Preliminary investigation of reproductive hormone profiles in the blacktip shark (Carcharhinus limbatus), a placental viviparous species, in southern Florida
Hannah J. Verkamp
A G * , Neil Hammerschlag B C , James Quinlan D , Joseph A. Langan E and James A. Sulikowski F
+ Author Affiliations
- Author Affiliations
A Department of Marine Sciences, University of New England, 11 Hills Beach Road, Biddeford, ME 04005, USA.
B Rosenstiel School of Marine and Atmospheric Science, University of Miami, 4600 Rickenbacker Causeway, Miami, FL 33149, USA.
C Abess Center for Ecosystem Science and Policy, University of Miami, 1365 Memorial Drive No. 230, Coral Gables, FL 33146, USA.
D Department of Mathematical Sciences, University of New England, 11 Hills Beach Road, Biddeford, ME 04005, USA.
E Graduate School of Oceanography, University of Rhode Island, 215 S Ferry Road, Narragansett, RI 02882, USA.
F School of Mathematical and Natural Sciences, Arizona State University West Campus, 4701 W. Thunderbird Road, Glendale, AZ 85306, USA.
G Present address: Commercial Fisheries Research Foundation, PO Box 278, Saunderstown, RI 02874, USA.
Marine and Freshwater Research 73(4) 520-527 https://doi.org/10.1071/MF21235
Submitted: 3 January 2021 Accepted: 17 November 2021 Published: 4 February 2022
© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing.
Abstract
Accurate reproductive information is crucial for the effective management of sharks. Here, we used non-lethal methods to evaluate reproductive hormone profiles of blacktip sharks (Carcharhinus limbatus) off the coast of southern Florida (FL) as part of a preliminary investigation of this species’ reproductive patterns in the region. Circulating testosterone concentrations in males ranged from 0.04 to 320.7 ng mL−1, and concentrations peaked during months previously shown to represent peak spermatogenic activity. In females, circulating concentrations of oestradiol (E2) ranged from 12.5 to 941.4 pg mL−1, and progesterone (P4) ranged from 30.1 to 821.2 pg mL−1. E2 peaked during months with peak vitellogenic and ovulatory activity in previous studies; P4 displayed less variability among months. In general, changes in monthly hormone concentrations align well with the timing of reproductive events in C. limbatus in other regions. However, because of low monthly sample sizes and a lack of reproductive status confirmation, the female profiles raise interesting questions about this population’s reproductive cycle that could be explored in future studies. Additional studies should collect larger monthly samples and incorporate supplementary data to provide more insight into the reproductive cycle of this species in southern FL.
Keywords: elasmobranch, estradiol, hormones, life history, non‐lethal methods, progesterone, testosterone.
References
Awruch, CA (2013). Reproductive endocrinology in chondrichthyans: the present and the future. General and Comparative Endocrinology 192, 60–70.| Reproductive endocrinology in chondrichthyans: the present and the future.Crossref | GoogleScholarGoogle Scholar | 23763870PubMed |
Awruch, CA, Jones, SM, Asorey, MG, and Barnett, A (2014). Non-lethal assessment of the reproductive status of broadnose sevengill sharks (Notorynchus cepedianus) to determine the significance of habitat use in coastal areas. Conservation Physiology 2, cou013.
| Non-lethal assessment of the reproductive status of broadnose sevengill sharks (Notorynchus cepedianus) to determine the significance of habitat use in coastal areas.Crossref | GoogleScholarGoogle Scholar | 27293634PubMed |
Baremore, IE, and Passerotti, MS (2013). Reproduction of the blacktip shark in the Gulf of Mexico. Marine and Coastal Fisheries 5, 127–138.
| Reproduction of the blacktip shark in the Gulf of Mexico.Crossref | GoogleScholarGoogle Scholar |
Branstetter, S (1987). Age and growth estimates for blacktip, Carcharhinus limbatus, and spinner, C. brevipinna, sharks from the northwestern Gulf of Mexico. Copeia 1987, 964.
