Mating Behaviour and Vibratory Signalling in Non-Hearing Cave Crickets Reflect Primitive Communication of Ensifera

Abstract

In Ensifera, the lack of well-supported phylogeny and the focus on acoustic communication of the terminal taxa hinders understanding of the evolutionary history of their signalling behaviour and the related sensory structures. For Rhaphidophoridae, the most relic of ensiferans following morphology-based phylogenies, the signalling modes are still unknown. Together with a detailed description of their mating process, we provide evidence on vibratory signalling for the sympatric European species Troglophilus neglectus and T. cavicola. Despite their temporal shift in reproduction, the species’ behaviours differ significantly. Signalling by abdominal vibration constitutes an obligatory part of courtship in T. neglectus, while it is absent in T. cavicola. Whole-body vibration is expressed after copulation in both species. While courtship signalling appears to stimulate females for mating, the function of post-copulation signals remains unclear. Mating and signalling of both species were found to take place in most cases on bark, and less frequently on other available substrates, like moss and rock. The signals’ frequency spectra were substrate dependent, but with the dominant peak always expressed below 120 Hz. On rock, the intensity of T. neglectus courtship signals was below the species’ physiological detection range, presumably constraining the evolution of such signalling in caves. The species’ behavioural divergence appears to reflect their divergent mating habitats, in and outside caves. We propose that short-range tremulation signalling in courtship, such as is expressed by T. neglectus, represents the primitive mode and context of mechanical signalling in Ensifera. The absence of high-frequency components in the signals may be related to the absence of the crista acoustica homologue (CAH) in the vibratory tibial organ of Rhaphidophoridae. This indirectly supports the hypothesis proposing that the CAH, as an evolutionary precursor of the ear, evolved in Ensifera along the (more) complex vibratory communication, also associated with signals of higher carrier frequency.

Neuronal Regression of Internal Leg Vibroreceptor Organs in a Cave-Dwelling Insect (Orthoptera: Rhaphidophoridae: <b><i>Dolichopoda araneiformis</i></b>)

“…These neuroanatomical features can be compared to data from T. neglectus [Jeram et al, 1995;Strauß et al, 2014], which mates outside caves and uses vibrational signals in intraspecific communication [Stritih and Čokl, 2012]. We hypothesize that troglobitic D. araneiformis experiences less selection pressure on vibration-sensitive organs and thus shows some sensory regression in comparison to T. neglectus .…”

“…This may apply to external mechanoreceptors like hair bristles and campaniform sensilla which may increase in numbers following leg elongation, rather than to internal vibrosensory organs. Rock, as the main substrate in caves, transmits vibrational signals of arthropods poorly [Elias et al, 2004;Hoch and Wessel, 2006;Stritih and Čokl, 2012]. Hence, the role of vibrational signaling in strict troglobites is likely reduced [López-Rodríguez and Tierno de Figueroa, 2012;Stritih and Čokl, 2012].…”

“…Rock, as the main substrate in caves, transmits vibrational signals of arthropods poorly [Elias et al, 2004;Hoch and Wessel, 2006;Stritih and Čokl, 2012]. Hence, the role of vibrational signaling in strict troglobites is likely reduced [López-Rodríguez and Tierno de Figueroa, 2012;Stritih and Čokl, 2012]. If troglophilic cave crickets which reproduce in the forests ( Troglophilus neglectus ) happen to emit vibrational signals on the rock, the signals occur below the sensory threshold of vibroreceptor organs in the leg [Stritih and Čokl, 2012;Stritih and Strauß, 2015] and are not detectable any more.…”

“…Hence, the role of vibrational signaling in strict troglobites is likely reduced [López-Rodríguez and Tierno de Figueroa, 2012;Stritih and Čokl, 2012]. If troglophilic cave crickets which reproduce in the forests ( Troglophilus neglectus ) happen to emit vibrational signals on the rock, the signals occur below the sensory threshold of vibroreceptor organs in the leg [Stritih and Čokl, 2012;Stritih and Strauß, 2015] and are not detectable any more. Thus, in strictly troglobitic species, the use of vibrational signaling can be expected to be severely limited.…”

“…Cave crickets generally lack wings and tympanal hearing organs in the foreleg tibiae, which are present in many other Ensifera [Ander, 1939;Leroy, 1967;Ingrisch and Rentz, 2009]. In particular the troglophilic species T. neglectus has been studied in detail for its life cycle and reproductive biology [Pehani et al, 1997;Stritih and Čokl, 2012], the anatomy and physiology of its mechanosensory organs and interneurons Jeram et al, 1995;Schrader et al, 2002;Stritih, 2009;Strauß et al, 2014], and its internal thorax morphology [Leubner et al, 2016]. This species is a nocturnal forest dweller that uses deep cave parts for overwintering, while in summer it resides primarily within leaf litter, decayed bark, trunks, and other similar desiccation-protecting shelters in the forest [Pehani et al, 1997;Karaman et al, 2011].…”