Tooth reorientation affects tooth function during prey processing and tooth ontogeny in the lesser electric ray, Narcine brasiliensis

Abstract

The dental anatomy of elasmobranch fishes (sharks, rays and relatives) creates a functional system that is more dynamic than that of mammalian dentition. Continuous dental replacement (where new teeth are moved rostrally to replace older ones) and indirect fibrous attachment of the dentition to the jaw allow teeth to reorient relative to the jaw over both long- and short-term scales, respectively. In this study, we examine the processing behavior and dental anatomy of the lesser electric ray Narcine brasiliensis (Ölfers, 1831) to illustrate that the freedom of movement of elasmobranch dentition allows a functional flexibility that can be important for complex prey processing behaviors. From static manipulations of dissected jaws and observations of feeding events in live animals, we show that the teeth rotate during jaw protrusion, resulting in a secondary grasping mechanism that likely serves to hold prey while the buccal cavity is flushed free of sediment. The function of teeth is not always readily apparent from morphology; in addition to short-term reorientation, the long-term dental reorientation during replacement allows a given tooth to serve multiple functions during tooth ontogeny. Unlike teeth inside the mouth, the cusps of external teeth (on the portion of the tooth pad that extends past the occlusal plane) lay flat, such that the labial faces act as a functional battering surface, protecting the jaws during prey excavation.

Introduction

Predatory vertebrates are often confronted with durable materials that pose functional barriers to nourishment (i.e., spines, scales, claws, endo- and exoskeletons). Because of this, prey are often ‘processed’ to remove indigestible or damaging components but retain edible food (Dean et al. 2005b). The ability to process highly complex food (food with digestible and indigestible portions) is found in all gnathostome clades, yet there is wide variation in the anatomy of tooth attachment to the jaw skeleton and the mechanism of dental replacement; in general, the strength of the former is inversely related to the rate of the latter (Patterson 1992; Williams 2001; Shimada 2002). In species with rarely replaced dentition (e.g., most mammals), teeth are wear-resistant and embedded in deep sockets. By contrast, species with continuous dental replacement discard, erode or resorb post-functional teeth. These teeth are indirectly attached to the jaw, either by an underlying mineralized connection (some bony fishes, amphibians, reptiles) or by unmineralized fibers that merge with the fibrous outer membrane of the jaw (elasmobranchs, some bony fishes) (Shellis 1982; Powlik 1995).

The dental anatomy and method of tooth replacement exhibited by elasmobranchs (sharks, rays and relatives) allows for movement of the teeth over two time-scales. The jaw cartilage and teeth are effectively separated by a thick underlying fibrous layer (the dental ligament). As the ligament grows it transports newly erupted teeth from the caudal (closer to the tail) to the rostral (closer to the nose) margins of the jaws, replacing older teeth that are shed or worn away (Shellis 1982; Powlik 1995; Williams 2001). This continuous dental replacement results in movement of teeth over ontogeny, where growth of the dental ligament allows a given tooth to occupy different rostrocaudal positions on the jaw (tooth ontogeny) (Shellis 1982; Williams 2001). The indirect fibrous attachment of the dentition also introduces the potential for movement of teeth during the short time span of feeding events (Frazzetta and Prange 1987; Frazzetta 1994; Powlik 1995). Because of the resiliency of their attachments, teeth may be erected, flattened or pivoted, but will return to their resting positions. It is unclear how much of this movement is direct and active (e.g., in response to muscles acting on the underlying fibrous layer), direct and passive (e.g., in response to displacement by a contact with a struggling prey item or hard tissue inclusion), or indirect (e.g., simply tracking the movement of the animal's jaw) (Springer 1961; Shellis 1982; Frazzetta and Prange 1987; Frazzetta, 1988, Frazzetta, 1994; Powlik 1995; Ramsay and Wilga 2007).

Elasmobranch dentitions are typically homodont or uniform in tooth shape (with some notable heterodontic exceptions; e.g., Heterodontus spp., Sphyrna tiburo), but may be specialized for a certain diet (e.g., eating hard prey, piscivory). Homodont dentitions are traditionally considered to be stereotyped in function and less effective at prey processing relative to heterodonty, wherein non-uniform teeth perform different functions (Liem et al. 2001). It is unknown how elasmobranch dental flexibility and attachment anatomy delimit the mechanical behavior of homodont teeth during processing, although authors have hypothesized that they allow teeth to reorient to more functional positions or to avoid difficult materials (Shellis 1982; Frazzetta and Prange 1987; Witzell 1987; Frazzetta 1994; Ramsay and Wilga 2007). In this study, we use manual manipulations, kinematic and anatomical examinations, and static modeling to show that elasmobranch dental anatomy, when paired with the use of a “hydrodynamic tongue” (precisely controlled water flow through the oral cavity to separate inedible material from edible tissue; Bemis and Lauder 1986; Dean et al. 2005b), can allow functional flexibility for complex processing despite the apparent limitations of uniform tooth shape.

