Elsevier

Zoology

Volume 114, Issue 2, April 2011, Pages 78-84
Zoology

Kinematics of swimming in two burrowing anguilliform fishes

https://doi.org/10.1016/j.zool.2010.10.004Get rights and content

Abstract

Anguilliform or eel-like fishes are typically bottom dwellers, some of which are specialized burrowers. Although specializations for burrowing are predicted to affect the kinematics of swimming, it remains unknown to what extent this is actually the case. Here we examine swimming kinematics and efficiency of two burrowing anguilliform species, Pisodonophis boro and Heteroconger hassi, with different degrees of specialization for burrowing. Our data suggest that differences in the swimming kinematics may indeed be related to the differences in burrowing specialization and style between both species. The resemblance between the swimming kinematics of P. boro and previously published data for Anguilla anguilla and Anguilla rostrata may be linked with the relatively limited burrowing specialization of P. boro and suggests an overall stereotypy in anguilliform forward-swimming patterns. The body of H. hassi, in contrast, is more specialized for tail-first burrowing and backward swimming bears a striking resemblance to the backward burrowing motions observed in this species. These motions differ significantly from backward swimming in Anguilla and in P. boro. The kinematics of forward swimming are, however, comparable across species. Thus, our data suggest that specializations for burrowing may affect swimming kinematics in anguilliform fishes, but also that forward swimming and burrowing are not necessarily incompatible. Future studies comparing the kinematics and mechanics of burrowing in these and other anguilliform fishes are needed to better understand how specializations for burrowing constrain backward swimming in H. hassi.

Introduction

Anguilliform or eel-like fishes are characterized by an elongated and flexible body and swim using backward moving waves of lateral body undulations. Their body shape seems particularly well suited for swimming through narrow passages in a complexly structured environment, rather than for a pelagic continuous swimming lifestyle (Nelson, 1994). Yet, extreme cases of horizontal and vertical sustained pelagic swimming are known for migratory species such as Anguilla anguilla or Anguilla rostrata (Aarestrup et al., 2009).

Some anguilliform species have adopted a burrowing lifestyle involving different levels of specialization. Although little is known about burrowing in anguilliform fishes in general, anecdotal observations suggest that these animals burrow by means of lateral undulations of the body, even in pelagic species like Anguilla japonica (Aoyama et al., 2005). Yet, species differ in whether they burrow head or tail first and this has consequences for their morphology. For example, tail-first burrowers have a more rigid distal tail segment allowing them to penetrate the substrate tail-first (De Schepper et al., 2007a, De Schepper et al., 2007b). An increased strengthening of intervertebral connections along the caudal region could also benefit burrowing, but may also, in turn, affect the flexibility of the tail, and consequently the kinematics of swimming.

Previous studies on anguilliform swimming have been limited to two closely related and morphologically similar species: A. anguilla (European eel) and A. rostrata (American eel). Although often considered good models for anguilliform fishes (Smith, 1989a), both the European and American eel are unusual as they undertake migrations to the Sargasso Sea involving continuous locomotion over thousands of kilometers without feeding (van Ginneken et al., 2005). In contrast, most tropical eel species migrate over much shorter distances to spawn (Aoyama et al., 2003). Given the presumably strong selection on efficient swimming and the deep sea origin (Inoue et al., 2010) of both Anguilla species, these animals may potentially not be the most representative models for locomotion in anguilliform fishes in general.

In the present study, we provide a kinematic description of swimming in two burrowing anguilliform fishes with a different degree of burrowing specialization: Pisodonophis boro (Ophichthidae) and Heteroconger hassi (Congridae) (Smith, 1989a, Smith, 1989b, De Schepper et al., 2007a, De Schepper et al., 2007b). The former species is a less specialized burrower, which burrows both head- and tail-first. The latter species is a specialized tail-first burrower. In the present paper we quantify the kinematics of forward swimming in both species and additionally provide base-line data on backward swimming. To test whether a burrowing lifestyle affects the kinematics and efficiency of swimming, we compare the swimming kinematics across species and to previously published data for migratory anguillids. We predict that the swimming kinematics of the more specialized H. hassi will be more divergent from A. anguilla and A. rostrata than those of the more generalized P. boro. Given the specialized tail morphology including a stiffening of the posteriormost segment (De Schepper et al., 2007b), we predict lower tail undulation amplitudes in H. hassi. Additionally, we predict that the tail-first burrowing H. hassi will be more constrained in its backward-swimming movements (i.e., display a more stereotyped movement pattern) than in its forward swimming, given its specialized burrowing behavior (Tyler and Smith, 1992).

