Prey capture behavior and kinematics of the Atlantic cownose ray, Rhinoptera bonasus
Introduction
Functional and dietary specialization typically come at the price of versatility. The jaw morphology of the cownose ray (Elasmobranchii: Batoidea: Rhinoptera bonasus) reflects its durophagous diet of benthic bivalve mollusks, crustaceans, and polychaetes (Bigelow and Schroeder, 1953; Orth, 1975; Smith, 1980; Schwartz, 1989; Collins, 2005): the symphyses are fused, stout ligaments limit the gape, and the cartilage is reinforced with calcified struts (Summers, 2000). Compared with more basal rays (Fig. 1), the jaws of cownose rays are extremely robust and the teeth have been reduced to an imbricated, pavement-like dentition.
The very factors that make this morphology suited for durophagy seem in conflict with the excavation behaviors needed to retrieve hard prey. Although R. bonasus is known to create large feeding pits (up to 1 m wide and 20–45 cm deep) when feeding in seagrass beds (Orth, 1975), the jaws are neither flexible nor protrusible enough to be shoved into the sand as a primary excavation tool (as in the lesser electric ray, Narcine brasiliensis; Dean and Motta, 2004). As a result, previous ecological and observational studies have hypothesized excavation mechanisms of either pectoral fin flapping or hydraulic jetting from the mouth or gills (VanBlaricom, 1976; Howard et al., 1977; Gregory et al., 1979).
In this study, we investigate the feeding behavior of the cownose ray in order to resolve the discordance between its jaw morphology and benthic feeding habit. We hypothesized a primarily hydraulic excavation mechanism for two reasons: (1) Like most myliobatid rays, cownose rays are active swimmers with greatly enlarged pectoral fins. Clearing a pit localized below the mouth would be much more difficult with fins where the margins are far removed from the center of the body; (2) suction feeding is apparently the basal prey capture mechanism conserved in all batoids except filter feeders (Motta, 2004). Hydrodynamic excavation (i.e., coughing) is simply the reverse of this process. For this reason, we also expected inertial suction feeding in our analysis of the cranial kinematics of prey capture.
Excavation and prey capture in cownose rays may also be aided by the fleshy cephalic lobes, which are modified anterior extensions of the pectoral fins. Cephalic lobes are only present in myliobatid rays, where the position and orientation varies considerably. In their most reduced condition, they form the immobile and unpaired rostra of bat rays (Myliobatis) and eagle rays (Aetobatus) (McEachran et al., 1996; McEachran and Aschliman, 2004). In cownose rays (Rhinoptera), they are protractile, paired cephalic lobes, which are further enlarged in Mobula spp. and Manta spp. into terminal cephalic wings (Nelson, 1994; McEachran et al., 1996; McEachran and Aschliman, 2004; Fig. 1). These lobes are covered in mechanotactile and electrosensory pores, similar to all elasmobranch rostra, and have a supposed sensory role. While cephalic lobes apparently serve a hydrodynamic function in filter feeders (Manta birostris, Mobula tarapacana; Notarbartolo-Di-Sciara and Hillyer, 1989; Motta, 2004), previous observations suggest they will be used by Rhinoptera to prevent the escape of benthic prey and/or to help push food into the mouth (Moss, 1977; Smith and Merriner, 1985; Schwartz, 1989; Summers, 2000). The reliance on pectoral fins for locomotion in derived batoids (Fig. 1) and the necessity of handling benthic prey also suggest that Rhinoptera may benefit from a mechanism for prey manipulation that does not involve the pectoral fins.
Section snippets
Natural feeding behavior
As a supplement to laboratory experiments, the feeding behavior of wild Rhinoptera bonasus was observed during April–July of 1998 in shallow waters of the Gulf of Mexico near Anna Maria Island, FL. Large schools of cownose rays (approximately 50–75 individuals) were followed in water 1 m deep over a sandy substrate. Qualitative data from several hours of footage were taken on prey approach, capture, and processing behavior with a Hi-8 video camera (Fuji H128SW) in an underwater housing. Footage
Observations of natural feeding
The active cephalic lobe use is a major functional motif in cownose ray feeding. For the sake of this discussion, lobes in resting position (flush with the ventral body wall) are considered ‘retracted’, lobes depressed and parallel to the sediment are ‘horizontally oriented’, and lobes depressed to a vertical orientation are ‘fully depressed’ (Fig. 2).
