HISTOLOGICAL STRUCTURE OF THE OCCIPITAL-SYNARCUAL JOINT OF THE JUVENILE SILVER CHIMAERA CHIMAERA PHANTASMA (CHIMAERIDAE): HEMIDIARTHROSIS AS ADAPTATION TO HIGH-AMPLITUDE HEAD MOVEMENTS
- Authors: Romanov A.V.1,2, Shakhparonov V.V.1, Kapitanova D.V.2, Korzun L.P.1
-
Affiliations:
- Lomonosov Moscow State University
- Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences
- Issue: Vol 65, No 6 (2025)
- Pages: 647–662
- Section: Articles
- URL: https://ogarev-online.ru/0042-8752/article/view/374220
- DOI: https://doi.org/10.7868/S3034514625060015
- ID: 374220
Cite item
Abstract
Keywords
About the authors
A. V. Romanov
Lomonosov Moscow State University; Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences
Email: romanovav@my.msu.ru
Moscow, Russia; Moscow, Russia
V. V. Shakhparonov
Lomonosov Moscow State UniversityMoscow, Russia
D. V. Kapitanova
Severtsov Institute of Ecology and Evolution, Russian Academy of SciencesMoscow, Russia
L. P. Korzun
Lomonosov Moscow State UniversityMoscow, Russia
References
- Гуртовой Н.Н., Матвеев Б.С., Дзержинский Ф.Я. 1976. Практическая зоотомия позвоночных (низшие хордовые, бесчелюстные, рыбы). М.: Высш. шк., 351 с.
- Дзержинский Ф.Я. 1972. Биомеханический анализ челюстного аппарата птиц. М.: Изд-во МГУ, 155 с.
- Ромейс Б. 1954. Микроскопическая техника. М.: Изд-во иностр. лит-ры, 719 с.
- Синельников Р.Д., Синельников Я.Р. 1989. Атлас анатомии человека. Т. 1. Учение о костях, соединении костей и мышцах. М.: Медицина, 344 с.
- Хэм А., Кормак Д. 1983. Гистология. Т. 3. М.: Мир, 293 с.
- Alexander R.McN. 1970. Mechanics of the feeding action of various teleost fishes // J. Zool. V. 162. № 2. P. 145–156. https://doi.org/10.1111/j.1469-7998.1970.tb01261.x
- Archer C.W., Dowthwaite G.P., Francis‐West P. 2003. Development of synovial joints // Birth Defects Res. C. V. 69. № 2. P. 144–155. https://doi.org/10.1002/bdrc.10015
- Askary A., Smeeton J., Paul S. et al. 2016. Ancient origin of lubricated joints in bony vertebrates // eLife. V. 5. Article e16415. https://doi.org/10.7554/eLife.16415
- Bemis W.E. 1986. Feeding systems of living Dipnoi: anatomy and function // J. Morphol. V. 190. № S1. P. 249–275. https://doi.org/10.1002/jmor.1051900417
- Bemis W.E., Lauder G.V. 1986. Morphology and function of the feeding apparatus of the lungfish, Lepidosiren paradoxa (Dipnoi) // J. Morphol. V. 187. № 1. P. 81–108. https://doi.org/10.1002/jmor.1051870108
- Berio F., Broyon M., Enault S. et al. 2021. Diversity and evolution of mineralized skeletal tissues in chondrichthyans // Front. Ecol. Evol. V. 9. Article 660767. https://doi.org/10.3389/fevo.2021.660767
- Cameron H.U. 1974. The intervertebral joint of the longnose gar, Lepisosteus osseus // Can. J. Zool. V. 52. № 7. P. 803–804. https://doi.org/10.1139/z74-107
- Camp A.L. 2021. A neck-like vertebral motion in fish // P.R. Soc. B. V. 288. № 1957. Article 20211091. https://doi.org/10.1098/rspb.2021.1091
