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Dental sexual dimorphism and morphology of Urotrygon microphthalmum

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Abstract

Dental sexual dimorphism has been described for different species of batoids, and it has been suggested that this differentiation is advantageous to reproduction in most cases. The aim of the present study was to investigate the morphology of the dentition in the ray Urotrygon microphthalmum using scanning electron microscopy. The present study brings a detailed description of morphological characteristics in males and females during ontogenetic development. Dental sexual dimorphism was observed both in maturing and mature males, while females maintain the same crushing shape dentition during all development stages. The teeth modification in males corresponds to the onset of maturation, which occurs when the animal reaches approximately 171.7 mm in total length, indicating that this morphological modification is closely related to mating behavior—grasp females during copulation thus ensuring body attachment and clasper insertion during swimming.

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References

  • Almeida Z, Nunes J, Costa C (2000) Presencia de Urotrygon microphthalmum (Elasmobranchii: Urolophidae) en aguas bajas de Maranhão (Brasil) y notas sobre su biología. Bol Investig Mar Costeras 29:67–72

    Google Scholar 

  • Belleggia M, Andrada N, Paglieri S, Cortés F, Massa AM, Figueroa DE, Bremec C (2016) Trophic ecology of yellownose skate Zearaja chilensis, a top predator in the south-western Atlantic Ocean. J Fish Biol 88:1070–1087

    Article  CAS  PubMed  Google Scholar 

  • Bigelow HB, Schroeder WC (1953) Fishes of the Western North Atlantic. Sawfishes, guitarfishes, skates and rays. Memoirs of the Sears Foundation for Marine Research, no. 1, part 2, pp 1–588

  • Boeseman M (1963) Notes on new or rare marine fishes from Surinam. Zool Med Leiden 38:295–301

    Google Scholar 

  • Cappetta H (1987) Chondrichthyes II. Mesozoic and Cenozoic Elasmobranchii. Gustav Fischer Verlag, New York, pp 1–193

    Google Scholar 

  • Carrier JC, Pratt HL Jr, Castro JI (2004) Elasmobranch reproduction. In: Carrier JC, Musick JA, Heithaus MR (eds) Biology of sharks and their relatives. CRC Press, Boca Raton, pp 269–286

    Chapter  Google Scholar 

  • Cervigón F, Alcalá A (1999) Los peces marinos de Venezuela, vol 5. Tiburones y Rayas, Fundación Museo del Mar

  • Delsman NC (1941) Résultats scientifiques des croisières du Navire-école Belge “Mercator”, vol. III, No. 3. Pisces. Mém Mus R Hist Nat Belg 2:47–82

    Google Scholar 

  • Dodd JM (1983) Reproduction in cartilaginous fishes (Chondrichthyes). In: Rankin JC, Pitcher TJ, Duggan RT (eds) Fish Physiol, vol 9. Academic Press, San Diego, pp 31–95

    Google Scholar 

  • Ellis JR, Shackley SE (1995) Ontogenic changes and sexual dimorphism in the head, mouth and teeth of the lesser spotted dogfish. J Fish Biol 47:155–164. doi:10.1111/j.1095-8649.1995.tb01881.x

    Article  Google Scholar 

  • Feduccia A, Slaughter BH (1974) Sexual dimorphism in skates (Rajidae) and its possible role in differential niche utilization. Evolution 28:164–168. doi:10.2307/2407249

    Article  Google Scholar 

  • Gadig OBF, Bezerra MA, Feitosa RD, Furtado-Neto MAA (2000) Ictiofauna marinha do Estado do Ceará, Brasil: I. Elasmobranchii. Arq Ciên Mar 33:127–132

    Google Scholar 

  • Gillis JA, Donoghue PCJ (2007) The homology and phylogeny of chondrichthyan tooth enameloid. J Morphol 268:33–49. doi:10.1002/jmor.10501

    Article  PubMed  Google Scholar 

  • Gravendeel R, Neer WV, Brinkhuizen D (2002) An identification key for dermal denticles of Rajidae from the North Sea. Int J Osteoarchaeol 12:420–441. doi:10.1002/oa.645

    Article  Google Scholar 

  • Gutteridge AN, Bennett MB (2014) Functional implications of ontogenetically and sexually dimorphic dentition in the eastern shovelnose ray, Aptychotrema rostrata. J Exp Biol 217:192–200. doi:10.1242/jeb.089326

