Биология моря, 2023, T. 49, № 3, стр. 149-165

Объединение мускулов челюстного аппарата некоторых видов костистых рыб (Teleostei): cтроение и функционирование

Е. С. Громова 1*, В. В. Махотин 1

1 Московский государственный университет (МГУ)
119991 Москва, Россия

* E-mail: zhenya_s@inbox.ru

Поступила в редакцию 06.10.2022
После доработки 10.12.2022
Принята к публикации 26.01.2023

Аннотация

Поперечнополосатые мышцы Teleostei иногда объединяются в сложные “надмускульные” комплексы. При этом отдельные мускулы у рыб соединяются между собой параллельно и/или последовательно. Группа параллельно расположенных мускулов объединяет свои силы для осуществления единого мощного функционального акта. Последовательно расположенные мускулы соединяются между собой, получая тем самым увеличенную амплитуду и скорость совершаемых движений. Для описываемых “надмускульных” комплексов предложен термин “сверхмускул”. В работе приведен обзор особенностей строения и функционирования сверхмускулов головы костистых рыб с параллельным и последовательным устройством. Обсуждается разнообразие причин формирования мышечных комплексов для разных таксонов Teleostei.

Ключевые слова: костистые рыбы Teleostei, функциональная морфология, челюстной аппарат, питание, объединение мышц, сверхмускулы

Список литературы

  1. Громова Е.С., Махотин В.В. Функциональная морфология висцерального аппарата семги Salmo salar // Вопр. ихтиол. 2016. Т. 56. № 4. С. 410–426.

  2. Громова Е.С., Махотин В.В. Морфофункциональные особенности висцерального аппарата рубиново-пепельной рыбы-попугая Scarus rubroviolaceus (Scaridae) // Вопр. ихтиол. 2020. Т. 60. № 2. С. 137–164.

  3. Громова Е.С., Дзержинский Ф.Я., Махотин В.В. Морфофункциональные особенности висцерального аппарата серебряной араваны Osteoglossum bicirrhosum // Вопр. ихтиол. 2017. Т. 57. № 4. С. 379–392.

  4. Иорданский Н.Н. Эволюция комплексных адаптаций. Челюстной аппарат амфибий и рептилий. М.: Наука. 1990. 310 с.

  5. Кэрролл Р. Палеонтология и эволюция позвоночных. М.: Мир. 1992. Т. 1. 280 с.

  6. Махотин В.В., Громова Е.С. Детали строения скелета, мышц и соединительнотканных элементов головы белого толстолобика Hypophthalmichthys molitrix (Cyprinidae) в связи с особенностями функционирования его висцерального аппарата // Вопр. ихтиол. 2019. Т. 59. № 1. С. 3–27.

  7. Ромейс Б. Микроскопическая техника // М.: Изд. иностранной литературы. 1953. 719 с.

  8. Aerts P. Variability of the fast suction feeding process in Astatotilapia elegans (Teleostei: Cichlidae): a hypothesis of peripheral feedback control // J. Zool. 2009. V. 220. № 4. P. 653–678. https://doi.org/10.1111/j.1469-7998.1990.tb04741.x

  9. Alexander R.McN. The functions and the mechanisms of the protrusible upper jaws of some acanthopterygian fish // J. Zool. 1967a. V. 151. P. 43–64.

  10. Alexander R.McN. Mechanisms of the jaws of some atheri-niform fish // J. Zool. 1967b. V. 151. № 2. P. 233–255.

  11. Boyle K.S., Tricas T.C. Sound production in the longnose butterflyfishes (genus Forcipiger): cranial kinematics, muscle activity and honest signals // J. Exp. Biol. 2011.V. 214. № 22. P. 3829–3842. https://doi.org/10.1242/jeb.062554

  12. Brocklehurst R., Porro L., Herrel A. et al. A digital dissection of two teleost fishes: comparative functional anatomy of the cranial musculoskeletal system in pike (Esox lucius) and eel (Anguilla anguilla) // J. Anat. 2019. V. 235. P. 189–204.

