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Zoomorphology

, Volume 136, Issue 3, pp 359–364 | Cite as

Microscopic aspects of the nictitating membrane in Carcharhinidae and Sphyrnidae sharks: a preliminary study

  • Aline Nayara Poscai
  • Bianca de Sousa Rangel
  • André Luis da Silva Casas
  • Natascha Wosnick
  • Alexandre Rodrigues
  • Rose Eli Grassi Rici
  • José Roberto Kfoury Junior
Original Paper

Abstract

The nictitating membrane is an anatomic structure exclusively exhibited by Carcharhiniformes, the largest order among sharks. Here we present a detailed description of morphological characteristics of the nictitating membrane through light microscopy (LM) and scanning electron microscopy (SEM) in the following shark species: Carcharhinus limbatus, Galeocerdo cuvier, Prionace glauca, Rhizoprionodon lalandii, R. porosus, Sphyrna lewini and S. zygaena. Differences in the microscopic aspects of dermal denticles from the species studied were observed. P. glauca, a pelagic shark, showed a well-developed protection apparatus when compared with other pelagic species, while coastal sharks showed even higher structural complexity. In the blue shark the denticles are enameled, presenting an extensive pulp cavity and a base inserted in a connective tissue. Moreover, the species exhibits the higher number of ridges (up to nine) of varied size and shape and the muscular tissue is inserted in the ventral region of the connective tissue. Dermal denticles from C. limbatus, R. lalandii, R. porosus, S. zygaena and G. cuvier exhibit up to five ridges with hexagonal ornamentations in the crown. In S. lewini and S. zygaena, the denticles are rounded shaped and glandular cells are present. The patterns observed in the present study suggest a high level of specialization and evolutionary conservation shaped by the function of the structure. In addition, we hypothesize that the morphological simplification observed in the membrane when compared to the dermal denticles from the skin, is an evolutionary trait that evolved to improve the dynamic and biomechanics of this highly mobile structure allowing this way, a rapid and efficient protection against abrasion, mainly during predation events.

Keywords

Nictitating membrane Dermal denticles Requiem sharks Electron microscopy 

Notes

Acknowledgements

We would like to thank CAPES (granted ANP and NW) for the support, the postgraduate program of Department of Surgery, Faculty of the Veterinary Medicine and Animal Science, University of São Paulo and the funding provided by FAPESP through contract number 2016/09095-2 (Granted to BRS).