This study examines the dentition of the lesser electric ray, Narcine brasiliensis (Ölfers, 1831) in which the homodont, single-cusped teeth are known to adopt different positions relative to the plane of the animal's gape and therefore present different functional surfaces during tooth ontogeny and during a given prey capture cycle (Dean 2003; Dean and Motta 2004b). Using this example, it is shown that the indirect attachment and continuous replacement of this morphologically “simple” homodont dentition play important roles in this species’ complex processing behavior.

Narcine brasiliensis is a small, gape-limited batoid that specializes on polychaetes and other benthic anguilliform prey; jaw protrusion is an important part of both prey capture and processing (Dean and Motta, 2004a, Dean and Motta, 2004b). The impressive freedom of movement of the jaws of elasmobranchs is afforded by varying degrees of dissociation of the jaws from the cranium. This is most pronounced in batoids, where the hyomandibular cartilages (the dorsal-most portions of the hyoid arch) frequently are the only means of skeletal support in the jaw suspension (Wilga et al. 2001; Wilga 2002). In addition to the kinesis of the jaws relative to the cranium, jaw protrusion in N. brasiliensis is enhanced by an additional degree of freedom at the flexible symphyses, which allows reorientation of the jaw rami (left and right halves of the jaw) relative to each other as well (Figs. 1A, B; Dean and Motta, 2004a, Dean and Motta, 2004b). Protrusion is accomplished by folding the jaws at the symphyses such that the angle drawn from one jaw joint to the other via the symphysis is obtuse at rest and acute at peak protrusion (Fig. 1B). As a result of this mechanism, this species exhibits the greatest degree of jaw protrusion recorded for an elasmobranch, extending its jaws up to 100% of its head length and driving them into the sand to excavate buried polychaetes by suction feeding (Dean and Motta 2004b). For the sake of this study, this medial compression of the jaw arch will be termed ‘mesial adduction’ to distinguish it from the adduction of the upper and lower jaws during jaw closure, as in chewing.

The ingestion of buried polychaetes by suction results in large amounts of sediment in the buccal cavity; teeth are engaged with the prey item during the separation of sediment and prey (processing), not during the initial suction capture event. Processing involves cyclic protrusion and retraction of the jaws but with the jaw protruded to a lesser absolute distance than in capture (Fig. 1C). These movements result in pressure pulses that flush sediment from the spiracles, gills and mouth (Fig. 1D; Dean and Motta 2004b). Prey items often emerge from the mouth during this winnowing behavior and are held between the teeth, typically across multiple processing protrusions, until they are re-ingested during a single pronounced protrusion event (Fig. 1D, ∼1050 ms).

The teeth of N. brasiliensis are attached to fibrous pads that overlie the symphyses of the palatoquadrate (upper jaw) and mandible (lower jaw) and span approximately 60% of the lateral gape (Fig. 2A; Bigelow and Schroeder 1953; Cappetta 1987; Dean and Motta 2004a). The extreme conformational change of the jaws also deforms these pads, repositioning the teeth relative to the plane of the ray's gape (Figs. 2B, C). During protrusion, individual teeth in a given file (rostrocaudal “column” or family of teeth) move in tandem, but adjacent tooth files separate from each other rostrally and bunch together caudally like the pleats on a Japanese fan (Fig. 2C; Dean 2003). It is unknown whether this reorientation plays a role in processing, where the jaws are repeatedly mesially adducted. It has been shown that rotation of the teeth is not used to “ratchet” prey into the mouth (Dean and Motta 2004b); however, depending on the timing of prey movement relative to the extent of jaw protrusion (and therefore teeth reorientation), the cyclic motion of the jaws may serve to either rend the prey or maintain a constant grasp on it.

In addition to momentary reorientation of the teeth relative to the animal's sagittal plane during feeding, the resting shape of the tooth pads also results in older (more rostral) and younger (more caudal) teeth presenting different functional surfaces (Figs. 2A, D, E) (Bigelow and Schroeder 1953; Cappetta 1988; Dean and Motta 2004a). Unlike in most other elasmobranchs, several rows of teeth are positioned outside of the mouth due to the length of the tooth pads, which exit the mouth and turn nearly 90° to cover the rostral portion of the jaw symphyses (Figs. 2A, D; Bigelow and Schroeder 1953; Dean and Motta 2004a). Teeth inside the mouth (i.e., caudal to the occlusal plane) have erect, caudally-oriented cusps, while those outside the mouth (i.e., rostral to the occlusal plane) have dorsally- or ventrally-oriented cusps in the lower and upper jaws, respectively, that lay flat against the diamond-shaped labial face (the rostral region below the cusp) of the next youngest tooth in the file (Fig. 2E). As a result, the labial faces of teeth exposed outside the mouth form an imbricated dentition (Figs. 2A, D).

Due to the short- and long-term changes of tooth position observed in N. brasiliensis, individual teeth may serve multiple functions. This study examines the functional effects of tooth reorientation during tooth ontogeny (i.e., by comparing the wear patterns of older and younger teeth) and during prey processing (i.e., by observing the interactions of prey and teeth and modeling them using static biomechanical models). By illustrating that positional changes affect and enhance the function of this dentition, it is argued that dental kinesis and continuous replacement create a plastic functional environment that permits complex processing behaviors.