Persistence of fish populations to longer, more intense, and more frequent mass mortality events.

Over the last decades, mass mortality events have become increasingly common across taxa with sometimes devastating effects on population biomass. In the aquatic environment, fish are sensitive to mass mortality events, particularly at the early life stages that are crucial for population dynamics. However, it has recently been shown for fish, that a single mass mortality event in early life typically does not lead to population collapse. Moreover, the frequency and intensity of extreme events that can cause mass mortality, such as marine heatwaves, are increasing. Here, we show that increasing frequency and intensity of mass mortality events may lead to population collapse. Since the drivers of mass mortality events are diverse, and often linked to climate change, it is challenging to predict the frequency and severity of future mass mortality events. As an alternative, we quantify the probability of population collapse depending on the frequency and intensity as well as the duration of mass mortality events. Based on 39 fish species, we show that the probability of collapse typically increases with increasing frequency, intensity, and duration of the mortality events. In addition, we show that the collapse depends on key traits such as natural mortality, recruitment variation, and density dependence. The presented framework provides quantitative estimates of the sensitivity of fish species to these increasingly common extreme events, which paves the way for potential mitigation actions to alleviate adverse impacts on harvested fish populations across the globe.

Attuning to a changing ocean.

The ocean is a lifeline for human existence, but current practices risk severely undermining ocean sustainability. Present and future social-ecological challenges necessitate the maintenance and development of knowledge and action by stimulating collaboration among scientists and between science, policy, and practice. Here we explore not only how such collaborations have developed in the Nordic countries and adjacent seas but also how knowledge from these regions contributes to an understanding of how to obtain a sustainable ocean. Our collective experience may be summarized in three points: 1) In the absence of long-term observations, decision-making is subject to high risk arising from natural variability; 2) in the absence of established scientific organizations, advice to stakeholders often relies on a few advisors, making them prone to biased perceptions; and 3) in the absence of trust between policy makers and the science community, attuning to a changing ocean will be subject to arbitrary decision-making with unforeseen and negative ramifications. Underpinning these observations, we show that collaboration across scientific disciplines and stakeholders and between nations is a necessary condition for appropriate actions.

Empirical evidence of nonlinearity in bottom up effect in a marine predator-prey system.

The strength of species interactions may have profound effects on population dynamics. Empirical estimates of interaction strength are often based on the assumption that the interaction strengths are constant. Barents Sea (BS) cod and capelin are two fish populations for which such an interaction has been acknowledged and used, under the assumption of constant interaction strength, when studying their population dynamics. However, species interactions can often be nonlinear in marine ecosystems and might profoundly change our understanding of food chains. Analysing long-term time series data comprising a survey over 37 years in the Arcto-boreal BS, using a state-space modelling framework, we demonstrate that the effect of capelin on cod is not linear but shifts depending on capelin abundance: while capelin is beneficial for cod populations at high abundance; below the threshold, it becomes less important for cod. Our analysis therefore shows the importance of investigating nonlinearity in species interactions and may contribute to an improved understanding on species assemblages.

Nonlinearity in interspecific interactions in response to climate change: Cod and haddock as an example.

Climate change has profound ecological effects, yet our understanding of how trophic interactions among species are affected by climate change is still patchy. The sympatric Atlantic haddock and cod are co-occurring across the North Atlantic. They compete for food at younger stages and thereafter the former is preyed by the latter. Climate change might affect the interaction and coexistence of these two species. Particularly, the increase in sea temperature (ST) has been shown to affect distribution, population growth and trophic interactions in marine systems. We used 33-year long time series of haddock and cod abundances estimates from two data sources (acoustic and trawl survey) to analyse the dynamic effect of climate on the coexistence of these two sympatric species in the Arcto-Boreal Barents Sea. Using a Bayesian state-space threshold model, we demonstrated that long-term climate variation, as expressed by changes of ST, affected species demography through different influences on density-independent processes. The interaction between cod and haddock has shifted in the last two decades due to an increase in ST, altering the equilibrium abundances and the dynamics of the system. During warm years (ST over ca. 4°C), the increase in the cod abundance negatively affected haddock abundance while it did not during cold years. This change in interactions therefore changed the equilibrium population size with a higher population size during warm years. Our analyses show that long-term climate change in the Arcto-Boreal system can generate differences in the equilibrium conditions of species assemblages.

