Abstract
The consequences of rising temperature to reproductive development in the lesser sandeel, Ammodytes marinus, were studied in captive fish held at three temperatures to reflect the present day and future predicted winter temperature of North Sea habitat. Our results showed that an increase in temperature of 5 °C led to more than a 2 month delay in the timing of oocyte maturation. The inverse relationship between the stage of ovarian development and temperature in A. marinus is in contrast with that seen in many early year spawners. A close relationship between relative ovary size and ovarian development, as well as an overlap in oocyte diameter among treatments suggested that this temperature effect is mediated via an energetic constraint on reproductive investment. Temperature had no effect on the potential fecundity—length relationship in December, and while the intensity of pre-ovulatory atresia did not reflect condition, it was found to increase with temperature and decrease with oocyte diameter. The magnitude of potential temperature-related changes in spawning phenology could have important implications to the future match between hatching times of A. marinus and prey availability, although this may be partially mitigated by the positive temperature dependence of embryonic development.
Similar content being viewed by others
References
Akaike H (1974) A new look at the statistical model identification. IEEE Trans Autom Control 19:716–723
Anthony J, Roby D, Turco K (2000) Lipid content and energy density of forage fishes from the northern Gulf of Alaska. J Exp Mar Biol Ecol 248:53–78
Berx B, Hughes SL (2009) Climatology of surface and near-bed temperature and salinity on the north-west European continental shelf for 1971–2000. Cont Shelf Res 29:2286–2292
Boulcott P, Wright PJ (2008) Critical timing for reproductive allocation in a capital breeder: evidence from sandeels. Aquat Biol 3: 31–40
Boulcott P, Wright PJ (2011) Variation in fecundity in the lesser sandeel: implications for regional management. J Mar Biol Assoc UK 91:1273–1280
Boulcott P, Wright P, Gibb F (2007) Regional variation in maturation of sandeels in the North Sea. ICES J Mar Sci 64:369–376
Boulcott P, Clarke J, Wright PJ (in review) Effects of size on spawning time in the lesser sandeel Ammodytes marinus. J Fish Biol
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 3:52–70
Bye VJ (1984) The role of environmental factors in the timing of reproductive cycles. In: Potts GW, Wootton RJ (eds) Reproductive strategies and tactics. Academic Press, London, pp 187–206
Carscadden J, Nakashima BS, Frank KT (1997) Effects of fish length and temperature on the timing of peak spawning in capelin (Mallotus villosus). Can J Fish Aquat Sci 54:781–787
Cushing DH (1990) Plankton production and year-class strength in fish populations: an update of the match/mismatch hypothesis. In: Blaxter JHS, Southward AJ (eds) Advances in marine biology. Academic Press Limited, San Diego, pp 249–293
Daan N, Bromley PJ, Hislop JRG, Nielsen NA (1990) Ecology of North sea fish. Neth J Sea Res 26:343–386
Davies PR, Hanyu I (1986) Effect of temperature and photoperiod on sexual maturation and spawning of the common carp. I. Under conditions of high temperature. Aquaculture 51:277–288
Durant J, Hjermann D, Ottersen G, Stenseth N (2007) Climate and the match or mismatch between predator requirements and resource availability. Clim Res 33:271–283
Fincham JI, Rijnsdorp AD, Engelhard GH (2013) Shifts in the timing of spawning in sole linked to warming sea temperatures. J Sea Res 75:69–76
Gauld JA (1990) Movements of lesser sandeels (Ammodytes marinus Raitt) tagged in the northwestern North sea. ICES J Mar Sci 46:229–231
Gauld J, Hutcheon J (1990) Spawning and fecundity in the lesser sandeel, Ammodytes marinus Raitt, in the north-western North sea. J Fish Biol 36:611–613
Gurkan Z, Christensen A, Maar M, Møller EF, Madsen KS, Munk P, Mosegaard H (2013) Spatio-temporal dynamics of growth and survival of Lesser Sandeel early life-stages in the North Sea: Predictions from a coupled individual-based and hydrodynamic–biogeochemical model. Ecol Model 250:294–306
Haynes TB, Robinson CLK (2011) Re-use of shallow sediment patches by Pacific sand lance (Ammodytes hexapterus) in Barkley Sound, British Columbia, Canada. Environ Biol Fish 92:1–12