| Age and growth estimates for blacktip, Carcharhinus limbatus, and spinner, C. brevipinna, sharks from the northwestern Gulf of Mexico.Crossref | GoogleScholarGoogle Scholar |
Brown, AM, Frazier, BS, and Gelsleichter, J (2020). Re-evaluation of reproductive cycle and fecundity of finetooth sharks Carcharhinus isodon (Valenciennes 1839) from the Northwest Atlantic Ocean, with new observations on ovarian cycle and reproductive endocrinology of biennially reproducing sharks. Journal of Fish Biology 97, 1780–1793.
| Re-evaluation of reproductive cycle and fecundity of finetooth sharks Carcharhinus isodon (Valenciennes 1839) from the Northwest Atlantic Ocean, with new observations on ovarian cycle and reproductive endocrinology of biennially reproducing sharks.Crossref | GoogleScholarGoogle Scholar |
Capapé, C, Seck, AA, Diatta, Y, Reynaud, C, Hemida, F, and Zaouali, J (2004). Reproductive biology of the blacktip shark, Carcharhinus limbatus (Chondrichthyes: Carcharhinidae) off West and North African coasts. Cybium 28, 275–284.
Carlson, JK, Sulikowski, JR, and Baremore, IE (2006). Do differences in life history exist for blacktip sharks, Carcharhinus limbatus, from the United States South Atlantic Bight and Eastern Gulf of Mexico. Environmental Biology of Fishes 77, 279–292.
| Do differences in life history exist for blacktip sharks, Carcharhinus limbatus, from the United States South Atlantic Bight and Eastern Gulf of Mexico.Crossref | GoogleScholarGoogle Scholar |
Castro, JI (1996). Biology of the Blacktip shark, Carcharhinus limbatus, off the southeastern United States. Bulletin of Marine Science 59, 508–522.
Coelho, R, and Erzini, K (2010). Depth distribution of the velvet belly, Etmopterus spinax, in relation to growth and reproductive cycle: the case study of a deep-water lantern shark with a wide-ranging critical habitat. Marine Biology Research 6, 381–389.
| Depth distribution of the velvet belly, Etmopterus spinax, in relation to growth and reproductive cycle: the case study of a deep-water lantern shark with a wide-ranging critical habitat.Crossref | GoogleScholarGoogle Scholar |
Compagno LJV (1984) ‘Sharks of the world: an annotated and illustrated catalogue of shark species known to date.’ FAO Fisheries Synopsis 125, FAO Species Catalogue 4. (United Nations Development Programme: Rome, Italy)
Driggers, WB, and Hoffmayer, ER (2009). Variability in the reproductive cycle of finetooth sharks, Carcharhinus isodon, in the northern Gulf of Mexico. Copeia 2009, 390–393.
| Variability in the reproductive cycle of finetooth sharks, Carcharhinus isodon, in the northern Gulf of Mexico.Crossref | GoogleScholarGoogle Scholar |
Driggers, WB, Oakley, DA, Ulrich, G, Carlson, JK, Cullum, BJ, and Dean, JM (2004). Reproductive biology of Carcharhinus acronotus in the coastal waters of South Carolina. Journal of Fish Biology 64, 1540–1551.
| Reproductive biology of Carcharhinus acronotus in the coastal waters of South Carolina.Crossref | GoogleScholarGoogle Scholar |
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, and White, WT (2014). Extinction risk and conservation of the world’s sharks and rays. eLife 3, e00590.
| Extinction risk and conservation of the world’s sharks and rays.Crossref | GoogleScholarGoogle Scholar | 24448405PubMed |
Gallagher, A, Serafy, J, Cooke, S, and Hammerschlag, N (2014). Physiological stress response, reflex impairment, and survival of five sympatric shark species following experimental capture and release. Marine Ecology Progress Series 496, 207–218.
| Physiological stress response, reflex impairment, and survival of five sympatric shark species following experimental capture and release.Crossref | GoogleScholarGoogle Scholar |
Gelsleichter J, Evans AN (2012) Hormonal regulation of elasmobranch physiology. In ‘Biology of sharks and their relatives’, 2nd edn. (Eds JC Carrier, JA Musick and MR Heithaus) pp. 313–338. (CRC Press: Boca Raton, FL, USA).
| Crossref |
Hammerschlag, N, and Sulikowski, J (2011). Killing for conservation: the need for alternatives to lethal sampling of apex predatory sharks. Endangered Species Research 14, 135–140.
