Contrasting post-ovulatory follicle production in fishes with different spawning dynamics (original) (raw)

Abstract

The assessment of postovulatory follicles (POFs) is of considerable importance when applying the Daily Egg Production Method (DEPM) since it is used to estimate both spawning frequency (S) and batch fecundity (F B), provided that daily cohorts of POFs are discernible. Atlantic sardine (Sardina pilchardus) and Atlantic mackerel (Scomber scombrus), two commercially valuable pelagic species with different spawning dynamics were investigated principally to evaluate the appropriateness of the POF method to properly reflect S and F B. For appropriate quantification, both the Weibel and the postovulatory follicles packing density (POFPD) method, the latter described in this paper, were applied and compared. In sardine, not only was the existence of one single daily POF cohort confirmed but also the estimated number of POFs in the cohort matched gravimetric F B results. Furthermore, the Weibel method and POFPD led to similar results. However, several daily POF cohorts cooccurred in the mackerel ovary. Therefore, POF-based estimation of F B only works for species such as sardine with a single, daily POF cohort. Likewise, in relation to estimation of S, the occurrence of single versus multiple POF cohorts makes the histological assignment of spawners to daily spawning classes either straightforward or difficult for species comparable to sardine or mackerel, respectively. In the latter case we suggest focusing in the largest, thus newest, POFs which correspond to the latest spawning event. Therefore, the appropriateness of the POF method in applications of the DEPM should be judged based on the spawning dynamics of the assessed species.

Loading...

Loading Preview

Sorry, preview is currently unavailable. You can download the paper by clicking the button above.

References (39)

