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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