  13. Bruch K. Die Wirbelteorie des Schadels, am Skelette des Lachsesgepruft // Aus den Abhandlungen der Senckenbergischen naturforschenden Gesellschaft. 1862. V. 4. Frankfurt am Main: V. Kramer. P. 1–58.

  14. Bruggemann J.H., Kuyper M.W.M., Breeman A.M. Comparative analysis of foraging and habitat use by the sympatric Caribbean parrotfish Scarus vetula and Sparisoma viride (Scaridae) // Mar. Ecol. Prog. Ser. 1994. V. 12. P. 51–66.

  15. Camp A.L., Konow N., Sanford C.P.J. Functional morpho-logy and biomechanics of the tongue bite apparatus in salmonid and osteoglossomorph fishes // J. Anatomy. 2009. V. 214. № 5. P. 717–728.

  16. Cohen K.E., Lucanus O., Summers A.P., Kolmann M.A. Lip service: Histological phenotypes correlate with diet and feeding ecology in herbivorous pacus // Anat. Rec. 2023. V. 306. № 2. P. 326–342. https://doi.org/10.1002/ar.25075

  17. Datovo A., Vari R.P. The jaw adductor muscle complex in teleostean fishes: evolution, homologies and revised nomenclature (Osteichthyes: Actinopterygii) // PloS One. 2013. V. 8. № 4. P. 1–23.

  18. Datovo A., Vari R.P. The adductor mandibulae muscle complex in lower teleostean fishes (Osteichthyes: Actinopterygii): comparative anatomy, synonymy, and phylogenetic implications // J. Linn. Soc. London, Zool. 2014. V. 171. P. 554–622.

  19. De Schepper N., Adriaens D., De Kegel B. Moringua edwardsi (Moringuidae: Anguilliformes): cranial specialization for head-first burrowing? // J. Morphol. 2005. V. 266. № 3. P. 356–368.

  20. De Schepper N., De Kegel B., Adriaens D. Pisodonophis boro (Ophichthidae: Anguilliformes): specialization for headfirst and tail-first burrowing? // J. Morphol. 2007. V. 268. № 2. P. 112–126.

  21. De Schepper N., Wassenbergh S.V., Adriaens D. Morphology of the jaw system in trichiurids: trade-offs between mouth closing and biting performance // J. Linn. Soc. London, Zool. 2008. V. 152. № 4. P. 717–736.

  22. Deprá G.C. Relações filogenéticas em Geophagini (Acanthopterygii, Cichlidae), utilizando caracteres miológicos. Tese (doutorado em Ecologia de Ambientes Aquáticos Continentais).Universidade Estadual de Maringá. 2019. 234 p.

  23. Dial T.R., Hernandez L.P., Brainerd E.L. Morphological and functional maturity of the oral jaws covary with offspring size in Trinidadian guppies // Sci. Rep. 2017. V. 7. № 1. P. 1–10, 5771.

  24. Drucker E.G., Jensen J.S. Functional analysis of a specia-lized prey processing behavior: winnowing by surfper-ches (Teleostei: Embiotocidae) // J. Morphol. 1991. V. 210. № 3. P. 267–287.

  25. Dutra G.M., Peixoto L.A.W., Abrahao V.P. et al. Morphology-based phylogeny of Eigenmanniinae Mago-Leccia, 1978 (Teleostei: Gymnotiformes: Sternopygidae), with a new classification // J. Zool. Syst. Res. 2021. P. 1–50. https://doi.org/10.1111/jzs.12535

  26. Eagderi S. Structural diversity in the cranial musculoskeletal system in Anguilliformes: an evolutionary-morphological study // Cand. Sci. (Biol.) Dissertation. Gent (Belgium): Universiteit Gent. 2010. P. 1–157.

  27. Eagderi S., Adriaens D. Cephalic morphology of Pythonichthys macrurus (Heterenchelyidae: Anguilliformes): specializations for head-first burrowing // J. Morphol. 2010. V. 271. P. 1053–1065.

  28. Eagderi S., Christiaens J., Boone M. et al. Functional morphology of the feeding apparatus in Simenchelys parasitica (Simenchelyinae: Synaphobranchidae), an alleged parasitic eel // Copeia. 2016. V. 104. № 2. P. 421–439.

