Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
RESEARCH ARTICLE

Microscopic organisation of the oviducal gland of the holocephalan elephant fish, Callorhynchus milii

Rachel M. Smith A B E , Terence I. Walker C and William C. Hamlett A D
+ Author Affiliations
- Author Affiliations

A Department of Zoology, The University of Melbourne, Victoria 3010, Australia.

B 4 Bloomfield Road, Ascot Vale, Victoria 3032, Australia.

C Primary Industries Research Victoria, PO Box 114, Queenscliff, Victoria 3225, Australia.

D Department of Anatomy & Cell Biology, Indiana University School of Medicine, South Bend Center for Medical Education, Notre Dame, IN 46530, USA.

E Corresponding author. Email: rachel.smith@csl.com.au

Marine and Freshwater Research 55(2) 155-164 https://doi.org/10.1071/MF01078
Submitted: 11 May 2001  Accepted: 23 January 2004   Published: 31 March 2004

Abstract

The study of chondrichthyan reproductive biology has a long history, but the structure and function of the holocephalan oviducal glands (OG) is poorly known; these organs are a vital component in the understanding of chondrichthyan life history. Histochemical techniques revealed that a fundamental zonation was evident in the OG of Callorhynchus milii, similar to most elasmobranchs. In sexually mature females, the following zones occurred (anterior to posterior): (1) club zone, periodic acid–Schiff positive (PAS+), indicating glycoprotein or any mucus substance containing neutral sugars, and Alcian blue positive, pH 2.5 (AB+), indicating the presence of sulfated and unsulfated acid glycosaminoglycans and sialoglycoproteins; (2) papillary zone (AB+); (3) baffle zone (PAS–, AB–); and (4) terminal zone (AB++). Using histological and histochemical techniques not used previously with the holocephalan group, we demonstrated that the structure and function of the OG zones were equivalent between oviparous elasmobranchs and C. milii, even though their final egg capsule morphologies differed. It was also evident that the club and papillary zones produce the egg jelly that surrounds the egg and the baffle zone formed the multilaminate egg capsule. Furthermore, the terminal zone had functions associated with sperm storage and the production of fine hairs that decorate the surface of the egg capsule.


Acknowledgments

We are grateful to Professor Marilyn Renfree, Dr Rob Day, Amy Beck, Matt Reardon, Joan Clark, Bruce Abaloz and David Paul of The University of Melbourne (UM) and to Russell Hudson of Primary Industries Research Victoria (PIRVic) who assisted this research. Most of this work was accomplished while W. C. H. was on sabbatical leave at UM. The research was supported by an Enhancing International Science Networks Visiting Fellowship (PIRVic) and a Visiting Research Scholar Travel Grant, 2000 (UM). The research was undertaken in support of a project entitled ‘Saw shark and elephant fish assessment and by-catch evaluation in the Southern Shark Fishery’. That project was undertaken by PIRVic and funded by the Australian Fisheries Research and Development Corporation (Project 1999/103).


References

Callard, I. P. , and Koob, T. J. (1993). Endocrine regulation of the elasmobranch reproductive tract. The Journal of Experimental Zoology 266, 368–377.


Conrath, C. L. , and Musick, J. A. (2002). Reproductive biology of the smooth dogfish, Mustelus canis, in the northwest Atlantic Ocean. Environmental Biology of Fishes 64, 367–377.
Crossref | GoogleScholarGoogle Scholar |

Cook, H. (1990). Carbohydrates. In ‘The Theory and Practice of Histological Techniques’, 3rd edn. (Eds. J. D. Bancroft and A. Stevens)  pp. 177–214. (Churchill Livingstone: London, UK.)

Dean, B. (1895). ‘Fishes, Living and Fossil. Columbia University Series III.’ (Columbia University: New York, USA.)

Dean, B. (1906). ‘Chimaeroid Fishes and Their Development.’ (Carnegie Institute: Washington, DC, USA.)

