Chapter One - Sensorimotor ecology of the insect antenna: Active sampling by a multimodal sensory organ

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Abstract

Insect antennae are actively moveable, multimodal sensory organs: they are sensorimotor systems. As such they are key to a wide range of different behaviours, ranging from spatial orientation, search and exploration to communication. The role of active movement in antennal sensory function has received increasing attention over the past decades. For example, modern tracking techniques revealed different antennal sampling strategies and action ranges, along with their dependence on behavioural context or sensory environment. At the same time, research on species with different antennal morphology now allow comparisons across insect orders, highlighting the significance of structural and motor constraints on antennal function. Finally, studies on sensory acquisition and processing have contributed a wealth of knowledge on distinct submodalities of mechano- and chemoreception. This includes the mechanosensation of posture, movement, gravity, contact location and surface texture, as well as chemosensation of smell and taste. Here, we review our current understanding of insect antennae as sensorimotor systems. In particular, we discuss how their behavioural function (A) depends on active movement, (B) how it is shaped by structural and motor constraints, and (C) how this relates to mechano- and chemoreception. Based on an overview of antennal function and structure we propose a major functional distinction into contact antennae as opposed to non-contact antennae. Focussing on contact antennae, we then address questions about (i) distinct antennal exploration and sampling patterns, (ii) whether and how they change with behavioural context, and (iii) whether and how they differ between sensory modalities.

Introduction

The antenna is the most complex sensory organ of insects, with the term ‘complex’ relating to a combination of two properties that make the antenna outstanding compared to all other sensory organs. The first of these properties is its musculo-skeletal apparatus that moves and positions the entire sensory appendage. In some insect taxa, for example in bees and ants, the arrangement of the antennal segments and joints also allows significant active change of the antennal posture. The second property which makes the complexity of the insect antenna exceed that of any other sensory organ is the presence of receptors from four sensory modalities: mechano-, chemo-, thermo- and hygroreceptors. In addition, antennal mechano- and chemoreceptors serve two or more submodalities that are often relevant for distinct behavioural functions (e.g. sensing posture or touch, smell or taste).

Antennal motor function is linked to the evolutionary history of this appendage. The insect antenna has evolved to become a dedicated sensory limb of the head. Like the mouthparts, it is serially homologous to the walking legs (e.g. Scholtz and Edgecombe, 2006), as underscored by long-standing developmental and genetical facts (e.g. Postlethwait and Schneiderman, 1971; Schmidt-Jensen, 1914). Owing to this serial homology, the antennal base retains much of the motor infrastructure and corresponding neural control mechanisms that are also present in walking legs (Krishnan and Sane, 2015). The antenna of all Insectaa consists of three functional segments, the scape, pedicel and flagellum (Fig. 1). Of these, only the most basal one—the scape—contains musculature. Accordingly, there are two joints that are actuated by musculature (Imms, 1939), and one passive link. The basal head-scape joint (HS-joint) moves the scape relative to the head. The scape-pedicel joint (SP-joint) moves the second antennal segment—the pedicel—relative to the scape. The passive link connects the pedicel with the third functional segment, the flagellum. Although passive rotation about this link is an important sensory cue, it cannot be moved actively by musculature. In order to emphasise the difference to proper, actuated joints, Staudacher et al. (2005) proposed to call this passive link the pedicel-flagellum junction. Here, we will stay with the more common term pedicel-flagellum joint (PF-joint).

The first objective of this review is to show that the antenna is a key sensory organ for a broad range of behaviours, as different as spatial orientation and course control, active search and exploration, and communication (the latter sometimes at the receiver end, sometimes at the emitter end). An integral part of most of these behavioural functions is the control of antennal movement and position, either by active movement of the HS- and SP-joints (Staudacher et al., 2005) or by feedback control of antennal posture, e.g., in flight (Taylor and Krapp, 2007). Therefore, the first aspect of antennal complexity mentioned above arises from the interaction of motor control and sensory acquisition. We will particularly emphasise this sensory-motor interaction with regard to active exploration of the near-range environment, and sampling events that involve physical contact of the antenna with an external object. Accordingly, we will distinguish ‘contact antennae’ from ‘non-contact antennae’ (Fig. 1), depending on whether the size and structure of the antenna allows for active sampling of external surfaces, thus acquiring information about touch and/or taste from physical contact events. In contrast, non-contact antennae normally do not encounter physical contact. Fig. 1 shows examples of contact events from two insect species, one with a filiform antenna being pulled past or pressed against an external object (Fig. 1B), and another with a geniculate antennae, the tip of which is bent as it is contacting the substrate (Fig. 1C).

The second aspect of antennal complexity mentioned above refers to multiple sensory submodalities subserving distinct behavioural functions. With regard to mechanoreception this involves the senses of posture, gravity, touch, airflow (or water flow) and sound (e.g. Kamikouchi et al., 2009; Robert and Göpfert, 2002; Staudacher et al., 2005; Taylor and Krapp, 2007). With regard to chemoreception this comprises the senses of smell and taste (e.g. Carlson, 1996; Elgar et al., 2018; Hansson and Stensmyr, 2011; Suh et al., 2014). Additional functions involve the sense of temperature and humidity (e.g. Altner and Loftus, 1985; Sayeed and Benzer, 1996). The afferents from all of these sensory modalities project to the second brain segment, the deutocerebrum (Homberg et al., 1989; Rospars, 1988), though some have collateral terminals in other parts of the central nervous system (CNS). This makes the deutocerebrum a key centre for multimodal information processing in the CNS. The second objective of this review is to highlight the multimodal nature of antennal information processing, with a focus on contact antennae.

