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The heat emitted by the host body constitutes a short distance orientation cue for most blood-sucking insects, as is the case of the kissing-bug Rhodnius prolixus. We evaluated here how kissing bugs assess the distance to a warm target, in order to reach it by displaying the Proboscis Extension Reflex (PER). We confronted blind-folded insects to a thermal source either at 35° or at 40 °C under both, open- and closed-loop conditions. The results showed that nymphs were able to estimate the distance to a thermal source just using thermal information. Free walking insects displayed PER with a maximum frequency at 5 mm from the object, even without touching it. Yet, our experiments showed that the insects need to walk freely to estimate the distance to the source accurately, i.e. performing the PER at a distance allowing them to reach the target with the tip of the proboscis. The distance at which PER was triggered was independent of the temperature of the thermal source (35° or 40 °C). Moreover, our results also unravelled that mechanical stimuli can be integrated with thermal cues, being capable of affecting the triggering of PER in kissing bugs. This is the first study providing evidence that blood-sucking vector insects use mechanoreception for eliciting their bites. We discuss our findings in the light of present models explaining the ability of kissing bugs to estimate the distance and the temperature of a potential food sources.

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Insects are the most evolutionarily and ecologically successful group of living animals, being present in almost all possible mainland habitats; however, they are virtually absent in the ocean, which constitutes more than 99% of the Earth's biosphere. Only a few insect species can be found in the sea but they remain at the surface, in salt marshes, estuaries, or shallow waters. Remarkably, a group of 13 species manages to endure long immersion periods in the open sea, as well as deep dives, i.e., seal lice. Sucking lice (Phthiraptera: Anoplura) are ectoparasites of mammals, living while attached to the hosts' skin, into their fur, or among their hairs. Among them, the family Echinophthiriidae is peculiar because it infests amphibious hosts, such as pinnipeds and otters, who make deep dives and spend from weeks to months in the open sea. During the evolutionary transition of pinnipeds from land to the ocean, echinophthiriid lice had to manage the gradual change to an amphibian lifestyle along with their hosts, some of which may spend more than 80% of the time submerged and performing extreme dives, some beyond 2000 m under the surface. These obligate and permanent ectoparasites have adapted to cope with hypoxia, high salinity, low temperature, and, in particular, conditions of huge hydrostatic pressures. We will discuss some of these adaptations allowing seal lice to cope with their hosts' amphibious habits and how they can help us understand why insects are so rare in the ocean.

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Lice from pinnipeds - sea lions, seals and walruses - are the only insects capable of surviving marine dives. Throughout their evolutionary history, they have adapted to tolerate hypoxia, high salinity, low temperature and, in particular, to tolerate conditions of high hydrostatic pressure. To understand the limits of the capacity of lice to survive during host deep dives, we conducted a series of controlled experiments in the laboratory. We collected lice from elephant seals and submitted the different life stages to high pressure conditions. Lice were first exposed to one of four hydrostatic pressures: 30, 80, 150 or 200 kg cm-2 They were then exposed a second time to higher or lower hydrostatic pressure conditions to test for the impact of the first experience, which could either be deleterious or trigger physiological adaption, allowing them a better tolerance to high pressure. We found that lice from elephant seals can tolerate hydrostatic pressures higher than 200 kg cm-2 (close to 200 atm), which is equivalent to 2000 m depth. Adults exhibited lower recovery times than nymphs after immersion at high hydrostatic pressure. Our findings show that lice have developed unique adaptations to endure extreme marine conditions. We discuss these extreme performances in relation to the morphological characteristics and physiological responses to diving in these insects.

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Major emergency efforts are being mounted for each vector-borne disease epidemiological crisis anew, while knowledge about the biology of arthropods vectors is dwindling slowly but continuously, as is the number of field entomologists. The discrepancy between the rates of production of knowledge and its use and need for solving crises is widening, in particular due to the highly differing time spans of the two concurrent processes. A worldwide web based search using multiple key words and search engines of onsite and online courses in English, Spanish, Portuguese, French, Italian and German concerned with the biology of vectors identified over 140 courses. They are geographically and thematically scattered, the vast majority of them are on-site, with very few courses using the latest massive open online course (MOOC) powerfulness. Over two third of them is given in English and Western Africa is particularity poorly represented. The taxonomic groups covered are highly unbalanced towards mosquitoes. A worldwide unique portal to guide students of all grades and levels of expertise, in particular those in remote locations, is badly needed. This is the objective a new activity supported by the Special Programme for Research and Training in Tropical Diseases (TDR).