Dean, B. (1912). Orthogenesis in the egg capsules of Chimaera.  Bulletin of the American Museum of Natural History 31, 35–40.


Feldheim, K. A. , Gruber, S. H. , and Ashley, M. V. (2001). Multiple paternity of a lemon shark litter (Chondrichthyes; Carcharhinidae). Copiea 2001, 781–786.


Feng, D. , and Knight, D. P. (1992). Secretion and stabilization of the egg capsule of the dogfish Scyliorhinus canicula.  Tissue & Cell 24, 773–790.
Crossref | GoogleScholarGoogle Scholar |

Feng, D. , and Knight, D. P. (1994). Structure and formation of the egg capsule tendrils in the dogfish Scyliorhinus canicula.  Philosophical Transactions of the Royal Society of London 343B, 285–302.


Fishelson, L. , and Baranes, A. (1998). Observations on the Oman shark, Iago omanensis (Triakidae), with emphasis on the morphological and cytological changes of the oviduct and yolk sac during gestation. Journal of Morphology 236, 151–165.
Crossref | GoogleScholarGoogle Scholar |

Hamlett, W. C. and  Koob, T. J. (1999). Female reproductive system. In ‘Sharks Skates and Rays. The Biology of Elasmobranch Fishes’. (Ed W. C. Hamlett.)  pp. 398–443. (The Johns Hopkins University Press: Baltimore, MD, USA.)

Hamlett, W. C. , Knight, D. P. , Koob, T. J. , Jezior, M. , Luong, T. , Rozycki, T. , Brunette, N. , and Hysell, M. K. (1998). Survey of oviducal gland structure and function in elasmobranchs. The Journal of Experimental Zoology 282, 399–420.
Crossref | GoogleScholarGoogle Scholar |

Hamlett, W. C., Hysell, M. K., Jezior, M., Rozycki, T., Brunette, N., and  Tumilty, K. (1999). Fundamental zonation in elasmobranch oviducal glands. In ‘Proceedings of the 5th Indo-Pacific Fish Conference, Nouméa, 1997’. (Eds. B. Seret and J.-Y. Sire)  pp. 271–280. (Society of French Ichthyology: Paris, France.)

Hamlett, W. C. , Musick, J. A. , Hysell, C. K. , and Sever, D. M. (2002). Uterine epithelial–sperm interaction, endometrial cycle and sperm storage in the terminal zone of the oviducal gland in the placental smoothhound, Mustelus canis.  The Journal of Experimental Zoology 292, 129–144.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Hamlett, W. C. , Fishelson, L. , Baranes, A. , Hysell, C. K. , and Sever, D. M. (2002). Ultrastructural analysis of sperm storage and morphology of the oviducal gland in the Oman shark, Iago omanensis (Triakidae). Marine and Freshwater Research 53, 601–613.
Crossref | GoogleScholarGoogle Scholar |

Hamlett, W. C., Greven, H. and  Schindler, J. (2003). Sperm storage in the Class Chondrichthyes & Class Osteichthyes. In ‘The New Panorama of Animal Evolution. Proceedings of the 18th International Congress of Zoology’. (Eds. A. Legakis, S. Sfenthourakis, R. Polymeni and M. Thessalou-Legaki)  pp. 405–413. (Pensoft: Moscow, Russia.)

Hobson, A. D. (1930). A note on the formation of the egg case of the skate. Journal of the Marine Biological Association of the UK 16, 577–581.


Humason, G. L. (1972). Staining connective tissue and muscle. In ‘Animal Tissue Techniques’, 3rd edn. (Ed G. L. Humason)  pp. 297–300. (WH Freeman and Co.: San Francisco, CA, USA.)

Knight, D. P. , and Feng, D. (1992). Formation of the dogfish egg case, a coextruded, multilayer laminate. Biomimetics 1, 151–175.


