Marine Biology

, Volume 162, Issue 9, pp 1879–1888 | Cite as

Maternal versus environmental constraints on the oocyte size of a marine pelagophil fish

  • K. GaniasEmail author
  • M. Rakka
  • E. Mantzouki
  • T. Vavalidis
  • M. Tsinganis
  • C. Nunes
Original Paper


We investigated maternal body size and environmental effects on the oocyte size of the Atlantic sardine, Sardina pilchardus, a marine pelagophil, using a novel, oocyte stage-specific approach which takes into account the spawning lag. In particular, we focused on anatomical constraints imposed by the maternal body cavity to the growth of the ovary and its oocytes during the course of vitellogenesis (VIT) and oocyte maturation (OM). We analyzed variability in oocyte size in VIT and OM ovaries as a factor of maternal size, ambient temperature (SST) and preservation medium (formalin vs. ethanol) using the spawning lag of recent and imminent spawners, respectively, as a covariate. We showed that oocyte size correlates with maternal size in OM ovaries but not in VIT ovaries. More specifically, 10 cm difference in maternal body length corresponds to 0.112 mm2 (or 12 %) difference in the cross section of fully hydrated oocytes just previous to ovulation. On the other hand there was no inverse relationship between OM oocyte size at spawning and batch fecundity. Ambient SST was not an important determinant of hydrated oocyte size since the same 12 % difference in oocyte size was estimated for the entire SST range of the study. We suggest that these stage-specific differences in the effect of maternal size on oocyte size are due to a functional relationship between the abdominal volume and ovarian size.


Oocyte Maturation Advanced Very High Resolution Radiometer Advanced Very High Resolution Radiometer Oocyte Size Batch Fecundity 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



This work was supported by the National Biological Sampling Programme (PNAB/EU DCF) for DEPM surveys funded by the European Union. Thanks are due to Dr. M.M. Angelico for helpful recommendations. Particular thanks are due to all IPMA staff that contributed to the collection of DEPM samples and the histological preparations. The work of M. Rakka, T. Vavalidis and E. Mantzouki was partly done within the framework of a collaboration between the School of Biology of AUTH and IPMA under the ERASMUS PLACEMENT PROGRAMME.

Compliance with ethical standards

Conflict of interest

We have no conflicts of interest to disclose.

Research involving human participants and/or animals

The present study did not involve any human participants and or animals.

Informed consent

We did not conduct any healthcare interventions to human participants.


