Reproductive Biology of the stingray Hypanus marianae, an endemic species from Southwestern Tropical Atlantic Ocean


  • Ana Rita Onodera Palmeira Nunes Universidade Federal do Maranhão (UFMA)
  • Getulio Rincon
  • Ricardo de Souza Rosa
  • Jorge Luiz Silva Nunes


The Brazilian Large-eyed stingray Hypanus marianae is the smallest species of the family Dasyatidae in Brazil. This study aims to provide data on the reproductive biology of this species captured in artisanal fisheries. A total of 299 individuals of H. marianae were recorded at monitoring landings and adult male to female sex ratio was significantly different (1:2.9), showed spatial segregations between males and females. The range was from 13.0 to 36.2cm in disc width (DW). Females reached greater size and mass (36.2cm DW and 1855g) than males (29.3 cm DW and 915g). Its reproductive systems analyses were studied based on 81 preserved specimens. The DW50 parameter was estimated at 26.1cm DW for females, whereas for males was 23.8cm DW. Only the left uterus is functional, and birth size was estimated at between 13.0–14.0cm DW. Vitellogenesis occurred concurrently with a short gestation (shorter than 6 months) and uterine fecundity is only one embryo per reproductive cycle, which seems to be asynchronous.

Keywords. maturity, fecundity, birth, embryos, Dasyatidae.

Biografia do Autor

Ana Rita Onodera Palmeira Nunes, Universidade Federal do Maranhão (UFMA)

Departamento de Oceanografia e Limnologia, área de ecologia e conservação de elasmobrânquios


Aguiar AA, Valentin J, Rosa RS. Habitat use by Dasyatis americana in a south-western Atlantic oceanic island. 2009. Journal of the Marine Biological Association of the United Kingdom, 89 (6): 1147–1152.

Alcock AW. 1892. On utero-gestation in Trygon bleekeri. Ann Mag Nat Hist, 6 (9): 417–427. Apud Babel JS. 1967. Reproduction, life history and ecology of the round stingray, Urolophus halleri. Cooper. Fishery Bulletin, 137: 1-104.

Babel JS. 1967. Reproduction, life history and ecology of the round stingray, Urolophus halleri. Cooper. Fishery Bulletin, 137: 1-104.

Basílio TH, Faria VV, Furtado-Neto MAA. 2008. Elasmobranch fauna of the Curu River estuary, Ceará State, Brazil. Arquivos de Ciências do Mar, Fortaleza, 41(2): 65 – 72.

Bigelow HB and Schroeder WC. 1953. Fishes of the Western North Atlantic. Sawfishes, guitarfishes, skates and rays. p. 1-514. In: Tee-Van J, Breder CM, Hildebrand SF, Parr AE, Schroeder W (Eds.). Fishes of the Western North Atlantic. Part 2. New Haven: Sears Foundation for Marine Research.

Branco-Nunes ISL, Albuquerque FV, Nunes DM, Oliveira PGV, Hazin FHV. 2016. First record of predation between Dasyatis species. Journal of Fish Biology, 89: 2178-2181.

Branstetter S. 1990. Early life-history implications of selected carcharhinoid and lamnoid sharks of Northwest Atlantic. p: 17-28. In: Pratt, H. L., S. H. Gruber, T. Taniuchi (Eds.). Elasmobranchs as living resources: advances in the biology, ecology, systematics, and the status of the fisheries. Seatle, NOAA Technical Report NMFS 90, 518p.

Capapé C. 1993. New data on the reproductive biology of the thorny stingray, Dasyatis centroura (Pisces: Dasyatidae) from off the Tunisian coasts. Environmental Biology of Fishes, 38: 73-80. doi:10.1007/bf00842905

Capapé C and Zaouali J. 1995. Reproductive biology of the marbled stingray, Dasyatis marmorata (Steindachner, 1892) (Pisces: Dasyatidae) in Tunisian waters (Central Mediterranean). Journal of Aquariculture and Aquatic Sciences, 7: 108-119.

Carrier JC, Pratt HL, Castro JI. 2004. Reproductive Biology of Elasmobranchs. p. 269-285. In: Carrier JC, Musick JA, Heithaus MR, editors. Biology of sharks and their relatives. Boca Raton, FL: CRC Press. 596p.