| Killing for conservation: the need for alternatives to lethal sampling of apex predatory sharks.Crossref | GoogleScholarGoogle Scholar |
Higgs, JM, Hoffmayer, ER, Sulikowski, JA, Driggers, WB, Stiller, DA, and Hendon, JM (2021). Reproductive biology of the finetooth shark (Carcharhinus isodon) in the northern Gulf of Mexico, with evidence of both annual and biennial reproduction. Marine and Freshwater Research 72, 693–708.
| Reproductive biology of the finetooth shark (Carcharhinus isodon) in the northern Gulf of Mexico, with evidence of both annual and biennial reproduction.Crossref | GoogleScholarGoogle Scholar |
Hoffmayer, ER, Sulikowski, JA, Hendon, JM, and Parsons, GR (2010). Plasma steroid concentrations of adult male Atlantic sharpnose sharks, Rhizoprionodon terraenovae, in the northern Gulf of Mexico, with notes on potential long term shifts in reproductive timing. Environmental Biology of Fishes 88, 1–7.
| Plasma steroid concentrations of adult male Atlantic sharpnose sharks, Rhizoprionodon terraenovae, in the northern Gulf of Mexico, with notes on potential long term shifts in reproductive timing.Crossref | GoogleScholarGoogle Scholar |
Hoffmayer, ER, Driggers, WB, Jones, LM, Hendon, JM, and Sulikowski, JA (2013). Variability in the reproductive biology of the Atlantic sharpnose shark in the Gulf of Mexico. Marine and Coastal Fisheries 5, 139–151.
| Variability in the reproductive biology of the Atlantic sharpnose shark in the Gulf of Mexico.Crossref | GoogleScholarGoogle Scholar |
Hueter, RE, Heupel, MR, Heist, EJ, and Keeney, DB (2005). Evidence of philopatry in sharks and implications for the management of shark fisheries. Journal of Northwest Atlantic Fishery Science 35, 239–247.
| Evidence of philopatry in sharks and implications for the management of shark fisheries.Crossref | GoogleScholarGoogle Scholar |
Irigoyen, A, De Wysiecki, A, Trobbiani, G, Bovcon, N, Awruch, C, Argemi, F, and Jaureguizar, A (2018). Habitat use, seasonality and demography of an apex predator: sevengill shark Notorynchus cepedianus in northern Patagonia. Marine Ecology Progress Series 603, 147–160.
| Habitat use, seasonality and demography of an apex predator: sevengill shark Notorynchus cepedianus in northern Patagonia.Crossref | GoogleScholarGoogle Scholar |
Kajiura, SM, and Tellman, SL (2016). Quantification of massive seasonal aggregations of blacktip sharks (Carcharhinus limbatus) in southeast Florida. PLoS One 11, e0150911.
| Quantification of massive seasonal aggregations of blacktip sharks (Carcharhinus limbatus) in southeast Florida.Crossref | GoogleScholarGoogle Scholar | 27027502PubMed |
Keeney, DB, and Heist, EJ (2006). Worldwide phylogeography of the blacktip shark (Carcharhinus limbatus) inferred from mitochondrial DNA reveals isolation of western Atlantic populations coupled with recent Pacific dispersal: blacktip shark phylogeography. Molecular Ecology 15, 3669–3679.
| Worldwide phylogeography of the blacktip shark (Carcharhinus limbatus) inferred from mitochondrial DNA reveals isolation of western Atlantic populations coupled with recent Pacific dispersal: blacktip shark phylogeography.Crossref | GoogleScholarGoogle Scholar | 17032265PubMed |
Keeney, DB, Heupel, MR, Hueter, RE, and Heist, EJ (2005). Microsatellite and mitochondrial DNA analyses of the genetic structure of blacktip shark (Carcharhinus limbatus) nurseries in the Northwestern Atlantic, Gulf of Mexico, and Caribbean Sea. Molecular Ecology 14, 1911–1923.
| Microsatellite and mitochondrial DNA analyses of the genetic structure of blacktip shark (Carcharhinus limbatus) nurseries in the Northwestern Atlantic, Gulf of Mexico, and Caribbean Sea.Crossref | GoogleScholarGoogle Scholar | 15910315PubMed |
Koob, TJ, and Callard, IP (1999). Reproductive endocrinology of female elasmobranchs: lessons from the little skate (Raja erinacea) and spiny dogfish (Squalus acanthias). The Journal of Experimental Zoology 284, 557–574.
