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Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
RESEARCH ARTICLE

Sexual development and maturity of the male brown banded bamboo shark, Chiloscyllium punctatum (Elasmobranchii : Hemiscylliidae)

Hesam Sephid A , Negin Salamat https://orcid.org/0000-0002-5565-3725 A B and Mohammad Ali Salari A
+ Author Affiliations
- Author Affiliations

A Department of Marine Biology, Faculty of Marine Sciences, Khorramshahr University of Marine Science and Technology, Khorramshahr, 64199-34619, Iran.

B Corresponding author. Email: salamatnegin@gmail.com

Marine and Freshwater Research 72(8) 1160-1172 https://doi.org/10.1071/MF20305
Submitted: 13 October 2020  Accepted: 20 January 2021   Published: 15 March 2021

Abstract

The present study aimed to assess the reproductive biology of male brown banded bamboo shark (Chiloscyllium punctatum). Morphological and histological changes in the reproductive tract and changes in gonad steroid testosterone were assessed in 110 male C. punctatum collected from Bahrakan Creek between January 2018 and March 2019. The reproductive tract in male C. punctatum consisted of a pair of testes, efferent ducts, epididymidis, ductus deferens, seminal vesicles, Leydig gland and claspers. Four sexual development stages were determined: (1) immature, no calcified claspers (2) maturing, partially calcified claspers; (3) active and resting adults. Both adult resting and active stages had calcified claspers. In this study, immature male C. punctatum without calcified claspers were found from August to October, maturing C. punctatum with partially calcified claspers were found from November to January and adult C. punctatum caught from February to April were active with calcified claspers, whereas adult fish collected from May to July and during the rest of the year (until mid-January in the following year) were in the resting stage with inactive testes. The testis had a lobular structure and the spermatocysts were arranged diametrically (i.e. along the cross-sectional width of the testis) in each lobule. Plasma testosterone concentrations were associated with histomorphological changes in the reproductive tract. Testosterone concentrations peaked in March in active males and then decreased significantly in resting males. Overall, the variations in the reproductive organs during different sexual maturity stages were consistent with their roles in the production, movement and release of spermatozoa.

Keywords: bamboo shark, Chiloscyllium punctatum, reproductive biology, sexual maturity, steroids.


References

Alimi, R., Savari, A., Movahedinia, A., Zakeri, M., and Salamat, N. (2013). Study of osmoregulation mechanisms in Chiloscyllium punctatum. M.Sc. Thesis, Khorramshahr University of Marine Science and Technology, Khorramshahr, Iran.

Awruch, C. A., Pankhurst, N. W., Frusher, S. D., and Stevens, J. D. (2008). Endocrine and Morphological Correlates of Reproduction in the Draughtboard Shark Cephaloscyllium laticeps (Elasmobranchii: Scyliorhinidae). The Journal of Experimental Zoology 309A, 184–197.
Endocrine and Morphological Correlates of Reproduction in the Draughtboard Shark Cephaloscyllium laticeps (Elasmobranchii: Scyliorhinidae).Crossref | GoogleScholarGoogle Scholar |

Awruch, C. A., Jones, S. M., Asorey, M. G., and Barnett, A. (2014). Non-lethal assessment of the reproductive status of broadnose sevengill sharks (Notorynchus cepedianus) to determine the significance of habitat use in coastal areas. Conservation Physiology 2, cou013.
Non-lethal assessment of the reproductive status of broadnose sevengill sharks (Notorynchus cepedianus) to determine the significance of habitat use in coastal areas.Crossref | GoogleScholarGoogle Scholar | 27293634PubMed |

Balart, E. F., Gonza’les-Garcıa, J., and Villavicencio-Garayzar, C. (2000). Notes on the biology of Cephalurus cephalus and Parmaturus xaniurus (Chondrichthyes: Scyliorhinidae) from the west coast of Baja California Sur, Mexico. Fish Bulletin 98, 219–221.

Chen, W. K., and Liu, K. M. (2006). Reproductive biology of whitespotted bamboo shark Chiloscyllium plagiosum in northern waters off Taiwan. Fisheries Science 72, 1215–1224.
Reproductive biology of whitespotted bamboo shark Chiloscyllium plagiosum in northern waters off Taiwan.Crossref | GoogleScholarGoogle Scholar |

Clark, E., and Von Schmidt, K. (1965). Sharks of the central gulf coast of Florida. Bulletin of Marine Science 15, 13–83.