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Major emergency efforts are being mounted for each vector-borne disease epidemiological crisis anew, while knowledge about the biology of arthropods vectors is dwindling slowly but continuously, as is the number of field entomologists. The discrepancy between the rates of production of knowledge and its use and need for solving crises is widening, in particular due to the highly differing time spans of the two concurrent processes. A worldwide web based search using multiple key words and search engines of onsite and online courses in English, Spanish, Portuguese, French, Italian and German concerned with the biology of vectors identified over 140 courses. They are geographically and thematically scattered, the vast majority of them are on-site, with very few courses using the latest massive open online course (MOOC) powerfulness. Over two third of them is given in English and Western Africa is particularity poorly represented. The taxonomic groups covered are highly unbalanced towards mosquitoes. A worldwide unique portal to guide students of all grades and levels of expertise, in particular those in remote locations, is badly needed. This is the objective a new activity supported by the Special Programme for Research and Training in Tropical Diseases (TDR).

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The thermal sense of triatomine bugs, vectors of Chagas disease, is unique among insects. Not only do these bugs exhibit the highest sensitivity to heat known in any animal up to date, but they can also perceive the infrared radiation emitted by the body of their warm-blooded hosts. The sensory basis of this capacity has just started to be unravelled. To shed additional light on our understanding of thermosensation, we initiated an analysis of the genetic basis of the thermal sense in Rhodnius prolixus. We tested the hypothesis that a TRPV (transient receptor potential vanilloid) channel receptor is involved in the evaluation of heat in this species. Two different approaches were adopted. Initially, we analysed the expression of a TRPV candidate for this function, i.e., RproIav, in different tissues. Subsequently, we tested the effects of capsaicin and capsazepine, two molecules known to interact with mammal TRPV1, using three different behavioural protocols for evaluating thermal responses: (1) proboscis extension response (PER), (2) thermopreference in a temperature gradient and (3) spatial learning in an operant conditioning context. Bioinformatic analyses confirmed that the characteristic features typical of the TRPV channel subfamily are found in the RproIav protein sequence. Molecular analysis showed that RproIav is expressed in R. prolixus, not only in the antennae, but also in other body structures bearing sensory organs. Behavioural experiments consistently revealed that capsaicin treated insects are less responsive to heat stimuli and prefer lower temperatures than non-treated insects, and that they fail to orient in space. Conversely, capsazepine induces the opposite behaviours. The latter data suggest that triatomine thermoreception is based on the activation of a TRP channel, with a similar mechanism to that described for mammal TRPV1. The expression of RproIav in diverse sensory structures suggests that this receptor channel is potentially involved in bug thermoreception. This constitutes solid evidence that thermosensation could be based on the activation of TRP receptors that are expressed in different tissues in R. prolixus. Whether RproIav channel is a potential target for the compounds tested and whether it mediates the observed effects on behaviour still deserves to be confirmed by further research.

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Despite the incredible success of insects in colonizing almost every habitat, they remain virtually absent in one major environment--the open sea. A variety of hypotheses have been raised to explain why just a few insect species are present in the ocean, but none of them appears to be fully explanatory. Lice belonging to the family Echinophthiriidae are ectoparasites on different species of pinnipeds and river otters, i.e. they have amphibious hosts, who regularly perform long excursions into the open sea reaching depths of hundreds of meters (thousands of feets). Consequently, lice must be able to support not only changes in their surrounding media, but also extreme variations in hydrostatic pressure as well as breathing in a low oxygen atmosphere. In order to shed some light on the way lice can survive during the diving excursions of their hosts, we have performed a series of experiments to test the survival capability of different instars of Antarctophthirus microchir (Phthiraptera: Anoplura) from South American sea lions Otaria flavescens, when submerged into seawater. These experiments were aimed at analyzing: (a) immersion tolerance along the louse life; (b) lice's ability to obtain oxygen from seawater; (c) physiological responses and mechanisms involved in survival underwater. Our experiments showed that the forms present in non-diving pups--i.e. eggs and first-instar nymphs--were unable to tolerate immersion in water, while following instars and adults, all usually found in diving hosts, supported it very well. Furthermore, as long as the level of oxygen dissolved in water was higher, the lice survival capability underwater increased, and the recovery period after returning to air declined. These results are discussed in relation to host ecology, host exploitation and lice functional morphology.

