Distribution and functional morphology of photomechanic infrared sensilla in flat bugs of the genus Aradus (Heteroptera, Aradidae)

Abstract

Globally the flat bug genus Aradus comprises about 200 species. About half a dozen Aradus species can be primarily found on burnt areas and, therefore, have been called pyrophilous. Bugs and their offspring feed on fungi growing on burnt wood. Recently, prothoracic infrared (IR) receptors have been described in the pyrophilous Australian species Aradus albicornis. In our study we investigated 10 Aradus species, once again including A. albicornis, and found prothoracic as well as hitherto unknown mesothoracic IR sensilla in A. albicornis, Aradus lugubris and Aradus fuscicornis. In Aradus flavicornis only prothoracic IR receptors were found. Currently the latter two species are not known as pyrophilous. However, there is considerable evidence that these flat bugs also approach forest fires.

In all four species where IR receptors were identified, the dome-shaped IR sensilla look very similar. An IR sensillum consists of an internal exocuticular sphere reinforced by consecutive layers of chitin fibres. In the center of the sphere, a microfluidic core is located which consists of a cup-shaped plug of cuticle and an underlying fluid filled annular channel surrounding the tip of the dendrite of a mechanosensitive neuron. Like the IR receptors of buprestid beetles of the genus Melanophila, the IR sensilla found in Aradus species can be classified as photomechanic IR receptors.

Introduction

Until recently the so-called photomechanic infrared (IR) sensilla of buprestid beetles of the genus Melanophila have represented a unique type of an IR receptor in animals (Evans, 1964, Schmitz et al., 1997). In the about 12 Melanophila species which all show the behaviour to approach forest fires and, therefore, are called pyrophilous (Champion, 1909, Evans, 1962, Linsley, 1943, Wikars, 1997), the IR receptors are housed in a pair of metathoracic pit organs (Evans, 1966, Schmitz and Bleckmann, 1997). The organs are located directly behind the coxae of the mesothoracic legs and each organ contains about 80 dome-shaped IR sensilla (Vondran et al., 1995). With regard to structure and function, the Melanophila IR receptors are fundamentally different from the IR organs of two other pyrophilous beetles: namely the Australian “Little Ash Beetle” Acanthocnemus nigricans (Acanthocnemidae) and the “Australian Fire Beetle” Merimna atrata (like Melanophila also a member of the family Buprestidae). In these two Australian beetles IR receptors are innervated by thermoreceptors which measure the increase in temperature caused by the absorption of IR radiation (Kreiss et al., 2005, Kreiss et al., 2007, Schmitz et al., 2001, Schmitz and Trenner, 2003). By contrast, the Melanophila IR sensilla are innervated by ciliary mechanoreceptors which most probably respond to a brief increase in pressure inside a little cuticular sphere having a diameter of 10 μm (Schmitz et al., 1997). The sphere is the decisive component of a photomechanic IR sensillum and contains a microfluidic core to which the tip of the mechanosensitive dendrite is fluidically coupled. Absorption of IR radiation causes thermal expansion primarily of the fluid inside the core enclosed in the outer shell of the sphere which causes a deformation of the dendritic membrane (Schmitz et al., 2007).

Recently, photomechanic IR receptors have also been found in the pyrophilous Australian flat bug Aradus albicornis (Aradidae) (Schmitz et al., 2008). Here, about a dozen IR sensilla are located on both sides of the prothorax posterior to the first pair of legs. The regions bearing the IR sensilla are called propleurae and are developed as rearward membranous extensions of the prothorax partly overlapping the mesothorax. Regarding their structure and function the IR receptors seem to be very similar to the Melanophila IR sensilla. However, sensilla are not arranged in a pit organ but are interspersed between hair mechanoreceptors which are distributed in large numbers all over the body of the bug. In contrast to the buprestid genus Melanophila which contains exclusively pyrophilous species, the vast majority of the about 200 species belonging to the aradid genus Aradus does not show a pyrophilous behaviour. First evidence that IR receptors may only be present in the 6 or 7 pyrophilous Aradus species has been provided by the study of Schmitz et al. (2008) because no prothoracic IR receptors were found in the non-pyrophilous species Aradus cinnamomeus and Aradus depressus. Also the wingless larvae of A. albicornis do not have prothoracic IR receptors.

In the present study an attempt was made to corroborate the hypothesis that IR sensilla in the genus Aradus are developed only in the pyrophilous members of the genus. We investigated a total of 10 species again including A. albicornis; four with a documented (Heiss and Pericart, 2007, Wikars, 1997) and six with hitherto undocumented pyrophilous behaviour. It could be demonstrated that three further species possess propleural IR receptors highly akin to those described in A. albicornis. Additionally small groups of 2–4 IR receptors more sunken into the surrounding cuticle than the sensilla located on the propleurae were discovered directly behind the coxae of the prothoracic and – previously unknown also in A. albicornis – of the mesothoracic pair of legs. After it has turned out that IR receptors of all Aradus species investigated so far are highly similar, the second intention of our attempt was an in depth study of the morphology of the aradid IR receptors. In the discussion, Aradus IR sensilla were compared with those of Melanophila beetles and the crucial components as well as the functional principle of a photomechanic insect IR receptor are highlighted.