Two swimming modes in Trachymedusae; bell kinematics and the role of giant axons.

Matthew E Meech,Claudia E Mills,Steven H D Haddock,Robert W Meech

doi:10.1242/jeb.239830

Abstract

ABSTRACTAlthough members of the Rhopalonematidae family (Cnidaria, Hydrozoa, Trachymedusae) are known to exhibit unusually powerful jet swimming in addition to their more normal slow swimming behaviour, for the most part, reports are rare and anecdotal. Many species are found globally at depths of 600–2000 m, and so observation and collection depend on using remotely operated submersible vehicles. With a combination of in situ video footage and laboratory measurements, we have quantified kinematic aspects of this dual swimming motion and its electrophysiology. The species included are from two Rhopalonematidae clades; they are Colobonema sericeum, Pantachogon haeckeli, Crossota millsae and two species of Benthocodon. Comparison is made with Aglantha digitale, a species from a third Rhopalonematidae clade brought to the surface by natural water movement. We find that although all Rhopalonematidae appear to have two swimming modes, there are marked differences in their neural anatomy, kinematics and physiology. Giant motor axons, known to conduct impulses during fast swimming in A. digitale, are absent from C. sericeum and P. haeckeli. Slow swimming is also different; in C. sericeum and its relatives it is driven by contractions restricted to the base of the bell, whereas in A. digitale it is driven by contractions in the mid-bell region. These behavioural differences are related to the position of the different clades on a ribosomal DNA-based phylogenetic tree. This finding allows us to pinpoint the phylogenetic branch point leading to the appearance of giant motor axons and escape swimming. They place the remarkable dual swimming behaviour of members of the Rhopalonematidae family into an evolutionary context.

Highlights

The phylum Cnidaria contains a diverse collection of life forms exhibiting a wide variety of behaviours
The exceptional maximum velocity of A. digitale is associated with the presence of two sets of giant axons, which are responsible for conducting excitation around and up the animal so that the entire musculature contracts within 100 ms
We find that members of the Rhopaloneminae and Crossota clades are capable of slow swimming, but that, unlike Aglantha, these contractions are confined to the bell margin

Summary

INTRODUCTION

The phylum Cnidaria contains a diverse collection of life forms exhibiting a wide variety of behaviours. The most extensive comparative description of medusan swimming is that of Gladfelter (1972, 1973), who picked out the trachymedusa Aglantha digitale as being of particular note because it gives “a single powerful contraction in response to a probe, which is considerably more effective than the normal type”. The exceptional maximum velocity of A. digitale is associated with the presence of two sets of giant axons, which are responsible for conducting excitation around and up the animal so that the entire musculature contracts within 100 ms This violent contraction means that the base of the bell-shaped body forms a nozzle through which the bell’s water contents are expelled at high velocity (Ford and Costello, 2000). We do not explore differences in generating the rhythmicity of swimming, but instead focus on the physiology and mechanics of the movement itself

MATERIALS AND METHODS

RESULTS

DISCUSSION