Climate change and fishing: a century of shifting distribution in North Sea cod

Globally, spatial distributions of fish stocks are shifting but although the role of climate change in range shifts is increasingly appreciated, little remains known of the likely additional impact that high levels of fishing pressure might have on distribution. For North Sea cod, we show for the first time and in great spatial detail how the stock has shifted its distribution over the past 100 years. We digitized extensive historical fisheries data from paper charts in UK government archives and combined these with contemporary data to a time‐series spanning 1913–2012 (excluding both World Wars). New analysis of old data revealed that the current distribution pattern of cod – mostly in the deeper, northern‐ and north‐easternmost parts of the North Sea – is almost opposite to that during most of the Twentieth Century – mainly concentrated in the west, off England and Scotland. Statistical analysis revealed that the deepening, northward shift is likely attributable to warming; however, the eastward shift is best explained by fishing pressure, suggestive of significant depletion of the stock from its previous stronghold, off the coasts of England and Scotland. These spatial patterns were confirmed for the most recent 3½ decades by data from fisheries‐independent surveys, which go back to the 1970s. Our results demonstrate the fundamental importance of both climate change and fishing pressure for our understanding of changing distributions of commercially exploited fish.     

Behavioral responses of Atlantic cod to sea temperature changes

Understanding responses of marine species to temperature variability is essential to predict impacts of future climate change in the oceans. Most ectotherms are expected to adjust their behavior to avoid extreme temperatures and minimize acute changes in body temperature. However, measuring such behavioral plasticity in the wild is challenging. Combining 4 years of telemetry‐derived behavioral data on juvenile and adult (30–80 cm) Atlantic cod (Gadus morhua), and in situ ocean temperature measurements, we found a significant effect of sea temperature on cod depth use and activity level in coastal Skagerrak. During summer, cod were found in deeper waters when sea surface temperature increased. Further, this effect of temperature was stronger on larger cod. Diel vertical migration, which consists in a nighttime rise to shallow feeding habitats, was stronger among smaller cod. As surface temperature increased beyond ~15°C, their vertical migration was limited to deeper waters. In addition to larger diel vertical migrations, smaller cod were more active and travelled larger distances compared to larger specimens. Cold temperatures during winter tended, however, to reduce the magnitude of diel vertical migrations, as well as the activity level and distance moved by those smaller individuals. Our findings suggest that future and ongoing rises in sea surface temperature may increasingly deprive cod in this region from shallow feeding areas during summer, which may be detrimental for local populations of the species.     

Mechanistic insights into the effects of climate change on larval cod

Understanding the biophysical mechanisms that shape variability in fisheries recruitment is critical for estimating the effects of climate change on fisheries. In this study, we used an Earth System Model (ESM) and a mechanistic individual‐based model (IBM) for larval fish to analyze how climate change may impact the growth and survival of larval cod in the North Atlantic. We focused our analysis on five regions that span the current geographical range of cod and are known to contain important spawning populations. Under the SRES A2 (high emissions) scenario, the ESM‐projected surface ocean temperatures are expected to increase by >1 °C for 3 of the 5 regions, and stratification is expected to increase at all sites between 1950–1999 and 2050–2099. This enhanced stratification is projected to decrease large (>5 μm ESD) phytoplankton productivity and mesozooplankton biomass at all 5 sites. Higher temperatures are projected to increase larval metabolic costs, which combined with decreased food resources will reduce larval weight, increase the probability of larvae dying from starvation and increase larval exposure to visual and invertebrate predators at most sites. If current concentrations of piscivore and invertebrate predators are maintained, larval survival is projected to decrease at all five sites by 2050–2099. In contrast to past observed responses to climate variability in which warm anomalies led to better recruitment in cold‐water stocks, our simulations indicated that reduced prey availability under climate change may cause a reduction in larval survival despite higher temperatures in these regions. In the lower prey environment projected under climate change, higher metabolic costs due to higher temperatures outweigh the advantages of higher growth potential, leading to negative effects on northern cod stocks. Our results provide an important first large‐scale assessment of the impacts of climate change on larval cod in the North Atlantic.     

