Local reflects global: Life stage-dependent changes in the phenology of coastal habitat use by North Sea herring.

Climate warming is affecting the suitability and utilization of coastal habitats by marine fishes around the world. Phenological changes are an important indicator of population responses to climate-induced changes but remain difficult to detect in marine fish populations. The design of large-scale monitoring surveys does not allow fine-grained temporal inference of population responses, while the responses of ecologically and economically important species groups such as small pelagic fish are particularly sensitive to temporal resolution. Here, we use the longest, highest resolution time series of species composition and abundance of marine fishes in northern Europe to detect possible phenological shifts in the small pelagic North Sea herring. We detect a clear forward temporal shift in the phenology of nearshore habitat use by small juvenile North Sea herring. This forward shift might be linked to changes in water temperatures in the North Sea. We next assessed the robustness of the effects we found with respect to monitoring design. We find that reducing the temporal resolution of our data to reflect the resolution typical of larger surveys makes it difficult to detect phenological shifts and drastically reduces the effect sizes of environmental covariates such as seawater temperature. Our study therefore shows how local, long-term, high-resolution time series of fish catches are essential to understand the general phenological responses of marine fishes to climate warming and to define ecological indicators of system-level changes.

Cross-basin and cross-taxa patterns of marine community tropicalization and deborealization in warming European seas.

Ocean warming and acidification, decreases in dissolved oxygen concentrations, and changes in primary production are causing an unprecedented global redistribution of marine life. The identification of underlying ecological processes underpinning marine species turnover, particularly the prevalence of increases of warm-water species or declines of cold-water species, has been recently debated in the context of ocean warming. Here, we track changes in the mean thermal affinity of marine communities across European seas by calculating the Community Temperature Index for 65 biodiversity time series collected over four decades and containing 1,817 species from different communities (zooplankton, coastal benthos, pelagic and demersal invertebrates and fish). We show that most communities and sites have clearly responded to ongoing ocean warming via abundance increases of warm-water species (tropicalization, 54%) and decreases of cold-water species (deborealization, 18%). Tropicalization dominated Atlantic sites compared to semi-enclosed basins such as the Mediterranean and Baltic Seas, probably due to physical barrier constraints to connectivity and species colonization. Semi-enclosed basins appeared to be particularly vulnerable to ocean warming, experiencing the fastest rates of warming and biodiversity loss through deborealization.

Why we cannot always expect life history strategies to directly inform on sensitivity to environmental change.

Variation in life history traits in animals and plants can often be structured along major axes of life history strategies. The position of a species along these axes can inform on their sensitivity to environmental change. For example, species with slow life histories are found to be less sensitive in their long-term population responses to environmental change than species with fast life histories. This provides a tantalizing link between sets of traits and population responses to change, contained in a highly generalizable theoretical framework. Life history strategies are assumed to reflect the outcome of life history tradeoffs that, by their very nature, act at the individual level. Examples include the tradeoff between current and future reproductive success, and allocating energy into growth versus reproduction. But the importance of such tradeoffs in structuring population-level responses to environmental change remains understudied. We aim to increase our understanding of the link between individual-level life history tradeoffs and the structuring of life history strategies across species, as well as the underlying links to population responses to environmental change. We find that the classical association between lifehistory strategies and population responses to environmental change breaks down when accounting for individual-level tradeoffs and energy allocation. Therefore, projecting population responses to environmental change should not be inferred based only on a limited set of species traits. We summarize our perspective and a way forward in a conceptual framework.

Accelerated viral dynamics in bat cell lines, with implications for zoonotic emergence.

Bats host virulent zoonotic viruses without experiencing disease. A mechanistic understanding of the impact of bats' virus hosting capacities, including uniquely constitutive immune pathways, on cellular-scale viral dynamics is needed to elucidate zoonotic emergence. We carried out virus infectivity assays on bat cell lines expressing induced and constitutive immune phenotypes, then developed a theoretical model of our in vitro system, which we fit to empirical data. Best fit models recapitulated expected immune phenotypes for representative cell lines, supporting robust antiviral defenses in bat cells that correlated with higher estimates for within-host viral propagation rates. In general, heightened immune responses limit pathogen-induced cellular morbidity, which can facilitate the establishment of rapidly-propagating persistent infections within-host. Rapidly-transmitting viruses that have evolved with bat immune systems will likely cause enhanced virulence following emergence into secondary hosts with immune systems that diverge from those unique to bats.

