A critical period of susceptibility to sound in the sensory cells of cephalopod hatchlings.

Marta Solé,Michel André,José-Manuel Fortuño,Marc Lenoir,Mike Van Der Schaar

doi:10.1242/bio.033860

Abstract

ABSTRACTThe cephalopod statocyst and lateral line systems are sensory organs involved in orientation and balance. Lateral lines allow cephalopods to detect particle motion and are used for locating prey or predators in low light conditions. Here, we show the first analysis of damaged sensory epithelia in three species of cephalopod hatchlings (Sepia officinalis, Loligo vulgaris and Illex coindetii) after sound exposure. Our results indicate lesions in the statocyst sensory epithelia, similar to what was found in adult specimens. The novelty is that the severity of the lesions advanced more rapidly in hatchlings than in adult animals; i.e. the degree of lesions seen in hatchlings immediately after noise exposure would develop within 48 h in adults. This feature suggests a critical period of increased sensitivity to acoustic trauma in those species as has been described in developing mammalian cochlea and avian basilar papilla. The hair cells in the lateral lines of S. officinalis followed the same pattern of damage occurrence, while those of L. vulgaris and I. coindetii displayed a decreasing severity of damage after 24 h. These differences could be due to dissimilarities in size and life stages between the three species.

Highlights

There is a considerable lack of information concerning the cephalopod’s reception of sounds (Packard et al, 1990; Bleckmann et al, 1991; Bullock and Budelmann, 1991; Budelmann et al, 1995; Hu et al, 2009; Kaifu et al, 2008; Mooney et al, 2010)
The early differentiation of the olfactory organ (Fig. S2F,G) in L. vulgaris hatchlings and the peculiar development of the epidermis together with its sensory cells allow comparing developmental processes within the molluscs phylum (Buresi et al, 2014; Polese et al, 2016). These results confirm that the statocyst and the lateral line sensory epithelia are specialised in sound perception, and can suffer acoustic trauma when exposed to loud sound sources while the other observed sensory epithelia are not affected
We showed in I. coindetii, additional sensory ciliated structures like lip chemoreceptors (Fig. 2); ciliated receptors and sensory cells are described on the finger-like papillae that distally fold the muscular lip around the beaks in O. joubini (Emery, 1975)

Summary

Introduction

There is a considerable lack of information concerning the cephalopod’s reception of sounds (Packard et al, 1990; Bleckmann et al, 1991; Bullock and Budelmann, 1991; Budelmann et al, 1995; Hu et al, 2009; Kaifu et al, 2008; Mooney et al, 2010). Cephalopods are sensitive to vibration stimuli and are able to perceive these stimuli through the statocyst receptor and the lateral line analogue systems (Budelmann et al, 1997; Budelmann and Bleckmann, 1988). Many cephalopods have lines of ciliated cells on their head and arms which are considered invertebrate analogue to the mechanoreceptive lateral lines of fish and aquatic amphibians. This is an example of convergent evolution between a sophisticated cephalopod and a vertebrate sensory system (Budelmann and Bleckmann, 1988). Stimulation of the lines with artificial water displacements of defined frequency and amplitude evoke receptor potentials with features very similar to the lateral microphonic potential of fish (Bleckmann et al, 1991; Budelmann et al, 1997; Budelmann and Bleckmann, 1988)

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Conclusion