On the morphology and possible function of two putative vibroacoustic mechanisms in derbid planthoppers (Hemiptera: Fulgoromorpha: Derbidae)

Highlights

• Supposed stridulatory organs are widespread in Derbidae.

• Their morphology does not appear well adapted to producing sound.

• Many derbids possess snapping organs, but we found no tymbal-like organs.

• Tergal glands produce wax filaments in some derbid larvae.

Abstract

A mechanism involving interaction of the metathoracic wing and third abdominal segment of derbid planthoppers was first discovered over a century ago, and interpreted as a stridulatory organ for sound production. Although referred to occasionally in later taxonomic works, the detailed morphology, systematic distribution, and behavioural significance of this structure have remained unknown, and its proposed use in sound production has never been corroborated. Here we examine the distribution and morphology of the supposed stridulatory organ of Derbidae and the recently-described vibratory mechanism of planthoppers – the snapping organ, across 168 species covering the entire taxonomic spectrum of the family. We find that many derbids possess snapping organs morphologically similar to those of other planthoppers, and find no evidence for the presence of tymbal organs, which were previously thought to generate vibrational signals in derbids. We find the supposed stridulatory mechanism to be widespread in Derbidae, and conclude that it provides several systematically and taxonomically important characters. Nevertheless, its morphology appears unsuitable for the production of sound, and we instead speculate that the mechanism plays a role in spreading chemical secretions or wax. Finally, we observe wax production by tergal glands in derbid larvae, and illustrate their external morphology in adults.

Introduction

Hemiptera, or true bugs, exploit acoustic and substrate-borne vibrational communication more than any other insect Order (Cocroft and Rodriguez, 2005). Hemipterans are known to generate such vibrations in various ways, including: (i) stridulation, where a scraper (plectrum) and a file (stridulitrum) are moved against one another to generate sound (Čokl et al., 2006); (ii) buzzing (Kavčič et al., 2013), in which the wings are vibrated to generate sound; (iii) percussion, where the legs tap against a surface (Žunič et al., 2008); (iv) tremulation, where the body vibrates relative to the legs (Žunič et al., 2008, Kavčič et al., 2013); (v) tymbal buckling, which is a bistable mechanism involving a buckling membrane, usually with ribs that pop bent then straight (Young and Bennet-Clark, 1995); and (vi) abdominal snapping, in which the abdomen is jerked up and down using a newly-described mechanism involving the snapping shut then open of a Y-shaped cuticular lobe (Davranoglou et al., 2019a). The last of these mechanisms, known as a snapping organ (Davranoglou et al., 2019a), is present throughout the planthoppers (Hemiptera: Fulgoromorpha), including within the family Delphacidae, in which the snapping organ appears to have been modified (Davranoglou et al., 2019a) into a highly-specialised structure referred to previously as a drumming organ (Mitomi et al., 1984). The only other vibroacoustic mechanisms identified in planthoppers to date are a supposed stridulatory apparatus found within the family Derbidae (see Kirkaldy, 1907).

Derbids are among the most taxonomically diverse planthoppers, with ca. 1700 described species occurring primarily in tropical and subtropical areas (Bartlett et al., 2014, Bourgoin, 2019). Their morphology is similarly diverse. Defining traits of derbids include a small and tapered apical labial segment; a row of spines on the second hind tarsal segment; and parameres that greatly extend beyond the abdomen (Wilson, 2005, Bartlett et al., 2014). Peculiar modifications in some taxa include forward-facing expansions of the pronotum known as subantennal processes; greatly enlarged, sexually dimorphic antennae; and unique antennal appendages (Emeljanov, 1996, Bourgoin and Yap, 2010, Bartlett et al., 2014). In terms of their habits, derbid larvae are considered mycophagous, and can be found in rotting logs and leaf litter (O'Brien and Wilson, 1985, Yang and Yeh, 1994, Howard et al., 2001, Gossner and Damken, 2018), whereas adults typically feed on monocot plants (often palms) and woody dicot plants (Wilson et al., 1994, Howard et al., 2001), often forming large aggregations under their leaves (Kirkaldy, 1907, O'Brien, 2002). Approximately 20 species are potential agricultural pests, and some may transmit phytoplasmas (Wilson, 2005, Brown et al., 2006, Halbert et al., 2014).

Within the Derbidae, substrate-borne vibrational signals have so far been recorded only from Cedusa spp., their origin having been speculatively attributed to as yet unknown tymbal organs (Tishechkin, 2003, Tishechkin, 2008). On the other hand, Davranoglou et al. (2019a) recently reported the presence of a snapping organ in some Derbidae, so it is reasonable to suppose that derbids may instead produce substrate-borne vibrations using an abdominal snapping mechanism similar to that of other planthoppers. Acoustic signalling has not yet been experimentally demonstrated in planthoppers, but the eminent hemipterist F.A.G. Muir reported noise emanating from hundreds of individuals of the derbid Muiria stridula Kirkaldy (1907), which were aggregating under a palm. Based on his observations of live animals, Muir identified the sound as being stridulatory in origin, and proposed a mechanism where a part of the metathoracic (hind) wing is modified into a stridulitrum and strikes against a field of hairs on the abdomen, supposed to act as a plectrum. Since Muir's original observations and illustrations (reported in Kirkaldy, 1907), the supposed stridulitrum has occasionally been used in descriptive taxonomy and classification of derbids (e.g., Fennah, 1952, Emeljanov, 1996, Banaszkiewicz and Szwedo, 2005), albeit that its detailed morphology, systematic distribution, homologies, and function have remained unstudied. The abdominal hairs that Muir interpreted as functioning as a plectrum have been neglected by most subsequent studies, and their structure and distribution has remained undocumented. In addition, there have been no subsequent observations of acoustic signalling in derbids that would confirm Muir's observations, and the function of this unusual mechanism has not been examined in a behavioural context.

In order to gain a better understanding of the morphological basis of vibroacoustic or vibrational communication in derbids, we examined the external morphology of the pregenital abdominal segments and putative stridulatory structures of 168 species of Derbidae, covering almost all currently recognised subfamilies, tribes, and subtribes of the family. We also investigated the internal morphology of one species using synchrotron-based micro computed tomography (SR-μCT). Our findings confirm the presence of a snapping organ in Derbidae, and present novel morphological information which may be important for reconstructing the systematics and taxonomy of Derbidae, and provide a new perspective on the functional morphology and behavioural significance of the supposed stridulatory mechanism of the group. Finally, we also show wax production from tergal glands in derbid larvae, and detail the external morphology of the tergal glands of adults for the first time.