Catastrophic dynamics limit Atlantic cod recovery.

Collapses and regime changes are pervasive in complex systems (such as marine ecosystems) governed by multiple stressors. The demise of Atlantic cod ( Gadus morhua) stocks constitutes a text book example of the consequences of overexploiting marine living resources, yet the drivers of these nearly synchronous collapses are still debated. Moreover, it is still unclear why rebuilding of collapsed fish stocks such as cod is often slow or absent. Here, we apply the stochastic cusp model, based on catastrophe theory, and show that collapse and recovery of cod stocks are potentially driven by the specific interaction between exploitation pressure and environmental drivers. Our statistical modelling study demonstrates that for most of the cod stocks, ocean warming could induce a nonlinear discontinuous relationship between fishing pressure and stock size, which would explain hysteresis in their response to reduced exploitation pressure. Our study suggests further that a continuing increase in ocean temperatures will probably limit productivity and hence future fishing opportunities for most cod stocks of the Atlantic Ocean. Moreover, our study contributes to the ongoing discussion on the importance of climate and fishing effects on commercially exploited fish stocks, highlighting the importance of considering discontinuous dynamics in holistic ecosystem-based management approaches, particularly under climate change.

Ticket to spawn: Combining economic and genetic data to evaluate the effect of climate and demographic structure on spawning distribution in Atlantic cod.

Climate warming and harvesting affect the dynamics of species across the globe through a multitude of mechanisms, including distribution changes. In fish, migrations to and distribution on spawning grounds are likely influenced by both climate warming and harvesting. The Northeast Arctic (NEA) cod (Gadus morhua) performs seasonal migrations from its feeding grounds in the Barents Sea to spawning grounds along the Norwegian coast. The distribution of cod between the spawning grounds has historically changed at decadal scales, mainly due to variable use of the northern and southern margins of the spawning area. Based on historical landing records, two major hypotheses have been put forward to explain these changes: climate and harvesting. Climate could affect the distribution through, for example, spatial habitat shifts. Harvesting could affect the distribution through impacting the demographic structure. If demographic structure is important, theory predicts increasing spawner size with migration distance. Here, we evaluate these hypotheses with modern data from a period (2000-2016) of increasing temperature and recovering stock structure. We first analyze economic data from the Norwegian fisheries to investigate geographical differences in size of spawning fish among spawning grounds, as well as interannual differences in mean latitude of spawning in relation to changes in temperature and demographic parameters. Second, we analyze genetically determined fish sampled at the spawning grounds to unambiguously separate between migratory NEA cod and potentially smaller sized coastal cod of local origin. Our results indicate smaller spawners farther away from the feeding grounds, hence not supporting the hypothesis that harvesting is a main driver for the contemporary spawning ground distribution. We find a positive correlation between annual mean spawning latitude and temperature. In conclusion, based on contemporary data, there is more support for climate compared to harvesting in shaping spawning ground distribution in this major fish stock in the North Atlantic Ocean.

Cascading effects of mass mortality events in Arctic marine communities.

Mass mortality events caused by pulse anthropogenic or environmental perturbations (e.g., extreme weather, toxic spills or epizootics) severely reduce the abundance of a population in a short time. The frequency and impact of these events are likely to increase across the globe. Studies on how such events may affect ecological communities of interacting species are scarce. By combining a multispecies Gompertz model with a Bayesian state-space framework, we quantify community-level effects of a mass mortality event in a single species. We present a case study on a community of fish and zooplankton in the Barents Sea to illustrate how a mass mortality event of different intensities affecting the lower trophic level (krill) may propagate to higher trophic levels (capelin and cod). This approach is especially valuable for assessing community-level effects of potential anthropogenic-driven mass mortality events, owing to the ability to account for uncertainty in the assessed impact due to uncertainty about the ecological dynamics. We hence quantify how the assessed impact of a mass mortality event depends on the degree of precaution considered. We suggest that this approach can be useful for assessing the possible detrimental outcomes of toxic spills, for example oil spills, in relatively simple communities such as often found in the Arctic, a region under increasing influence of human activities due to increased land and sea use.