- Camp A.L., Brainerd E.L. 2014. Role of axial muscles in powering mouth expansion during suction feeding in largemouth bass (Micropterus salmoides) // J. Exp. Biol. V. 217. № 8. P. 1333–1345. https://doi.org/10.1242/jeb.095810
- Camp A.L., Roberts T.J., Brainerd E.L. 2015. Swimming muscles power suction feeding in largemouth bass // P. Natl. Acad. Sci. USA. V. 112. № 28. P. 8690–8695. https://doi.org/10.1073/pnas.1508055112
- Camp A.L., Roberts T.J., Brainerd E.L. 2018. Bluegill sunfish use high power outputs from axial muscles to generate powerful suction-feeding strikes // J. Exp. Biol. V. 221. № 11. Article jeb178160. https://doi.org/10.1242/jeb.178160
- Claeson K.M. 2011. The synarcual cartilage of batoids with emphasis on the synarcual of Rajidae // J. Morphol. V. 272. № 12. P. 1444–1463. https://doi.org/10.1002/jmor.10996
- Claeson K.M., Hilger A. 2011. Morphology of the anterior vertebral region in elasmobranchs: special focus, Squatiniformes // Foss. Rec. V. 14. № 2. P. 129–140. https://doi.org/10.1002/mmng.201100003
- Combes S.A., Daniel T.L. 2001. Shape, flapping and flexion: wing and fin design for forward flight // J. Exp. Biol. V. 204. № 12. P. 2073–2085. https://doi.org/10.1242/jeb.204.12.2073
- Davies D.V. 1948. The synovial joints of the skate (Raia) // J. Anat. V. 82. Pt. 1–2. P. 9–20.
- Dean B. 1906. Chimaeroid fishes and their development // Carnegie Inst. Wash. Publ. № 32. 194 p. https://doi.org/10.5962/bhl.title.29471
- Dean M.N., Summers A.P. 2006. Mineralized cartilage in the skeleton of chondrichthyan fishes // Zoology. V. 109. № 2. P. 164–168. https://doi.org/10.1016/j.zool.2006.03.002
- Didier D.A. 1995. Phylogenetic systematics of extant chimaeroid fishes (Holocephali, Chimaeroidei) // Am. Mus. Novit. № 3119. 86 p.
- Dowthwaite G.P., Flannery C.R., Flannelly J. et al. 2003. A mechanism underlying the movement requirement for synovial joint cavitation // Matrix Biol. V. 22. № 4. P. 311–322. https://doi.org/10.1016/S0945-053X(03)00037-4
- Dzerzhinsky F.Ya. 2017. The mystery of the two‐unit skull of the Sarcopterygii: a trap for functional morphologists // J. Zool. V. 301. № 2. P. 85–101. https://doi.org/10.1111/jzo.12405
- Gartner S.M., Whitlow K.R., Laurence-Chasen J.D. et al. 2022. Suction feeding of West African lungfish (Protopterus annectens): an XROMM analysis of jaw mechanics, cranial kinesis, and hyoid mobility // Biol. Open. V. 11. № 9. Article bio059447. https://doi.org/10.1242/bio.059447
- Grobecker D.B. 1983. The ‘lie-in-wait’ feeding mode of a cryptic teleost, Synanceia verrucosa // Predators and prey in fishes. Developments in environmental biology of fishes. V. 2. Dordrecht: Springer. P. 29–40. https://doi.org/10.1007/978-94-009-7296-4_5
- Haines R.W. 1942. Eudiarthrodial joints in fishes // J. Anat. V. 77. Pt. 1. P. 12–19.
