Environmental Biology of Fishes

, Volume 101, Issue 12, pp 1693–1699 | Cite as

First observation on the mating behaviour of the marbled ray, Taeniurops meyeni, in the tropical Eastern Pacific

  • C. Arnés-UrgellésEmail author
  • E. M. Hoyos-Padilla
  • F. Pochet
  • P. Salinas-de-León


Elasmobranch reproductive behaviour remains understudied, particularly for batoids (rays). Most of the information available originates from opportunistic observations of mating scars in the wild and/or from individuals held in captivity. Here we describe the first complete mating sequence of the marbled ray (Taeniurops meyeni) in the wild. The event was filmed at Isla del Coco National Park in Costa Rica, in the Tropical Eastern Pacific. The complete sequence lasted approximately 3 hrs and is defined by the following behaviours: (1) close following or chasing: a group of males swim in a close formation chasing an individual female; (2) pre-copulatory biting: oral grasping of the female’s posterior pectoral fin by the males, with anterior bending of one clasper and rotation of the pelvic region towards the female’s cloaca; (3) copulation/ insertion of the male’s clasper followed by ‘ventral to ventral’ position and energetic thrusting of the male’s pelvic region; (4) post-copulatory behaviour: the male removes its clasper from the female’s cloaca while releasing her posterior pectoral fin and (5) separation: the male sets the female free and separates himself from the group. The mating behaviour described here shares some similarities with the few other studies of batoids in the wild and highlights the need to further understand their mating system to guide conservation plans for this vulnerable species.


Elasmobranch Batoids Reproduction Life-history Isla del coco 



We thank the Undersea Hunter Group for allowing us to use this underwater video footage for our analyses. We also thank Dr. Florencia Cerutti and the crew of M/V Argo for their helpful comments on this manuscript. We are grateful to the Helmsley Charitable Trust for their financial support. This publication is contribution number 2213 of the Charles Darwin Foundation for the Galapagos Islands. This research was approved by the Charles Darwin Research Station Ethics Committee.

Supplementary material

10641_2018_818_MOESM1_ESM.mp4 (77.4 mb)
ESM 1 (MP4 79,232 kb)


