The Evaporative Function of Cockroach Hygroreceptors

Insect hygroreceptors associate as antagonistic pairs of a moist cell and a dry cell together with a cold cell in small cuticular sensilla on the antennae. The mechanisms by which the atmospheric humidity stimulates the hygroreceptive cells remain elusive. Three models for humidity transduction have been proposed in which hygroreceptors operate either as mechanical hygrometers, evaporation detectors or psychrometers. Mechanical hygrometers are assumed to respond to the relative humidity, evaporation detectors to the saturation deficit and psychrometers to the temperature depression (the difference between wet-bulb and dry-bulb temperatures). The models refer to different ways of expressing humidity. This also means, however, that at different temperatures these different types of hygroreceptors indicate very different humidity conditions. The present study tested the adequacy of the three models on the cockroach’s moist and dry cells by determining whether the specific predictions about the temperature-dependence of the humidity responses are indeed observed. While in previous studies stimulation consisted of rapid step-like humidity changes, here we changed humidity slowly and continuously up and down in a sinusoidal fashion. The low rates of change made it possible to measure instantaneous humidity values based on UV-absorption and to assign these values to the hygroreceptive sensillum. The moist cell fitted neither the mechanical hygrometer nor the evaporation detector model: the temperature dependence of its humidity responses could not be attributed to relative humidity or to saturation deficit, respectively. The psychrometer model

The evaporative function of cockroach hygroreceptors.

Insect hygroreceptors associate as antagonistic pairs of a moist cell and a dry cell together with a cold cell in small cuticular sensilla on the antennae. The mechanisms by which the atmospheric humidity stimulates the hygroreceptive cells remain elusive. Three models for humidity transduction have been proposed in which hygroreceptors operate either as mechanical hygrometers, evaporation detectors or psychrometers. Mechanical hygrometers are assumed to respond to the relative humidity, evaporation detectors to the saturation deficit and psychrometers to the temperature depression (the difference between wet-bulb and dry-bulb temperatures). The models refer to different ways of expressing humidity. This also means, however, that at different temperatures these different types of hygroreceptors indicate very different humidity conditions. The present study tested the adequacy of the three models on the cockroach's moist and dry cells by determining whether the specific predictions about the temperature-dependence of the humidity responses are indeed observed. While in previous studies stimulation consisted of rapid step-like humidity changes, here we changed humidity slowly and continuously up and down in a sinusoidal fashion. The low rates of change made it possible to measure instantaneous humidity values based on UV-absorption and to assign these values to the hygroreceptive sensillum. The moist cell fitted neither the mechanical hygrometer nor the evaporation detector model: the temperature dependence of its humidity responses could not be attributed to relative humidity or to saturation deficit, respectively. The psychrometer model, however, was verified by the close relationships of the moist cell's response with the wet-bulb temperature and the dry cell's response with the dry-bulb temperature. Thus, the hygroreceptors respond to evaporation and the resulting cooling due to the wetness or dryness of the air. The drier the ambient air (absolutely) and the higher the temperature, the greater the evaporative temperature depression and the power to desiccate

Revisiting Theories of Humidity Transduction: A Focus on Electrophysiological Data

Understanding the mechanism of humidity transduction calls for experimental data and a theory to interpret the data and design new experiments. A comprehensive theory of humidity transduction must start with agreement on what humidity parameters are measured by hygroreceptors and processed by the brain. Hygroreceptors have been found in cuticular sensilla of a broad range of insect species. Their structural features are far from uniform. Nevertheless, these sensilla always contain an antagonistic pair of a moist cell and a dry cell combined with a thermoreceptive cold cell. The strategy behind this arrangement remains unclear. Three main models of humidity transduction have been proposed. Hygroreceptors could operate as mechanical hygrometers, psychrometers or evaporation detectors. Each mode of action measures a different humidity parameter. Mechanical hygrometers measure the relative humidity, psychrometers indicate the wet-bulb temperature, and evaporimeters refer to the saturation deficit of the air. Here we assess the validity of the different functions by testing specific predictions drawn from each of the models. The effect of air temperature on the responses to humidity stimulation rules out the mechanical hygrometer function, but it supports the psychrometer function and highlights the action as evaporation rate detector. We suggest testing the effect of the flow rate of the air stream used for humidity stimulation. As the wind speed strongly affects the power of evaporation, experiments with changing saturation deficit at different flow rates would improve our knowledge on humidity transduction

