Precaudal Vertebrae in the Postcranial Region of Moray Eels Form Ventral Processes.

Publisher: Wiley Country of Publication: United States NLM ID: 0406125 Publication Model: Print Cited Medium: Internet ISSN: 1097-4687 (Electronic) Linking ISSN: 00222887 NLM ISO Abbreviation: J Morphol Subsets: MEDLINE

Publication: <2005- > : Hoboken, N.J. : Wiley
Original Publication: 1931- : Philadelphia, Pa. : Wistar Institute of Anatomy and Biology

Eels*/anatomy & histology ; Spine*/anatomy & histology; Animals ; Tomography, X-Ray Computed

Fish vertebrae are primarily morphologically classified into precaudal vertebrae jointed to the ribs and caudal vertebrae with hemal spines, through which the caudal artery and veins pass. Moray eels (family Muraenidae) capture prey by directly biting, combining oral and pharyngeal jaw. During feeding motions, they exhibit various head manipulations, such as neurocranial elevation, ventral flexion, and horizontal shaking, with their postcranial region acting like the neck of amniotes. However, the bone morphology supporting these movements remains unclear. In this study, the vertebral morphologies of the Kidako moray (Gymnothorax kidako), starry moray (Echidna nebulosa), pink-lipped moray (Echidna rhodochilus), tidepool snake moray (Uropterygius micropterus), and Seychelles moray (Anarchias seychellensis) were investigated using X-ray computed tomography. These five species exhibited longitudinal ventral processes in the second to approximately 12th precaudal vertebrae with canals for blood vessels, structurally similar to hemal spines. In addition, the morphology of the precaudal vertebrae in three Anguilliformes species closely related to moray eels and two Gasterosteiformes species, including a seahorse that flexes its head ventrally as a feeding motion, was compared with that of moray eels. However, no remarkable ventral processes were observed in their precaudal vertebrae in the postcranial region, suggesting that these structural features in the postcranial vertebrae were preserved in Muraenidae but not necessarily required for the fish to bend its head ventrally. Although the functional significance of the ventral process has yet to be determined, our findings highlight a novel aspect of fish vertebral morphology.
(© 2024 The Author(s). Journal of Morphology published by Wiley Periodicals LLC.)

