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First published online May 19, 2008
Journal of Experimental Biology 211, 1729-1736 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.016014

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Novel sensory modalities for navigation and other behaviours

Integrative biology of an embryonic respiratory behaviour in pond snails: the `embryo stir-bar hypothesis'

Jeffrey I. Goldberg^1,*, Shandra A. Doran¹, Ryan B. Shartau¹, Julia R. Pon¹, Declan W. Ali², Rose Tam¹ and Shihuan Kuang³

¹ Department of Biological Sciences, University of Calgary, Calgary, Alberta, Canada, T2N 1N4
² Department of Biological Sciences, University of Alberta, Edmonton, Alberta, Canada, T6G 2E9
³ Department of Animal Sciences, Purdue University, West Lafayette, IN 47907-2054, USA

^* Author for correspondence (e-mail: jeff.goldberg{at}ucalgary.ca)

Accepted 12 February 2008

Summary

Embryos of freshwater snails undergo direct development from single cell to juvenile inside egg masses that are deposited on vegetation and other substratum in pond, lake and stream habitats. Helisoma trivolvis, a member of the Planorbidae family of basommatophoran snails, has served as a model for studying the developmental and physiological roles for neurotransmitters during embryogenesis. Early studies revealed that H. trivolvis embryos from stage E15 to E30, the period between gastrulation and the trochophore–juvenile transition, display a cilia-driven behaviour consisting of slow basal rotation and transient periods of rapid rotation. The discovery of a bilateral pair of early serotonergic neurons, named ENC1, which project an apical process to the embryo surface and basal neurites to ciliated cells, prompted the hypothesis that each ENC1 is a dual-function sensory and motor neuron mediating a physiological embryonic response. This article reviews our past and present studies and addresses questions concerning this hypothesis, including the following. (1) What environmental signal regulates ENC1 activity and rotational behaviour? (2) Does ENC1 function as both a primary sensory and motor neuron underlying the rotational behaviour? (3) What are the sensory transduction mechanisms? (4) How does ENC1 regulate ciliary beating? (5) Do other basommatophoran species have similar neural–ciliary pathways and behavioural responses? (6) How is the behaviour manifest in the dynamic natural environment? In this review, we introduce the `embryo stir-bar hypothesis', which proposes that embryonic rotation is a hypoxia-sensitive respiratory behaviour responsible for mixing the egg capsule fluid, thereby enhancing delivery of environmental oxygen to the embryo.

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