Skip to main content

Advertisement

Log in

Bonefish (Albula vulpes) oocyte lipid class and fatty acid composition related to their development

  • Published:
Environmental Biology of Fishes Aims and scope Submit manuscript

Abstract

Bonefish (Albula vulpes) are a valuable fishery resource of tropical and subtropical ecosystems worldwide. Despite their importance, there is limited information on bonefish life history and ecology. The present study aims to describe, for the first time, oocytes development and their lipid characteristics in wild bonefish during the reproductive season in different tidal flat locations in Grand Bahama Island, Bahamas. Our results have shown that Bonefish follow group-synchronous ovarian development and produce lipid-rich eggs [total lipid (TL) content was >26% of wet mass (WM)]. The major lipid class was a neutral lipid: the wax esters and steryl esters (WE-SE; >48% of TL), suggesting their use to support buoyancy and/or energy storage. Fatty acid (FA) composition of bonefish oocytes was characterized by high levels of monoenes in the neutral lipid fraction (i.e. 16:1 and 18:1n-9) indicating their probable role as energy fuel. However, the most abundant fatty acids in the polar lipids were docosahexaenoic acid (DHA; 22:6 n-3 > 15% of total polar FA), eicosapentaenoic acid (EPA; 20:5 n-3 > 13% of total polar FA) and arachidonic acid (ARA; 20:4 n-6 > 4% of total polar FA) which were selectively conserved among the tidal flat locations, suggesting their importance as essential constituents of cell membranes during the development of bonefish oocytes. Our results bring useful information concerning the reproductive physiology of bonefish and not only serve as a benchmark for determining the nutrient requirements to produce high quality eggs from bonefish captive broodstock, but also will help establish meaningful management practices for this species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

ALC:

fatty alcohol

ARA:

arachidonic acid

BB:

Barbary beach

CA:

cortical alveolus

CBE:

Crabbing Bay east

DHA:

docosahexaenoic acid

EFA:

essential fatty acids

EPA:

eicosapentaenoic acid

FA:

fatty acid

FFA:

free fatty acids

HC:

hydrocarbon

KET:

ketones

LV:

late vitellogenic

MUFA:

monunsaturated fatty acids

PL:

phospholipids

PG:

primary growth

PUFA:

polyunsaturated fatty acids

SDWC:

South Deep Water Caye

SFA:

saturated fatty acids

ST:

sterols

TAG:

triacylglycerol

TL:

total lipids

WE-SE:

wax ester - steryl ester

WM:

wet mass

References

  • Alexander EC (1961) A contribution to the life history, biology and geographical distribution of bonefish, Albula vulpes (Linnaeus). Carlsberg Foundation. Copenhagen, Netherlands, p 51

    Google Scholar 

  • Anderson AJ, Arthington AH, Anderson S (1990) Lipid classes and fatty acid composition of the eggs of some Australian fish. Comp Biochem Physiol B Biochem Mol Biol 96(2):267–270

    Article  Google Scholar 

  • Arendt KE, Jonasdottir SH, Hansen PJ, Gartner S (2005) Effects of dietary fatty acids on the reproductive success of the calanoid copepod Temora longicornis. Mar Biol 146:513–530

    Article  CAS  Google Scholar 

  • Asturiano JF, Sorbera LA, Ramos J, Kime DE, Carrilo M, Zanuy S (2000) Hormonal regulation of the European sea bass reproductive cycle: an individualized female approach. J Fish Biol 56(5):1155–1172

    Article  CAS  Google Scholar 

  • Asturiano JF, Sorbera LA, Ramos Jara J, Kime DE, Carrillo M, Zanuy S (2002) Group-synchronous ovarian development, spawning and spermiation in the European sea bass (Dicentrarchus labrax L.) could be regulated by shifts in gonadal steroidogenesis. Sci Mar 66(3):273–282

    Article  Google Scholar 

  • Bachan MM, Fleming IA, Trippel EA (2012) Maternal allocation of lipid classes and fatty acids with seasonal egg production in Atlantic cod (Gadus morhua) of wild origin. Mar Biol 159(10):2281–2297

    Article  CAS  Google Scholar 

  • 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 15:285–290

    Google Scholar 

  • Bell JG, Sargent JR (2003) Arachidonic acid in aquaculture feeds: current status and future opportunities. Aquaculture 218(1–4):491–499

