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Advances in the aquatic sciences
RESEARCH ARTICLE (Open Access)

Uterine fluid composition of the dwarf ornate wobbegong shark (Orectolobus ornatus) during gestation

Megan T. Ellis A B and Nicholas M. Otway A
+ Author Affiliations
- Author Affiliations

A Industry and Investment NSW, Port Stephens Fisheries Institute, Taylors Beach, NSW 2316, Australia.

B Corresponding author. Email: sharkymegs@hotmail.com

Marine and Freshwater Research 62(6) 576-582 https://doi.org/10.1071/MF10138
Submitted: 15 June 2010  Accepted: 8 January 2011   Published: 24 June 2011

Journal Compilation © CSIRO Publishing 2011 Open Access CC BY-NC-ND

Abstract

Low fecundity in chondrichthyans makes them extremely susceptible to fishing, so understanding the various reproductive strategies in this group is vital for management. Knowledge of the uterine fluid (UF) composition throughout gestation is fundamental to this understanding, yet is restricted to a few species. This study focussed on the UF composition of the wobbegong (Orectolobus ornatus), which inhabits coastal waters off eastern Australia. The UF was quantified throughout pregnancy. Fluids surrounding uterine eggs had a complex composition, with mean urea (98.48 mmol L–1), sodium (560.25 mmol L–1) and potassium (13.93 mmol L–1) concentrations significantly greater than those in seawater. A change in composition, from complex to simple, occurred after 3–4 months gestation. Major electrolyte concentrations then resembled seawater for the remainder of gestation, suggesting the flushing of the uteri with seawater and evidenced by fluctuating low levels of urea. The gestation period reflected the time for metabolism of yolk stores, osmotic and ionic adjustment, development of functioning immunological systems and prevention of external yolk sac damage. Our study is the first documentation of UF composition for a wobbegong shark and increases understanding of its reproductive biology.

Additional keywords: biochemistry, elasmobranch, reproduction.


References

Burger, J. W., and Loo, T. L. (1959). Bromination of phenol red by the dogfish, Squalus acanthias. Science 129, 778–779.
Bromination of phenol red by the dogfish, Squalus acanthias.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaG1MXmvVOhtg%3D%3D&md5=3d21de883c9c843866ef0e9e278f9871CAS | 13635012PubMed |

Carraro, R., and Gladstone, W. (2006). Habitat preferences and site fidelity of the ornate wobbegong shark (Orectolobus ornatus) on rocky reefs of New South Wales. Pacific Science 60, 207–223.
Habitat preferences and site fidelity of the ornate wobbegong shark (Orectolobus ornatus) on rocky reefs of New South Wales.Crossref | GoogleScholarGoogle Scholar |

Cavanagh, R., Kyne, P., Fowler, S. L., Musick, J. A., and Bennett, M. B. (2003). ‘The Conservation Status of Australasian Chondrichthyans. Report of the IUCN Shark Specialist Group Australia and Oceania regional Red List Workshop.’ (University of Queensland: Brisbane.)

Chan, D. K. O., and Phillips, J. G. (1966). The embryology of the rectal gland of the spiny dogfish Squalus acanthias L. Journal of Anatomy 100, 899–903.
| 1:STN:280:DyaF2s7ns1Wqsg%3D%3D&md5=5d0c0d41d5c179706351f7841700fef1CAS | 5969984PubMed |

Chatzispyrou, A., and Megalofonou, P. (2005). Sexual maturity, fecundity and embryonic development of the spiny dogfish, Squalus acanthias, in the eastern Mediterranean Sea. Journal of the Marine Biological Association of the United Kingdom 85, 1155–1161.
Sexual maturity, fecundity and embryonic development of the spiny dogfish, Squalus acanthias, in the eastern Mediterranean Sea.Crossref | GoogleScholarGoogle Scholar |

Compagno, L. J. V. (2002). ‘FAO Species Catalogue. Sharks of the World. An Annotated and Illustrated Catalogue of Shark Species Known to Date. Volume 2. Bullhead, Mackerel and Carpet Sharks (Heterodontiformes, Lamniformes and Orectolobiformes).’ (FAO: Rome.)