  29. Elshoud-Oldenhave M. Prey-capture in the pikeperch Stizostedion lucioperca (Linnaeus, 1758) (Teleostei, Percidae): A structural and functional analysis // Zoomorphologie. 1979. V. 93. P. 1–32.

  30. Elshoud-Oldenhave M.J.W., Osse J.W.M. Functional morphology of the feeding system in the ruff – Gymnocephalus cernua (L. 1758) (Teleostei, Percidae) // J. Morph. 1976. V. 150. № 2. P. 399–422. https://doi.org/10.1002/jmor.1051500210

  31. Farina S.C., Bemis W.E. Functional morphology of gill ventilation of the goosefish, Lophius americanus (Lophiiformes: Lophiidae) // Zoology. 2016. V. 119. P. 207–215.

  32. Field J.G. Contributions to the functional morphology of fishes. Part II. The feeding mechanism of the angler-fish, Lophius piscatorius Linnaeus // Zool. Afr. 1966. V. 2. № 1. P. 45–67.

  33. Figueiredo F.J., Gallo V., Santos H.R.S. A new appraisal of the suspensorium of albulid fishes // Arq. Mus. Nac. Rio de Janeiro. 2002. V. 60. № 3. P. 127–130.

  34. Fink W.L. Phylogenetic interrelationships of the stomiid fishes (Teleostei: Stomiiformes) // Misc. Publ. - Mus. Zool. Univ. Michigan. 1985. № 171. P. 1–127.

  35. Fink W.L., Weitzman S.H. Relationships of the stomiiform fishes (Teleostei), with a description of Diplophos // Bull. Mus. Comp. Zool. 1982. V. 150. № 2. P. 31–93.

  36. Finley N.L. Jaw-dropping sculpins: comparative functional morphology and evolution of the cottoid feeding apparatus. Honors Theses, Whitman College. 2017. 29 p.

  37. Ghasemzadeh J. Musculoskeletal anatomy of the flathead grey mullet Mugil cephalus // Biology, Ecology and Culture of Grey Mullet (Mugilidae). Florida: CRC Press. 2016. P. 128–164.

  38. Greene C.W., Greene C.H. The skeletal musculature of the king salmon // Bull. US Bureau Fish. 1913. V. 33. P. 21–60.

  39. Grubich J.R. Prey capture in Actinopterygian fishes: a review of suction feeding motor patterns with new evidence from an elopomorph fish, Megalops atlanticus // Amer. Zool. 2001. V. 41. P. 1258–1265.

  40. Hilton E.J. Comparative osteology and phylogenetic systematics of fossil and living bony-tongue fishes (Actinopterygii, Teleostei; Osteoglossomorpha) // J. Linn. Soc. London, Zool. 2003.V. 137. P. 1−100.

  41. Howard K.G., Claisse J.T., Clark T.B. et al. Home range and movement patterns of the redlip parrotfish (Scarus rubroviolaceus) in Hawaii // Mar. Biol. 2013. V. 160. № 7. P. 1583–1595. https://doi.org/10.1007/s00227-013-2211-y

  42. Howes G.J. The cranial musculature and taxonomy of characoid fishes of the tribes Cynodontini and Chara-cini // Bull. Br. Mus. Nat. Hist. Zool. 1976. V. 29. № 4. P. 203–248.

  43. Howes G.J. Cranial muscles of gonorynchiform fishes, with comments on generic relationships // Bull. Br. Mus. Nat. Hist. Zool. 1985. V. 49. № 2. P. 273–303.

  44. Huby A., Lowie A., Herrel A. et al. Functional diversity in biters: the evolutionary morphology of the oral jaw system in pacus, piranhas and relatives (Teleostei: Serrasalmidae) // Biol. J. Linn. Soc. 2019. V. 127. № 4. P. 722–741.

  45. Huby A., Parmentier E. Actinopterygians: head, jaws and muscles // Heads, jaws and muscles. Fascinating Life Sciences. Springer, Cham. 2019. P. 93–117.

