Burrowing and subsurface locomotion in anguilliform fish: behavioral specializations and mechanical constraints.

Fish swimming is probably one of the most studied and best understood locomotor behaviors in vertebrates. However, many fish also actively exploit sediments. Because of their elongate body shape, anguilliform fishes are not only efficient swimmers but also very maneuverable. Consequently, many species live in complexly structured environments near the bottom and many are known to burrow into the sediment. To better understand burrowing and subsurface locomotion in anguilliform fish we provide descriptive kinematic data on subsurface locomotion in a burrowing eel (Pisodonophis boro) using videofluoroscopy. We also measured the maximal forces that can be exerted by this species during head-first and tail-first burrowing, and explored the implications of head-first burrowing on mechanical stress distribution in the skull. Our data show that P. boro uses lateral undulation to penetrate and move in sandy sediments under water. The kinematics of subsurface locomotion are different from those observed during swimming and are characterized by a very high slip factor. These observations differ considerably from recently published data in terrestrial sand-swimming lizards, and suggest that the sediment behaves like a solid rather than a frictional fluid. Finally, our finite element models show that the cranial shape and structure in the head-first burrowing P. boro is mechanically more suited for head-first burrowing than that of an obligate tail-first burrowing species, Heteroconger hassi.

Pisodonophis boro (ophichthidae: anguilliformes): specialization for head-first and tail-first burrowing?

The rice paddy eel, Pisodonophis boro (P. boro), is of special interest because of its peculiar burrowing habits. P. boro penetrates the substrate tail-first, a technique common for ophichthids, but it is able to burrow head-first as well. P. boro exhibits three feeding modes: inertial feeding, grasping, and spinning. Rotational feeding is a highly specialized feeding mode, adopted by several elongate, aquatic vertebrates and it is likely that some morphological modifications are related to this feeding mode. The detailed morphology of the head and tail of P. boro is examined with the goal to apportion the anatomical specializations among head-first burrowing, tail-first burrowing, and rotational feeding. The reduced eyes, covered with thick corneas may be beneficial for protection during head-first burrowing, but at the same time decreased visual acuity may have an impact on other sensory systems (e.g. cephalic lateral line system). The elongated and pointed shape of the skull is beneficial for substrate penetration. The cranial bones and their joints, which are fortified, are advantageous for resisting high mechanical loads during head-first burrowing. The aponeurotic connection between epaxial and jaw muscles is considered beneficial for transferring these forces from the body to the head during rotational feeding. Hypertrophied jaw muscles facilitate a powerful bite, which is required to hold prey during spinning movements and variability in the fiber angles of subdivisions of jaw muscles may be beneficial for preventing the lower jaw from being dislodged or opened. Furthermore, firm upper (premaxillo-ethmovomerine complex) and lower jaws (with robust coronoid processes) and high neurocranial rigidity are advantageous for a solid grip to hold prey during rotational feeding. The pointed shape of the tail and the consolidated caudal skeleton are beneficial for their tail-first burrowing habits. It is quite likely that the reduction of the caudal musculature is related to the tail-first burrowing behavior because the subtle movements of the caudal fin rays are no longer required.

Kinematics of swimming in two burrowing anguilliform fishes.

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.