With these two objectives in mind, we will discuss the shortcomings of the current, entirely shape-based typology of insect antennae (Weber, 1933) and propose a function-based alternative. Rather than antennal shape alone, our typology uses parameters related to sensorimotor abilities and action range. For example, it emphasises the behavioural significance of the spatial boundary that divides the sensory environment into a near-range domain that is within reach of the antenna, and a far-range domain that lies beyond its reach. From a theoretical point of view, the behavioural relevance of this spatial boundary is threefold: First, it delimits the action volume of the antenna and, therefore, the possible range of physical contacts between the antenna and external objects. As a consequence, it delimits the working ranges of the mechanosensory submodality of touch and the chemosensory submodality of taste, both of which require physical contacts. Second, since action volumes of multiple limbs may overlap, contact locations within such overlap volumes may be reached by more than one limb, effectively allowing for transfer of spatial information from one limb to another (Dürr and Schilling, 2018), such that physical contact of the antenna can be reached for by a leg. Third, it delimits a range of ‘fixed-delay encoding events’. This is because physical contact events effectively couple the encoding of proprioceptive cues about antennal posture and movement at the time of contact on the one hand, and exteroceptive cues about touch or taste of the contact location on the other. Since all contact-related cues coincide physically, their neural correlates arrive at the CNS with fixed delay. In contrast, far-range cues such as sound and smell may be encoded coincidentally without having been emitted at the same time. As a consequence, the magnitude of the ‘environmental delay’ between emission and detection is unknown. Whereas the ambiguity in environmental delay is resolved for contact events, it remains for non-contact events.

We will begin with a survey of the various behavioural functions of the insect antenna, based on published experimental work on eight insect orders. It focuses on (i) sensorimotor interaction of antennal movement and sensory acquisition and on (ii) bi- or multimodal interaction on either side of the contact boundary. Table 1 summarises the content of this Section 2, loosely grouping antennal functions into three categories that mainly involve passive sensing (hearing, orientation and escape behaviour), and three categories that mainly involve active sensing (manipulation, exploration and communication). This grouping refers to Staudacher et al. (2005) who used the term ‘passive sensing’ for behaviours that typically do not require antennal movement other than feedback control of a more or less fixed antennal posture. In contrast, active sensing involves deliberate change of antennal posture to enable or at least to improve sensory acquisition in the first place. As it will become clear, this distinction between passive and active sensing becomes slightly more complicated when including multiple sensory modalities (Staudacher et al., 2005 covered mechanoreception only).

Following the survey, Section 3 will discuss how both the motor apparatus of the antenna and the structural properties of the flagellum impose constraints on behavioural function, thus providing parameters that can be used for a typology based on sensorimotor function. Finally, Section 4 will discuss current knowledge about the integration of mechanosensory and chemosensory information. This will be contrasted for two examples: contact-free airflow sensing and olfaction on the one hand, and contact-bound sensing of touch and taste on the other.

Section snippets

Behavioural functions of the insect antenna

As a pair of ‘feelers’, insect antennae typically have been treated as passive sensory ‘receivers’ that provide sensory information for the animal to base its actions on. Accordingly, early research on antennae focused on the diversity, distribution and sexual dimorphism of sensilla along the flagellum (e.g. Böhm, 1911), or the effect of partial or complete antennectomy on behavioural responses to attractive or aversive stimuli (e.g. olfaction: Glaser, 1927; touch: Brecher, 1929;

Developmental, structural and biomechanical constraints of antennal function

The various functional contexts of the insect antenna that were described in the previous Section 2 are mirrored by a large diversity of morphological forms on the one hand (e.g. Krishnan and Sane, 2015; Weber, 1933) and a wide range of different sensilla types on the other (e.g. Schneider, 1964; Zacharuk, 1985). Both antennal form and sensorisation constrain the behavioural function of an antenna. Key aspects of antennal form concern the developmental origin of its structural differentiation (

Antennal movement and multimodal integration

Given the involvement of antennae in multimodal control of behaviour (Section 2) and the structural and biomechanical constraints on active antennal movement, exploration and sampling (Section 3), this final Section 4 will discuss where multimodal information is integrated to trigger, modulate or control active antennal movement. To this end, we will focus on the integration of mechano- and chemosensory information in (i) behaviours involving non-contact information about wind and smell, and

Summary and conclusions

The main objective of this review was to outline the behavioural diversity and multi-facetted significance of active antennal movement, along with the multimodal complexity of the insect antenna. Not only is the antenna the most complex sensory organ of insects, it is also a sensorimotor system in itself. Accordingly, we claim that the study and understanding of insect antennae requires an integrative approach that seeks to explain the behavioural function of an antenna (Section 2) in relation

Acknowledgements

We thank Silvia Verwiebe for helping with the selection, documentation and identification of the specimens, Annelie Exter for producing the focal-stack images of Fig. 6, and Anke Fleischer for assistance with correcting and editing the chapter. The swarm optimisation algorithm used in conjunction with Fig. 5 was programmed by Tristan Walter, under co-supervision of VD and Mario Botsch (now TU Dortmund). The corresponding behavioural recording and manual tracking of antennal postures was done by

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