Reproductive strategy of the Pacific cownose ray Rhinoptera steindachneri in the southern Gulf of California
María I. Burgos-Vázquez A E , Valeria E. Chávez-García A B , Víctor H. Cruz-Escalona A , Andrés F. Navia C and Paola A. Mejía-Falla C D
+ Author Affiliations
- Author Affiliations
A Instituto Politécnico Nacional, Centro Interdisciplinario de Ciencias Marinas, Av. Instituto Politécnico Nacional s/n Col, Playa Palo de Santa Rita Apdo, Postal 592, Código Postal 23096, La Paz, BCS, México.
B Universidad del Mar, Ciudad Universitaria, Puerto Ángel, Distrito de San Pedro Pochutla, Código Postal 70902, Oaxaca, México.
C Fundación colombiana para la investigación y conservación de tiburones y rayas, SQUALUS, Calle 10A #72-35, Cali, Colombia.
D Wildlife Conservation Society, Avenida 5N #22N-11, Cali, Colombia.
E Corresponding author. Email: itzigueri@gmail.com
Marine and Freshwater Research 70(1) 93-106 https://doi.org/10.1071/MF18096
Submitted: 13 March 2018 Accepted: 20 May 2018 Published: 27 August 2018
Abstract
Rhinoptera steindachneri is one of the most common batoid species in the artisanal gill net fishery of the Gulf of California. In this study we investigated its reproductive biology based on 317 specimens caught in Bahía de la Paz, Mexico. Females measured up to 94.2-cm disc width (DW) and males reached 82.5 cm DW; there were no significant differences in size or weight between sexes. The median size at maturity was estimated at 68.5 cm DW for males and 71.8 cm DW for females, and the median size at pregnancy was 84.3 cm DW. Only the left ovary and uterus were functional; a maximum of six preovulatory vitellogenic follicles per female was recorded, although uterine fecundity was one embryo per female. Ovulation and birth occurred in May, June and July, with birth sizes ranging from 38.1 to 42 cm DW. R. steindachneri in Bahía de la Paz exhibited low fecundity, large size at maturity and birth and a continuous and synchronous annual reproductive cycle.
Additional keywords: batoids, birth size, fecundity, life history, Myliobatiformes, size at maturity.
References
Alkusairy, H., Ali, M., Saad, A., Reynaud, C., and Capape, C. (2014). Maturity, reproductive cycle, and fecundity of spiny butterfly ray, Gymnura altavela (Elasmobranchii: Rajiformes: Gymnuridae), from the coast of Syria (eastern Mediterranean). Acta Ichthyologica et Piscatoria 44, 229–240.| Maturity, reproductive cycle, and fecundity of spiny butterfly ray, Gymnura altavela (Elasmobranchii: Rajiformes: Gymnuridae), from the coast of Syria (eastern Mediterranean).Crossref | GoogleScholarGoogle Scholar |
Bernal, D., Carlson, J. K., Goldman, K. J., and Lowe, C. G. (2012). Energetics, metabolism, and endothermy in sharks and rays. In ‘Biology of Sharks and Their Relatives’, 2nd edn. (Eds J. C. Carrier, J. A. Musick, and M. R. Heithaus.) pp. 211–237. (CRC Press: Boca Raton, FL, USA.)
Bizzarro, J. B., Smith, W. D., Márquez-Farias, J. F., and Hueter, R. E. (2007). Artisanal fisheries and reproductive biology of the golden cownose ray, Rhinoptera steindachneri Evermann and Jenkins, 1891, in the northern Mexican Pacific. Fisheries Research 84, 137–146.
| Artisanal fisheries and reproductive biology of the golden cownose ray, Rhinoptera steindachneri Evermann and Jenkins, 1891, in the northern Mexican Pacific.Crossref | GoogleScholarGoogle Scholar |
Brown, J. H., Allen, A. P., and Gillooly, J. F. (2007). The metabolic theory of ecology and the role of body size in marine and freshwater ecosystems. In ‘Body Size: the Structure and Function of Aquatic Ecosystems’. (Eds A. G. Hildrew, D. G. Raffaelli, and R. Edmonds-Brown.). pp. 1–15. (Cambridge University Press: Cambridge, UK.)