  1. Barbosa M, Magurran AE (2006) Female mating decisions: maximizing fitness? J Fish Biol 68:1636–1661CrossRefGoogle Scholar
  2. Byrne RJ, Avise JC (2012) Genetic mating system of the brown smoothhound shark (Mustelus henlei), including a literature review of multiple paternity in other elasmobranch species. Mar Biol 159:749–756CrossRefGoogle Scholar
  3. Carrier JC, Pratt HL Jr, Martin LK (1994) Group reproductive behaviors in free-living nurse sharks, Ginglymostoma cirratum. Copeia 1994:646–656CrossRefGoogle Scholar
  4. Chapman DD, Corcoran MJ, Harvey GM, Malan S, Shivji MS (2003) Mating behavior of southern stingrays, Dasyatis americana (Dasyatidae). Environ Biol Fish 68:241–245CrossRefGoogle Scholar
  5. Cortés-Núñez J (2008) Historia de la investigación marina de la Isla del Coco, Costa Rica. History of marine research at Cocos Island, Costa Rica. Rev Biol Trop 56:1–18Google Scholar
  6. Daly-Engel TS, Grubbs RD, Holland KN, Toonen RJ, Bowen BW (2006) Assessment of multiple paternity in single litters from three species of carcharhinid sharks in Hawaii. Environ Biol Fish 76:419–424CrossRefGoogle Scholar
  7. Daly-Engel TS, Grubbs RD, Bowen BW, Toonen RJ (2007) Frequency of multiple paternity in an unexploited tropical population of sandbar sharks (Carcharhinus plumbeus). Can J Fish Aquat Sci 64:198–204CrossRefGoogle Scholar
  8. Feldheim KA, Gruber SH, Ashley MV (2001) Multiple paternity of a lemon shark litter (Chondrichthyes: Carcharhinidae). Copeia 2001:781–786CrossRefGoogle Scholar
  9. Fitzpatrick JL, Kempster RM, Daly-Engel TS, Collin SP, Evans JP (2012) Assessing the potential for post-copulatory sexual selection in elasmobranchs. J Fish Biol 80:1141–1158CrossRefGoogle Scholar
  10. Friedlander AM, Zgliczynski BJ, Ballesteros E, Aburto-Oropeza O, Bolaños A, Sala E (2012) The shallow-water fish assemblage of Isla del coco National Park, Costa Rica: structure and patterns in an isolated, predator-dominated ecosystem. Rev Biol Trop 60:321–338Google Scholar
  11. Gómez LS, Mejía-Falla PA (2008) Aspectos pesqueros de los batoideos capturados artesanalmente en las localidades de Juanchaco y La Bocana, Pacífico colombiano Libro de resúmenes I Encuentro colombiano sobre condrictios 66Google Scholar
  12. Gordon I (1993) Pre-copulatory behaviour of captive sandtiger sharks, Carcharias taurus. The reproduction and development of sharks, skates, rays and ratfishes (pp. 159–164). Spring DorCrossRefGoogle Scholar
  13. Henningsen AD (2000) Notes on reproduction in the southern stingray, Dasyatis americana (Chondrichthyes: Dasyatidae), in a captive environment. Copeia 2000:826–828CrossRefGoogle Scholar
  14. Henningsen AD, Smale MJ, Gordon I, Garner R, Marin-Osorno RA, Kinnunen NI (2004) Captive breeding and sexual conflict in elasmobranchs. The Elasmobranch Husbandry Manual: Captive Care of Sharks, Rays and their Relatives.’(Eds M. Smith, D. Warmolts, D. Thorney and R. Heuter.) pp 237–248Google Scholar
  15. Jacoby DM, Busawon DS, Sims DW (2010) Sex and social networking: the influence of male presence on social structure of female shark groups. Behav Ecol 21:808–818CrossRefGoogle Scholar
  16. Johnson RH, Nelson DR (1978) Copulation and possible olfaction-mediated pair formation in two species of carcharhinid sharks. Copeia 1978:539–542CrossRefGoogle Scholar
  17. Kajiura SM, Sebastian AP, Tricas TC (2000) Dermal bite wounds as indicators of reproductive seasonality and behaviour in the Atlantic stingray, Dasyatis sabina. Environ Biol Fish 58:23–31CrossRefGoogle Scholar
  18. Klimley AP (1980) Observations of courtship and copulation in the nurse shark, Ginglymostoma cirratum. Copeia 1980:878Google Scholar
  19. Kyne PM, White WT (2015) Taeniurops meyeni. The IUCN red list of threatened species 2015: e.T60162A68646736.
  20. Last P, Naylor G, Séret B, White W, de Carvalho M, Stehmann M, eds (2016) Rays of the world. Csiro PubGoogle Scholar
  21. Le Port A, Lavery S, Montgomery JC (2012) Conservation of coastal stingrays: seasonal abundance and population structure of the short-tailed stingray Dasyatis brevicaudata at a marine protected area. ICES J Mar Sci 69:1427–1435CrossRefGoogle Scholar
  22. Lucifora LO, Menni RC, Escalante AH (2002) Reproductive ecology and abundance of the sand tiger shark, Carcharias taurus, from the southwestern Atlantic. ICES J Mar Sci 59:553–561CrossRefGoogle Scholar
  23. Luer CA, Gilbert PW (1985) Mating behavior, egg deposition, incubation period, and hatching in the clearnose skate, Raja eglanteria. Environ Biol Fish 13:161–171CrossRefGoogle Scholar
  24. Lyons K, Chabot CL, Mull CG, Paterson Holder CN, Lowe CG (2017) Who's my daddy? Considerations for the influence of sexual selection on multiple paternity in elasmobranch mating systems. Ecol Evol 7:5603–5612CrossRefGoogle Scholar
  25. McCosker JE, Rosenblatt RH (2010) The fishes of the Galápagos Archipelago: An update 1. Proc Calif Acad Sci 61:167Google Scholar
  26. 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. J Fish Biol 80:1246–1266CrossRefGoogle Scholar
  27. Mull CG, Lowe CG, Young KA (2010) Seasonal reproduction of female round stingrays (Urobatis halleri): steroid hormone profiles and assessing reproductive state. Gen Comp Endocrinol 166:379–387CrossRefGoogle Scholar
