Discussion

Although widely geographically spread out, all European eels spawn in the Sargasso Sea and form one panmictic population. Some of their biological characteristics, such as age at maturation, growth, fecundity, can vary greatly depending on where they spend their growth phase, the yellow stage. It is unknown whether eels from certain regions contribute more to the spawning stock and whether this may change from year to year. The success of Anguilla anguilla as a species is probably linked to its incredible plasticity in terms of life-history strategies and biological characteristics. In the context of the decline, it is essential that all components of the population contribute to the spawning stock. The decline in recruitment has been more pronounced in the North than in the rest of Europe (1.9% versus 8.9% of the references levels in 1960-1979, ICES 2019). Norway represents the limit of the distribution area and it is there that changes in densities are more likely be detected. The time-series from the river Imsa is important for monitoring the stock. The Norwegian red list assessment for eel has also been based on this time-series. The previous assessment has used a mean age at maturation of 8 years based on the previous studies (Vøllestad &Jonsson, 1986, 1988). The present study reporting a mean age of 19 years for female silver eels will likely have an impact on the next revision of the Norwegian red listing (currently assessed as Vulnerable, VU).

Otolith processing methods and reading uncertainty

As expected, there were large differences in age estimates of eels between the two different methods, in toto (IT) and grinding and polishing (GP). The age difference was 11 y on average with a maximum of 29 y. The differences were not systematic, but ages using GP were always older than using IT. The present study confirms that GP is a better method for estimating age in the European eel than clearing of whole otoliths in ethanol. Cracking and burning was previously tested on otoliths of Imsa eels, but the burnt otoliths were difficult to read (Vøllestad & Jonsson, 1988). Revealing annuli on the otoliths is not the only challenge related to age estimation in eels. A proper validation of age determination is still lacking, especially for older eels (over 20 years) from northern latitudes, where growth is slow. In other words, it is uncertain whether all the annuli represent winter marks, since some can be very tightly distributed, forming bundles of annuli. In the present study, it was considered unlikely that all these bundled marks represented an annual increment; rather, one year was assigned to each bundle. In the absence of definitive annulus identification this was the best approach. It may have led to some under-estimation, but this was to some degree accounted for in the Otolith Uncertainty Index (OUI).
Further, in our study, 5% of the otoliths were unreadable. In comparison, this proportion was 10-30% for eels caught in Mediterranean lagoons where eels frequently change salinity and habitat (Panfilli and Ximenes, 1994). Still, 39% of the otoliths from the Imsa were difficult to read (OUI, level 3: uncertainty > 5 years). These may have qualified as “unreadable” by Panfilli and Ximenes (1994), but here we chose to assign a high uncertainty rather than discarding them.
Using otoliths of known age, Svedäng et al. (1998) showed that younger eels were consistently over-aged while older eels were under-aged. The reason for overestimations was the presence of supernumerary zones in younger eels that were misidentified as annuli. For older eels, it is difficult to detect annuli in the outer slow-growing part of the otolith. An additional inconsistency was found in readings by the same reader over time which could vary up to 6 years (Svedäng et al., 1998). The unknown age of glass eels at metamorphosis may add one to two years of uncertainty to the total age. Similarly, the outer bands may not be fully revealed at the edge of the otolith by a polishing and grinding method causing an under-ageing.
Some otoliths, however, are very clear and can be easily interpreted. Therefore, it is important to include some measure of confidence around the age determination, at least, until there is a proper age validation method. We suggest a simple method by implementing an otolith uncertainty index (OUI) such as described in the present study. Depending on the type of output where age data is needed, ranging from population dynamics models to management advice, subsets of data can be selected based on their OUI. The development of machine learning methods for automatic otolith image analyses is promising (Moen et al., 2018). An OUI index will also be useful in that sense, for selecting suitable learning datasets.