Burgos-Vázquez, M. I., Mejía-Falla, P. A., Cruz-Escalona, V. H., and Brown-Peterson, N. J. (2017). Reproductive strategy of the giant electric ray in the southern gulf of California. Marine and Coastal Fisheries 9, 577–596.
| Reproductive strategy of the giant electric ray in the southern gulf of California.Crossref | GoogleScholarGoogle Scholar |
Capapé, C., Zaouali, J., Tomasini, J. A., and Bouchereau, J. L. (1992). Reproductive biology of the spiny butterfly ray, Gymnura altavela (Linnaeus, 1758) (Pisces: Gymnuridae) from off the Tunisian coasts. Scientia Marina 56, 347–355.
Colonello, J. H., Christiansen, H. E., Cousseau, M. B., and Macchi, G. J. (2013). Uterine dynamics of the southern eagle ray Myliobatis goodei (Chondrichthyes: myliobatidae) from the southwest Atlantic Ocean. Italian Journal of Zoology 80, 187–194.
| Uterine dynamics of the southern eagle ray Myliobatis goodei (Chondrichthyes: myliobatidae) from the southwest Atlantic Ocean.Crossref | GoogleScholarGoogle Scholar |
Conrath, C. L., and Musick, J. A. (2012). Reproductive biology of elasmobranchs. In ‘Biology of Sharks and Their Relatives’, 2nd edn. (Eds J. C. Carrier, J. A. Musick, and M. R. Heithaus.) pp. 291–311. (CRC Press: Boca Raton, FL, USA.)
Cortés, E. (2000). Life history patterns and correlations in sharks. Reviews in Fisheries Science 8, 299–344.
| Life history patterns and correlations in sharks.Crossref | GoogleScholarGoogle Scholar |
Flores-Pineda, P. A., Villavicencio-Garáyzar, C., and Tovar-Ávila, J. (2008). Biología reproductiva y evaluación de riesgo ecológico del gavilán dorado (Rhinoptera steindachneri Evermann y Jenkins 1891) en Bahía Almejas, Baja California Sur, México. In ‘III Simposium Nacional de Tiburones y Rayas’. (Eds A. Díaz Sánchez and C. Aguilar.) pp. 79–83. (Sociedad Mexicana de Peces Cartilaginosos (SOMEPEC)–Universidad Autónoma de México (UNAM)–Alianza WWF-TELCEL, Ciudad Universitaria: Ciudad de México, México.)
Frisk, M. G., Miller, T. J., and Fogarty, M. J. (2002). The population dynamics of little skate Leucoraja erinacea, winter skate Leucoraja ocellata, and barndoor skate Dipturus laevis: predicting exploitation limits using matrix analyses. ICES Journal of Marine Science 59, 576–586.
| The population dynamics of little skate Leucoraja erinacea, winter skate Leucoraja ocellata, and barndoor skate Dipturus laevis: predicting exploitation limits using matrix analyses.Crossref | GoogleScholarGoogle Scholar |
González-González, L del V. (2018). Diversidad de los peces batoideos de la zona sur de la Isla Espíritu Santo, BCS, México. M.Sc. Thesis, Centro Interdisciplinario de Ciencias Marinas del Instituto Politécnico Nacional, La Paz, México.
Hamlett, W. C., and Koob, T. J. (1999). Female reproductive system. In ‘Sharks, Skates and Rays: The Biology of Elasmobranch Fish’. (Ed. W. C. Hamlett.) pp 398–444. (Johns Hopkins University Press: Baltimore, MD, USA.)
Hamlett, W. C., Wourms, J. P., and Smith, J. W. (1985). Stingray placental analogues: structure of trophonemata in Rhinoptera bonasus. Journal of Submicroscopic Cytology 17, 541–550.
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 structure and function in elasmobranchs. The Journal of Experimental Zoology 282, 399–420.
| Survey of oviducal structure and function in elasmobranchs.Crossref | GoogleScholarGoogle Scholar |
Hamlett, W. C., Kormarik, C. G., Storrie, M., Serevy, B., and Walker, T. I. (2005). 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, USA.)
Hoening, J. M., and Gruber, S. H. (1990). Life-history patterns in the elasmobranchs: implications for fisheries management. In ‘Elasmobranchs as Living Resources: Advances in the Biology, Ecology, Systematics, and the Status of the Fisheries’. (Eds H. L. Pratt Jr, S. H. Gruber, and T. Taniuchi.) NOAA Technical Report NMFS 90, pp. 1–16. (NOAA/National Marine Fisheries Service: Seattle, WA, USA.)