Reliability of flipper-banded penguins as indicators of climate change.

In 2007, the Intergovernmental Panel on Climate Change highlighted an urgent need to assess the responses of marine ecosystems to climate change. Because they lie in a high-latitude region, the Southern Ocean ecosystems are expected to be strongly affected by global warming. Using top predators of this highly productive ocean (such as penguins) as integrative indicators may help us assess the impacts of climate change on marine ecosystems. Yet most available information on penguin population dynamics is based on the controversial use of flipper banding. Although some reports have found the effects of flipper bands to be deleterious, some short-term (one-year) studies have concluded otherwise, resulting in the continuation of extensive banding schemes and the use of data sets thus collected to predict climate impact on natural populations. Here we show that banding of free-ranging king penguins (Aptenodytes patagonicus) impairs both survival and reproduction, ultimately affecting population growth rate. Over the course of a 10-year longitudinal study, banded birds produced 41% [corrected] fewer chicks and had a survival rate 16 percentage points [corrected] lower than non-banded birds, demonstrating a massive long-term impact of banding and thus refuting the assumption that birds will ultimately adapt to being banded. Indeed, banded birds still arrived later for breeding at the study site and had longer foraging trips even after 10 years. One of our major findings is that responses of flipper-banded penguins to climate variability (that is, changes in sea surface temperature and in the Southern Oscillation index) differ from those of non-banded birds. We show that only long-term investigations may allow an evaluation of the impact of flipper bands and that every major life-history trait can be affected, calling into question the banding schemes still going on. In addition, our understanding of the effects of climate change on marine ecosystems based on flipper-band data should be reconsidered.

Testing for effects of climate change on competitive relationships and coexistence between two bird species.

Climate change is expected to have profound ecological effects, yet shifts in competitive abilities among species are rarely studied in this context. Blue tits (Cyanistes caeruleus) and great tits (Parus major) compete for food and roosting sites, yet coexist across much of their range. Climate change might thus change the competitive relationships and coexistence between these two species. Analysing four of the highest-quality, long-term datasets available on these species across Europe, we extend the textbook example of coexistence between competing species to include the dynamic effects of long-term climate variation. Using threshold time-series statistical modelling, we demonstrate that long-term climate variation affects species demography through different influences on density-dependent and density-independent processes. The competitive interaction between blue tits and great tits has shifted in one of the studied sites, creating conditions that alter the relative equilibrium densities between the two species, potentially disrupting long-term coexistence. Our analyses show that long-term climate change can, but does not always, generate local differences in the equilibrium conditions of spatially structured species assemblages. We demonstrate how long-term data can be used to better understand whether (and how), for instance, climate change might change the relationships between coexisting species. However, the studied populations are rather robust against competitive exclusion.

Large biomass reduction effect on the relative role of climate, fishing, and recruitment on fish population dynamics.

Many species around the world have collapsed, yet only some have recovered. A key question is what happens to populations post collapse. Traditionally, marine fish collapses are linked to overfishing, poor climate, and recruitment. We test whether the effect on biomass change from these drivers remains the same after a collapse. We used a regression model to analyse the effect of harvesting, recruitment, and climate variability on biomass change before and after a collapse across 54 marine fish populations around the world. The most salient result was the change in fishing effect that became weaker after a collapse. The change in sea temperature and recruitment effects were more variable across systems. The strongest changes were in the pelagic habitats. The resultant change in the sensitivity to external drivers indicates that whilst biomass may be rebuilt, the responses to variables known to affect stocks may have changed after a collapse. Our results show that a general model applied to many stocks provides useful insights, but that not all stocks respond similarly to a collapse calling for stock-specific models. Stocks respond to environmental drivers differently after a collapse, so caution is needed when using pre-collapse knowledge to advise on population dynamics and management.