Abrams, R. W., M. D. Abrams, and M. W. Schein. 1983. “Diurnal Observations on the Behavioral Ecology of Gymnothorax moringa (Cuvier) and Muraena miliaris (Kaup) on a Caribbean Coral Reef.” Coral Reefs 1, no. 3: 185–192. https://doi.org/10.1007/BF00571196.
Agur, A. M., and A. F. Dalley. 2009. Grant's Atlas of Anatomy. Lippincott Williams & Wilkins.
Ahlberg, P. E., J. A. Clack, and H. Blom. 2005. “The Axial Skeleton of the Devonian Tetrapod Ichthyostega.” Nature 437, no. 7055: 137–140. https://doi.org/10.1038/nature03893.
Bergert, B. A., and P. C. Wainwright. 1997. “Morphology and Kinematics of Prey Capture in the Syngnathid Fishes Hippocampus erectus and Syngnathus floridae.” Marine Biology 127, no. 4: 563–570. https://doi.org/10.1007/s002270050046.
Bird, N. C., and P. M. Mabee. 2003. “Developmental Morphology of the Axial Skeleton of the Zebrafish, Danio rerio (Ostariophysi: Cyprinidae).” Developmental Dynamics 228, no. 3: 337–357. https://doi.org/10.1002/dvdy.10387.
Bogduk, N., and S. Mercer. 2000. “Biomechanics of the Cervical Spine. I: Normal Kinematics.” Clinical Biomechanics 15, no. 9: 633–648. https://doi.org/10.1016/S0268-0033(00)00034-6.
Bruner, E., and V. Bartolino. 2008. “Morphological Variation in the Seahorse Vertebral System.” International Journal of Morphology 26, no. 2: 247–262. https://doi.org/10.4067/S0717-95022008000200002.
Burke, A. C., C. E. Nelson, B. A. Morgan, and C. Tabin. 1995. “Hox Genes and the Evolution of Vertebrate Axial Morphology.” Development 121, no. 2: 333–346. https://doi.org/10.1242/dev.121.2.333.
Busscher, I., J. J. W. Ploegmakers, G. J. Verkerke, and A. G. Veldhuizen. 2010. “Comparative Anatomical Dimensions of the Complete Human and Porcine Spine.” European Spine Journal 19, no. 7: 1104–1114. https://doi.org/10.1007/s00586-010-1326-9.
Camp, A., and E. Brainerd. 2013. “Role of Axial Muscles in Powering Mouth Expansion During Suction Feeding in Largemouth Bass.” Journal of Experimental Biology 217, no. pt. 8: 1333–1345. https://doi.org/10.1242/jeb.095810.
Camp, A. L. 2021. “A Neck‐Like Vertebral Motion in Fish.” Proceedings of the Royal Society B: Biological Sciences 288, no. 1957: 20211091. https://doi.org/10.1098/rspb.2021.1091.
Camp, A. L., T. J. Roberts, and E. L. Brainerd. 2015. “Swimming Muscles Power Suction Feeding in Largemouth Bass.” Proceedings of the National Academy of Sciences of Sciences of the United States of America 112, no. 28: 8690–8695. https://doi.org/10.1073/pnas.1508055112.
Carroll, A. M., and P. C. Wainwright. 2006. “Muscle Function and Power Output During Suction Feeding in Largemouth Bass, Micropterus salmoides.” Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 143, no. 3: 389–399. https://doi.org/10.1016/j.cbpa.2005.12.022.
Carroll, A. M., P. C. Wainwright, S. H. Huskey, D. C. Collar, and R. G. Turingan. 2004. “Morphology Predicts Suction Feeding Performance in Centrarchid Fishes.” Journal of Experimental Biology 207, no. pt. 22: 3873–3881. https://doi.org/10.1242/jeb.01227.
Clothier, C. R. 1950. A Key to Some Southern California Fishes Based on Vertebral Characters‐No. 79. Fish Bulletin. San Diego: US: Library–Scripps Digital Collection. https://escholarship.org/uc/item/0d16v6j8.
Cohn, M. J., and C. Tickle. 1999. “Developmental Basis of Limblessness and Axial Patterning in Snakes.” Nature 399, no. 6735: 474–479. https://doi.org/10.1038/20944.
Collar, D. C., J. S. Reece, M. E. Alfaro, P. C. Wainwright, and R. S. Mehta. 2014. “Imperfect Morphological Convergence: Variable Changes in Cranial Structures Underlie Transitions to Durophagy in Moray Eels.” American Naturalist 183, no. 6: E168–E184. https://doi.org/10.1086/675810.
Collar, D. C., P. C. Wainwright, M. E. Alfaro, L. J. Revell, and R. S. Mehta. 2014. “Biting Disrupts Integration to Spur Skull Evolution in Eels.” Nature Communications 5: 5505. https://doi.org/10.1038/ncomms6505.