Chapman DD, Corcorana MJ, Harveya GM, Malanb S, Shivjia MS. 2003. Mating behavior of southern stingrays, Dasyatis americana (Dasyatidae). Environmental Biology of Fishes, 68: 241–245. doi:10.1023/a:1027332113894

Conrath CR. Reproductive Biology. 2004. p. 133-164. In: Musick JA, Bonfil R (Eds.). Elasmobranchs Fisheries Management Techniques. Singapore: APEC Secretariat. 370p.

Cortés E. 2000. Life history patterns and correlations in sharks. Reviews in Fisheries Science, 8: 299–344.

Costa TLA, Thayer JA, Mendes LF. 2015. Population characteristics, habitat and diet of a recently discovered stingray Hypanus marianae: implications for conservation. Journal of Fish Biology, 86: 527–543.

Costa TLA, Pennino MG, Mendes LF. 2017. Identifying ecological barriers in marine environment: The case study of Dasyatis marianae. Marine Environmental Research, 125: 1-9.

Da Silva VEL, Teixeira EC, Fabré NN, Batista VS. 2018. Reproductive biology of the longnose stingray Hypanus guttatus (Bloch & Schneider, 1801) from the northeastern coast of Brazil. Cahiers de Biologie Marine, 59: 467-472. DOI: 10.21411/CBM.A.C4BC192C

Dulvy NK, Fowler SL, Musick JA, Canavah RD, Kyne PM, Harrison LR, et al. 2014. Extinction risk and conservation of the world’s sharks and rays. Elife, 3: e00590.

Ebert DA. 2002. Ontogenetic changes in the diet of the sevengill shark (Notorynchus cepedianus). Marine and Freshwater Research, 56: 1089–1098.

Ebert DA and Cowley PD. 2003. Diet, feeding behaviour and habitat utilization of the blue stingray Dasyatis chrysonota (Smith, 1828) in South African waters. Marine and Freshwater Research, 54: 957–965.

Gomes UL, Rosa RS, Gadig OBF. 2000. Dasyatis macrophthalma sp. n.: A new species of stingray (Chondrichthyes: Dasyatidae) from the Southwestern Atlantic. Copeia, 2: 510–515.[0510:DMSNAN]2.0.CO;2

Grubbs RD. 2010. Ontogenetic shifts in movements and habitat use. p. 319–350. .In: Carrier JC, Musick JA, Heithaus MR (Eds.). Sharks and Their Relatives, Vol.II. Boca Raton, FL: CRC Press. 746p.

Hamlett WC and Koob, TC. 1999. The female reproductive system. p. 398-443. In: Hamlett WC (Ed.). Sharks, skates and rays: the biology of elasmobranchs fishes. Baltimore: John Hopkins Press. 624p.

Hamlett WC, Kormanik GA, Storrie MT, Stevens B, Walker TI. 2005. Chondrichthyan parity, lecithotrophy and matrotrophy. p. 395–434. In: Hamlett WC (Ed.). Reproductive biology and phylogeny of chondrichthyes. Enfield (NH): Science Publishers Inc. 576p.

Henningsen A. 2000. Notes on reproduction in the southern stingray, Dasyatis americana (Chondrichthyes: Dasyatidae), in a captive environment. Copeia, 3: 826–828.[0826:NORITS]2.0.CO;2

Heupel MR, Carlson JK, Simpfendorfer CA. 2007. Shark nursery areas: concepts, definition, characterization and assumptions. Marine Ecology Progress Series, 337: 287–297.

Kajiura SM, Sebastian AP, Tricas TC. 2000. Dermal bite wounds as indicators of reproductive seasonality and behaviour in the Atlantic stingray, Dasyatis sabina. Environmental Biology of Fishes, 58: 23–31.

Kinney MJ and Simpfendorfer CA. 2009. Reassessing the value of nursery areas to shark conservation and management. Conservation Letters, 2: 53–60.

Klimley AP. 1987. The determinants of sexual segregation in the scalloped hammerhead shark, Sphyrna lewini. Environmental Biology of Fishes, 18 (1): 27-40. doi:10.1007/bf00002325

Last PR, Naylor GJP, Manjaji-Matsumoto BM. 2016. A revised classification of the family Dasyatidae (Chondrichthyes: Myliobatiformes) based on new morphological and molecular insights. Zootaxa, 4139 (3): 345–368.