Evolution of the age distribution of silver eels in the river Imsa

As expected, age at silvering varied greatly in the eels from the river Imsa (females: 8-35 years; males: 9-23 years), but the overall mean varied only slightly across decades (from 19 to 21 years in the 2010s). Since most age readings had an associated uncertainty of 3 to 4 years, this 3-year increase is meaningless, although statistically significant. Actually, given the disappearance of young silver eels (less than 15 y) during the more recent decades, it is surprising that the mean and median age were not more affected. However, mean age of silver eels is bound to increase even more in the river Imsa with the consistently low numbers of ascending recruits the last 2-3 decades. But in 2009 and 2014, elver recruitment increased and almost reached the 10 000-individual threshold. An effect on the number of silver eels might not be detected before at least 10-15 years later. If these two peaks do affect the number of silver eels, it will not happen before 2022. In any case, if recruitment does not improve, this increase will be short-lived, and perhaps non-detectable due to the low levels during most of the last 15 years.

Length at silvering

Eels are present in many types of habitats and salinities: coastal, lagoons, lakes, rivers, marshes, fjords, and estuaries. Length (and not only age) distributions can vary greatly among these habitats (Vøllestad 1992; Vøllestad & Jonsson 1986; Svedäng, Neuman, & Wickström, 1996; Holmgren, Wickström, & Clevestam, 1997; Melia et al., 2006; Durif et al., 2009; Poole et al. 2018). All eels need to accumulate fuel for the sustained high-intensity swimming necessary for the journey to the Sargasso Sea, but females will face higher energetic demands in order to produce eggs. This leads to different life-history strategies and a sexual dimorphism based on differences in length at maturity (Bertin, 1956; Tesch, 2003). Male eels migrate at around 35 cm (in this study 40 cm), minimizing the duration of their yellow stage, while females migrate at sizes of 40 to 130 cm, optimizing their size to reach a higher fecundity (Helfman, Facey, & Hales, 1987; Vøllestad, 1992; Tesch, 2003; Durif et al., 2009). In the northern part of the distribution area, eels (males and females) are on average larger than in southern areas, and this has been linked to the increasing distance they have to swim to reach the spawning area (Tesch, 2003; Durif et al, 2009; Vøllestad, 1992). Yet in the present study, which was located at a relatively high latitude (58.9⁰ N), most female eels migrated at a body length around 60 cm and a small contingent of eels migrated at body length around 40-55 cm. Possibly, some eels could have stopovers on their way to the Sargasso Sea; but in the case of Norway, there is no obvious location for a stopover, since silver eel spawners take the northern route (north of the Shetlands) rather than through the Dover straight (Kettle, Vøllestad, & Wibig, 2011; Westerberg, Sjöberg, Lagenfelt, Aarestrup, & Righton, 2014). The best gonad-to-body size ratio under experimental artificial maturation, was found in eels longer than 70 cm (Durif, Dufour, & Elie, 2006). Once a specific size is reached, a period of high growth probably triggers silvering (Huang et al., 1998; Durif et al., 2005). Recent work in reproductive endocrinology has identified the kisspeptin system as essential for the onset of puberty in mammals but also in teleost fish (Seminara et al., 2003; Zohar et al., 2010; Pasquier et al., 2018). In eels, kisspeptins regulate the expression of gonadotropins. They may be the link between environmental factors and the reproductive axis through the regulation of growth hormone (Huang et al, 1998; Zohar et al., 2010; Kim, Choi, Park, & Choi, 2015).

