Prerequisites: insect antenna, insect mechanoreceptors.

Thermoreceptors are temperature sensors, whilst hygroreceptors are moisture-sensors. Very often the two
are combined in insects, into dual-function thermohygroreceptors. The mode of operation of these
remarkable sensors is poorly understood.

Thermohygroreceptors

A thermoreceptor is a temperature (or heat-flow) sensor. Hygroreceptors are moisture-sensors or
water-sensors. It is common to find dual-purpose thermo and hygroreceptor sensilla in insects - so-called
thermohygroreceptors. These can take many different forms but are usually pointed/trichoid hairs
(Altner
et al., 1983), or blunt pegs/cones which may be enclosed inside a pit (coeloconic sensilla) (Altner
and Prillinger, 1980). These sensilla are non-porous, except for a terminal moulting pore (which may lead
to confusion with gustatory sensilla which have a pore in their tip to allow liquids to contact the sensory
dendrites inside); some thermo-hygroreceptive sensilla also contain olfactory sensory cells, in which case
the walls may be multi-porous, with the pores allowing diffusable gases to reach the sensory cells within.

A typical thermo-hygroreceptive sensillum contains 2-5 sensory cells (though three cells is the most
common), with four striking features (see Altner and Prillinger, 1980): 1) The dendritic outer segments of
only two of the cells extend into the lumen of the peg. 2) The dendrite which does not enter the peg is
usually flattened and forms characteristic lamellae (layered sheets). 3) The outer dendrites which are
found within the lumen of the peg, fill the lumen completely (there is no receptor lymph cavity) and tightly.
4) These latter dendrites usually contain many prominent microtubules.

Lamellated outer dendrites were first discovered in the cave beetle
Speophyes lucidulus
(Corbière-Tichané, 1971). Corbière-Tichané assumed a sensitivity to light, but since
Speophyes is a cave
beetle, to infrared (IR) radiation in particular. This was supported by the fact that the lamellae react with
osmium, as do photoreceptor outer segments (due to the presence of rhodopsin). However,
electrophysiology has revealed hygro- and thermoreceptive units in the antenna, which respond to
changes in air temperature, but not to IR emission (Altner and Prillinger, 1980). Thus, the presence of a
lamellated dendrite appears to correspond to thermoreceptor activity. Many other electrophysiological
studies have confirmed that non-porous sensilla are thermohygrorecetors (e.g. see Altner and Prillinger,
1980; Altner
et al., 1983; Haug, 1985).

The two dendrites occupying the lumen, correspond to hygroreceptor units, identified electrophysiologically
(e.g. Becker, 1978), generally one dry-air and one moist-air sensitive cell. The fact that these dendrites
are well-packed with microtubules, often surrounded by electron-dense material, is suggestive of a
mechanoreceptive role, as in the tubular body of other mechanoreceptors. It has been suggested that a
swelling process, in the presence of moisture, could lead to the exertion of mechanical forces on the
dendritic membranes of the hygroreceptors, which would then be specialised mechanoreceptors (Altner
and Prillinger, 1980; Steinbrecht and Muller, 1991). Thermo-hygroreceptive sensilla apparently occur very
infrequently on the insect integument, and so are probably often overlooked and are incompletely
understood.
Heat and moisture sensors in insects
References

Altner, H. and Loftus, R. 1985. Ultrastructure and function of insect thermo- and hygroreceptors. Ann. Rev.
Entomol.
30: 273-95.

Altner, H. and Prillinger, L. 1980. Ultrastructure of invertebrate chemo-, thermo-, and hygroreceptors and
its functional significance. International Review of Cytology 67: 69-139.

Altner, I., Hatt. H., and Altner, H. 1983. Structural properties of bimodal chemo- and mechanosensitive
setae on the pereiopod chelae of the crayfish, Austropotamobius torrentium. Cell Tissue Res. 242: 357-
374.

Becker, D. 1978. Doctoral dissertation, Univ. Regensburg.

Corbiere-Tichane, G. 1971. J. Microsc. 10, 191-202.

Haug, T. 1985. Ultrastructure of the dendritic outer segments of sensory cells in poreless ("no-pore")
sensilla of insects. A cryofixation study. Cell Tissue Res. 242, 313-322.

Skilbeck, C.A. and anderson, M. 1996. The ultrastructure, morphology and distribution of sensilla on the
antennae of the adult parasitoids Aleochara bilineata Gyll. and Aleochara bipustulata L. (Coleoptera:
Staphylinidae).
Int. J. Insect Morphol. & Embryol. 25: 261-280.

