ICHTHYOLOGY LAB. School of Biology, Aristotle University of Thessaloniki, Greece

1. FISH REPRODUCTION AND FISHERIES [FRESH], Final Conference Vigo 16-20 May 2011 Determining the indeterminate: a conceptual mechanism for the regulation of the fecundity pattern in marine teleosts Konstantinos Ganias ICHTHYOLOGY LAB. School of Biology, Aristotle University of Thessaloniki, Greece Jerry Ostriker (1971) Sci Am: the nature of pulsars

2. Determining the indeterminate: a conceptual mechanism for the regulation of the fecundity pattern in marine teleosts Brief historic overview on potential annual fecundity Evolving concepts in the pre- John Hunter age The legendary 80s The rise of a new (golden) era Modeling fecundity regulation patterns Conceptual model Simulation model Validation of the model Oocyte density vs. oocyte diameter Case studies Relating fecundity patterns to fish biology/ecology

3. Evolving concepts in the pre- John.Hunter era Potential annual fecundity Fecundity & ichtyoplankton methods 1897 • Hensen & Apstein Fulton 1898 first proposed the idea that the biomass of a stock can be estimated from its spawn studied 36 species; observed differences in OSFD between pelagic and demersal species. In species with demersal eggs there was clear size separation between yolked – unyolkedoocytes before the advent of spawning whilst in pelagic spawners there was no clear demarkation. Association with the duration of the spawning season. Clarke • Cushing • The number of pilchards in the channel 1934 1936 combined fecundity with ichtyoplankton data to provide estimates of abundance Hickling & Rutenberg 1957 • Saville • Estimation of the abundance of a fish stock from egg and larval surveys Qaqsim & Qayyum 1962 estimated SSB by dividing an estimate of egg production by the product of batch fecundity and the %females (assuming S=1) 1963 Macer 1974 • Lockwood et al. Morse 1981 estimated SSB of mackerel using the AEPM [classic application] the main assumption for multiple spawners was that all eggs to be spawned in a season are yolked at the beginning of the season. Spawning ends when these yolked eggs are depleted [Hunter & Leong 1981]` The AEPM was the only ichtyoplankton method for estimating SSB until the 1980’s

4. Clark [1934} showed for sardine that intermediate batches in the OSFD would neither be reabsorbed nor spawned in later years (increased in size along with the spawning mode)

5. Hickling & Rutenberg [1936] 4 species; similar results with Fulton

6. Qaqsim & Qayyum [1962] 19 freshwater species; similar results with Fulton

7. Macer [1974]: 19 freshwater species; similar results with Fulton

8. Morse [1980]: FISH BULL VOL.78 mackerel (Scomberscombrus); Mid-Atlantic Bight

9. The legendary 80s Potential annual fecundity Fecundity & ichtyoplankton methods Hunter & Goldberg FISH. BULL, Vol. 77 Introduced the POF method Parker FISH. BULL, Vol. 78 1980 DeMartini & Fountain FISH. BULL, Vol. 79 1981 Introduction of the DEPM Hunter & Leong FISH. BULL, Vol. 79 Lines of evidence for continuous spawning during the spawning season. NOAA DEPM Manual 1985 Hunter & Macewicz NOAA DEPM Manual Introduction of the terms Indeterminate-Determinate fecundity Lo et al. ICES J Mar Sci Hunter et al. CalCOFi, Vol. 30 Introduction of the DFRM 1989 Lines of evidence for Determinate spawners Bull Mar Sci SPECIAL VOLUME on ichtyoplankton methods Hunter et al. FISH. BULL, Vol. 90 1992 Potential bath fecundity in Determinate spawners 1993

10. Hunter & Leong [1981]: FISH BULL VOL.79 Spawning energetics of northern anchovy

11. Use of terms determinate/indeterminate fecundity in the literrature Influence of the 2 DEPM manual papers Hunter et al. [1985] Spawning frequency Cit=267 Hunter & Macewicz [1985] Batch fecundity Cit.=189

12. Lines of evidence for: Indeterminate fecundityHunter& Leong[1981] • Large S during the spawning months whilst at any time the caloric content of the ovary corresponded to 1-2 batches • Inverse relationship between the number of the spawning batches and the maturation rate of the ovary • Egg maturation is continuous until all oocytes are spawned Indeterminate fecundityHunteret al.[1989] • Formulation of a gap between the standing stock and less mature oocytes • Total fecundity declined with the spawning season • Total fecundity was lower in females having POFs • Mean oocyte diameter increased over the spawning season Accuracy in potential annual fecundityHunteret al.[1992] • That fecundity is determinate • Total fecundity declined with the spawning season • Total fecundity was lower in females having POFs • Mean oocyte diameter increased over the spawning season

