Asian Pac J Trop Biomed 2011; 1(4): 279-284 279

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Document heading doi:10.1016/S2221-1691(11)60043-9 襃 2011 by the Asian Pacific Journal of Tropical Biomedicine. All rights reserved. The association of Triatoma maculata (Ericsson 1848) with the Thecadactylus rapicauda (Houttuyn 1782) (Reptilia: : Gekkonidae): a strategy of domiciliation of the Chagas disease peridomestic vector in Venezuela?

1 2 1 1 1 1 3 4 Reyes-Lugo M *, Reyes-Contreras M , Salvi I , Gelves W , Avilán A , Llavaneras D , Navarrete LF , Cordero G , Sánchez EE6, Rodríguez-Acosta A3,5

1Medical Entomology Section, Institute of Tropical Medicine, Universidad Central de Venezuela, Caracas, Venezuela 2School of Biology, Universidad Simón Bolívar, Caracas, Venezuela 3Immunochemistry Section, Tropical Medicine Institute, Universidad Central de Venezuela, Caracas, Venezuela 4Tropical Zoology Institute, Universidad Central de Venezuela, Caracas, Venezuela 5Instituto Nacional de Higiene “Rafael Rangel, Caracas, Venezuela 6Texas A&M University-Kingsville, Department of Chemistry, Kingsville, Texas, USA

ARTICLE INFO ABSTRACT

Article history: Objective: To investigate the bioecological relationship between Chagas disease peridomestic Received 10 March 2011 Methods: I Received in revised form 27 March 2011 vectors and as source of feeding. n a three-story building, triatomines were 17 2011 captured by direct search and electric vacuum cleaner search in and outside the building. Then, Accepted April Triatoma maculata T. maculata Available online 30 April 2011 age structure of the captured ( ) were identified and recorded. Results: T. maculata Reptiles living in sympatric with the triatomines were also searched. Thecadactylus rapicauda Keywords: were found living sympatric with ( ) and they bit residents of the T. maculata Chagas disease apartment building in study. A total of 1 448 individuals of were captured within three Gekkonidae days, of which 74.2% (1 074 eggs) were eggs, 21.5% were nymphs at different stages, and 4.3% were Conclusions: T. maculata T. rapicauda ThecadactylusReduviidae rapicauda adults. The association of and is an effective strategy Triatoma maculate of colonizing dwellings located in the vicinity of the habitat where both are present; and Trypanosoma cruzi therefore, could have implications of high importance in the intradomiciliary transmission of Vector domiciliation Chagas disease.

