Abstract
Energetic condition is one of the most important factors that influence fitness and reproductive performance in vertebrates. Yet, we lack evidence on how energetic states change in response to reproduction in large marine vertebrates. In the present study, we used a non-lethal approach to assess relationships among reproductive stage, circulating steroid hormones (testosterone and relative corticosteroid levels), plasma fatty acids, and the ketone body β-hydroxybutyrate in male sharks of two species with divergent ecologies, the benthic nurse shark (Ginglymostoma cirratum) and the epipelagic blacktip shark (Carcharhinus limbatus). We found higher relative corticosteroid levels in adult nurse sharks during the pre-mating period and in blacktip sharks during the mating period. Higher levels of β-hydroxybutyrate were found in adult nurse sharks during the mating period, but concentrations of this ketone body did not significantly vary across reproductive stages in blacktip sharks. We also detected reduced percentages of essential fatty acids during the mating period of both nurse and blacktip sharks. Taken together, our findings suggest that nurse and blacktip sharks differ in their energetic strategy to support reproduction, however, they likely rely on physiologically important fatty acids during mating, to support spermatogenesis.
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References
Arts MT, Kohler CC (2009) Health and condition in fish: the influence of lipids on membrane competency and immune response. In: Arts MT, Brett MT, Kainz MJ (eds) Lipids in aquatic ecosystems. Springer, New York, pp 237–256
Awruch CA (2013) Reproductive endocrinology in chondrichthyans: the present and the future. Gen Comp Endocrinol 192:60–70. https://doi.org/10.1016/j.ygcen.2013.05.021
Awruch CA (2016) Reproduction strategies. In: Shadwick RE, Farrell P, Brauner CJ (eds) Physiology of Elasmobranch Fishes, in Fish Physiology, vol. 34A, Academic Press, New York, pp. 255‒310. https://doi.org/10.1016/B978-0-12-801289-5.00007-9
Baeza R, Mazzeo I, Vílchez MC, Gallego V, Peñaranda DS, Pérez L, Asturiano JF (2014) Effect of thermal regime on fatty acid dynamics in male European eels (Anguilla anguilla) during hormonally-induced spermatogenesis. Aquac 430:86–97. https://doi.org/10.1016/j.aquaculture.2014.03.045
Baeza R, Mazzeo I, Vílchez MC, Gallego V, Peñaranda DS, Pérez L, Asturiano JF (2015) Relationship between sperm quality parameters and the fatty acid composition of the muscle, liver and testis of European eel. Comp Biochem Phys A 181:79–86. https://doi.org/10.1016/j.cbpa.2014.11.022
Baremore IE, Passerotti MS (2013) Reproduction of the blacktip shark in the Gulf of Mexico. Mar Coast Fish 5:127–138. https://doi.org/10.1080/19425120.2012.758204
Becerril-García EE, Arellano-Martínez M, Bernot-Simon D, Hoyos-Padilla EM, Galván-Magaña F, Godard-Codding C (2020) Steroid hormones and chondrichthyan reproduction: physiological functions, scientific research, and implications for conservation. Peer J 8:e9686. https://doi.org/10.7717/peerj.9686
Beckmann CL, Mitchell JG, Stone DAJ, Huveneers C (2014) Inter-tissue differences in fatty acid incorporation as a result of dietary oil manipulation in Port Jackson sharks (Heterodontus portusjacksoni). Lipids 49:577–590. https://doi.org/10.1007/s11745-014-3887-6
Bobe J, Labbé C (2010) Egg and sperm quality in fish. Gen Comp Endocrinol 165:535–548. https://doi.org/10.1016/j.ygcen.2009.02.011
Budge SM, Iverson SJ, Koopman HN (2006) Studying trophic ecology in marine ecosystems using fatty acids: a primer on analysis and interpretation. Mar Mamm Sci 22:759–801. https://doi.org/10.1111/j.1748-7692.2006.00079.x
