Environmental Biology of Fishes

, Volume 101, Issue 1, pp 137–151 | Cite as

Age and growth assessment of western North Atlantic spiny butterfly ray Gymnura altavela (L. 1758) using computed tomography of vertebral centra

  • K. T. Parsons
  • J. Maisano
  • J. Gregg
  • C. F. Cotton
  • R. J. Latour
Article

Abstract

Life history strategies of batoid fishes have evolved within dynamic marine ecosystems. Adaptations in reproductive and developmental biology are paramount to the survival of species, and therefore knowledge of growth rates to maturity is fundamental for identifying constraints on the conservation of populations. The butterfly rays (Myliobatiformes: Gymnuridae) are highly derived batoids with generally low reproductive potentials for which age and growth information remains unknown. In this study we applied high-resolution X-ray computed tomography (HRXCT) to vertebral centra from a stingray for the first time to estimate age, and used a multimodel approach to investigate growth of spiny butterfly ray, Gymnura altavela. Estimated ages of the oldest male and female were 11 and 18 yrs. at disk widths (WD) 1355 mm and 2150 mm, respectively. Disk width-at-age data were analyzed using three growth models (von Bertalanffy, logistic, Gompertz), and the most parsimonious and empirically supported model was the logistic function with sex treated as a fixed effect on asymptotic disk width (WD ) and k parameters. Model parameter estimates were (males) WD  = 1285.46 ± 67.27 mm, k = 0.60 ± 0.10, and (females) WD  = 2173.51 ± 129.78 mm, k = 0.27 ± 0.04. Results indicated sexually dimorphic growth patterns, with males growing faster and reaching asymptotic size at earlier ages than females. These age and growth results are the first reported for the genus, and suggest that G. altavela grows at a similar rate as some teleosts and batoids, and relatively fast among chondrichthyans.

Keywords

Myliobatiformes Gymnuridae HRXCT Growth coefficient Logistic growth model 

Notes

Acknowledgements

We thank the staff of the Virginia Institute of Marine Science (VIMS) Survey Programs (ChesMMAP, NEAMAP, VASMAP, Juvenile Fish and Blue Crab Survey) and the Northeast Fisheries Science Center Multispecies Bottom Trawl Survey for providing specimens for this study. We are grateful to Captains Jimmy Ruhle, Durand Ward and John Olney Jr. for their contributions to vessel operations, and John Galbraith for ensuring access to exceptionally large specimens. We also recognize Julia White and Kamila Aguiar Gabaldo for their assistance with processing vertebrae and HRXCT images. Thanks to M. Kolmann, J. McDowell, and E. Hilton for reviewing previous versions of this paper. Funding for VIMS Survey Programs was provided by: NOAA Chesapeake Bay Office, the Virginia Environmental Endowment, the U.S. Fish and Wildlife Service, and the Virginia Marine Resources Commission (ChesMMAP); the Atlantic States Marine Fisheries Commission, the Mid Atlantic Fisheries Management Council, the Commercial Fisheries Research Foundation, and the Northeast Fisheries Science Center (NEAMAP); NOAA Fisheries (Silver Spring, MD) (VASMAP); the U.S. Fish and Wildlife Service and the Virginia Marine Resources Commission (Juvenile Fish and Blue Crab Survey). This is contribution number 3674 of the Virginia Institute of Marine Science, College of William & Mary.

Compliance with ethical standards

Field work and sampling were conducted in compliance with protocols approved by the College of William & Mary Institutional Animal Care and Use Committee (IACUC). All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. This article does not contain any studies with human participants performed by any of the authors.

