BEHAVIOR, CHEMICAL ECOLOGY
Feeding Patterns of Triatoma longipennis Usinger (Hemiptera, Reduviidae) in Peridomestic Habitats of a Rural Community in Jalisco State, Mexico SIMONE FRE´DE´RIQUE BRENIE`RE,1 SILVIA PIETROKOVSKY,2 ´ N GASTE´LUM,3 MARIE-FRANCE BOSSENO,1 MARIA MARGARITA SOTO,3 EZEQUIEL MAGALLO ALI OUAISSI,1FELIPE LOZANO KASTEN,3 AND CRISTINA WISNIVESKY-COLLI2
J. Med. Entomol. 41(6): 1015Ð1020 (2004)
ABSTRACT We analyzed triatomine blood feeding patterns to evaluate the role of peridomiciles in Trypanosoma cruzi transmission at the rural village of Tepehuaje de Morelos at Jalisco State, Mexico (1999). A total of 206 bugs were collected in 11 out of 26 households (42.3%). Nymphs predominated in the collections (64.9% of the total). Except for one Triatoma barberi female, a species that belongs to the protracta species complex, all adults were Triatoma longipennis, a species of the phyllosoma complex. Triatomines were exclusively present in peridomestic sites mainly piles of tiles and bricks, and none were found indoors. Overall infection rate was 56.6% and no signiÞcant differences (P ⬎ 0.05) were observed between nymphs and adults or males and females. IdentiÞed blood meals were chicken (29.4%), opossum (20.9%), pig (24.5%), murid (20.9%), dog (3.5%), and armadillo (0.7%). No gut content reacted against anti-human, anti-bovine, anti-rabbit, and anti-cat sera. In contrast to Þfth nymphs and adults, 87% of the small nymphs fed on one host, indicating that they are less mobile than other stages. Most Þfth nymphs and adults fed on domestic hosts, while small nymphs mainly fed on opossum and murid. Infection blood-meal indexes were around 50% for single meals on opossum and murid, stressing their importance as trypanosome donors. Peridomiciles in Tepehuaje could be regarded as interaction sites among domestic and wild and synanthropic mammals and triatomines, which would facilitate circulation of the same T. cruzi strains between domestic and sylvatic cycles. Stone-made walls and building materials, which hold synanthropic rodents and opossums, should be considered as targets for vector control measures. KEY WORDS Triatoma longipennis, peridomestic habitat, feeding patterns, Mexico
CHAGAS DISEASE IS ONE of the most important vectorborne diseases affecting many Latin American countries, where ⬇16 Ð18 million people are currently infected with Trypanosoma cruzi and around 11 million are at risk of infection (World Health Organization 1991). Despite numerous epidemiological and clinical reports, the prevalence and the geographical distribution of Chagas disease in Mexico is poorly known, and only recently it has been considered as a priority by health authorities. In Mexico, 18 of the 31 species of triatomines recorded have been found naturally infected with T. cruzi (Lent and Wygodzynsky 1979, Carcavallo et al. 1997). Little information on the re1 Institut de Recherche pour le De ´ veloppement, UR 08, Pathoge´ nie des Trypanosomatide´ s, 911 Av. Agropolis, BP 64501, 34394 Montpellier Cedex, France. 2 Unidad Ecologõ´a de Reservorios y Vectores de Para ´sitos, Departamento de Ecologõ´a, Gene´ tica y Evolucio´ n, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, 1428 Buenos Aires, Argentina. 3 Departamento de Salud Pu ´ blica del Centro, Universitario de Ciencias de la Salud de la Universidad de Guadalajara, Apartado postal 4-119, Guadalajara, Jalisco, Mexico.
