Diverse anguilliform swimming kinematics in Pacific hagfish (Eptatretusstoutii) and Atlantic hagfish (Myxineglutinosa)

Abstract

Anguilliform mode swimmers pass waves of lateral bending down their elongate bodies to propel forward. Hagfishes (Myxinidae) are classified as anguilliform swimmers, but their unique habits and reduced morphology—including a flexible body lacking a vertebral column—have the potential to translate into unique swimming behaviour within this broad classification. Their roles as active scavengers and hunters can require considerable bouts of swimming, yet quantitative data on hagfish locomotion are limited. Here, we aim to provide a more complete mechanistic understanding of hagfish swimming by quantifying whole-body kinematics of steady swimming in Pacific hagfish (Eptatretus stoutii (Lockington, 1878)) and Atlantic hagfish (Myxine glutinosa L., 1758), species from the two main lineages of Myxinidae. We analyzed high-speed video of hagfishes swimming at voluntary swim speeds and found that both species swim using high-amplitude undulatory waves. Swim speed is generally frequency-modulated, but patterns in wave speed, wavelength, and amplitude along the body and across swim speeds are variable, implying versatile mechanisms for the control of swim speed in these highly flexible fishes. We propose mechanistic explanations for this kinematic variability and compare hagfish with other elongate swimmers, demonstrating that the hagfish’s rich locomotory repertoire adds variety to the already diverse set of locomotory kinematics found in anguilliform swimmers.

Mechanisms of anguilliform locomotion in fishes studied using simple three-dimensional physical models

“…Anguilliform locomotion in fishes is common to many elongate species and is often defined as occurring when more than one wavelength of body bending is present at any given time (e.g., Webb 1975, Lindsey 1978. This mode of swimming has been studied in a number of species, including hagfish (Long et al 2002, Lim andWinegard 2015), eels (Gillis 1998, Tytell 2004, lamprey (Tytell et al 2010, Dabiri et al 2014, Williams and McMillen 2015, and swimming snakes (Jayne 1985, Munk 2008. Hagfishes (Myxinidae) are anguilliform swimmers that are particularly well-approximated by simple physical models.…”

“…Their bodies, which are mostly cylindrical with some lateral compression toward the caudal end (figure 1; Hart 1973), lack discrete fins and a fully developed vertebral column, retaining a flexible cartilaginous notochord into adulthood instead (Long et al 2002, Ota et al 2011. As a result, there is relatively little variation in body flexibility along the length of hagfish, and rod-like approximations are a reasonable first approach to understand patterns of body oscillation which have recently been studied experimentally in live hagfish (Lim and Winegard 2015).…”

“…A series of traced midlines from sequential instances in time, each separated by Δt = 0.04 s, are overlaid on top of one another to indicate the lateral amplitude envelope for a typical whole tail beat cycle. Modified from Lim and Winegard (2015).…”

Evolution of the notochord

“…Animals swimming by undulation include some vertebrates (especially elongate fishes [ 1 ]) and diverse invertebrates [ 2 – 13 ] (Table 1 ). These movements are generated when longitudinal muscles contract against a hydrostatic skeleton.…”

Hagfish Houdinis: biomechanics and behavior of squeezing through small openings

“…Although it was long believed that hagfishes are mostly sedentary animals, it has more recently come to light that they can be active scavengers and hunters that rely on elaborate locomotor and behavioral repertoires (Zintzen et al, 2011;Lim and Winegard, 2015). Hagfishes are burrowers (Gustafson, 1935;Strahan, 1963;Fernholm, 1974) and anguilliform-mode swimmers (Adam, 1960), and they are capable of tying themselves into knots (Adam, 1960;Clark et al, 2016).…”