Steinbrecht, R.A. and Muller, B. 1991. The thermo-/hygrosensitive sensilla of the silkmoth, Bombyx mori:
morphological changes after dry- and moist-adaptation. Cell Tissue Res. 266, 441-456.

Tichy, H. and Kallina, W. 2010. Insect Hygroreceptor Responses to Continuous Changes in Humidity
and Air Pressure.
Neurophysiol 103: 3274–3286.
Figure 1: Above: a scanning electron micrograph of the antenna of Aleochara
bilineata
, showing a large basiconic olfactory receptive peg, of which there are 4
on the tip of the antenna, and a sensory hair (arrow) with a short tapering tip
which has the typical structure of a heat sensor (thermoreceptor) - see fig.2 for a
cross-section. The central peg is about 5 micrometres long, the.arrowed hair
about 6 micrometres long.
olfactory-thermohygroreceptor?
Figure 2. Left: a cross-section through a
double-walled peg-sensillum of
Aleochara
bilineata
of the type shown in figure 1 as seen in
the transmission electron microscope. The outer
surface contains grooves running the length of
the peg. The cuticular wall (dark grey) consists of
an outer cylinder, the outer wall (ow), joined by
radial spokes (s) to an inner cylinder, or inner wall
(iw). Between the spokes chambers of
darkly-staining liquid (lymph) can be seen - the
outer lymph chambers (ol). In the centre is a
cavity containing (lightly-staining) lymph (il, inner
lymph chamber) and, in this case, five dendritic
branches (d) can be seen in cross-section.
Although it has been reported that there are no
obvious pores in the outer wall (Skilbeck and
Anderson, 1996) grooves filled with
electron-dense material have been seen to
connect the outer lymph chambers to pores in the
outer cuticle wall. This section has two apparent
pores lying in the grooves, so although pores are
hard to detect in these sensilla they do appear to
be present. However, these pores seem to lack
the usual pore tubule arrangement seen in the
majority of chemoreceptors, but this is typical of
double-walled olfactory receptors.

These pegs therefore seem to be what are called
double-walled multiporous sensilla. Sensilla of this
type, in other insect species, have been shown to
have a thermoreceptive and an olfactory function,
and this is generally their assumed function,
though some are reported to be
thermohygroreceptors only. In this type of sensor
there is no apparent ultrastructural difference
between the thermosensitive and chemoreceptive
dendrites. None have a lamellated structure and
all extend to the tip of the peg. It is not clear how
these receptors detect temperature and/or
moisture. Closer to the base of the peg, the
spokes tend to disappear and the inner wall,
apparently an extension of the sheath more tightly
encircles the dendrites, but it is dificult to see how
any of these sensilla could detect moisture by a
hygromechanical mechanism.
A sensillum of this structure is characteristic of a dual-function olfactory-thermoreceptor, which might
or might not have an additional hygroreceptive function. The actual function of this sensillum could be
unequivocally observed by electrical recordings in the living specimen, but in insects determining sensory
modality from structure gives a reliable indication of a sensor's function. Such measurements have been
performed on similar sensilla in other insect species, which is how their function was first ellucidated.

Sometimes one or more of the spokes are absent, or only partially formed and not connecting to the outer
wall. Thus the outer lymph chambers are apparently connected. In particular, the spokes disappear
completely towards the base of the peg, followed by the grooves as the base of the peg becomes smooth
(and indistinguishable from the bases of single-walled basiconic pegs).

Adaptive evolution

It is remarkable, but understandable, that nature has taken something like the cilium, an organ of
locomotion in more archaic organisms, and adapted it into a variety of sensors in insects. This is a natural
extension of its use - cilia are projections from the cell surface and so well placed to sense the environment.
In adapting from locomotion to sensation, most of these senory cilia have lost their power of active
movement.  It is also remarkable how the cuticular structures associated with these 'cilia', now sensory
dendrites, have become adapted to function as various mechanoreceptors, including touch receptors,
proprioceptors and vibration/auditory sensors, chemoreceptors and now, as we have seen,
thermohygroreceptors and air-pressure sensors. It is frustrating, however, that so little work is done on
these systems these days, when we still don't know how these minute and highly sensitive temperature and
moisture sensors actually work! What a potential loss to micro engineering that humanity is still ignorant in
these matters!
such a way that the inner lymph-cavity shrinks and the wall constricts around the sensory dendrites. In this
state the inner wall squeezes and places pressure on the dendrites, which get squeezed against the
expanded inner wall. This squeezing of the dendrites may activate the dendrites to send signals to the
sensory cell body and, if the stimulus is strong enough, the cell body will relay the signals to the central
nervous system (as action potentials travelling in sensory axons). Thus, these moisture sensitive dendrites
are thought to function as pressure sensors and so are fundamentally mechanoreceptive. Thus, this
sensillum is a device called a
hygromechanical transducer.

