Muscular adaptations in swimming scale worms (Polynoidae, Annelida).

Marc C Allentoft-Larsen,Kakani Katija,Joost Daniels,Brett C Gonzalez,Katrine Worsaae,Karen Osborn

doi:10.1098/rsos.210541

Abstract

Annelids are predominantly found along with the seafloor, but over time have colonized a vast diversity of habitats, such as the water column, where different modes of locomotion are necessary. Yet, little is known about their potential muscular adaptation to the continuous swimming behaviour required in the water column. The musculature and motility were examined for five scale worm species of Polynoidae (Aphroditiformia, Annelida) found in shallow waters, deep sea or caves and which exhibit crawling, occasional swimming or continuous swimming, respectively. Their parapodial musculature was reconstructed using microCT and computational three-dimensional analyses, and the muscular functions were interpreted from video recordings of their locomotion. Since most benthic scale worms are able to swim for short distances using body and parapodial muscle movements, suitable musculature for swimming is already present. Our results indicate that rather than rearrangements or addition of muscles, a shift to a pelagic lifestyle is mainly accompanied by structural loss of muscle bundles and density, as well as elongation of extrinsic dorsal and ventral parapodial muscles. Our study documents clear differences in locomotion and musculature among closely related annelids with different lifestyles as well as points to myoanatomical adaptations for accessing the water column.

Highlights

Annelids are predominantly found along with the seafloor, but over time have colonized a vast diversity of habitats, such as the water column, where different modes of locomotion are necessary
This study has provided insight into the myoanatomy associated with locomotion in scale worms
Adaptations for continuous swimming are a reduction in the number, density, volume, as well as a lengthening of parapodial muscles, as seen in G. jameensis and P. iliffei

Summary

Introduction

Annelids are predominantly found along with the seafloor, but over time have colonized a vast diversity of habitats, such as the water column, where different modes of locomotion are necessary. Or continuously swimming errantian annelids have originated independently within multiple families and are here defined as animals capable of spending long periods of time suspended in the water column, maintaining their position there These ‘continuous swimmers’ are found in the water column of the deep sea, open ocean and caves [22,23], with those occurring in the open ocean referred to as holopelagic. Morphological studies of benthic errantian annelids have suggested that short and less manoeuvrable parapodia with numerous muscle groups such as those found in Aphroditidae represent the plesiomorphic condition of recent Errantia [5]. This muscle arrangement may be useful when dragging an elongate body across various substrates or even burrowing into them [5,9]. New comparative studies of parapodial myoanatomy are important for understanding parapodial evolution and functional significance for the diversification of lifestyles [5,8,9]

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Results

Discussion

Conclusion