Burgess HG, Branstetter S (2009) Carcharhinus limbatus. The IUCN Red List of Threatened Species. 2009:e.T3851A10124862. Available from: https://doi.org/10.2305/IUCN.UK.2009-2.RLTS.T3851A10124862.en
Carlson J, Charvet P, Blanco-Parra MP, Briones Bell-lloch A, Cardenosa D, Derrick D, Espinoza E, Herman K, Morales-Saldaña JM, Naranjo-Elizondo B, Pérez Jiménez JC, Schneider EVC, Simpson NJ, Talwar BS, Pollom R, Pacoureau N, Dulvy NK (2021) Ginglymostoma cirratum. The IUCN Red List Threatened Species 2021:e.T144141186A3095153. https://doi.org/10.2305/IUCN.UK.2021-1.RLTS.T144141186A3095153.en
Castro JI (1996) Biology of the blacktip shark, Carcharhinus limbatus, off the southeastern United States. Bull Mar Sci 59:508–522
Castro JI (2000) The biology of the nurse shark, Ginglymostoma cirratum, off the Florida east coast and the Bahama Islands. Environ Biol Fish 58:1–22. https://doi.org/10.1023/A:1007698017645
Clark CJ (2012) The role of power versus energy in courtship: what is the ‘energetic cost’of a courtship display? Anim Behav 84:269–277. https://doi.org/10.1016/j.anbehav.2012.04.012
Colbachini H, Pizzutto CS, Jorge-Neto PN, Gutierrez RC, Gadig OBF (2020) Body movement as an indicator of proceptive behavior in nurse sharks (Ginglymostoma cirratum). Environ Biol Fish 103:1257–1263. https://doi.org/10.1007/s10641-020-01018-y
Colombo SM, Wacker A, Parrish CC, Kainz MJ, Arts MT (2017) A fundamental dichotomy in long-chain polyunsaturated fatty acid abundance between and within marine and terrestrial ecosystems. Environ Rev 25:163–174. https://doi.org/10.1139/er-2016-0062
Cortés E (2000) Life history patterns and correlations in sharks. Rev Fish Sci 8:299–344
Crespi EJ, Williams TD, Jessop TS, Delehanty B (2013) Life history and the ecology of stress: how do glucocorticoid hormones influence life-history variation in animals? Funct Ecol 27:93–106. https://doi.org/10.1111/1365-2435.12009
Dalsgaard J, John MS, Kattner G, Müller-Navarra D, Hagen W (2003) Fatty acid trophic markers in the pelagic marine environment. Adv Mar Biol 46:225–340. https://doi.org/10.1016/S0065-2881(03)46005-7
Dudley SFJ, Cliff G (1993) Sharks caught in the protective gill nets off Natal, South Africa. 7. The blacktip shark Carcharhinus limbatus (Valenciennes). Afr J Mar Sci 13:237–254. https://doi.org/10.2989/025776193784287356
Dulvy NK, Forrest RE (2010) Life histories, population dynamics, and extinction risks in chondrichthyans. In Carrier JC, Musick JA, Heithaus MR, Sharks and Their Relatives II: Biodiversity, Adaptive Physiology, and Conservation. CRC Press, pp. 655–696
Ebert DA, Dando M, Fowler S (2021) Sharks of the World: A complete guide. Princeton University Press. Princeton, New Jersey, USA, p 607
Evans AN, Rimoldi JM, Gadepalli RS, Nunez BS (2010) Adaptation of a corticosterone ELISA to demonstrate sequence-specific effects of angiotensin II peptides and C-type natriuretic peptide on 1α-hydroxycorticosterone synthesis and steroidogenicmRNAs in the elasmobranch interrenal gland. J Steroid Biochem Mol Biol 120:149–154. https://doi.org/10.1016/j.jsbmb.2010.03.025
Gallagher AJ, Serafy JE, Cooke SJ, Hammerschlag N (2014) Physiological stress response, reflex impairment, and survival of five sympatric shark species following experimental capture and release. Mar Ecol Prog Ser 496:207–218. https://doi.org/10.3354/meps10490
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 26:389–401. https://doi.org/10.1023/B:FISH.0000009292.70958.65
Gonzalez De AM, Frazier BS, Belcher C, Gelsleichter J (2020) Reproductive cycle and fecundity of the bonnethead Sphyrna tiburo L. from the northwest Atlantic Ocean. J Fish Biol 97:1733–1747. https://doi.org/10.1111/jfb.14537