Coughlin, D. J., and A. M. Carroll. 2006. “In Vitro Estimates of Power Output by Epaxial Muscle During Feeding in Largemouth Bass.” Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 145, no. 4: 533–539. https://doi.org/10.1016/j.cbpa.2006.08.026.
Dierickx, K., W. Wouters, and W. Van Neer. 2017. “Comparative Osteological Study of Three Species of Distinct Genera of Haplotilapiini (Cichlidae).” Cybium 41, no. 3: 223–235. https://www.researchgate.net/publication/319458490_Comparative_osteological_study_of_three_species_of_distinct_genera_of_Haplotilapiini_Cichlidae#fullTextFileContent.
Eagderi, S. 2010. “Structural Diversity in the Cranial Musculoskeletal System in Anguilliformes: An Evolutionary‐Morphological Study.” Ghent University, Ghent, Belgium. http://www.evomorph.ugent.be/Publications/Eagderi%202010%20Text.pdf.
Espíndola, V. C., G. D. Johnson, and M. C. C. De Pinna. 2023. “Facial and Opercular Muscles in the Anguilliformes (Elopomorpha: Teleostei): Comparative Anatomy and Phylogenetic Implications for the Basal Position of Protanguilla.” Journal of Morphology 284, no. 3: e21556. https://doi.org/10.1002/jmor.21556.
Ferry‐Graham, L. A., and G. V. Lauder. 2001. “Aquatic Prey Capture in Ray‐Finned Fishes: A Century of Progress and New Directions.” Journal of Morphology 248, no. 2: 99–119. https://doi.org/10.1002/jmor.1023.
Fielitz, C. 2002. “Previously Unreported Pectoral Bones in Moray Eels (Anguilliformes: Muraenidae).” Copeia 2002, no. 2: 483–488. http://www.jstor.org/stable/1448067.
Fjelldal, P. G., G. K. Totland, T. Hansen, et al. 2013. “Regional Changes in Vertebra Morphology During Ontogeny Reflect the Life History of Atlantic Cod (Gadus morhua L.).” Journal of Anatomy 222, no. 6: 615–624. https://doi.org/10.1111/joa.12049.
Ford, E. 1937. “Vertebral Variation in Teleostean Fishes.” Journal of the Marine Biological Association of the United Kingdom 22, no. 1: 1–60. https://doi.org/10.1017/S0025315400011863.
Franklin, C. E., and I. A. Johnston. 1997. “Muscle Power Output During Escape Responses in an Antarctic Fish.” Journal of Experimental Biology 200, no. pt. 4: 703–712. https://doi.org/10.1242/jeb.200.4.703.
Fricke, R., W. N. Eschmeyer, and R. Van Der Laan. 2024. “Eschmeyers's Catalog of Fishes: Genera/Species by Family/Subfamily.” Version (2 April 2024). http://researcharchive.calacademy.org/research/ichthyology/catalog/fishcatmain.asp.
Galbusera, F. 2018. “The Spine: Its Evolution, Function, and Shape.” In Biomechanics of the Spine, edited by F. Galbusera and H.‐J. Wilke, 3–9. Academic Press. https://doi.org/10.1016/C2016-0-04439-X.
Galbusera, F., and T. Bassani. 2019. “The Spine: A Strong, Stable, and Flexible Structure With Biomimetics Potential.” Biomimetics 4, no. 3: 60. https://doi.org/10.3390/biomimetics4030060.
Grande, L., and W. E. Bemis. 1998. “A Comprehensive Phylogenetic Study of Amiid Fishes (Amiidae) Based on Comparative Skeletal Anatomy. An Empirical Search for Interconnected Patterns of Natural History.” Supplement, Journal of Vertebrate Paleontology 18, no. S1: 1–696. https://doi.org/10.1080/02724634.1998.10011114.
Gudo, M., and D. G. Homberger. 2002. “The Functional Morphology of the Pectoral Fin Girdle of the Spiny Dogfish (Squalus acanthias): Implications for the Evolutionary History of the Pectoral Girdle of Vertebrates.” Senckenbergiana Lethaea 82, no. 1: 241–252. https://doi.org/10.1007/BF03043787.
Hirasawa, T., S. Fujimoto, and S. Kuratani. 2016. “Expansion of the Neck Reconstituted the Shoulder‐Diaphragm in Amniote Evolution.” Development, Growth & Differentiation 58, no. 1: 143–153. https://doi.org/10.1111/dgd.12243.