Jacobsen, I. P., Johnson, J. W., and Bennett, M. B. (2009). Diet and reproduction in the Australian butterfly ray, Gymnura australis, from northern and north-eastern Australia. Journal of Fish Biology 75, 2475–2489.
| Diet and reproduction in the Australian butterfly ray, Gymnura australis, from northern and north-eastern Australia.Crossref | GoogleScholarGoogle Scholar |
King, J. R., and McFarlane, G. A. (2003). Marine fish life history strategies: applications to fishery management. Fisheries Management and Ecology 10, 249–264.
| Marine fish life history strategies: applications to fishery management.Crossref | GoogleScholarGoogle Scholar |
Lombardi-Carlson, L. A., Cortés, E., Parsons, G. R., and Manire, C. A. (2003). Latitudinal variation in life-history traits of bonnethead sharks, Sphyrna tiburo, (Carcharhiniformes, Sphyrnidae) from the eastern Gulf of Mexico. Marine and Freshwater Research 54, 875–883.
| Latitudinal variation in life-history traits of bonnethead sharks, Sphyrna tiburo, (Carcharhiniformes, Sphyrnidae) from the eastern Gulf of Mexico.Crossref | GoogleScholarGoogle Scholar |
Márquez-Farías, J. F. (2007). Reproductive biology of shovelnose guitarfish (Rhinobatos productus) from the eastern Gulf of California México. Marine Biology 151, 1445–1454.
| Reproductive biology of shovelnose guitarfish (Rhinobatos productus) from the eastern Gulf of California México.Crossref | GoogleScholarGoogle Scholar |
Martin, L. K., and Cailliet, G. M. (1988). Aspects of the reproduction of the Bat Ray, Myliobatis californica, in central California. Copeia 1988, 754–762.
| Aspects of the reproduction of the Bat Ray, Myliobatis californica, in central California.Crossref | GoogleScholarGoogle Scholar |
Mejía-Falla, P. A. (2012). Historia de vida y demografía de la raya espinosa Urotrygon rogersi en dos áreas con distintos niveles de presión pesquera. Ph.D. Thesis, Universidad del Valle, Cali, Colombia.
Mejía-Falla, P. A., Navia, A. F., and 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.
| Reproductive variables of Urotrygon rogersi (Batoidea: Urotrygonidae): a species with a triannual reproductive cycle in the Eastern Tropical Pacific Ocean.Crossref | GoogleScholarGoogle Scholar |
Møller, A. P. (1994). Directional selection on directional asymmetry: testes size and secondary sexual characters in birds. Proceedings. Biological Sciences 258, 147–151.
| Directional selection on directional asymmetry: testes size and secondary sexual characters in birds.Crossref | GoogleScholarGoogle Scholar |
Mollet, H. F., Cliff, G., Pratt, H. L., and Stevens, J. D. (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.
Musick, J. A., and Ellis, J. K. (2005). Reproductive evolution of Chondrichthyes. In ‘Reproductive Biology and Phylogeny of Chondrichthyes: Sharks, Batoids, and Chimaeras’. (Ed. W. C. Hamlett.) pp. 45–79. (Science Publishers, Inc.: Enfield NH, USA.)
Navarro-González, J. A., Bohórquez-Herrera, J., Navia, A. F., and Cruz-Escalona, V. H. (2012). Diet composition of batoids on the continental shelf off Nayarit and Sinaloa, Mexico. Ciencias Marinas 38, 347–362.
| Diet composition of batoids on the continental shelf off Nayarit and Sinaloa, Mexico.Crossref | GoogleScholarGoogle Scholar |
Neer, J. A., and Thompson, B. A. (2005). Life history of the cownose ray, Rhinoptera bonasus, in the northern Gulf of Mexico, with comments on geographic variability in life history traits. Environmental Biology of Fishes 73, 321–331.
| Life history of the cownose ray, Rhinoptera bonasus, in the northern Gulf of Mexico, with comments on geographic variability in life history traits.Crossref | GoogleScholarGoogle Scholar |
Pabón-Aldana, K. A. (2016). Edad y crecimiento de la raya tecolote, Rhinoptera steindachneri (Evermann & Jenkins, 1891) en la Bahía de La Paz, Baja California Sur, México. M.Sc. Thesis, Centro Interdisciplinario de Ciencias Marinas, La Paz, México.