Corrigan, S., Huveneers, C., Schwartz, T. S., Harcourt, R. G., and Beheregaray, L. B. (2008). Genetic and reproductive evidence for two species of ornate wobbegong shark Orectolobus spp. on the Australian east coast. Journal of Fish Biology 73, 1662–1675.
Genetic and reproductive evidence for two species of ornate wobbegong shark Orectolobus spp. on the Australian east coast.Crossref | GoogleScholarGoogle Scholar |

Evans, D. H. (1981). The egg case of the oviparous elasmobranch, Raja erinacea, does osmoregulate. The Journal of Experimental Biology 92, 337–340.

Evans, D. H., Oikari, A., Kormanik, G. A., and Mansberger, L. (1982). Osmoregulation by the prenatal spiny dogfish, Squalus acanthias. The Journal of Experimental Biology 101, 295–305.
| 1:CAS:528:DyaL3sXhsFyitrg%3D&md5=0a21670ce0f0c4b4113b11227236753bCAS |

Files, T., and Lombardi, J. (1993). Free amino acids in the uterine fluids of four species of viviparous sharks (Squalus acanthias, Carcharhinus plumbeus, Mustelus canis, and Rhizoprionodon terraenovae). Comparative Biochemistry and Physiology 104B, 583–588.
| 1:CAS:528:DyaK3sXitlSnu7w%3D&md5=cb94f74c0a66d93d62b42ec217a5d107CAS |

Gilbert, P. W. (1958). The ability of yolk-sac stage dogfish pups to survive outside the uterus. Bulletin of the Mount Desert Island Biological Laboratory 1958, 68..

Gilmore, R. G., Jr, Putz, O., and Dodrill, J. W. (2005). Oophagy, intrauterine cannibalism and reproductive strategy in lamnoid sharks. In ‘Reproductive Biology and Phylogeny of Chondrichthyes: Sharks, Batoids and Chimaeras’. (Ed. W. C. Hamlett.) pp. 435–462. (Science Publishers: Enfield, NH.)

Hamlett, W. C., and Hysell, M. K. (1998). Uterine specializations in elasmobranchs. The Journal of Experimental Zoology 282, 438–459.
Uterine specializations in elasmobranchs.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.)

Hamlett, W. C., Eulitt, A. M., Jarrell, R. L., and Kelly, M. A. (1993). Uterogestation and placentation in elasmobranchs. The Journal of Experimental Zoology 266, 347–367.
Uterogestation and placentation in elasmobranchs.Crossref | GoogleScholarGoogle Scholar |

Hamlett, W. C., Jones, C. J. P., and Paulesa, L. R. (2005a). Placentatrophy in sharks. In ‘Reproductive Biology and Phylogeny of Chondrichthyes: Sharks, Batoids and Chimaeras’. (Ed. W. C. Hamlett.) pp. 463–502. (Science Publishers: Enfield, NH.)

Hamlett, W. C., Kormanik, G. A., Storrie, M. T., Stevens, B., and Walker, T. I. (2005b). Chondrichthyan parity, lecithotrophy and matrotrophy. In ‘Reproductive Biology and Phylogeny of Chondrichthyes: Sharks, Batoids and Chimaeras’. (Ed. W. C. Hamlett.) pp. 395–434. (Science Publishers: Enfield, NH.)

Hart, S., Wrathmell, A. B., and Harris, J. E. (1986). Ontogeny of gut-associated lymphoid tissue (GALT) in the dogfish Scyliorhinus canicula L. Veterinary Immunology and Immunopathology 12, 107–116.
Ontogeny of gut-associated lymphoid tissue (GALT) in the dogfish Scyliorhinus canicula L.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL2s%2FitVKhsw%3D%3D&md5=dee4f983c9a820329ef1e2d5938e03f1CAS | 3765334PubMed |

Huveneers, C. (2006). Redescription of two species of wobbegongs (Chondrichthyes: Orectolobidae) with elevation of Orectolobus halei Whitley 1940 to species level. Zootaxa 2006, 29–51.

Huveneers, C. (2007). The ecology and biology of wobbegong sharks (Genus Orectolobus) in relation to the commercial fishery in New South Wales, Australia. PhD Thesis, Macquarie University, Sydney.

Huveneers, C., Otway, N. M., and Harcourt, R. G. (2007). Morphometric relationships and catch composition of wobbegong sharks (Chondrichthyes: Orectolobus) commercially fished in New South Wales, Australia. Proceedings of the Linnean Society of New South Wales 128, 243–249.

