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Human Cultural Practices Illuminate the Blood Meal Sources of Cave Dwelling Chagas Vectors (Triatoma Dimidiata)In Guatemala and Belize

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Human Cultural Practices Illuminate the Blood Meal Sources of Cave Dwelling Chagas Vectors (Triatoma Dimidiata)In Guatemala and Belize Hunting, Swimming, and Worshiping: Human Cultural Practices Illuminate the Blood Meal Sources of Cave Dwelling Chagas Vectors (Triatoma dimidiata)in Guatemala and Belize Lori Stevens1*, M. Carlota Monroy2, Antonieta Guadalupe Rodas2, Patricia L. Dorn3 1 Department of Biology, College of Arts and Sciences, University of Vermont, Burlington, Vermont, United States of America, 2 Escuela de Biologia, Universidad de San Carlos de Guatemala, Ciudad de Guatemala, Guatemala, 3 Department of Biological Sciences, Loyola University New Orleans, New Orleans, Louisiana, United States of America Abstract Background: Triatoma dimidiata, currently the major Central American vector of Trypanosoma cruzi, the parasite that causes Chagas disease, inhabits caves throughout the region. This research investigates the possibility that cave dwelling T. dimidiata might transmit the parasite to humans and links the blood meal sources of cave vectors to cultural practices that differ among locations. Methodology/Principal Findings: We determined the blood meal sources of twenty-four T. dimidiata collected from two locations in Guatemala and one in Belize where human interactions with the caves differ. Blood meal sources were determined by cloning and sequencing PCR products amplified from DNA extracted from the vector abdomen using primers specific for the vertebrate 12S mitochondrial gene. The blood meal sources were inferred by $99% identity with published sequences. We found 70% of cave-collected T. dimidiata positive for human DNA. The vectors had fed on 10 additional vertebrates with a variety of relationships to humans, including companion animal (dog), food animals (pig, sheep/goat), wild animals (duck, two bat, two opossum species) and commensal animals (mouse, rat). Vectors from all locations fed on humans and commensal animals. The blood meal sources differ among locations, as well as the likelihood of feeding on dog and food animals. Vectors from one location were tested for T. cruzi infection, and 30% (3/10) tested positive, including two positive for human blood meals. Conclusions/Significance: Cave dwelling Chagas disease vectors feed on humans and commensal animals as well as dog, food animals and wild animals. Blood meal sources were related to human uses of the caves. We caution that just as T. dimidiata in caves may pose an epidemiological risk, there may be other situations where risk is thought to be minimal, but is not. Citation: Stevens L, Monroy MC, Rodas AG, Dorn PL (2014) Hunting, Swimming, and Worshiping: Human Cultural Practices Illuminate the Blood Meal Sources of Cave Dwelling Chagas Vectors (Triatoma dimidiata) in Guatemala and Belize. PLoS Negl Trop Dis 8(9): e3047. doi:10.1371/journal.pntd.0003047 Editor: Eric Dumonteil, Universidad Auto´noma de Yucata´n, Mexico Received October 2, 2013; Accepted June 16, 2014; Published September 11, 2014 Copyright: ß 2014 Stevens et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: This study received financial support from NeTropica (www.netropica.org), National Institutes of Health (USA) Grant 1R15 A1079672-01A (http://www. nih.gov), and NSF grant BCS-1216193 as part of the joint NSF-NIH-USDA Ecology and Evolution of Infectious Diseases program (http://www.nsf.gov). Any opinions, findings, and conclusions or recommendations expressed in this material are those of the authors and do not necessarily reflect the views of the funding agencies. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. * Email: [email protected] Introduction popular tourist attraction and workers are known to sleep in the caves to guard against vandalism. Although bat guano is harvested Humans have been attracted to caves for much of our history in many Latin American countries and the United States, our for purposes as varied as religious ceremonies to simply shelter. In study did not include locations where this occurs. Guatemala people use caves for several cultural practices including The parasite that causes Chagas disease, Trypanosoma cruzi,is religious ceremonies, tourism, and shelter [1]. In the department transmitted by blood feeding triatomine insects [2]. These vectors of Pete´n in northern Guatemala, caves are often used by hunters are generally wide-ranging feeders and what they feed on is an for sleeping and shelter from rain, especially in the rainy season. important aspect of epidemiological risk; for example, human Also in northern Guatemala, caves in the department of Alta blood meals may mean increased risk of transmission to humans Verapaz are sacred places and sometimes the site of Mayan [3]. religious ceremonies; tourists also visit some caves. The religious The species Triatoma dimidiata is currently the major vector of ceremonies occur seasonally