M74 in Gulf of Bothnia and Bothnian Sea

The reproductive disorder “M74” causes mortality among yolk-sac fry of Baltic salmon. The de-velopment of M74 is linked with a deficiency in the salmon eggs of antioxidants, such as thiamine (vitamin B1), together with signs of oxidative stress and an unbalance in fatty acids of the paren-tal fish. The ultimate cause of M74 is unclear, but seems to be coupled to the species composition and flow of thiamine in the Baltic Sea food web (Keinänen et al., 2012; Ejsmond et al., 2019; Ma-janeva et al., 2020). More background information about the M74 syndrome can be found in the Stock Annex (Annex 3).

When calculated from Swedish and Finnish data combined, the proportion of salmon females whose offspring hatched in 2020 displayed increased mortality was on average 1%, compared to 6% in the preceding year (Table 3.4.1.1). The M74 incidences presented in Table 3.4.1.1 predom-inantly represent the percentage of females in a hatchery with a recorded increase in offspring mortality. In the rivers Simojoki, Tornionjoki, Kemijoki and Iijoki, however, mortalities are re-ported for the proportion of females affected by M74 and the mean percentage yolk-sac fry mor-tality (Table 3.4.1.2). In Swedish hatcheries, where only the proportion of females affected is reg-istered (and not the mean percentage yolk-sac fry mortality), the average proportion of offspring groups with increased M74-like mortality in 2020 across hatcheries was 1% (range 0–4%), com-pared to 7% (0–24%) in 2019 and 18% (11–22%) in 2018 (Table 3.2.1.1). Thus, the incidence of the M74 syndrome has decreased to the same low level as in the reproductive periods 2011/2012–

2013/2014, when no M74-related mortality was reported in the Finnish M74 monitoring data (Ta-ble 3.4.1.2) and historically low proportions of affected females were reported from Swedish hatcheries (Table 3.4.1.3).

In Finnish data, annual M74 estimates are based on female-specific experimental incubations in which M74 symptom-related mortality has been ascertained by observations of yolk-sac fry (un-til the reproductive period 2009/2010) and/or comparing mortalities with the thiamine concen-tration of eggs (from 1994/1995 and onwards) (Figure 3.4.1.1). From 2011/2012 to 2017/2018, Finn-ish data of the incidence of M74 are principally based on the free thiamine concentration of un-fertilized eggs, which has a strong correlation with M74-related mortality of yolk-sac fry (Vuo-rinen and Keinänen, 1999; Keinänen et al., 2014; 2018). However, control female-specific incuba-tions have been run at a hatchery (Vuorinen et al., 2014). Two type of results are presented: (1) the average yolk-sac fry mortality, and (2) the proportion of females with offspring affected by M74, (Keinänen et al., 2000; 2008; 2014; 2018; Vuorinen et al., 2014).

In line with the recent decrease in M74, the thiamine concentration in unfertilized eggs in autumn 2020 (reproductive period 2020/2021), computed as a mean for females from Finnish Bothnian Bay rivers, continued to increase compared to the preceding year (Figure 3.4.1.1); the concentra-tion was of the approximately magnitude as in the reproductive periods 2011/2012–2013/2014, when no M74-related mortality was reported in the Finnish M74 monitoring data (Table 3.4.1.2).

A yearly prognosis for the incidence of M74 in offspring groups (females) is carried out based on the concentration of free thiamine in eggs vs. yolk-sac fry mortality (%) relating to thiamine deficiency in female-specific laboratory incubations (in Finnish M74 monitoring data from the reproduction period 1995/1996‒2009/2010, n = 1009). The limit values of free thiamine used in prognosis are: for 100% mortality ≤0.2 nmol/g, for occurrence of M74 mortality ≤0.5 nmol/g, but excluding possible late M74 (M74?) ≤1.0 nmol/g. The prognosis for the proportions of M74 mor-tality among offspring groups hatching in spring 2021 was 0% (Table 3.4.1.1).

Mean annual yolk-sac fry mortalities and proportions of M74 females correlate significantly, but the M74 frequency has usually been somewhat higher than the offspring M74 mortality, es-pecially in years when many offspring groups with mild M74 occur, i.e. when only a propor-tion of yolk-sac fry die. In years when the M74 syndrome is moderate in most offspring groups, the difference between the proportion of M74 females and mean yolk-sac fry mortality can ex-ceed 20 percentage units (Keinänen et al., 2008). Currently (from 2019/2020 and onwards) the incidence of M74 in Finnish M74-monitoring is exclusively determined from the concentrations of free thiamine in unfertilized eggs. Proportions of M74 females and offspring mortalities are derived from the model by relating the free thiamine concentrations with yolk-sac fry mortali-ties from laboratory incubations in the spawning years 1994−2009 from the Finnish M74 moni-toring data. As mentioned above, in contrast to in Finland, Swedish data across the time-series are based only on the proportion of females whose offspring display increased mortality re-gardless of the proportion dying (Table 3.4.1.3).