Predatory walls may impair climate warming-associated population expansion.

Climate change has a profound impact on species distribution and abundance globally, as well as local diversity, which affects ecosystem functioning. In particular, changes in population distribution and abundance may lead to changes in trophic interactions. Although species can often shift their spatial distribution when suitable habitats are available, it has been suggested that predator presence can be a constraint on climate-related distribution shifts. We test this using two well-studied and data-rich marine environments. Focusing on a pair of sympatric fishes, Atlantic haddock Melanogrammus aeglefinus and cod Gadus morhua, we study the effect of the presence and abundance of the latter on the former distribution. We found that the distribution of cod and increased abundance may limit the expansion of haddock to new areas and could consequently buffer ecosystem changes due to climate change. Though marine species may track the rate and direction of climate shifts, our results demonstrate that the presence of predators may limit their expansion to thermally suitable habitats. By integrating climatic and ecological data at scales that can resolve predator-prey relationships, this analysis demonstrates the usefulness of considering trophic interactions to gain a more comprehensive understanding and to mitigate the effects of climate change on species distributions.

Long-term annual and spatial variation of polygyny in the white-throated dipper (Cinclus cinclus).

Mating strategies are key components in the fitness of organisms, and notably in birds the occurrence of monogamy versus polygyny has attracted wide interest. We address this by a very comprehensive dataset (2899 breeding events spanning the years 1978-2019) of the white-throated dipper Cinclus cinclus. Though the mating system of this species has been regarded as generally monogamous, we find that 7% of all breeding events were performed by polygynous males (approximately 15% of all pairs). The fraction of polygyny has been stable over the entire study period irrespective of population size. The assumption that polygyny is most common at low population density was not supported. Surprisingly, there was no difference between polygynous and monogamous males with regard to the quality of the territories they inhabited, ranked according to their overall frequency of use. The most common age group, first-year breeders, dominated among monogamous males, while among polygynous males second-year breeders were most common, followed by third and first-year breeders. The primary females were in general older than females mated to monogamous males, also when controlled for their general frequency in the population. The majority of the two females mated to a polygynous male, bred in the vicinity of each other. The probability for a male to be involved in polygyny more than once, was significantly higher than by chance, suggesting phenotypic quality differences among males.

King penguin population threatened by Southern Ocean warming.

Seabirds are sensitive indicators of changes in marine ecosystems and might integrate and/or amplify the effects of climate forcing on lower levels in food chains. Current knowledge on the impact of climate changes on penguins is primarily based on Antarctic birds identified by using flipper bands. Although flipper bands have helped to answer many questions about penguin biology, they were shown in some penguin species to have a detrimental effect. Here, we present for a Subantarctic species, king penguin (Aptenodytes patagonicus), reliable results on the effect of climate on survival and breeding based on unbanded birds but instead marked by subcutaneous electronic tags. We show that warm events negatively affect both breeding success and adult survival of this seabird. However, the observed effect is complex because it affects penguins at several spatio/temporal levels. Breeding reveals an immediate response to forcing during warm phases of El Niño Southern Oscillation affecting food availability close to the colony. Conversely, adult survival decreases with a remote sea-surface temperature forcing (i.e., a 2-year lag warming taking place at the northern boundary of pack ice, their winter foraging place). We suggest that this time lag may be explained by the delay between the recruitment and abundance of their prey, adjusted to the particular 1-year breeding cycle of the king penguin. The derived population dynamic model suggests a 9% decline in adult survival for a 0.26 degrees C warming. Our findings suggest that king penguin populations are at heavy extinction risk under the current global warming predictions.

Stock collapse and its effect on species interactions: Cod and herring in the Norwegian-Barents Seas system as an example.