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Akaike H (1973) Information theory as an extension of the maximum likelihood. In: Petrov BN, Csaki F (eds) Proceedings of the second international symposium on information theory. Akademiai Kiado, Budapest, pp 267–228Google Scholar
  2. Alkusairy H, Ali M, Saad A, Reynaud C, Capapé C (2014) Maturity, reproductive cycle, and fecundity of spiny butterfly ray, Gymnura altavela (Elasmobranchii: Rajiformes: Gymnuridae), from the coast of Syria (eastern Mediterranean). Acta Ichthyol Piscat 44(3):229–240CrossRefGoogle Scholar
  3. Başusta A, Başusta N, Sulikowski JA, Driggers WB, Demirhan SA, Cicek E (2012) Length-weight relationships for nine species of batoids from the Iskenderun Bay, Turkey. J Appl Ichthyol 28(5):850–851CrossRefGoogle Scholar
  4. Beamish RJ, Fournier DA (1981) A method for comparing the precision of a set of age determinations. Can J Fish Aquat Sci 38:982–983CrossRefGoogle Scholar
  5. Beverton RJH, Holt SJ (1957) On the dynamics of exploited fish populations. U K Minist Agric Fisheries, Fish Investig (Series 2) 19:533Google Scholar
  6. Bigelow HB, Schroeder WC (1953) Fishes of the Western North Atlantic. Sawfishes, Guitarfishes, Skates, Rays, and Chimaeroids, No. 1, Part 2. Yale University Press. Memoirs Sears Foundation for Marine Research, Yale Univ., New HavenGoogle Scholar
  7. Bini G (1967) Atlante dei pesci delle coste italiane. Vol. I. Leptocardi, Ciclostomi, Selaci. Mondo Sommerso Editrice, Milano, pp 206Google Scholar
  8. Bornatowski H, Wosnick N, Do Carmo WPD, Corrêa MFM, Abilhoa V (2014) Feeding comparisons of four batoids (Elasmobranchii) in coastal waters of southern Brazil. J Mar Biol Assoc UK 94:1491–1499.  https://doi.org/10.1017/S0025315414000472 CrossRefGoogle Scholar
  9. Bowker AH (1948) A test for symmetry in contingency tables. J Am Stat Assoc 43(244):572–574CrossRefPubMedGoogle Scholar
  10. Brander K (1981) Disappearance of common skate Raja batis from the Irish Sea. Nature 290:48–49CrossRefGoogle Scholar
  11. Brown CA, Gruber SH (1988) Age assessment of the lemon shark, Negaprion brevirostris, using tetracycline validated vertebral centra. Copeia 1988:747–753Google Scholar
  12. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information theoretic approach, 2nd edn. Springer, NYGoogle Scholar
  13. Cailliet GM, Goldman KJ (2004) Age determination and validation in chondrichthyan fishes. In: Carrier J, Musick JA, Heithaus M (eds) Biology of sharks and their relatives. CRC Press, Boca Raton, pp 399–448Google Scholar
  14. Cailliet GM, Smith WD, Mollet HF, Goldman KJ (2006) Chondrichthyan growth studies: an updated review, stressing terminology, sample size sufficiency, validation, and curve fitting. In: Carlson JK, Goldman KJ (eds) Age and growth of Chondrichthyan fishes: new methods, techniques and analysis. Springer, Dordrecht, pp 211–228Google Scholar
  15. Campana SE, Annand MC, McMillan JI (1995) Graphical and statistical methods for determining the consistency of age determinations. Trans Am Fish Soc 124:131–138CrossRefGoogle Scholar
  16. Capapé C, Zaouli J, Tomansini JA, Bouchereau JL (1992) Reproductive biology of the spiny butterfly ray, Gymnura altavela (Linneaus, 1758) (Pisces: Gymnuridae) from off the Tunisian coasts. Sci Mar 56:347–355Google Scholar
