The Neural and Behavioral Basis of Chemical Communication in Terrestrial Crustaceans

Abstract

Within Crustacea, representatives of at least five major taxa have succeeded in the transition from an aquatic to a fully terrestrial lifestyle: Isopoda, Amphipoda, Astacida, Anomura, and Brachyura. Land-living crustaceans are fascinating animals that during a very limited time period at an evolutionary time scale have adapted to a number of diverse terrestrial habitats in which they have become highly successful, and in some case the predominant life forms. Living on land raises new questions regarding the evolution of chemical communication because a transition from sea to land means that molecules need to be detected in gas phase instead of in water solution. The odor stimulus also changes from mainly hydrophilic molecules in aqueous solution to mainly hydrophobic in the gaseous phase. Behavioral studies have provided evidence that some land-living crustaceans, namely terrestrial hermit crabs (Anomura, Coenobitidae) have achieved high efficiency in detecting food from a distance and in responding to airborne odors, in short, that they have evolved an excellent sense of distance olfaction. How do crustaceans on land solve the tasks of odor detection and odor information processing and how have the new selection pressures reshaped the sense of smell? In the present contribution, we review the current knowledge on morphological aspects of the olfactory system of terrestrial crustaceans focusing on representatives of the Anomura and Isopoda. Terrestrial members of the latter taxon have greatly reduced first antennae and seem to have given up their deutocerebral olfactory pathway. Instead, they have shifted gustatory abilities to the second antennae and the tritocerebrum but it remains to be shown if these animals evolved an effective system of aerial olfaction. Within the Anomura, however, terrestrial hermit crabs (Coenobitidae) have greatly inflated those parts of the brain that are responsible for primary olfactory processing, the olfactory lobes. Electro-antennographic detection studies with the well developed first antennae of the giant robber crab Birgus latro demonstrated the capacity of this organ to detect volatile chemical information. These experiments point to an olfactory system as sensitive as the most sensitive general odor detecting olfactory sensory neurons found in insects and that therefore is well suited to explore the terrestrial olfactory landscape. We also summarize ongoing efforts to explore olfactory-guided behavior of the giant robber crab on Christmas Island, Indian Ocean. We conclude that comparative studies between fully aquatic crustaceans and closely related terrestrial taxa provide a powerful means of investigating the evolution of chemosensory adaptations in these two environments. Future studies must address three main aspects: the behavior towards active odors (both pheromones and other semiochemicals) has to be clearly shown and quantified, the chemical identity of key odor cues and the source of these compounds have to be established, and the sensory base of detection and information processing in the chemical senses need to be further studied.