| Reproductive endocrinology of female elasmobranchs: lessons from the little skate (Raja erinacea) and spiny dogfish (Squalus acanthias).Crossref | GoogleScholarGoogle Scholar | 10469994PubMed |
Manire, CA, and Rasmussen, LEL (1997). Serum concentrations of steroid hormones in the mature male bonnethead shark, Sphyrna tiburo. General and Comparative Endocrinology 107, 414–420.
| Serum concentrations of steroid hormones in the mature male bonnethead shark, Sphyrna tiburo.Crossref | GoogleScholarGoogle Scholar | 9268622PubMed |
Manire, CA, Rasmussen, LEL, Hess, DL, and Hueter, RE (1995). Serum steroid hormones and the reproductive cycle of the female bonnethead shark, Sphyrna tiburo. General and Comparative Endocrinology 97, 366–376.
| Serum steroid hormones and the reproductive cycle of the female bonnethead shark, Sphyrna tiburo.Crossref | GoogleScholarGoogle Scholar | 7789751PubMed |
Natanson, LJ, Deacy, BM, Joyce, W, and Sulikowski, J (2019). Presence of a resting population of female porbeagles (Lamna nasus), indicating a biennial reproductive cycle, in the western North Atlantic Ocean. Fishery Bulletin 117, 70–77.
| Presence of a resting population of female porbeagles (Lamna nasus), indicating a biennial reproductive cycle, in the western North Atlantic Ocean.Crossref | GoogleScholarGoogle Scholar |
Nau, MR, O’Brien, JK, Schmitt, TL, Nollens, HH, and Robeck, TR (2018). Diagnostic assessment of reproductive status in white-spotted bamboo sharks (Chiloscyllium plagiosum). Animal Reproduction Science 197, 48–57.
| Diagnostic assessment of reproductive status in white-spotted bamboo sharks (Chiloscyllium plagiosum).Crossref | GoogleScholarGoogle Scholar | 30170880PubMed |
Parsons, GR (1993). Geographic variation in reproduction between two populations of the bonnethead shark, Sphyrna tiburo. Environmental Biology of Fishes 38, 25–35.
| Geographic variation in reproduction between two populations of the bonnethead shark, Sphyrna tiburo.Crossref | GoogleScholarGoogle Scholar |
Parsons GR, Hoffmayer ER, Frank J, Bet-Sayad W (2008) A review of shark reproductive ecology: life history and evolutionary implications. In ‘Fish reproduction’, (Ed. MJ Rocha) pp. 435–469. (CRC Press: Boca Raton, FL, USA).
| Crossref |
Prohaska, BK, Tsang, PCW, Driggers, WB, Hoffmayer, ER, and Sulikowski, JA (2013a). Development of a nonlethal and minimally invasive protocol to study elasmobranch reproduction. Marine and Coastal Fisheries 5, 181–188.
| Development of a nonlethal and minimally invasive protocol to study elasmobranch reproduction.Crossref | GoogleScholarGoogle Scholar |
Prohaska, BK, Tsang, PCW, Driggers, WB, Hoffmayer, ER, Wheeler, CR, Brown, AC, and Sulikowski, JA (2013b). Assessing reproductive status in elasmobranch fishes using steroid hormones extracted from skeletal muscle tissue. Conservation Physiology 1, cot028.
| Assessing reproductive status in elasmobranch fishes using steroid hormones extracted from skeletal muscle tissue.Crossref | GoogleScholarGoogle Scholar | 27293612PubMed |
Rasmussen, LEL, and Gruber, SH (1993). Serum concentrations of reproductively-related circulating steroid hormones in the free-ranging lemon shark, Negaprion brevirostris. Environmental Biology of Fishes 38, 167–174.