Genomic divergence between the migratory and stationary ecotypes of Atlantic cod

Atlantic cod displays a range of phenotypic and genotypic variations, which includes the differentiation into coastal stationary and offshore migratory types of cod that co‐occur in several parts of its distribution range and are often sympatric on the spawning grounds. Differentiation of these ecotypes may involve both historical separation and adaptation to ecologically distinct environments, the genetic basis of which is now beginning to be unravelled. Genomic analyses based on recent sequencing advances are able to document genomic divergence in more detail and may facilitate the exploration of causes and consequences of genome‐wide patterns. We examined genomic divergence between the stationary and migratory types of cod in the Northeast Atlantic, using next‐generation sequencing of pooled DNA from each of two population samples. Sequence data was mapped to the published cod genome sequence, arranged in more than 6000 scaffolds (611 Mb). We identified 25 divergent scaffolds (26 Mb) with a higher than average gene density, against a backdrop of overall moderate genomic differentiation. Previous findings of localized genomic divergence in three linkage groups were confirmed, including a large (15 Mb) genomic region, which seems to be uniquely involved in the divergence of migratory and stationary cod. The results of the pooled sequencing approach support and extend recent findings based on single‐nucleotide polymorphism markers and suggest a high degree of reproductive isolation between stationary and migratory cod in the North‐east Atlantic.     

Long‐term dynamics in microbial eukaryotes communities: a palaeolimnological view based on sedimentary DNA

Assessing the extent to which changes in lacustrine biodiversity are affected by anthropogenic or climatic forces requires extensive palaeolimnological data. We used high‐throughput sequencing to generate time‐series data encompassing over 2200 years of microbial eukaryotes (protists and Fungi) diversity changes from the sedimentary DNA record of two lakes (Lake Bourget in French Alps and Lake Igaliku in Greenland). From 176 samples, we sequenced a large diversity of microbial eukaryotes, with a total 16 386 operational taxonomic units distributed within 50 phylogenetic groups. Thus, microbial groups, such as Chlorophyta, Dinophyceae, Haptophyceae and Ciliophora, that were not previously considered in lacustrine sediment record analyses appeared to be potential biological markers of trophic status changes. Our data suggest that shifts in relative abundance of extant species, including shifts between rare and abundant taxa, drive ecosystem responses to local and global environmental changes. Community structure shift events were concomitant with major climate variations (more particularly in Lake Igaliku). However, this study shows that the impacts of climatic fluctuations may be overpassed by the high‐magnitude eutrophication impacts, as observed in the eutrophicated Lake Bourget. Overall, our data show that DNA preserved in sediment constitutes a precious archive of information on past biodiversity changes.     

Evaluating within‐population variability in behavior and demography for the adaptive potential of a dispersal‐limited species to climate change

Multiple pathways exist for species to respond to changing climates. However, responses of dispersal‐limited species will be more strongly tied to ability to adapt within existing populations as rates of environmental change will likely exceed movement rates. Here, we assess adaptive capacity in Plethodon cinereus, a dispersal‐limited woodland salamander. We quantify plasticity in behavior and variation in demography to observed variation in environmental variables over a 5‐year period. We found strong evidence that temperature and rainfall influence P. cinereus surface presence, indicating changes in climate are likely to affect seasonal activity patterns. We also found that warmer summer temperatures reduced individual growth rates into the autumn, which is likely to have negative demographic consequences. Reduced growth rates may delay reproductive maturity and lead to reductions in size‐specific fecundity, potentially reducing population‐level persistence. To better understand within‐population variability in responses, we examined differences between two common color morphs. Previous evidence suggests that the color polymorphism may be linked to physiological differences in heat and moisture tolerance. We found only moderate support for morph‐specific differences for the relationship between individual growth and temperature. Measuring environmental sensitivity to climatic variability is the first step in predicting species' responses to climate change. Our results suggest phenological shifts and changes in growth rates are likely responses under scenarios where further warming occurs, and we discuss possible adaptive strategies for resulting selective pressures.     

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.     