13. Ichtyoplankton methods In egg or larva production, procedures are standardized and well understood [Smith and Richardson, 1977] Fecundity estimates continue to be the Achilles heel of ichthyoplankton-based biomass estimation [Hunter & Lo, 1993] Stratoudakis et al. [2006] Fish & Fish

14. 1987 1990 2001

15. Greer Walker et al. [1993] Fecundity assessment of Atlantic mackerel (Scomberscombrus) mixed evidence • Formation of a gap between the standing stock and less mature oocytes Indeterminate …Hiatus doesn’t develop prior to spawning and the small hiatus that develops during spawning is not typical of determinate spawners… • Total fecundity declines with the spawning season Determinate …The total number of vitellogenic oocytes declines markedly during spawning… • Total fecundity is lower in females having POFs Determinate …Females with POFs contain fewer vitellogenic follicles than the prespawning fish… • Seasonal evolution of oocytediameter increased over the spawning seasonIndeterminate …the diameter of the vitellogenic follicles remained constant with progress through spawning…

16. Greer Walker et al. [1993]: Fecundity assessment of Atlantic mackerel (Scomberscombrus) additional criteria • Production of PVOs during the spawning season Determinate …there was a reduction in the number of oocytes at the size range of the threshold with the progress towards spawning …the number of PVOs produced during the current season approximates to that required to produce the potential annual fecundity in the following year… • Seasonal pattern of atresiaDeterminate …maximum atresia occurs 2/3 on the way through spawning and not at the end of spawning… • Oocyte growth vs. duration of the spawning season Determinate …VOs mature over a period of 140-154d and it is therefore not possible for an oocyte to mature during the spawning period which lasts between 60-90d… …this evidence suggests that although AM is not typical fish with determinate fecundity because of a well developed hiatus the majority of the data, particularly the evidence from oocyte growth rates means that for practical purposes it can be regarded as having determinate fecundity …

17. Recruitment of oocytes during the spawning period Hunter et al. [1992] Greer Walker et al. [1993]

18. Recruitment of oocytes during the spawning period evidence from applications of the autodiametric method Kurita & Kjesbu [2008] Witthames et al. [2009] Korta et al. [2010] A. Herring [determinate] B. Herring [determinate] Lower power of the autodiametric method for the indeterminate species: due to production of oocytes below the size threshold of measured oocytes (<200μm) Fit was significantly improved when the threshold size of measured oocytes decreased to 90μm, indicating production of PVOs during the spawning season Stage specific validity of the autodiametric method

19. Witthames & Greer Walker [1995] Fecundity assessment of NA sole (Soleasolea) • Oocyte growth vs. duration of the spawning season …the observed maximum growth rate even when adjusted for the positive influence of temperature allowed little scope for PVOs to complete maturation during a spawning period of 60d … …2 closely related populations of sole (Solea lascaris & Solea impar) display quite larger spawning periods (135 and 105d respectively). These 2 populations show continuous recruitment of oocytes during the spawning season and thus indeterminate fecundity …

20. Conceptual model for the regulation of the fecundity pattern Case a. determinancy: oocyte growth > spawning period [batch recruitment period] Oocyte growth 5th batch 4th batch +lag 3rd batch 2nd batch 1st batch No batch recruitment t = Batch recruitment period Spawning period Case b. indeterminancy: oocyte growth < spawning period [batch recruitment period] -lag Oocyte growth 5th batch 4th batch 3rd batch 2nd batch 1st batch batch recruitment t = Batch recruitment period Spawning period

21. Simulation model 3 populations of multiple spawners shedding the same number of spawning batches per season [10 batches] displaying the same interspawning interval [11d] which does not change through the season Each batch consists of 50 oocytes; their sizes [area] come from a normal distribution Oocytegrowth is linear with time and the %growth [600%] corresponded to the growth from POs to FOM Spawning season is the same for the 3 populations [11*10=110d OR 3m 20d] Oocyte growth [time period of oocytes to grow from POs to FOM] differed Population A: 143d [4m 23d] Larger that the spawning season Population B: 75d [2m 15d] Closer to the spawning season Population C: 28d Much smaller than the spawning season

