HISTOLOGICAL STRUCTURE OF THE OCCIPITAL-SYNARCUAL JOINT OF THE JUVENILE SILVER CHIMAERA CHIMAERA PHANTASMA (CHIMAERIDAE): HEMIDIARTHROSIS AS ADAPTATION TO HIGH-AMPLITUDE HEAD MOVEMENTS

Cover Page

Cite item

Full Text

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription Access

Abstract

The results of a histological study of intersegmental joints of the spine are presented for the juvenile silver chimaera Chimaera phantasma. Its occipital-synarcual joint and the joints of the articular processes have a large cavity. The fibrous tissue surrounding the latter connects the articular surfaces, which are thus not totally separated by a cavity. We interpret both joints as hemidiarthroses. There are layers of dense fibrous connective tissue (synarthroses) between the elements of the vertebral arches. The boundaries between the segments in the synarcual are determined only by the spinal nerves. Mineralized cartilage is found only in the synarcual. Our data clearly indicate specialization of the occipital-synarcual joint, since this is the only diarthrosis in the chimaera's spine. Further studies are needed to understand the mechanisms of joint development; however, the cavity itself may indicate adaptation to an extended range of motion in the joint. Early mineralization of the synarcual may testify on the joint load during compression. Clarification of the biological role of this articulation requires observations of the animal in nature. Taking into account both literary sources and the data of present study, we assume that the mobility of the chimaera head is important for tearing off food objects attached to the substrate.

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 University

Moscow, Russia

D. V. Kapitanova

Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences

Moscow, Russia

L. P. Korzun

Lomonosov Moscow State University

Moscow, Russia

References

  1. Гуртовой Н.Н., Матвеев Б.С., Дзержинский Ф.Я. 1976. Практическая зоотомия позвоночных (низшие хордовые, бесчелюстные, рыбы). М.: Высш. шк., 351 с.
  2. Дзержинский Ф.Я. 1972. Биомеханический анализ челюстного аппарата птиц. М.: Изд-во МГУ, 155 с.
  3. Ромейс Б. 1954. Микроскопическая техника. М.: Изд-во иностр. лит-ры, 719 с.
  4. Синельников Р.Д., Синельников Я.Р. 1989. Атлас анатомии человека. Т. 1. Учение о костях, соединении костей и мышцах. М.: Медицина, 344 с.
  5. Хэм А., Кормак Д. 1983. Гистология. Т. 3. М.: Мир, 293 с.
  6. 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
  7. 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
  8. 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
  9. 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
  10. 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
  11. 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
  12. 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
  13. 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
  14. 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
  15. 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
  16. 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
  17. 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
  18. 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
  19. 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
  20. Davies D.V. 1948. The synovial joints of the skate (Raia) // J. Anat. V. 82. Pt. 1–2. P. 9–20.
  21. Dean B. 1906. Chimaeroid fishes and their development // Carnegie Inst. Wash. Publ. № 32. 194 p. https://doi.org/10.5962/bhl.title.29471
  22. 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
  23. Didier D.A. 1995. Phylogenetic systematics of extant chimaeroid fishes (Holocephali, Chimaeroidei) // Am. Mus. Novit. № 3119. 86 p.
  24. 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
  25. 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
  26. 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
  27. 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
  28. Haines R.W. 1942. Eudiarthrodial joints in fishes // J. Anat. V. 77. Pt. 1. P. 12–19.
  29. 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
  30. 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
  31. 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
  32. Jollie M. 1962. Chordate morphology. N.Y.: Reinhold, 478 p. https://doi.org/10.5962/bhl.title.6408
  33. 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
  34. 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
  35. 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
  36. 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
  37. 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
  38. 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
  39. 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
  40. Lubosch W. 1909. Anpassungserscheinungen bei der Verkalkung des Selachierknorpels // Anat. Anzeiger. V. 35. № 1. P. 1–8.
  41. 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
  42. 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
  43. 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
  44. 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
  45. 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.
  46. 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
  47. Oxford textbook of rheumatology. 2013. Oxford: Oxford Univ. Press., 1522 p. https://doi.org/10.1093/med/9780199642489.001.0001
  48. 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
  49. 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.
  50. 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
  51. 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
  52. 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
  53. 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
  54. 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
  55. Smith M.D. 2011. The normal synovium // Open Rheumatol. J. V. 5. Suppl. 1: M2. P. 100–106. https://doi.org/10.2174/1874312901105010100
  56. 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
  57. 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
  58. 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
  59. 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
  60. 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
  61. 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
  62. 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
  63. 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
  64. 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

Supplementary Files
Action
1. JATS XML

Copyright (c) 2025 Russian Academy of Sciences

Согласие на обработку персональных данных

 

Используя сайт https://journals.rcsi.science, я (далее – «Пользователь» или «Субъект персональных данных») даю согласие на обработку персональных данных на этом сайте (текст Согласия) и на обработку персональных данных с помощью сервиса «Яндекс.Метрика» (текст Согласия).