Environmental Biology of Fishes

, Volume 102, Issue 2, pp 209–219 | Cite as

Seasonal and spatial changes in sex hormone levels and oocyte development of bonefish (Albula vulpes)

  • Cameron Luck
  • Sahar Mejri
  • Justin Lewis
  • Paul S. Wills
  • Marty Riche
  • Jonathan Shenker
  • Aaron Adams
  • Matthew J. AjemianEmail author


Bonefish (Albula vulpes) support an economically important fishery, yet little is known regarding the reproductive biology of this species. Blood and oocyte samples were collected from wild female bonefish (Albula vulpes) during (February and April, 2017) and outside (September, 2017) the spawning season in Grand Bahama Island, The Bahamas. Fish reproductive state was evaluated using histological analysis of the oocytes and determination of sex hormone levels of 17β-estradiol and testosterone in the plasma. The presence of three different cohorts of oocytes in bonefish females suggests group-synchronous ovarian development. Levels of 17β-estradiol were low in individuals sampled outside of the spawning season relative to fish sampled during spawning months. Testosterone levels did not change as female bonefish entered the spawning season. Within the spawning season, bonefish are commonly found along shallow water flats, or in pre-spawn aggregations (PSA). The diameters of late vitellogenic oocytes collected from PSA fish were significantly larger than those from the flats fish. Levels of 17β-estradiol did not differ between PSA and flats fish; however, testosterone levels were significantly higher in fish from the PSA. These results indicate that as bonefish are transitioning to the PSA from flats habitats, vitellogenesis is still occurring. However, when and where final maturation commences in reproductively active bonefish remains unclear.


Bonefish Reproductive development Sex hormone Oocyte 



This study was financially supported by Bonefish & Tarpon Trust (BTT) and National Fish and Wildlife Foundation (NFWF). We are grateful for the lodging and water access provided by East End Lodge. The experimental protocol for this study received approval from Florida Atlantic University’s Institutional Animal Care and Use Committee (Animal Use Protocol #A16-34).