  46. Humphrey D.R., Reed D.J. Separate cortical systems for control of joint movement and joint stiffness: reciprocal activation and coactivation of antagonist muscles // Adv. Neurol. 1983. V. 39. P. 347–372.

  47. Johnson G.D. Revisions of anatomical descriptions of the pharyngeal jaw apparatus in moray eels of the family Muraenidae (Teleostei: Anguilliformes) // Copeia. 2019. V. 107. № 2. P. 341–357. https://doi.org/10.1643/CI-19-211

  48. Johnson G.D., Patterson C. Relationships of Lower Euteleostean Fishes / Interrelationships of Fishes. Eds M.L.J. Stiassny, L.R. Parenti, G.D. Johnson. New York: Acad. Press. 1996. P. 251−332.

  49. Kenaley C.P. Exploring feeding behaviour in deep-sea dra-gonfishes (Teleostei: Stomiidae): jaw biomechanics and functional significance of a loosejaw // Biol. J. Linn. Soc. 2012. V. 106. № 1. P. 224–240.

  50. Konow N., Sanford C.P.J. Biomechanics of a convergently derived prey-processing mechanism in fishes: evidence from comparative tongue-bite apparatus morphology and raking kinematics // J. Exp. Biol. 2008a. V. 211. P. 3378–3391.

  51. Konow N., Sandford C.P.J. Is a congruently derived muscle-activity pattern driving novel raking behaviours in teleost fishes? // J. Exp. Biol. 2008b. V. 211. P. 989–999. https://doi.org/10.1242/jeb.013078

  52. Konow N., Bellwood D.R., Wainwright P.C., Kerr A.M. Evolution of novel jaw joints promote trophic diversity in coral reef fishes // Biol. J. Linn. Soc. 2008. V. 93. P. 545–555.

  53. Konow N., Krijestorac B., Sanford C.P.J. et al. Prey proces-sing in the Siamese fighting fish (Betta splendens) // J. Comp. Physiol. 2013. V. 199. P. 641–651. https://doi.org/10.1007/s00359-013-0819-5

  54. Lauder G.V. Evolution of the feeding mechanism in primitive actinopterygian fishes: a functional anatomical analysis of Polypterus, Lepisosteus and Amia // J. Morph. 1980a. V. 163. № 3. P. 283–317.

  55. Lauder G.V. The suction feeding mechanism in sunfishes (Lepomis): an experimental analysis // J. Exp. Biol. 1980b. V. 88. № 1. P. 49–72.

  56. Lauder G.V. Intraspecific functional repertoires in the fee-ding mechanism of the characoid fishes Lebiasina, Hoplias and Chalceus // Copeia. 1981. P. 154–168.

  57. Lauder G.V. Food capture. Fish biomechanics. Eds P.W. Webb, D. Weihs. Praeger Publishers, New York. 1983. 311 p.

  58. Lauder G.V. Aquatic feeding in lower vertebrates / Functional vertebrate morphology. Eds M. Hildebrand, D.M. Bramble, K.F. Liem, D.B. Wake. Cambridge, MA: Harvard Univ. Press. 1985. 229 p.

  59. Lauder G.V., Lanyon L.E. Functional anatomy of feeding in the bluegill sunfish, Lepomis macrochirus: in vivo measurement of bone strain // J. Exp. Biol. 1980. V. 84. P. 33–55.

  60. Lauder G.V., Liem K.F. The feeding mechanism and cephalic myology of Salvelinus fontinalis: form, function, and evolutionary significance // Charrs: Salomnids of the Genus Salvelinus. Ed. E.K. Balon. Netherlands: Junk Publishers. 1980. P. 365–390.

  61. Lauder G.V., Liem K.F. Prey capture by Luciocephalus pulcher: implications for models of jaw protrusion in teleost fishes // Environ. Biol. Fishes. 1981. V. 6. № 3/4. P. 257–268.