Huveneers, C., Walker, T. I., Otway, N. M., and Harcourt, R. G. (2007). Reproductive synchrony of three sympatric species of wobbegong shark (genus Orectolobus) in New South Wales, Australia: reproductive parameter estimates necessary for population modelling. Marine and Freshwater Research 58, 765–777.
Reproductive synchrony of three sympatric species of wobbegong shark (genus Orectolobus) in New South Wales, Australia: reproductive parameter estimates necessary for population modelling.Crossref | GoogleScholarGoogle Scholar |

Jollie, W. P., and Jollie, L. G. (1967). Electron microscopic observations on accommodations to pregnancy in the uterus of the spiny dogfish, Squalus acanthias. Journal of Ultrastructure Research 20, 161–178.
Electron microscopic observations on accommodations to pregnancy in the uterus of the spiny dogfish, Squalus acanthias.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaF1c7itlyhuw%3D%3D&md5=d5da857cef052345de5c803249071b9dCAS | 5625089PubMed |

Jones, B. C., and Geen, G. H. (1977). Reproduction and embryonic development of spiny dogfish (Squalus acanthias) in the strait of Georgia, British Columbia. Journal of the Fisheries Research Board of Canada 34, 1286–1292.

Jones, R. T., and Price, K. S. (1967). A method for maintaining spiny dogfish, Squalus acanthias, pups artificially. Copeia 1967, 471–472.
A method for maintaining spiny dogfish, Squalus acanthias, pups artificially.Crossref | GoogleScholarGoogle Scholar |

Jones, T. S., and Ugland, K. I. (2001). Reproduction of female spiny dogfish, Squalus acanthias, in the Oslofjord. Fish Bulletin 99, 685–690.

Jones, K. B., Wine, R. N., Garrity, C. A., and Lombardi, J. (1990). Composition of uterine fluid in four species of viviparous sharks. American Zoologist 30, 83a..

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

Kormanik, G. A. (1988). Time course establishment of the uterine seawater conditions in late-term pregnant spiny dogfish (Squalus acanthias). The Journal of Experimental Biology 137, 443–456.
| 1:STN:280:DyaL1M%2FpsVajug%3D%3D&md5=e406a8c4b7aa7b880f4266e9a65a586dCAS | 3145320PubMed |

Kormanik, G. A. (1992). Ion and osmoregulation in prenatal elasmobranchs: evolutionary implications. American Zoologist 32, 294–302.

Kormanik, G. A. (1993). Ionic and osmotic environment of developing elasmobranch embryos. Environmental Biology of Fishes 38, 233–240.
Ionic and osmotic environment of developing elasmobranch embryos.Crossref | GoogleScholarGoogle Scholar |

Kormanik, G. A., Lofton, A. J., and Vibbard, D. E. (1991). The ontogeny of mitochondria-rich cells in embryos of the spiny dogfish¸ Squalus acanthias. Bulletin of the Mount Desert Island Biological Laboratory 30, 4–7.

Last, P. R., and Stevens, J. D. (2009). ‘Sharks and Rays of Australia.’ (CSIRO Publishing: Melbourne.)

Lloyd-Evans, P. (1993). Development of the lymphomyeloid system in the dogfish, Scyliorhinus canicula. Developmental and Comparative Immunology 17, 501–514.
Development of the lymphomyeloid system in the dogfish, Scyliorhinus canicula.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2c7jtFWnug%3D%3D&md5=8ff29c6ad5dc3c581e58252475307904CAS | 8299849PubMed |

Lombardi, J., Jones, K. B., Garrity, C. A., and Files, T. (1993). Chemical composition of uterine fluid in four species of viviparous sharks (Squalus acanthias, Carcharhinus plumbeus, Mustelus canis and Rhizoprionodon terraenovae). Comparative Biochemistry and Physiology 105A, 91–102.
| 1:CAS:528:DyaK3sXktVGhs78%3D&md5=c44eeeda828c78fac1c8515623f4685eCAS |

Luer, C. A., Walsh, C. J., and Bodine, A. B. (2004). The immune system of sharks, skates and rays. In ‘Biology of Sharks and Their Relatives’. (Eds J. C. Carrier, J. A. Musick and M. R. Heithaus.) pp. 369–395. (CRC Press: London.)