Lutton BV, George J, Murrin CR, Fileti LA, Callard IP. 2005. The Elasmobranch Ovary. pp. 237–281. In: Hamlett WC (Ed.). Reproductive biology and phylogeny of Chondrichthyes. Enfield (NH): Science Publishers Inc. 576p.

Martin LK and Cailliet GM. 1988. Aspects of the reproduction of the bat ray, Myliobatis californica, in central California. Copeia, 3: 754–762. doi:10.2307/1445398

Martins APB, Heupel MR, Chin A, Simpfendorfer CA. 2018. Batoid nurseries: definition, use and importance. Marine Ecology Progress Series, 595: 253–267.

Maruska KP, Cowie EG, Tricas TC. 1996. Periodic gonadal activity and protracted mating in elasmobranch fishes. Journal of Experimental Zoology, 276 (3): 219-232. doi:10.1002/(sici)1097-010x(19961015)276:3<219::aid-jez6>;2-q

McEachran, JD, De Carvalho, MR. Dasyatidae. 2002. Dasyatidae. p. 562-571. In: Carpenter, KE (Ed.). The Living Marine Resources of the Western Central Atlantic. Vol. 1: Introduction, Molluscs, Crustaceans, Hagfishes, Sharks, Batoid Fishes and Chimaeras. FAO Species Identification Guide for Fisheries Purposes. Rome: Food and Agriculture Organization of the United Nations (FAO).

Mejía-Falla PA, Navia AF, Cortés E. 2012. Reproductive variables of Urotrygon rogersi (Batoidea: Urotrygonidae): a species with a triannual reproductive cycle in the Eastern Tropical Pacific Ocean. Journal of Fish Biology, 80: 1246-1266.

Mollet HF, Cliff G, Pratt HL, Stevens JD. 2000. Reproductive biology of the female shortfin mako, Isurus oxyrinchus Rafinesque, 1810, with comments on the embryonic development of lamnoids. Fishery Bulletin, 98: 299–318.

Motta FS, Moura RL, Francini-Filho RB, Namora RC. 2009. Notas sobre a biologia reprodutiva e alimentar de elasmobrânquios no Parque Estadual Marinho Parcel Manoel Luís, Maranhão – Brasil. Pan American Journal of Aquatic Sciences, 4 (4): 593-598.

Pratt HL and Carrier JC. 2005. Elasmobranch courtship and mating behaviour. p. 129–170. In: Hamlett WC (Ed.). Reproductive biology and phylogeny of Chondrichthyes. Enfield (NH): Science Publishers Inc. 576p.

Ramírez-Mosqueda E, Pérez-Jiménez JC, Mendoza-Carranza M. 2012. Reproductive parameters of the southern stingray Dasyatis americana in southern gulf of Mexico. Latin American Journal of Aquatic Research, 40(2): 335- 344. DOI: 10.3856/vol40-issue2-fulltext-8

Ranzi S. 1934. Le basi fisio-morfologische dello sviluppo embrionale dei Selaci - Parti II e III. Pubblicazioni della Stazione Zoologica di Napoli, 13: 331-437. Apud Wourms JP. 1977. Reproduction and Development in Chondrichthyan Fishes. American Zoologist, 17 (2): 379-410.

Reed JK and Gilmore RG. 1981. Inshore occurrence and nuptial behavior of the roughtail stingray, Dasyatis centroura (Dasyatidae), on the continental shelf, East Central Florida. Northeast Gulf Science, 5 (1); 59-62.

Rosa, R. & Furtado, M. 2016. Hypanus marianae. The IUCN Red List of Threatened Species 2016: e.T45925A104128768. Downloaded on 29 July 2019.

Rosa RS, Gadig OBF. 2014. Conhecimento da diversidade dos Chondrichthyes marinhos no Brasil: a contribuição de José Lima de Figueiredo. Arquivos de Zoologia, 45: 89-104.

Santos HRS, Gomes UL, Gadig OBF. 2006. The variation of colour pattern of the brazilian big-eyed stingray Hypanus marianae Gomes, Rosa & Gadig, 2000. (Myliobatiformes, Dasyatidae). Boletim do Museu Nacional, 522: 1-5.

Shibuya A and Rosa RS. 2011. Diet composition of Hypanus marianae (Elasmobranchii: Dasyatidae) of Paraíba state, Brazil. Arquivos de Ciências do Mar, 44(2): 89 – 92.

