One rhinophore likely provides sufficient sensory input for odour-based navigation by the nudibranch mollusc, Tritonia diomedea

Abstract

Abstract Tritonia diomedea (synonymous with T. tetraquetra) navigates in turbulent odour plumes, crawling upstream towards prey and downstream to avoid predators. This is likely accomplished by odour-gated rheotaxis, but other possibilities have not been excluded. Our goal was to test whether T. diomedea uses odour-gated rheotaxis and simultaneously determine which of the cephalic sensory organs (rhinophores and oral veil) are required for navigation. In a first experiment, slugs showed no coherent responses to streams of odour directed at single rhinophores. In a second experiment, navigation in prey and predator odour plumes was compared between animals with unilateral rhinophore lesions, denervated oral veils, or combined unilateral rhinophore lesions plus denervated oral veils. In all treatments, animals navigated similarly to control and sham operated animals, indicating a single rhinophore is sufficient sensory input for navigation (assuming a distributed flow measurement system would also be affected by the denervations). Amongst various potential navigational strategies, only odour-gated positive rheotaxis can produce the navigation tracks we observed in prey plumes while receiving input from a single sensor. Thus, we provide strong evidence that T. diomedea uses odour-gated rheotaxis in attractive odour plumes, with odours and flow detected by the rhinophores. In predator plumes, slugs turned downstream to varying degrees rather than orienting directly downstream for crawling, resulting in greater dispersion for negative rheotaxis in aversive plumes. These conclusions are the first explicit confirmation of odour-gated rheotaxis as a navigational strategy in gastropods, and are also a foundation for exploring the neural circuits that implement odour-gated rheotaxis.