    Article  PubMed  Google Scholar 

  • Hamlett WC, Kormanik G, Storrie M, Stevens B, Walker TI (2005) Chondrichthyan parity, lecithotrophy and matrotrophy. In: Jamieson BGM (ed) Reproductive biology and phylogeny of Chondrichthyes, vol 3. Reproductive biology and phylogeny of chondrichthyes. Sharks, batoids and chimaeras. Science Publishers, Enfield, pp 395–434

    Google Scholar 

  • Kajiura SM, Tricas TC (1996) Seasonal dynamics of dental sexual dimorphism in the Atlantic stingray Dasyatis sabina. J Exp Biol 199:2297–2306

    PubMed  Google Scholar 

  • 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 Fishes 58:23–31. doi:10.1023/A:1007667108362

    Article  Google Scholar 

  • Kemp NE (1999) Integumentary system and teeth. In: Hamlett WC (ed) Sharks, skates and rays: the biology of elasmobranch fishes. John Hopkins University Press, Baltimore, pp 43–68

    Google Scholar 

  • McCourt RM, Kerstitch AN (1980) Mating behavior and sexual dimorphism in dentition in the stingray Urolophus concentricus from the Gulf of California. Copeia. doi:10.2307/1444479

    Google Scholar 

  • McEachran JD (1977) Sexual dimorphism in skates (Rajidae). Evolution 31:218–220. doi:10.2307/2407559

    Article  Google Scholar 

  • McEachran JD, Carvalho MR (2000) Urotrygonidae. In: Carpenter KE (ed) The living marine resources of the Western Central Atlantic. Volume 1: Introduction, molluscs, crustaceans, hagfishes, sharks, batoid fishes, and chimaeras. FAO Species Identification Guide for Fishery Purposes and American Society of Ichthyologists and Herpetologists Special Publication No. 5. FAO, Rome, pp 572–574

  • Moss SA (1972) Tooth replacement and body growth rates in the smooth dogfish, Mustelus canis (Mitchill). Copeia 4:808–811

    Article  Google Scholar 

  • Moss SA (1977) Feeding mechanisms in sharks. Am Zool 17:355–364. doi:10.1093/icb/17.2.355

    Article  Google Scholar 

  • Motta PJ (2004) Prey capture behavior and feeding mechanics of elasmobranchs. In: Carrier J, Musick J, Heithaus M (eds) Biology of sharks and their relatives. CRC Press, Boca Raton, pp 165–202

    Chapter  Google Scholar 

  • Motta PJ, Huber DR (2012) Prey capture behavior and feeding mechanics of elasmobranchs. In: Carrier J, Musick J, Heithaus M (eds) Biology of sharks and their relatives, 3rd edn. CRC Press, Boca Raton, pp 153–209

    Chapter  Google Scholar 

  • Motta PJ, Wilga CD (2001) Advances in the study of feeding behaviors, mechanisms, and mechanics of sharks. Environ Biol Fishes 60:131–156. doi:10.1007/978-94-017-3245-1_10

    Article  Google Scholar 

  • Navia AF, Torres A, Mejía-Falla PA, Giraldo A (2011) Sexual, ontogenetic, temporal and spatial effects on the diet of Urotrygon rogersi (Elasmobranchii:Myliobatiformes). J Fish Biol 78:1213–1224

    Article  CAS  PubMed  Google Scholar 

  • Nordell SE (1994) Observations of the mating behavior and dentition of the round stingray, Urolophus halleri. Environ Biol Fishes 39:219–229. doi:10.1007/BF00005124

    Article  Google Scholar 

  • Rangel BS, Rodrigues S, Malavasi-Bruno E, Will SEA, Favaron PO, Amorim AF, Rici REG (2014a) 3-D aspects of the dentition in rays of genus: Atlantoraja, Rhinobatos and Zapteryx from Southeastern and South of Brazil. In: Méndez-Vilas A (ed) Microscopy: advances in scientific research and education. Microscopy book series—2014 edition. FORMATEX, Badajoz, pp 3–9

    Google Scholar 

  • Rangel BS, Rodrigues S, Favaron PO, Amorim AF, Rici REG (2014b) Structure and dental sexual dimorphism in Dasyatis hypostigma (Santos & Carvalho, 2004) (Myliobatiformes, Dasyatidae). In: Méndez-Vilas A (ed) Microscopy: advances in scientific research and education. Microscopy book series—2014 edition. FORMATEX, Badajoz, pp 89–94

    Google Scholar 

  • Reif WE (1982) Evolution of dermal skeleton and dentition in vertebrates. The odontode regulation theory. In: Hecht MK, Wallace B, Prance GT (eds) Evolutionary biology. Plenum Press, New York, pp 287–368. doi:10.1007/978-1-4615-6968-8_7