Rays fed in the shallow, nearshore habitat either early in the morning or later in the afternoon when visibility was clear (>3 m horizontal) and
Expansive phase protrusion and spiracle kinematics
The food/prey capture behavior of R. bonasus is characterized by nearly constant locomotion, prey excavation by buccal oscillations, and dexterous food manipulation with the cephalic lobes and jaws. The cownose ray uses inertial suction to capture food, employing a kinematic pattern that is generally consistent with other elasmobranchs (Motta, 2004). In particular, our data illustrate notable aspects of upper jaw and spiracle movements, likely related to this species’ benthic suction feeding.
Summary
Prey/food capture in R. bonasus is distinguished by unique methods of excavation, winnowing and prey handling. Inertial suction capture is facilitated by the timing of spiracle, mouth, and gill slit movements which ensure that water only enters through the mouth. Excavation of buried food under these conditions is accomplished by repeated jaw opening and closing movements. These buccal oscillations re-suspend the sand and food, allowing partial external winnowing of edible and inedible items.
Acknowledgments
This research was funded by the University of South Florida-Mote Marine Laboratory Graduate Fellowship in Elasmobranch Biology to D.E. Sasko, and a UCI CORCLR grant to M.N. Dean. Equipment was funded by NSF Grant No. IBN9807863 to P.J. Motta and R.E. Hueter. Special thanks to the MML and Mote Aquarium staff for assistance in obtaining and caring for the rays. This work was greatly enhanced by discussions with the Motta lab and the USF-FIT FISH group, and by indefatigable statistics help from
References (52)
- et al.
Feeding behavior and kinematics of the lesser electric ray, Narcine brasiliensis
Zoology
(2004) - et al.
Quantification of flow during suction feeding in bluegill sunfish
Zoology
(2003) - et al.
Interrelationships of the batoid fishes (Chondrichthyes: Batoidea)
Reproduction, life history, and ecology of the round stingray, Urolophus halleri Cooper
Fish. Bull.
(1967)Fine analysis of predatory and defensive motor events in Torpedo marmorata (Pisces)
J. Exp. Biol.
(1986)- et al.
Morphology and function of the feeding apparatus of the lungfish, Lepidosiren paradoxa (Dipnoi)
J. Morphol.
(1986) - et al.
Sawfishes, guitarfishes, skates and rays. Fishes of the western North Atlantic
Mem. Sears Mem. Found. Mar. Res.
(1953) - et al.
Night-shocker: predatory behavior of the Pacific electric ray (Torpedo californica)
Science
(1978) - et al.
Functional morphology of prey capture in the sturgeon, Scaphirhynchus albus
J. Morphol.
(2003) Observations on the habits and distribution of certain fishes taken on the coast of North Carolina
Bull. Am. Mus. Nat. Hist.
(1910)
Eating without hands or tongue: specialization, elaboration and the evolution of prey processing mechanisms in cartilaginous fishes
Bio. Lett.
Food capture kinematics of the suction feeding horn shark, Heterodontus francisci
Environ. Biol. Fish.
Feeding mechanisms in sharks and other elasmobranchs
Movements of cephalic components during feeding in some requiem sharks (Carcharhiniformes: Carcharhinidae)
Copeia
Anatomical comparison of the cephalic musculature of some members of the Superfamily Myliobatoidea (Chondrichthyes): implications for evolutionary understanding
Anat. Rec. (Part A)
Comparative anatomy of the Superfamily Myliobatoidea (Chondrichthyes) with some comments on phylogeny
J. Morphol.
On how some rays (Elasmobranchia) excavate feeding depressions by jetting water
J. Sed. Petrol.
History of the spotted eagle ray, Aetobatus narinari, together with a study of its external structures
Carn. Inst. Wash.
Captive husbandry and bioenergetics of the spiny butterfly ray, Gymnura altavela (Linnaeus)
Zool. Biol.
Biogenic sedimentary structures formed by rays
J. Sed. Petrol.
Water flow patterns during prey capture by teleost fishes
J. Exp. Biol.
Functional morphology
Prehensile use of perioral bristles during feeding and associated behaviors of the Florida manatee (Trichechus manatus latirostris)
Mar. Mamm. Sci.
Food handling ability and feeding-cycle length of manatees feeding on several species of aquatic plants
J. Mamm.
Morphology of the mechanosensory lateral line system in elasmobranch fishes: ecological and behavioral considerations
Environ. Biol. Fish.
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