Bats can carry viruses that are deadly to other mammals without themselves showing serious symptoms. In fact, bats are natural reservoirs for viruses that have some of the highest fatality rates of any viruses that people acquire from wild animals ­ including rabies, Ebola and the SARS coronavirus. Bats have a suite of antiviral defenses that keep the amount of virus in check. For example, some bats have an antiviral immune response called the interferon pathway perpetually switched on. In most other mammals, having such a hyper-vigilant immune response would cause harmful inflammation. Bats, however, have adapted anti-inflammatory traits that protect them from such harm, include the loss of certain genes that normally promote inflammation. However, no one has previously explored how these unique antiviral defenses of bats impact the viruses themselves. Now, Brook et al. have studied this exact question using bat cells grown in the laboratory. The experiments made use of cells from one bat species ­ the black flying fox ­ in which the interferon pathway is always on, and another ­ the Egyptian fruit bat ­ in which this pathway is only activated during an infection. The bat cells were infected with three different viruses, and then Brook et al. observed how the interferon pathway helped keep the infections in check, before creating a computer model of this response. The experiments and model helped reveal that the bats' defenses may have a potential downside for other animals, including humans. In both bat species, the strongest antiviral responses were countered by the virus spreading more quickly from cell to cell. This suggests that bat immune defenses may drive the evolution of faster transmitting viruses, and while bats are well protected from the harmful effects of their own prolific viruses, other creatures like humans are not. The findings may help to explain why bats are often the source for viruses that are deadly in humans. Learning more about bats' antiviral defenses and how they drive virus evolution may help scientists develop better ways to predict, prevent or limit the spread of viruses from bats to humans. More studies are needed in bats to help these efforts. In the meantime, the experiments highlight the importance of warning people to avoid direct contact with wild bats.

Parasite resource manipulation drives bimodal variation in infection duration.

Over a billion people on earth are infected with helminth parasites and show remarkable variation in parasite burden and chronicity. These parasite distributions are captured well by classic statistics, such as the negative binomial distribution. But the within-host processes underlying this variation are not well understood. In this study, we explain variation in macroparasite infection outcomes on the basis of resource flows within hosts. Resource flows realize the interactions between parasites and host immunity and metabolism. When host metabolism is modulated by parasites, we find a positive feedback of parasites on their own resources. While this positive feedback results in parasites improving their resource availability at high burdens, giving rise to chronic infections, it also results in a threshold biomass required for parasites to establish in the host, giving rise to acute infections when biomass fails to clear the threshold. Our finding of chronic and acute outcomes in bistability contrasts with classic theory, yet is congruent with the variation in helminth burdens observed in human and wildlife populations.

Feeding Immunity: Physiological and Behavioral Responses to Infection and Resource Limitation.

Resources are a core currency of species interactions and ecology in general (e.g., think of food webs or competition). Within parasite-infected hosts, resources are divided among the competing demands of host immunity and growth as well as parasite reproduction and growth. Effects of resources on immune responses are increasingly understood at the cellular level (e.g., metabolic predictors of effector function), but there has been limited consideration of how these effects scale up to affect individual energetic regimes (e.g., allocation trade-offs), susceptibility to infection, and feeding behavior (e.g., responses to local resource quality and quantity). We experimentally rewilded laboratory mice (strain C57BL/6) in semi-natural enclosures to investigate the effects of dietary protein and gastrointestinal nematode (Trichuris muris) infection on individual-level immunity, activity, and behavior. The scale and realism of this field experiment, as well as the multiple physiological assays developed for laboratory mice, enabled us to detect costs, trade-offs, and potential compensatory mechanisms that mice employ to battle infection under different resource conditions. We found that mice on a low-protein diet spent more time feeding, which led to higher body fat stores (i.e., concentration of a satiety hormone, leptin) and altered metabolite profiles, but which did not fully compensate for the effects of poor nutrition on albumin or immune defenses. Specifically, immune defenses measured as interleukin 13 (IL13) (a primary cytokine coordinating defense against T. muris) and as T. muris-specific IgG1 titers were lower in mice on the low-protein diet. However, these reduced defenses did not result in higher worm counts in mice with poorer diets. The lab mice, living outside for the first time in thousands of generations, also consumed at least 26 wild plant species occurring in the enclosures, and DNA metabarcoding revealed that the consumption of different wild foods may be associated with differences in leptin concentrations. When individual foraging behavior was accounted for, worm infection significantly reduced rates of host weight gain. Housing laboratory mice in outdoor enclosures provided new insights into the resource costs of immune defense to helminth infection and how hosts modify their behavior to compensate for those costs.

Collective behavior as a driver of critical transitions in migratory populations.