- Huber D.R., Dean M.N., Summers A.P. 2008. Hard prey, soft jaws and the ontogeny of feeding mechanics in the spotted ratfish Hydrolagus colliei // J. R. Soc. Interface. V. 5. № 25. P. 941–953. https://doi.org/10.1098/rsif.2007.1325
- Inada T., Garrick J.A.F. 1979. Rhinochimaera pacifica, a long-snouted chimaera (Rhinochimaeridae), in New Zealand waters // Jpn. J. Ichthyol. V. 25. № 4. P. 235–243. https://doi.org/10.11369/jji1950.25.235
- Jimenez Y.E., Camp A.L., Grindall J.D., Brainerd E.L. 2018. Axial morphology and 3D neurocranial kinematics in suction-feeding fishes // Biol. Open. V. 7. № 9. Article bio036335. https://doi.org/10.1242/bio.036335
- Jollie M. 1962. Chordate morphology. N.Y.: Reinhold, 478 p. https://doi.org/10.5962/bhl.title.6408
- Kim M., Koyama E., Saunders C.N. et al. 2022. Synovial joint cavitation initiates with microcavities in interzone and is coupled to skeletal flexion and elongation in developing mouse embryo limbs // Biol. Open. V. 11. № 6. Article bio059381. https://doi.org/10.1242/bio.059381
- Kim S.-G., Ha J.-W., Park J.-C. 2004. Histological changes in the temporomandibular joint in rabbits depending on the extent of mandibular lengthening by osteodistraction // Brit. J. Oral Max. Surg. V. 42. № 6. P. 559–565. https://doi.org/10.1016/j.bjoms.2004.06.018
- Lauder G.V. Jr. 1979. Feeding mechanics in primitive teleosts and in the halecomorph fish Amia calva // J. Zool. Т. 187. № 4. С. 543–578. https://doi.org/10.1111/j.1469-7998.1979.tb03386.x
- Lauder G.V. Jr. 1980. Evolution of the feeding mechanism in primitive actinopterygian fishes: a functional anatomical analysis of Polypterus, Lepisosteus, and Amia // J. Morphol. V. 163. № 3. P. 283–317. https://doi.org/10.1002/jmor.1051630305
- Lauder G.V., Liem K.F. 1981. Prey capture by Luciocephalus pulcher: implications for models of jaw protrusion in teleost fishes // Environ. Biol. Fish. V. 6. № 3/4. P. 257–268. https://doi.org/10.1007/BF00005755
- Lemberg J.B., Shubin N.H., Westneat M.W. 2019. Feeding kinematics and morphology of the alligator gar (Atractosteus spatula, Lacépède, 1803) // J. Morphol. V. 280. № 10. P. 1548–1570. https://doi.org/10.1002/jmor.21048
- Lesiuk T.P., Lindsey C.C. 1978. Morphological peculiarities in the neck-bending Amazonian characoid fish Rhaphiodon vulpinus // Can. J. Zool. V. 56. № 4. P. 991–997. https://doi.org/10.1139/z78-139
- Lubosch W. 1909. Anpassungserscheinungen bei der Verkalkung des Selachierknorpels // Anat. Anzeiger. V. 35. № 1. P. 1–8.
- Motta P.J., Wilga C.D. 2001. Advances in the study of feeding behaviors, mechanisms, and mechanics of sharks // Environ. Biol. Fish. V. 60. № 1–3. P. 131–156. https://doi.org/10.1023/A:1007649900712
- Murray P.D.F., Drachm D.B. 1969. The role of movement in the development of joints and related structures: the head and neck in the chick embryo // Development. V. 22. № 3. P. 349–371. https://doi.org/10.1242/dev.22.3.349
- Nakaya K. 1995. Hydrodynamic function of the head in the hammerhead sharks (Elasmobranchii: Sphyrnidae) // Copeia. V. 1995. № 2. P. 330–336. https://doi.org/10.2307/1446895
- Newell G.E., Roper H.D.G. 1935. A note on the feeding habits of Chimaera monstrosa // J. Mar. Biol. Assoc. UK. V. 20. № 1. P. 99–102. https://doi.org/10.1017/S0025315400010080
- Osborne A.C., Lamb K.J., Lewthwaite J.C. et al. 2002. Short-term rigid and flaccid paralyses diminish growth of embryonic chick limbs and abrogate joint cavity formation but differentially preserve pre-cavitated joints // J. Musculoskelet. Neuronal Interact. V. 2. № 5. P. 448–456.
- Osse J.W.M. 1969. Functional morphology of the head of the perch (Perca fluviatilis L.): an electromyographic study // Neth. J. Zool. V. 19. № 3. P. 289–392. https://doi.org/10.1163/002829669X00134
- Oxford textbook of rheumatology. 2013. Oxford: Oxford Univ. Press., 1522 p. https://doi.org/10.1093/med/9780199642489.001.0001
- Pears J.B., Johanson Z., Trinajstic K. et al. 2020. Mineralization of the Callorhinchus vertebral column (Holocephali; Chondrichthyes) // Front. Genet. V. 11. Article 571694. https://doi.org/10.3389/fgene.2020.571694
- Persson M. 1983. The role of movements in the development of sutural and diarthrodial joints tested by long-term paralysis of chick embryos // J. Anat. V. 137. Pt 3. P. 591–599.