Of the two dendrites which enter the lumen of the peg, and branch, one is thought to be moisture-sensitive,
the other dry-sensitive. It is the moisture-sensitive dendrite which responds to pressure as the inner wall
expands and constricts around it. The dry receptor, responds when it expands as the wall dries, shrinks
and moves outwards (Tichy and kallina, 2010). The moisture-sensitive receptor also responds to
increasing air pressure, the dry receptor to decreasing air pressure, supporting the hygromechanical
transducer model. However, the exact mechanism of operation of these sensors is not firmly established.

Double-walled olfactory receptors

These are grooved pegs, often coeloconic. It is not always clear whether, or not, double-walled grooved
pegs have pores in their walls, since these pores possess no pore tubules and may be clogged by a
secretion (Altner and Prillinger, 1980). Electrophysiological studies reveal that many of these sensilla are
dual-purpose olfactory and thermo- and/or hygroreceptors, although some are exclusively
thermo-hygroreceptors, none have been found to have an exclusively olfactory function (Boeckh, 1967;
Kafka, 1970; Davis, 1974; Kaib, 1974; Altner et al., 1977,78,81).

Double-walled sensilla in Aleochara

In Aleochara bilineata, about 20 of these sensilla occur on the tip-most segment of the antenna
(antennomere F9) increasing in density towards the tip. One such sensillum is shown in the photograph at
the top of the page (fig. 1). They are blunt, slightly tapered pegs, about 5um in length, and less than 1um
across at their base, and taper only slightly for most of their length, before tapering very steeply to a point
in the last 0.5um of their length.

In cross-section these pegs have an inner and an outer cuticular wall, connected by
cuticular spokes
which are separated by outer lymph chambers (see below). The outer surface of the pegs contains 9-13
grooves, the spokes connect to the outer wall where the grooves lie. Sometimes the grooves possess clear
central channels, which are blocked by electron-dense material. (In electron micrographs, materials
appearing dark are said to be electron dense or darkly-staining, since they absorb and scatter electrons
from the electron beam). The chamber within the inner wall contains some lymph, but is largely occupied by
closely-spaced dendritic branches (Fig. 2). Initially a single dendrite enters the peg, then branches into
three dendrites about mid-way along the peg. Each of these branches apparently forks again, as typically
4 or 5 branches are seen in sections towards the tip of the peg. The tapering tips of these pegs consist
entirely of cuticle, with a diminishing number of external grooves.
thermohygroreceptor
Above: a section through a typical thermohygroreceptor peg. Such a peg is often quite short and
embedded in a pit, or dome with a central pore, in the insect cuticle, forming a coeloconic (peg in
a pit) sensillum. The pit presumably holds moisture, increasing the sampling time for the
hygroreceptor to function, or may protect the pegs, which do not have flexible sockets, from
breakage. Two dendrites are tightly packed inside the cuticle, surrounded by a sheath which is
an extension of the scolopale sheath (see
mechanoreceptors). In addition, these sensilla
typically have a thermoreceptive dendrite (e.g. a cold-sensitive receptor) in the base of the peg.
olfactory-thermohygroreceptor? labeled
Single-walled non-porous thermohygroreceptors often
occur as single pegs, with inflexible sockets, inside pits.
They are often concentrated near the tip of the antenna,
where several occur as a rule. Their low frequency and
inconspicuous appearance makes them hard to detect, but
they seem to be present on many insects though it takes a
thorough study to locate them. In
Aleochara bilineata there
are about five of these, in a diagonal row, on the tipmost
segment of the antenna. Unfortunately, however, no
sections have been obtained through these structures so
we can not be certain they are of the thermohygroreceptive
type, though they fit all the criteria based on position,
number and external appearance. The pore to the pit
enclosing this sensory peg is only about 1 micrometre
across!