Compagno, L. J. V. (2001). 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 Species Catalogue for Fishery Purposes, Food and Agriculture Organization of the United Nations, Rome, Italy.

De Rêgo, M. G., Fitzpatrick, J. L., Hazin, F. H., Araujo, M. L., da Silveira, M. L., Oliveira, P. G. V., and Neto, J. E. (2015). Characterization of testicular morphology and spermatogenesis in the nurse sharks Ginglymostoma cirratum (Bonnaterre, 1788). Zoomorphology 134, 117–123.
Characterization of testicular morphology and spermatogenesis in the nurse sharks Ginglymostoma cirratum (Bonnaterre, 1788).Crossref | GoogleScholarGoogle Scholar |

De Rêgo, M. G., Fitzpatrick, J. L., Hazin, F. H., Araujo, M. L., Barros, M. D., and Neto, J. E. (2016). Comparison of the morphology and histomorphometry of spermatogenic cyst of three shark species with diametric testes. Anatomical Record 299, 759–768.
Comparison of the morphology and histomorphometry of spermatogenic cyst of three shark species with diametric testes.Crossref | GoogleScholarGoogle Scholar |

Del Mar Pedreros-Sierra, T., and Ramirez-Pinilla, M. P. (2015). Morphology of the reproductive tract and acquisition of sexual maturity in males of Potamotrygon magdalenae (Elasmobranchii: Potamotrygonidae). Journal of Morphology 276, 273 –289.
Morphology of the reproductive tract and acquisition of sexual maturity in males of Potamotrygon magdalenae (Elasmobranchii: Potamotrygonidae).Crossref | GoogleScholarGoogle Scholar |

Dudgeon, C. L., Bennett, M. B., and Kyne, P. M. (2016). Grey carpetshark Chiloscyllium punctatum. In ‘The IUCN Red List of Threatened Species’. e.T41872A68616745. (International Union for Conservation of Nature and Natural Resources.) Available at https://www.iucnredlist.org/species/41872/68616745 [Verified 9 February 2021].

Fischer, J., Erikstein, K., D’Offay, B., Barone, M., and Guggisberg, S. (2012). Review of the implementation of the International Plan of Action for the Conservation and Management of Sharks. FAO Fisheries and Aquaculture Circular 1076, Food and Agriculture Organization of the United Nations, Rome, Italy.

Gelsleichter, J., Rasmussen, L. E. L., Manire, C. A., Tyminski, B., Chang, B., and Lombardi-Carlson, L. (2002). Serum steroid concentrations and development of reproductive organs during puberty in male bonnethead sharks, Sphyrna tiburo. Fish Physiology and Biochemistry 26, 389–401.
Serum steroid concentrations and development of reproductive organs during puberty in male bonnethead sharks, Sphyrna tiburo.Crossref | GoogleScholarGoogle Scholar |

Gračan, R., and Lackovic, G. (2016). Histological and morphological aspects of reproduction in male blackspotted smooth-hound Mustelus punctulatus in the Adriatic Sea (Eastern Mediterranean Sea). Journal of Marine Biology 2016, 1–6.
Histological and morphological aspects of reproduction in male blackspotted smooth-hound Mustelus punctulatus in the Adriatic Sea (Eastern Mediterranean Sea).Crossref | GoogleScholarGoogle Scholar |

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

Hamlett, W. C., Reardon, M., Clark, J., and Walker, T. I. (2002). Ultrastructure of sperm storage and male genital ducts in a male holocephalan, the elephant fish, Callorhynchus milii. The Journal of Experimental Zoology 292, 111–128.
Ultrastructure of sperm storage and male genital ducts in a male holocephalan, the elephant fish, Callorhynchus milii.Crossref | GoogleScholarGoogle Scholar | 11754028PubMed |

Harahush, B. K., Fischer, A. B. P., and Collin, S. P. (2007). Captive breeding and embryonic development of Chiloscyllium punctatum Muller and Henle, 1838 (Elasmobranchii: Hemiscyllidae). Fish Biology 71, 1007–1022.
Captive breeding and embryonic development of Chiloscyllium punctatum Muller and Henle, 1838 (Elasmobranchii: Hemiscyllidae).Crossref | GoogleScholarGoogle Scholar |