Growth of eels

The new age estimates using the grinding and polishing (GP) method indicate that eels in the river Imsa spend a substantially longer period as yellow eels in freshwater than previously thought (Vøllestad & Jonsson, 1986). Previous estimates of silver eels in the river Imsa, suggested a mean age of 5 years for male and 8 years for female silver eels (Vøllestad et al., 1986), while the new estimates indicated a mean age of 15 years for males and 19 years for females. At the time it was concluded that eels in the river Imsa grew quickly, with a mean size increment of around 70 mm y-1, which is comparable to growth in brackish water and in southern Europe (Rossi & Colombo 1976; Vøllestad, 1985; Acou et al., 2003). In the river Imsa, slower growth is more likely (this study: 30 mm y-1, because at these latitudes the growth season is shorter than in southern Europe as eels stop feeding when the water is colder than 8-10℃ (Vøllestad et al., 1986; Riley, Walker, Bendall, & Ives, 2011; Westerberg & Sjöberg, 2015). This was also visible through the patterns of the annuli. Tight, numerous rings are interpreted as short growth seasons. Our method to determine growth rate was simple and did not take into account changing growth rates over the lifetime. The new mean growth estimate in the river Imsa is 30 mm y-1, which is less than half of what was previously documented. This new value is in line with newer growth estimates of eels in freshwater and in the northern part of the distribution range (Aprahamian 2000; Arai, Kotake, & McCarthy, 2006; Lin, Lozys, Shiao, Iizuka, & Tzeng, 2007; Simon, 2007, 2015; Silm, Bernotas, Haldna, Järvalt, & Nõges, 2017).
Growth of eels in the river Imsa has not changed since the 1980s. This was contrary to what was expected. Water temperature has also increased due to climate change and this has provided longer growth seasons. Additionally, a reduced number of ascending recruits has led to a lower density of yellow eels in the freshwater habitat; this should have resulted in better growth and faster onset of the silvering process, leading up to silver eel descending at a younger age in recent years than in previous periods. Early analyses based on different ageing methodology did indicate density-dependent mortality in Imsa (Vøllestad & Jonsson, 1988), opening the possibility also for density-dependent growth.
There were very few individuals younger than 15 years in the samples from 2012-2016. This agrees with the large reduction in recruitment from the late1990s. The recruitment has remained low since then, with almost no recruitment in several years in the mid-2000s and later (Figure 6). This gives us extra confidence in the new age estimations. Silver eels younger than 15 years from 2012-2016 have entered the river after 1997-2001, hence with the large decline in recruitment a large decline in this age group was also expected. The IT method would have estimated most eels sampled in the 2010s to be around 10 years old with a cutoff value at 5 years, meaning a decline around 2007-2011. This was not the case and therefore estimates from the GP method are more likely.

Sex ratio

Male eels have always been scarce in the river Imsa; in the 1980s they represented 3-7% of the total run, but they all disappeared in the 2010s (Poole et al, 2018). Sex determination in eels is metagamic, meaning it is non-genetic (Geffroy & Bardonnet, 2016). Sex ratios are indeed skewed at individual localities and there is a geographic bias associated with latitude and longitude (Helfman et al. 1987; Oliveira, McCleave, & Wippelhauser, 2001; Davey & Jellyman, 2005). The general pattern is that male eels are more abundant at southern latitudes and mainly in the lower reaches of rivers, whereas females dominate at higher latitudes and with increasing distance to the sea. Additionally, high eel densities are usually associated with higher proportions of males (Parsons, Vickers, & Warden, 1977; Beentjes & Jellyman, 2003, 2015; Davey & Jellyman 2005; Laffaille, Acou, Guillouët, Mounaix, & Legault, 2006; Harrison, Walker, Pinder, Briand, & Aprahamian, 2014); although, a study done in a laboratory showed opposite results (Huertas & Cerda, 2006). This later study, and others, also suggest that sex determination occurs during the first 3 months of growth (Davey & Jellyman, 2005; Huertas & Cerda, 2006).
The density factor may affect sex ratio through 1) food availability, depletion of food resources and lower growth or 2) through social interactions: possibly through odors of conspecifics or even through cannibalistic behaviors which would skew the sex ratio since females are larger than males (Davey & Jellyman, 2005).
Eel density in the Imsa catchment has severely decreased following the decline in recruitment since the late 2000s (Figure 6). However, in our study, growth has remained unchanged over the decades, and therefore cannot explain the disappearance of male eels. Therefore, social interactions (i.e.: density-dependence) are probably important for determining sex in eels.