  1. Altringham, J.D., Block, B.A., 1997. Why do tuna maintain elevated slow muscle tem- peratures? Power output of muscle isolated from endothermic and ectothermic fish. J. Exp. Biol. 200, 2617-2627.
  2. Anderson, K.C., Alix, M., Charitonidou, K., Thorsen, A., Thorsheim, G., Ganias, K., Schmidt, T.C.D.S., Kjesbu, O.S., 2020. Development of a new "ultrametric" method for assessing spawning progression in female teleost serial spawners. Sci. Rep. https://doi.org/10.1038/s41598-020-66601-w.
  3. Aragón, L., Aranda, G., Santos, A., Medina, A., 2010. Quantification of ovarian follicles in bluefin tuna Thunnus thynnus by two stereological methods. J. Fish Biol. 77, 719-730. https://doi.org/10.1111/j.1095-8649.2010.02713.x.
  4. Brown-Peterson, N.J., Wyanski, D.M., Saborido-Rey, F., Macewicz, B.J., Lowerre-Barbieri, S.K., 2011. A Standardized Terminology for Describing Reproductive Development in Fishes. Mar. Coast. Fish. 3, 52-70. https://doi.org/10.1080/19425120.2011.555724.
  5. Dickson, K.A., 1995. Unique adaptations of the metabolic biochemistry of tunas and billfishes for life in the pelagic environment. Environ. Biol. Fishes 42, 65-97.
  6. Emerson, L.S., Walker, M.G., Witthames, P.R., 1990. A stereological method for esti- mating fish fecundity. J. Fish Biol. 36, 721-730. https://doi.org/10.1111/j.1095- 8649.1990.tb04326.x.
  7. Ganias, K., 2013. Determining the indeterminate: Evolving concepts and methods on the assessment of the fecundity pattern of fishes. Fish. Res. 138, 23-30. https://doi.org/ 10.1016/j.fishres.2012.05.006.
  8. Ganias, K., 2012. Thirty years of using the postovulatory follicles method: Overview, problems and alternatives. Fish. Res. 117-118, 63-74. https://doi.org/10.1016/j. fishres.2011.01.009.
  9. Ganias, K., Murua, H., Claramunt, G., Dominguez-Petit, R., Goncalves, P., Juanes, F., Keneddy, J., Klibansky, N., Korta, M., Kurita, Y., Lowerre-Barbieri, S., Macchi, G., Matsuyama, M., Medina, A., Nunes, C., Plaza, G., Rideout, R., Somarakis, S., Thorsen, A., Uriarte, A., Y.M, 2014. Egg Production. Handb. Appl. Fish. Reprod. Biol. Stock Assess. Manag. 109 pp. .
  10. Ganias, K., Marmara, D., Solla, A., Garabana, D., Dominguez-Petit, R., 2018. Atlantic mackerel daily spawning dynamics and implications for batch fecundity estimations. ICES J. Mar. Sci. 75, 1647-1654. https://doi.org/10.1093/icesjms/fsy033.
  11. Ganias, K., Nunes, C., Stratoudakis, Y., 2007. Degeneration of postovulatory follicles in the Iberian sardine Sardina pilchardus: Structural changes and factors affecting re- sorption. Fish. Bull. 105, 131-139.
  12. Ganias, K., Nunes, C., Vavalidis, T., Rakka, M., Stratoudakis, Y., 2011. Estimating Oocyte growth rate and its potential relationship to spawning frequency in teleosts with indeterminate fecundity. Mar. Coast. Fish. 3, 119-126. https://doi.org/10.1080/ 19425120.2011.555729.
  13. Ganias, K., Rakka, M., Mantzouki, E., Vavalidis, T., Tsinganis, M., Nunes, C., 2015. Maternal versus environmental constraints on the oocyte size of a marine pelagophil fish. Mar. Biol. 162, 1879-1888. https://doi.org/10.1007/s00227-015-2719-4.
  14. Ganias, K., Rakka, M., Vavalidis, T., Nunes, C., 2010. Measuring batch fecundity using automated particle counting. Fish. Res. 106, 570-574. https://doi.org/10.1016/j. fishres.2010.09.016.
  15. Grier, H.J., Neidig, C.L., Quagio-Grassiotto, I., 2017. Development and fate of the post- ovulatory follicle complex, postovulatory follicle, and observations on folliculogen- esis and oocyte atresia in ovulated common snook, Centropomus undecimalis (Bloch, 1792). J. Morphol. 278, 547-562. https://doi.org/10.1002/jmor.20652.
  16. Haslob, H., Kraus, G., Saborido-Rey, F., 2003. The dynamics of postovulatory follicle degeneration and oocyte growth in Baltic sprat. pp. 281-289.
  17. Hunter, J.R., Macewicz, B.J., 1985. Measurement of spawning frequency in multiple spawning fishes. In: Lasker, R. (Ed.), NOAA Technical Report NMFS, pp. 79-94.
  18. Hunter, J.R., Macewicz, B.J., Sibert, H.R., 1986. The spawning frequency of skipjack tuna, Katsuwonus pelamis, from the South Pacific. Fish. Bull. 84, 895-903.
  19. ICES, 2016. Report of the Working Group on Atlantic Fish Larvae and Egg Surveys (WGALES). Thessaloniki, Greece. pp. 110.
  20. Kjesbu, O.S., Thorsen, a., Fonn, M., 2011. Quantification of Primary and Secondary Oocyte Production in Atlantic Cod by Simple Oocyte Packing Density Theory. Mar. Coast. Fish. 3, 92-105. https://doi.org/10.1080/19425120.2011.555714.