  1. Adams A, Shenker JM, Jud ZR, Lewis JP, Carey E, Danylchuk AJ (2018) Identifying pre-spawning aggregation sites for bonefish (Albula vulpes) in The Bahamas to inform habitat protection and species conservation. Environ Biol Fish (this issue)Google Scholar
  2. Barannikova IA, Bayunova LV, Semenkova TB (2004) Serum levels of testosterone, 11-ketotestosterone and oestradiol-17β in three species of sturgeon during gonadal development and final maturation induced by hormonal treatment. J Fish Biol 64:1330–1338CrossRefGoogle Scholar
  3. Barber BJ (1996) Gametogenesis of eastern oysters, Crassostrea virginica (Gmelin 1791) and Pacific oysters, Crassostrea gigas (Thunberg 1793) in disease-endemic lower Chesapeake Bay. J Shellfish Res 15:285–290Google Scholar
  4. Bommelaer MC, Billard R, Breton B (1981) Changes in plasma gonadotropin after ovariectomy and estradiol supplementation at different stages at the end of the reproductive cycle in the rainbow trout (Salmo gairdneri R.). Reprod Nutr Dev 21(6A):989–997CrossRefGoogle Scholar
  5. Boucek RE, Lewis JP, Stewart BD, Jud ZR, Carey E, Adams AJ (2018) Measuring site fidelity and homesite-to-pre-spawning site connectivity of Bonefish (Albula vulpes): using mark-recapture to inform habitat conservation. Environ Biol Fish (this issue)Google Scholar
  6. Brown-Peterson NJ, Wyanski DM, Saborido-Rey F, Macewicz BJ, Lowerre-Barbieri SK (2011) A standardized terminology for describing reproductive development in fishes. Mar Coast Fish 3(1):52–70CrossRefGoogle Scholar
  7. Campbell CM, Walsh JM, Idler DR (1976) Steroid in the plasma of the winter flounder (Pseudopleuronectes americanus). A seasonal study and investigation of steroid involvement in oocyte maturation. Gen Comp Endocrinol 29:14–20CrossRefGoogle Scholar
  8. Colton DE, Alevizon WS (1983) Movement patterns of bonefish, Albula vulpes, in Bahamian waters. Fish Bull 81(1):148–154Google Scholar
  9. Crabtree RE, Harnden CW, Snodgrass D, Stevens C (1996) Age, growth, and mortality of bonefish, Albula vulpes, from the waters of the Florida Keys. Fish. Bull. 94:442–451Google Scholar
  10. Crabtree R, Snodgrass D, Harnden C (1997) Maturation and reproductive seasonality in bonefish, Albula vulpes, from the waters of the Florida keys. Fish Bull 95:456–465Google Scholar
  11. Crabtree RE, Stevens C, Snodgrass D, Stengard FJ (1998) Feeding habits of bonefish, Albula vulpes, from the waters of the Florida keys. Fish Bull 96:754–766Google Scholar
  12. Crim LW, Peter RE, Billard R (1981) Onset of gonadotropic hormone accumulation in the immature trout pituitary gland in response to estrogen or aromatizable androgen steroid hormones. Gen Comp Endocrinol 44:374–381CrossRefGoogle Scholar
  13. Danylchuk AJ, Cooke SJ, Goldberg TL, Suski CD, Murchie KJ, Danylchuk SE, Philipp DP (2011) Aggregations and offshore movements as indicators of spawning activity of bonefish (Albula vulpes) in the Bahamas. Mar Biol 158(9):1981–1999CrossRefGoogle Scholar
  14. Danylchuk AJ, Lewis JP, Jud ZR, Shenker J, Adams AJ (2018) Behavioral observations of bonefish during prespawning aggregations in The Bahamas: clues to drive broader conservation efforts. Environ Biol Fish (this issue)Google Scholar
  15. Fedler T (2010) The economic impact of flats fishing in The Bahamas, Report prepared for the Bahamian flats fishing alliance pp 20Google Scholar
  16. Fedler A (2013) Economic impacts of the Florida Keys flats fishery. Report to Bonefish & Tarpon Trust, Key Largo Florida. Accessed 25 Jan 2017
  17. Fourqurean J, Robblee M (1999) Florida bay: a history of recent ecological changes. Estuaries 22:345–357CrossRefGoogle Scholar
  18. Hildebrand SF (1963) Family Albulidae. In: Bigelow HB, Bradbury MG, Dymond JR, Greeley JR, Hildebrand SF, Mead GW, Miller RR, Rivas LR, Schroeder WC, Suttkus RD, Vladykov VD (eds) Fishes of the western North Atlantic. Sears Foundation for Marine Research, Yale University, New Haven, pp 132–147Google Scholar
  19. Idler DR, Hwang SJ, Crim LW, Reddin D (1981) Determination of sexual maturation stages of Altantic salmon (Salmo salar) captured at sea. Can J Fish Aquat Sci 38(4):405–413CrossRefGoogle Scholar
  20. Ijiri S, Kazeto Y, Takeda N, Chiba H, Adachi S, Yamauchi K (1995) Changes in serum steroid hormones and steroidogenic availability of ovarian follicles during artificial maturation of cultivated Japanese eel, Anguilla japonica. Aquaculture 135:3–16CrossRefGoogle Scholar
  21. Johannes RE, Yeeting B (2000) I-Kiribati knowledge and management of Tarawa’s lagoon resources. Atoll Res Bull 489:1–24CrossRefGoogle Scholar
  22. Kagawa H (2013) Oogenesis in Teleost Fish. Aqua-BioSci Monogr 6(4):99–127CrossRefGoogle Scholar
  23. Kime D (1998) Introduction to fish reproduction. In: Endocrine disruption in fish. Boston, MA, pp 81–107Google Scholar
  24. Lambert JGD, Thisjssen JH, Eylath V (1971) Conversion of 3H-androsteredione and 3H-T to 3H-oestradiol-17β in vitro by the ovary of the guppy, Poecilia reticulate. Proc K Ned Akad Wet 74:52–59Google Scholar
  25. Larkin MF (2011) Assessment of South Florida’s bonefish stock. Open Access Dissertations. 632. Accessed 25 Jan 2017
  26. Layman CA, Silliman BR (2002) Preliminary survey and diet analysis of juvenile fishes of an estuarine creek on Andros Island, Bahamas. Bull Mar Sci 70:199–210Google Scholar