Smith DW, Cailliet GM, Melendez EM. 2007. Maturity and growth characteristics of a commercially exploited stingray, Dasyatis dipterura. Marine of Freshwater Research, 58: 54–66.

Snelson FF, Williams-Hooper SE, Schmid TH. 1988. Reproduction and ecology of the Atlantic stingray, Dasyatis sabina, in Florida coastal lagoons. Copeia: 729–739. 10.2307/1445395

Snelson FF, Williams-Hooper SE, Schmid TH. 1989. Biology of the bluntnose stingray, Dasyatis sayi, in Florida Coastal Lagoons. Bulletin of Marine Science, 45(1): 15-25.

Springer S. 1967. Social organization of sharks populations. p. 149-174. In: Gilbert PW, Matheson RF, Rall DP (Eds.). Sharks, Skates and Rays. Baltimore: John Hopkins Press. 624p.

Stevens JD, Bonfil R, Dulvy NK, Walker PA. 2000. The effects of fishing on sharks, rays, and chimaeras (Chondrichthyans), and the implications for marine ecosystems. ICES Journal of Marine Science, 57: 476–494. doi:10.1006/jmsc.2000.0724

Struhsaker P. 1969. Observations on the biology and distribution of the thorny stingray, Dasyatis centroura (Pisces: Dasyatidae). Bulletin of Marine Science, 19 (2): 456–481.

Thorson TB. 1983. Observations on the morphology, ecology and life history of the euryhaline stingray, Dasyatis guttata (Bloch and Schneider 1801). Acta Biologica Venezuelica, 11 (4): 95-125.

Véras DP, Branco ISL, Hazin FHV, Wor C, Tolotti MT. 2009. Preliminary analysis of the reproductive biology of pelagic stingray (Pteroplatytrygon violacea) in the Southwestern Atlantic. Collective Volume of Scientific Papers ICCAT, 64(5): 1755-1764. 10.1071/MF13008

Walker TI. 2005. Reproduction in Fisheries Science, p. 82–127. In: Hamlett WC (Ed.). Reproductive Biology and Phylogeny of Chondrichthyes: Sharks, Batoids and Chimaeras. Enfield, New Hampshire: Science Publishers Inc. 576p.

Wallman HL and Bennett WA. 2006. Effects of parturition and feeding on thermal preference of Atlantic stingray, Dasyatis sabina (Lesueur). Environmental Biology of Fishes, 75:259–267. doi:10.1007/s10641-006-0025-1

Wearmouth VJ, D.W. Sims DW. 2010. Sexual segregation in elasmobranchs. Biologia Marina Mediterranea, 17 (1): 236-239.

White WT, Platell ME, Potter IC. Relationship between reproductive biology and age composition and growth in Urolophus lobatus (Batoidea: Urolophidae). Marine Biology, 2001; 138: 135-147. doi:10.1007/s002270000436

White WT, 2007. Species and size compositions and reproductive biology of rays (Chondrichthyes, Batoidea) caught in target and non-target fisheries in eastern Indonesia. Journal of Fish Biology, 70: 1809–1837.

Wosnick N, Awruch CA, Adams KR, Gutierre SMM, Bornatowski H, Prado AC, Freire CA. 2018. Impacts of fisheries on elasmobranch reproduction: high rates of abortion and subsequent maternal mortality in the shortnose guitarfish. Animal Conservation. Print ISSN 1367-9430.

Wourms JP. 1977. Reproduction and Development in Chondrichthyan Fishes. American Zoologist, 17 (2): 379-410. doi:10.1093/icb/17.2.379

Wourms JP. 1981. Viviparity: the maternal-fetal relationship in fishes. American Zoologist, 21: 473–515. doi:10.1093/icb/21.2.473

Yokota L and Lessa RP. 2006. A nursery area for sharks and rays in northeastern Brazil. Environmental Biology of Fishes, 75, 349–360. doi:10.1007/s10641-006-0038-9

Yokota L and Lessa RP. 2007. Reproductive biology of three ray species: Gymnura micrura (Bloch & Schneider, 1801), Dasyatis guttata (Bloch & Schneider, 1801) and Hypanus marianae (Gomes, Rosa & Gadig, 2000), caught by artisanal fisheries in Northeastern Brazil. Cahiers de Biologie Marine, 48: 249-257.