1. Introduction the 1960s, the Chagas disease endemic areas in the country possessed triatomine vector infestation indexes of 70% in It is estimated that in Central and South America there small villages. This alarming infestation prompted chemical 12 16 existTrypanosoma approximate cruzily T.to cruzi million people infected control programs and improvement in the construction of ( ) [1] with inT. e ncruzidem ic areas . In rural housing. As a consequence of the anti-triatomine Venezuela, the areas at háigher risk of infection have battle, the percentage of humans testing positive for Chagas traditionally been Anzo tegui, Barinas, Cojedes, Carabobo, antibodies decreased significantly to 6.2% in 1995 and even Trujillo, Aragua, Yaracuy and Portuguesa states, which lower (4.3%) in 1996[3]. 66 8% [2] 20 represent . confirmed cases of Chagas disease . During At the first half of the th century, the followinT.g ocruzirder of importance for the three main vRhodniusector spec prolixusies of ( in VenR.e zprolixusuela was Triatomaestablish emaculatad: StT.al *Corresponding author: Matias Reyes-Lugo, Medical Entomology Section, Institute of 1859) ( ), (Erichson 1848) ( Tropical Medicine, Universidad Central de Venezuela, Caracas, Venezuela. maculata Panstrongylus geniculatus P. ) ( 1811) ( Tel: +58-212-6053632 geniculatus and Latreille Fex: +58-212-6053505 ). This classification was based on the epidemic E-mail: [email protected] Foundation Project: Supported by Proyecto Control de Vectores IMT-UCV. relevancies for the Chagas disease such as hematophagic habits, times of defecation, rates of natural infection Reyes-Lugo M et al./Asian Pac J Trop Biomed 2011; 1(4): 279-284 280 T. cruzi Phytolacaceae Poaceae Polygonaceae Portulacaeae with and the biological attributes that made them Rubiaceae Sapindaceae, Smilacaeae, Ulmaceae, Vitaceae, compatible with domiciliary environments. Zygophyllaceae, Mimosacea, , , , In Latin America, within the last two decades, different and [11]. Currently, this woodland studies have emphasized the significant changes in the is under heavy construction. Charallave, the nearest town diversity of triatomine species, which were originally wild; is essentially a mosaic of suburban areas, including a small however, now have intruded residential homes and have relict forest, which at an earlier time covered a large area, [4] P. geniculatussubsequently been domiciled . This was the case for and secondary savannas of different dimensions. Charallave , where populations of peri and intradomiciliary held 14 329 homes in 1990[19] and 129 213 inhabitants in have been reported in Brazil and Venezuela[4-6]. 2005[12]. Concomitantly, it has been suggested that it could be playing 2.3. Triatomines search an imporT.tan cruzit role in the maintenance of the domestic cycle of inside certain social-environmental [5,6] conditions . P. geniculatus T. Triatomines were detected in an exhaustive, manually 2007 cruzi In November , was responsible for revised building, exteriorly and interiorly. The roof, walls oral transmission of 123 patients in Chacao (Reyes- and floors were inspected externally. Internally, all furniture, Lugo personal communication) by guava juice contaminated objects and equipment were revised. The direct search with feces of this triatomine, and it was also suspected of included a total of 10 hours, nine participants, for a capture infecting 50 individuals in Chichiriviche de la Costa in effort of 1.11 hours/man. M 2009 (R A ) A 6 arch odriguez- costa personal communication n electric vacuum cleaner conn襆ected to a m-hose with 4 ( 15 110 botT.h lomaculatacations within the state of Miranda, Venezuela. a diameter of cm was used Genie brand, PB Model / 120 60 7 8 1 5 10 [4] can be found in Aruba, Bonaire, Brazil, - V, Hz, . amp, e.g.. Peak HP Wet-Dry gallons for Colombia, Curazao, Guyana, Suriname and Venezuela[7], it areas difficult to access ( cracks and holes in floors, walls is an ornitophilic specie, considered opportunistic because and roofs, cumu’ lative objects, switetcches and lamps, conduit ) on occasion it has been found to colonize nearT. h maculataenhouses of the building s electric system, . The vacuum cleaner in Brazil and Venezuela[8,9]. At the same time, samples were analyzed in the laboratory with the help of a is considered to be responsible for the Chagas diseases magnifying stereoscopic (Wild, Germany). Entomological peridomestic cycle in some of the countries mentioned pincers and a fine paintbrush were used to separate the live [10,14] above . This work dT.es cmaculataribes for the first time a and dead triatomines, as well as other parts of their anatomy, population of domThecadactylusiciliated rapicauda stronT.gly rapicauda associated exuviae and collected eggs. The identification oéf theé insects ( ) with the gecko was carriedet o alut according to methods of Ramir z-P rez and (Houttuyn 1782) (Reptilia: Squamata: Saurian: Gekkonidae), Carcavallo [13,14]. which is distributed in Central and South America[10]. The triatomines (live, dead as well as exhuvia and eggs), collected by both methods, were separated and stored in 600 2. Materials and methods properly identified mL, plastic containers. The were transferred in a 20 L, polycarbonate container with ice 2.1. Ethical statement and a humid atmosphere in ordeT.r tmaculatao maintain the insects at a constant environment. The live were maintained in our Insectary to start a new colony. During the search The human study (blood samples test) was performed for triatomines, information was gathered in regards to in accordance with the principles of the Declaration of characteristics of the inspected areas. For instance, the size Helsinki, and the norms of the Tropical Medicine Institute of of the residential area, living conditions and description of the Universidad Central de Venezuela Bioethics Committee. surrounding area sin. Tsituhe temperature and the environmental All the experimental events concerning the use of relative humidity were also measured. live animals were done by specialized personnel. The The geckos, living in sympatric with the triatomines, Venezuelan pertinent regulations as well as institutional were also captured manually using entomology nets and guidelines, according to protocols approved by the Tropical transferred to the Tropical Medicine Institute Serpentarium Medicine Institute of the Universidad Central de Venezuela for their later identification with the Donoso-Barros (1968) Bioethics Committee. keys[15]. 2.2. Study area 2.4. Detection of T. cruzi