    Chapter  Google Scholar 

  • Rosa RS (2004) Urotrygon microphthalmum. In IUCN red list of threatened species, version 2013.1. www.iucnred-list.org. Accessed 29 Oct 2013

  • Santander-Neto J, Lessa R (2013) Hermaphroditic smalleyed roundray (Urotrygon microphthalmum) from north-eastern Brazil. Mar Biodivers Rec 6(e60):4p. doi:10.1017/S1755267213000353

    Google Scholar 

  • Santander-Neto J, Araújo MLG, Lessa RP (2016) Reproductive biology of Urotrygon microphthalmum (Batoidea: Urotrygonidae) from northeastern Brazil, Tropical West Atlantic. J Fish Biol. doi:10.1111/jfb.12951

    Google Scholar 

  • Springer S (1960) Natural history of the sandbar shark, Eulamia milberti. Fish Bull (Wash DC) 61:1–38

    Google Scholar 

  • Taniuchi T, Shimizu M (1993) Dental sexual dimorphism and food habits in the stingray Dasyatis akajei from Tokyo Bay, Japan. Nippon Suisan Gakk 59:53–60. doi:10.2331/suisan.59.53

    Article  Google Scholar 

  • Tricas TC (1980) Courtship and mating-related behaviors in myliobatid rays. Copeia 3:553–556. doi:10.2307/1444540

    Article  Google Scholar 

  • Underwood CJ, Johanson Z, Welten M, Metscher B, Rasch LJ, Fraser GJ, Smith MM (2015) Development and evolution of dentition pattern and tooth order in the skates and rays (Batoidea; Chondrichthyes). PLoS ONE 10(4):e0122553. doi:10.1371/journal.pone.0122553

    Article  PubMed  PubMed Central  Google Scholar 

  • Wilga CD, Motta PJ, Sanford CP (2007) Evolution and ecology of feeding in elasmobranchs. Integr Comp Biol 47:55–69. doi:10.1093/icb/icm029

    Article  PubMed  Google Scholar 

  • Yabumoto Y, Goto M, Yano K, Uyeno T (1997) Dentition of a female megamouth, Megachasma pelagios, collected from Hakata Bay, Japan. In: Yano K, Morrissey JF, Yabumoto Y, Nakaya K (eds) Biology of the megamouth shark. Tokai University Press, Tokai, pp 63–75

    Google Scholar 

Download references

Acknowledgments

We are grateful to the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for Scientific initiation scholarship, the Brazilian funding agency Fundação de Amparo à Ciência e Tecnologia do Estado de Pernambuco (FACEPE) for providing a Doctor of Science scholarship (IBPG-0934-2.04/10) to J.S.-N. and a research Grant was assigned by Conselho Nacional de Desenvolvimento Científico e Tecnológico_CNPq (Pq 303251/2010-7) to R.P.L. The authors would like to thank the anonymous reviewers. We also thank Natascha Wosnick for revising the manuscript.

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Authors and Affiliations

  1. Departamento de Cirurgia da Faculdade de Medicina Veterinária e Zootecnia da Universidade de São Paulo, Rua Professor Orlando Marques Paiva, s/n, São Paulo, SP, 05508-270, Brazil

    Bianca de Sousa Rangel & Rose Eli Grassi Rici

  2. Instituto Federal do Espírito Santo, Campus Piúma, Rua Augusto da Costa Oliveira, 660, Praia Doce, Piúma, Espírito Santo, CEP 29285-000, Brazil

    Jones Santander-Neto

  3. Programa de Pós-graduação em Biologia Animal, Universidade Federal de Pernambuco, Rua Prof. Moraes Rego, 1235, Cidade Universitária, Recife, CEP 50670-420, Brazil

    Jones Santander-Neto & Rosangela Lessa

  4. Laboratório de Dinâmica de Populações Marinhas—DIMAR, Departamento de Pesca e Aquicultura, Universidade Federal Rural de Pernambuco, Rua Dom Manuel de Medeiros s/n, Dois Irmãos, CEP 52171-900, Brazil

    Rosangela Lessa

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  1. Bianca de Sousa Rangel
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  2. Jones Santander-Neto
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Correspondence to Bianca de Sousa Rangel.

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Communicated by A. Schmidt-Rhaesa.

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de Sousa Rangel, B., Santander-Neto, J., Rici, R.E.G. et al. Dental sexual dimorphism and morphology of Urotrygon microphthalmum . Zoomorphology 135, 367–374 (2016). https://doi.org/10.1007/s00435-016-0312-0

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