Variation in the post‐smolt growth pattern of wild one sea‐winter salmon (Salmo salar L.), and its linkage to surface warming in the eastern North Atlantic Ocean

Christopher D Todd,Nora N Hanson,Lars Boehme,Ana R Marques,Crawford W Revie

doi:10.1111/jfb.14552

Abstract

Variation in circulus spacing on the scales of wild Atlantic salmon is indicative of changes in body length growth rate. We analyzed scale circulus spacing during the post-smolt growth period for adult one sea-winter salmon (n = 1947) returning to Scotland over the period 1993-2011. The growth pattern of the scales was subjectively and visually categorized according to the occurrence and zonal sequence of three intercirculus spacing criteria ("Slow", "Fast" and "Check" zones). We applied hierarchical time-series cluster analysis to the empirical circulus spacing data, followed by post hoc analysis of significant changes in growth patterns within the 20 identified clusters. Temporal changes in growth pattern frequencies showed significant correlation with sea surface temperature anomalies during the early months of the post-smolt growth season and throughout the Norwegian Sea. Since the turn of the millennium, we observed (a) a marked decrease in the occurrence of continuous Fast growth; (b) increased frequencies of fish showing an extended period of initially Slow growth; and (c) the occurrence of obvious growth Checks or hiatuses. These changes in post-smolt growth pattern were manifest also in decreases in the mean body length attained by the ocean midwinter, as sea surface temperatures have risen.

Highlights

Counts and measurements of the numbers and spacing of growth rings deposited on the calcified portion of teleost scales can provide detailed archival data on the age and growth history of individual fish (e.g. Bilton and Robins, 1971; Casselman, 1987)
With specific reference to Scotland, a recent analysis of the ICES Working Group on North Atlantic Salmon (ICES, 2018) reported that the general decline in pre-fishery abundance of maturing salmon was forecast to continue. These declines likely reflect falling survivorship at sea (Olmos et al, 2019), but it is important to note that run-timing of returning 1SW adults in Scotland has shown progressive delays since the turn of the millennium (Todd et al, 2012) and that marine growth amongst European stocks has been compromised in recent decades (Bacon et al, 2009; Bal et al, 2017; Jonsson et al, 2016; Todd et al, 2008)
The perception is that these changes in growth performance and phenology are not a direct physiological response of salmon to a warming ocean climate, but are indirectly driven by ocean warming and manifest as changes in the availability of epipelagic prey to salmon at sea (e.g. Beaugrand and Reid, 2012; Jonsson et al, 2016; Nicola et al, 2018; Piou & Prévost, 2013; Todd et al, 2008)

Summary

Introduction

Counts and measurements of the numbers and spacing of growth rings (circuli) deposited on the calcified portion of teleost scales can provide detailed archival data on the age and growth history of individual fish (e.g. Bilton and Robins, 1971; Casselman, 1987). The marine circuli on wild Pacific and Atlantic salmonid scales typically show considerable variation in their spacing, often in distinct zones of differing width which may reflect marked intra-seasonal variation in growth rate. A wider inter-circulus spacing can be indicative of increased growth rate in body length (Fisher and Pearcy, 2005; Peyronnet et al, 2007), but the latter may be manifest by increased numbers of circuli (Haraldstad et al, 2016). Notwithstanding the likely complexity of environmental temperature and prey availability influencing circulus formation, measures both of the numbers and spacing of marine circuli for wild juvenile Atlantic salmon (Salmo salar L.) in their first (= post-smolt) marine growth season have been interpreted as indicators of growth variation, and with possible linkage to changes in size-related mortality at sea Notwithstanding the likely complexity of environmental temperature and prey availability influencing circulus formation, measures both of the numbers and spacing of marine circuli for wild juvenile Atlantic salmon (Salmo salar L.) in their first (= post-smolt) marine growth season have been interpreted as indicators of growth variation, and with possible linkage to changes in size-related mortality at sea (e.g. Hogan and Friedland, 2010; Friedland et al, 2000, 2006, 2009; McCarthy et al, 2008; Peyronnet et al, 2007)

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