  17. Casey JG, Pratt HL, Stillwell C (1985) Age and growth of the sandbar shark (Carcharhinus plumbeus) from the western North Atlantic. Can J Fish Aquat Sci 42(5):963–975CrossRefGoogle Scholar
  18. Chang WYB (1982) A statistical method for evaluating the reproducibility of age determination. Can J Fish Aquat Sci 39:1208–1210CrossRefGoogle Scholar
  19. Cuevas-Zimbrón E, Sosa-Nishizaki O, Pérez-Jiménez JC, O’Sullican JB (2012) An analysis of the feasibility of using caudal vertebrae for ageing the spinetail devilray, Mobula japonica (Müller and Henle, 1841). Environ Biol Fish 96(8):907–914CrossRefGoogle Scholar
  20. Daiber FC, Booth RA (1960) Notes on the biology of the butterfly rays, Gymnura altavela and Gymnura micrura. Copeia 1960:137–139Google Scholar
  21. Dale JJ, Holland KN (2012) Age, growth and maturity of the brown stingray (Dasyatis lata) around Oahu, Hawai’i. Mar Freshw Res 63:475–484CrossRefGoogle Scholar
  22. Dulvy NK, Metcalfe JD, Glanville J, Pawson MG, Reynolds JD (2000) Fishery stability, local extinctions, and shifts in community structure in skates. Conserv Biol 14(1):283–293CrossRefGoogle Scholar
  23. Dulvy NK, Fowler SL, Musick JA, Cavanagh RD, Kyne PM, Harrison LR, Carlson JK, Davidson LN, Fordham SV, Francis MP, Pollock CM, Simpfendorfer CA, Burgess GH, Carpenter KE, Compagno LJ, Ebert DA, Gibson C, Heupel MR, Livingstone SR, Sanciangco JC, Stevens JD, Valenti S, White WT (2014) Extinction risk and conservation of the World's sharks and rays. Elife, Cambridge 3:e00590.  https://doi.org/10.7554/eLife.00590 Google Scholar
  24. Ebert DA, Bizzarro JJ (2007) Standardized diet compositions and trophic levels of skate (Chondrichthyes: Rajiformes: Rajoidei). Environ Biol Fish 80(2–3):221–237CrossRefGoogle Scholar
  25. Ebert DA, Stehmann MFW (2013) Sharks, batoids, and chimeras of the North Atlantic. FAO Species Catalogue for Fishery Purposes, No. 7. Food and Agriculture Organization, RomeGoogle Scholar
  26. Evans GT, Hoenig JM (1998) Testing and viewing symmetry in contingency tables, with application to readers of fish ages. Biometrics 54:620–629CrossRefGoogle Scholar
  27. Fisher RA, Call GC, Grubbs RD (2013) Age, growth, and reproductive biology of cownose rays (Rhinoptera bonasus) in Chesapeake Bay. Mar Coast Fish Dynam Manag Ecosys Sci 5(1):225–234Google Scholar
  28. Frisk MG (2010) Life history strategies of batoids. In: Carrier JC, Musick JA, Heithaus MR (eds) Sharks and their relatives II: biodiversity, adaptive physiology, and conservation. CRC Press, Boca Raton, pp 283–316CrossRefGoogle Scholar
  29. Frisk MG, Miller TJ, Martell SJD, Sosebee K (2008) New hypothesis helps explain elasmobranch ‘outburst’ on Georges Bank in the 1980s. Ecol Appl 18:234–245CrossRefPubMedGoogle Scholar
  30. Froese R (2006) Cube law, condition factor and weight–length relationships: history, meta-analysis and recommendations. J Appl Ichthyol 22:241–253CrossRefGoogle Scholar
  31. Geraghty PT, Jones AS, Stewart J, MacBeth WG (2012) Micro-computed tomography: an alternative method for shark ageing. J Fish Biol 80:1292–1299CrossRefPubMedGoogle Scholar
  32. Goldman KJ (2005) Age and growth of elasmobranch fishes. In: Musick JA, Bonfil R (eds) Management techniques for elasmobranch fisheries. FAO Fish Tech Pap 474, Rome, pp 97–132Google Scholar