  62. Liem K.F. Modulatory multiplicity in the feeding mechanism in cichlid fishes, as exemplified by the invertebrate pickers of Lake Tanganyika // J. Zool. 1979. V. 189. № 1. P. 93–125. https://doi.org/10.1111/j.1469-7998.1979.tb03954.x

  63. Liem K.F. Adaptive significance of intra- and interspecific differences in the feeding repertoires of cichlid fishes // Amer. Zool. 1980a. V. 20. P. 295–314.

  64. Liem K.F. Acquisition of energy by teleosts: adaptive mecha-nisms and evolutionary patterns. Environmental physiology of fishes // Plenum Press. New York. 1980b. P. 299–334.

  65. Liem F.K., Osse J.W.M. Biological versatility, evolution, and food resource exploitation in african cichlid fishes // Am. Zool. 1975. V. 15. № 2. P. 427–454.

  66. Luca C.J., Mambrito B. Voluntary control of motor units in human antagonist muscles: coactivation and reciprocal activation // J. Neurophysiol. 1987. V. 58. № 3. P. 525–542.

  67. MacDonald I. Burial mechanics of the pacific sandfish: the role of the ventilatory pump and physical constraints on the behavior // MSc Thesis, Northern Arizona University, Flagstaff, AZ. 2015. 49 p.

  68. Martinez C.M., Tovar A.J., Wainwright P.C. A novel intramandibular joint facilitates feeding versatility in the sixbar distichodus // J. Exp. Biol. 2022. V. 225. № 2. P. 1–16. https://doi.org/10.1242/jeb.243621

  69. Mehta R.S. Ecomorphology of the moray bite: relationship between dietary extremes and morphological diversity // Physiol. Biochem. Zool. 2009. V. 82. № 1. P. 90–103.

  70. Meyer J., Herrel A., Belpaire C. et al. Broader head, stronger bite: In vivo bite forces in European eel Anguilla anguilla // J. Fish Biol. 2018. V. 92. № 1. P. 268–273.

  71. Moritz T., Britz R. Ontogeny and homology of the basipte-rygoid articulation in Pantodon buchholzi (Teleostei: Osteoglossomorpha) // Zool. J. Linn. Soc. 2005. V. 144. № 1. P. 1–13.

  72. Olivier D., Wassenbergh S., Parmentier E., Frederich B. Unprecedented biting performance in herbivorous fish: how the complex biting system of Pomacentridae circumvents performance trade-offs // Am. Nat. 2021. V. 197. № 5. P. 156–172.

  73. Osse J.W.M. Functional morphology of the head of the perch (Perca fluviatilis L.): an electromyographic study // Neth. J. Zool. 1969. V. 19. P. 289–392.

  74. Pankratz D.S. The cranial musculature of the toadfish (Opsanus tau) // J. Morph. Physiol. 1927. V. 45. P. 209–231.

  75. Pastana M.N.L., Johnson G.D., Datovo A. Comprehensive phenotypic phylogenetic analysis supports the monophyly of stromateiform fishes (Teleostei: Percomorphacea) // Zool. J. Linn. Soc. 2022. V. 195. № 3. P. 841–963.

  76. Peixoto L.A.W., Pinna M. Patterns of diversification and phylogenetic structure in the dorsolateral head musculature of Neotropical electric eels (Ostariophysi: Gymnotiformes), with a myological synonymy // Neotrop. Ichthyol. 2022. V. 20. № 1. P. 1–117. https://doi.org/10.1590/1982-0224-2021-0009

  77. Pietsch T.W. Phylogenetic relationships of trachinoid fishes of the family Uranoscopidae // Copeia. 1989. V. 1989. № 2. P. 253–303.

  78. Sanderson S.L. Variation in neuromuscular activity during prey capture by trophic specialists and generalists (Pisces: Labridae) // Brain Behav. Evol. 1988. V. 32. № 5. P. 257–268. https://doi.org/10.1159/000116554

  79. Sanford C.P.J. Salmonoid fish osteology and phylogeny (Teleostei: Salmonoidei) // Thes. Zool. 2000. V. 33. P. 1–264.

  80. Sanford C.P.J. Kinematic analysis of a novel feeding mecha-nism in the brook trout Salvelinus fontinalis (Teleostei: Salmonidae): behavioral modulation of a functional novelty // J. Exp. Biol. 2001. V. 204. P. 3905–3916. https://doi.org/10.1242/jeb.204.22.3905

  81. Sanford C.P., Lauder G.V. Functional morphology of the “tongue-bite” in the osteoglossomorph fish Notopterus // J. Morphol. 1989. V. 202. P. 379–408.