  1. Baith K, Lindsay R, Fu G, McClain CR (2001) Data analysis system developed for ocean color satellite sensors. EOS Trans Am Geophys Union 82:202CrossRefGoogle Scholar
  2. Bernal M, Borchers D, Valdes L et al (2001) A new ageing method for eggs of fish species with daily spawning synchronicity. Can J Fish Aquat Sci 58:2330–2340CrossRefGoogle Scholar
  3. Blaxter J, Hunter JR (1982) The biology of the clupeoid fishes. Adv Mar Biol 20:1–123CrossRefGoogle Scholar
  4. Casey KS, Brandon TB, Cornillon P, Evans R (2010) The past, present, and future of the AVHRR pathfinder SST program. Oceanography from space. Springer, Dordrecht, pp 273–287Google Scholar
  5. Castro LR, Claramunt G, Krautz MC et al (2009) Egg trait variation in anchoveta Engraulis ringens: a maternal response to changing environmental conditions in contrasting spawning habitats. Mar Ecol Prog Ser 381:237–248. doi: 10.3354/Meps07922 CrossRefGoogle Scholar
  6. Cerdà J, Fabra M, Raldúa D (2007) Physiological and molecular basis of fish oocyte hydration. In: Babin PJ, Cerdà J, Lubzens E (eds) The fish oocyte: from basic studies to biotechnological applications. Springer, Dordrecht, pp 349–396CrossRefGoogle Scholar
  7. Chambers RC (1997) Environmental influences on egg and propagule sizes in marine fishes. In: Chambers RC, Trippel EA (eds) Early life history and recruitment in fish populations. Chapman & Hall, London, pp 63–102CrossRefGoogle Scholar
  8. Claramunt G, Herrera G (1994) A new method to estimate the fraction of daily spawning females and the numbers of spawning in Sardinops sagax in northern Chile. Sci Mar 58:169–177Google Scholar
  9. Claramunt G, Herrera G, Pizarro P (1994) Potential annual production of eggs according to sizes of Sardinops sagax in northern Chile. Rev Biol Mar Valpso 29:147–166Google Scholar
  10. Coombs SH, Boyra G, Rueda LD et al (2004) Buoyancy measurements and vertical distribution of eggs of sardine (Sardina pilchardus) and anchovy (Engraulis encrasicolus). Mar Biol 145:959–970. doi: 10.1007/s00227-004-1389-4 CrossRefGoogle Scholar
  11. Daoulas C, Economou A (1986) Seasonal variation of egg size in the sardine, Sardina pilchardus Walb., of the Saronikos Gulf: causes and probable explanation. J Fish Biol 28:449–457CrossRefGoogle Scholar
  12. Duarte CM, Alcaraz M (1989) To produce many small or few large eggs: a size-independent reproductive tactic of fish. Oecologia 80:401–404CrossRefGoogle Scholar
  13. Fulton TW (1898) On the growth and maturation of the ovarian eggs of teleostean fishes. 16th annual report of the Fishery Board for Scotland, part 3, pp 83–134Google Scholar
  14. Ganias K (2003) Oceanographic and biological study of sardine Sardina pilchardus (Walb., 1792) ichthyoplankton production in coastal waters of central Greece. University of ThessalyGoogle Scholar
  15. Ganias K (2009) Linking sardine spawning dynamics to environmental variability. Estuar Coast Shelf Sci 84:402–408. doi: 10.1016/j.ecss.2009.07.004 CrossRefGoogle Scholar
  16. Ganias K, Somarakis S, Machias A, Theodorou A (2004) Pattern of oocyte development and batch fecundity in the Mediterranean sardine. Fish Res 67:13–23. doi: 10.1016/j.fishres.2003.08.008 CrossRefGoogle Scholar
  17. Ganias K, Nunes C, Stratoudakis Y (2007) Degeneration of sardine (Sardina pilchardus) postovulatory follicles: structural changes and factors affecting resorption. Fish Bull 105:131–139Google Scholar
  18. Ganias K, Rakka M, Vavalidis T, Nunes C (2010) Measuring batch fecundity using automated particle counting. Fish Res 106:570–574. doi: 10.1016/j.fishres.2010.09.016 CrossRefGoogle Scholar
  19. Ganias K, Nunes C, Rakka M et al (2011) Estimating oocyte growth rate and its potential relationship to spawning frequency in teleosts with indeterminate fecundity. Mar Costal Fish 3:119–126. doi: 10.1080/19425120.2011.555729 CrossRefGoogle Scholar
  20. Ganias K, Murua H, Claramunt G et al (2014) Egg production. In: Dominguez-Petit R, Murua H, Saborido-Rey F, Trippel EA (eds) Handbook of applied fisheries reproductive biology for stock assessment and management. Digital CSIC, Madrid, p 110Google Scholar
  21. Garrido S, Rosa R, Ben-Hamadou R et al (2007) Effect of maternal fat reserves on the fatty acid composition of sardine (Sardina pilchardus) oocytes. Comp Biochem Physiol 148:398–409. doi: 10.1016/j.cbpb.2007.07.008 CrossRefGoogle Scholar
  22. Green BS (2008) Maternal effects in fish populations. Adv Mar Biol 54:1–105CrossRefGoogle Scholar
