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      Countercurrent heat exchange and thermoregulation during blood-feeding in kissing bugs

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          Abstract

          Blood-sucking insects experience thermal stress at each feeding event on endothermic vertebrates. We used thermography to examine how kissing-bugs Rhodnius prolixus actively protect themselves from overheating. During feeding, these bugs sequester and dissipate the excess heat in their heads while maintaining an abdominal temperature close to ambient. We employed a functional-morphological approach, combining histology, µCT and X-ray-synchrotron imaging to shed light on the way these insects manage the flow of heat across their bodies. The close alignment of the circulatory and ingestion systems, as well as other morphological characteristics, support the existence of a countercurrent heat exchanger in the head of R. prolixus, which decreases the temperature of the ingested blood before it reaches the abdomen. This kind of system has never been described before in the head of an insect. For the first time, we show that countercurrent heat exchange is associated to thermoregulation during blood-feeding.

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          Many insect species have adopted the blood of birds and mammals as their main or even only food. Yet, blood is not freely available in nature, but it circulates inside vessels hidden under the skin of animals much bigger than the insect and capable of defending themselves from getting bitten. To succeed in getting a meal, blood-sucking insects must be able to feed quickly and take in as much blood as possible. Each time that they do this, a huge amount of warm fluid enters their body in just a few minutes. The blood temperature can be up to 20° or 25°C warmer than the insect itself. Moreover, an insect called a kissing bug may ingest up to 10 times its own weight in only fifteen minutes. The consequence is overheating and potentially harmful thermal stress.

          Kissing bugs do not seem to suffer any harmful consequence of taking massive meals from warm-blooded animals. But why? The answer was unexpected: they simply do not warm up when they take a blood meal. However, it was not known how they manage to cool down the ingested blood.

          By combining classical methods of studying anatomy with state of the art technologies, Lahondère et al. discovered that kissing bugs possess a sophisticated heat exchanger inside their heads. It works by transferring the heat associated with the ingested blood to the haemolymph (insect blood); these fluids circulate in opposite directions inside ducts that are close to each other in the head.

          The discovery of a new system used by insects to cope with thermal stress expands our knowledge of insect physiology and opens new lines of research. The kissing bug heat exchanger could also serve as inspiration for equivalent technological systems. Last but not least, kissing bugs spread the parasites that cause Chagas disease in the Americas. Finding ways to disrupt the heat exchanger could prevent kissing bugs from feeding on blood, and so help to control the spread of disease.

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          Most cited references39

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          Integrating Thermal Physiology and Ecology of Ectotherms: A Discussion of Approaches

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            The Biology of Blood-Sucking in Insects

            M Lehane (2005)
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              • Record: found
              • Abstract: not found
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              Insect Thermoregulation

              M L A May (1979)
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                Author and article information

                Contributors
                Role: Reviewing Editor
                Journal
                eLife
                Elife
                eLife
                eLife
                eLife Sciences Publications, Ltd
                2050-084X
                21 November 2017
                2017
                : 6
                : e26107
                Affiliations
                [1 ]deptInstitut de Recherche sur la Biologie de l'Insecte UMR 7261 CNRS - Université François Rabelais ToursFrance
                [2 ]deptInstituto de Ciências Biológicas Universidade Federal de Minas Gerais Belo HorizonteBrazil
                [3 ]deptDepartment of Physiology, College of Medicine University of Saskatchewan SaskatoonCanada
                [4 ]Canadian Light Source Inc. SaskatoonCanada
                University of Cincinnati United States
                University of Cincinnati United States
                Author notes
                [§]

                Department of Biology, University of Washington, Seattle, United States.

                [†]

                These authors contributed equally to this work.

                [‡]

                These authors also contributed equally to this work.

                Author information
                https://orcid.org/0000-0003-3703-0302
                Article
                26107
                10.7554/eLife.26107
                5697934
                29157359
                049a1a6c-e33f-49ca-b041-047b81669194
                © 2017, Lahondère et al

                This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

                History
                : 16 February 2017
                : 22 October 2017
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100007526, Université François-Rabelais;
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100003593, Conselho Nacional de Desenvolvimento Científico e Tecnológico;
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100002322, Coordenação de Aperfeiçoamento de Pessoal de Nível Superior;
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100004901, Fundação de Amparo à Pesquisa do Estado de Minas Gerais;
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100000038, Natural Sciences and Engineering Research Council of Canada;
                Award ID: Discovery operating grant
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100001665, Agence Nationale de la Recherche;
                Award ID: ANR-08-MIE-007 EcoEpi
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100004794, Centre National de la Recherche Scientifique;
                Award Recipient :
                The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
                Categories
                Research Article
                Ecology
                Custom metadata
                A novel thermoregulatory mechanism in blood-sucking insects, vectors of human disease, is described using a functional-morphological approach.

                Life sciences
                thermoregulation,haematophagy,vector biology,functional morphology,insect physiology,rhodnius prolixus,other

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