  82. Sanford C.P.J., Lauder G.V. Kinematics of the tongue-bite apparatus in osteoglossomorph fishes // J. Exp. Biol. 1990. V. 154. P. 137–162.

  83. Tran L.X., Maekawa Y., Soyano K., Ishimatsu A. Morphological comparison of the feeding apparatus in herbivorous, omnivorous and carnivorous mudskippers (Gobiidae: Oxudercinae) // Zoomorphology. 2021. V. 140. № 3. P. 387–404. https://doi.org/10.1007/s00435-021-00530-8

  84. Travers R.A. A review of the Mastacembeloidei, a suborder of synbranchiform teleost fishes. Part 1. Anatomical descriptions // Bull. Brit. Mus. (Nat. Hist.), Zool. 1984. V. 46. № 1. P. 1–133.

  85. Tulenko F.J., Currie P. Zebrafish myology // The zebrafish in biomedical research. Biology, husbandry, diseases and research applications. Academic Press. 2020. P. 115–121.

  86. Turingan R.G., Wainwright P.C. Morphological and functional bases of durophagy in the queen triggerfish, Balistes vetula (Pisces, Tetraodontiformes) // J. Morphol. 1993. V. 215. P. 101–118.

  87. Vari R.P. Anatomy, relationships and classification of the families Citharinidae and Distichodontidae (Pisces, Characoidea) // Bull. Br. Mus. (Nat. Hist.), Zool. 1979. V. 36. № 2. P. 261–344.

  88. Velasco-Hogan A., Huang W., Serrano C. et al. Tooth structure, mechanical properties, and diet specialization of Piranha and Pacu (Serrasalmidae): a comparative study // Acta Biomater. 2021. V. 134. P. 531–545.

  89. Vita G., Zanata A.M., Datovo A. Anatomy and ontogenetic changes of the facial and gular musculature of the tetra Astyanax brucutu: a remarkable case of adaptation to durophagy // J. Anat. 2020. V. 237. № 2. P. 1–15. https://doi.org/10.1111/joa.13280

  90. Wainwright P.C., Sanford C.P.J., Reilly S.M., Lauder G.V. Evolution of motor patterns: aquatic feeding in salamanders and ray-finned fishes // Brain Behav. Evol. 1989. V. 34. № 6. P. 329–341.

  91. Wassenbergh S., Dries B., Herrel A. New insights into muscle function during pivot feeding in seahorses // PloS One. 2014. V. 9. № 10. P. 1–9. https://doi.org/10.1371/journal.pone.0109068

  92. Werneburg I. Morphology of the jaw, suspensorial, and opercle musculature of Beloniformes and related species (Teleostei: Acanthopterygii), with a special refe-rence to the m. adductor mandibulae complex // PeerJ. 2015. V. 3. P. 1–53.

  93. Westneat M.W. Evolution of levers and linkages in the feeding mechanisms of fishes // Integr. Comp. Biol. 2004.V. 44. № 5. P. 378–389.

  94. Winterbottom R. A descriptive synonymy of the striated muscles of the Teleostei // Proc. Acad. Nat. Sci. Philadelphia. 1974a. V. 125. P. 225–317.

  95. Winterbottom R. The familial phylogeny of the Tetraodontiformes (Acanthopterygii: Pisces) as evidenced by their comparative myology // Smiths. Contrib. Zool. 1974, V. 155. P. l–201. https://doi.org/10.5479/si.00810282.155

  96. Ziermann J.M., Diogo R. Development of head muscles in fishes and notes on phylogeny-ontogeny links. A basis for evo-devo and developmental research on fish muscles // Evolution and development of fishes. Cambridge Univ. Press. 2018. V. 172. P. 172–187. https://doi.org/10.1017/9781316832172.011

Дополнительные материалы отсутствуют.