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      Marking Triatoma brasiliensis, Triatoma pseudomaculata and Rhodnius nasutus Nymphs with Trace Elements: Element Persistence and Effects of Marking on Insect Mortality

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          Abstract

          Background

          Field ecologists often rely on mark-release-recapture (MRR) experiments to estimate population dynamics parameters for a given species. In the case of a medically important taxon, i.e., a disease vector, inferences on species survival and dispersal rates are particularly important as they have the potential to provide insights into disease transmission dynamics in endemic areas. Medical entomologists have traditionally used fluorescent dusts to externally mark the cuticle of insects. However, dust marking is usually restricted to the adult life stage because immature insects lose the mark when they molt.

          Methodology/Principal Findings

          We evaluated the efficacy of 13 trace elements in marking nymphs of three native Brazilian Chagas disease vectors: Triatoma brasiliensis, Triatoma pseudomaculata, and Rhodnius nasutus. Cr and Cu were detected in over 97% of T. brasiliensis (34/35 31/31 for Cr and Cu), while Cu and Mn were detected in more than 95% of T. pseudomaculata (29/29 for Cu and 28/29 for Mn) tested 120 days after marking. Only Mn marked over 90% of R. nasutus nymphs (38/41). Overall, trace elements had no negative effects on T. pseudomaculata longevity, but As-marked T. brasiliensis nymphs (p<0.01), and Cd-marked R. nasutus nymphs (p<0.01) had significantly shorter lifespan.

          Conclusions/Significance

          Previous evidence shows that there is little or no genetic differentiation between populations at the microgeographic level, which often precludes indirect estimations of dispersal capability based on genetic markers. In such situations, MRR studies are more suitable as they measure insect movement directly from one site to another, instead of effective migration (i.e. gene flow). The determination of a reliable and persistent marking method is the first step towards the development of meaningful ecological estimates through the application of MRR methodology. Here, we have identified trace elements that can be used for mark and recapture studies of three triatomine species in Brazil.

          Author Summary

          Mark, release and recapture (MRR) is one of the most powerful techniques employed by field ecologists, and is used to provide relevant estimates of natural populations such as dispersal, survival rates, and population densities. A reliable, persistent and effective marking method is a sine qua non condition to conduct a MRR experiment. Despite their relevance as Chagas disease vectors in the Americas, triatomine bugs have seldom been subjected to MRR studies. So far, estimates on triatomine dispersal have largely relied on molecular/genetic approaches, which are not direct measurements of the distance between the release and recapture point. We evaluated the persistence and efficiency of trace elements, chemicals present in very low quantities in the organism of a targeted species, to mark the nymphs of three Chagas disease vectors of the Brazilian caatinga biome, Triatoma brasiliensis, T. pseudomaculata, and Rhodnius nasutus. At least one trace element was shown to be a good marker for each triatomine species: more than 97% of T. brasiliensis were still marked with Cr and Cu after 120 days; more than 95% of T. pseudomaculata were marked with Cu and Mn and more than 90% of R. nasutus were marked with Mn 120 days after marking. Only As-marked T. brasiliensis and Cd-marked R. nasutus nymphs had significantly shorter lifespan. We believe these findings show that trace elements are a reliable and persistent marking method for triatomine nymphs and hope this is the first step towards the development of meaningful ecological estimates through the application of the MRR methodology.

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          Most cited references28

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          Efficient genetic markers for population biology.

          Population genetics has come of age. Three important components have come together: efficient techniques to examine informative segments of DNA, statistics to analyse DNA data and the availability of easy-to-use computer packages. Single-locus genetic markers and those that produce gene genealogies yield information that is truly comparable among studies. These markers answer biological questions most efficiently and also contribute to much broader investigations of evolutionary, population and conservation biology. For these reasons, single-locus and genealogical markers should be the focus of the intensive genetic data collection that has begun owing to the power of genetics in population biology.
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            The main sceneries of Chagas disease transmission. The vectors, blood and oral transmissions - A comprehensive review

            This review deals with transmission of Trypanosoma cruzi by the most important domestic vectors, blood transfusion and oral intake. Among the vectors, Triatoma infestans, Panstrongylus megistus, Rhodnius prolixus, Triatoma dimidiata, Triatoma brasiliensis, Triatoma pseudomaculata, Triatoma sordida, Triatoma maculata, Panstrongylus geniculatus, Rhodnius ecuadoriensis and Rhodnius pallescens can be highlighted. Transmission of Chagas infection, which has been brought under control in some countries in South and Central America, remains a great challenge, particularly considering that many endemic countries do not have control over blood donors. Even more concerning is the case of non-endemic countries that receive thousands of migrants from endemic areas that carry Chagas disease, such as the United States of America, in North America, Spain, in Europe, Japan, in Asia, and Australia, in Oceania. In the Brazilian Amazon Region, since Shaw et al. (1969) described the first acute cases of the disease caused by oral transmission, hundreds of acute cases of the disease due to oral transmission have been described in that region, which is today considered to be endemic for oral transmission. Several other outbreaks of acute Chagas disease by oral transmission have been described in different states of Brazil and in other South American countries.
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              Short report: dispersal of Aedes aegypti in an urban area after blood feeding as demonstrated by rubidium-marked eggs.