    Article  CAS  Google Scholar 

  • Bell JG, Tocher DR, Sargent JR, Sargent JR (1994) Effect of supplementation with 20:3(n-6), 20:4(n-6) and 20:5(n-3) on the production of prostaglandins E and F of the 1-, 2- and 3-series in turbot (Scophthalmus maximus) brain astroglial cells in primary culture. Biochim Biophys Acta 1211:335–342

    Article  CAS  Google Scholar 

  • Bessonart M, Izquierdo MS, Salhi M, Hernández-Cruz CM, González MM, Fernández-Palacios H (1999) Effect of dietary arachidonic acid levels on growth and survival of gilthead sea bream (Sparus aurata L.) larvae. Aquaculture 179(1):265–275

    Article  CAS  Google Scholar 

  • Bogevik AS (2011) Marine wax ester digestion in salmonid fish: a review. Aquac Res 42(11):1577–1593

    Article  CAS  Google Scholar 

  • Bransden MP, Battaglene SC, Goldsmid RM, Dunstan GA, Nichols PD (2007) Broodstock condition, egg morphology and lipid content and composition during the spawning season of captive striped trumpeter, Latris lineata. Aquaculture 268(1):2–12

    Article  CAS  Google Scholar 

  • Brooks S, Tyler CR, Sumpter JP (1997) Egg quality in fish: what makes a good egg? Rev Fish Biol Fish 7(4):387–416

    Article  Google Scholar 

  • Carrillo M, Bromage N, Zanuy S, Serrano R, Prat F (1989) The effect of modifications in photoperiod on spawning time, ovarian development and egg quality in the sea bass (Dicentrarchus labrax L.). Aquaculture 81(3):351–365

    Article  Google Scholar 

  • Colton DE, Alevizon WS (1983) Feeding ecology of bonefish in bahamian waters. Trans Am Fish Soc 112(2A):178–184

    Article  Google Scholar 

  • Copeman L, Laurel B (2010) Experimental evidence of fatty acid limited growth and survival in Pacific cod larvae. Mar Ecol Prog Ser 412:259–272

    Article  CAS  Google Scholar 

  • Copeman LA, Parrish CC, Brown JA, Harel M (2002) Effects of docosahexaenoic, eicosapentaenoic, and arachidonic acids on the early growth, survival, lipid composition and pigmentation of yellowtail flounder (Limanda ferruginea): a live food enrichment experiment. Aquaculture 210(1):285–304

    Article  CAS  Google Scholar 

  • Crabtree RE, Snodgrass D, Harnden CW (1997) Maturation and reproductive seasonality in bonefish, Albula vulpes, from the waters of the Florida keys. Fish Bull 95:456–465

    Google Scholar 

  • 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(4):754–766

    Google Scholar 

  • Crockett EL (1998) Cholesterol function in plasma membranes from ectotherms: membrane specific roles in adaptation to temperature. Am Zool 38:291–304

    Article  CAS  Google Scholar 

  • Danylchuk A, Danylchuk SE, Cooke SJ, Goldberg TL, Koppelman J, Philipp DP (2008) Ecology and management of bonefish (Albula spp) in the Bahamian archipelago. In: Ault JS (ed) Biology and management of the world tarpon and bonefish fisheries. CRC press. Florida, Boca Raton, pp 79–92

    Google Scholar 

  • Danylchuk AJ et al (2011) Aggregations and offshore movements as indicators of spawning activity of bonefish (Albula vulpes) in the Bahamas. Mar Biol 158(9):1981–1999

    Article  Google Scholar 

  • Eldridge MF, Joseph JD, Taberski KM, Seaborn GT (1983) Lipid and fatty acid composition of the endogenous energy sources of striped bass (Morone saxatilis) eggs. Lipids 18:510–513

    Article  CAS  Google Scholar 

  • Falk-Petersen S, Sargent JR, Hopkins CCE, Vaja B (1982) Ecological investigations on the zooplankton community of Balsfjorden, northern Norway: lipids in the euphausiids Thysanoessa raschi and T. inermis during spring. Mar Biol 68(1):97–102