Pérez-Jiménez, J. C. (2011). Reproductive biology of the cownose ray Rhinoptera bonasus (Elasmobranchii) in the Southeastern Gulf of Mexico. Hidrobiológica 21, 159–167.
Piner, K. R., Hamel, O. S., Menkel, J. L., Wallace, J. R., and Hutchinson, C. E. (2005). Age validation of canary rockfish (Sebastes pinniger) from off the Oregon coast (USA) using the bomb radiocarbon method. Canadian Journal of Fisheries and Aquatic Sciences 62, 1060–1066.
| Age validation of canary rockfish (Sebastes pinniger) from off the Oregon coast (USA) using the bomb radiocarbon method.Crossref | GoogleScholarGoogle Scholar |
Poulakis, G. R. (2013). Reproductive biology of the cownose ray in the Charlotte Harbor estuarine system, Florida. Marine and Coastal Fisheries 5, 159–173.
| Reproductive biology of the cownose ray in the Charlotte Harbor estuarine system, Florida.Crossref | GoogleScholarGoogle Scholar |
Poulakis, G. R., and Grier, H. J. (2014). Ontogenetic testicular development and spermatogenesis in rays: the cownose ray, Rhinoptera bonasus, as a model. Environmental Biology of Fishes 97, 1013–1029.
| Ontogenetic testicular development and spermatogenesis in rays: the cownose ray, Rhinoptera bonasus, as a model.Crossref | GoogleScholarGoogle Scholar |
Pratt, H. L. (1979). Reproduction of the blue shark, Prionace glauca. Fishery Bulletin 77, 445–470.
Robertson, D. R., and Allen, G. R. (2015). Peces Costeros del Pacífico Oriental Tropical: sistema de Información en línea. Versión 2.0 Instituto Smithsonian de Investigaciones Tropicales, Balboa, República de Panamá.
Romero‐Caicedo, A. F., and Carrera‐Fernández, M. (2015). Reproduction of the whitesnout guitarfish Rhinobatos leucorhynchus in the Ecuadorian Pacific Ocean. Journal of Fish Biology 87, 1434–1448.
| Reproduction of the whitesnout guitarfish Rhinobatos leucorhynchus in the Ecuadorian Pacific Ocean.Crossref | GoogleScholarGoogle Scholar |
Salinas-González, F., Zaytsev, O., and Vyacheslav, M. (2003). Formación de la estructura termohalina del agua en la Bahía de La Paz de verano a otoño. Ciencias Marinas 29, 51–65.
Schwartz, F. J. (1990). Mass migratory congregation and movements of several species of cownose rays, genus Rhinoptera: a worldwide review. Journal of the Elisha Mitchell Scientific Society 106, 10–13.
Smith, W. D., and Bizzarro, J. J. (2006). Rhinoptera steindachneri (golden cownose ray, hawkray, Pacific cownose ray). Available at http://www.iucnredlist.org/details/60130/0 [Verified 15 June 2018].
Smith, J. W., and Merriner, J. V. (1986). Observations on the reproductive biology of the cownose ray, Rhinoptera bonasus, in Chesapeake Bay. Fishery Bulletin 84, 871–877.
Smith, S. E., Au, D. W., and Show, C. (1998). Intrinsic rebound potential of 26 species of Pacific sharks. Marine and Freshwater Research 49, 663–678.
| Intrinsic rebound potential of 26 species of Pacific sharks.Crossref | GoogleScholarGoogle Scholar |
Smith, W. D., Cailliet, G. M., and Melendez, E. M. (2007). Maturity and growth characteristics of a commercially exploited stingray, Dasyatis dipterura. Marine and Freshwater Research 58, 54–66.
| Maturity and growth characteristics of a commercially exploited stingray, Dasyatis dipterura.Crossref | GoogleScholarGoogle Scholar |
Sokal, R. R., and Rohlf, F. J. (1998). ‘Biometry: The Principles and Practice of Statistics in Biological Research.’ (Freeman: New York, NY, USA.)
