Skip to main content

Advertisement

SpringerLink
Log in

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

  • Original Paper
  • Published:
Zoomorphology Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Bell JP, Satchell GH (1963) An undescribed unilateral ocular reflex in the dogfish Squalus acanthias. Austr J Exp Biol 41:221–234

    Article  CAS  Google Scholar 

  • Cappetta H (1987) Chondrichthyes II. Mesozoic and Cenozoic Elasmobranchii. Gustav Fischer, New York, pp 1–193

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Compagno LJV (1988) Sharks of the order carcharhiniformes. Princeton University Press, New Jersey, p 572

    Google Scholar 

  • 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 501–548

    Google Scholar 

  • Crawford MLJ, Marc RE (1976) Light transmission of cat and monkey eyelids. Vision Res 16:323–324

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • Dillon EM, Norris RD, Dea AO (2017) Dermal denticles as a tool to reconstruct shark communities. Mar Ecol Prog Ser 566:117–134

    Article  Google Scholar 

  • 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 496:207–218

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Gruber SH, Myrberg AA (1977) Approaches to the study of the behavior of sharks. Am Zool 17:471–486

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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 325–368

    Google Scholar 

  • 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 43–68

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Marshall LJ (2011) The fin blue line: Quantifying fishing mortality using shark fin morphology. Dissertation, University of Tasmania

  • 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

    Article  Google Scholar 

  • 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):1096–1110

    Article  PubMed  Google Scholar 

  • 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 7:521–528

    Article  Google Scholar 

  • Puff C, Herder V, Philipp A, Baumgartner W (2008) Lymphangiosarcoma in the nictitating membrane of a horse. J Veter Diagn Invest 20:108–110

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Raschi W, Tabit C (1992) Functional aspects of placoid scales: a review and update. Aust J Mar Fresh Res 43:123–147

    Article  Google Scholar 

  • Reif WE (1978) Protective and hydrodynamic function of the dermal skeleton of elasmobranchs. Neues Jahrbuch Für Geologie Und Paläontologie 157:33–141

    Google Scholar 

  • Ritter EK, Godknecht AJ (2000) Agonistic displays in the blacktip shark (Carcharhinus limbatus). Copeia 2000:282–284

    Article  Google Scholar 

Download references

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).

Author information

Authors and Affiliations

  1. Setor de Anatomia, Departamento de Cirurgia da Faculdade de Medicina Veterinária e Zootecnia da Universidade de São Paulo, São Paulo, SP, Brazil

    Aline Nayara Poscai, Bianca de Sousa Rangel & José Roberto Kfoury Junior

  2. Departamento de Fisiologia, Instituto de Biociências, Universidade de São Paulo, Rua do Matão, travessa 14, no 321, Cidade Universitária, São Paulo, SP, Brazil

    Bianca de Sousa Rangel

  3. Laboratório de Biologia Animal, Universidade Federal do Acre, Campus Floresta, Cruzeiro do Sul, AC, Brazil

    André Luis da Silva Casas

  4. Departamento de Fisiologia, Setor de Ciências Biológicas, Universidade Federal do Paraná, Centro Politécnico, Curitiba, Paraná, 81531-990, Brazil

    Natascha Wosnick

  5. Instituto de Pesca /APTA/SAA/SP, Av. Bartolomeu de Gusmão, 192, Santos, SP, 11030-500, Brazil

    Alexandre Rodrigues

  6. Central de Facilidades à Pesquisa da Faculdade de Medicina Veterinária e Zootecnia da Universidade de São Paulo, Rua Professor Orlando Marques Paiva, s/n, São Paulo, SP, 05508-270, Brazil

    Rose Eli Grassi Rici

Authors
  1. Aline Nayara Poscai
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bianca de Sousa Rangel
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. André Luis da Silva Casas
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Natascha Wosnick
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Alexandre Rodrigues
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Rose Eli Grassi Rici
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. José Roberto Kfoury Junior
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Aline Nayara Poscai.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Poscai, A.N., de Sousa Rangel, B., da Silva Casas, A.L. et al. Microscopic aspects of the nictitating membrane in Carcharhinidae and Sphyrnidae sharks: a preliminary study. Zoomorphology 136, 359–364 (2017). https://doi.org/10.1007/s00435-017-0351-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00435-017-0351-1

Keywords

Search

Navigation