    Article  CAS  Google Scholar 

  • Fedler T (2010) The economic impact of flats fishing in the Bahamas. Report, the Bahamas National Trust, bonefish and tarpon trust, Fisheries Conservation Foundation

  • Fedler T (2013) Economic impact of the Florida keys flats fishery. Report, Bonefish and tarpon trust, Key Largo, Florida

  • Fedler T (2014) 2013 Economic impact of flats fishing in Belize. Report, Bonefish and tarpon trust, Key Largo, Florida

  • Folch J, Lees M, Sloane Stanley GH (1957) A simple method for the isolation and purification of total lipids from animal tissues. Biol Chem 226(1):497–509

    CAS  Google Scholar 

  • Fuiman LA, Faulk CK (2013) Batch spawning facilitates transfer of an essential nutrient from diet to eggs in a marine fish. Biol Lett 9:20130593

    Article  Google Scholar 

  • Fuiman LA, Ojanguren AF (2011) Fatty acid content of eggs determines antipredator performance of fish larvae. J Exp Mar Biol Ecol 407:155–165

    Article  CAS  Google Scholar 

  • Fuiman LA, Connelly TL, Lowerre-Barbieri SK, McClelland JW (2015) Egg boons: central components of marine fatty acid food webs. Ecology 96(2):362–372

    Article  Google Scholar 

  • Harel M, Tandler A, Kissil GW, Applebaum SW (1994) The kinetics of nutrient incorporation into body tissues of gilthead seabream (Sparus aurata) females and the subsequent effects on egg composition and egg quality. Br J Nutr 72:45–58

    Article  CAS  Google Scholar 

  • Howard R, Stanley D (1999) The tie that binds: eicosanoids in invertebrate biology. Ann Entomol Soc Am 92:880–890

    Article  CAS  Google Scholar 

  • Ishizaki Y, Masuda R, Uematsu K, Shimizu K, Arimoto MT (2001) The effect of dietary docosahexaenoic acid on schooling behavior and brain development in larval yellowtail. J Fish Biol 58:1691–1703

    Article  CAS  Google Scholar 

  • Johannes R, Yeeting B (2000) I-Kiribati knowledge and management of Tarawa’s lagoon resources. Atoll Res Bull 498:1–24

    Article  Google Scholar 

  • Kayama M, Hirata HT (1986) Effect of water temperature on the desaturation of fatty acids in carp. Bull Jpn Soc Sci Fish 52(5):853–857

    Article  CAS  Google Scholar 

  • Kjørsvik E, Mangor-Jensen A, Holmefjord I (1990) Egg quality in fishes. In: Blaxter JHS, Southward AJ (eds) Advances in marine biology, vol 26. Academic Press, New York, pp 71–113

    Google Scholar 

  • Koven W et al (2001) The effect of dietary arachidonic acid (20:4n−6) on growth, survival and resistance to handling stress in gilthead seabream (Sparus aurata) larvae. Aquaculture 193(1):107–122

    CAS  Google Scholar 

  • Lepage G, Roy C (1984) Improved recovery of fatty acid through direct transesterification without prior extraction or purification. J Lipid Res 25:1391–1396

    CAS  Google Scholar 

  • March BE (1993) Essential fatty acids in fish physiology. Can J Physiol Pharmacol 71(9):684–689

    Article  CAS  Google Scholar 

  • Marteinsdottir G, Begg GA (2002) Essential relationships incorporating the influence of age, size and condition on variables required for estimation of reproductive potential in Atlantic cod Gadus morhua. Mar Ecol Prog Ser 235:235–256

    Article  Google Scholar 

  • Marty Y, Delaunay F, Moal J, Samain JF (1992) Changes in the fatty acid composition of Pecten maximus (L.) during larval development. J Exp Mar Biol Ecol 163(2):221–234

    Article  CAS  Google Scholar 

  • Mayer I, Shackley SE, Witthames PR (1990) Aspects of the reproductive biology of the bass, Dicentrarchus labrax L. II. Fecundity and pattern of oocyte development. J Fish Biol 36(2):141–148

    Article  Google Scholar 

  • McKenzie DJ, Higgs DA, Dosanjh BS, Deacon G, Randall DJ (1998) Dietary fatty acid composition inluences swimming performance in Atlantic salmon (Salmo salar) in seawater. Fish Physiol Biochem 19:111–122