Knight, D. P. , Feng, D. , Stewart, M. , and King, E. (1993). Changes in macromolecular organization in collagen assemblies during secretion in the nidamental gland and formation of the egg capsule wall in the dogfish Scyliorhinus canicula.  Philosophical Transactions of the Royal Society of London 341B, 419–436.


Knight, D. P. , Feng, D. , and Stewart, M. (1996). Structure and function of the selachian egg case. Biological Reviews 71, 81–111.
Crossref | GoogleScholarGoogle Scholar |

Koob, T. J. , and Straus, J. W. (1998). On the role of egg jelly in Raja erinacea.  Bulletin of the Mt. Desert Island Biological Laboratory 37, 117–119.


Lewis, D. N. and  Fellars, J. F. (1988). Processing of polymer liquid crystals. In ‘High Modulus Polymers: Approaches to Design and Development’. (Eds. P. A. E. Zacharides, R. S. Porter, R. Polymeni and M. Thessalou-Legaki)  pp. 28–36. (Marcell Dekker: New York, USA.)

Lo Bianco, S. (1909). Notizie biologiche riguardanti specialmente il periodo di maturita sessuale degli animali del golfo di Napoli. Mitteilungen an der zoolischen Station zu Neapel 19, 513–791.


Metten, H. (1939). Studies on the reproduction of the dogfish. Philosophical Transactions of the Royal Society of London 230B, 217–238.


Metten, H. (1944). The fate of spermatozoa in the female dogfish (Scyliorhinus canicula). The Quarterly Journal of Microscopical Science 84, 283–295.


Nalini, K. P. (1940). Structure and function of the nidamental gland of Chiloscyllium griseum (Mull. and Henle). Proceedings of the Indian Academy of Science 128, 189–214.


Prasad, R. R. (1945). The structure, phylogenetic significance, and function of the nidamental glands of some elasmobranchs of the Madras coast. Proceedings of the National Institute of Sciences India 11, 282–303.


Prasad, R. R. (1945). Further observations on the structure and function of the nidamental glands of a few elasmobranchs of the Madras coast. Proceedings of the Indian Academy of Science 22, 368–373.


Prasad, R. R. (1948). Observations on the nidamental glands of Hydrolagus colliei, Raja rhina and Platyrhinoids triseriatus.  Copeia 1948, 54–57.


Pratt, H. L. (1993). The storage of spermatozoa in the oviducal glands of western north Atlantic sharks. Environmental Biology of Fishes 38, 139–149.


Rusaouën, M. (1976). The dogfish shell gland, a histochemical study. Journal of Experimental Marine Biology and Ecology 23, 267–283.
Crossref | GoogleScholarGoogle Scholar |

Saville, K. J. , Lindley, A. M. , Maries, E. G. , Carrier, J. C. , and Pratt, H. L. (2002). Multiple paternity in the nurse shark, Ginglymostoma cirratum.  Environmental Biology of Fishes 63, 347–351.
Crossref | GoogleScholarGoogle Scholar |

Stanley, H. P. (1963). Urogenital morphology in the chimaeroid fish Hydrolagus colliei (Lay and Bennett). Journal of Morphology 112, 99–125.
PubMed |

Stevens, A. (1990). The haemotoxylins. In ‘The Theory and Practice of Histological Techniques’, 3rd edn. (Eds. J. D. Bancroft, A. Stevens, R. Polymeni and M. Thessalou-Legaki)  pp. 107–118. (Churchill Livingstone: London, UK.)

Storrie, M. T., Walker, T. I., Laurenson, L., and  Hamlett, W. C. (2001). Aplacental yolk sac viviparity in the gummy shark, Mustelus antarcticus. In ‘Sixth Indo-Pacific Fish Conference Scientific Programme and Book of Abstracts, 20–25 May 2001, Durban, South Africa’. (Oceanographic Research Institute: Durban, South Africa.)

Threadgold, L. T. (1957). A histochemical study of the shell gland of Scyliorhinus caniculus.  The Journal of Histochemistry and Cytochemistry 5, 159–166.
PubMed |