22. Simulation model procedure Batch production and growth was simulated using a 2D vector animation software [Synfig Studio] Each particle was a perfect circle and held its own position in the panel taking care not to overlap while it grows with other particles Timescale was set in a way that each second corresponds to 1 month [divided into 30f] Particles were grouped to 10 groups [batches] Each batch was set to grow, appear, and disappear based on the hypothesized oocyte growth of each population [28, 75, 143f] Sequential batches appeared every 11f Each frame could be saved as different image [6f/s]

23. Model output Population A Oocyte growth period Oocyte recruitment period Spawning period Determinate spawner • No recruitment of new batches during the spawning season • No hiatus before the onset of spawning • Total fecundity: dome shaped pattern with time • Oocyte size: increase constantly over time • Growing hiatus inside the spawning season

24. Model output Population B Oocyte growth period Oocyte recruitment period Spawning period Indeterminate spawner • Recruitment of new batches during the spawning season • No hiatus before and during most of the spawning season • Total fecundity: dome shaped pattern with timed • Oocyte size: increase for most of the period • Growing towards the end of the spawning season

25. Model output Population C Oocyte growth period Oocyte recruitment period Spawning period Indeterminate spawner • Recruitment of new batches during the spawning season • Highly modal, 2/3 batches • Total fecundity: stable for most of the season • Oocyte size: stable for most of the period • Hiatus: only at the end of the spawning season

26. Model output c. indeterminate spawner Stabilization phase [Kjesbu 2010] max TF determinate max TF intermediate Dynamic equilibrium period [POFs] max TF indeterminate S.P. indeterminate S.P. intermediate S.P. determinate constant increasing

27. Validation of the model Oocyte density vs. oocyte diameter OPD=total number of objects/total area Hunter et al. [1992]

28. Case studies sardine Multinomial model Analysis of time lags [YV1 vs. YG] >> spawning period: 143d oocyte growth: 45d prespawners postspawners spawners 45d 72 215

29. Case studies 3 3 1 1 1 4 2 2 sardine Mediterranean sardine Atlantic sardine S=0.09 ISI=11d Oocyte growth=45d #batches=45/11=4 Ganias [2011] Mar Coast Fish Ganias [2008] Mar Biol OSFD in histo-sections Batch fecundity : total fecundity #batches=4-5

30. Case studies seasonal pattern of OSFD in determinate spawners Kjesbu et al. [1990] CJFAS Witthames & Greer-Wlaker [1995] Hunter & Macewicz [1989] seasonal pattern of OSFD in indeterminate spawners Merlucciusproductus Merlucciusmerluccius Hunter & Macewicz [2003] Murua & Motos [2006] J Fish Biol

31. Case studies Shape of OSFD Kjesbu et al. [1990] CJFAS

32. Case studies seasonal pattern of total fecundity in determinate spawners sablefish sole Macewicz & Hunter [1994] CalCOFi Witthames [2003] CalCOFi Kjesbu [2010]

33. Case studies Other relationships c Skjæraasenetal. (2010) MEPS

34. Case studies Other relationships c Kjesbu [1994] J Fish Biol start of spawning time, cod

35. Relating fecundity pattern to fish biology/ecology Basic assumptions for determinate/indeterminate spawners

36. Relating fecundity pattern to fish biology/ecology Latitudinal shifts un spawning season N. American herring stocks N. Atlantic sardine stocks Hay [1986]

37. Relating fecundity pattern to fish biology/ecology Effect of temperature on oocyte growth rate Witthames & Greer-Walker [1995] 9.60C Barents Sea 50C Kurita et al. [2010] Kjesbu et al. [2010]

38. Relating fecundity pattern to fish biology/ecology Lag in spawning season Kjesbu et al. [2011] CJFAS Rijnsdorp & Witthames [2005] Steeper

39. Relating fecundity pattern to fish biology/ecology Lag in spawning season Data from 68 stocks of multiple spawning species

40. Relating fecundity pattern to fish biology/ecology Lag in spawning season

41. Relating fecundity pattern to fish biology/ecology Lag in spawning season Dover sole Atlantic cod Greenland halibut Hunter et al. [1993] Fish Bul Kjesbu et al. [2011] MCF Kennedy et al. [1993] CJFAS

42. Relating fecundity pattern to fish biology/ecology Boreal vs. tropical temperate BOREAL latitude TEMPERATE TROPICAL Murua & Saborido-Rey. [2003] 26/33 [ca. 80%] revised NA fish stocks: determinate

43. Thank you Ian Curtis