Temporal profiles of absolute humidity, temperature and wind speed recorded while traveling through different habitats.

<p><b>A.</b> Open grassy field. <b>B.</b> Deciduous forest. <b>C.</b> Edge habitat characterized by overhanging canopy and grassland. In each habitat, temporal profiles of relative humidity (<i>a</i>), saturation deficit (<i>b</i>) and water vapor pressure (<i>c</i>) were determined from the measured values of absolute humidity (<i>f</i>) and air temperature (<i>e</i>). Peak wind speeds (<i>d</i>) were not reflected in the profiles of relative humidity (<i>a</i>), saturation deficit (<i>b</i>) and water vapor pressure. <i>aH</i> absolute humidity, <i>Pw</i> water vapor pressure, <i>rH</i> relative humidity, <i>SD</i> saturation deficit, <i>T</i> temperature.</p

Simultaneously recorded responses of a pair of moist and dry cells from a single sensillum to small amplitude changes in humidity.

<p><b>A.</b> Time course of the responses and the parameters controlled during the recording, and the corresponding activity of the moist and dry cells. <i>a</i> and <i>b</i>, instantaneous impulse frequency of both cells. <i>c</i>, time course of the relative humidity. <i>d</i>, time course of the saturation deficit. <i>e</i>, time course of the water vapor pressure. <i>f</i>, time course of the temperature. <i>g</i>, digitized action potentials of the moist and dry cells recorded with a single electrode and discriminated on-line. <b>B.</b> Impulse frequency of the moist and dry cells during the oscillations in relative humidity shown in A plotted as a function of instantaneous relative humidity and its rate of change. Multiple regressions which utilize 3-dimensional planes (<i>F</i> = <i>a</i>+<i>b drH/dt</i>+<i>c rH</i>; where <i>F</i> is the impulse frequency, and <i>a</i> the height of the regression plane) were calculated to determine the simultaneous effects of the rate of change in the relative humidity (<i>b</i> slope) and the instantaneous relative humidity (<i>c</i> slope) and the response frequency of both cell types. <i>Pw</i> water vapor pressure, <i>R²</i> coefficient of determination, <i>rH</i> relative humidity, <i>SD</i> saturation deficit, <i>T</i> temperature, <i>V</i> volt.</p

Effects of atmospheric temperature on the hygroreceptors responses as predicted by the three humidity transduction models.

