Otolith annual growth increments for cod populations in the Northeast Atlantic

Large-scale, climate-induced synchrony in the productivity of fish populations is becoming more pronounced in the world's oceans. As synchrony increases, a population's 'portfolio' of responses can be diminished, in turn reducing its resilience to strong perturbation. Here we argue that the costs and benefits of trait synchronization, such as the expression of growth rate are context dependent. Synchrony among individuals could actually be beneficial for populations if growth is optimized during favourable conditions and then declines under poor conditions when a broader portfolio of responses is needed. Importantly, growth synchrony among individuals within populations has seldom been measured, despite well-documented evidence of synchrony across populations. Here, we used century-scale time series of annual otolith growth to test for changes in growth synchronization among individuals within multiple populations of a marine keystone species (Atlantic cod, Gadus morhua). On the basis of 74,662 annual growth increments recorded in 13,749 otoliths, we detected a rising conformity in long-term growth rates within northeast Atlantic cod populations in response to both favorable growth conditions and a large-scale, multidecadal mode of climate variability similar to the East Atlantic Pattern. The within-population synchrony was distinct from the across-population synchrony commonly reported for large-scale environmental drivers. Climate-linked, among-individual growth synchrony was also identified in other Northeast Atlantic pelagic, deep-sea and bivalve species. We hypothesize that growth synchrony buffers marine populations to changing climate and growth conditions through its effect on the phenotypic expression of growth diversity, and thus provides an unexpected, but pervasive and stabilizing impact on marine population productivity.Funding provided by: Icelandic Centre for ResearchCrossref Funder Registry ID: http://dx.doi.org/10.13039/501100001840Award Number: 173906-051Growth chronologies were based on cod sampled at annual intervals over periods of up to 94 years from five major cod populations in the Northeast Atlantic (Table S1). For the migratory populations of Norway and Iceland, samples were collected from the main spawning grounds during the spawning season (Norway: the Lofoten archipelago, January - early May; southwestern Iceland: March – May). The Faroe cod population was sampled on the Faroe plateau spawning grounds during the spawning season (February – April) at bottom depths shallower than 150 m. The Godthaabsfjord cod population on the west coast of Greenland (64°N, 51°W, NAFO Division 1D) was sampled mainly (88%) between April and September, with small numbers caught during the reminder of the year. Cod from the inshore area around Sisimiut, West Greenland (66°45'N, 53°30'W, NAFO Division 1B) were primarily caught during June to August (70%), whereas the rest were caught during April, May, September and October. Most samples were collected with research or commercial bottom trawls, supplemented by commercial longlines, jigs, and pound nets. Otoliths from the above samples were subsequently retrieved from otolith archives at the Faroese Marine Research Institute (Faroe Islands), Greenland Institute for Natural Resources (Greenland), Marine and Freshwater Research Institute (Iceland), and Institute of Marine Research (Norway). Due to a probable size-selectivity bias, otoliths from fish caught using gillnets were excluded from the Icelandic and Norwegian selection (Smoliński et al. 2020a, Denechaud et al. 2020). In order to robustly estimate growth variation across growth years and annual fish cohorts, large sample sizes from multiple overlapping cohorts are required (Morrongiello et al. 2012, Smoliński et al. 2020b). Wherever possible, samples for the Icelandic and North East Arctic (NEA) cod populations consisted of at least 50 otoliths per year from mature fish (age 8 or older), although the sampling target was 30 otoliths per year for the Faroese (ages 5-6), Godthaabsfjord (ages 5-6), and Sisimiut (ages 4-10) populations. The accuracy of the age determinations was high (Smoliński et al. 2020a). Otolith growth chronologies Otolith growth chronologies were constructed from series of annual increment widths measured from digitized images of sectioned otoliths. Since the date and age at capture (corresponding to the otolith margin) was known, each increment could be assigned a year and age of formation. Norwegian, Icelandic, and Faroese (1980-1990 only) otoliths were embedded in epoxy and sectioned transversely through the core (Smoliński et al. 2020a, Denechaud et al. 2020). The Godthaabsfjord, Sisimiut, and post-1990 Faroese otoliths were sectioned without embedding and subsequently heat-treated to increase the contrast between opaque and translucent zones (Christiensen 1964). All images were captured under reflected light using high-resolution image analysis systems. Increment widths (μm) were measured along an axis drawn from the otolith core to the distal edge, thus intersecting the maximum number of annual increments at a perpendicular angle (Figure 1A). In Norway and Iceland, because the position of the core was not always clear, the longest diameter of the first increment was marked and the intersection point between the diameter and the measuring axis was used as the origin for the measurements (Denechaud et al. 2020). Because of this difference, the width of the innermost increment was not included in the analysis of the Icelandic samples. Annual increments were measured as the width of a translucent and opaque zone pair: from the medial edge (distal edge in the case of Iceland and NEA) of the opaque zone to the end of the subsequent translucent zone, and were measured across the entire growth sequence of each otolith. Here, the data analysis was restricted to increments formed at ages 1 to 6, since these ages were represented in all populations and most fish were still sexually immature such that inter-annual growth fluctuations more likely reflected environmental conditions and/ or population abundance rather than the energetic costs of reproduction