Infrared and temperature perception in bloodsucking bugs

The triatomine bugs Triatoma and Rhodnius act as main vectors of Chagas disease, a protozoan infection that constitutes not only one of the most serious sanitarian problems in Latin America but has an important social and economic impact on the region. About 20 million people are infected with this disease and more than 100 million are at risk of becoming infected, i.e. 25% of the population of Latin America. Their mechanism of host finding and orientation is not understood in detail, but involves detection of CO2, infrared (IR) radiation and different odor stimuli. Wigglesworth et al. (1934), Lazzari and Nùñez (1989), and Schmitz et al. (2006) have shown that triatomine bugs sense IR radiation and approach a thermal source in complete darkness guided solely by IR radiation. It is recognized that these bugs are the only group of blood feeding insects where the ability to perceive the infrared (IR) radiation emitted by the host body has been demonstrated. But what does this ability mean in terms of receptor function? Radiation may be detected as electromagnetic waves or as an increase in temperature of the absorbing structures. If the sense organ has the capacity to detect radiation, the temperature of both the intervening media and the sense organ will not affect orientation. But if the warming effect of IR absorption is the adequate stimulus, not only the temperature of the environment and the sense organ will tend to bias detection. Heat conductance and capacity, spatial dimensions of the sense organ, along with its thermal interaction with other parts of the body, will determine the efficiency of the IR stimulus and the contribution of the IR sense to orientation. In cooperation with Prof. Claudio Lazzari (University of Tours, France), one of today`s leading experts on the orientation behavior and sensory physiology of triatomine bugs, we will clarify the nature of the adequate stimulus of the bug`s IR sense organs. It is our primary aim to provide electrophysiological evidence for IR receptors in the cave organ and in the peg-shaped sensilla which are known to house thermoreceptors responding to convective heat. We will describe the response characteristics of these sense organs and analyze how much information is contained in their responses about IR radiation and temperature stimulation. We will determine the increment in radiant heat that produces the same change in the discharge rates of the IR receptors as a given increment in temperature due to convection. The amount of IR radiation required to produce the same effect as a 1C change in temperature will indicate the ability of the different sense organs to absorb and transfer radiant heat. Low values of IR radiation suggest adaptation for IR detection. If the prime stimulus is IR radiation, we can utilize the slope and width of the input-output functions to estimate the distance over which the IR receptors can sense the direction of a warm blooded host. By outlining structural features of the IR sense organs and tracing the connections with physiology we will determine the sense-organ`s design responsible for the efficient transfer of radiant heat.

In the blood-sucking bug Rhodnius prolixus, we have clarified the sensory basis for the detection of infrared radiation (IR). The IR sensors are ordinary thermoreceptors which respond to the warming effect due to IR absorption. For the first time we have shown how the increase in T of the IR sensor by increasing the power of IR is discriminated from the T increase by warm air (convection). The results of our studies gained insights into the functioning of IR sense organs and allowed estimating the distance at which the bugs IR sense is able to detect the warm blooded host.Extracellular recordings revealed two types of warm cells in morphologically different sense organs, the peg-in-pit sensilla (PS) and the tapered hairs (TH). Slowly fluctuating changes in both air T and IR power evoked small but clear-cut differences between the responses of the two types of warm cells. The warm cells in PS sensilla (PSw-cells) produced stronger responses to T oscillations than the warm cells in TH (THw-cells). Oscillations in IR did the reverse: they stimulated the latter more strongly than the former. The reversal in the relative excitability of the two warm cell types provides a criterion to distinguish between slow changes in T and IR. The existence of strongly responsive warm cells for one or the other stimulus in a paired comparison is the distinguishing feature of a combinatory coding mechanism. This mechanism enables the information provided by the difference or the ratio between the response magnitudes of both cell types to be utilized by the nervous system in the neural code for T and IR. These two coding parameters remained constant, although response strength changed when the oscillation period was altered. To discriminate between slow changes in T and IR two things are important: which sensory cell responded to either stimulus and how strong was the response. The label warm or infrared cell may indicate its classification, but the functions are only given in the context of activity produced in parallel sensory cells. For the ability to detect unambiguously IR stimuli, it is not necessary that a sense organ responds to the non-thermal effect of IR radiation the information about IR stimulation is represented in the rate of discharge two types of warm cells.We have shown that the two warm cells respond well to IR oscillations if the background T operates by natural convection, but poorly at forced convection, even if the background T is higher than at natural convection. Background IR radiation strongly affects the responses to T oscillations; the discharge rates of both warm cells are higher the higher the strength of the IR background. A comparison of the responses of the warm cells with the T measured inside small model objects shaped like a cylinder, a cone or a disc indicates that passive thermal effects of the sense organs rather than intrinsic properties of the sensory cells are responsible for the observed behavior.