- Romanov A.V., Shakhparonov V.V., Gerasimov K.B., Korzun L.P. 2024. Occipital‐synarcual joint mobility in ratfishes (Chimaeridae) and its possible adaptive role // J. Morphol. V. 285. № 6. Article e21740. https://doi.org/10.1002/jmor.21740
- Rux D., Deckerb R.S., Koyamaa E., Pacifici M. 2019. Joints in the appendicular skeleton: developmental mechanisms and evolutionary influences // Curr. Top. Dev. Biol. V. 133. P. 119–151. https://doi.org/10.1016/bs.ctdb.2018.11.002
- Schnell N.K., Bernstein P., Maier W. 2008. The “pseudo‐craniovertebral articulation” in the deep‐sea fish Stomias boa (Teleostei: Stomiidae) // J. Morphol. V. 269. № 5. P. 513–521. https://doi.org/10.1002/jmor.10584
- Schnell N.K., Britz R., Johnson G.D. 2010. New insights into the complex structure and ontogeny of the occipito‐vertebral gap in barbeled dragonfishes (Stomiidae, Teleostei) // J. Morphol. V. 271. № 8. P. 1006–1022. https://doi.org/10.1002/jmor.10858
- Sharma N., Haridy Y., Shubin N. 2025. Synovial joints were present in the common ancestor of jawed fish but lacking in jawless fish // PLOS Biol. V. 23. № 2. Article e3002990. https://doi.org/10.1371/journal.pbio.3002990
- Smith M.D. 2011. The normal synovium // Open Rheumatol. J. V. 5. Suppl. 1: M2. P. 100–106. https://doi.org/10.2174/1874312901105010100
- Tchernavin V.V. 1948. On the mechanical working of the head of bony fishes // P. Zool. Soc. Lond. V. 118. № 1. P. 129–143. https://doi.org/10.1111/j.1096-3642.1948.tb00369.x
- Walker M.B., Kimmel C.B. 2007. A two-color acid-free cartilage and bone stain for zebrafish larvae // Biotech. Histochem. V. 82. № 1. P. 23–28. https://doi.org/10.1080/10520290701333558
- Westneat M.W., Olsen A.M. 2015. How fish power suction feeding // P. Natl. Acad. Sci. USA. V. 112. № 28. P. 8525–8526. https://doi.org/10.1073/pnas.1510522112
- Whitlow K.R., Ross C.F., Gidmark N.J. et al. 2022. Suction feeding biomechanics of Polypterus bichir: investigating linkage mechanisms and the contributions of cranial kinesis to oral cavity volume change // J. Exp. Biol. V. 225. № 3. Article jeb243283. https://doi.org/10.1242/jeb.243283
- Whyte J.R., González L., Cisneros A.I. et al. 2002. Fetal development of the human tympanic ossicular chain articulations // Cells Tiss. Organs. V. 171. № 4. P. 241–249. https://doi.org/10.1159/000063124
- Wilga C.D., Motta P.J., Sanford C.P. 2007. Evolution and ecology of feeding in elasmobranchs // Integr. Comp. Biol. V. 47. № 1. P. 55–69. https://doi.org/10.1093/icb/icm029
- Wilga C.D., Maia A., Nauwelaerts S., Lauder G.V. 2012. Prey handling using whole-body fluid dynamics in batoids // Zoology. V. 115. № 1. P. 47–57. https://doi.org/10.1016/j.zool.2011.09.002
- Wilga C., Dumont E., Ferry L. 2024. The effect of tessellation on stiffness in the hyoid arch of elasmobranchs // J. Morphol. V. 285. № 3. Article e21681. https://doi.org/10.1002/jmor.21681
- Wintrich T., Scaal M., Böhmer C. et al. 2020. Palaeontological evidence reveals convergent evolution of intervertebral joint types in amniotes // Sci. Rep. V. 10. № 1. Article 14106. https://doi.org/10.1038/s41598-020-70751-2
Supplementary files