Section snippets

Study animals

The fish used in this study were obtained through commercial trade. P. boro eels were maintained at 25 °C in a freshwater aquarium, the bottom of which was covered with gravel. H. hassi is a marine species and individuals were maintained in an aquarium with artificial salt water (salinity = 24%, temperature = 25 °C), the bottom of which was covered with a 25 cm layer of sand. For the acquisition of the kinematic data, three individuals of P. boro and two individuals of H. hassi were used. The P. boro

Kinematics of swimming

As illustrated in Fig. 1, forward swimming in both species is characterized by lateral body undulations with amplitudes increasing from snout to tail tip (P. boro: r2 = 0.99, P < 0.001; H. hassi: r2 = 0.83, P = 0.002; Fig. 3). This increase is less constant for H. hassi, which has an amplitude profile that levels off in the tail region (body position 0.7–0.9 in Fig. 3) before increasing further toward the tail tip. The undulation amplitudes are not significantly correlated with the position along the

Comparative swimming kinematics

Forward swimming in both P. boro and H. hassi follows the same general trends observed for other fishes using undulatory swimming modes (Alexander, 2003), with the undulation amplitude increasing from the snout towards the tail tip during forward swimming. The undulation frequency is correlated with the specific swimming speed, while the tail tip amplitude, undulation wave length and stride length are not. The undulation frequency increases with increasing swimming speed, indicating that higher

Acknowledgement

Funded by a research program of the fund for scientific research, Flanders (FWO-Vl G.0388.00).

References (25)

  • K. Aarestrup et al.

    Oceanic spawning migration of the European eel (Anguilla anguilla)

    Science

    (2009)
  • R.McN. Alexander

    Principles of Animal Locomotion

    (2003)
  • J. Aoyama et al.

    Short-distance spawning migration of tropical fresh water eels

    Biol. Bull.

    (2003)
  • J. Aoyama et al.

    First observations of the burrows of Anguilla japonica

    J. Fish Biol.

    (2005)
  • M.-L. Bauchot et al.

    Sur Heteroconger longissimus Günther (Téléostéen anguilliforme) et quelques aspects de sa biologie

    Bull. Mus. Natl. Hist. Nat., Sér.

    (1958)
  • K. D’Août et al.

    A kinematic comparison of forward and backward swimming in the eel Anguilla anguilla

    J. Exp. Biol.

    (1999)
  • N. De Schepper et al.

    Pisodonophis boro (Ophichthidae: Anguilliformes): specialization for head-first and tail-first burrowing?

    J. Morphol.

    (2007)
  • N. De Schepper et al.

    Morphological specializations in Heterocongrinae (Anguilliformes: Congridae) related to burrowing and feeding

    J. Morphol.

    (2007)
  • G.B. Gillis

    Environmental effects on undulatory locomotion in the American eel Anguilla rostrata: kinematics in water and on land

    J. Exp. Biol.

    (1998)
  • J.G. Inoue et al.

    Deep-ocean origin of the freshwater eels

    Biol. Lett.

    (2010)
  • M.J. Lighthill

    Note on the swimming of slender fish

    J. Fluid Mech.

    (1960)
  • M.J. Lighthill

    Aquatic animal propulsion of high hydromechanical efficiency

    J. Fluid Mech.

    (1970)
  • Cited by (14)

    • Implementing 3-D high maneuvers with a novel biomimetic robotic fish

      2014, IFAC Proceedings Volumes (IFAC-PapersOnline)
    View all citing articles on Scopus
    View full text