The ability of Rhodnius prolixus (Hemiptera; Reduviidae) to approach a thermal source solely by its infrared radiation

doi:10.1016/S0022-1910(99)00163-8

Journal of Insect Physiology

Volume 46, Issue 5, May 2000, Pages 745-751

https://doi.org/10.1016/S0022-1910(99)00163-8 Get rights and content

Abstract

The ability of the haematophagous bug Rhodnius prolixus to approach a pure IR source only by its long-wave infrared radiation (IR) was investigated. To exclude any heated air from reaching the bug a cooled IR-transmitting window was placed between the IR-source (a Peltierelement heated to 35°C) and the bug. Starved bugs were tested under invisible short-wave IR illumination (λ<1 μm) in order to exclude also any visual cues. The number of bugs approaching the IR-source was significantly increased compared to the controls in which the IR-source was turned off (χ²-test, P<0.01). Our results show that Rhodnius prolixus can use infrared stimuli to find a host.

Introduction

Haematophagous bugs (Reduviidae) obligatory depend on the blood of vertebrates. Bloodsucking bugs of the genus Rhodnius and Triatoma are the vectors of Chagas disease. They detect and orient to thermal sources from distances up to several centimetres (Hase, 1932, Wigglesworth and Gillett, 1934, Núñez, 1987, Lazzari and Núñez, 1989). In order to be attractive, a thermal source must have a surface temperature close to that of warm blooded animals (Wigglesworth and Gillett, 1934, Fujita and Kloetzel, 1976, Lazzari, 1990, Flores and Lazzari, 1996). Behavioural experiments have shown that Triatoma infestans exhibits the highest thermal sensitivity known from all animals (Lazzari, 1990, Lazzari and Núñez, 1991). When the bugs are directly in front of a thermal source they usually extend their proboscis. This rostral reflex, which exclusively takes place in the context of feeding, i.e. immediately before a bug bites a host (Lazzari, 1990) does however not require a direct physical contact with a warm surface (Wigglesworth and Gillett, 1934).

It was assumed that bloodsucking bugs detect the warm air transported by convection and/or the temperature gradients which occur in the vicinity of all thermal sources. Special experiments made by Wigglesworth and Gillett (1934) to test infrared sensitivity yielded no indication that Rhodnius prolixus can perceive infrared (IR) radiation. However, recently Lazzari and Núñez (1989) published that Triatoma infestans can detect the IR-radiation emitted by a thermal source. In the presence of an IR-stimulus both antennal movements and the general locomotor activity were significantly increased. However, the temperatures of the filters interposed between the IR source and the bugs were measured with an accuracy of 0.1°C. It is known that insects can detect differences in air temperature of only a few hundredth of a degree (Altner and Loftus, 1985). Because Lazzari and Nunez cannot rule out that the filter temperature has increased by less than 0.1°C it is possible that the filter did provide an unwanted secondary heat source. In addition Lazarri and Nunez did not attempt to analyse whether unrestrained Chagas bugs do approach a pure IR-source.

The goal of the present paper was to test whether Rhodnius prolixus is sensitive to pure IR-radiation. In addition we investigated how these bugs approached an IR-source.

Section snippets

Experimental animals

Adult Rhodnius prolixus (body length 20 mm) were obtained from the breeding stock of the BAYER AG, Animal Health Division, Landwirtschaftszentrum Monheim (Leverkusen, Germany). Bugs were kept at room temperature (21–23°C: 40–50% r.h.) in a terrarium with sheets of zigzag-folded filter paper offering hiding-places. Animals had access to water and were exposed to a natural light–dark cycle 12L:12D (photophase 06.00–18.00 hr). Every four weeks we fed the bugs on rabbits at the Animal Health