    Article  CAS  Google Scholar 

  • Mejri S, Tremblay R, Vandenberg G, Moren M, Khemis IB, Audet C (2017) Differences in nutrient content of eggs and larvae as indicators for improvement of broodstock nutrition in walleye (Sander vitreus) production. Can J Zool 95(5):299–310

    Article  CAS  Google Scholar 

  • Mojica RJ, Shenker JM, Harnden CW, Wagner DE (1995) Recruitment of bonefish, Albula vulpes, around lee stocking island, Bahamas. Fish Bull 93(4):666–674

    Google Scholar 

  • Montero D et al (2003) Vegetable lipid sources for gilthead seabream (Sparus aurata): effects on fish health. Aquaculture 225:353–370

    Article  CAS  Google Scholar 

  • Mourente G, Vázquez R (1996) Changes in the content of total lipid, lipid classes and their fatty acids of developing eggs and unfed larvae of the Senegal sole (Solea senegalensis). Fish Physiol Biochem 15(3):221–235

    Article  CAS  Google Scholar 

  • Murchie KJ (2010) Physiological ecology and behaviour of bonefish (Albula vulpes) in tropical tidal flats ecosystems. Carleton University, Dissertation

    Book  Google Scholar 

  • Murua H, Saborido-Rey F (2003) Female reproductive strategies of marine fish species of the North Atlantic. J Northwest Atl Fish Sci 31:23–31

    Article  Google Scholar 

  • Mustafa T, Srivastava KC (1989) Prostaglandins (eicosanoids) and their role in ectothermic organisms. Adv Comp Environ Physiol 5:157–207

    Article  Google Scholar 

  • Navas JM et al (1997) The impact of seasonal alteration in the lipid composition of broodstock diets on egg quality in the European sea bass. J Fish Biol 51(4):760–773

    Article  CAS  Google Scholar 

  • Nevenzel JC (1970) Occurrence, function and biosynthesis of wax esters in marine organisms. Lipids 5(3):308–319

    Article  CAS  Google Scholar 

  • Normando FT et al (2009) Reproduction and fecundity of tucunaré, Cichla kelberi (Perciformes: Cichlidae), an exotic species in Três Marias reservoir, southeastern Brazil. J Appl Ichthyol 25(3):299–305

    Article  Google Scholar 

  • Olivar MP, Fortuno JM (1991) Guide to ichthyoplankton of the Southeast Atlantic (Benguela current region), vol 55. Consejo superior de Ivestigaciones Científicas. Instituto de Ciencias del Mar, Barcelona, Spain, p 381

    Google Scholar 

  • Padrón D, Lindley VF, Pfeiler E (1996) Changes in lipid composition during metamorphosis of bonefish (Albula sp.) leptocephali. Lipids 31(5):513–519

    Article  Google Scholar 

  • Parenti LR, Grier HJ (2004) Evolution and phylogeny of gonad morphology in bony fishes. Integr Comp Biol 44(5):333–348

    Article  Google Scholar 

  • Parrish CC (1987) Separation of aquatic lipid classes by chromarod thin-layer chromatography with measurement by Iatroscan flame ionization detection. Can J Fish Aquat Sci 44:722–731

    Article  CAS  Google Scholar 

  • Parrish CC (1999) Determination of total lipid, lipid classes, and fatty acids in aquatic samples. In: Arts MT, Wainman BC (eds) Lipids in freshwater ecosystems. Springer Verlag, New York, pp 4–20

    Chapter  Google Scholar 

  • Phleger CF, Nichols PD, Virtue P (1997) The lipid, fatty acid and fatty alcohol composition of the myctophid fish Electrona antarctica: high level of wax esters and food chain implications. Antarct Sci 9:258–265

    Article  Google Scholar 

  • Rainuzzo JR, Reitan KI, Olsen Y (1997) The significance of lipids at early stages of marine fish: a review. Aquaculture 155(1–4):103–115

    Article  CAS  Google Scholar 

  • Sargent JR, Lee RF, Nevenzel JC (1976) Marine wax esters. In: Kolattukudy P (ed) Chemistry and biochemistry of natural waxes. Elsvier. Amsterdam, Netherlands, pp 51–91