References

  1. Bell JP, Satchell GH (1963) An undescribed unilateral ocular reflex in the dogfish Squalus acanthias. Austr J Exp Biol 41:221–234CrossRefGoogle Scholar
  2. Cappetta H (1987) Chondrichthyes II. Mesozoic and Cenozoic Elasmobranchii. Gustav Fischer, New York, pp 1–193Google Scholar
  3. Ciena AP, Rangel BS, Bruno CEM, Miglino MA, Amorim AF, Rici REG, Watanabe I (2015) Morphological aspects of oral denticles in the Sharpnose shark Rhizoprionodon lalandii (Muller and Henle, 1839) (Elasmobranchii, Carcharhinidae). Anat Histol Embryol 45:109–114. DOI: 10.1111/ahe.12178 CrossRefPubMedGoogle Scholar
  4. Compagno LJV (1988) Sharks of the order carcharhiniformes. Princeton University Press, New Jersey, p 572Google Scholar
  5. COMPAGNO LJV (2005) Checklist of living Chondrichthyes. In: Hamlett WC (eds) Reproductive biology and phylogeny of Chondrichthyes: sharks, batoids and chimaeras. Science Publishes, Inc, United States, pp 501–548Google Scholar
  6. Crawford MLJ, Marc RE (1976) Light transmission of cat and monkey eyelids. Vision Res 16:323–324CrossRefPubMedGoogle Scholar
  7. Danylchuk AJ, Suski CD, Mandelman JW, Murchie KJ, Haak CR, Brooks AML, Cook SJ (2014) Hooking injury, physiological status and short-term mortality of juvenile lemon sharks (Negaprion bevirostris) following catch-and-release recreational angling. Conser Physiol. doi: 10.1093/conphys/cot036 Google Scholar
  8. Dillon EM, Norris RD, Dea AO (2017) Dermal denticles as a tool to reconstruct shark communities. Mar Ecol Prog Ser 566:117–134CrossRefGoogle Scholar
  9. Gallagher AJ, Serafy JE, Cooke SJ, Hammerschlag N (2014) Physiological stress response, reflex impairment, and survival of five sympatric shark species following experimental capture and release. Mar Ecol Prog Ser 496:207–218CrossRefGoogle Scholar
  10. Gravendeel R, Neer WV, Brinkhuizen D (2002) An identification key for dermal denticles of Rajidae from the North Sea. Int J Osteoarchaeol 12:420–441. doi: 10.1002/oa.645 CrossRefGoogle Scholar
  11. Gruber SH, Myrberg AA (1977) Approaches to the study of the behavior of sharks. Am Zool 17:471–486CrossRefGoogle Scholar
  12. Gruber SH, Schneiderman N (1975) Classical conditioning of the nictitating membrane response of the lemon shark (Negaprion brevirostris). Behav Res Methods Instrum 7:430–434. doi: 10.3758/BF03201554 CrossRefGoogle Scholar
  13. Hueter RE, Mann DA, Maruska KP, Sisneros JA, Demski LS (2004) Sensory biology of elasmobranchs. In: Carrier JC, Musick JA, Heithaus MR (eds) Biology of sharks and their relatives. CRC, Boca Raton, pp 325–368Google Scholar
  14. Kemp NE (1999) Integumentary system and teeth. In: Hamlett WC (ed) Sharks, skates and rays: the biology of elasmobranch fishes. John Hopkins University Press, Baltimore, pp 43–68Google Scholar
  15. Klećkowska-Nawrot J, Dzięgiel P (2007) Morphology of the third eyelid and superficial gland of the third eyelid on pig fetuses. Anat Histol Embryol 36:428–432. doi: 10.1111/j.1439-0264.2007.00780.x CrossRefPubMedGoogle Scholar
  16. Laranjeira ME, Guimarães JP, Amorim AF, Rotundo M, Rici REG, Mari RB (2015) Ultrastructure of dermal denticles in sharpnose shark (Rhizoprionodon lalandii)(Elasmobranchii, Carcharhinidae). Microsc Res Tech 78(10):859–864. doi: 10.1002/jemt.22546 CrossRefPubMedGoogle Scholar
  17. Marshall LJ (2011) The fin blue line: Quantifying fishing mortality using shark fin morphology. Dissertation, University of TasmaniaGoogle Scholar
  18. Mello WC, De Carvalho JJ, Brito PMM (2013) Microstructural morphology in early dermal denticles of hammerhead sharks (Elasmobranchii: Sphyrnidae) and related taxa. Acta Zool-Stockholm 94:147–153. doi: 10.1111/j.1463-6395.2011.00547.x CrossRefGoogle Scholar
  19. Motta P, Habegger ML, Lang A, Hueter R, Davis J (2012) Scale morphology and flexibility in the shortfin mako Isurus oxyrinchus and the blacktip shark Carcharhinus limbatus. J Morphol 273(10):1096–1110CrossRefPubMedGoogle Scholar
  20. Pires AG, Algueró MC, Mendes JL, Trindade H, Correia M (2008) Immunophenotyping of lymphocyte subsets in the third eyelid tissue in dogs (Canis familiaris): Morphological, microvascular, and secretory aspects of this ocular adnexa. Microsc Res Tech 7:521–528CrossRefGoogle Scholar
  21. Puff C, Herder V, Philipp A, Baumgartner W (2008) Lymphangiosarcoma in the nictitating membrane of a horse. J Veter Diagn Invest 20:108–110CrossRefGoogle Scholar
  22. Rangel BS, Ciena AP, Wosnick N, Amorim AF, Kfoury-Junior JR, Rici REG (2016) Ecomorphology of oral papillae and denticles ofZapteryx brevirostris (Chondrichthyes, Rhinobatidae). Zoomorph 135:189–195. doi: 10.1007/s00435-016-0304-0 CrossRefGoogle Scholar
  23. Raschi W, Tabit C (1992) Functional aspects of placoid scales: a review and update. Aust J Mar Fresh Res 43:123–147CrossRefGoogle Scholar
  24. Reif WE (1978) Protective and hydrodynamic function of the dermal skeleton of elasmobranchs. Neues Jahrbuch Für Geologie Und Paläontologie 157:33–141Google Scholar
  25. Ritter EK, Godknecht AJ (2000) Agonistic displays in the blacktip shark (Carcharhinus limbatus). Copeia 2000:282–284CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • Aline Nayara Poscai
    • 1
  • Bianca de Sousa Rangel
    • 1
    • 2
  • André Luis da Silva Casas
    • 3
  • Natascha Wosnick
    • 4
  • Alexandre Rodrigues
    • 5
  • Rose Eli Grassi Rici
    • 6
  • José Roberto Kfoury Junior
    • 1
  1. 1.Setor de AnatomiaDepartamento de Cirurgia da Faculdade de Medicina Veterinária e Zootecnia da Universidade de São PauloSão PauloBrazil
  2. 2.Departamento de Fisiologia, Instituto de BiociênciasUniversidade de São PauloSão PauloBrazil
  3. 3.Laboratório de Biologia AnimalUniversidade Federal do AcreCruzeiro do SulBrazil
  4. 4.Departamento de Fisiologia, Setor de Ciências BiológicasUniversidade Federal do Paraná, Centro PolitécnicoCuritibaBrazil
  5. 5.Instituto de Pesca /APTA/SAA/SPSantosBrazil
  6. 6.Central de Facilidades à Pesquisa da Faculdade de Medicina Veterinária e Zootecnia da Universidade de São PauloSão PauloBrazil

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