lationship between sylvatic and domestic transmission cycles is available. Most of triatomines present in human dwellings and peridomestic areas are also found in sylvatic biotopes, making implementation of vector control strategies problematic (Za´rate and Za´rate 1985, Velasco-Castrejo´ n and Guzma´n-Bracho 1986). In addition, little information on the relationship between the sylvatic and domestic transmission cycles is available. Analysis of blood sources from different triatomine species contributes to an understanding of some aspects of the biology of these insects and the epidemiology of Chagas disease in the context of vectorÐ host interactions. However, data on blood-meal sources have been more frequently obtained under experimental conditions than from the Þeld, despite the high diversity of vector species and epidemiological scenarios. Studies on the feeding proÞle of the most important triatomine species indicate that chickens, humans, and dogs are the main blood sources. This is the case with Triatoma infestans, the most important domiciliated vector in South America, Triatoma sordida and Tria-
0022-2585/04/1015Ð1020$04.00/0 䉷 2004 Entomological Society of America
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toma rubrovaria, secondary vectors in Bolivia and Uruguay, respectively, Triatoma dimidiata, one of the major species from Mexico to the west of South America, and Panstrongylus megistus, principally domiciliated in parts of northeastern and eastern Brazil (Quintal and Polanco 1977, Wisnivesky-Colli et al. 1987, Fernandes et al. 1992, Rodrigues et al. 1992, Salvatella et al. 1994, Gurtler et al. 1996, Noireau et al. 1997). Chickens do not act as T. cruzi reservoirs because they are refractory to infection, but they play a signiÞcant role in the maintenance of peridomestic populations of T. infestans (Lopez et al. 1999). However, domestic animals such as goats, pigs, and rabbits have also been recorded as blood sources for this and other triatomine species (Quintal and Polanco 1977, Wisnivesky-Colli et al. 1982). Triatoma longipennis and T. picturata, which belong to the phyllosoma complex, are found exclusively in xeric areas and high plains of the PaciÞc coast of Mexico. The epidemiological importance of these species is suggested by the high rates of T. cruzi infection in specimens collected from various villages at the Jalisco State (Magallo´ n-Gaste´ lum et al. 1998, Martinez-Ibarra et al. 2001). The aim of this study was to use triatomine blood feeding patterns to evaluate the role of peridomiciles in T. cruzi transmission in a rural village in Jalisco State, Mexico. Materials and Methods Study Area. The study was conducted in a rural community of Tepehuaje de Morelos located 1.5 km east of the head of San Martin de Hidalgo municipality in the Jalisco State (20⬚25⬘ N, 103⬚54⬘ W). Tepehuaje is located in a semiarid region characterized by a deciduous seasonal forest, which had been cleared to provide land for cultivation around the village. Main crops are sugarcane (Saccharum officinarum), corn (Zea mays), and Maguey tequilero (Agave tequilana). The minimum and maximum annual mean temperatures are 20 and 28⬚C, respectively, and annual rainfall averages range between 987.6 and 1,349 mm, with a dry season between October and June (data collected from Inegi organization with the following URL: http://www.inegi.gov.mx/inegi/default.asp). At the time of the study, the village was composed of 641 houses and had 2,523 inhabitants. Most of the houses consisted of four rooms (kitchen, dining room, and two bedrooms) with a cement roof (60%, the others were of tiles and sheet metal), mosaic ßoor (88%), and brick walls covered with plaster or cement (92%). The most frequent animals in peridomestic areas were chickens, dogs, sheep, goats, and pigs. Collection of Triatomines. A total of 26 households were arbitrary selected and inspected during November 1999. Two persons searched for triatomines indoors and outdoors at daytime with ßashlights. Sites examined inside dwellings were mattresses, picture frames, posters, and wall crevices. Peridomestic sites involved piles of tiles and bricks, Þrewood, chicken houses and pens, and near cattle and dogs. The search