Results

After removal of the upper part of the starting device and application of the breathing air stimulus all bugs which remained for at least 10 s on the platform were monitored for the next 10 min. Without the Peltierelement switched on, i.e. in the controls, 52 out of 60 bugs began to walk around, eight bugs remained in akinesis. Similar results were obtained with the Peltierelement switched on. Now 56 out of 60 bugs started to walk around, six remained in akinesis. Only those bugs which did not

Discussion

Bloodsucking bugs rely mainly on thermal and chemical cues for host finding (Núñez, 1982, Núñez, 1987, Lazzari and Núñez, 1991, Taneja and Guerin, 1995). Heat is one of the major cues used by triatomine bugs to locate a host (Hase, 1932, Wigglesworth and Gillett, 1934, Flores and Lazzari, 1996). Bloodsucking bugs are known to probe any warm surface provided its temperature is between 32 and 45°C (Lazzari, 1990). In Rhodnius prolixus biting can be evoked only by surface temperatures between 36

Acknowledgements

We thank Drs. G. Nentwig and M. Arnold of the Animal Health Division of the Bayer AG (Landwirtschaftszentrum Monheim in Leverkusen, Germany) for generously supplying us with Rhodnius prolixus and for giving the possibility to feed the bugs on rabbits. We are indebted to Dr. R. Zelick for his helpful comments and improvement of the English of an earlier draft of the manuscript. The graduate students A. Wallraff and J. Dahnke helped us with the time-consuming experiments. We are indebted to Prof.

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Cited by (46)