Microevolution in time and space: SNP analysis of historical DNA reveals dynamic signatures of selection in Atlantic cod

Little is known about how quickly natural populations adapt to changes in their environment and how temporal and spatial variation in selection pressures interact to shape patterns of genetic diversity. We here address these issues with a series of genome scans in four overfished populations of Atlantic cod (Gadus morhua) studied over an 80‐year period. Screening of >1000 gene‐associated single‐nucleotide polymorphisms (SNPs) identified 77 loci that showed highly elevated levels of differentiation, likely as an effect of directional selection, in either time, space or both. Exploratory analysis suggested that temporal allele frequency shifts at certain loci may correlate with local temperature variation and with life history changes suggested to be fisheries induced. Interestingly, however, largely nonoverlapping sets of loci were temporal outliers in the different populations and outliers from the 1928 to 1960 period showed almost complete stability during later decades. The contrasting microevolutionary trajectories among populations resulted in sequential shifts in spatial outliers, with no locus maintaining elevated spatial differentiation throughout the study period. Simulations of migration coupled with observations of temporally stable spatial structure at neutral loci suggest that population replacement or gene flow alone could not explain all the observed allele frequency variation. Thus, the genetic changes are likely to at least partly be driven by highly dynamic temporally and spatially varying selection. These findings have important implications for our understanding of local adaptation and evolutionary potential in high gene flow organisms and underscore the need to carefully consider all dimensions of biocomplexity for evolutionarily sustainable management.     

Climatic and biotic extreme events moderate long‐term responses of above‐ and belowground sub‐Arctic heathland communities to climate change

Climate change impacts are not uniform across the Arctic region because interacting factors causes large variations in local ecosystem change. Extreme climatic events and population cycles of herbivores occur simultaneously against a background of gradual climate warming trends and can redirect ecosystem change along routes that are difficult to predict. Here, we present the results from sub‐Arctic heath vegetation and its belowground micro‐arthropod community in response to the two main drivers of vegetation damage in this region: extreme winter warming events and subsequent outbreaks of the defoliating autumnal moth caterpillar (Epirrita autumnata). Evergreen dwarf shrub biomass decreased (30%) following extreme winter warming events and again by moth caterpillar grazing. Deciduous shrubs that were previously exposed to an extreme winter warming event were not affected by the moth caterpillar grazing, while those that were not exposed to warming events (control plots) showed reduced (23%) biomass from grazing. Cryptogam cover increased irrespective of grazing or winter warming events. Micro‐arthropods declined (46%) following winter warming but did not respond to changes in plant community. Extreme winter warming and caterpillar grazing suppressed the CO₂ fluxes of the ecosystem. Evergreen dwarf shrubs are disadvantaged in a future sub‐Arctic with more stochastic climatic and biotic events. Given that summer warming may further benefit deciduous over evergreen shrubs, event and trend climate change may both act against evergreen shrubs and the ecosystem functions they provide. This is of particular concern given that Arctic heath vegetation is typically dominated by evergreen shrubs. Other components of the vegetation showed variable responses to abiotic and biotic events, and their interaction indicates that sub‐Arctic vegetation response to multiple pressures is not easy to predict from single‐factor responses. Therefore, while biotic and climatic events may have clear impacts, more work is needed to understand their net effect on Arctic ecosystems.     

Contrasting Demographic Structure of Short‐ and Long‐lived Pioneer Tree Species on Amazonian Forest Edges

Although tropical forests have been rapidly converted into human‐modified landscapes, tree species response to forest edges remains poorly examined. In this study, we addressed four pioneer tree species to document demographic shifts experienced by this key ecological group and make inferences about pioneer response to forest edges. All individuals with dbh ≥ 1 cm of two short‐lived (Bellucia grossularioides and Cecropia sciadophylla) and two long‐lived species (Goupia glabra and Laetia procera) were sampled in 20 1‐ha forest edge plots and 20 1‐ha forest interior plots in Oiapoque and Manaus, Northeast and Central Amazon, respectively. As expected, pioneer stem density with dbh ≥ 1 cm increased by around 10–17‐fold along forest edges regardless of species, lifespan, and study site. Edge populations of long‐lived pioneers presented 84–94 percent of their individuals in sapling/subadult size classes, whereas edge populations of short‐lived pioneers showed 56–97 percent of their individuals in adult size classes. These demographic biases were associated with negative and positive net adult recruitment of long‐ and short‐lived pioneers, respectively. Our population‐level analyses support three general statements: (1) native pioneer tree species proliferate along forest edges (i.e., increased density), at least in terms of non‐reproductive individuals; (2) pioneer response to edge establishment is not homogeneous as species differ in terms of demographic structure and net adult recruitment; and (3) some pioneer species, particularly long‐lived ones, may experience population decline due to adult sensitivity to edge‐affected habitats.     