Jimenez, Y. E., and E. L. Brainerd. 2020. “Dual Function of Epaxial Musculature for Swimming and Suction Feeding in Largemouth Bass.” Proceedings of the Royal Society B: Biological Sciences 287, no. 1919: 20192631. https://doi.org/10.1098/rspb.2019.2631.
Johnson, G. D. 2019. “Revisions of Anatomical Descriptions of the Pharyngeal Jaw Apparatus in Moray Eels of the Family Muraenidae (Teleostei: Anguilliformes).” Copeia 107, no. 2: 341–357. https://doi.org/10.1643/CI-19-211.
Kambic, R. E., A. A. Biewener, and S. E. Pierce. 2017. “Experimental Determination of Three‐Dimensional Cervical Joint Mobility in the Avian Neck.” Frontiers in Zoology 14: 37. https://doi.org/10.1186/s12983-017-0223-z.
Kardong, K. V. 2019. Vertebrates: Comparative Anatomy, Function, Evolution. 8th ed. New York: McGraw‐Hill Education.
Kley, N. J., and E. L. Brainerd. 2002. “Post‐Cranial Prey Transport Mechanisms in the Black Pinesnake, Pituophis melanoleucus Lodingi: An X‐Ray Videographic Study.” Zoology 105, no. 2: 153–164. https://doi.org/10.1078/0944-2006-00056.
Lauder, G. V. 1985. “Chapter 12. Aquatic Feeding in Lower Vertebrates.” In Functional Vertebrate Morphology, edited by H. Milton, M. B. Dennis, F. L. Karel, and B. W. David, 210–229. Cambridge, MA, London: Harvard University Press. https://doi.org/10.4159/harvard.9780674184404.c12.
Liem, K. F. 1978. “Modulatory Multiplicity in the Functional Repertoire of the Feeding Mechanism in Cichlid Fishes. I. Piscivores.” Journal of Morphology 158, no. 3: 323–360. https://doi.org/10.1002/jmor.1051580305.
Makushok, V. M. 1958. “The Morphology and Classification of the Northern Blennioid Fishes (Stichaeoidae, Blennioidei, Pisces).” Trudy Zoologicheskogo Instituta AN SSSR 25: 3–129. https://cir.nii.ac.jp/crid/1572543024342651648.
Matsui, I., and T. Takai. 1959. “Osteology of the Japanese Eel, Anguilla japonica TEMMINCK et SCHLEGEL.” Journal of National Fisheries University 8, no. 2: 173–182. https://www2.fish-u.ac.jp/kenkyu/sangakukou/kenkyuhoukoku/08/08-2-7.pdf.
Mehta, R. S. 2009. “Ecomorphology of the Moray Bite: Relationship Between Dietary Extremes and Morphological Diversity.” Physiological and Biochemical Zoology 82, no. 1: 90–103. https://doi.org/10.1086/594381.
Mehta, R. S., and K. R. Donohoe. 2021. “Snowflake Morays, Echidna nebulosa, Exhibit Similar Feeding Kinematics in Terrestrial and Aquatic Treatments.” Journal of Experimental Biology 224, no. 11. https://doi.org/10.1242/jeb.234047.
Mehta, R. S., and P. C. Wainwright. 2007a. “Biting Releases Constraints on Moray Eel Feeding Kinematics.” Journal of Experimental Biology 210, no. Pt 3: 495–504. https://doi.org/10.1242/jeb.02663.
Mehta, R. S., and P. C. Wainwright. 2007b. “Raptorial Jaws in the Throat Help Moray Eels Swallow Large Prey.” Nature 449, no. 7158: 79–82. https://doi.org/10.1038/nature06062.
Mehta, R. S., and P. C. Wainwright. 2008. “Functional Morphology of the Pharyngeal Jaw Apparatus in Moray Eels.” Journal of Morphology 269, no. 5: 604–619. https://doi.org/10.1002/jmor.10612.
Miller, T. J. 1989. “Feeding Behavior of Echidna nebulosa, Enchelycore pardalis, and Gymnomuraena zebra (Teleostei: Muraenidae).” Copeia 1989, no. 3: 662–672. https://doi.org/10.2307/1445493.
Moretto, W. I., A. K. Stahl, and R. S. Mehta. 2022. “Effects of Acute Temperature Change on California Moray Prey Manipulation and Transport Behavior.” Zoology 154: 126030. https://doi.org/10.1016/j.zool.2022.126030.
Morin‐Kensicki, E. M., E. Melancon, and J. S. Eisen. 2002. “Segmental Relationship Between Somites and Vertebral Column in Zebrafish.” Development 129, no. 16: 3851–3860. https://doi.org/10.1242/dev.129.16.3851.
Nelson, G. J. 1967. “Branchial Muscles in Representatives of Five Eel Families.” Pacific Science 21: 348–363. https://core.ac.uk/download/pdf/5097083.pdf.
Nelson, J. S., T. C. Grande, and M. V. H. Wilson. 2016. Fishes of the World. 5th ed. Wiley. https://books.google.co.jp/books?id=Yqw7CwAAQBAJ.
