Marine Biology

, Volume 157, Issue 12, pp 2613–2624 | Cite as

Evaluating ultrasonography as a non-lethal method for the assessment of maturity in oviparous elasmobranchs

  • Jonathan M. Whittamore
  • Craig Bloomer
  • Grainne M. Hanna
  • Ian D. McCarthyEmail author
Original Paper


Due to the impacts of commercial fishing on elasmobranchs, future research and management necessitates reliable and accurate information on life history. For females, maturity assessment is limited to dissection, and it is not desirable to be removing large numbers in order to assess the reproductive characteristics of a population. The present study evaluated ultrasonography as a potential, non-lethal method for assessing the maturity status of two oviparous elasmobranchs, the thornback ray (Raja clavata) and small-spotted catshark (Scyliorhinus canicula). Ultrasound permitted visualisation and measurement of the ovary in R. clavata, and the shell gland, ovarian follicles and egg capsules within the oviducts for S. canicula. With the exception of the ovary in R. clavata, the dimensions of these structures on the sonograms were directly corroborated by in situ measurements, and ultrasound was verified as an accurate and reliable method of making quantitative and qualitative assessments of these internal reproductive structures.


Reproductive Tract Ovarian Follicle Reproductive Structure Total Body Length Ovary Size 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



The authors would like to thank the Captain and crew of the R. V. Prince Madog, along with Mr. G. Parry-Jones and Mr. B. Roberts, for collection of fish used in this study, Mr. G. Hughes for technical assistance, and two anonymous referees for their helpful comments on the manuscript. Many thanks are also extended to Dynamic Imaging Ltd and Mr. G. Frasier for ultrasound technical support. This study formed part of MSc theses which were submitted by C. Bloomer (2005) and G. Hanna (2006) to Bangor University. This project was supported by a small research grant from the Fisheries Society of the British Isles (FSBI) to J. Whittamore and I. McCarthy.