  28. Nordell SE (1994) Observations of the mating behavior and dentition of the round stingray, Urolophus halleri. Environ Biol Fish 39:219–229CrossRefGoogle Scholar
  29. Oliver S, Braccini M, Newman SJ, Harvey ES (2015) Global patterns in the bycatch of sharks and rays. Mar Pol 54:86–97CrossRefGoogle Scholar
  30. Pierce SJ, Pardo SA, Bennett MB (2009) Reproduction of the blue-spotted maskray Neotrygon kuhlii (Myliobatoidei: Dasyatidae) in south-East Queensland, Australia. J Fish Biol 74:1291–1308CrossRefGoogle Scholar
  31. Pratt HL, Carrier JC (2001) A review of elasmobranch reproductive behavior with a case study on the nurse shark, Ginglymostoma cirratum. Environ Biol Fish 60:157–188CrossRefGoogle Scholar
  32. Pratt HL, Tanaka S (1994) Sperm storage in male elasmobranchs: a description and survey. J Morphol 219:297–308CrossRefGoogle Scholar
  33. Salinas-de-León P, Acuña-Marrero D, Rastoin E, Friedlander AM, Donovan MK, Sala E (2016) Correction: largest global shark biomass found in the northern Galápagos Islands of Darwin and wolf. PeerJ 4:e1911CrossRefGoogle Scholar
  34. Salinas-de-León P, Bertolotti A, Chong-Montenegro C, Gomes-Do-Régo M, Preziosi RF (2017a) Reproductive biology of the endangered white-spotted sand bass Paralabrax albomaculatus endemic to the Galapagos Islands. Endanger Species Res 34:301–309CrossRefGoogle Scholar
  35. Salinas-de-León P, Hoyos-Padilla EM, Pochet F (2017b) First observation on the mating behaviour of the endangered scalloped hammerhead shark Sphyrna lewini in the tropical eastern Pacific. Environ Biol Fish 100:1603–1608CrossRefGoogle Scholar
  36. Sibaja-Cordero JA (2008) Tendencias espacio-temporales de los avistamientos de fauna marina en los buceos turísticos (Isla del Coco, Costa Rica). Rev Biol Trop 56:113–132Google Scholar
  37. Smith WD, Bizzarro JJ, Cailliet GM (2009) The artisanal elasmobranch fishery on the east coast of Baja California, Mexico: characteristics and management considerations. Cienc Mar 35:209–236CrossRefGoogle Scholar
  38. Spalding MD, Fox HE, Allen GR, Davidson N, Ferdana ZA, Finlayson MAX, Halpern BS, Jorge MA, Lombana AL, Lourie SA, Martin KD (2007) Marine ecoregions of the world: a bioregionalization of coastal and shelf areas. BioSci 57:573–583CrossRefGoogle Scholar
  39. Stobutzki IC, Miller MJ, Heales DS, Brewer DT (2002) Sustainability of elasmobranchs caught as bycatch in a tropical prawn (shrimp) trawl fishery. Fish Bull 100:800–821Google Scholar
  40. Tricas TC (1980) Courtship and mating-related behaviors in myliobatid rays. Copeia 1980:553–556CrossRefGoogle Scholar
  41. Tricas TC, Le Feuvre EM (1985) Mating in the reef white-tip shark Triaenodon obesus. Mar Biol 84:233–237CrossRefGoogle Scholar
  42. Tricas TC, Maruska KP, Rasmussen LE (2000) Annual cycles of steroid hormone production, gonad development, and reproductive behavior in the Atlantic stingray. Gen Comp Endocrinol 118:209–225CrossRefGoogle Scholar
  43. Usseglio P, Friedlander AM, DeMartini EE, Schuhbauer A, Schemmel E, de Léon PS (2015) Improved estimates of age, growth and reproduction for the regionally endemic Galapagos sailfin grouper Mycteroperca olfax (Jenyns, 1840). PeerJ e1270:3Google Scholar
  44. Wang G, Cai W, Gan B, Wu L, Santoso A, Lin X, Chen Z, McPhaden MJ (2017) Continued increase of extreme El Niño frequency long after 1.5° C warming stabilization. Nat Clim Chang 7:p568, 568, 572CrossRefGoogle Scholar
  45. Wearmouth VJ, Sims DW (2008) Sexual segregation in marine fish, reptiles, birds and mammals: behaviour patterns, mechanisms and conservation implications. Adv Mar Biol 54:107–170CrossRefGoogle Scholar
  46. White ER, Myers MC, Flemming JM, Baum JK (2015) Shifting elasmobranch community assemblage at Cocos Island—an isolated marine protected area. Conserv Biol 29:1186–1197CrossRefGoogle Scholar
  47. Whitney NM, Pratt HL Jr, Carrier JC (2004) Group courtship, mating behaviour and siphon sac function in the whitetip reef shark, Triaenodon obesus. Anim Behav 68:1435–1442CrossRefGoogle Scholar
  48. Worm B, Davis B, Kettemer L, Ward-Paige CA, Chapman D, Heithaus MR, Kessel ST, Gruber SH (2013) Global catches, exploitation rates, and rebuilding options for sharks. Mar Pol 40:194–204CrossRefGoogle Scholar
  49. Yano K, Sato F, Takahashi T (1999) Observations of mating behavior of the manta ray, Manta birostris, at the Ogasawara Islands, Japan. Ichthyol Res 46:289–296CrossRefGoogle Scholar
  50. Young RF (1993) Observation of the mating behaviour of the yellow stingray, Urolophus jamaicensis. Copeia 1993(3):879–880CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  • C. Arnés-Urgellés
    • 1
    Email author
  • E. M. Hoyos-Padilla
    • 2
    • 3
  • F. Pochet
    • 4
  • P. Salinas-de-León
    • 1
    • 5
  1. 1.Charles Darwin Research Station, Charles Darwin FoundationGalapagosEcuador
  2. 2.Pelagios KakunjáLa PazMexico
  3. 3.Fins Attached: Marine Research and ConservationColorado SpringsUSA
  4. 4.Undersea Hunter GroupSan JoseCosta Rica
  5. 5.Pristine Seas, National Geographic SocietyWashingtonUSA

Personalised recommendations