and are associated with periodic Chagas disease in Central America [4]. Some vector populations pilgrimages. In Belize, the Rio Frio caves in the Cayo District are a are found entirely in sylvan ecotopes, including caves; whereas PLOS Neglected Tropical Diseases | www.plosntds.org 1 September 2014 | Volume 8 | Issue 9 | e3047 Blood Meal Sources of Cave Triatoma dimidiata Author Summary important because it takes vectors some time to emerge from hiding spots, presumably attracted by CO exhaled by the Caves have enduring appeal to humans, and their lure in searchers. Triatomine nymphs in these caves are pale colored Central America includes tourism, religious ceremonies compared to nearby non-cave vectors, and have been observed to and shelter. The major Chagas disease vector in this emerge from hiding in cracks and crevices of the cave walls and region, Triatoma dimidiata, inhabits caves throughout its ceiling within a half hour following humans entering the cave. range. We challenge the assumption that cave-dwelling Adults are darker in color and easy to see in the caves because of vectors are not important for human transmission by the contrast with the limestone walls. Vectors were identified as T. determining blood meal sources of vectors collected in dimidiata sensu lato based on published taxonomic keys [11]. caves from three locations that differ in the activities of The human cultural practices in the caves differ among humans at the caves, and link the results to cultural practices that differ among locations. Seventy percent of locations. Near the municipality of San Luis, Pete´n, insect vectors cave-collected vectors were positive for human DNA, and were collected from a small cave located on a privately owned fed on 10 additional vertebrates with relationships to cattle farm. This particular cave was selected because the owner of humans varying from companion animal (dog), food the farm requested a survey to find the origin of vectors found in animals (pig, sheep/goat), wild animals (duck, bat, opos- their home. Access to the cave is restricted and only local hunters sum) to commensal animals (mouse, rat). Feeding sources and farm workers know of the cave; however, feral dogs from the relate to human activities that vary among locations, for nearby village may enter the cave in the rainy season. In Pete´n, example, human and food animals were the main sources hunting is a traditional weekend entertainment and caves are in Cahabo´n caves, located within deforested areas that are frequently used as overnight shelters. In this region, caves are not now agricultural fields and houses. We tested vectors from used for religious purposes and although hunters and their dogs one location for infection with the Chagas disease parasite may sleep and seek shelter in the caves, domesticated animals and found 30% (3 of 10) infected, including two of the other than dogs are not brought to caves. There are no houses three vectors from this location that had evidence of near the cave, it is surrounded by pasture areas for cattle. human blood. Humans should be aware of potential In Alta Verapaz, caves near Lanquı´n and Cahabo´n were consequences of visiting and sleeping in caves. examined. Grutas de Lanquı´n, a complex of caves known to be infested with T. dimidiata [12] was chosen because the main cave others are nearly entirely domesticated and some move between is a tourist attraction and is used for Mayan religious ceremonies. ecotopes [5–9]. It is generally thought that sylvan vectors are not The Lanquı´n River runs through the center of the cave. important for human transmission; however, few data are Thousands of bats inhabiting the cave provide a popular daily available to support this assumption. It is important to know if tourist attraction as they leave en masse at twilight. Ceremonial they are feeding on humans to help prevent transmission and to stone altars within the cave are still used by local residents for target control. Mayan religious ceremonies that are performed at night. Candles Because Chagas disease is the most economically important and offerings to the gods are found inside the cave. There are parasitic disease in Latin America with 8–10 million persons several cave entrances but municipality guards control access. infected [10], we decided to investigate the potential role of cave Human houses are located nearby. dwelling T. dimidiata in transmission of T. cruzi to humans. To Santa Maria cave, in the municipality of Cahabo´n, maintains investigate the possibility that cave-dwelling, sylvatic, T. dimidiata the tradition of seasonal pilgrimages organized by descendants of contribute to the human transmission cycle, we determined the the Maya. Travelers leave offerings to the gods in the cave, blood meal sources of T. dimidiata collected from caves in three including sacrificial animals, pottery, candles, liquor, plant resins, regions of Central America where T. dimidiata is the main vector. and tamales. There are houses near the one main entrance to the We tested the hypothesis that T.
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