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lasted around one man per hour in each area. The collected insects were placed in separate labeled plastic ßasks according to the capture site and transported to the laboratory. Processing of Triatomines. IdentiÞcation of triatomines was according to the keys of Lent and Wygodzinsky (1979). Adult specimens were identiÞed to species, but morphological similarities only allowed nymphs to be identiÞed to the phyllosoma complex. Feces from each bug, obtained by abdominal pressure, were mixed with phosphate-buffered saline and examined for the presence of ßagellates by direct microscope observation at 400⫻ magniÞcation. Then bugs were individually dissected under a safety hood. Promesenteric contents were obtained as previously described (Wisnivesky-Colli et al. 1980) and diluted 1:3 in 0.15 M phosphate-buffered saline (pH 7.2). Powdered gentian violet was added to a Þnal concentration of 0.025% to kill all parasites and make further manipulation of the samples safety. All samples were kept at ⫺20⬚C until processing. Immunodiffusion Testing of Blood Meals. Double diffusion tests (DD) were performed using 3.5 ml of 1.3% puriÞed agar (Oxoid Agar) in a 0.05 M veronalhydrochloric acid buffer solution, pH 8.2, per slide. Details of this technique were reported in a previous paper (Wisnivesky-Colli et al. 1982). Ten antisera were tested against the promesenteric contents of triatomines. Commercial antisera (Rockland, Gilbertsville, PA) were rabbit anti-dog, anti-cat, antimuridae, and anti-chicken sera, as well as goat antirabbit sera. Anti-armadillo, anti-pig, anti-opossum, anti-human, and anti-bovidae sera were obtained from rabbits inoculated with total serum of each species at our laboratory in Buenos Aires as reported before (Wisnivesky-Colli et al. 1982). Serial dilutions of the antisera (1:2Ð1:32) were faced against the homologous and heterologous sera diluted from 1:2Ð1:2,096. Finally the dilution of the antisera that gave a clear reaction against the homologous serum (at least one sharp band) and at the same time did not cross-reacted with any heterologous antisera was chosen to test the promesenteric contents of bugs. Human serum was the positive control included with each analysis. To characterize the feeding proÞle, armadillos and opossums were considered sylvatic animals, and murids were considered synanthropic ones. Statistical Analysis. We used the infective bloodmeal index of Wisnivesky-Colli et al. (1982) to evaluate the reservoir potential of blood-meal hosts. The proportions of nymphs and adults having fed on domestic hosts and sylvatic/synanthropic mammals were compared using a 2 test. Results Collection, Identification, and Prevalence of Infection in Triatomines. A total of 206 bugs were collected in 11 of 26 households (42.3%). Triatomines were exclusively present in peridomestic sites. Most of the bugs (79%) were found in piles of tiles and bricks. The number of collected bugs ranged from only some
BRENIE` RE ET AL.: HOST FEEDING SOURCES OF T. longipennis
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Table 1. Number and percentage of triatomines infected with T. cruzi that were collected from peridomiciles, in the community of Tepehuaje de Morelos, Jalisco, Mexico, during Nov. 1999 Feces examination No. of examined bugs No. of positive bugs % of positive bugs
Phyllosoma complex nymphs
T. longipennis adults
2nd
3rd
4th
5th
Total
Male
Female
Total
9 5 55.5
49 28 57.1
44 24 54.5
39 24 61.5
141 81 57.4
34 15 44.1
28 19 67.8
62 34 54.8