Needham, J., and Needham, D. M. (1930). Nitrogen excretion in selachian ontogeny. The Journal of Experimental Biology 7, 7–18.
| 1:CAS:528:DyaA3cXitVensA%3D%3D&md5=15bea361b31d44b696395c26ae065bc9CAS |

Price, K. S., and Daiber, F. C. (1967). Osmotic environments during fetal development of dogfish, Mustelus canis (Mitchill) and Squalus acanthias Linnaeus, and some comparisons with skates and rays. Physiological Zoology 40, 248–260.
| 1:CAS:528:DyaF1cXlslKruw%3D%3D&md5=a3ea296f1cb3ce98f8972ebf69007530CAS |

Read, L. J. (1968). Ornithine–urea cycle enzymes in early embryos of the dogfish Squalus suckleyi and the skate Raja binoculata. Comparative Biochemistry and Physiology 24, 669–674.
Ornithine–urea cycle enzymes in early embryos of the dogfish Squalus suckleyi and the skate Raja binoculata.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF1cXlslOisw%3D%3D&md5=ecb81db3bf4e048974209ab254ffb9dcCAS | 5651305PubMed |

Read, L. J. (1968). Urea and trimethylamine oxide levels in elasmobranch embryos. The Biological Bulletin 135, 537–547.
Urea and trimethylamine oxide levels in elasmobranch embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF1MXjsFCmsA%3D%3D&md5=1f11a9b040e2de584b1e1266d087a210CAS |

Rumfelt, L. L., McKinney, E. C., Taylor, E., and Flajnik, M. F. (2002). The development of primary and secondary lymphoid tissues in the nurse shark Ginglymostoma cirratum: B-cell zones precede dendritic immigration and T-cell zone formation during ontogeny of the spleen. Scandinavian Journal of Immunology 56, 130–148.
The development of primary and secondary lymphoid tissues in the nurse shark Ginglymostoma cirratum: B-cell zones precede dendritic immigration and T-cell zone formation during ontogeny of the spleen.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XmvVarsrs%3D&md5=ffeab051698195b600e19d5e260b2641CAS | 12121433PubMed |

Scandol, J., Rowling, K., and Graham, K. (Eds) (2008). Status of fisheries resources in NSW 2006/07. NSW Department of Primary Industries, Sydney.

Snecedor, G. W., and Cochran, G. W. (1967). ‘Statistical Methods.’ (Iowa State University Press: Ames, IA.)

Sokal, R. R., and Rohlf, F. J. (1969). ‘Biometry.’ (WH Freeman: San Francisco, CA.)

Stevens, B. (2001). Uterine and oviducal mechanisms for gestation in the common saw shark, Pristiophorus cirratus. BSc (Hons) Thesis, University of Melbourne, Melbourne.

Sunye, P. S., and Vooren, C. M. (1997). On cloacal gestation in angel sharks from southern Brazil. Journal of Fish Biology 50, 86–94.
On cloacal gestation in angel sharks from southern Brazil.Crossref | GoogleScholarGoogle Scholar |

Thorson, T. B., and Gerst, J. W. (1972). Comparison of some parameters of serum and uterine fluid of pregnant, viviparous sharks (Carcharhinus leucas) and serum of their near-term young. Comparative Biochemistry and Physiology 42A, 33–40.

Von Bonde, C. (1945). Stages in the development of picked or spiny dogfish, Squalus acanthias Linn. The Biological Bulletin 88, 220–232.
Stages in the development of picked or spiny dogfish, Squalus acanthias Linn.Crossref | GoogleScholarGoogle Scholar |

Witschi, E. (1956). ‘Development of Vertebrates.’ (W. B. Saunders: Philadelphia, PA.)

Wourms, J. P. (1977). Reproduction and development in chondrichthyan fishes. American Zoologist 17, 379–410.

Wourms, J. P., and Lombardi, J. (1992). Reflections on the evolution of piscine viviparity. American Zoologist 32, 276–293.

Wourms, J. P., Groves, B. D., and Lombardi, J. (1988). The maternal–embryonic relationship in viviparous fishes. In ‘Fish Physiology. Volume 11. Part B, Viviparity and Posthatching Juveniles’. (Eds W. S. Hoar and D. J. Randall.) pp. 1–134. (Academic Press: New York, NY.)