              Strategies for the control of Aedes aegypti during urban outbreaks of dengue or yellow fever assume that this species has a maximum flight range of 50-100 meters. Because Ae. aegypti distributes its eggs among several oviposition sites, we postulated that dispersal is driven by the search for oviposition sites, so an ovipositing female may have to fly much further than 50-100 meters to lay all of her eggs. We developed a method for marking Ae. aegypti eggs with a rare alkali metal (rubidium) and showed that in an urban area, oviposition activity in a single gonotrophic cycle lasts several days and covers an area at least 840 meters in diameter (55.4 hectares). We suggest that current practice for the control of dengue and yellow fever transmission by focal treatments with insecticides 50-100 meters around presumed or confirmed cases is unlikely to be effective. Moreover, source reduction (the elimination of breeding sites) may enhance dissemination of virus-infected mosquitoes by reducing the number of available oviposition sites.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Negl Trop Dis
                PLoS Negl Trop Dis
                plos
                plosntds
                PLoS Neglected Tropical Diseases
                Public Library of Science (San Francisco, CA USA )
                1935-2727
                1935-2735
                30 March 2016
                March 2016
                : 10
                : 3
                : e0004548
                Affiliations
                [1 ]Laboratório de Transmissores de Hematozoários, Instituto Oswaldo Cruz, Fiocruz, Rio de Janeiro, Brazil
                [2 ]Laboratório de Ecoepidemiologia da Doença de Chagas, Instituto Oswaldo Cruz, Fiocruz, Rio de Janeiro, Brazil
                [3 ]Laboratório de Desenvolvimento Analítico, Departamento de Química Analítica, Instituto de Química, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil
                [4 ]Laboratório de Epidemiologia e Sistemática Molecular, Instituto Oswaldo Cruz, Fiocruz, Rio de Janeiro, Brazil
                University of Perugia, ITALY
                Author notes

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: CVB OS MML RMdF. Performed the experiments: CVB OS ASF RES. Analyzed the data: CVB ASF MRD RES FAM RMdF. Contributed reagents/materials/analysis tools: OS RES MML. Wrote the paper: FAM RMdF.

                Article
                PNTD-D-15-01680
                10.1371/journal.pntd.0004548
                4814127
                27027503
                4b368f7f-9fa5-4baf-a7bc-9a6c8b04e215
                © 2016 Valença-Barbosa 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.

                History
                : 1 October 2015
                : 24 February 2016
                Page count
                Figures: 6, Tables: 5, Pages: 16
                Funding
                FAM received a grant from the MCTI/CNPq/MS-SCTIE—Decit 40/2012, Grant 404522/2012-2. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Physical Sciences
                Chemistry
                Analytical Chemistry
                Trace Elements
                Biology and Life Sciences
                Organisms
                Animals
                Invertebrates
                Arthropoda
                Insects
                Medicine and Health Sciences
                Epidemiology
                Disease Vectors
                Insect Vectors
                Biology and Life Sciences
                Developmental Biology
                Metamorphosis
                Nymphs
                Medicine and Health Sciences
                Epidemiology
                Disease Vectors
                Triatoma
                Biology and Life Sciences
                Anatomy
                Body Fluids
                Blood
                Medicine and Health Sciences
                Anatomy
                Body Fluids
                Blood
                Biology and Life Sciences
                Physiology
                Body Fluids
                Blood
                Medicine and Health Sciences
                Physiology
                Body Fluids
                Blood
                Medicine and Health Sciences
                Hematology
                Blood
                Medicine and Health Sciences
                Epidemiology
                Disease Vectors
                Research and Analysis Methods
                Model Organisms
                Animal Models
                Rhodnius
                Medicine and Health Sciences
                Epidemiology
                Disease Vectors
                Insect Vectors
                Rhodnius
                Biology and Life Sciences
                Organisms
                Animals
                Invertebrates
                Arthropoda
                Insects
                Rhodnius
                Custom metadata
                All relevant data are within the paper.

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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