Chemical Ecology of Arachnids - Morphology, Behaviour, and Semiochemicals

Arachnids represent a diverse and ecologically influential paraphyletic assemblage of chelicerate arthropods that has colonized virtually every terrestrial habitat. Arachnids contribute to ecosystems as predators, parasites and decomposers. Yet, the chemical mechanisms that allow arachnids to interact with the environment remain strikingly understudied relative to their taxonomic breadth. Much of what is known for insect chemical communications has yet to be investigated for arachnids. Compared to insects, arachnids lack antennae and only share two out of three chemo-receptor families which mediate chemoreception across Insecta. The sophisticated and structural diversity with which arachnids taste and smell recently gained appreciation. Here, we compare the diverse modified appendages that enable gustation and olfaction of arachnids: from pectines of scorpions and malleoli of solifuges to the Haller’s organ of ticks and the antenniform legs of amblypygids. The detected chemical information mediates basic behaviours including mate recognition and choice, social interactions, prey or host detection and predator avoidance. Our review provides a comprehensive synthesis of arachnid chemical ecology, from sensory detection to behavioural response. We provide an overview of the diversity of arachnid behaviours in response to semiochemicals, from pheromones through cuticular hydrocarbons to kairomones. The few identified semiochemicals produced by arachnids are likewise discussed and compared against those of the better studied insects. We catalogue the underlying morpho-anatomy of chemosensory organs across Arachnida and discuss where investigations could yet reveal chemosensory structures. We record the electrophysiological evidence linking sense organs to specific semiochemicals as well as sense organs to behavioural responses, highlighting the technical challenges and recent methodological advancements. Yet critical questions persist for the chemical ecology of Arachnida: Which chemoreceptor families detect pheromones, kairomones, and other semiochemicals? Where are the chemosensory organs located on the body, apart from the few that have been identified? Recent advances in genomics, transcriptomics, electrophysiology, and metabolomics now offer unprecedented opportunities to bridge knowledge gaps. Comparative analyses of chemoreceptor gene candidates amongst transcript profiles, coupled with computer tracked behavioural assays, are beginning to reveal the molecular and neural mechanisms that shape arachnid chemical communication. We identify the ongoing challenges that can now be addressed with improved methodology. Particularly the scarcity of identified pheromones across most Arachnida or the near absence of integrative studies in smaller, historically neglected orders. By integrating perspectives from evolutionary biology, chemical ecology at different spatial scales, neurology and metabolomics, we outline priority directions for future research to uncover the breadth, complexity, and evolutionary origins of chemical communication across Arachnida.