<p><b>A</b>. Humidity stimulation consists of constant amplitude oscillating change in vapor pressure, illustrated by the orange zone. <b>Ba</b>. The constant amplitude oscillating change in vapor pressure in <i>A</i> produces, with rising temperature, continuously deceasing oscillations in relative humidity (<i>left axis</i>), illustrated by the blue zone. Impulse frequency of a moist cell responding to oscillations in relative humidity is predicted to oscillate within blue zone (<i>right axis</i>). <b>Bb</b>. Same plot as in <i>Ba</i> but with turned y-axis (<i>left axis</i>) to illustrate the relative humidity stimulus eliciting excitatory responses in a dry cell. Impulse frequency of a dry cell responding to oscillations in relative humidity is proposed to oscillate within red zone (<i>right axis</i>). <b>Ca</b>. Constant amplitude oscillating change in vapor pressure in <i>A</i> produces, with rising temperature, continuously increasing oscillations in saturation deficit (<i>left axis</i>), illustrated by the red zone. Impulse frequency of a dry cell responding to oscillations in saturation deficit is predicted to oscillate within red zone (<i>right axis</i>). <b>Cb</b>. Same plot as in <i>Ca</i> but with turned y-axis (<i>left axis</i>) to illustrate the saturation deficit stimulus eliciting excitatory responses in a moist cell. Impulse frequency of a moist cell responding to oscillations in saturation deficit is predicted to oscillate within blue zone (<i>right axis</i>). <b>Da</b>. Constant amplitude oscillating change in vapor pressure in <i>A</i> produces, with rising temperature, continuously increasing oscillations in wet-bulb temperature (<i>left axis</i>), illustrated by the blue zone. Impulse frequency of a moist cell responding to oscillations in wet-bulb temperature is predicted to oscillate within blue zone (<i>right axis</i>). <b>Db</b>. Dry-bulb temperature as function of air temperature. Impulse frequency of a dry cell responding to the dry-bulb temperature is predicted to increase with rising temperature (<i>right axis</i>). <i>Pw</i> water vapor pressure, <i>Ps</i> saturation water vapor pressure. <i>Arrows</i> point in the direction of increasing axis values.</p

Humidity stimulation expressed as saturation deficit.

<p>Effect of temperature on the parameters of the regression plane utilized to determine the response characteristic of the moist cell (<b>A</b>) and the dry cell (<b>B</b>) to oscillating changes in the saturation deficit. <i>Aa</i> and <i>Ba</i>: <i>yo</i> intercept of the regression plane with the <i>F</i> axis reflecting the height of the regression plane plotted as function of temperature. <b>Ab</b> and <b>Bb</b>. Gain for the rate of change of the saturation deficit plotted as function of temperature. <b>Ac</b> and <b>Bc</b>. Gain for the instantaneous saturation deficit plotted as function of temperature. Relationships approximated by linear regressions [<i>f</i> = <i>yo</i>+<i>aT</i>]. <i>R²</i>, coefficient of determination; the number of points per plot was 30. <i>Arrows</i> point in the direction of increasing axis values. <i>F</i> impulse frequency, <i>SD</i> saturation deficit.</p

Humidity profile showing the parameters analysed.

<p>Peak and trough amplitudes are values over the zero level, durations of the upward and downward slopes are the periods between successive peaks and troughs, and the values of the upward and downward slopes are the velocities with which humidity is rising and falling, respectively.</p

Humidity stimulation expressed as vapour pressure.

<p>Impulse frequency of a moist cell and a dry cell located in the same sensillum during three consecutive oscillations in vapor pressure as a function of instantaneous vapor pressure and its rate of change. Multiple regressions which utilize three-dimensional planes [<i>F</i> = <i>yo</i>+<i>a</i> (Δ<i>Pw</i>/Δt)+<i>bPw</i>; where <i>F</i> is the impulse frequency and <i>yo</i> is the intercept of the regression plane with the <i>F</i> axis reflecting the height of the regression plane] were calculated to determine the gain of the responses for the instantaneous vapor pressure (<i>b</i>-slope) and its rate of change (<i>a</i>-slope). Impulse frequency of the moist cell increases linearly with rising instantaneous vapor pressure and its rate of change, in the dry cell with falling instantaneous vapor pressure and its rate of change. <i>R²</i>, coefficient of determination; the number of points per plot is 130. <i>Arrows</i> point in the direction of increasing axis values. <i>F</i> impulse frequency, <i>Pw</i> water vapor pressure.</p

Fluctuation statistics of humidity, temperature and wind speed values for a typical measurement trip through a deciduous forest.

<p>The mean peak values, the mean trough values, the mean amplitudes between peaks and troughs, as well as the mean rates of upward change and of downward change are significantly different (t-test, <i>p</i><0.001) from the corresponding values of the open grassy field (<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0099032#pone-0099032-t002" target="_blank">Table 2</a>).</p