Henderson, C., Reeve, A. J., and Ambu-Ali, A. (2014). Microanatomy of the male and female reproductive tracts in the long-tailed butterfly ray Gymnura poecilura, an elasmobranch with unusual characteristics. Fish Biology 84, 297–313.
Microanatomy of the male and female reproductive tracts in the long-tailed butterfly ray Gymnura poecilura, an elasmobranch with unusual characteristics.Crossref | GoogleScholarGoogle Scholar |

Heupel, M. R., Whittier, J. M., and Bennett, M. B. (1999). Plasma steroid hormone profiles and reproductive biology of the Epaulette shark, Hemiscyllium ocellatum. The Journal of Experimental Zoology 284, 586–594.
Plasma steroid hormone profiles and reproductive biology of the Epaulette shark, Hemiscyllium ocellatum.Crossref | GoogleScholarGoogle Scholar | 10469996PubMed |

Hoese, D. F., Bray, D. J., Paxton, J. R., and Allen, G. R. (2006). Cheilodactylidae. In ‘Zoological Catalogue of Australia’. (Eds P. L. Beesley and A. Wells.) Volume 35, part 2, pp. 1355–1359. (ABRS: Canberra, ACT, Australia; and CSIRO Publishing: Melbourne, Vic., Australia.)

Hoffmayer, E. R., Driggers, W. B., Jones, L. M., Hendon, J. M., and Sulikowski, J. A. (2013). Variability in the Reproductive Biology of the Atlantic Sharpnose Shark in the Gulf of Mexico. Marine and Coastal Fisheries 5, 139–151.
Variability in the Reproductive Biology of the Atlantic Sharpnose Shark in the Gulf of Mexico.Crossref | GoogleScholarGoogle Scholar |

Holden, M. J., and Raitt, D. F. S. (1974). Manual of fisheries science part 2 – methods of resource investigation and their application. FAO Fisheries Technical Paper 115, rev. 1, Food and Agriculture Organization of the United Nations, Rome, Italy.

Last, P. R., and Stevens, J. D. (2009). ‘Sharks and Rays of Australia’, 2nd edn. (CSIRO Publishing: Melbourne, Vic., Australia.)

Lüpold, S., Linz, G. M., Rivers, J. W., Westneat, D. F., and Birkhead, T. R. (2009). Sperm competition selects beyond relative testes size in birds. Evolution 63, 391–402.
Sperm competition selects beyond relative testes size in birds.Crossref | GoogleScholarGoogle Scholar | 19215291PubMed |

Manire, C. A., and Rasmussen, L. E. L. (1997). Serum concentrations of steroid hormones in the mature male bonnethead shark, Sphyrna tiburo. General and Comparative Endocrinology 107, 414–420.
Serum concentrations of steroid hormones in the mature male bonnethead shark, Sphyrna tiburo.Crossref | GoogleScholarGoogle Scholar | 9268622PubMed |

Maruska, K. P., Cowie, E. G., and Tricas, T. C. (1996). Periodic gonadal activity and protracted mating in elasmobranch fishes. The Journal of Experimental Zoology 276, 219–232.
Periodic gonadal activity and protracted mating in elasmobranch fishes.Crossref | GoogleScholarGoogle Scholar |

Onimaru, K., Motone, F., Kiyatake, I., Nishida, K., and Kuraku, S. (2018). A staging table for the embryonic development of the brownbanded bamboo shark (Chiloscyllium punctatum). Developmental Dynamics 247, 712–723.
A staging table for the embryonic development of the brownbanded bamboo shark (Chiloscyllium punctatum).Crossref | GoogleScholarGoogle Scholar | 29396887PubMed |

Parsons, G. R., and Grier, H. J. (1992). Seasonal changes in shark testicular structure. The Journal of Experimental Zoology 261, 173–184.
Seasonal changes in shark testicular structure.Crossref | GoogleScholarGoogle Scholar |

Piercy, A. N., Gelsleichter, J. J., and Snelson, F. F. (2003). Morphological and histological changes in the genital ducts of the male Atlantic stingray, Hypanus sabinus, during the seasonal reproductive cycle. Fish Physiology and Biochemistry 29, 23–35.
Morphological and histological changes in the genital ducts of the male Atlantic stingray, Hypanus sabinus, during the seasonal reproductive cycle.Crossref | GoogleScholarGoogle Scholar |