Both the Norwegian Spring Spawning herring (Clupea harengus) and the Northeast Arctic (NEA) cod (Gadus morhua) are examples of strong stock reduction and decline of the associated fisheries due to overfishing followed by a recovery. Cod and herring are both part of the Barents Sea ecosystem, which has experienced major warming events in the early (1920-1940) and late 20th century. While the collapse or near collapse of these stocks seems to be linked to an instability created by overfishing and climate, the difference of population dynamics before and after is not fully understood. In particular, it is unclear how the changes in population dynamics before and after the collapses are associated with biotic interactions. The combination of the availability of unique long-term time series for herring and cod makes it a well-suited study system to investigate the effects of collapse. We examine how species interactions may differently affect the herring and cod population dynamic before and after a collapse. Particularly we explore, using a GAM modeling approach, how herring could affect cod and vice versa. We found that the effect of cod biomass on herring that was generally positive (i.e., covariation) but the effect became negative after the collapse (i.e., predation or competition). Likewise a change occurred for the cod, the juvenile herring biomass that had no effect before the collapse had a negative effect after. Our results indicate that the population collapses may alter the inter-specific interactions and response to abiotic environmental changes. While the stocks are at similar abundance levels before and after the collapses, the system is potentially different in its functioning and may require different management action.

Population variability under stressors is dependent on body mass growth and asymptotic body size.

The recruitment and biomass of a fish stock are influenced by their environmental conditions and anthropogenic pressures such as fishing. The variability in the environment often translates into fluctuations in recruitment, which then propagate throughout the stock biomass. In order to manage fish stocks sustainably, it is necessary to understand their dynamics. Here, we systematically explore the dynamics and sensitivity of fish stock recruitment and biomass to environmental noise. Using an age-structured and trait-based model, we explore random noise (white noise) and autocorrelated noise (red noise) in combination with low to high levels of harvesting. We determine the vital rates of stocks covering a wide range of possible body mass (size) growth rates and asymptotic size parameter combinations. Our study indicates that the variability of stock recruitment and biomass are probably correlated with the stock's asymptotic size and growth rate. We find that fast-growing and large-sized fish stocks are likely to be less vulnerable to disturbances than slow-growing and small-sized fish stocks. We show how the natural variability in fish stocks is amplified by fishing, not just for one stock but for a broad range of fish life histories.

Contrasting effects of rising temperatures on trophic interactions in marine ecosystems.

In high-latitude marine environments, primary producers and their consumers show seasonal peaks of abundance in response to annual light cycle, water column stability and nutrient availability. Predatory species have adapted to this pattern by synchronising life-history events such as reproduction with prey availability. However, changing temperatures may pose unprecedented challenges by decoupling the predator-prey interactions. Here we build a predator-prey model accounting for the full life-cycle of fish and zooplankton including their phenology. The model assumes that fish production is bottom-up controlled by zooplankton prey abundance and match or mismatch between predator and prey phenology, and is parameterised based on empirical findings of how climate influences phenology and prey abundance. With this model, we project possible climate-warming effects on match-mismatch dynamics in Arcto-boreal and temperate biomes. We find a strong dependence on synchrony with zooplankton prey in the Arcto-boreal fish population, pointing towards a possible pronounced population decline with warming because of frequent desynchronization with its zooplankton prey. In contrast, the temperate fish population appears better able to track changes in prey timing and hence avoid strong population decline. These results underline that climate change may enhance the risks of predator-prey seasonal asynchrony and fish population declines at higher latitudes.

Northeast Arctic cod population persistence in the Lofoten-Barents Sea system under fishing.