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BACKGROUND: Triatomine bugs are the insect vectors of Trypanosoma cruzi, the etiological agent of Chagas disease. These insects are known to aggregate inside shelters during daylight hours and it has been demonstrated that within shelters, the aggregation is induced by volatiles emitted from bug feces. These signals promote inter-species aggregation among most species studied, but the chemical composition is unknown. METHODOLOGY/PRINCIPAL FINDINGS: In the present work, feces from larvae of the three species were obtained and volatile compounds were identified by solid phase microextraction-gas chromatography-mass spectrometry (SPME-GC-MS). We identified five compounds, all present in feces of all of the three species: Triatoma infestans, Panstrongylus megistus and Triatoma brasiliensis. These substances were tested for attractivity and ability to recruit insects into shelters. Behaviorally active doses of the five substances were obtained for all three triatomine species. The bugs were significantly attracted to shelters baited with blends of 160 ng or 1.6 µg of each substance. CONCLUSIONS/SIGNIFICANCE: Common compounds were found in the feces of vectors of Chagas disease that actively recruited insects into shelters, which suggests that this blend of compounds could be used for the development of baits for early detection of reinfestation with triatomine bugs.

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Many arthropod species have adopted vertebrate blood as their main food source. Blood is rich in nutrients and, except for the presence of parasites, sterile. However, this food source is not freely available, nor is obtaining it devoid of risk. It circulates inside vessels hidden underneath the skin of mobile hosts that are able to defend themselves and even predate the insects that try to feed on them. Thus, the haematophagous lifestyle is associated with major morphological, physiological and behavioural adaptations that have accumulated throughout the evolutionary history of the various lineages of blood-sucking arthropods. These adaptations have significant consequences for the evolution of parasites as well as for the epidemiology of vector-transmitted diseases. In this review article, we analyse various aspects of the behaviour of triatomine bugs to illustrate how each behavioural trait represents a particular adaptation to their close association with their hosts, which may easily turn into predators. Our aim is to offer to the reader an up-to-date integrative perspective on the behaviour of Chagas disease vectors and to propose new research avenues to encourage both young and experienced colleagues to explore this aspect of triatomine biology.

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Triatomines have been important model organisms for behavioural research. Diverse reports about triatomine host search, pheromone communication in the sexual, shelter and alarm contexts, daily cycles of activity, refuge choice and behavioural plasticity have been published in the last two decades. In recent times, a variety of molecular genetics techniques has allowed researchers to investigate elaborate and complex questions about the genetic bases of the physiology of insects. This, together with the current characterisation of the genome sequence of Rhodnius prolixus allows the resurgence of this excellent insect physiology model in the omics era. In the present revision, we suggest that studying the molecular basis of behaviour and sensory ecology in triatomines will promote a deeper understanding of fundamental aspects of insect and, particularly, vector biology. This will allow uncovering unknown features of essential insect physiology questions for a hemimetabolous model organism, promoting more robust comparative studies of insect sensory function and cognition.