The study area was in a three-story residential building Parasitological conventional techniques (Giemsa staining ( ) ) Car-arte in the town of Pitahaya State of Miranda, and agar-blood cultures wereT. a pcruziplied to determine Venezuela, which locates 45 km south of Caracas. It is 293 the presence of promastigots of in the captured m above sea level near a dry tropical forest. Pitahaya has tT.ri amaculatatomines. The intestinal contents and fresh feces of some a total annual precipitation of 1 350 mm and an average specimens were used in these techniques. annual temperature of 26 曟. The plants that characterize A morphological comparison between intact red blood tLoganiaceaehe surroundinMalpighiaceaeg ecosystem beMalvaceaelong to the fMeliaceaeamilies of cells in’ the digestive tract of some triatomines and the Moraceae Nyctaginaceae, Orchidaceae, Passifloraceae, , geckos red blood cells was carried out with the purpose , , , , of establishing the blood ingest origin in the triatomines. Reyes-Lugo M et al./Asian Pac J Trop Biomed 2011; 1(4): 279-284 281 Didelphis marsupialis ( ) However, opossum T. f emaculataces were apartment consists of a sitting and dining room, a kitchen observed in a nearby area. The colony of T. rapicauda with a laundry area, two bedrooms and two bathrooms, studied in Pitahaya was feeding off the geckos ( which were typical modern 21st century homes. The walls Houttuyn 1782), which was evidenced by the presence of and ceilings were built with clay blocks and had a nice nucleated red blood cells (characteristic of reptiles) found paint finish; the floor of the first-story apartment was made in the colony when analyzed in the laboratory. In addition to of cement and was sealed with an epoxy coat, while the feeding off the geckos, at leT.a smaculatat ten individuals were feeding floors of the rest of the apartments were made of ceramic. off humans. The colony of moved from’ the roof The residence in study had a water pipe system and the to the bedrooms via the conduit of the building s electric electric power ran through internal wired ducts. However, system. T. maculata these services were functional only for the first floor. At The human inhabitants bitten by weT.re the moment of this study, in this floor, some rooms and a cruzisubjected to clinical and parasitological studies for bathroom were being used as a depot for material, and bats infection at the Tropical Medicine Institute of the and geckos were observed living in and around these areas Universidad Central de Venezuela. (Figure 1). All floors contained many light switches (some without switch plates), uncovered lamps, and 15 functional 3. Results incandescent light bulbs were distributed throughout the external part of the building and in the stairways (Figure 1). 3.1. Description of the homes colonized by T. maculata Five people occupied the building, which included the watchman living on the first floor and the family in study, (3 6 T. maculata composed of four members years old boy, years old girl, T 36 42 ) he homes occupied by were in a2 three-story years old mother and years old father , on the second building with a total of three apartments (200 m each). Each floor. The third floor was uninhabited without windows or

Figure 1. T. maculata The homes colonized by . ’ ’ T. maculata A: ApartmT.en trapicauda complex located in PitahT.ay amaculata, Miranda state, Venezuela 10曘12 2339 N and 66曘51 1326 W, where was associated with the gecko . B: Location of ® colony. Trash accumulation, due to the falling leaves from the neighboring trees, can be seen. The improvised roof with metal sheets, acerolit and wooden pieces placed in the exit of the stairway which leads to the roof was dismantled, and a vacuum cleaner was used to collect samples.