Population growth, and hence the population's persistence, is affected by several factors such as climate, species interaction, and harvesting pressure. Proper resource management requires an understanding of these factors. We apply techniques based upon age-structured population matrices to analyze estimated stock sizes derived from annual bottom trawl sampling in the winter feeding area of northeast Arctic cod (Gadus morhua L.) from 1981 to 2003. We run generalized additive models to explain population growth rate by different explanatory variables. Cod population growth was found to be positively related to the abundance of capelin (Mallotus villosus Miller), negatively related to the number of cannibalistic cod with a two-year lag, and marginally positively related to the winter North Atlantic Oscillation index (NAO). This model remains true independently from the population status (i.e., fished or non-fished). Capelin abundance is the main variable that to some degree can be adjusted in order to maintain the population size at a given level of cod harvesting. Our results point to the importance of managing conjointly cod and capelin stocks.

Body mass and clutch size may modulate prolactin and corticosterone levels in eiders.

Altered body condition, increased incubation costs, and egg loss are important proximate factors modulating bird parental behavior, since they inform the adult about its remaining chances of survival or about the expected current reproductive success. Hormonal changes should reflect internal or external stimuli, since corticosterone levels (inducing nest abandonment) are known to increase while body condition deteriorates, and prolactin levels (stimulating incubation) decrease following egg predation. However, in a capital incubator that based its investment on available body reserves and naturally lost about half of its body mass during incubation, corticosterone should be maintained at a low threshold to avoid protein mobilization for energy supply. This study focused on the regulation of corticosterone and prolactin release in such birds during incubation, when facing egg manipulation (control, reduced, or increased) or a stressful event. Blood samples were taken before and after clutch manipulation and at hatching. Corticosterone levels were determined before and after 30 min of captivity. Female eiders exhibited a high hypothalamic-pituitary-adrenal sensitivity, plasma concentration of corticosterone being increased by four- to fivefold following 30 min of captivity. The adrenocortical response was not modified by body mass loss but was higher in birds for which clutch size was increased. In the same way, females did not show different prolactin levels among the experimental groups. However, when incubation started, prolactin levels were correlated to body mass, suggesting that nest attendance is programmed in relation to the female initial body condition. Moreover, due to an artifactual impact of bird manipulation, increased baseline corticosterone was associated with a prolactin decrease in the control group. These data suggest that, in eiders, body mass and clutch size modification can modulate prolactin and corticosterone levels, which cross-regulate each other in order to finely control incubation behavior.

Timing and abundance as key mechanisms affecting trophic interactions in variable environments.

Climatic changes are disrupting otherwise tight trophic interactions between predator and prey. Most of the earlier studies have primarily focused on the temporal dimension of the relationship in the framework of the match-mismatch hypothesis. This hypothesis predicts that predator's recruitment will be high if the peak of the prey availability temporally matches the most energy-demanding period of the predators breeding phenology. However, the match-mismatch hypothesis ignores the level of food abundance while this can compensate small mismatches. Using a novel time-series model explicitly quantifying both the timing and the abundance component for trophic relationships, we here show that timing and abundance of food affect recruitment differently in a marine (cod/zooplankton), a marine-terrestrial (puffin/herring) and a terrestrial (sheep/vegetation) ecosystem. The quantification of the combined effect of abundance and timing of prey on predator dynamics enables us to come closer to the mechanisms by which environment variability may affect ecological systems.

Trophic interactions under climate fluctuations: the Atlantic puffin as an example.

Co-occurrence in food requirements of offspring and food availability is a key factor determining breeding success. Prey availability is typically dependent on environmental conditions that are different from those influencing the predator's decision regarding whether or not to initiate breeding, and is not always optimal at the peak of reproduction requirements. We investigated this relationship to understand better what determines the fledging success of the Atlantic puffin (Fratercula arctica). Colony data from Røst (northern Norway) covering a period of 27 years were analysed with parallel data on sea temperature and the size and abundance of the puffins' main prey (the Norwegian spring-spawning herring, Clupea harengus). By fitting statistical models to the fledging success, we found that one effect of climate on this population of Atlantic puffins is indirect and mediated by sea temperature affecting the availability of first-year herring. The best model also demonstrates that the breeding success of the Røst puffins may be quantitatively predicted from the size of first-year herring and sea temperature.