Triggering the proboscis extension reflex (PER) in Rhodnius prolixus
2021, Journal of Insect Physiology
Citation Excerpt :
The heat emitted by the body of warm-blooded vertebrates, represents a major cue for short-range orientation in blood-sucking arthropods (Lazzari, 2009; 2020;; Zermoglio et al., 2017). Kissing bugs vectors of Chagas disease (WHO, 2020), exhibit the highest thermal sensitivity known in animals (Lazzari, 2009) and they are the sole haematophagous insects in which the capacity to perceive radiant heat has been demonstrated (Lazzari and Núñez, 1989; Schmitz et al., 2000; Zopf et al., 2014a; 2014b). For these bugs, the thermal cue is the only host associated signal, both necessary and sufficient to induce the proboscis extension reflex (PER) and to induce them to bite an object (Wigglesworth and Gillett, 1934; Flores and Lazzari, 1996; Vinauger et al., 2013).
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.
Active dispersal in Triatoma infestans (Klug, 1834) (Hemiptera: Reduviidae: Triatominae): Effects of nutritional status, the presence of a food source and the toxicological phenotype
2020, Acta Tropica
In Argentina, the main vector of Chagas disease is Triatoma infestans (Klug, 1834). In recent years, the presence of T. infestans was reported in human dwelling after spraying with pyrethroids in several locations in Argentina. The presence of these insects can be attributed, among other factors, to colonization by bugs from sylvatic or peridomestic populations or to the evolution of resistance to insecticides. In both cases, the dispersal of insects is a determining factor. The aim was to determinate the interaction of dispersal with feeding, food resource and resistance to insecticides. Three nutritional states were obtained with the number of feeds (NF) offered (0, 1 or 2). The resistant females were evaluated only with NF1. The experimental arena was 10 m long and contained two shelters. Groups of 30 virgin females of each NF were released in one of the shelters and were able to move during 3 days/nights. Females without possibility of dispersal were the controls. Results showed that the individuals dispersed mainly walking regardless of the number of feeds, the presence of food resource and toxicological phenotype. This type of dispersal presented energy costs in susceptible individuals but not in resistant ones. The numbers of feeds that determined low nutritional states showed greater dispersal and activity associated with the shelter. The presence of a food source had an effect on the dispersal capacity and this depended on the number of feeds. There was a decrease in the dispersal in individuals with one feeding and an absence of response in fasted individuals and with two feeds. On the other hand, a lower dispersal tendency were found in resistant females compared to susceptible females, suggesting that resistance to deltamethrin is associated with adaptive costs.
The thermal sense of blood-sucking insects: why physics matters
2019, Current Opinion in Insect Science
Blood-sucking arthropods exploit multimodal information for locating and recognising potential hosts. The heat emitted by the body of endothermic vertebrates constitutes a major cue for orientation. To exploit it in a reliable way, insects must be able to deal with two variants of thermal information, that is heat exchange and temperature fluctuations. Evaluating whether or not an object qualifies as a host by its temperature requires solving thermodynamic ambiguities in a context where temperature increase at the receptor level is just one, yet insufficient, piece of information. To be exploitable, this piece of information needs to be integrated with other variables. Here, I discuss the physical constraints associated to thermal orientation, as well as the way different blood-sucking insects acquire and make use of heat to recognise a host.
Keeping cool: Kissing bugs avoid cannibalism by thermoregulating
2018, Journal of Insect Physiology
Kissing bugs possess a highly developed thermal sense and when starved, they attempt to bite any object which temperature is close to that of a warm-blooded host. At each feeding event, these insects take massive meals in just a few minutes. One could then expect fed-bugs being heated-up by the ingested warm blood and so becoming attractive to starved conspecifics. This is not however the case, arising the question about why cannibalism is very rare among these insects. Recently, the ability of thermoregulating during feeding has been demonstrated in Rhodnius prolixus. These bugs possess a countercurrent heat-exchanger that cools down the ingested blood, before it reaches the abdomen. We hypothesise that avoiding thermal stress is not the only adaptive advantages of this mechanism, but could also help avoiding cannibalism. We tested this hypothesis by quantifying cannibalism by never-fed first-instar larvae on: (1) just-fed 5th instar bugs, (2) artificially heated just-fed bugs, (3) heated or (4) non-heated objects of the same size. In line with our hypothesis, non-heated just-fed bugs were not attacked by the 1st instar larvae, whereas heated bugs and object triggered biting behaviour in starved bugs, which performed either cleptohaematophagy or haemolymphagy on heated bugs. We conclude that cannibalism triggered by thermal stimuli has been one of the selection pressures that gave origin to thermoregulation during feeding on kissing bugs.
What does heat tell a mosquito? Characterization of the orientation behaviour of Aedes aegypti towards heat sources
2017, Journal of Insect Physiology
Citation Excerpt :
Given these results, we could hypothesize that the thermal sense of different haematophagous is not organized or developed similarly, although the basis for this comparison remains weak, since only triatomine bugs and mosquitoes have been studied in detail. While bugs are sensitive to IR and use radiant heat to locate a potential host (Lazzari and Núñez, 1989; Schmitz et al., 2000; Zopf et al., 2014a,b), mosquitoes do not use this information (Peterson and Brown, 1951; this study), and the way in which these species acquire and use thermal information seems to be directly related to their biology. Kissing bugs are haematophagous during their whole life and are mostly walking insects (even though adults can perform dispersive flights).
The use of heat as a cue for the orientation of haematophagous insects towards hot-blooded hosts has been acknowledged for many decades. In mosquitoes, thermoreception has been studied at the molecular, physiological and behavioural levels, and the response to heat has been evaluated in multimodal contexts. However, a direct characterization of how these insects evaluate thermal sources is still lacking. In this study we characterize Aedes aegypti thermal orientation using a simple dual choice paradigm, providing direct evidence on how different attributes of heat sources affect their choice. We found that female mosquitoes, but not males, are able to discriminate among heat sources that are at ambient, host-range and deleterious temperatures when no other stimuli are present, eliciting a positive response towards host-range and an avoidance response towards deleterious temperatures. We also tested the preference of females according to the size and position of the sources. We found that females do not discriminate between heat sources of different sizes, but actively orientate towards closer sources at host temperature. Furthermore, we show that females cannot use IR radiation as an orientation cue. Orientation towards a host involves the integration of cues of different nature in distinct phases of the orientation. Although such integration might be decisive for successful encounter of the host, we show that heat alone is sufficient to elicit orientation behaviour. We discuss the performance of mosquitoes’ thermal behaviour compared to other blood-sucking insects.
An inside look at the sensory biology of triatomines
2017, Journal of Insect Physiology
Citation Excerpt :
Triatomines show astonishing heat sensitivity and are capable of sensing IR radiation (Lazzari, 2009). This capability allows bugs to recognize a potential host and estimate its distance based solely on thermal information without being affected by factors such as wind, which can disrupt conduction gradients and convective currents (Flores and Lazzari, 1996; Lazzari and Nuñez, 1989a; Schmitz et al., 2000; Lazzari, 2009). Triatomines use thermal information not only to find their hosts, but also for choosing resting places (Lorenzo and Lazzari, 1999), synchronize their circadian system (Lazzari, 1992), and locate blood-vessels hidden under the skin of vertebrate hosts (Ferreira et al., 2007).
Although kissing bugs (Triatominae: Reduviidae) are perhaps best known as vectors of Chagas disease, they are important experimental models in studies of insect sensory physiology, pioneered by the seminal studies of Wigglesworth and Gillet more than eighty years ago. Since then, many investigations have revealed that the thermal, hygric, visual and olfactory senses play critical roles in the orientation of these blood-sucking insects towards hosts. Here we review the current knowledge about the role of these sensory systems, focussing on relevant stimuli, sensory structures, receptor physiology and the molecular players involved in the complex and cryptic behavioural repertoire of these nocturnal insects. Odours are particularly relevant, as they are involved in host search and are used for sexual, aggregation and alarm communication. Tastants are critical for a proper recognition of hosts, food and conspecifics. Heat and relative humidity mediate orientation towards hosts and are also important for the selection of resting places. Vision, which mediates negative phototaxis and flight dispersion, is also critical for modulating shelter use and mediating escape responses. The molecular bases underlying the detection of sensory stimuli started to be uncovered by means of functional genetics due to both the recent publication of the genome sequence of Rhodnius prolixus and the availability of modern genome editing techniques.