insects (1 or 2) in four households to larger collections (8 Ð36) in six other households, and 82 bugs were collected in another household. Nymphs predominated (64.9% of total), and most of them were third to Þfth instars; no Þrst-instar nymphs were found. Except for one T. barberi female, all adults were T. longipennis, and therefore, nymphs were assigned to the phyllosoma complex. Female to male ratio was 1:1.25. The overall infection rate was 56.6% (115/ 203), and no signiÞcant differences (P ⬎ 0.05) were observed between the proportions of infected nymphs and adults (0.57 versus 0.55, 2 ⫽ 0.037, 1 df) or infected males and females (0.44 versus 0.68, 2 ⫽ 2.601, 1 df; Table 1). Blood-Meal Analysis. The gut contents of 192 insects were analyzed by double diffusion test, and 114 (59.4%) were identiÞed to host species or class. The one T. barberi female reacted against anti-opossum and anti-pig sera. The remaining 113 specimens of T. longipennis collected in 10 different households fed on a blood-meal host (91/113, 80.5%), with smaller numbers feeding on two hosts (19/113, 16.8%; Table 2). Sixty-nine of 113 (61.1%) reactive bugs were nymphs, of which 58 (84%) had fed on only one host. All insects having fed only on opossums and most bugs solely containing murid blood were second- to fourth-instar nymphs. When multiple blood-meal sources of Þfthinstar nymphs and adults were considered together, they outnumbered those of young nymphs (16/22). The total number of T. longipennis feedings was 143 because of multiple blood-meal sources. IdentiÞed blood meals were as follows: chicken (29.4%), opos-
sum (20.9%), pig (24.5%), murid (20.9%), dog (3.5%), and armadillo (0.7%). No gut content reacted against anti-human, anti-bovine, anti-rabbit, and anti-cat sera. The proportion of blood meals taken from domestic hosts (chicken, pig, dog) was not signiÞcantly different than that taken from sylvatic or synanthropic mammals (opossum, armadillo, murid; P ⬎ 0.05, 2 ⫽ 3.2, 1 df). Blood meals of sylvatic and synanthropic versus domestic origin were from bugs captured in six and nine different habitats, respectively. The proportion of blood meals of sylvatic and synanthropic origin was 60.6% (54/89) for nymphs and 13% (12/54) for adults; in contrast, the proportion of blood meals of domestic origin predominated among adults (87%). These proportions were signiÞcantly different (2 ⫽ 31.28, 1 df, P ⬍ 0.0001), even if the sample of 82 bugs collected in a single house, which represent ⬇60% of the total nymph sample, was deleted from the analysis (2 ⫽ 4.41, 1 df, P ⬍ 0.05). Trypanosoma cruzi Infection Rates of Bugs in Relation to Blood-Meal Source. Bugs taking single and multiple blood meals were analyzed separately. Infective blood-meal index for bugs having fed on one host ranged from 28.6 (on pig) to 56.2% (on chicken), and similar indexes (⬇50%) were obtained for opossum and murid hosts (Table 3). Discussion The predominance of nymphs and the occurrence of second to Þfth instars in the samples indicated that the phyllosoma complex had successfully colonized
Table 2. Blood sources identified from triatomines collected in peridomestic habitats in the community of Tepehuaje de Morelos, Jalisco, Mexico, during Nov. 1999 Phyllosoma complex nymphs
T. longipennis adults
Blood source
Total no. of bugs
2nd
3rd
4th
5th
Total
%
Male
Female
Total
%
Chicken Opossum Muridae Pig Chicken and muridae Chicken and dog Chicken and pig Opossum and muridae Opossum and pig Muridae and pig Muridae and armadillo Pig and dog Chicken and opossum and pig Opossum and muridae and pig Opossum and pig and dog Total
32 20 18 21 4 3 2 5 2 1 1 1 1 1 1 113
Ñ 1 1 Ñ Ñ Ñ Ñ Ñ Ñ Ñ Ñ Ñ Ñ Ñ Ñ 2
2 12 4 1 Ñ Ñ Ñ 2 Ñ Ñ Ñ 1 Ñ Ñ Ñ 22
Ñ 7 11 3 Ñ Ñ Ñ 3 Ñ Ñ Ñ Ñ Ñ Ñ Ñ 24
9 Ñ 1 6 1 1 Ñ Ñ 1 Ñ 1 Ñ Ñ 1 1 22
11 20 17 10 1 1 Ñ 5 1 Ñ 1 1 Ñ 1 1 70
15.7 28.6 24.3 14.3 1.4 1.4
13 Ñ 1 9 2 Ñ Ñ Ñ Ñ 1 Ñ Ñ Ñ Ñ Ñ 26
8 Ñ Ñ 2 1 2 2 Ñ 1 Ñ Ñ Ñ 1 Ñ Ñ 17
21 Ñ 1 11 3 2 2 Ñ 1 1 Ñ Ñ 1 Ñ Ñ 43
48.8 Ñ 2.3 25.6 7.0 4.7 4.7 Ñ 2.3 2.3 Ñ Ñ 2.3 Ñ Ñ 100
7.1 1.4 1.4 1.4 1.4 1.4 100
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Table 3. Relationship between blood-meal source and T. cruzi infection rates in triatomines collected in peridomiciles in the community of Tepehuaje de Morelos, Jalisco, Mexico, during Nov. 1999 Single feedings Source
No. bugs positive/no. bugs with blood meals on
Opossum Muridae Pig Chicken Total
10/20 10/18 6/21 18/32 44/91
Multiple feedings Indexa (%)
No. bugs positive/no. bugs with blood meals on
Indexa (%)
50.0 55.5 28.6 56.2 48.4
6/11 6/12 6/10 8/10 26/43
54.5 50.0 60.0 80.0 60.5
a Infective blood-meal index ⫽ (no. of bugs positive for Trypanosoma cruzi with a blood meal on host X/no. of bugs examined with a blood meal on host X) ⫻ 100.