Hamlett WC, Kormanik GA, Storrie M, Stevens B, Walker TI (2005) Chondrichthyan parity, lecithotrophy and matrotrophy. In: Hamlett WC (ed) Reproductive biology and phylogeny of Chondrichthyes: sharks, batoids and chimaeras. Science, Enfield, NH, pp 395−434
Hammer Ø, Harper DA, Ryan PD (2001) PAST: Paleontological statistics software package for education and data analysis. Palaeontol Electron 4:1–9
Hammerschlag N, Skubel RA, Sulikowski J, Irschick DJ, Gallagher AJ (2018) A comparison of reproductive and energetic states in a marine apex predator (the Tiger Shark, Galeocerdo cuvier). Physiol Bioch Zool 91:933–942. https://doi.org/10.1086/698496
Hoffmayer ER, Sulikowski JA, Hendon JM, 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. Environ Biol Fishes 88:1–7. https://doi.org/10.1007/s10641-010-9603-3
Hu J, Zhang Z, Shen WJ, Azhar S (2010) Cellular cholesterol delivery, intracellular processing and utilization for biosynthesis of steroid hormones. Nutr Metab 7:47. https://doi.org/10.1186/1743-7075-7-47
Iki A, Anderson WG, Deck CA, Ogihara MH, Ikeba K, Kataoka H, Hyodo S (2020) Measurement of 1α hydroxycorticosterone in the Japanese banded houndshark, Triakis scyllium, following exposure to a series of stressors. Gen Comp Endocrinol 292:113440. https://doi.org/10.1016/j.ygcen.2020.113440
Iverson SJ (2009) Tracing aquatic food webs using fatty acids: from qualitative indicators to quantitative determination. In: Arts MT, Brett MT, Kainz M (eds) Lipids in aquatic ecosystems. Springer, New York, NY, pp 281−308
Izquierdo MS, Fernandez-Palacios H, Tacon AGJ (2001) Effect of broodstock nutrition on reproductive performance of fish. Aquac 197:25–42. https://doi.org/10.1016/S0044-8486(01)00581-6
Kajiura SM, Tellman SL (2016) Quantification of massive seasonal aggregations of blacktip sharks (Carcharhinus limbatus) in Southeast Florida. PLoS ONE 11:e0150911. https://doi.org/10.1371/journal.pone.0150911
Kelly JR, Scheibling RE (2012) Fatty acids as dietary tracers in benthic food webs. Mar Ecol Prog Ser 446:1–22. https://doi.org/10.3354/meps09559
Le Moal M, Gascuel-Odoux C, Ménesguen A, Souchon Y, Étrillard C, Levain A, Pinay G (2019) Eutrophication: a new wine in an old bottle? Sci Total Environ 651:1–11. https://doi.org/10.1016/j.scitotenv.2018.09.139
Lund I, Steenfeldt SJ, Banta G, Hansen BW (2008) The influence of dietary concentrations of arachidonic acid and eicosapentaenoic acid at various stages of larval ontogeny on eye migration, pigmentation and prostaglandin content of common sole larvae (Solea solea L.). Aquaculture 276(1–4):143–153
Lyons K, Wynne-Edwards KE (2019) Legacy environmental polychlorinated biphenyl contamination attenuates the acute stress response in a cartilaginous fish, the Round Stingray. Stress 22:395–402. https://doi.org/10.1080/10253890.2019.1570125
Manire CA, Rasmussen LEL (1997) Serum concentrations of steroid hormones in the mature male bonnethead shark, Sphyrna tiburo. Gen Comp Endocrinol 107:414–420. https://doi.org/10.1006/gcen.1997.6937
Manire CA, Rasmussen LEL, Maruska KP, Tricas TC (2007) Sex, seasonal, and stress-related variations in elasmobranch corticosterone concentrations. Comp Biochem Physiol A Mol Integr Physiol 148:926–935. https://doi.org/10.1016/j.cbpa.2007.09.017
McMeans BC, Arts MT, Fisk AT (2012) Similarity between predator and prey fatty acid profiles is tissue dependent in Greenland sharks (Somniosus microcephalus): implications for diet reconstruction. J Exp Mar Biol Ecol 429:55–63. https://doi.org/10.1016/j.jembe.2012.06.017