  23. Guisande C, Riveiro I, Sola A, Valdes L (1998) Effect of biotic and abiotic factors on the biochemical composition of wild eggs and larvae of several fish species. Mar Ecol Prog Ser 163:53–61. doi: 10.3354/Meps163053 CrossRefGoogle Scholar
  24. Jons D, Miranda E (1997) Ovarian weight as an index of fecundity, maturity, and spawning periodicity. J Fish Biol 50:150–156CrossRefGoogle Scholar
  25. Jung K-M, Folkvord A, Kjesbu OS, Sundby S (2014) Experimental parameterisation of principal physics in buoyancy variations of marine teleost eggs. PLoS ONE 9:e104089. doi: 10.1371/journal.pone.0104089 CrossRefGoogle Scholar
  26. Kamler E (2005) Parent–egg–progeny relationships in teleost fishes: an energetic perspective. Rev Fish Biol Fish 15:399–421CrossRefGoogle Scholar
  27. Kilpatrick KA, Podesta GP, Evans R (2001) Overview of the NOAA/NASA advanced very high resolution radiometer Pathfinder algorithm for sea surface temperature and associated matchup database. J Geophys Res 106:9179–9197CrossRefGoogle Scholar
  28. Kjesbu OS (1989) The spawning activity of cod, Gadus morhua. J Fish Biol 34:195–206CrossRefGoogle Scholar
  29. Leal EM, Castro LR, Claramunt G (2009) Variability in oocyte size and batch fecundity in anchoveta (Engraulis ringens, Jenyns 1842) from two spawning areas off the Chilean coast. Sci Mar 73:59–66. doi: 10.3989/scimar.2009.73n1059 CrossRefGoogle Scholar
  30. Matsuoka M, Konishi Y (1996) Morphological characteristics of unfertilized eggs of the Japanese sardine, compared with fertilized ones. Fish Sci 62:855–859Google Scholar
  31. Morimoto H, Watanabe Y, Yamashita Y, Oozeki Y (1994) Effects of maternal nutritional conditions on number, size and lipid content of hydrated eggs in the Japanese sardine from Tosa Bay, southwestern Japan. International workshop: survival strategies in early life stages of marine resources, Yokohama, Japan, 11–14 Oct 1994Google Scholar
  32. Pebesma EJ (2004) Multivariable geostatistics in S: the gstat package. Comput Geosci 30:683–691CrossRefGoogle Scholar
  33. R Development Core Team (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
  34. Rakka M, Ganias K (2015) Assessing species and stage specific effects of preservation on fish ovarian material over different temporal scales. Mediterr Mar Sci. doi: 10.12681/mms.1205 Google Scholar
  35. Ré P (1981) Seasonal occurrence, mortality and dimensions of sardine eggs Sardina pilchardus (Walbaum) off Portugal. Cybium 5:41–48Google Scholar
  36. Riveiro I, Guisande C, Lloves M et al (2000) Importance of parental effects on larval survival in Sardina pilchardus. Mar Ecol Prog Ser 205:249–258CrossRefGoogle Scholar
  37. Somarakis S, Ganias K, Tserpes G, Koutsikopoulos C (2004) On gonadal allometry and the use of the gonosomatic index: a case study in the Mediterranean sardine, Sardina pilchardus. Mar Biol 146:181–189CrossRefGoogle Scholar
  38. Stratoudakis Y, Coombs S, de Lanzos AL et al (2007) Sardine (Sardina pilchardus) spawning seasonality in European waters of the northeast Atlantic. Mar Biol 152:201–212CrossRefGoogle Scholar
  39. Thorsen A, Fyhn HJ (1996) Final oocyte maturation in vivo and in vitro in marine fishes with pelagic eggs; yolk protein hydrolysis and free amino acid content. J Fish Biol 48:1195–1209Google Scholar
  40. Trippel EA, Neil SRE (2004) Maternal and seasonal differences in egg sizes and spawning activity of northwest Atlantic haddock (Melanogrammus aeglefinus) in relation to body size and condition. Can J Fish Aquat Sci 61:2097–2110CrossRefGoogle Scholar
  41. Tsuruta Y, Hirose K (1989) Internal regulation of reproduction in the Japanese anchovy (Engraulis japonica) as related to population fluctuation. Can Spec Publ Fish Aquat Sci 108:111–119Google Scholar
  42. Valdes Szeinfeld E (1991) Cannibalism and intraguild predation in clupeoids. Mar Ecol Prog Ser 79:17–26CrossRefGoogle Scholar
  43. Zwolinski J, Mason E, Oliveira PB, Stratoudakis Y (2006) Fine-scale distribution of sardine (Sardina pilchardus) eggs and adults during a spawning event. J Sea Res 56:294–304CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • K. Ganias
    • 1
    Email author
  • M. Rakka
    • 1
  • E. Mantzouki
    • 1
  • T. Vavalidis
    • 1
  • M. Tsinganis
    • 1
  • C. Nunes
    • 2
  1. 1.School of BiologyAristotle University of ThessalonikiThessaloníkiGreece
  2. 2.IPMA - Instituto Português do Mar e da AtmosferaLisbonPortugal

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