  33. Heithaus MR, Frid A, Vaudo JJ, Worm B, Wirsing AJ (2010) Unraveling the ecological importance of elasmobranchs. In: Carrier JC, Musick JA, Heithaus MR (eds) Sharks and their relatives II: biodiversity, adaptive physiology, and conservation. CRC Press, Boca Raton, pp 607–633Google Scholar
  34. Henningsen AD (1996) Captive husbandry and bioenergetics of the spiny butterfly ray, Gymnura altavela (Linnaeus). Zoo Biol 15(2):135–142CrossRefGoogle Scholar
  35. Hilton EJ, Schnell NK, Konstantinidis P (2015) When tradition meets technology: systematic morphology of fishes in the early 21st century. Copeia 103(4):858–873CrossRefGoogle Scholar
  36. Hoenig JM, Gruber SH (1990) Life-history patterns in the elasmobranchs: implications for fisheries management. NOAA NMFS Technical Report 90. National Marine Fisheries Service, Washington DC, pp 1–16Google Scholar
  37. Hoenig JM, Morgan MJ, Brown C (1995) Analyzing differences between two age determination methods by tests of symmetry. Can J Fish Aquat Sci 52:364–368CrossRefGoogle Scholar
  38. Ismen A (2003) Age, growth, reproduction and food of common stingray (Dasyatis pastinaca L., 1758) in Iskenderun Bay, the eastern Mediterranean. Fish Res 60:PII S0165-7836(02):00058–00059Google Scholar
  39. Jacobsen IP, Bennett MB (2010) Age and growth of Neotrygon picta, Neotrygon annotata and Neotrygon kuhlii from north-east Australia, with notes on their reproductive biology. J Fish Biol 77:2405–2422CrossRefPubMedGoogle Scholar
  40. Jacobsen IP, Bennett MB (2011) Life history of the blackspotted whipray Himantura astra. J Fish Biol 78(4):1249–1268CrossRefPubMedGoogle Scholar
  41. Jacobsen IP, Johnson JW, Bennett MB (2009) Diet and reproduction in the Australian butterfly ray Gymnura australis from northern and north-eastern Australia. J Fish Biol 75:2475–2489CrossRefPubMedGoogle Scholar
  42. Kimura DK (2008) Extending the von Bertalanffy growth model using explanatory variables. Can J Fish Aquat Sci 65(9):1879–1891CrossRefGoogle Scholar
  43. Kume G, Furumitsu K, Yamaguchi A (2008) Age, growth and age at sexual maturity of fan ray Platyrhina sinensis (Batoidea: Platyrhinidae) in Ariake Bay, Japan. Fish Sci 74:736–742CrossRefGoogle Scholar
  44. Linnaeus C (1758) Systema Naturae, Ed. X. Systema naturae per regna tria naturae, secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis. Tomus I. Editio decima, reformata. Holmiae 1:1–824Google Scholar
  45. Maisey JG (2001a) CT-scan reveals new cranial features in Devonian chondrichthyan “Cladoduswildungensis. J Vertebr Paleontol 21:807–810CrossRefGoogle Scholar
  46. Maisey JG (2001b) Remarks on the inner ear of elasmobranchs and its interpretation from skeletal labyrinth morphology. J Morphol 250:236–264CrossRefPubMedGoogle Scholar
  47. Maisey JG (2004) Morphology of the braincase in the Broadnose Sevengill shark Notorynchus (Elasmoobranchii, Hexanchiformes), based on CT scanning. Am Mus Novit 3429:1–52CrossRefGoogle Scholar
  48. Mandelman JW, Cicia AM, Ingram GW, Driggers WB, Coutre KM, Sulikowski JA (2012) Short-term post-release mortality of skates (family Rajidae) discarded in a western North Atlantic commercial otter trawl fishery. Fish Res 139:76–84CrossRefGoogle Scholar
  49. Martin LK, Cailliet GM (1988) Age and growth determination of the bat ray, Myliobatis californica gill, in Central California. Copeia 1988:754–762Google Scholar