In the hatching years 1992–1996, the M74 syndrome resulted in a high mortality of salmon yolk-sac fry with an M74 frequency (i.e. the proportion of the females whose offspring were affected) over 50% in most Swedish and Finnish rivers (Table 3.4.1.1). Since then the incidence of M74 has on average decreased. However, it has varied greatly even between successive years with ele-vated mortalities in some years (e.g. 1999, 2002, and 2006–2007) compared to others with low or non-existent mortalities (e.g. 1998, 2003–2005 and 2011–2015). In the reproductive period 2011/2012, the incidence of M74 could be considered as non-existent for the first time since the large outbreak in the 1990s. However, M74 returned in the reproductive period 2015/2016.

In years with a high M74 incidence, there has been a tendency that estimates of M74 mortality have been higher in Finland than in Sweden, but this difference seems to have disappeared in the years when the mortality has been low (Figure 3.4.1.2). The difference may be due to the fact that, in Finland all females caught for M74 monitoring have been included, whereas in Sweden females that have displayed uncoordinated swimming (wigglers) have been excluded from in-cubation.

Wiggling females are known to inevitably produce offspring that all die from M74. The propor-tion of wiggling females was high in the early and mid-1990s (Fiskhälsan, 2007). Trends and annual fluctuations in average proportions of M74-affected females have been very similar in Swedish and Finnish rivers (Figure 3.4.1.2). However, in some years M74 has been insignificant or absent in the Finnish M74 monitoring, whereas rather high M74 frequencies have been re-ported from some Swedish rivers. It seems that those Swedish results may rather result from technical failures or too high or variable water temperatures, as reported by Börjeson (2013).

In the ongoing Finnish M74 monitoring the estimated mortality and proportions of females af-fected have been ascertained by measuring the thiamine concentration of eggs (Figure 3.4.1.1).

Between 2015/2016 and 2018/2019, corresponding information was also obtained from two Swe-dish hatcheries (ICES, 2020a). In the Finnish M74 data, the annual M74 incidence among the monitored Bothnian Bay rivers has been very similar. Therefore, it is relevant to express the pro- portion of M74 females and annual M74 mortality as an average of all individual monitored salmon females (and respective offspring groups) that ascended those rivers (Keinänen et al., 2014). However, there may be some differences between salmon populations from rivers in the Bothnian Bay and in the Bothnian Sea, if migration routes and feeding grounds during the whole feeding migration differ, as reported by Jacobson et al. (2020). This could also explain different mortalities, reported during the early 1990s (Table 3.4.1.1), among offspring of salmon from the River Mörrum in AU 4, from where smolts descend directly into the Baltic Proper.

As described above, the incidence of M74 decreased and was virtually non-existent in 2012–2015.

However, the thiamine concentrations in unfertilized eggs of salmon ascended the rivers of the Gulf of Bothnia decreased in autumn 2015, and were even lower in salmon ascended in autumn 2016. Thus, after several favourable years, M74 again impaired salmon yolk-sac fry survival in 2016–2018. As detailed in the Stock Annex (Annex 3), the level of M74 in salmon shows a positive correlation to the abundance of important prey species in the Baltic, especially young sprat. The return of M74 in 2016–2018 thus has been suggested to be the consequence of an exceptionally strong year class of sprat hatched in 2014 (ICES, 2017b). Young sprat were exceptionally numer-ous in the northern areas of the Baltic Proper and Gulf of Finland. Moreover, the year class of herring (Clupea harengus) in 2014 was strong, e.g. in the Bothnian Sea (Raitaniemi, 2018).

In unfertilized eggs of salmon having ascended the Lithuanian River Neris in autumn 2017, the free thiamine concentrations were considerably higher compared to salmon of the Gulf of Both-nian rivers, and the incidence of M74 in hatching years 2018–2020 was very low or almost insig-nificant (albeit based on a small number of sampled fish). Apparently, those salmon have been feeding in the southern Baltic Proper, where the presence of cod, contrary to the northern Baltic Sea, has reduced sprat from its exceptionally high year class 2014 (ICES, 2017b). Thus, young

sprat from the year 2014 have been less numerous in the southern Baltic Proper than in the north-ern areas of the Baltic Sea (Raitaniemi, 2018), and the herring biomass as food for salmon, e.g. in SD 25, has been higher than that of sprat (Jacobson et al., 2018).

In the Stock Annex (Annex 3, Section C.1.6), a description is given of a Bayesian hierarchical model applied to the Gulf of Bothnian (GoB) monitoring data (Tables 3.4.1.2 and 3.4.1.3) of M74 occurrence from rivers in Finland and Sweden, to obtain annual estimates of the M74-derived yolk-sac fry mortality. This information is needed to fully assess the effects of M74 on the repro-ductive success of spawners. Besides annual estimates of M74 mortality in the rivers, where such has been recorded, the model provides annual estimates of the mortality for any GoB river, in which no monitoring has been carried out (Table 4.2.2.2, Figure 4.2.2.2). Most of the wild stocks, including all smaller wild rivers in the GoB, belong to this group. The results demonstrate that in some years, the actual M74 mortality among offspring has been lower than the proportion of M74 females indicated, which apparently is related (see above) to mildness of the syndrome, i.e.

to partial mortalities in offspring groups.