Mercure F, Van der Kraak G (1995) Inhibition of gonadotropin-stimulated ovarian steroid production by polyunsaturated fatty acids in teleost fish. Lipids 30:547–554. https://doi.org/10.1007/BF02537030
Moorhead SG, Gallagher AJ, Merly L, Hammerschlag N (2020) Variation of body condition and plasma energy substrates with life stage, sex, and season in wild-sampled nurse sharks Ginglymostoma cirratum. In press, J Fish Biol
Norambuena F, Estévez A, Mañanós E, Bell JG, Carazo I, Duncan N (2013) Effects of graded levels of arachidonic acid on the reproductive physiology of Senegalese sole (Solea senegalensis): Fatty acid composition, prostaglandins and steroid levels in the blood of broodstock bred in captivity. Gen Comp Endocrinol 191:92–101. https://doi.org/10.1016/j.ygcen.2013.06.006
Parrish CC (2009) Essential fatty acids in aquatic food webs. In: Arts MT, Brett MT, Kainz MJ (eds) Lipids in aquatic ecosystems. Springer, New York, NY, pp 309–326
Parrish CC, Abrajano TA, Budge SM, Helleur RJ, Hudson ED, Pulchan K, Ramos C (2000) Lipid and phenolic biomarkers in marine ecosystem: analysis and applications. In: Wangersky PJ (ed) Marine Chemistry. Springer, New York, NY, pp 193–212
Parrish CC, Nichols PD, Pethybridge H, Young JW (2015) Direct determination of fatty acids in fish tissues: quantifying top predator trophic connections. Oecologia 177:85–95. https://doi.org/10.1007/s00442-014-3131-3
Pérez L, Asturiano JF, Tomás A, Zegrari S, Barrera R, Espinós FJ, Navarro JC, Jover M (2000) Induction of maturation and spermiation in the male European eel: assessment of sperm quality throughout treatment. J Fish Biol 57:1488–1504. https://doi.org/10.1111/j.1095-8649.2000.tb02227.x
Pratt HL, Carrier JC (2001) A review of elasmobranch reproductive behavior with a case study on the nurse shark, Ginglymostoma cirratum. Environ Biol Fish 60:157–188. https://doi.org/10.1023/A:1007656126281
Pratt HL, Pratt TC, Morley D, Lowerre-Barbieri S, Collins A, Carrier JC, Hart KM, Whitney NM (2018) Partial migration of the nurse shark, Ginglymostoma cirratum (Bonnaterre), from the Dry Tortugas Islands. Environ Biol Fish 101:515–530. https://doi.org/10.1007/s10641-017-0711-1
Rangel BS, Hussey NE, Niella Y, Martinelli LA, Gomes AD, Moreira RG (2020) Neonatal nutritional strategy of a viviparous elasmobranch with extremely low reproductive output. Mar Ecol Prog Ser 638:107–121. https://doi.org/10.3354/meps13261
Rangel BS, Hammerschlag N, Sulikowski J, Moreira RG (2021a) Dietary and reproductive biomarkers in a generalist apex predator reveal differences in nutritional ecology across life stages. Mar Ecol Prog Ser 664:149–163. https://doi.org/10.3354/meps13640
Rangel BS, Hammerschlag N, Moreira RG (2021b) Urban living influences the nutritional quality of a juvenile shark species. Sci Total Environ 776:146025. https://doi.org/10.1016/j.scitotenv.2021.146025
Rêgo MG, Fitzpatrick J, Hazin FH, de Araújo MLG, Silveira LM, Oliveira PG, Evêncio-Neto J (2015) Characterization of testicular morphology and spermatogenesis in the nurse sharks Ginglymostoma cirratum (Bonnaterre, 1788). Zoomorphology 134:117–123. https://doi.org/10.1007/s00435-014-0240-9
Romero LM (2002) Seasonal changes in plasma glucocorticoid concentrations in free-living vertebrates. Gen Comp Endocrinol 128:1–24. https://doi.org/10.1016/S0016-6480(02)00064-3
Romero LM, Wingfield JC (2015) Tempests, poxes, predators, and people: stress in wild animals and how they cope. Oxford University Press, New York, NY, p 614. https://doi.org/10.1093/acprof:oso/9780195366693.001.0001
Ruiz-Jarabo I, Barragán-Méndez C, Jerez-Cepa I, Fernández-Castro M, Sobrino I, Mancera JM, Aerts J (2019) Plasma 1α-hydroxycorticosterone as biomarker for acute stress in catsharks (Scyliorhinus canicula). Front Physiol 10:1217. https://doi.org/10.3389/fphys.2019.01217