  27. Lubzen E, Young G, Bobe J, Cerda J (2010) Oogenesis in teleosts: how fish eggs are formed. Gen Comp Endocrinol 165:367–389CrossRefGoogle Scholar
  28. Mandich A, Massari A, Bottero S, Pizzicori P, Goos H, Marino G (2004) Plasma sex steroid and vitellogenin profiles during gonad development in wild Mediterranean amberjack (Seriola dumerilii). Mar Biol 144:127–138CrossRefGoogle Scholar
  29. Murchie KJ, Cooke SJ, Danylchuk AJ (2010) Seasonal energetics and condition of bonefish from different subtropical tidal creeks in Eleuthera, the Bahamas. Mar Coast Fish 2:249–262CrossRefGoogle Scholar
  30. Murchie KJ, Cooke SJ, Danylchuk AJ, Danylchuk SE, Goldberg TL, Suski CD, Philipp DP (2013) Movement patterns of bonefish (Albula vulpes) in tidal creeks and coastal waters of Eleuthera, the Bahamas. Fish Res 147:404–412CrossRefGoogle Scholar
  31. Nagahama Y, Yamashita M (2008) Regulation of oocyte maturation in fish. Develop Growth Differ 50:195–219CrossRefGoogle Scholar
  32. R Core Team (2014) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Accessed 10 Feb 2017
  33. Rehage JS, Santos RO, Kroloff EKN, Heinen JE, Lai Q, Black B, Boucek RE, Adams AJ (2018) How has the quality of bonefishing changed? Quantitative temporal patterns in the South Florida Flats Fishery using local ecological knowledge. Environ Biol Fish (this issue)Google Scholar
  34. Rocha M, Rocha E (2006) Morphofunctional aspects of reproduction from synchronous to asynchronous fishes-an overview. In: Reinecke M, Zaccone G, Kappor B (eds) Fish endocrinology. Science Publishers, New Hampshire, pp 571–624Google Scholar
  35. Rottmann RW, Shireman JV, Chapman FA (1991) Determining sexual maturity of brood stock for induced spawning of fish. SRAC Publ 423:1–4Google Scholar
  36. Santos RO, Rehage JS, Adams AJ, Black BD, Osborne J, Kroloff EKN (2017) Quantitative assessment of a data-limited recreational bonefish fishery using a time-series of fishing guides reports. PLoS One 12(9):1–19Google Scholar
  37. Scott AP, Bye VJ, Baynes SM (1980) Seasonal variations in sex steroids of female rainbow trout (Salmo gairdneri). J Fish Biol 17:587–592CrossRefGoogle Scholar
  38. Scott AP, MacKenzie DS, Stacey NE (1983a) Endocrine changes during natural spawning in the white sucker, Catostomus commersoni. Gen Comp Endocrinol 56:349–359CrossRefGoogle Scholar
  39. Scott AP, Sumpter JP, Hardiman PA (1983b) Hormone changes during ovulation in the rainbow trout (Salmo gairdneri). Gen Comp Endocrinol 49:128–134CrossRefGoogle Scholar
  40. Sower SA, Freamat M, Kavanaugh SI (2009) The origins of the vertebrate hypothalamic–pituitary–gonadal (HPG) and hypothalamic–pituitary–thyroid (HPT) endocrine systems: new insights from lampreys. Gen Comp Endocrinol 161:20–29CrossRefGoogle Scholar
  41. Stuart-Kregor PAC, Sumpter JP, Dodd JM (1981) The involvement of gonadotrophin and sex steroids in the control of reproduction in the parr and adults of Atlantic salmon, Salmo salar L. J Fish Biol 18(1):59–72CrossRefGoogle Scholar
  42. Taghizadeh V, Imanpoor MR, Mehdinejad N (2013) Study the seasonal steroid hormones of common carp in Caspian Sea, Iran. Springerplus 2(1):193CrossRefGoogle Scholar
  43. Ueda H, Hiroi O, Hara A, Yamauchi K, Nahahama Y (1984) Changes in serum concentrations of steroid hormones, thyroxine, and vitellogenin during spawning migration of the chum salmon, Oncorhynchus keta. Gen Comp Endocrinol 53:203–211CrossRefGoogle Scholar
  44. Wallace R, Selman K (1981) Cellular and dynamic aspects of oocyte growth in teleosts. Am Zool 21:325–343CrossRefGoogle Scholar
  45. Wallace EM, Tringali MD (2016) Fishery composition and evidence of population structure and hybridization in the Atlantic bonefish species complex (Albula vulpes). Mar Biol 163:142CrossRefGoogle Scholar
  46. West G (1990) Methods of assessing ovarian development in fishes: a review. Aust J Mar Freshwat Res 41:199–222CrossRefGoogle Scholar
  47. Whitehead C, Bromage NR, Forster JRM, Matty AJ (1978) The effects of alterations in photoperiod on ovarian development and spawning time in the rainbow trout (Salmo gairdneri). Ann Biol Anim Biochim Biophys 18(4):1035–1043CrossRefGoogle Scholar
  48. Wilson C, Scotto L, Scarpa J, Volety A, Laramore S, Haunert D (2005) Survey of water quality, oyster reproduction an oyster health status in the St. Lucie estuary. J Shellfish Res 24(1):157–165CrossRefGoogle Scholar
  49. Zupa R, Rodrõâguez C, Mylonas CC, Rosenfeld H, Fakriadis I, Papadaki M, Pérez J, Pousis C, Basilone G, Corriero A (2017) Comparative study of reproductive development in wild and captive-reared greater amberjack seriola dumerili (Risso, 1810). PLoS One 12(1):1–28CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  • Cameron Luck
    • 1
  • Sahar Mejri
    • 1
  • Justin Lewis
    • 2
  • Paul S. Wills
    • 1
  • Marty Riche
    • 1
  • Jonathan Shenker
    • 3
  • Aaron Adams
    • 1
    • 2
  • Matthew J. Ajemian
    • 1
    Email author
  1. 1.Harbor Branch Oceanographic InstituteFlorida Atlantic UniversityFort PierceUSA
  2. 2.Bonefish and Tarpon TrustCoral GablesUSA
  3. 3.Florida Institute of TechnologyMelbourneUSA

Personalised recommendations