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

Abstract

Tritonia diomedea (synonymous with Tritonia tetraquetra) navigates in turbulent odour plumes, crawling upstream towards prey and downstream to avoid predators. This is probably 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 to 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 and denervated oral veils. In all treatments, animals navigated in a similar manner to that of control and sham-operated animals, indicating that a single rhinophore provides sufficient sensory input for navigation (assuming that 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 mediate odour-gated rheotaxis.

Diversity of cilia-based mechanosensory systems and their functions in marine animal behaviour

“…In fish, lamprey and tadpoles rheoreception is mediated by hair cells in the lateral line [247]. Aquatic invertebrates such as nudibranchs, brittle stars and flatworms also respond to the effects of turbulence and flow [248][249][250][251][252][253][254][255]. Ciliated sensory cells have been proposed as potential flow receptors in these and other animals [256,257] but, to our knowledge, direct physiological evidence is still lacking.…”

Olfactory navigation in aquatic gastropods

“…If they cannot, then both chemotaxis and odour-gated rheotaxis remain possibilities. To my knowledge, this test has only been carried out on one gastropod (McCullagh et al, 2014), supporting odour-gated rheotaxis as the strategy used by T. diomedea. Fully unravelling the complexities of sense organs and navigational strategies in different conditions will require testing in both still and moving water, while also manipulating the sensory input available from different sense organs.…”

“…Moreover, the navigational relevance of the food extracts used as stimuli in these experiments is not clear. Finally, in T. diomedea, although the sensory organs that detect the odours and flow used to guide navigation are well characterized (McCullagh et al, 2014;Wyeth and Willows, 2006b), we do not know how this input is integrated to control the crawling and turning motor neurons identified in other studies (Cain et al, 2006;Murray et al, 1992Murray et al, , 2006Popescu and Willows, 1999;Redondo and Murray, 2005) Open questions Predator avoidance navigation behaviour…”

“…However, there is evidence that T. diomedea can navigate with a single sensor and without substantial casting (which could permit spatial sampling of any odour gradients), suggesting it probably uses odour-gated rheotaxis (Fig. 4;McCullagh et al, 2014). As both strategies can be effective in odour plumes, categorically distinguishing the two is experimentally challenging (Box 1).…”

Chemosensory afference in the tentacle nerve ofLymnaea stagnalis

“…However, a major gap in this work has been in fully understanding the peripheral components of the sensory systems (Croll 2003). Numerous studies have explored the neuroanatomy and functional roles of gastropod cephalic sensory organs (e.g., Fredman and Jahan-Parwar 1980; Chase and Tolloczko 1993; Gobbeler and Klussmann-Kolb 2007; Wollesen et al 2007; Wyeth and Croll 2011; McCullagh et al 2014). Yet, the sensory modalities remain unknown for the abundant and varied putative peripheral sensory cell types, as does much of the peripheral neural circuitry and functional integration with the central nervous system (Wyeth 2019).…”