Table 1 T. maculata The number of specimens captured by developmental stages in the studied building. Method of capture Stage of a b,c development Direct searching Vacuum cleaner Live Deaths Complete exhuvias Live Complete exhuvias Total % d d Eggs 10 35 300 0 729 1074 74.2 Nymphs I 7 4 3 3 1 18 1.2 Nymphs II 15 5 18 1 1 40 2.8 Nymphs III 8 16 30 4 2 60 4.1 Nymphs IV 24 14 8 2 1 49 3.4 Nymphs V 76 37 26 1 5 145 10.0 Females 15 4 20 1 2 42 2.9 Males 8 3 6 0 3 20 1.4 Total 163 118 411 12 744 1448 100.0 a b Time used during direct roof search: nine participants /10 hours = 1.11 hour/person T 1 6 c ime used with an electric vacuum cleaner roof search: two participants = h Odontomachus min. Ligaeidae Collected coPiralidaemposition : triatomines, 522 grams of trash and 538 grams of paper; spp (Formicidae; Hymenoptera), ( ) ( ) dHemiptera , Lepidoptera were the associated fauna found. Corium Reyes-Lugo M et al./Asian Pac J Trop Biomed 2011; 1(4): 279-284 282 doors. The toilet and hygiene conditions of the inhabited Domiciliation of triatomines can be visualized as areas were deemed appropriaT.te .maculata an expansion of the evolutionary plan from predator The largest colony of T. rapicauda next to a small to a particular area within a habitat occupied by a ( ) population of the geckos ’ 20 individuals hematophagous organism, whe“re th”e domestic habitat merely was discovered on the building s roof, which was an area symbolizes a specific type of bed prepared by vertebrates. containing wooden, plastic and metallic sheets in a scattered The course of action is a specialized one and given that fashion. Between these sheets, an accumulation of dirt, dried it appears to engage generalizations such as genetics in leaves (4 kg) and rust (8 kg) was found. addition to morphological characters, it is possible to accept The mean temperature and relative humidity registered in the process to be permanent[16]. the three consecutive days (April 19-21, 2007; 14:00 h) inside the Chagas disease mainly occurs in the poor, rural areas aparT.tm maculataent, exactly below the improvised roof of sheets where of Mexico, Central and South America and in very rare the colony, was (29.65暲3.46) 曟 and (54.21暲12.58)%, occasion in the Southern United States[17]. In Central and respectively. South America, these blood sucking bugs are consequences 3.2. Capture and age structure of the T. maculata domiciliary of human activities intruding on the original habitats of populations these insects, which lead to the formation of mosaic areas of vegetation coverage next to homes. These environmental alterations affect the populations of wild triatomines when The results of the captureT.d maculatatriatomine s are presented in reducing their living areas and their food sources, so that the Table 1. The total number of was 1 448 and eggs ultimate effect is the establishment of triatomine populations collected inside the apartment complex acount for 74.2% in peridomicile and intradomicile[18]. In addition, the (1 074 eggs), Nymphs were 21.5%, and adults were 4.3%. All distribution and dispersion of the triatomines has also the captured triatomines were engorged with blood, with been associated with the change in climatic conditions, the exception of two newly emerged adults (1 female and 1 biogeographical aspects, and the nature of the shrubbery ) [19] male evidenced by the nymph V exhuvia foundT. n maculataext to the environment . captured adults. During the inspection of the The following characteristics play key roles in developing nest, a gecko burrow was discovered with 20 individuals domicile triatomine populations: (1) similar microclimatic (another gecko was seen escaping), varying in ages and sizes, conditions of homes to the natural ecotopes, particularly and also including some eggs (Figure 2). the temperature and relative humidity, (2) scarcity of wild Thirteen nymphs were manually captured by the animals for blood feeding, and (3) drastic environmental inhabitants in the apartment complex and brought to modifications to their natural habitats forcing them to seek the Tropical Medicine Institute where the entomological shelter next to homes. The persistence of these stimuli will inspection was carried out. Ten triatomines were located allow triatomine populations to better adaptation to that in the space between the two mattresses occupied by the habitat once the colonizing process has been initiated[18]. children, and the mother captured three at the moment that Some of the original wild triatomines thaP.t h geniculatusave adapted the triatomines were ingurgitating on one of the children. fairlyEratyrus well to mucronatusrecent domiciliation are: Panstrongylus rufotuberculatusand inTriatoma Venezue ldimidiataa; Triatoma infestansin Colombia; Triatoma in Costa Rrubovariaica; Triatomain Paragu asordiday and B razil; Triatoma guasayana in Uruguay; Triatoma maculataand in Argentina; in Brazil and [5,19-24] Colombia . T. maculata Many of the locations where is currently present have different levels of human interventions, such as housing construction and farming areas, the main factors of the original habitat modifications for this triatomine. In Veneázuela, in píarticular, they are found in the states of Aínzo tegui, Bol var, Lara, Mí iranda, Nueñva Esparta (Antol n del Campo, Marcano, D az and Mari o municipalities) and Sucre. These triatomines, contrarily to past observations, have increased their presence in domiciles and peridomiciles in different towns throughout these VeneT.zu maculataelan states. For instance, in the Venezuelan Figure 2. T. rapicauda T. maculata T.Gu acruziyana , Triatoma wrangelias found naturally infected with A gecko captured in a nest, in an and [25]. The disappearance of apartment complex in Pitahaya, Miranda state. To the bottom right of their natural habitats has occurred in parallel with the the photo, another gecko can be seen escaping. disappearance of their natural feeding sources. Alternatively, it is considered that this condition could favor its biotic 4. Discussion potential because it increases the contact frequency with the blood of mammals in peri and intradomicile[10], which possesses epidemiological importance in Chagas disease