Abstract
Observations of synchronous rapid growth of embryos and ovarian follicles in pregnant females during the half-year December–May leading to parturition, ovulation, mating, and fertilization suggest Urolophus cruciatus has the capacity for an annual reproductive cycle. Conversely, the higher proportion of the pregnant females in the population carrying eggs than carrying embryos in utero during December–May and all pregnant females in the population only carrying eggs in utero during June–November indicate a longer reproductive cycle. Analysis based on the usual assumptions implies that the species most likely exhibits a biennial cycle with ~18-month period of diapause following ovulation prior to ~6-month period of rapid embryogenesis. However, it is feasible that the period of the cycle is triennial with ~30-month period of diapause or alternatively diapause varies among individuals and varies from year to year. Rather than exhibiting a fixed-term reproductive cycle where obligatory diapause leads to parturition timed every year to provide favourable conditions for neonates, as suggested for several other chondrichthyan species, U. cruciatus may exhibit facultative diapause where the period of diapause and hence the reproductive cycle varies depending on the prevailing environmental conditions or density-dependent factors as described for many terrestrial species. U. cruciatus is highly matrotrophic (>4000 % wet mass gain from ovum to full-term embryo), litter size (1–4) increases with maternal length, sex ratio among embryos is 1:1, and male breeding condition varies seasonally with peak sperm production coinciding with female ovulation.
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References
Beauchamp JJ, Olson JS (1973) Corrections for bias in regression estimates after logarithmic transformation. Ecology 54:1403–1407. doi:10.2307/1934208
Braccini JM, Gillanders BM, Walker TI (2006) Determining reproductive parameters for population assessments of chondrichthyan species with asynchronous ovulation and parturition: piked spurdog (Squalus megalops) as a case study. Mar Freshw Res 57:105–119. doi:10.1071/MF05076
Driggers WB, Hoffmayer ER (2009) Variability in the reproductive cycle of finetooth sharks, Carcharhinus isodon, in the northern gulf of Mexico. Copeia 2009:390–393. doi:10.1643/CE-08-167
Fahy DP, Spieler RE, Hamlett WC (2007) Preliminary observations on the reproductive cycle and uterine fecundity of the yellow stingray, Urobatis jamaicensis (Elasmobranchii: Myliobatiformes: Urolophidae) in southeast Florida, USA. Raffles Bull Zool Supplement:131–139
Hanchet S (1988) Reproductive biology of Squalus acanthias from the east coast, South Island, New Zealand. N Z J Mar Freshw Res 22:537–549. doi:10.1080/00288330.1988.9516324
Huveneers C, Walker TI, Otway NM, Harcourt RG (2007) Reproductive synchrony of three sympatric species of wobbegong shark (genus Orectolobus) in New South Wales, Australia: reproductive parameter estimates necessary for population modelling. Mar Freshw Res 58:765–777. doi:10.1071/MF06187
Last PR, Stevens JD (2009) Sharks and rays of Australia. Second. CSIRO Publishing, Melbourne
Marshall LJ, White WT, Potter IC (2007) Reproductive biology and diet of the southern fiddler ray, Trygonorrhina fasciata (Batoidea: Rhinobatidae), an important trawl bycatch species. Mar Freshw Res 58:104–115. doi:10.1071/MF05165
Mead RA (1993) Embryonic diapause in vertebrates. J Exp Zool 266:629–641. doi:10.1002/jez.1402660611
Morris JA (1999) Aspects of the reproductive biology of the bluntnose stingray, Dasyatis say, in the Indian river lagoon system. Doctoral dissertation, University of Central Florida, Florida
Musick JA, Ellis JK (2005) Reproductive evolution of chondrichthyans. In: Hamlett William C (ed) Reproductive biology and phylogeny of chondrichthyes: sharks, batoids and chimaeras. Science Publishers, Plymouth, pp 45–79
Ramírez-Mosqueda E, Pérez-Jiménez JC, Mendoza-Carranza M (2012) Reproductive parameters of the southern stingray Dasyatis americana in southern gulf of Mexico. Lat Am J Aquat Res 40:335–344. doi:10.3856/vol40-issue2-fulltext-8
Renfree MB, Shaw G (2000) Diapause. Annu Rev Physiol 62:353–375. doi:10.1146/annurev.physiol.62.1.353
Rocha F, Gadig OBF (2013) Reproductive biology of the guitarfish Rhinobatos percellens (Chondrichthyes, Rhinobatidae) from the Sao Paulo Coast, Brazil, western South Atlantic Ocean. J Fish Biol 82:306–317. doi:10.1111/j.1095-8649.2012.03493.x
