Oogenesis and reproductive investment of Atlantic herring are functions of not only present but long-ago environmental influences as well

Abstract

Following general life history theory, immediate reproductive investment (egg mass × fecundity/body mass) in oviparous teleosts is a consequence of both present and past environmental influences. This clarification questions the frequent use of season-independent (general) fecundity formulas in marine fish recruitment studies based on body metrics only. Here we test the underlying assumption of no lag effect on gametogenesis in the planktivorous, determinate-fecundity Atlantic herring (Clupea harengus) displaying large plasticity in egg mass and fecundity, examining Norwegian summer-autumn spawning herring (NASH), North Sea autumn-spawning herring (NSAH), and Norwegian spring-spawning herring (NSSH). No prior reproductive information existed for NASH. Compared with the 1960s, recent reproductive investment had dropped markedly, especially for NSAH, likely reflecting long-term changes in zooplankton biography and productivity. As egg mass was characteristically small for autumn spawners, although large for spring spawners (cf. different larval feeding conditions), fecundity was the most dynamic factor within reproductive investment. For the data-rich NSSH, we showed evidence that transient, major declines in zooplankton abundance resulted in low fecundity over several subsequent seasons, even if Fulton's condition factor (K) turned high. Temporal trends in K slope (K on total length) were, however, informative. These results clarify that fecundity is defined by (i) dynamics of primary (standing stock) oocytes and (ii) down-regulation of secondary oocytes, both processes intimately linked to environmental conditions but operating at different timescales. Thus, general fecundity formulas typically understate interannual variability in actual fecundity. We therefore argue for the use of segmented fecundity formulas linked to dedicated monitoring programs.fishery | fecundity | zooplankton | lag effect | recruitment

Oocyte recruitment and fecundity type in fishes: Refining terms to reflect underlying processes and drivers

“…In addition, species with very slow oocyte growth rates such as Greenland halibut ( Reinhardtius hippoglossoides , Pleuronectidae) must begin oocyte recruitment to SG in the reproductive cycle prior to the spawning season they are spawned (Kennedy et al., ). Oocyte recruitment to SG with a duration greater than a year is reported both for total spawners like the Norwegian spring‐spawning herring, C. harengus, (dos Santos Schmidt et al., ) and for batch spawning determinate spawners like the Northeast Arctic cod (Thorsen & Kjesbu, ) and results in the appearance of a new cohort of SG oocytes which is clearly distinguished from the current season's crop (Figure ). This may also explain the cortical alveoli oocytes observed on striped mullet and striped bass at the time of spawning.…”

“…Because few fished populations have demonstrated senescence, maximum reproductive age is often considered comparable to maximum age. In most fishes, the reproductive cycle occurs at the annual scale (Bye, 1984;Rideout, Rose, & Burton, 2005) and includes a phase during which gonads are developing, a spawning capable phase (synonymous with the spawning period), followed by a phase in which gonads regress, to eventually enter the regenerating phase, indicative of reproductive inactivity (Brown-Peterson, Wyanski, Saborido-Rey, Macewicz, & Lowerre-Barbieri, 2011). At the individual level, the reproductive period is defined as the time between the onset of recruitment to SG and the spawning of the last oocytes during a reproductive cycle.…”

“…Total spawners by definition have determinate fecundity as all SG oocytes to be spawned are developed synchronously. Batch spawners, however, spawn multiple times within a spawning period, and fecundity type may be more commonly defined by the oocyte growth period (OGP) to spawning period ratio than internal control of SG recruitment events (Ganias et al, 2015;Rideout et al, 2005). Batch spawners with indeterminate fecundity exhibit "unrestricted" SG recruitment and will continue to recruit batches to be spawned within the spawning season (i.e.…”

The Reproductive Biology of Female Atlantic Herring in U.S. Waters: Validating Classification Schemes for Assessing the Importance of Spring and Skipped Spawning

“…Spring‐ and fall‐spawning Atlantic Herring in the Gulf of Maine and Georges Bank showed distinct oocyte development cycles, which are similar to the differences between Norwegian spring and summer spawners that initiate oocyte development at different times (dos Santos et al. ). In contrast, autumn‐ and winter‐spawning herring in the North Sea initiate oocyte development at the same time, with both development and down‐regulation occurring over a longer period in the latter, leading to fewer but larger eggs (van Damme et al.…”

Common trends in recruitment dynamics of north‐east Atlantic fish stocks and their links to environment, ecology and management

“…Consequently, the composition and condition of the spawning stock likely play an important role for stock productivity and resilience (Hixon et al., ). Our analysis also showed that time lags between condition, fecundity and spawning success can be detected, confirming previous findings (dos Santos Schmidt et al., ). It remains to be explored whether simplified proxies such as spawner demographics or mean weight are sufficiently capable of capturing these dynamics or whether better measurements are necessary.…”