  21. Korta, M., Murua, H., Kurita, Y., Kjesbu, O.S., 2010. How are the oocytes recruited in an indeterminate fish? Applications of stereological techniques along with advanced packing density theory on European hake (Merluccius merluccius L.). Fish. Res. 104, 56-63. https://doi.org/10.1016/j.fishres.2010.01.010.
  22. Kurita, Y., Kjesbu, O.S., 2009. Fecundity estimation by oocyte packing density formulae in determinate and indeterminate spawners: Theoretical considerations and applica- tions. J. Sea Res. 61, 188-196. https://doi.org/10.1016/j.seares.2008.10.010.
  23. Lang, E.T., Brown-Peterson, N.J., Peterson, M.S., Slack, W.T., 2012. Seasonal and Tidally Driven Reproductive Patterns in the Saltmarsh Topminnow, Fundulus jenkinsi. Copeia 2012, 451-459. https://doi.org/10.1643/cp-10-187.
  24. Mackie, M.C., Lewis, P.D., Gaughan, D.J., Newman, S.J., 2005. Variability in spawning frequency and reproductive development of the narrow-barred Spanish mackerel (Scomberomorus commerson) along the west coast of Australia. Fish. Bull. 103, 344-354.
  25. Medina, A., Abascal, F.J., Aragón, L., Mourente, G., Aranda, G., Galaz, T., Belmonte, A., Serna, J.M. De, García, S., 2007. Influence of sampling gear in assessment of re- productive parameters for bluefin tuna in the western. Mediterranean 337, 221-230.
  26. Medina, A., Abascal, F.J., Megina, C., Garcia, A., 2002. Stereological assessment of the reproductive status of female atlantic northern bluefin tuna during migration to mediterranean spawning grounds through the Strait of Gibraltar. J. Fish Biol. 60, 203-217. https://doi.org/10.1006/jfbi.2001.1835.
  27. Mouchlianitis, F., Minos, G., Ganias, K., 2020. Timing of oocyte recruitment within the ovulatory cycle of Macedonian shad, Alosa macedonica, a batch spawning fish with indeterminate fecundity. Theriogenology. https://doi.org/10.1016/j.theriogenology. 2020.01.050.
  28. Parker, K., 1980. A direct method for estimating northern anchovy, Engraulis mordax, spawning biomass. Fish. Bull. 78, 541-544.
  29. Priede, I.G., Watson, J.J., 1993. An evaluation of the daily egg production method for estimating biomass of Atlantic mackerel (Scomber scombrus). Bull. Mar. Sci. 53, 891-911.
  30. Saber, S., Macías, D., de Urbina, J.O., Kjesbu, O.S., 2016. Contrasting batch fecundity estimates of albacore (Thunnus alalunga), an indeterminate spawner, by different laboratory techniques. Fish. Res. 176, 76-85. https://doi.org/10.1016/j.fishres.2015\. 12.013.
  31. Saber, S., Macías, D., Ortiz de Urbina, J., Kjesbu, O.S., 2015. Stereological comparison of oocyte recruitment and batch fecundity estimates from paraffin and resin sections using spawning albacore (Thunnus alalunga) ovaries as a case study. J. Sea Res. 95, 226-238. https://doi.org/10.1016/j.seares.2014.05.003.
  32. Schaefer, K., 1996. Spawning time, frequency and batch fecundity of yellowfin tuna, Thunnus albacares, from Clipperton Atoll in the eastern Pacific Ocean. Fish. Bull. 94, 98-112.
  33. Schaefer, K.M., 2001. Assessment of skipjack tuna (Katsuwonus pelamis) spawning ac- tivity in the eastern Pacific Ocean. Fish. Bull. 99, 343-350.
  34. Sterio, D.C., 1984. The unbiased estimation of number and sizes of arbitrary particles using the disector. J. Microsc. 134, 127-136. https://doi.org/10.1111/j.1365-2818\. 1984.tb02501.x.
  35. Thorsen, A., Kjesbu, O.S., 2001. A rapid method for estimation of oocyte size and po- tential fecundity in Atlantic cod using a computer-aided particle analysis system. J. Sea Res. 46, 295-308.
  36. Weibel, E.R., Kistler, G.S., Scherle, W.F., 1966. Practical stereological methods for mor- phometric cytology. J. Cell Biol. 30, 23-38. https://doi.org/10.1083/jcb.30.1.23.
  37. White, G.G., Munroe, T.A., Austin, H.M., 2003. Reproductive seasonality, fecundity, and spawning frequency of tautog (Tautoga onitis) in the lower Chesapeake Bay and coastal waters of Virginia. Fish. Bull. 101, 424-442.
  38. Witthames, P.R., Greenwood, L.N., Dominguez, R., Korta, M., Kjesbu, O.S., Thorsen, A., Murua, H., Saborido-Rey, F., 2009. Advances in methods for determining fecundity: Application of the new methods to some marine fishes. Fish. Bull. 107, 148-164.
  39. Witthames, P.R., Thorsen, A., Kjesbu, O.S., 2010. The fate of vitellogenic follicles in ex- perimentally monitored Atlantic cod Gadus morhua (L.): Application to stock as- sessment. Fish. Res. 104, 27-37. https://doi.org/10.1016/j.fishres.2009.11.008.