbed by deforestation in order to cultivate corn (Zea mays L.) and other vegetable crops, as well as to gather fodder for cattle. These areas have also been heavily sprayed with insecticides, which could have eradicated triatomines. On the other hand, a possible explanation for the lack of specimens in the three towns in the Cuatitlan area is tree felling, which is being done to make new roads through the mountains, and deforestation, which is being done to supply fancy woods for the furniture industry.

Our survey inside human dwellings did not result in the collection of T. bolivari and T. brailovskyi. A possible explanation is that both species could be classified, according to the classification by Zeledón (1983), as totally sylvatic insects whose adults, although attracted by the lights of human houses that they sometimes invade, are unable to colonize them. The modified Noireau traps also failed; apparently T. bolivari and T. brailovskyi were not attracted to the rats inside the traps. Efforts to collect these species in rodent burrows and other natural ecotopes also failed. Consequently, we believe that these two species are naturally associated with birds rather than rodents, as previously proposed (Carcavallo et al. 1987). Also, both species are apparently stenophagic, since collected specimens refused to feed on hens (Gallus gallus L.) in the laboratory, pigeons (Columba livia Gmelin), rabbits (Oryctolagus cuniculus L.), rats (inline image), and even human beings. A similar behavior was recorded for Cavernicola pilosa Barber [associated with bats such as Desmodus rotundus (Geoffroy)] and Psammolestes coreodes Bergroth (associated with different kinds of birds, such as Phacellodomus sibilatrix (Sclater) (Lent and Wygodzinsky 1979).

The Universal Black Light Traps also failed to collect specimens of T. bolivari and T. brailovskyi, suggesting that they were not attracted by these traps, despite their reported attraction to white lights, as illustrated by T. dimidiata (Latreille) in Yucatan, Mexico (Rebollar-Téllez et al. 2009), in contrast to a related species, T. gerstaeckeri (Stål), in northern Mexico (Martínez-Ibarra et al. 1992). It is concluded that T. bolivari and T. brailovskyi invade human dwellings because they are attracted by white lights, and that they can potentially carry sylvatic T. cruzi strains, as was recorded for at least 20 species, including those involved in T. cruzi transmission to humans (Zeledón 1983). It is also suggested that T. bolivari and T. brailovskyi have disappeared from some environmentally disturbed areas and they are now confined to two very small coastal areas in western Mexico. In the case of T. bolivari, another small coastal area of distribution was recorded (Ramsey et al. 2000). More studies on these two species are necessary to gain a better understanding of their current distribution.

Ancillary