  1. Awruch CA, Frusher SD, Pankhurst NW, Stevens JD (2008) Non-lethal assessment of reproductive characteristics for management and conservation of sharks. Mar Ecol Prog Ser 355:277–285CrossRefGoogle Scholar
  2. Barone M, De Ranieri S, Fabiani O, Pirone A, Serena F (2007) Gametogenesis and maturity stages scale of Raja asterias Delaroche, 1909 (Chondrichthyes, Rajidae) from the South Ligurian Sea. Hydrobiologia 580:245–254CrossRefGoogle Scholar
  3. Blythe B, Helfrich LA, Beal WE, Bosworth B, Libey GS (1994) Determination of sex and maturational status of striped bass (Morone saxatilis) using ultrasonic imaging. Aquaculture 125:175–184CrossRefGoogle Scholar
  4. Bonar SA, Thomas GL, Paully GB (1989) Use of ultrasonic images for rapid nonlethal determination of sex and maturity of Pacific herring. N Am J Fish Manag 9:364–366CrossRefGoogle Scholar
  5. Bosworth BG, Holland M, Brazil BL (2001) Evaluation of ultrasound imagery and body shape to predict carcass and fillet yield in farm-raised catfish. J Anim Sci 79:1483–1490PubMedGoogle Scholar
  6. Bryan JL, Wildhaber ML, Papoulias DM, DeLonay AJ, Tillitt DE, Annis ML (2007) Estimation of gonad volume, fecundity, and reproductive stage of shovelnose sturgeon using sonography and endoscopy with application to the endangered pallid sturgeon. J Appl Ichthyol 23:411–419CrossRefGoogle Scholar
  7. Carrier JC, Murru FL, Walsh MT, Pratt HL (2003) Assessing reproductive potential in nurse sharks (Ginglymostoma cirratum) using ultrasonography and endoscopy: an example of bridging the gap between field research and captive studies. Zoo Biol 22:179–187CrossRefGoogle Scholar
  8. Daly J, Gunn I, Kirby N, Jones R, Galloway D (2007) Ultrasound examination and behaviour scoring of captive broadnose sevengill sharks, Notorynchus cepedianus (Peron, 1807). Zoo Biol 26:383–395CrossRefPubMedGoogle Scholar
  9. Davenport J (1993) Ultrasonography: a non-invasive tool for the study of structure and mechanical events in marine animals. J Mar Biol Ass UK 73:461–464CrossRefGoogle Scholar
  10. Dulvy NK, Metcalfe JD, Glanville J, Pawson MG, Reynolds JD (2000) Fishery stability, local extinctions, and shifts in community structure in skates. Cons Biol 14:283–293CrossRefGoogle Scholar
  11. Dulvy NK, Baum JK, Clarke S, Compagno LJV, Cortés E, Domingo A, Fordham S, Fowler S, Francis MP, Gibson C, Matínez J, Musick JA, Soldo A, Stevens JD, Valenti S (2008) You can swim but you can’t hide: the global status and conservation of oceanic pelagic sharks and rays. Aquat Conserv Mar Freshw Ecosyst 18:459–482CrossRefGoogle Scholar
  12. Ebert DA, Compagno LJV, Cowley PD (2006) Reproductive biology of catsharks (Chondrichthyes: Scyliorhinidae) off the west coast of southern Africa. ICES J Mar Sci 63:1053–1065Google Scholar
  13. Ellis JR, Shackley SE (1997) The reproductive biology of Scyliorhinus canicula in the Bristol Channel, UK. J Fish Biol 51:361–372Google Scholar
  14. Evans AF, Fitzpatrick MS, Siddens LK (2004) Use of ultrasound imaging and steroid hormone concentrations to identify maturational status in adult steelhead. N Am J Fish Manag 24:967–978CrossRefGoogle Scholar
  15. Gelsleichter J, Rasmussen LEL, Manire CA, Tyminski J, Chang B, Lombardi-Carlson L (2002) Serum steroid concentrations and development of reproductive organs during puberty in male bonnethead sharks, Sphyrna tiburo. Fish Physiol Biochem 26:389–401CrossRefGoogle Scholar
  16. Gili C, Papini L, Vannozzi I, Romagnoli S (2006) Ultrasonographic monitoring of the fetal growth of common seals (Phoca vitulina vitulina). Vet Rec 159:116–118CrossRefPubMedGoogle Scholar
  17. Gridelli S, Diana A, Parmeggiani A, Cipone M, Preziosi R (2003) Goitre in large and small spotted dogfish, Scyliorhinus stellaris (L.) and Scyliorhinus canicula (L.). J Fish Dis 26:687–690CrossRefPubMedGoogle Scholar
  18. Grimaldi AM, Agnisola C, Fiorito G (2007) Using ultrasound to estimate brain size in the cephalopod Octopus vulgaris Cuvier in vivo. Brain Res 1183:66–73CrossRefPubMedGoogle Scholar
  19. Gumpenberger M (2002) Ultrasound diagnosis—ultrasonic detection of spinal malformation in a Chub (Leuciscus leuciscus L.). Vet Radiol Ultrasound 43:584–585CrossRefPubMedGoogle Scholar
  20. Hall AJ, McConnell BJ (2007) Measuring changes in juvenile gray seal body composition. Mar Mam Sci 23:650–665CrossRefGoogle Scholar
  21. Henderson AC, Casey A (2001) Reproduction and growth in the lesser-spotted dogfish Scyliorhinus canicula (Elasmobranchii; Scyliorhinidae), from the west coast of Ireland. Cah Biol Mar 42:397–405Google Scholar
  22. Holden MJ (1975) The fecundity of Raja clavata in British waters. J Cons Int Explor Mer 36:110–118Google Scholar
  23. Jennings CA, Will TA, Reinert TR (2005) Efficacy of a high- and low-frequency ultrasonic probe for measuring ovary volume and estimating fecundity of striped bass Morone saxatilis in the Savannah River Estuary. Fish Res 76:445–453CrossRefGoogle Scholar
  24. Karlsen O, Holm JC (1994) Ultrasonography, a non-invasive method for sex determination in cod (Gadus morhua). J Fish Biol 44:965–971Google Scholar
  25. King AJ, Henderson SM, Schmidt MH, Cole AG, Adam SA (2005) Using ultrasound to understand vascular and mantle contributions to venous return in the cephalopod Sepia officinalis L. J Exp Biol 208:2071–2082CrossRefPubMedGoogle Scholar
