Raptorial jaws in the throat help moray eels swallow large prey

Most bony fishes rely on suction mechanisms to capture and transport prey. Once captured, prey are carried by water movement inside the oral cavity to a second set of jaws in the throat, the pharyngeal jaws, which manipulate the prey and assist in swallowing. Moray eels display much less effective suction-feeding abilities. Given this reduction in a feeding mechanism that is widespread and highly conserved in aquatic vertebrates, it is not known how moray eels swallow large fish and cephalopods. Here we show that the moray eel (Muraena retifera) overcomes reduced suction capacity by launching raptorial pharyngeal jaws out of its throat and into its oral cavity, where the jaws grasp the struggling prey animal and transport it back to the throat and into the oesophagus. This is the first described case of a vertebrate using a second set of jaws to both restrain and transport prey, and is the only alternative to the hydraulic prey transport reported in teleost fishes. The extreme mobility of the moray pharyngeal jaws is made possible by elongation of the muscles that control the jaws, coupled with reduction of adjacent gill-arch structures. The discovery that pharyngeal jaws can reach up from behind the skull to grasp prey in the oral jaws reveals a major innovation that may have contributed to the success of moray eels as apex predators hunting within the complex matrix of coral reefs. This alternative prey transport mode is mechanically similar to the ratcheting mechanisms used in snakes—a group of terrestrial vertebrates that share striking morphological, behavioural and ecological convergence with moray eels.

[1]  Kurt Schwenk,et al.  Feeding : form, function, and evolution in tetrapod vertebrates , 2000 .

[2]  T. Higham,et al.  Spatial and temporal patterns of water flow generated by suction-feeding bluegill sunfish Lepomis macrochirus resolved by Particle Image Velocimetry , 2005, Journal of Experimental Biology.

[3]  M. Hixon,et al.  Predation, Prey Refuges, and the Structure of Coral‐Reef Fish Assemblages , 1993 .

[4]  E. Brainerd,et al.  Post-cranial prey transport mechanisms in the black pinesnake, Pituophis melanoleucus lodingi: an x-ray videographic study. , 2002, Zoology.

[5]  G. Nelson Gill Arches of Teleostean Fishes of the Order Anguilliformes , 1966 .

[6]  M. W. Schein,et al.  Diurnal observations on the behavioral ecology ofGymnothorax moringa (Cuvier) andMuraena miliaris (Kaup) on a Caribbean coral reef , 1983, Coral Reefs.

[7]  G. Fraser,et al.  Evolution and development of complex biomechanical systems: 300 million years of fish jaws. , 2005, Zebrafish.

[8]  D. Cundall CHAPTER 9 – Feeding in Snakes , 2000 .

[9]  J. E. Randall Food habits of reef fishes of the West Indies , 1967 .

[10]  Karel F. Liem,et al.  Evolutionary Strategies and Morphological Innovations: Cichlid Pharyngeal Jaws , 1973 .

[11]  J. Parrish,et al.  Piscivory in a coral reef fish community , 1986 .

[12]  M. Hixon,et al.  Predation effects on early post-settlement survivorship of coral-reef fishes , 1995 .

[13]  A. M. Carroll,et al.  Morphology predicts suction feeding performance in centrarchid fishes , 2004, Journal of Experimental Biology.

[14]  G. Nelson Branchial Muscles in Representatives of Five Eel Families , 1967 .

[15]  P. Wainwright,et al.  Biting releases constraints on moray eel feeding kinematics , 2007, Journal of Experimental Biology.

[16]  G Dingerkus,et al.  Enzyme clearing of alcian blue stained whole small vertebrates for demonstration of cartilage. , 1977, Stain technology.

[17]  M. Westneat,et al.  Evolution of Levers and Linkages in the Feeding Mechanisms of Fishes1 , 2004, Integrative and comparative biology.

[18]  H. E. Winn,et al.  Activity Patterns, Diet, and Shelter Site Use for Two Species of Moray Eels, Gymnothorax moringa and Gymnothorax vicinus, in Belize , 2003, Copeia.

[19]  M. Alfaro,et al.  Motor Control Across Trophic Strategies: Muscle Activity of Biting and Suction Feeding Fishes1 , 2001 .

[20]  K. Schwenk CHAPTER 2 – An Introduction to Tetrapod Feeding , 2000 .

[21]  D. Kramer,et al.  Estimating the density and biomass of moray eels (Muraenidae) using a modified visual census method for hole-dwelling reef fauna , 2005, Environmental Biology of Fishes.

[22]  Tracy J. Miller Knotting: a previously undescribed feeding behavior in muraenid eels , 1987 .

[23]  J. Dymond,et al.  Fishes of the western North Atlantic. , 1963 .

[24]  G. Steven Fishes of the Western North Atlantic , 1949, Nature.

[25]  Lauder,et al.  Kinematics of feeding in bluegill sunfish: is there a general distinction between aquatic capture and transport behaviors? , 1995, The Journal of experimental biology.

[26]  G. Lauder Functional design and evolution of the pharyngeal jaw apparatus in euteleostean fishes , 1983 .

[27]  P. Wainwright,et al.  Scaling the feeding mechanism of largemouth bass (Micropterus salmoides): kinematics of prey capture , 1995, The Journal of experimental biology.