BACKGROUND: Mass migrations are among the most striking examples of animal movement in the natural world. Such migrations are major drivers of ecosystem processes and strongly influence the survival and fecundity of individuals. For migratory animals, a formidable challenge is to find their way over long distances and through complex, dynamic environments. However, recent theoretical and empirical work suggests that by traveling in groups, individuals are able to overcome these challenges and increase their ability to navigate. Here we use models to explore the implications of collective navigation on migratory, and population, dynamics, for both breeding migrations (to-and-fro migrations between distinct, fixed, end-points) and feeding migrations (loop migrations that track favorable conditions). RESULTS: We show that while collective navigation does improve a population's ability to migrate accurately, it can lead to Allee effects, causing the sudden collapse of populations if numbers fall below a critical threshold. In some scenarios, hysteresis prevents the migration from recovering even after the cause of the collapse has been removed. In collectively navigating populations that are locally adapted to specific breeding sites, a slight increase in mortality can cause a collapse of genetic population structure, rather than population size, making it more difficult to detect and prevent. CONCLUSIONS: Despite the large interest in collective behavior and its ubiquity in many migratory species, there is a notable lack of studies considering the implications of social navigation on the ecological dynamics of migratory species. Here we highlight the potential for a previously overlooked Allee effect in socially migrating species that may be important for conservation and management of such species.

When less is more: positive population-level effects of mortality.

Experimental and theoretical studies show that mortality imposed on a population can counter-intuitively increase the density of a specific life-history stage or total population density. Understanding positive population-level effects of mortality is advancing, illuminating implications for population, community, and applied ecology. Reconciling theory and data, we found that the mathematical models used to study mortality effects vary in the effects predicted and mechanisms proposed. Experiments predominantly demonstrate stage-specific density increases in response to mortality. We argue that the empirical evidence supports theory based on stage-structured population models but not on unstructured models. We conclude that stage-specific positive mortality effects are likely to be common in nature and that accounting for within-population individual variation is essential for developing ecological theory.

Cohort dynamics give rise to alternative stable community states.

Many ecological systems can exhibit alternative stable states (ASS), which implies that ecological communities may diverge depending on their initial state, despite identical environmental conditions. Here we present a new mechanism that can cause ASS in competition systems. Using a physiologically structured model of competing populations, representing Baltic Sea sprat and herring and their resources, we show how cohort-driven population cycles may result in priority effects leading to ASS. Similar mechanisms could, depending on mortality level, also result in a "resident strikes back" phenomenon. We argue that the prerequisites for the occurrence of ASS in our model system, that is, communities with competing populations exhibiting cohort cycles and variation in size at maturation, may be common in ecological systems.

Predators with multiple ontogenetic niche shifts have limited potential for population growth and top-down control of their prey.

Catastrophic collapses of top predators have revealed trophic cascades and community structuring by top-down control. When populations fail to recover after a collapse, this may indicate alternative stable states in the system. Overfishing has caused several of the most compelling cases of these dynamics, and in particular Atlantic cod stocks exemplify such lack of recovery. Often, competition between prey species and juvenile predators is hypothesized to explain the lack of recovery of predator populations. The predator is then considered to compete with its prey for one resource when small and to subsequently shift to piscivory. Yet predator life history is often more complex than that, including multiple ontogenetic diet shifts. Here we show that no alternative stable states occur when predators in an intermediate life stage feed on an additional resource (exclusive to the predator) before switching to piscivory, because predation and competition between prey and predator do not simultaneously structure community dynamics. We find top-down control by the predator only when there is no feedback from predator foraging on the additional resource. Otherwise, the predator population dynamics are governed by a bottleneck in individual growth occurring in the intermediate life stage. Therefore, additional resources for predators may be beneficial or detrimental for predator population growth and strongly influence the potential for top-down community control.

Size- and food-dependent growth drives patterns of competitive dominance along productivity gradients.

Patterns of coexistence among competing species exhibiting size- and food-dependent growth remain largely unexplored. Here we studied mechanisms behind coexistence and shifts in competitive dominance in a size-structured fish guild, representing sprat and herring stocks in the Baltic Sea, using a physiologically structured model of competing populations. The influence of degree of resource overlap and the possibility of undergoing ontogenetic diet shifts were studied as functions of zooplankton and zoobenthos productivity. By imposing different size-dependent mortalities, we could study the outcome of competition under contrasting environmental regimes representing poor and favorable growth conditions. We found that the identity of the dominant species shifted between low and high productivity. Adding a herring-exclusive benthos resource only provided a competitive advantage over sprat when size-dependent mortality was high enough to allow for rapid growth in the zooplankton niche. Hence, the importance of a bottom-up effect of varying productivity was dependent on a strong top-down effect. Although herring could depress shared resources to lower levels than could sprat and also could access an exclusive resource, the smaller size at maturation of sprat allowed it to coexist with herring and, in some cases, exclude it. Our model system, characterized by interactions among size cohorts, allowed for consumer coexistence even at full resource overlap at intermediate productivities when size-dependent mortality was low. Observed shifts in community patterns were crucially dependent on the explicit consideration of size- and food-dependent growth. Accordingly, we argue that accounting for food-dependent growth and size-dependent interactions is necessary to better predict changes in community structure and dynamics following changes in major ecosystem drivers such as resource productivity and mortality, which are fundamental for our ability to manage exploitation of living resources in, e.g., fisheries.