Heath MR, Neat FC, Pinnegar JK, Reid DG, Sims DW, Wright PJ (2012) Review of climate change impacts on marine fish and shellfish around the UK and Ireland. Aquat Conserv 22:337–367
Hislop J, Harris M, Smith J (1991) Variation in the calorific value and total energy content of the lesser sandeel (Ammodytes marinus) and other fish preyed on by seabirds. J Zool 224:501–517
ICES (1995) Report of the ICES Workshop on Sandeel Otolith Analysis. ICES CM 1995/G:4
Jansen T, Gislason H (2011) Temperature affects the timing of spawning and migration of North Sea mackerel. Cont Shelf Res 31:64–72
Kennedy J, Witthames PR, Nash RDM, Fox CJ (2008) Is fecundity in plaice (Pleuronectes platessa L.) down-regulated in response to reduced food intake during autumn? J Fish Biol 72:78–92
Kennedy J, Skjæraasen JE, Nash RDM, Thorsen A, Slotte A, Hansen T, Kjesbu OS (2009) Do capital breeders like Atlantic herring (Clupea harengus) exhibit sensitive periods of nutritional control on ovary development and fecundity regulation? Can J Fish Aquat Sci 67:16–27
Kjesbu O (1994) Time of start of spawning in Atlantic cod (Gadus morhua) females in relation to vitellogenic oocyte diameter, temperature, fish length and condition. J Fish Biol 45:719–735
Kjesbu OS, Righton D, Krüger-Johnsen M, Thorsen A, Michalsen K, Fonn M, Witthames PR (2010) Thermal dynamics of ovarian maturation in Atlantic cod (Gadus morhua). Can J Fish Aquat Sci 67:605–625
Kurita Y, Meier S, Kjesbu OS (2003) Oocyte growth and fecundity regulation by atresia of Atlantic herring (Clupea harengus) in relation to body condition throughout the maturation cycle. J Sea Res 49:203–219
Langham NPE (1971) The distribution and abundance of larval sandeels (Ammodytidae) in Scottish waters. J Mar Biol Assoc UK 51:597–707
Le Cren ED (1951) The length–weight relationship and seasonal cycle in gonad weight and condition in the perch (Perca fluviatilis). J Anim Ecol 20:201–219
Leder EH, Danzmann RG, Ferguson MM (2006) The candidate gene, clock, localizes to a strong spawning time quantitative trait locus region in rainbow trout. J Hered 97:74–80
Lowe JA, Howard TP, Pardaens A, Tinker J, Holt J, Wakelin S, Milne G, Leake J, Wolf J, Horsburgh K, Reeder T, Jenkins G, Ridley J, Dye S, Bradley S (2009). Marine and coastal projections, UK Climate Projections science report. Met Off Hadley Centre Exeter UK
Lynam C, Halliday N, Höffle H, Wright P, van Damme C, Edwards M, Pitois S (2013) Spatial patterns and trends in abundance of larval sandeels in the North Sea: 1950–2005. ICES J Mar Sci 70:540–553
Ma Y, Kjesbu OS, Jørgensen T (1998) Effects of ration on the maturation and fecundity in captive Atlantic herring (Clupea harengus). Can J Fish Aquat Sci 55:900–908
Macer C (1966) Sand eels (Ammodytidae) in the south-western North sea; their biology and fishery. Min Agric Fish Food Fish Invest Ser 2 24:1–55
Migaud H, Davie A, Taylor J (2010) Current knowledge on the photoneuroendocrine regulation of reproduction in temperate fish species. J Fish Biol 76:27–68
Miranda LA, Chalde T, Elisio M, Strüssmann CA (2013) Effects of global warming on fish reproductive endocrine axis, with special emphasis in pejerrey Odontesthes bonariensis. Gen Comp Endocrinol 192:45–54
Óskarsson G, Kjesbu O, Slotte A (2002) Predictions of realised fecundity and spawning time in Norwegian spring-spawning herring (Clupea harengus). J Sea Res 48:59–79
Otterå H, Agnalt A-L, Thorsen A, Kjesbu OS, Dahle G, Jørstad K (2012) Is spawning time of marine fish imprinted in the genes? A two-generation experiment on local Atlantic cod (Gadus morhua L.) populations from different geographical regions. ICES J Mar Sci 69:1722–1728
Pankhurst N, Porter M (2003) Cold and dark or warm and light: variations on the theme of environmental control of reproduction. Fish Physiol Biochem 28:385–389
Pope J, Shepherd JG, Webb J (1994) Successful surf-riding on size spectra - the secret of survival in the sea. Philos Trans R Soc Lond B Biol Sci 343:41–49
Raitt DS (1934) A Preliminary Account of the Sandeels of Scottish Waters. ICES J Mar Sci 9:365–372
Reay P (1970) Synopsis of biological data on North Atlantic sandeels of the genus Ammodytes (A. tobianus, A. dubius, A. americanus and A. marinus). FAO Fish Synop No 82
Régnier T, Gibb FM, Wright PJ (2017) Importance of mismatch in a winter hatching species: evidence from lesser sandeel. Mar Ecol Prog Ser 567:185–197