Reyes-Lugo M et al./Asian Pac J Trop Biomed 2011; 1(4): 279-284 283 í transmission. In Talaigua Nuevo (Bol var, Colombia), it it is common to observe in Center and South America was demonstrated that this species verified the life cycle reptiles of the Gekkonidae family colonizing homes located ( ) inside the domT.i ccruziile, feeding on mammals, reaching a in areas occupied by tropical forests dry and rainy . This 58.3% index of natural infection, thus taking on the colonization could be considered as a mechanism that responsibility for the intradomicile transmission of this fa cT.il irapicaudatates the domiciliation of triatomines. protozoan. In Venezuela immature stages of triatomines have is usually associated to debris and corrugated been observed feeding on mammals inside homes; however, metallic roofs in abandoned constructions[36], which T. cruzi [25,26] resulting negative to T. imaculatanfection . corresponds with the current work. These geckos have been Other indicatives of the biotic potential could described in rainy, humid and dry primary and secondary be the fact that it can multiply in conditions of low humidity tropical forests, from 0 to 650 m altitude. They are a and relatively high temperature[27] and their proven ability nocturnal species usually found around house lights, where [28] to feed on lizards and snakes . TT.hi smaculata would explain the they can be found feeding on insects. This situation can findings in this current work of 1 448 specimens possess particular relevance for the indirect transmission of 20 at different developT.m erapicaudant stages co-inhabiting with Chagas diseases in those communities that are located near specimens of geckos ( ). these ecosystems; for they have been known to travel freely Furthermore, the distribution of these individuals to and from these communities. collected in different development stages is in agreement Nowadays, at least in Venezuela, it is relatively more with the population levels described for this species found common to observe populations of peri or intradomiciliary in henhouses in Brazil and with a population equivalent geckos thanT. p emaculataridomiciliary pigs and hens in the area tRhodniuso that rep oprolixusrted for a typical domiciliary speT.cie maculatas such as occupied by . The association triatomine-gecko [8,9]. In Roraima (Brazil), in the domestic environment could have implications of was the most numerous species found in henhouses, with high importance for intradomiciliary transmission of Chagas a peridomiciliary infestation index of 16.7% (number of disease due to its eclectic alimentary habits on birds, reptiles triatomines captured/number of captured 暳 100) and a and mammals. It has been reported that trypanosomes are crowding index of 12 500% (number of triatomines captured/ able to infect reptiles[37,38]. These investigators successfully 100)[17] numT.b emaculatar of houses 暳 . infected reptiles with parasites from patients with is considered to be responsible for trypanosomiasis, verifying that reptiles could etb eal reservoirs maintaining the domestic cycle of Chagas disease in the for human trypanosomes. Furthermore, Njagu [39] found peridomicile environmenT.t i ncruzi the towns where it has been pathogenic mammalian trypanosomes in monitor lizards in detected[8-29], with their natural infection indexes an endemic area for human trypanosomiasis, substantiating varying from 0% to 58.3%[23,29]. This peridomiciliation is that reptiles are reservoirs for these parasites. of particular interest in Chagas disease transmission. The matter becomes more prominence, reT.c arapicaudalling the work The adaptation of vector species to human dwellings in done by Medina[40], in which he found that was ( defT.or ecruzisted areas is thought to be linked to recent findings easily infected with Leishmania parasites a Trypanosomatid of in human populations in the Amazon[30,31] where protozoa-related) add to this that parasites can invade the the low frequency of human autochthonous cases of Chagas bloodstream in reptiles, we can understand the interest of disease contrasts with the high infection index found in deepening the study on lizards and clarify their status as [32] reservoirs and vec’tors . potential reservoirs of human trypanosomiasis. The triatomines colonization strategy to the contemporary Although, in this particular study, thT.e tcruziriatomines found peri-urban domicile appears novel if taken into feeding on the geckos were negative for , the fact that consideration with the existing knowledge, which points out geckos provide a source of food for these triatomines in these that the process of colonization of the domestic environment domesticated areas could indirectly pose problematic in the by these insects normally begins in the peridomiciliary spread of Chagas disease. All of these findings may have surroundings. These surrounding include the housings of significant repercussions on potential policies to control domestic animals or in the burRattusrows o rattusf small synanthropics Chagas disease, and could also explain earlier outbreaks of ( ) mDidelphisammals s umarsupialisch as pigs, rodents and marsupials human trypanosomiasis in Venezuela. ( ) . The latter two are thosT.e mcruziost frequently cited, which are also considered as Conflict of interest statement reservoirs in the urban environment[33]. Today, triatomines have been observed to be associated with wild or domestic birds, and in rare opportunities with We declare that we have no conflict of interest. mammals [21,23], validating the discovery in this report as the first descriptionT., tmaculatao our knowledge, of co-hT.ab rapicaudaitation between Acknowledgements the triatomine T. rapicauda and the gecko . The gecko, , is a depredatory opportunist species that feeds mainly on insects. The possibility to We would like to thank the family of Pitahaya Town who feed on triatomines comes about through their reported kindly allowed us to conduct this study in the building. consumption of other invertebrates such as terrestrial [34,35] moT.ll urapicaudasks and arachnids . References has a wide geographical distribution. 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