Assuntos

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Many arthropod species have adopted vertebrate blood as their main food source. Blood is rich in nutrients and, except for the presence of parasites, sterile. However, this food source is not freely available, nor is obtaining it devoid of risk. It circulates inside vessels hidden underneath the skin of mobile hosts that are able to defend themselves and even predate the insects that try to feed on them. Thus, the haematophagous lifestyle is associated with major morphological, physiological and behavioural adaptations that have accumulated throughout the evolutionary history of the various lineages of blood-sucking arthropods. These adaptations have significant consequences for the evolution of parasites as well as for the epidemiology of vector-transmitted diseases. In this review article, we analyse various aspects of the behaviour of triatomine bugs to illustrate how each behavioural trait represents a particular adaptation to their close association with their hosts, which may easily turn into predators. Our aim is to offer to the reader an up-to-date integrative perspective on the behaviour of Chagas disease vectors and to propose new research avenues to encourage both young and experienced colleagues to explore this aspect of triatomine biology.

Assuntos

RESUMO

Triatomines have been important model organisms for behavioural research. Diverse reports about triatomine host search, pheromone communication in the sexual, shelter and alarm contexts, daily cycles of activity, refuge choice and behavioural plasticity have been published in the last two decades. In recent times, a variety of molecular genetics techniques has allowed researchers to investigate elaborate and complex questions about the genetic bases of the physiology of insects. This, together with the current characterisation of the genome sequence of Rhodnius prolixus allows the resurgence of this excellent insect physiology model in the omics era. In the present revision, we suggest that studying the molecular basis of behaviour and sensory ecology in triatomines will promote a deeper understanding of fundamental aspects of insect and, particularly, vector biology. This will allow uncovering unknown features of essential insect physiology questions for a hemimetabolous model organism, promoting more robust comparative studies of insect sensory function and cognition.

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We studied the behavioural response of body lice and head lice to white light. We also evaluated the influence of starvation and the presence of other individuals on this response. Experiments were performed in a rectangular arena, half of which was illuminated and the other half kept in the dark. Two experiments were performed: in the first, a single louse was released into the arena for 60 min and the percentage of time spent in the illuminated half was recorded; in the second experiment, a group of lice was released and the number of insects in the illuminated half was recorded. The results showed that the average number of lice and time spent in the illuminated side of the arena was statistically higher than for the controls. Starvation did not influence the reaction of lice, but the number of insects in the illuminated area did increase with the size of the group. This study shows that human lice are photopositive towards white light and that this behaviour is not affected by the nutritional state of the insects. Moreover, it is enhanced by the presence of other lice.

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The robber fly Mallophora ruficauda is one of the principal pests of apiculture in the Pampas region of Argentina. Larvae are solitary ectoparasitoids of third-instar scarab beetle larvae. Females of M. ruficauda do not lay eggs on or near the hosts, but on tall grasses. After hatching, larvae are dispersed by the wind and drop to the ground, where they dig and search for potential hosts. It is known that second-instar larvae of M. ruficauda exhibit active host-searching behaviour towards their preferred hosts, i.e., third-instar larvae of Cyclocephala signaticollis. Although host-location seems to be mediated by chemical cues, the mechanism of orientation and the sensory organs involved in host location remain unknown. We carried out behavioural experiments in the laboratory to address these questions. We also tested whether the orientation behaviour is exclusively based on the use of chemical cues. We found that larvae of M. ruficauda detect the chemicals with chemosensilla on the maxillary palps. Only one maxillary palp suffices for orientation, but their bilateral ablation abolishes orientation. Besides, an hexane extract of the host body was as attractive as a live host. Our results support that M. ruficauda larvae find their hosts underground by means of chemoklinotaxis.

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Living in close association with a vertebrate host and feeding on its blood requires different types of adaptations, including behavioural adjustments. Triatomines exhibit particular traits associated with the exploitation of their habitat and food sources and these traits have been the subject of intense analysis. Many aspects of triatomine behaviour have been relatively well characterised and some attempts to exploit the behaviours have been undertaken. Baited traps based on host-associated cues, artificial refuges and light-traps are some of the tools used. Here we discuss how our knowledge of the biology of Chagas disease vectors may help us sample and detect these insects and even increase the efficiency of control measures.