| Serum concentrations of reproductively-related circulating steroid hormones in the free-ranging lemon shark, Negaprion brevirostris.Crossref | GoogleScholarGoogle Scholar |
Rigby CL, Carlson J, Chin A, Derrick D, Dicken M, Pacoureau N (2021) Blacktip shark Carcharhinus limbatus. In ‘The IUCN Red List of Threatened Species 2021’. e.T3851A2870736. (International Union for Conservation of Nature and Natural Resources). Available at https://www.iucnredlist.org/species/3851/2870736 [Accessed 17 November 2021]
Simpfendorfer, CA, Heupel, MR, White, WT, and Dulvy, NK (2011). The importance of research and public opinion to conservation management of sharks and rays: a synthesis. Marine and Freshwater Research 62, 518–527.
| The importance of research and public opinion to conservation management of sharks and rays: a synthesis.Crossref | GoogleScholarGoogle Scholar |
Sulikowski, JA, Tsang, PCW, and Huntting Howell, W (2004). An annual cycle of steroid hormone concentrations and gonad development in the winter skate, Leucoraja ocellata, from the western Gulf of Maine. Marine Biology 144, 845–853.
| An annual cycle of steroid hormone concentrations and gonad development in the winter skate, Leucoraja ocellata, from the western Gulf of Maine.Crossref | GoogleScholarGoogle Scholar |
Sulikowski, JA, Driggers, WB, Ford, TS, Boonstra, RK, and Carlson, JK (2007). Reproductive cycle of the blacknose shark Carcharhinus acronotus in the Gulf of Mexico. Journal of Fish Biology 70, 428–440.
| Reproductive cycle of the blacknose shark Carcharhinus acronotus in the Gulf of Mexico.Crossref | GoogleScholarGoogle Scholar |
Sulikowski, J, Wheeler, C, Gallagher, A, Prohaska, B, Langan, J, and Hammerschlag, N (2016). Seasonal and life-stage variation in the reproductive ecology of a marine apex predator, the tiger shark Galeocerdo cuvier, at a protected female-dominated site. Aquatic Biology 24, 175–184.
| Seasonal and life-stage variation in the reproductive ecology of a marine apex predator, the tiger shark Galeocerdo cuvier, at a protected female-dominated site.Crossref | GoogleScholarGoogle Scholar |
Swinsburg W, Kohler NE, McCandless CT (2012) ‘Mark/recapture data for the blacktip shark, Carcharhinus limbatus, in the Gulf of Mexico from the NEFSC Cooperative Shark Tagging Program.’ SEDAR29-WP-16. (SEDAR: North Charleston, SC, USA.)
Tinari, AM, and Hammerschlag, N (2021). An ecological assessment of large coastal shark communities in South Florida. Ocean and Coastal Management 211, 105772.
| An ecological assessment of large coastal shark communities in South Florida.Crossref | GoogleScholarGoogle Scholar |
Tsang, PCW, and Callard, IP (1987). Morphological and endocrine correlates of the reproductive cycle of the aplacental viviparous dogfish, Squalus acanthias. General and Comparative Endocrinology 66, 182–189.
| Morphological and endocrine correlates of the reproductive cycle of the aplacental viviparous dogfish, Squalus acanthias.Crossref | GoogleScholarGoogle Scholar |
Weigmann, S (2016). Annotated checklist of the living sharks, batoids and chimaeras (Chondrichthyes) of the world, with a focus on biogeographical diversity: annotated global checklist of chondrichthyes. Journal of Fish Biology 88, 837–1037.
| Annotated checklist of the living sharks, batoids and chimaeras (Chondrichthyes) of the world, with a focus on biogeographical diversity: annotated global checklist of chondrichthyes.Crossref | GoogleScholarGoogle Scholar | 26860638PubMed |
Yano, K, and Tanaka, S (1988). Size at maturity, reproductive cycle, fecundity, and depth segregation of the deep sea squaloid sharks Centroscymnus owstoni and C. coelolepis in Suruga Bay, Japan. Nippon Suisan Gakkaishi 54, 167–174.
| Size at maturity, reproductive cycle, fecundity, and depth segregation of the deep sea squaloid sharks Centroscymnus owstoni and C. coelolepis in Suruga Bay, Japan.Crossref | GoogleScholarGoogle Scholar |
Wood, SN (2011). Fast stable restricted maximum likelihood and marginal likelihood estimation of semiparametric generalized linear models. Journal of the Royal Statistical Society (B) 73, 3–36.
Wood SN (2017) ‘Generalized additive models: an introduction with R.’ 2nd edn. (CRC Press: Boca Raton, FL, USA)
