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Transition from sea to land: Olfactory function and adaptations in terrestrial crustaceans

Final Report Summary - LAND CRAB OLFACTION (Transition from sea to land: Olfactory function and adaptations in terrestrial crustaceans)

Project context and objectives

The ability to recognise and react to chemical cues in the environment is essential for most animals. The objectives of this research project have been to investigate odour-directed behaviour and its underlying neurobiological substrate in terrestrial crustaceans (Coenobitidae), and to compare olfactory function and principles of these terrestrial crabs with closely related marine crustaceans and with more ancient related insects, so as to further understand how environmental and evolutionary forces dictate specific adaptations in olfactory systems.

Work performed

Two main systems have been studied: the land hermit crab Coenobita clypeatus and the robber crab Birgus latro. Previous studies have shown that Coenobitidae use olfaction on land, and superb processing capacities of their olfactory system have been indicated (reviewed by Hansson et al., 2011, In: Breithaupt & Thiel (eds) Chemical communication in crustaceans). However, virtually nothing is known about what type of chemical compounds were detected. In order to identify active odorants, electroantennogram (EAG) recordings were performed in C. clypeatus, screening 140 compounds from different chemical classes. Antennular response was established to several carboxylic acids, aldehydes and amines, a few alcohols and to water vapour, whereas several other odorants tested, typically used as foraging cues by insects (e.g. esters, lactones and ketons), were physiologically inactive. Interestingly, different chemical groups generate reverse EAG responses, which also appears for Coenobita compressus and the marine hermit crab Pagurus bernhardus. Furthermore, the behavioural relevance of some physiologically active compounds was verified in a two-choice bioassay with C. clypeatus. Here it was found that, although not attractive in itself, water vapour is critical for natural and synthetic odorants to induce behavioural responses, since crabs were only attracted to, or repelled by, odorants when presented in combination with water. The great importance of humidity on olfaction was confirmed by running EAG under different humidity levels, where the physiological response was found to be much greater at higher humidity in C. clypeatus, whereas no such effect was found in the fruit fly Drosophila melanogaster. Finally, it was found that when a highly attractive, complex food odour was fractionated based on polarity, only the most polar fraction remained attractive to the crabs. In conclusion, our results reveal that although functional on land, the olfactory system of C. clypeatus seems to be restricted to a limited number of water-soluble molecules as olfactory stimuli, and that high humidity is most critical for its function, possibly because of the animals' aquatic origin.

In addition, field experiments were carried out on Christmas Island, as part of a collaborative research project investigating chemical/population ecology of B. latro. Results suggest that B. latro has evolved an olfactory system further adapted to life on land, since also typical terrestrial, hydrophobic odorants generate physiological and behavioural activity. Developing single sensillum recordings and optical imaging techniques in C. clypeatus have been part of this research project, and is presently being carried on by others within the host department.

Main results

The results of this research project have importance for understanding mechanisms and constraints in arthropod olfaction, significantly within basic, fundamental research by contributing to our general understanding of the olfactory sense, as well as in future applications within applied research e.g. when designing biological traps for pest/invasive species. Additionally, an increased knowledge base of the life and ecology of these land crabs has significance for tropical ecosystem management.