Simpfendorfer CA (1992) Reproductive strategy of the Australian sharpnose shark, Rhizoprionodon taylori (Elasmobranchii: carcharhinidae), from Cleveland Bay, northern Queensland. Mar Freshw Res 43:67–75. doi:10.1071/MF9920067
Snelson FF, Williams-Hooper Sherry E, Schmid Thomas H (1989) Biology of the bluntnose Stingray, Dasyatis sayi, in Florida coastal lagoons. Bull Mar Sci 45:15–25
Treloar MA (2001) The ecology and biology of Urolophus cruciatus and Urolophus expansus (Urolophidae) in south-eastern Australia. Deakin University, Warrnambool
Trinnie FI, Walker TI, Jones PL, Laurenson LJ (2009) Reproductive biology of the eastern shovelnose stingaree Trygonoptera imitata from south-eastern Australia. Mar Freshw Res 60:845. doi:10.1071/MF08165
Trinnie FI, Walker TI, Jones PL, Laurenson LJ (2012) Biennial reproductive cycle in an extensive matrotrophic viviparous batoid: the sandyback stingaree Urolophus bucculentus from south-eastern Australia. J Fish Biol 80:1267–1291. doi:10.1111/j.1095-8649.2012.03259.x
Trinnie FI, Walker TI, Jones PL, Laurenson LJ (2014a) Asynchrony and regional differences in the reproductive cycle of the greenback stingaree Urolophus viridis from south-eastern Australia. Environ Biol Fishes 98:425–441. doi:10.1007/s10641-014-0273-4
Trinnie FI, Walker TI, Jones PL, Laurenson LJ (2014b) Regional differences in the reproductive parameters of the sparsely-spotted stingaree, Urolophus paucimaculatus, from south-eastern Australia. Mar Freshw Res 65:943. doi:10.1071/MF13275
Walker TI (2005) Reproduction in fisheries science. In: Hamlett WC (ed) Reproductive Biology and phylogeny of chondrichthyes: sharks, rays and chimaeras. Science Publishers, Enfield, pp 81–127
Walker TI (2007) Spatial and temporal variation in the reproductive biology of gummy shark Mustelus antarcticus (Chondrichthyes: Triakidae) harvested off southern Australia. Mar Freshw Res 58:67–97. doi:10.1071/MF06074
Walker TI, Gason AS (2007) Shark and other chondrichthyan byproduct and bycatch estimation in the Southern and eastern scalefish and shark fishery. Final report to Fisheries Research and Development Corporation. Project No. 2001/007. Primary Industries Reseach Victoria, Queenscliff
Waltrick D, Awruch C, Simpfendorfer C (2012) Embryonic diapause in the elasmobranchs. Rev Fish Biol Fish 22:849–859. doi:10.1007/s11160-012-9267-5
Waltrick D, Jones SM, Simpfendorfer CA, Awruch CA (2014) Endocrine control of embryonic diapause in the Australian sharpnose shark Rhizoprionodon taylori. PLoS One. doi:10.1371/journal.pone.0101234
White WT, Potter IC (2005) Reproductive biology, size and age compositions and growth of the batoid Urolophus paucimaculatus, including comparisons with other species of the Urolophidae. Mar Freshw Res 56:101–110. doi:10.1071/MF04225
White WT, Platell ME, Potter IC (2001) Relationship between reproductive biology and age composition and growth in Urolophus lobatus (Batoidea: Urolophidae). Mar Biol 138:135–147. doi:10.1007/s002270000436
White WT, Hall NG, Potter IC (2002) Reproductive biology and growth during pre- and postnatal life of Trygonoptera personata and T. mucosa (Batoidea: Urolophidae). Mar Biol 140:699–712. doi:10.1007/s00227-001-0756-7
Yamaguchi A, Taniuchi T, Shimizu M (2000) Geographic variations in reproductive parameters of the starspotted dogfish, Mustelus manazo, from five localities in Japan and in Taiwan. Environ Biol Fishes 57:221–233. doi:10.1023/A:1007558324902
Acknowledgments
Professional fishermen and technical staff, students and volunteers at the Department of Primary Industries (DPI) Queenscliff Centre and the Victorian Marine Science Consortium are acknowledged for collection of specimens, and Anne Gason of DPI provided advice on statistical analyses and management of data.
Funding
This project was funded by an Australian Fisheries Research and Development Corporation grant (FRDC Project 2002/003) and a Deakin University PhD scholarship.
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Trinnie, F.I., Walker, T.I., Jones, P.L. et al. Reproductive cycle of Urolophus cruciatus in south-eastern Australia: Does the species exhibit obligate or facultative diapause?. Mar Biol 163, 226 (2016). https://doi.org/10.1007/s00227-016-2976-x
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DOI: https://doi.org/10.1007/s00227-016-2976-x