Annelids are predominantly found along the seafloor, but over time have colonised 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 continuously swimming 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 and caves that exhibit crawling, occasional swimming or continuous swimming, respectively. Their parapodial musculature was reconstructed using microCT and computational 3D analyses and the muscular functions interpreted from video recordings of their locomotion. Since most benthic annelids are able to swim for short distances using body and parapodial muscle movements, suitable musculature for swimming and a pelagic lifestyle is already present. Our results also 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. In addition, our study documents clear differences in locomotion and muscular arrangement among closely related annelids with different lifestyles as well as points to myoanatomical adaptations for accessing the water column.

All video recordings were taken within 24 hours from species sampling. High-speed recordings of P.iliffei’s locomotion were taken using a monochrome camera (Sanstreak Edgertronic SC1) with different lens configurations: 2x microscope Olympus objective with adapter and extension tubes and Nikon 50 mm f/1.8lens with 12 mm or 20 mm extension tubes) at 900 fps. Extension tubes were used to achieve proper focus with the microscope objectives and to reduce the minimum focus distance with the other objectives.- Brightfield illumination was obtained by use of LED light sources and a large-diameter (200 mm) condenser lens. Locomotion of G. jameensis and H. imbricata were recorded using a Panasonic HC-VX980 Camcorder respectively at 50 and 25 fps. Locomotion recordings did not include M. longipalpa nor Branchipolynoe sp. due to lack of live specimens. Pelagomacellicephala iliffei was recorded in a square plexiglass water tank 18x15centimetres, whereas H. imbricata was recorded in a 250mLplastic algae culturing vessel. Gesiella jameensis was recorded in a 9 cm petri dish with black velvet background. All containers were filled with their respective ambient cave or seawater and having adequate space for free swimming. Selected sequences were digitized and analysed using the software DLTdv8 (Hedrick, 2008).

Locomotion of Pelagomacellicephala iliffei in lab setup, swimming, and closeup

Locomotion of Harmothoe imbricata in lab setup, crawling, and swimming

Locomotion of Gesiella jameensis in lab setup, swimming and crawling and in live recordings from cave system, swimming

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