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Journal of Insect Physiology

Abstract

Introduction

Section snippets

Experimental animals

Results

Discussion

Acknowledgements

References (24)

The role of the antennae in Triatoma infestans: Orientation towards thermal sources

Journal of Insect Physiology

The response to radiant heat and the estimation of the temperature of distant sources in Triatoma infestans

Journal of lnsect Physiology

Fine structure and physiology of the infrared receptor of beetles belonging to the genus Melanophila (Coleoptera, Buprestidae)

International Journal of Insect Morphology and Embryology

Ultrastructure and function of insect thermo- and hygroreceptors

Annual Review of Entomology

Infrared receptors in Melanophila acuminata DeGeer

Nature

Perception of infrared radiation from forest fires by Melanophila acuminata DeGeer (Buprestidae Coleoptera)

Ecology

Factors affecting feeding by bloodsucking insects

Annual Review of Entomology

A resposta de Rhodnius prolixus a estimulos termicos

Revista de Sociedade Brasileira de Medicina Tropical

Alimentação de Rhodnius prolixus no laboratorio

Anais da Academia Brasileira de Ciências

Erfassung und Messung von Wärmestrahlung

Zeitschrift für Parasitenkunde

The radiation of heat born the human body. III. The human skin as a black-body indicator

Journal of Clinical Investigation

Cited by (46)

Triggering the proboscis extension reflex (PER) in Rhodnius prolixus

Active dispersal in Triatoma infestans (Klug, 1834) (Hemiptera: Reduviidae: Triatominae): Effects of nutritional status, the presence of a food source and the toxicological phenotype

The thermal sense of blood-sucking insects: why physics matters

Keeping cool: Kissing bugs avoid cannibalism by thermoregulating

What does heat tell a mosquito? Characterization of the orientation behaviour of Aedes aegypti towards heat sources

An inside look at the sensory biology of triatomines