Genomic analyses of a “living fossil”: The endangered dove‐tree

Davidia involucrata Baill, also known as the dove‐tree, is a living fossil and an endangered species currently restricted to the mountains of southwestern and central China. It has a beautiful and innovative trait of high horticultural value: two white bracts covering the flower caputila. Here, we report on the chromosome‐scale genome of this species using single‐molecule real‐time long reads and chromosome conformation capture (Hi‐C) techniques. This species has a larger genome size of 1,169 Mb and contains relatively more genes (42,554) than the closely related species Camptotheca acuminata (397 Mb and 31,825 genes). Both species shared one recent whole genome duplication before their divergence. The expansion of the repetitive elements after their divergence contributed greatly to the increase in the genome size of the dove‐tree. Photosynthesis‐related genes were almost absent or showed reduced expression in the bracts of the dove‐tree, while defence‐ and chemical‐related genes increased greatly, highlighting the important roles of the bracts in protecting flowers and attracting pollinators. The effective population size of the dove‐tree continuously decreased during the climate changes of the Quaternary. Such climate sensitivity should be fully considered in conservation efforts for this relict endangered species in the context of continuous climate warming in the future.     

Long‐term stasis and short‐term divergence in the phenotypes of microsnails on oceanic islands

Phenotypic divergence is often unrelated to genotypic divergence. An extreme example is rapid phenotypic differentiation despite genetic similarity. Another extreme is morphological stasis despite substantial genetic divergence. These opposite patterns have been viewed as reflecting opposite properties of the lineages. In this study, phenotypic radiation accompanied by both rapid divergence and long‐term conservatism is documented in the inferred molecular phylogeny of the micro land snails Cavernacmella (Assimineidae) on the Ogasawara Islands. The populations of Cavernacmella on the Sekimon limestone outcrop of Hahajima Island showed marked divergence in shell morphology. Within this area, one lineage diversified into types with elongated turret shells, conical shells and flat disc‐like shells without substantial genetic differentiation. Additionally, a co‐occurring species with these types developed a much larger shell size. Moreover, a lineage adapted to live inside caves in this area. In contrast, populations in the other areas exhibited no morphological differences despite high genetic divergence among populations. Accordingly, the phenotypic evolution of Cavernacmella in Ogasawara is characterized by a pattern of long‐term stasis and periodic bursts of change. This pattern suggests that even lineages with phenotypic conservatism could shift to an alternative state allowing rapid phenotypic divergence.     

Long‐term monitoring of tropical alpine habitat change,Andean anurans,and chytrid fungus in the Cordillera Vilcanota,Peru: Results from a decade of study

The Cordillera Vilcanota in southern Peru is the second largest glacierized range in the tropics and home to one of the largest high‐alpine lakes, Sibinacocha (4,860 m). Here, Telmatobius marmoratus (marbled water frog), Rhinella spinulosa (Andean toad), and Pleurodema marmoratum (marbled four‐eyed frog) have expanded their range vertically within the past century to inhabit newly formed ponds created by ongoing deglaciation. These anuran populations, geographically among the highest (5,200–5,400 m) recorded globally, are being impacted by the chytrid fungus Batrachochytrium dendrobatidis (Bd), and the disease it causes, chytridiomycosis. In this study, we report results from over a decade of monitoring these three anuran species, their habitat, and Bd infection status. Our observations reveal dynamic changes in habitat including ongoing rapid deglaciation (18.4 m/year widening of a corridor between retreating glaciers from 2005 to 2015), new pond formation, changes in vegetation in amphibian habitat, and widespread occurrence of Bd in amphibians in seven sites. Three of these sites have tested positive for Bd over a 9‐ to 12‐year period. In addition, we observed a widespread reduction in T. marmoratus encounters in the Vilcanota in 2008, 2009, and 2012, while encounters increased in 2013 and 2015. Despite the rapid and dynamic changes in habitat under a warming climate, continued presence of Bd in the environment for over a decade, and a reduction in one of three anuran species, we document that these anurans continue to breed and survive in this high Andean environment. High variability in anuran encounters across sites and plasticity in these populations across habitats, sites, and years are all factors that could favor repopulation postdecline. Preserving the connectivity of wetlands in the Cordillera Vilcanota is therefore essential in ensuring that anurans continue to breed and adapt as climate change continues to reshape the environment.