Nowroozi, B. N., C. J. Harper, B. De Kegel, D. Adriaens, and E. L. Brainerd. 2012. “Regional Variation in Morphology of Vertebral Centra and Intervertebral Joints in Striped Bass, Morone saxatilis.” Journal of Morphology 273, no. 4: 441–452. https://doi.org/10.1002/jmor.11034.
Patterson, C., and G. D. Johnson. 1995. “The Intermuscular Bones and Ligaments of Teleostean Fishes.” Smithsonian Contributions to Zoology no. 559: 1–83. https://doi.org/10.5479/si.00810282.559.
Prince, V. E., L. Joly, M. Ekker, and R. K. Ho. 1998. “Zebrafish Hox Genes: Genomic Organization and Modified Colinear Expression Patterns in the Trunk.” Development 125, no. 3: 407–420. https://doi.org/10.1242/dev.125.3.407.
Rockwell, H., F. G. Evans, and H. C. Pheasant. 1938. “The Comparative Morphology of the Vertebrate Spinal Column. Its Form as Related to Function.” Journal of Morphology 63, no. 1: 87–117. https://doi.org/10.1002/jmor.1050630105.
Sakashita, M., S. Yamasaki, K. Yaji, A. Kawamoto, and S. Kondo. 2021. “Three‐Dimensional Topology Optimization Model to Simulate the External Shapes of Bone.” PLoS Computational Biology 17, no. 6: e1009043. https://doi.org/10.1371/journal.pcbi.1009043.
Schnell, N. K., and G. D. Johnson. 2017. “Evolution of a Functional Head Joint in Deep‐Sea Fishes (Stomiidae).” PLoS One 12, no. 2: e0170224. https://doi.org/10.1371/journal.pone.0170224.
Shubin, N., E. B. Daeschler, and F. A. Jenkins. 2015. “4 Origin of the Tetrapod Neck and Shoulder.” In Great Transformations in Vertebrate Evolution, edited by P. D. Kenneth, S. Neil, and L. B. Elizabeth, 63–76. Chicago: University of Chicago Press. https://doi.org/10.7208/9780226268392-005.
Smith, D. G., S. V. Bogorodsky, A. O. Mal, and T. J. Alpermann. 2019. “Review of the Moray Eels (Anguilliformes: Muraenidae) of the Red Sea, With Description of a New Species.” Zootaxa 4704, no. 1: 1–87. https://doi.org/10.11646/zootaxa.4704.1.1.
Song, J., and L. R. Parenti. 1995. “Clearing and Staining Whole Fish Specimens for Simultaneous Demonstration of Bone, Cartilage, and Nerves.” Copeia 1995, no. 1: 114–118. https://doi.org/10.2307/1446805.
Suniaga, S., T. Rolvien, A. Vom Scheidt, et al. 2018. “Increased Mechanical Loading Through Controlled Swimming Exercise Induces Bone Formation and Mineralization in Adult Zebrafish.” Scientific Reports 8, no. 1: 3646. https://doi.org/10.1038/s41598-018-21776-1.
Sweetser, P. W., and E. J. Hilton. 2016. “Osteology of the Crescent Gunnel Pholis laeta and the Phylogeny of the Family Pholidae (Cottiformes, Zoarcoidei).” Journal of Fish Biology 89, no. 3: 1666–1691. https://doi.org/10.1111/jfb.13084.
Ward, A. B., and E. L. Brainerd. 2007. “Evolution of Axial Patterning in Elongate Fishes.” Biological Journal of the Linnean Society 90, no. 1: 97–116. https://doi.org/10.1111/j.1095-8312.2007.00714.x.
Ward, A. B., and R. S. Mehta. 2014. “Differential Occupation of Axial Morphospace.” Zoology 117, no. 1: 70–76. https://doi.org/10.1016/j.zool.2013.10.006.
Woltering, J. M., F. J. Vonk, H. Müller, et al. 2009. “Axial Patterning in Snakes and Caecilians: Evidence for an Alternative Interpretation of the Hox Code.” Developmental Biology 332, no. 1: 82–89. https://doi.org/10.1016/j.ydbio.2009.04.031.
Zsoldos, R. R., and T. F. Licka. 2015. “The Equine Neck and Its Function During Movement and Locomotion.” Zoology 118, no. 5: 364–376. https://doi.org/10.1016/j.zool.2015.03.005.

Research Project Grant R05B016 from Kawasaki Medical School; Faculty research expenses from Kawasaki Medical School; JSPS KAKENHI Grant Number JP22K15155

Keywords: Anguilliformes; bone morphometry; cervical vertebrae; neck; pectoral girdle

Date Created: 20240916 Date Completed: 20240916 Latest Revision: 20240916

20240916

10.1002/jmor.21776

39279215