  50. McEachran JD, Capapé C (1984) Gymnuridae. In: Whitehead PJP, Bauchot M-L, Hureay JC, Nielsen J, Tortonese E (eds) Fishes of the north-eastern Atlantic and the Mediterranean. Vol 1 Unesco, Paris, pp 203–204Google Scholar
  51. McEachran JD, de Carvalho MR (2002) Batoid Fishes. 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 and American Society of Ichthyologists and Herpetologists Special Publication No. 5, Rome, FAO, pp 508–589Google Scholar
  52. McEachran JD, Dunn KA (1998) Phylogenetic analysis of skates, a morphologically conservative clade of elasmobranchs (Chondrichthyes: Rajidae). Copeia 1998:271–290CrossRefGoogle Scholar
  53. McEachran JD, Séret B (1990) Gymnuridae. In: Quero JC, Hureau JC, Karrer C, Post A, Saldanha L (eds) Check-list of the fishes of the eastern tropical Atlantic (CLOFETA), Vol 1. JNICT, Lisbon; SEI, Paris; and UNESCO, Paris, pp 64–66Google Scholar
  54. Mejía-Falla PA, Cortés E, Navia AF, Zapata FA (2014) Age and growth of the round stingray Urotrygon rogersi, a particularly fast-growing and short-lived elasmobranch. PLoS One 9(4):e96077.  https://doi.org/10.1371/journal.pone.0096077 CrossRefPubMedPubMedCentralGoogle Scholar
  55. Mollet HF, Ezcurra JM, O’Sullivan JB (2002) Captive biology of the pelagic stingray, Dasyatis violacea (Bonaparte, 1832). Mar Freshw Res 53:531–541CrossRefGoogle Scholar
  56. Moyer JK, Riccio ML, Bemis WE (2015) Development and microstructure of tooth histotypes in the blue shark, Prionace glauca (Carcharhiniformes: Carcharhinidae) and the great white shark, Carcharodon carcharias (Lamniformes: Lamnidae). J Morphol 276:797–817CrossRefPubMedGoogle Scholar
  57. Murawski SA (1991) Can we manage our multispecies fisheries? Fisheries 16(5):5–13CrossRefGoogle Scholar
  58. Natanson LJ (1993) Effect of temperature on band deposition in the little skate, Raja erinacea. Copeia 1993:199–206CrossRefGoogle Scholar
  59. Naylor GJP, Caira JN, Jensen K, Rosana K, White W, Last P (2012) A DNA sequence based approach to the identification of shark and ray species and its implications for global elasmobranch diversity and parasitology. Bull Am Mus Nat Hist 367, p 263CrossRefGoogle Scholar
  60. Neer JA, Thompson BA (2005) Life history of the cownose ray, Rhinoptera bonasus, in the northern Gulf of Mexico, with comments on geographic variability in life history traits. Environ Biol Fish 73:321–331CrossRefGoogle Scholar
  61. O’Shea OR, Braccini M, McAuley R, Speed CW, Meekan MG (2013) Growth of tropical dasyatid rays estimated using a multi-analytical approach. PLoS One 8(10):e77194.  https://doi.org/10.1371/journal.pone.0077194 CrossRefPubMedPubMedCentralGoogle Scholar
  62. Okamura H, Punt AE, Semba Y, Ichinokawa M (2013) Marginal increment analysis: a new statistical approach of testing for temporal periodicity in fish age verification. J Fish Biol 82:1239–1249Google Scholar
  63. Özbek EO, Çardak M, Kebapçioğlu T (2016) Spatio-temporal patterns of abundance, biomass and length-weight relationships of Gymnura altavela (Linnaeus, 1758) (Pisces: Gymnuridae) in the Gulf of Antalya, Turkey (Levantine Sea). J Black Sea/Mediterr Environ 21:169–190Google Scholar
  64. Quinn TJ, Deriso RB (1999) Quantitative fish dynamics. Oxford University Press, New York, p 560Google Scholar
  65. R Development Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  66. Raje SG (2003) Some aspects of biology of four species of rays off Mumbai water. Indian J Fish 50(1):89–96Google Scholar