some peridomiciles of Tepehuaje. Despite the occasional presence of bugs inside dwellings reported by inhabitants of the village, we only collected triatomines outdoors, and none of them had fed on humans. This contrasts with studies conducted in peridomestic populations of other species, in which feedings on humans were frequent (Carcavallo et al. 1998). The absence of human blood meals in our study is possibly related to low indoor infestation rates and to the poor capacity of these triatomines to establish inside houses. In a previous study conducted in a rural community at the State of Nayarit in Mexico, the peridomestic area was also largely infested by T. picturata and T. longipennis, and only three specimens were collected indoors (Magallo´ n-Gaste´ lum et al. 2001). Nevertheless, these species must exhibit a variable propensity to colonize human dwellings (indoors) in different villages as previously reported (Magallo´ nGaste´ lum et al. 1998, Bautista et al. 1999, MartinezIbarra et al. 2001). However, clinical cases of Chagas disease have been associated with endemic areas where species of the phyllosoma complex are present in the villages, but the relationship with indoor and/or outdoor colonization is unknown (Tay et al. 1992, Garcõ´a de Alba Garcõ´a et al. 1996, Lozano Kasten et al. 1993, 1997, Rangel-Flores et al. 2001). Blood-meal analysis provides valuable information on the behavior of bugs. In contrast to Þfth-instar nymphs and adults, most of the young nymphs had fed on one host. This would indicate that young nymphs are less mobile than the other stages, because the taking of multiple blood meals has been proposed as an indicator of mobility by Barreto (1979). The majority of Þfth-instar nymphs and adults fed on domestic hosts, whereas small nymphs mainly fed on sylvatic and/or synanthropic hosts (opossum and murid). Most of young bugs were caught from building materials stored for a long-term period by human inhabitants. These sites would provide shelter for synanthropic rodents and opossums. Nymphs and adults showed high and similar T. cruzi infection rates, indicating that infection was acquired from initial meals at early developmental stages. Insects with single meals on chicken showed an infection blood index of 56.2%, having presumably acquired T. cruzi infection as young nymphs. Because blood-meal antigens can be detected for as long as 4 mo after
ingestion, the infective meal was probably diluted by repeated feedings on uninfected hosts (chicken). It is worth noting that 67% of adults contained a chicken blood meal, while only 18% of nymphs did. The lack of an increase in the infection rate between nymphs and adults undoubtedly results from the fact that chicken are refractory to T. cruzi infection. Infection blood-meal index for single meals on opossum and murid were around 50% each, pointing out the potential importance of these mammals as trypanosome donors to triatomine populations. Opossums of genus Didelphis are well-known reservoirs of T. cruzi over the North and South American continents (World Health Organization 1991). In a literature review, Schweigmann (1994) reported that T. cruzi infection prevalence averaged 30.7% (811/2636) for D. virginiana, D. marsupialis, and D. albiventris. Similarly, murids such as rats and mice are considered important reservoirs because they usually move between sylvatic and domestic habitats coming in contact with humans and domiciliated triatomines and because they reach high population densities in peridomiciles. Natural T. cruzi infections in synanthropic rodents (Rattus rattus, R. norvegicus, M. musculus) have been reported from Texas to southern Brazil (Barretto 1979, Herrera and Urdaneta-Morales 1997, Noireau et al. 1997). Sylvatic triatomines are generally associated with a variety of wild mammals, whereas domiciliated species use domestic hosts as their main blood-meal source. However, these trophic patterns are being modiÞed by intense anthropic activities that change natural environments. In Rõ`o de Janeiro, Brazil, Goncalves et al. (2000) reported that sylvatic T. vitticeps adults invading domiciles had fed on both wild (armadillo, wild pig, opossum, and rodent) and domestic hosts (human, bird, horse). In Santiago del Estero, Argentina, sylvatic T. guasayana collected in peridomestic biotopes had mainly fed on domestic blood sources as well as wild hosts (opossum, reptile, skunk, and armadillo) (Gajate et al. 1996). In Northern Co´ rdoba, Argentina, domiciliated T. infestans collected in peridomestic premises, although mainly fed on domestic hosts, showed some feedings on cavy, opossum, and murid (Wisnivesky-Colli et al. 1982). In Yucata´n, Mexico, blood sources of domiciliated T. dimidiata collected indoors and outdoors of the village of Izamal
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BRENIE` RE ET AL.: HOST FEEDING SOURCES OF T. longipennis
included opossum, bat, and armadillo as sylvatic mammals (25% of blood meals; Quintal et al. 1977) but no information on insect stages and capture sites were described. Conversely, opossum was absent among mammalian feedings of T. dimidiata collected in peridomestic structures in Panama (Christensen et al. 1988). In brief, our results corroborate the high infection rates of bugs belonging to the phyllosoma complex generally observed in Mexico. The high proportion of adults fed on domestic hosts indicates the potential capacity of this species complex to successfully settle in peridomestic environments. Peridomiciles in Tepehuaje could be regarded as sites of interaction among domestic, wild, and synanthropic mammals and triatomines, and the same T. cruzi strains would be expected to circulate between domestic and sylvatic transmission cycles. To control vector populations in Tepehuaje, special consideration should be given to those ecotopes holding synanthropic rodents and opossums, such as stone walls and stored building materials. Acknowledgments We thank C. A. Garza Avila for assistance in Þeldwork. This work was supported by the Institut de Recherche pour le De´ veloppement and the Consejo Nacional de Investigaciones Cientõ´Þcas y Te´ cnicas, PID 98-00, no. 1080.
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Received 20 October 2003; accepted 11 July 2004.
