Growth portfolios buffer climate-linked environmental change in marine systems.

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. Contrary to prevailing views, synchrony among individuals could actually be beneficial for populations if growth synchrony increases during favorable conditions, and then declines under poor conditions when a broader portfolio of responses could be useful. 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 five 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 in good years and growth asynchrony in poorer years reflects adaptive trait optimization and bet hedging, respectively, that could confer an unexpected, but pervasive and stabilizing, impact on marine population productivity in response to large-scale environmental change.

Otolith "spawning zones" across multiple Atlantic cod populations: Do they accurately record maturity and spawning?

Specific changes identified in the otolith macrostructure of Northeast Arctic cod as "spawning zones" are presumed to represent spawning events, but recent experimental studies have challenged this relationship. Because these zones are not routinely recorded outside of Norway, otoliths from multiple Atlantic cod populations with different life history and environmental traits were first examined to see if spawning zones could be identified as a general characteristic of cod. Then, a large archival collection of cod otoliths was used to investigate temporal changes in the occurrence of spawning zones and test for correlations between maturity at age derived from otolith spawning zones and gonad maturity stages. This study shows that spawning zones likely are a universal trait of Atlantic cod and not limited to certain environments or migratory behaviors as previously proposed. Maturity at age derived from spawning zone data showed trends consistent with those from gonad examinations. However, spawning zones appear to form with a one- or two-year lag with sexual maturity, which is suspected to reflect a stabilizing of energy partitioning after the first spawning events. Our results illustrate the potential for use of spawning zones, for example in species or populations with limited available maturity data, and highlights the need for addressing the physiological processes behind their formation.

Differences in metabolic rate between two Atlantic cod (Gadus morhua) populations estimated with carbon isotopic composition in otoliths.

The isotopic composition of inorganic carbon in otoliths (δ13Coto) can be a useful tracer of metabolic rates and a method to study ecophysiology in wild fish. We evaluated environmental and physiological sources of δ13Coto variation in Icelandic and Northeast Arctic (NEA) cod (Gadus morhua) over the years 1914-2013. Individual annual growth increments of otoliths formed at age 3 and 8 were micromilled and measured by isotope-ratio mass spectrometry. Simultaneously, all annual increment widths of the otoliths were measured providing a proxy of fish somatic growth. We hypothesized that changes in the physiological state of the organism, reflected by the isotopic composition of otoliths, can affect the growth rate. Using univariate and multivariate mixed-effects models we estimated conditional correlations between carbon isotopic composition and growth of fish at different levels (within individuals, between individuals, and between years), controlling for intrinsic and extrinsic effects on both otolith measurements. δ13Coto was correlated with growth within individuals and between years, which was attributed to the intrinsic effects (fish age or total length). There was no significant correlation between δ13Coto and growth between individuals, which suggests that caution is needed when interpreting δ13Coto signals. We found a significant decrease in δ13Coto through the century which was explained by the oceanic Suess effect-admixture of isotopically light carbon from fossil fuel. We calculated the proportion of the respired carbon in otolith carbonate (Cresp) using carbon isotopic composition in diet and dissolved inorganic carbon of the seawater. This approach allowed us to correct the values for each stock in relation to these two environmental baselines. Cresp was on average 0.275 and 0.295 in Icelandic and NEA stock, respectively. Our results provide an insight into the physiological basis for differences in growth characteristics between these two cod stocks, and how that may vary over time.

A century of fish growth in relation to climate change, population dynamics and exploitation.

Marine ecosystems, particularly in high-latitude regions such as the Arctic, have been significantly affected by human activities and contributions to climate change. Evaluating how fish populations responded to past changes in their environment is helpful for evaluating their future patterns, but is often hindered by the lack of long-term biological data available. Using otolith increments of Northeast Arctic cod (Gadus morhua) as a proxy for individual growth, we developed a century-scale biochronology (1924-2014) based on the measurements of 3,894 fish, which revealed significant variations in cod growth over the last 91 years. We combined mixed-effect modeling and path analysis to relate these growth variations to selected climate, population and fishing-related factors. Cod growth was negatively related to cod population size and positively related to capelin population size, one of the most important prey items. This suggests that density-dependent effects are the main source of growth variability due to competition for resources and cannibalism. Growth was also positively correlated with warming sea temperatures but negatively correlated with the Atlantic Multidecadal Oscillation, suggesting contrasting effects of climate warming at different spatial scales. Fishing pressure had a significant but weak negative direct impact on growth. Additionally, path analysis revealed that the selected growth factors were interrelated. Capelin biomass was positively related to sea temperature and negatively influenced by herring biomass, while cod biomass was mainly driven by fishing mortality. Together, these results give a better understanding of how multiple interacting factors have shaped cod growth throughout a century, both directly and indirectly.