  67. Ranzi S (1934) Le basi fisio-morfologiche dello sviluppo embrionale dei Selaci. Parti II e III. Pubblication Stazione Zoologica di Napoli 13:331–437Google Scholar
  68. IUCN Red List (2016) International Union for conservation of nature and natural resources – IUCN red list of threatened species. http://www.iucnredlist.org/. Accessed 07 Feb 2017
  69. Ricker WE (1979) Growth rates and models. In: Hoar WS, Randall DJ (eds) Fish physiology. Vol VIII. Academic Press, New York, pp 677–743Google Scholar
  70. Ridewood WG (1921) On the calcification of the vertebral centra in sharks and rays. Phil trans R Soc B. Biologicals 210:311–407Google Scholar
  71. Ritz C, Streibig JC (2008) Nonlinear regression with R. Springer. Springer, New York, p 144Google Scholar
  72. Robins CR, Ray GC (1986) A field guide to Atlantic coast fishes of North America. Houghton Mifflin Company, Boston, p 354Google Scholar
  73. Romine JG, Musick JA, Johnson RA (2013) Compensatory growth of the sandbar shark in the western North Atlantic including the Gulf of Mexico. Mar Coast Fish 5:189–199CrossRefGoogle Scholar
  74. Schultze HP, Cloutier R (1991) Computed-tomography and magnetic resonance imaging studies of Latimeria chalumnae. Environ Biol Fish 32:159–181CrossRefGoogle Scholar
  75. Schwartz FJ (1984) Sharks, sawfish, skates, and rays of the Carolinas. Special Publication, Institute of Marine Sciences, University of North Carolina, Morehead CityGoogle Scholar
  76. Seber GAF (1982) The estimation of animal abundance and related parameters, 2nd edn. The Blackburn Press, Caldwell, p 654Google Scholar
  77. Simpfendorfer CA, Heupel MR, White WT, Dulvy NK (2011) The importance of research and public opinion to conservation management of sharks and rays: a synthesis. Mar Freshw Res 62:518–527CrossRefGoogle Scholar
  78. Smart JJ, Chin A, Tobin AJ, Simpfendorfer CA (2016) Multimodel approaches in shark and ray growth studies: strengths, weaknesses and the future. Fish Fish 17(4):955–971CrossRefGoogle Scholar
  79. Smith WD, Cailliet GM, Melendez EM (2007) Maturity and growth characteristics of a commercially exploited stingray, Dasyatis dipterura. Aust J Mar Freshwat Res 58:54–66CrossRefGoogle Scholar
  80. Smith JW, Merriner JV (1987) Age and growth, movements and distribution of the cownose ray, Rhinoptera bonasus, in Chesapeake Bay. Estuaries 10(2):153–164CrossRefGoogle Scholar
  81. Sprugel DG (1983) Correcting for bias in log-transformed allometric equations. Ecology 64:209–210CrossRefGoogle Scholar
  82. Stevens JD, Walker TI, Cook SF, Fordham S (2005) Threats faced by chondrichthyan fishes. In: Fowler SL, Cavanagh R, Camhi M, Burgess GH, Caillet GM, Fordham S, Simpfendorfer CA, Musick JA (eds) Sharks, rays and chimaeras: the status of the Chondrichthyan fishes. IUCN species survival commission shark specialist group, gland and, Cambridge, pp 48–57Google Scholar
  83. Sulikowski JA, Morin MD, Suk SH, Howell WH (2003) Age and growth of the winter skate, Leucoraja ocellata, in the Gulf of Maine. Fish Bull 101:405–413Google Scholar
  84. Sulikowski JA, Elzey S, Kneebone J, Jurek J, Huntting Howell W, Tsang PCW (2007) The reproductive cycle of the smooth skate, Malacoraja senta, in the Gulf of Maine. Aust J Mar Freshwat Res 58:98–103CrossRefGoogle Scholar
