Raptorial jaws in the throat help moray eels swallow large prey

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Abstract

Most bony fishes rely on suction mechanisms to capture and transport prey1. 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 swallowing1,2. Moray eels display much less effective suction-feeding abilities3. 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 cephalopods4,5,6,7. 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 jaws8, coupled with reduction of adjacent gill-arch structures9. 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 reefs10,11. This alternative prey transport mode is mechanically similar to the ratcheting mechanisms used in snakes12,13—a group of terrestrial vertebrates that share striking morphological, behavioural14 and ecological convergence with moray eels.

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Figure 1: Radiographs in left lateral view depicting the extreme positions of the pharyngeal jaws in M. retifera during prey transport.
Figure 2: The oral gape cycle in relation to the pharyngeal jaw cycle in M. retifera.
Figure 3: Detailed anatomy of the pharyngeal jaw apparatus in M. retifera.
Figure 4: Functional morphological model of pharyngeal jaw movement in M. retifera.

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Acknowledgements

We thank M. E. Alfaro, D. C. Collar, S. W. Day, H. W. Greene, N. J. Kley, A. H. Krakauer, R. D. Mehta, J. T. Redwine, A. Sinsheimer, T. W. Schoener and K. Vanderveen for comments on various drafts of this manuscript. We thank N. J. Kley for discussions regarding prey transport in vertebrates. H. Tran and L. B. Feng provided assistance with video collections. We are grateful to R. E. Pollard, C. Stafford, T. B. Waltzek and E. R. Wisner for help with radiographs and videofluoroscopy. P. Kysar provided technical assistance with scanning electron microscopy. We thank the California Academy of Sciences and the Harvard Museum of Comparative Zoology for specimen loans. Funding was provided by the American Association of University Women and by the National Science Foundation.

Author Contributions R.S.M. designed research, performed research and wrote the manuscript. P.C.W. helped design the study, contributed to the interpretation of anatomy and video, and participated in writing the manuscript.

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Correspondence to Rita S. Mehta.

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Supplementary information

Supplementary Video 1

This file contains Supplementary Video 1. This movie shows a portion of prey transport behaviour of the reticulated moray eel, Muraena retifera. Prey transport in lateral view reveals the upper pharyngeal jaw ensnaring a piece of squid prey apprehended by the oral jaws (MOV 6596 kb)

Supplementary Video 2

This file contains Supplementary Video 2 This movie shows a feeding sequence in lateral view of the reticulated moray eel, Muraena retifera. Morays apprehend prey by biting. During prey transport, the upper pharyngeal jaws ensnare squid prey. (MOV 5353 kb)

Supplementary Video 3

This file contains Supplementary Video 3. This movie shows the reticulated moray eel, Muraena retifera transporting a long piece of squid (5 cm). The feeding sequence is in lateral view and reveals how the reticulated moray can use multiple alternating movements of the oral and pharyngeal jaws to transport long prey. (MOV 54761 kb)

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Mehta, R., Wainwright, P. Raptorial jaws in the throat help moray eels swallow large prey. Nature 449, 79–82 (2007) doi:10.1038/nature06062

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