    Google Scholar 

  • Sargent JR, Bell JG, Bell MV, Henderson RJ, Tocher DR (1995) Requirement criteria for essential fatty acids. J Appl Ichthyol 11(3–4):183–198

    Article  CAS  Google Scholar 

  • Sargent JR, McEvoy LA, Bell JG (1997) Requirements, presentation and sources of polyunsaturated fatty acids in marine fish larval feeds. Aquaculture 155(1–4):117–127

    Article  CAS  Google Scholar 

  • Sargent J, Bell G, McEvoy L, Tocher D, Estevez A (1999a) Recent developments in the essential fatty acid nutrition of fish. Aquaculture 177(1–4):191–199

    Article  CAS  Google Scholar 

  • Sargent J, McEvoy L, Estevez A, Bell G et al (1999b) Lipid nutrition of marine fish during early development: current status and future directions. Aquaculture 179(1–4):217–229

    Article  CAS  Google Scholar 

  • Sargent J, Tocher D, Bell J (2002) The lipids. In: Halver JE, Hardy RW (eds) Fish nutrition, 3rd edn. Elsevier (Academic Press), San Diego, pp 181–257

    Google Scholar 

  • Shields RJ, Bell JG, Luizi FS, Gara B, Bromage NR, Sargent JR (1999) Natural copepods are superior to enriched Artemia nauplii as feed for halibut larvae (Hippoglossus hippoglossus) in terms of survival, pigmentation and retinal morphology: relation to dietary essential fatty acids. J Nutr 129:1186–1194

    Article  CAS  Google Scholar 

  • Solomon FN, Ramnarine IW (2007) Reproductive biology of white mullet, Mugil curema (Valenciennes) in the southern caribbean. Fish Res 88(1):133–138

    Article  Google Scholar 

  • Spener F, Sand DM (1970) Neutral aloxylipids and wax esters of mullet (Mugil cephalus) roe. Comp Biochem Physiol 34:715–719

    Article  CAS  Google Scholar 

  • Sundby S, Boyd AJ, Hutchings L, O'Toole MJ, Thorisson K, Thorsen A (2001) Interaction between cape hake spawning and the circulation in the northern Benguela upwelling ecosystem. S Afr J Mar Sci 23(1):317–336

    Article  Google Scholar 

  • Tocher DR (2003) Metabolism and functions of lipids and fatty acids in teleost fish. Rev Fish Sci 11(2):107–184

    Article  CAS  Google Scholar 

  • Van Der Kraak G, Biddiscombe S (1999) Polyunsaturated fatty acids modulate the properties of the sex steroids binding protein in goldfish. Fish Physiol Biochem 20:115–123

    Article  Google Scholar 

  • Wacker A, Von Elert E (2001) Polyunsaturated fatty acids: evidence for non-substitutable biochemical resources in Daphnia galeata. Ecology 82:2507–2520

    Article  Google Scholar 

  • Wade MG, Van Der Kraak G (1993) Regulation of prostaglandins E and F production in the goldfish testes. J Exp Zool 266:108–115

    Article  CAS  Google Scholar 

  • Wiegand MD (1996) Composition, accumulation and utilization of yolk lipids in teleost fish. Rev Fish Biol Fisher 6(3):259–286

    Article  Google Scholar 

  • Wilson C, Scotto L, Scarpa J, Volety A, Laramore S, Haunert D (2005) Survey of water quality, oyster reproduction, and oyster health status in the St. Lucie estuary. J Shellfish Res 24(1):157–165

    Article  Google Scholar 

Download references

Acknowledgements

This study was financially supported by Bonefish & Tarpon Trust (BTT) and National Fish and Wildlife Foundation (NFWF). We are grateful to J. Lewis, W. Halstead, Z. Nilles, and C. Robinson for their extensive help during fieldwork and lab work.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sahar Mejri.

Ethics declarations

Ethical approval

The experimental protocol received approval from the Florida Atlantic University’s Institutional Animal Care and use Committee (IACUC, protocol A16–34).

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mejri, S., Luck, C., Tremblay, R. et al. Bonefish (Albula vulpes) oocyte lipid class and fatty acid composition related to their development. Environ Biol Fish 102, 221–232 (2019). https://doi.org/10.1007/s10641-018-0825-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10641-018-0825-0

Keywords

Navigation