Trinnie, F. I., Walker, T. I., Jones, P. L., and Laurenson, L. J. (2015). Asynchrony and regional differences in the reproductive cycle of the greenback stingaree Urolophus viridis from south-eastern Australia. Environmental Biology of Fishes 98, 425–441.
| Asynchrony and regional differences in the reproductive cycle of the greenback stingaree Urolophus viridis from south-eastern Australia.Crossref | GoogleScholarGoogle Scholar |
Villavicencio-Garáyzar, G. C. (1993). Biología reproductiva de Rhinobatos productos (Pisces: Rhinobatidae), en Bahía Almejas, Baja California Sur, México. Revista de Biología Tropical 41, 777–782.
Villavicencio-Garáyzar, C. J. (1996). Reproductive biology of the Pacific cownose, Rhinoptera steindachneri, in Baja California, México. In ‘Proceedings of the American Elasmobranch Society 12th Annual Meeting’, 13–19 June 1996, New Orleans, LA, USA. (Ed. S. A. Moss.) Abstract. (American Elasmobranch Society.)
Villavicencio-Garáyzar, C. J. V., Hoffman, C. D., and Melendez, E. M. (1994). Tamaño y reproducción de la raya Dasyatis longus (Pisces: Dasyatidae), en Bahía Almejas, Baja California Sur, México. Revista de Biología Tropical 42, 375–377.
Villavicencio-Garáyzar, C. J. (2000). Áreas de crianza de tiburones en el Golfo de California. Universidad Autónoma de Baja California Sur Área Interdisciplinaria de Ciencias del Mar Informe final SNIBCONABIO proyecto L054, pp. 1–121, Mexico City, México.
Walker, T. I. (2005). Reproduction in fisheries science. In ‘Reproductive Biology and Phylogeny of Chondrichthyes: Sharks, Batoids, and Chimaeras’. (Ed. W. C. Hamlett.) pp. 81–127. (Science Publishers: Enfield, NH, USA).
Walker, T. I. (2007). Spatial and temporal variation in the reproductive biology of gummy shark Mustelus antarcticus (Chondrichthyes: Triakidae) harvested off southern Australia. Marine and Freshwater Research 58, 67–97.
| Spatial and temporal variation in the reproductive biology of gummy shark Mustelus antarcticus (Chondrichthyes: Triakidae) harvested off southern Australia.Crossref | GoogleScholarGoogle Scholar |
White, W. T., and Potter, I. C. (2005). Reproductive biology, size and age compositions and growth of the batoid Urolophus paucimaculatus, including comparisons with other species of the Urolophidae. Marine and Freshwater Research 56, 101–110.
| Reproductive biology, size and age compositions and growth of the batoid Urolophus paucimaculatus, including comparisons with other species of the Urolophidae.Crossref | GoogleScholarGoogle Scholar |
Wourms, J. P. (1977). Reproduction and development in Chondrichthyan fishes. American Zoologist 17, 379–410.
| Reproduction and development in Chondrichthyan fishes.Crossref | GoogleScholarGoogle Scholar |
Wourms, J. P., and Lombardi, J. (1992). Reflections on the evolution of piscine viviparity. American Zoologist 32, 276–293.
| Reflections on the evolution of piscine viviparity.Crossref | GoogleScholarGoogle Scholar |
Yamaguchi, A., Taniuchi, T., and Shimizu, M. (2000). Geographic variations in reproductive parameters of the starspotted dogfish, Mustelus manazo, from five localities in Japan and in Taiwan. Environmental Biology of Fishes 57, 221–233.
| Geographic variations in reproductive parameters of the starspotted dogfish, Mustelus manazo, from five localities in Japan and in Taiwan.Crossref | GoogleScholarGoogle Scholar |
Yokota, L., Goitein, R., Gianeti, M. D., and Lessa, R. T. P. (2012). Reproductive biology of the smooth butterfly ray Gymnura micrura. Journal of Fish Biology 81, 1315–1326.
| Reproductive biology of the smooth butterfly ray Gymnura micrura.Crossref | GoogleScholarGoogle Scholar |
Zaitsev, O., Sánchez-Montante, O., and Saldivar-Reyes, M. (2010). Seasonal variations of the thermohaline structure in the Magdalena–Almejas Bay lagoon system and adjacent sea. Ciencias Marinas 36, 413–432.
| Seasonal variations of the thermohaline structure in the Magdalena–Almejas Bay lagoon system and adjacent sea.Crossref | GoogleScholarGoogle Scholar |