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Living in close association with a vertebrate host and feeding on its blood requires different types of adaptations, including behavioural adjustements. Triatomines exhibit particular traits associated with the exploitation of their habitat and food sources and these traits have been the subject of intense analysis. Many aspects of triatomine behaviour have been relatively well characterised and some attempts to exploit the behaviours have been undertaken. Baited traps based on host-associated cues, artificial refuges and light-traps are some of the tools used. Here we discuss how our knowledge of the biology of Chagas disease vectors may help us sample and detect these insects and even increase the efficiency of control measures.

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BACKGROUND: It is known that some blood-sucking insects have the ability to reach vessels under the host skin with their mouthparts to feed blood from inside them. However, the process by which they locate these vessels remains largely unknown. Less than 5% of the skin is occupied by blood vessels and thus, it is not likely that insects rely on a "random search strategy", since it would increase the probability of being killed by their hosts. Indeed, heterogeneities along the skin surface might offer exploitable information for guiding insect's bites. METHODOLOGY/PRINCIPAL FINDINGS: We tested whether the bug Rhodnius prolixus can evaluate temperature discontinuities along the body surface in order to locate vessels before piercing the host skin. When placed over a rabbit ear, the bug's first bites were mostly directed towards the main vessels. When insects were confronted to artificial linear heat sources presenting a temperature gradient against the background, most bites were directly addressed to the warmer linear source, notwithstanding the temperature of both, the source and the background. Finally, tests performed using uni- and bilaterally antennectomized insects revealed that the bilateral integration of thermal inputs from both antennae is necessary for precisely directing bites. CONCLUSIONS/SIGNIFICANCE: R. prolixus may be able to exploit the temperature differences observed over the skin surface to locate blood vessles. Bugs bite the warmest targets regardless of the target/background temperatures, suggesting that they do not bite choosing a preferred temperature, but select temperature discontinuities along the skin. This strategy seems to be an efficient one for finding blood vessels within a wide temperature range, allowing finding them on different hosts, as well as on different areas of the host body. Our study also adds new insight about the use of antennal thermal inputs by blood sucking bugs.

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The present paper reports for the first time the capture of wild Triatoma brasiliensis and Triatoma pseudomaculata by means of light traps in Brazil. We tested commercially available lighting devices powered by batteries to attract the bugs to a white piece of cloth in the field. Two main findings showed to be significant: first, the results presented here show that light traps can be used for sampling these species in wild environments; second, they reveal that house colonization by triatomines may also happen as a consequence of the arrival of flying sylvatic bugs guided by artificial light sources. In addition, we discuss the effect of some environmental and biological factors on triatomine flight activity modulation.

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Compounds from the metasternal and Brindley's glands of the blood-sucking bug, Triatoma infestans, were identified by solid phase microextraction (SPME) and gas chromatography-mass spectrometry. Volatile compounds released by adult bugs during copulation or after mechanical disturbance were also characterized. Six compounds were identified and found consistently in all samples from metasternal glands. The most abundant were 3-pentanone, 2-methylbutanol, 3-pentanol, and an unidentified compound. The metasternal gland blends did not differ qualitatively between sexes. Compounds found in Brindley's glands were short chain acids, alcohols, esters, and a ketone with no qualitative differences between sexes. Isobutyric acid was the main component of this blend, and two new confirmed compounds were described as products of these glands: 2-butanone and 2-methylbutyric acid. 3-Pentanone was collected from the headspace over 33% of the copulating pairs of T. infestans. Volatiles found in the headspace of disturbed T. infestans adults included short-chain fatty acids, alcohols, esters, and ketones, with no qualitative differences between sexes. Both types of glands apparently discharge their contents after disturbance. However, most of the volatiles released by bugs after disturbance came from Brindley's glands. The locomotor activity of fourth instars increased significantly after stimulation with the odors emitted by disturbed adults, as compared with larvae stimulated by the odor of undisturbed adults or by clean air. We also studied the directional behavioral response of fifth instars to the disturbance scent in a locomotion compensator. Larvae exposed to volatiles released by disturbed adults walked away from the direction of the odor. The results suggest that this blend or part of it functions as an alarm pheromone for T. infestans. We suggest that the metasternal glands of this species are involved both in the sexual and the alarm contexts, and that the Brindley's glands probably have both alarm and defensive roles.

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