  26. Kneebone J, Ferguson DE, Sulikowski JA, Tsang PCW (2007) Endocrinological investigation into the reproductive cycles of two sympatric skate species, Malacoraja senta and Amblyraja radiata, in the western Gulf of Maine. Environ Biol Fish 80:257–265CrossRefGoogle Scholar
  27. Koob TJ, Callard IP (1999) Reproductive endocrinology of female elasmobranchs: lessons from the little skate (Raja erinacea) and spiny dogfish (Squalus acanthias). J Exp Zool 284:557–574CrossRefPubMedGoogle Scholar
  28. Koob TJ, Tsang P, Callard IP (1986) Plasma estradiol, testosterone and progesterone levels during the ovulatory cycle of the little skate, Raja erinacea. Biol Reprod 35:267–275CrossRefPubMedGoogle Scholar
  29. Martin RW, Myers J, Sower SA, Phillips DJ, McAuley C (1983) Ultrasonic imaging, a potential tool for sex determination of live fish. N Am J Fish Manag 3:258–264CrossRefGoogle Scholar
  30. Martin-Robichaud DJ, Rommens M (2001) Assessment of sex and evaluation of ovarian maturation of fish using ultrasonography. Aquac Res 32:113–120CrossRefGoogle Scholar
  31. Mattson NS (1991) A new method to determine sex and gonad size in live fishes by using ultrasonography. J Fish Biol 39:673–677CrossRefGoogle Scholar
  32. Myers RA, Baum JK, Shepherd TD, Powers SP, Peterson CH (2007) Cascading effects of the loss of apex predatory sharks from a coastal ocean. Science 315:1846–1850CrossRefPubMedGoogle Scholar
  33. Newman DM, Jones PL, Ingram BA (2008) Sexing accuracy and indicators of maturation status in captive Murray cod Maccullochella peelii peelii using non-invasive ultrasonic imagery. Aquaculture 279:113–119CrossRefGoogle Scholar
  34. Roebuck TR, Steinman KJ, Gearhart S, Reidarson TR, McBain JF, Monfort SL (2004) Reproductive physiology and development of artificial insemination technology in killer whales (Orcinus orca). Biol Reprod 71:650–660CrossRefGoogle Scholar
  35. Rogers SI, Ellis JR (2000) Changes in the demersal fish assemblages of British coastal waters during the 20th Century. ICES J Mar Sci 57:866–881CrossRefGoogle Scholar
  36. Ryland JS, Ajayi TO (1984) Growth and population dynamics of three Raja species (Batoidei) in Carmarthen Bay, British Isles. J Cons Int Explor Mer 41:111–120Google Scholar
  37. Shields RJ, Davenport J, Young C, Smith PL (1993) Oocyte maturation and ovulation in the Atlantic halibut, Hippoglossus hippoglossus (L.), examined using ultrasonography. Aquac Fish Manag 24:181–186Google Scholar
  38. Stehmann MFW (2002) Scales of maturity stages for sharks, skates and rays, and chimaeras. Arch Fish Mar Res 50:30–48Google Scholar
  39. 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 J Mar Sci 57:476–494CrossRefGoogle Scholar
  40. Sulikowski JA, Tsang PCW, Howell WH (2004) An annual cycle of steroid hormone concentrations and gonad development in the winter skate, Leucoraja ocellata, from the western Gulf of Maine. Mar Biol 144:845–853CrossRefGoogle Scholar
  41. Sulikowski JA, Tsang PCW, Howell WH (2005) Age and size at sexual maturity for the winter skate, Leucoraja ocellata, in the western Gulf of Maine based on morphological, histological and steroid hormone analyses. Environ Biol Fish 72:429–441CrossRefGoogle Scholar
  42. Sulikowski JA, Kneebone J, Elzey S, Jurek J, Howell WH, Tsang PCW (2006) Using the composite variables of reproductive morphology, histology and steroid hormones to determine age and size at sexual maturity for the thorny skate Amblyraja radiata in the western Gulf of Maine. J Fish Biol 69:1449–1465CrossRefGoogle Scholar
  43. Sulikowski JA, Driggers WB, Ingram GW, Kneebone J, Ferguson DE, Tsang PCW (2007) Profiling plasma steroid hormones: a non-lethal approach for the study of skate reproductive biology and its potential use in conservation management. Environ Biol Fish 80:285–292CrossRefGoogle Scholar
  44. Sumpter JP, Dodd JM (1979) The annual reproductive cycle of the female lesser spotted dogfish, Scyliorhinus canicula L., and its endocrine control. J Fish Biol 15:687–695CrossRefGoogle Scholar
  45. Walsh MT, Pipers FS, Brendemuehl CA, Murru FL (1993) Ultrasonography as a diagnostic tool in shark species. Vet Radiol Ultrasound 34:213–218CrossRefGoogle Scholar
  46. Whiteman EA, Jennings CA, Nemeth RS (2005) Sex structure and potential female fecundity in an Epinephelus guttatus spawning aggregation: applying ultrasonic imaging. J Fish Biol 66:983–995CrossRefGoogle Scholar
  47. Whittamore JM, McCarthy ID (2005) The population biology of the thornback ray, Raja clavata in Caernarfon Bay, North Wales. J Mar Biol Ass UK 85:1089–1094CrossRefGoogle Scholar
  48. Will TA, Reiner TR, Jennings CA (2002) Maturation and fecundity of a stock-enhanced population of striped bass in the Savannah River Estuary, USA. J Fish Biol 60:532–544Google Scholar
  49. Williams DL, Goddard PJ, Brancker WM (2007) Ultrasonographic examination of ocular lesions in farmed halibut. Vet J 173:456–458CrossRefPubMedGoogle Scholar
  50. Wourms JP (1977) Reproduction and development in Chondrichthyan fishes. Am Zool 17:379–410Google Scholar
  51. Zweibel WJ, Sohaey R (1998) Introduction to ultrasound. WB Saunders Co, PhiladelphiaGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Jonathan M. Whittamore
    • 2
  • Craig Bloomer
    • 1
  • Grainne M. Hanna
    • 1
  • Ian D. McCarthy
    • 1
    Email author
  1. 1.School of Ocean Sciences, College of Natural SciencesBangor UniversityAngleseyUK
  2. 2.School of BiosciencesUniversity of ExeterExeterUK

Personalised recommendations