Kinematics of swimming in two burrowing anguilliform fishes
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).
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