Robards MD, Piatt J, Rose G (1999a) Maturation, fecundity, and intertidal spawning of Pacific sand lance in the northern Gulf of Alaska. J Fish Biol 54:1050–1068
Robards MD, Anthony JA, Rose GA, Piatt JF (1999b) Changes in proximate composition and somatic energy content for Pacific sand lance (Ammodytes hexapterus) from Kachemak Bay, Alaska relative to maturity and season. J Exp Mar Bio Ecol 242:245–258
Sims DW, Wearmouth VJ, Genner MJ, Southward AJ, Hawkins SJ (2004) Low-temperature driven early spawning migration of a temperate marine fish. J Anim Ecol 73:333–341
Sinclair M, Tremblay MJ (1984) Timing of spawning of Atlantic herring (Clupea harengus) populations and the match-mismatch theory. Can J Fish Aquat Sci 41:1055–1065
Smigielski AS, Halavik TA, Buckley LJ, Drew SM, Laurence GC (1983) Spawning, embryo development and growth of the American sand lance Ammodytes americanus in the laboratory. Mar Ecol Prog Ser 14:287–292
Sokal RR, Rohlf FJ (1995) Biometry, 3rd edn. Freeman, New York
Taranger GL, Carrillo M, Schulz RW, Fontaine P, Zanuy S, Felip A, Weltzien F-A, Dufour S, Karlsen Ø, Norberg B (2010) Control of puberty in farmed fish. Gen Comp Endocrinol 165:483–515
Thorsen A, Kjesbu O (2001) A rapid method for estimation of oocyte size and potential fecundity in Atlantic cod using computer-aided particle analysis system. J Sea Res 46:295–308
Tobin D, Wright PJ (2011) Temperature effects on female maturation in a temperate marine fish. J Exp Mar Bio Ecol 403:9–13
Tveiten H, Johnsen HK (1999) Temperature experienced during vitellogenesis influences ovarian maturation and the timing of ovulation in common wolffish. J Fish Biol 55:809–819
van Deurs M, Hartvig M, Steffensen JF (2011) Critical threshold size for overwintering sandeels (Ammodytes marinus). Mar Biol 158:2755–2764
van Der Kraak G, Pankhurst N (1997) Temperature effects on the reproductive performance of fish. In: Wood CM, McDonald DG (eds) Global warming: implications for freshwater and marine fish. Cambridge University Press, Cambridge, pp 159–176
Wanless S, Wright PJ, Harris M, Elston DA (2004) Evidence for decrease in size of lesser sandeels Ammodytes marinus in a North Sea aggregation over a 30-year period. Mar Ecol Prog Ser 279:237–246
Ware DM, Tanasichuk RW (1989) Biological basis of maturation and spawning waves in Pacific herring (Clupea harengus pallasi). Can J Fish Aquat Sci 46:1776–1784
Winslade PR (1971) Behavioural and embryological investigations of the lesser sandeel, Ammodytes marinus Raitt. Thesis, University East Anglia
Wood SN (2011) Fast stable restricted maximum likelihood and marginal likelihood estimation of semiparametric generalized linear models. J Royal Stat Soc (B) 73:3–36
Wright PJ, Bailey MC (1996) Timing of hatching in Ammodytes marinus from Shetland waters and its significance to early growth and survivorship. Mar Biol 126:143–152
Wright PJ, Trippel EA (2009) Fishery-induced demographic changes in the timing of spawning: consequences for reproductive success. Fish Fish 10:283–304
Wright PJ, Orpwood J, Scott BE (2017) Impact of rising temperature on reproductive investment in a capital breeder: the lesser sandeel. J Exp Mar Bio Ecol 486:52–58
Acknowledgements
Ben Williamson, Clive Norris, Rory Long, and Brian Gall for providing technical support for the experimental work, Iain Gibb for age reading, Francis Neat, Declan Tobin, and Martha O’Sullivan for assisting with tagging and measuring the fish and Marlene Quintal for assistance with oocyte analysis. Georg Engelhard and two reviewers provided helpful comments on an earlier version of this manuscript. This work was funded by the Scottish Government (ROAME MF0765 and ST007), and all experimental work was carried out under a United Kingdom Home Office licence.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Ethical approval
All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All work was carried out in accordance with the U.K. Animals Scientific Procedures Act 1986.
Additional information
Responsible Editor: G. H. Engelhard.
Reviewed by P. R. Witthames and E. Johnsen.
Rights and permissions
About this article
Cite this article
Wright, P.J., Orpwood, J.E. & Boulcott, P. Warming delays ovarian development in a capital breeder. Mar Biol 164, 80 (2017). https://doi.org/10.1007/s00227-017-3116-y
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00227-017-3116-y