Time series covering up to four decades reveals major changes and drivers of marine growth and proportion of repeat spawners in an Atlantic salmon population

Abstract

Wild Atlantic salmon populations have declined in many regions and are affected by diverse natural and anthropogenic factors. To facilitate management guidelines, precise knowledge of mechanisms driving population changes in demographics and life history traits is needed. Our analyses were conducted on (a) age and growth data from scales of salmon caught by angling in the river Etneelva, Norway, covering smolt year classes from 1980 to 2018, (b) extensive sampling of the whole spawning run in the fish trap from 2013 onwards, and (c) time series of sea surface temperature, zooplankton biomass, and salmon lice infestation intensity. Marine growth during the first year at sea displayed a distinct stepwise decline across the four decades. Simultaneously, the population shifted from predominantly 1SW to 2SW salmon, and the proportion of repeat spawners increased from 3 to 7%. The latter observation is most evident in females and likely due to decreased marine exploitation. Female repeat spawners tended to be less catchable than males by anglers. Depending on the time period analyzed, marine growth rate during the first year at sea was both positively and negatively associated with sea surface temperature. Zooplankton biomass was positively associated with growth, while salmon lice infestation intensity was negatively associated with growth. Collectively, these results are likely to be linked with both changes in oceanic conditions and harvest regimes. Our conflicting results regarding the influence of sea surface temperature on marine growth are likely to be caused by long‐term increases in temperature, which may have triggered (or coincided with) ecosystem shifts creating generally poorer growth conditions over time, but within shorter datasets warmer years gave generally higher growth. We encourage management authorities to expand the use of permanently monitored reference rivers with complete trapping facilities, like the river Etneelva, generating valuable long‐term data for future analyses.

Overruled by nature: A plastic response to an ecological regime shift disconnects a gene and its trait

“…Although these changes are thought to be caused by a regime-shift in oceanic conditions in 2005 23 , whether they reflect rapid evolution or plastic responses is unknown. The same trends towards later maturation have also been documented in the salmon population inhabiting the river Etne on the west coast of Norway, where the proportion of fish maturing after one year at sea dropped from 63% in the period 1983-84 to 34% in 2018-19 27 . The main objective of the present study was to investigate whether the observed changes in age at maturation were the result of phenotypic plasticity, or alternatively, evolution in the gene(s) influencing this trait.…”

“…2022), whether they reflect rapid evolution or plastic responses is unknown. The same trends towards later maturation have also been documented in the salmon population inhabiting the river Etne on the west coast of Norway, where the proportion of fish maturing after one year at sea dropped from 63% in the period 1983-84 to 34% in 2018-19 (Harvey et al . 2022).…”

“…This result seems to indicate a change in environmental conditions, creating a situation where the influence of vgll3 was effectively bypassed before natural selection had time to operate, whereas selection had the time to modify the allelic frequencies at the six6 locus before the influence of this gene was also bypassed. This hypothesis is strongly supported by the observations of sudden change in age at maturation in many Atlantic salmon populations inhabiting Northeast Atlantic rivers 23 , including the population in the river Etne 27 , where a highly distinct and sudden drop in early marine growth was reported in 2005 and subsequently, referred to as an ecological regime shift in the northeast Atlantic ocean 23 .…”

“…This result seems to indicate a change in environmental conditions, creating a situation where the influence of vgll3 was effectively bypassed before natural selection had time to operate, whereas selection had the time to modify the allelic frequencies at the six6 locus before the influence of this gene was also bypassed. This hypothesis is strongly supported by the observations of sudden change in age at maturation in many Atlantic salmon populations inhabiting Northeast Atlantic rivers(Vollset et al 2022), including the population in the river Etne(Harvey et al 2022), where a highly distinct and sudden drop in early marine growth was reported in 2005 and subsequently, referred to as an ecological regime shift in the northeast Atlantic ocean(Vollset et al 2022).As this, and other salmon population in the Northeast Atlantic were subjected to the same ecological regime shift, leading to consistently reduced marine growth rates and increased age at maturation, we conclude that growth-driven plasticity has almost completely bypassed the combined influence of vgll3 and six6 within on age at maturation, and furthermore, on resolving the sexual conflict for this trait in Atlantic salmon. Together with the interaction between vgll3 and six6 described in the historical data, the dissociation between genes and age at maturation represents an original finding that changes our understanding of the genetic architecture of age at maturation in Atlantic salmon.…”

Strong effects of temperature, population and age-at-maturity genotype on maturation probability for Atlantic salmon in a common garden setting

“…Further, some males never leave their home river and instead mature at a small size at the parr life stage, and so, mature individuals returning from the sea can be several thousand times larger than their mature river-bound counterparts. In recent decades, wild Atlantic salmon stocks have been in decline, with factors suggested to have contributed to this decline including climate change, aquaculture, illegal fishing, hydropower dams and harvesting of prey species (Chaput, 2012;Czorlich et al, 2022;Dadswell et al, 2021;Harvey et al, 2022;ICES, 2019;Vollset et al, 2022). Some of these factors have also been associated with life-history changes in the wild stocks, with some populations experiencing a decrease in the number or proportion of early-maturing individuals (Vollset et al, 2022), while others are reporting a decrease in large, late-maturing, individuals (Czorlich et al, 2018(Czorlich et al, , 2022Olmos et al, 2019).…”