Link between ascending recruits and descending silver eels

In the light of the low annual number of ascending juvenile eels and the relatively high number of silver eels, a mean age of silver eels at 19 years for females and 15 years for males indicates that mean annual mortality in freshwater has to be very low (<<10%). The termination of eel fishing in the Imsa water course in 2006 has likely contributed to a reduced freshwater mortality, but natural mortality may anyway appear to have been very low all through the study period. In a river-lake system mainly inhabited by invertebrate-feeding brown trout (Salmo trutta ), whitefish (Coregonus lavaretus ), Arctic charr (Salvelinus alpinus ) and three-spined sticklebacks (Gasterosteus aculeatus ), the main predation mortality in eels is likely restricted to the very early yellow eel stages. There are reports of minks being caught in the trap and which probably also cause some mortality.
Because of the long residency in freshwater (>15 years) for eels in the river Imsa, even a time series of more than 40 years is too short to allow a robust analysis of the relationship between the number of ascending recruits and the resultant number of descending silver eels. The wide silver eel age distributions, together with the stochastic environmental effect on the silvering process and annual number of descending eels, mask any potential signal from the variation in number of recruits. The annual variation in the number of recruits will be reflected in a large number of silver eel cohorts, resulting in a very smoothed signal from the variation in recruits. For example, as the age variation in female silver eels in river Imsa spans 35 years (minimum age = 5 years, maximum age = 39 years), a time series of 44 years (since 1975) will only include the complete number of silver eels for approximately five cohorts of recruits. In addition, as the environmental and habitat variables may have changed substantially during the 44 year period (for example temperature, Poole et al., 2018), we cannot expect a stable relationship between the numbers of ascending recruits and silver eels over the years, and attempting to split the time series into periods with relatively similar environmental conditions and fit models to these will be futile.
In addition, we know little about the factors governing growth, mortality and strategic choices during the freshwater life phase of eels, so it will be difficult to parameterize a model adequately. For example, how should we include the effect of density in the model? Will reduced overall densities mainly affect densities in unfavorable habitats or habitats further from the sea (above the lakes), while density remain high in favorable habitats, as indicated by Boulenger et al. (2016)? Will the effect of increased density be increased mortality, due to more competition for resources or more predation from older eels, or reduced growth due to displacement to lower quality habitats? At very low densities, other effects like Allee effects, depensatory mechanisms, changing sex-ratios or life history strategies can also obscure the relationship (see references in Poole et al., 2018; Sandlund et al., 2017). One should also note that developing river-wise stock-recruitment models for European eel is not possible. The species is panmictic (Palm, Dannewitz, Prestegaard, & Wickström, 2009; Als et al., 2011), with a biology that implies a weak, or no, connection between the number of silver eels leaving any watercourse for spawning in the Sargasso Sea and the number of glass eels returning to that watercourse.
In conclusion, the method of revealing annuli is one of the elements that can improve the precision and the accuracy of age estimates. Grinding and polishing the otolith seems a better method than reading the age “in toto” for older eels with a lifetime of more than one decade. However, beyond the method, there are two types of errors associated with age determination in fish: a process error related to how well the otolith reflects the complete growth record of the fish throughout its lifetime, and observation errors linked to the interpretation of these annuli (Campana, 2001). In eels, several studies have verified the correspondence between otolith structures and seasonal increments (Moriarty, 1983; Chrisnall & Kalish 1993; Oliveira, 1996; Svedäng et al., 1998), however, reading age of slow-growing eels remains a challenge. Separating false checks from real winter marks will require a proper validation of the growth increments, especially for the northern part of the distribution area where growth is slower and occurs over a shorter period. The new age distribution we determined, however, was consistent with the dynamics of elver recruitment in the river Imsa since 1975. This gives us some extra confidence in our age determination: eels have been spending on average 19 years in freshwater since the 1980s and this has only slightly increased during the 2010 (mean of 21 years). Still, the variation around these numbers is considerable, from 5 to 39 years, and this means that eels from up to 34 cohorts of recruits (elvers, small yellow eels) can be included in each year’s group of descending silver eels. In this case, developing a model that links annual numbers of ascending recruits and silver eels is likely futile.
Acknowledgments
This study was funded by the Norwegian Environment Agency, the Norwegian Institute for Nature Research, and the European Inland Fisheries and Aquaculture Advisory Commission (EIFAAC) and the authors would like to acknowledge the long-term commitment to maintaining the monitoring stations. We would like to gratefully thank the technical and field staff at Imsa.
Conflict of interest
None declared.
Author contribution
All authors were involved in the conception and design of the article. Additionally, CMFD wrote the paper, analyzed and read the otoliths, analyzed and interpreted the data; OHD was involved in writing the paper, analyzed and interpreted the data. LAV analyzed the historical otolith collection and was involved in interpretation of data, drafting, and revising the manuscript. OTS, EBT, and RP were involved in interpretation of data, drafting, and revising. KB was involved in sampling the otoliths and maintenance of the time series. RHEL and SS processed and read the otoliths.
Data Availability statement
The authors agree to deposit the data in Dryad if/when the article is published.
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