  85. Tamini LL, Chiaramont GE, Perez JE, Cappozzo HL (2006) Batoids in a coastal trawl fishery of Argentina. Fish Res 77(3):326–332CrossRefGoogle Scholar
  86. Teixeira EC, Silva VEL, Fabré NN, Batista VS (2016) Length–weight relationships for four stingray species from the tropical Atlantic Ocean. J Appl Ichthyol 33:594–596CrossRefGoogle Scholar
  87. Thorson JT, Simpfendorfer CA (2009) Gear selectivity and sample size effects on growth curve selection in shark age and growth studies. Fish Res 98:75–84CrossRefGoogle Scholar
  88. Vooren CM, Piercy AN, Snelson Jr. FF, Grubbs RD, Notarbartolo di Sciara G, Serena S (2007) Gymnura altavela. The IUCN red list of threatened species 2007: e.T63153A12624290  https://doi.org/10.2305/IUCN.UK.2007.RLTS.T63153A12624290.en. Accessed on 07 Feb 2017
  89. Walker PA, Hessen HJL (1996) Long-term changes in ray populations in the North Sea. ICES J Mar Sci 53:1085–1093CrossRefGoogle Scholar
  90. Walker PA, Hislop JRG (1998) Sensitive skates or resilient rays? Spatial and temporal shifts in ray species composition in the central and north-western North Sea between 1930 and the present day. ICES J Mar Sci 55:392–402CrossRefGoogle Scholar
  91. Walls RHL, Vacchi M, Notarbartolo di Sciara G, Serena F, Dulvy NK (2016) Gymnura altavela. The IUCN red list of threatened species 2016: e.T63153A16527909. Accessed 07 Feb 2017Google Scholar
  92. White WT, Dharmadi (2007) Species and size compositions and reproductive biology of rays (Chondrichthyes, Batoidea) caught in target and non-target fisheries in eastern Indonesia. J Fish Biol 70:1809–1837CrossRefGoogle Scholar
  93. White WT, Platell ME, Potter IC (2001) Relationship between reproductive biology and age composition and growth in Urolophus lobatus (Batoidea: Urolophidae). Mar Biol 138:135–147CrossRefGoogle Scholar
  94. 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 140:699–712CrossRefGoogle Scholar
  95. White J, Simpfendorfer CA, Tobin AJ, Heupel MR (2014) Age and growth parameters of shark-like batoids. J Fish Biol 84:1340–1353CrossRefPubMedGoogle Scholar
  96. Wigley SE, McBride HM, McHugh NJ (2003) Length-weight relationships for 74 fish species collected during NEFSC research vessel bottom trawl surveys, 1992-99. NOAA Tech Memo NMFS NE 171:26Google Scholar
  97. Witmer LM, Ridgely RC, Dufeau DL, Semones MC (2008) Using CT to peer into the past: 3D visualization of the brain and ear regions of birds, crocodiles, and nonavian dinosaurs. In: Endo H, Frey R (eds) Anatomical imaging: towards a new morphology. Springer-Verlag, Tokyo, pp 67–88CrossRefGoogle Scholar
  98. Yokota L, Goitein R, Gianeti MD, Lessa RTP (2012) Reproductive biology of the smooth butterfly ray Gymnura micrura. J Fish Biol 81(4):1315–1326CrossRefPubMedGoogle Scholar
  99. Zhu L, Li L, Liang Z (2009) Comparison of six statistical approaches in the selection of appropriate fish growth models. Chin J Oceanol Limnol 27:457–467CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2017

Authors and Affiliations

  • K. T. Parsons
    • 1
  • J. Maisano
    • 2
  • J. Gregg
    • 1
  • C. F. Cotton
    • 3
  • R. J. Latour
    • 1
  1. 1.Virginia Institute of Marine ScienceCollege of William & MaryGloucester PointUSA
  2. 2.Department of Geological SciencesThe University of TexasAustinUSA
  3. 3.Florida State University Coastal and Marine LaboratorySt. TeresaUSA

Personalised recommendations