Sardenne F, Kraffe E, Amiel A, Fouché E, Debrauwer L, Ménard F, Bodin N (2017) Biological and environmental influence on tissue fatty acid compositions in wild tropical tunas. Comp Biochem Physiol A Mol Integr Physiol 204:17–27. https://doi.org/10.1016/j.cbpa.2016.11.007
Speers-Roesch B, Treberg JR (2010) The unusual energy metabolism of elasmobranch fishes. Comp Biochem Physiol A Mol Integr Physiol 155:417–434. https://doi.org/10.1016/j.cbpa.2009.09.031
Soulsbury CD (2019) Income and capital breeding in males: energetic and physiological limitations on male mating strategies. J Exp Biol 222:184895. https://doi.org/10.1242/jeb.184895
Tinari AM, Hammerschlag N (2021) An ecological assessment of large coastal shark communities in South Florida. Ocean Coast Manag 211(1):105772. https://doi.org/10.1016/j.ocecoaman.2021.105772
Tocher DR (2003) Metabolism and functions of lipids and fatty acids in teleost fish. Rev Fish Sci 11:107–184. https://doi.org/10.1080/713610925
Tocher DR (2010) Fatty acid requirements in ontogeny of marine and freshwater fish. Aquacult Res 41:717–732. https://doi.org/10.1111/j.1365-2109.2008.02150.x
Valls E, Navarro J, Barria C, Coll M, Fernandez-Borras J, Rotllant G (2016) Seasonal, ontogenetic and sexual changes in lipid metabolism of the small-spotted catshark (Scyliorhinus canicula) in deep-sea free-living conditions. J Exper Mar Biol Ecol 483:59–63. https://doi.org/10.1016/j.jembe.2016.07.001
Verkamp H (2019) Nonlethal assessment of reproductive parameters in sharks: studies on the blacktip shark (Carcharhinus limbatus) and white shark (Carcharodon carcharias), Master Thesis, University of New England
Wathes DC, Abayasekara DRE, Aitken RJ (2007) Polyunsaturated fatty acids in male and female reproduction. Biol Reprod 77:190–201. https://doi.org/10.1095/biolreprod.107.060558
Whitney NM, Lear KO, Gaskins LC, Gleiss AC (2016) The effects of temperature and swimming speed on the metabolic rate of the nurse shark (Ginglymostoma cirratum, Bonaterre). J Exp Mar Biol Ecol 477:40–46. https://doi.org/10.1016/j.jembe.2015.12.009
Williams CT, Klaassen M, Barnes BM, Buck CL, Arnold W, Giroud S, Vetter SG, Ruf T (2017) Seasonal reproductive tactics: annual timing and the capital-to-income breeder continuum. Philos Trans R Soc B Biol Sci 372:20160250. https://doi.org/10.1098/rstb.2016.0250
Wood CM, Walsh PJ, Kajimura M, McClelland GB, Chew SF (2010) The influence of feeding and fasting on plasma metabolites in the dogfish shark (Squalus acanthias). Comp Biochem Physiol A Mol Integr Physiol 155:435–444. https://doi.org/10.1016/j.cbpa.2009.09.006
Acknowledgements
We deeply acknowledge the members of the University of Miami Shark Research and Conservation Program, especially Abigail Tinari, for research support. We also thank Kelly Quinn and Alexandre Huber for the courtesy of allowing us to use the illustrations.
Funding
Disney Conservation Fund, The Batchelor Foundation, Save Our Seas Foundation, Fundação de Amparo à Pesquisa do Estado de São Paulo- FAPESP (Grants #2014/16320-7 and #2017/25273-0, PhD’s scholarship to BSR).
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Communicated by Donovan P German.
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S. Rangel, B., Hammerschlag, N., Sulikowski, J.A. et al. Physiological markers suggest energetic and nutritional adjustments in male sharks linked to reproduction. Oecologia 196, 989–1004 (2021). https://doi.org/10.1007/s00442-021-04999-4
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DOI: https://doi.org/10.1007/s00442-021-04999-4