Piercy, A. N., Murie, D. J., and Gelsleichter, J. J. (2016). Histological and morphological aspects of reproduction in the sandbar shark Carcharhinus plumbeus in the US south-eastern Atlantic Ocean and Gulf of Mexico. Journal of Fish Biology 88, 1708–1730.
Histological and morphological aspects of reproduction in the sandbar shark Carcharhinus plumbeus in the US south-eastern Atlantic Ocean and Gulf of Mexico.Crossref | GoogleScholarGoogle Scholar | 27021112PubMed |

Porforough, F., Salamat, N., and Movahedinia, A. (2018). Ovarian maturatıon stages in Arabian carpet shark, Chiloscyllium arabicum Gubanov, 1980 (Orectolobiformes, Hemiscylliidae) during spring and autumn in the Persian Gulf. International Journal of Aquatic Biology 6, 321–329.

Pratt, H. L. (1988). Elasmobranch gonad structure: a description and survey. Copeia 1988, 719–729.
Elasmobranch gonad structure: a description and survey.Crossref | GoogleScholarGoogle Scholar |

Pratt, H. L., and Tanaka, S. (1994). Sperm storage in male elasmobranchs: a description and survey. Journal of Morphology 219, 297–308.
Sperm storage in male elasmobranchs: a description and survey.Crossref | GoogleScholarGoogle Scholar | 8169955PubMed |

Prisco, M., Liguoro, A., D’Onghia, B., Ricchari, L., Andreuccetti, P., and Angelini, F. (2002). Fine structure of Leydig and Sertoli cells in the testis of immature and mature spotted ray Torpedo marmorata. Molecular Reproduction and Development 63, 192–201.
Fine structure of Leydig and Sertoli cells in the testis of immature and mature spotted ray Torpedo marmorata.Crossref | GoogleScholarGoogle Scholar |

Rinchard, J., Kestemont, P., Kühn, E., and Fostier, A. (1993). Seasonal changes in plasma levels of steroid hormones in an asynchronous fish the gudgeon Gobio gobio L.(Teleostei, Cyprinidae). General and Comparative Endocrinology 92, 168–178.
Seasonal changes in plasma levels of steroid hormones in an asynchronous fish the gudgeon Gobio gobio L.(Teleostei, Cyprinidae).Crossref | GoogleScholarGoogle Scholar | 8282168PubMed |

Roff, D. A. (1983). An allocation model of growth and reproduction in fish. Canadian Journal of Fisheries and Aquatic Sciences 40, 1395–1404.
An allocation model of growth and reproduction in fish.Crossref | GoogleScholarGoogle Scholar |

Sourdaine, P., and Garnier, D. H. (1993). Stage-dependent modulation of Sertoli cell steroid production in dogfish (Scyliorhinus canicula). Journal of Reproduction and Fertility 97, 133–142.
Stage-dependent modulation of Sertoli cell steroid production in dogfish (Scyliorhinus canicula).Crossref | GoogleScholarGoogle Scholar | 8385221PubMed |

Tricas, T. C., Maruska, K. P., and Rasmussen, L. E. L. (2000). Annual cycles of steroid hormone production, gonad development, and reproductive behavior in the Atlantic stingray. General and Comparative Endocrinology 118, 209–225.
Annual cycles of steroid hormone production, gonad development, and reproductive behavior in the Atlantic stingray.Crossref | GoogleScholarGoogle Scholar | 10890563PubMed |

Walker, T. I. (2005). Reproduction in fisheries science. In ‘Reproductive Biology and Phylogeny of Chondrichthyes: Shark, Batoids and Chimaeras’. (Ed. W. C. Hamlett. ) pp. 81–127. (Science Publishers: Enfield, NH, USA.)

Wyffels, J. T., George, R., Adams, L., Adams, C., Clauss, T., Newton, A., Hyatt, M. W., Yach, C., and Penfold, L. M. (2020). Testosterone and semen seasonality for the sand tiger shark Carcharias taurus. Biology of Reproduction 102, 876–887.
Testosterone and semen seasonality for the sand tiger shark Carcharias taurus.Crossref | GoogleScholarGoogle Scholar | 31836894PubMed |