A reconstruction of parasite burden reveals one century of climate-associated parasite decline.

Long-term data allow ecologists to assess trajectories of population abundance. Without this context, it is impossible to know whether a taxon is thriving or declining to extinction. For parasites of wildlife, there are few long-term data-a gap that creates an impediment to managing parasite biodiversity and infectious threats in a changing world. We produced a century-scale time series of metazoan parasite abundance and used it to test whether parasitism is changing in Puget Sound, United States, and, if so, why. We performed parasitological dissection of fluid-preserved specimens held in natural history collections for eight fish species collected between 1880 and 2019. We found that parasite taxa using three or more obligately required host species-a group that comprised 52% of the parasite taxa we detected-declined in abundance at a rate of 10.9% per decade, whereas no change in abundance was detected for parasites using one or two obligately required host species. We tested several potential mechanisms for the decline in 3+-host parasites and found that parasite abundance was negatively correlated with sea surface temperature, diminishing at a rate of 38% for every 1 °C increase. Although the temperature effect was strong, it did not explain all variability in parasite burden, suggesting that other factors may also have contributed to the long-term declines we observed. These data document one century of climate-associated parasite decline in Puget Sound-a massive loss of biodiversity, undetected until now.

Avoiding critical thresholds through effective monitoring.

A major challenge in sustainability science is identifying targets that maximize ecosystem benefits to humanity while minimizing the risk of crossing critical system thresholds. One critical threshold is the biomass at which populations become so depleted that their population growth rates become negative-depensation. Here, we evaluate how the value of monitoring information increases as a natural resource spends more time near the critical threshold. This benefit emerges because higher monitoring precision promotes higher yield and a greater capacity to recover from overharvest. We show that precautionary buffers that trigger increased monitoring precision as resource levels decline may offer a way to minimize monitoring costs and maximize profits. In a world of finite resources, improving our understanding of the trade-off between precision in estimates of population status and the costs of mismanagement will benefit stakeholders that shoulder the burden of these economic and social costs.

Assessing the potential for demographic restoration and assisted evolution to build climate resilience in coral reefs.

Interest is growing in developing conservation strategies to restore and maintain coral reef ecosystems in the face of mounting anthropogenic stressors, particularly climate warming and associated mass bleaching events. One such approach is to propagate coral colonies ex situ and transplant them to degraded reef areas to augment habitat for reef-dependent fauna, prevent colonization from spatial competitors, and enhance coral reproductive output. In addition to such "demographic restoration" efforts, manipulating the thermal tolerance of outplanted colonies through assisted relocation, selective breeding, or genetic engineering is being considered for enhancing rates of evolutionary adaptation to warming. Although research into such "assisted evolution" strategies has been growing, their expected performance remains unclear. We evaluated the potential outcomes of demographic restoration and assisted evolution in climate change scenarios using an eco-evolutionary simulation model. We found that supplementing reefs with pre-existing genotypes (demographic restoration) offers little climate resilience benefits unless input levels are large and maintained for centuries. Supplementation with thermally resistant colonies was successful at improving coral cover at lower input levels, but only if maintained for at least a century. Overall, we found that, although demographic restoration and assisted evolution have the potential to improve long-term coral cover, both approaches had a limited impact in preventing severe declines under climate change scenarios. Conversely, with sufficient natural genetic variance and time, corals could readily adapt to warming temperatures, suggesting that restoration approaches focused on building genetic variance may outperform those based solely on introducing heat-tolerant genotypes.

The shadow model: how and why small choices in spatially explicit species distribution models affect predictions.

The use of species distribution models (SDMs) has rapidly increased over the last decade, driven largely by increasing observational evidence of distributional shifts of terrestrial and aquatic populations. These models permit, for example, the quantification of range shifts, the estimation of species co-occurrence, and the association of habitat to species distribution and abundance. The increasing complexity of contemporary SDMs presents new challenges-as the choices among modeling options increase, it is essential to understand how these choices affect model outcomes. Using a combination of original analysis and literature review, we synthesize the effects of three common model choices in semi-parametric predictive process species distribution modeling: model structure, spatial extent of the data, and spatial scale of predictions. To illustrate the effects of these choices, we develop a case study centered around sablefish (Anoplopoma fimbria) distribution on the west coast of the USA. The three modeling choices represent decisions necessary in virtually all ecological applications of these methods, and are important because the consequences of these choices impact derived quantities of interest (e.g., estimates of population size and their management implications). Truncating the spatial extent of data near the observed range edge, or using a model that is misspecified in terms of covariates and spatial and spatiotemporal fields, led to bias in population biomass trends and mean distribution compared to estimates from models using the full dataset and appropriate model structure. In some cases, these suboptimal modeling decisions may be unavoidable, but understanding the tradeoffs of these choices and impacts on predictions is critical. We illustrate how seemingly small model choices, often made out of necessity or simplicity, can affect scientific advice informing management decisions-potentially leading to erroneous conclusions about changes in abundance or distribution and the precision of such estimates. For example, we show how incorrect decisions could cause overestimation of abundance, which could result in management advice resulting in overfishing. Based on these findings and literature gaps, we outline important frontiers in SDM development.

A structured seabird population model reveals how alternative forage fish control rules benefit seabirds and fisheries.

Fisheries for forage fish may affect the survival and reproduction of piscivorous predators, especially seabirds. However, seabirds have evolved life history strategies to cope with natural fluctuations in prey and it is difficult to separate effects of fishing on seabirds from impacts of natural variability. To date, potential impacts of forage fisheries on seabirds have mainly been explored using ecosystem models that simplify seabird-forage-fish dynamics. We sought to explore how different forage fish harvest policies affect seabirds, accounting for structured population dynamics, life history specifics, and variation in forage fish dependencies across life stages; and how impacts vary across seabird and forage fish life histories. To explore these impacts, we developed an age-stage structured seabird model that incorporates seabird diet specialization, foraging behavior, and reproductive strategy, as well as different functional responses between prey availability and adult survival, juvenile survival, reproductive success, and breeder propensity. We parameterized this model for two contrasting seabird life histories: (1) a low fecundity, limited foraging range, diet specialist ("restricted"); and (2) a high fecundity, wide ranging, diet generalist ("flexible"). Each was paired with two different forage fish prey archetypes that were fished under various control rules. The restricted seabird population was expectedly less robust to constant fishing pressure than the flexible seabird, and this sensitivity was mainly due to functional response parameterization, rather than other life history parameters. Particularly, the restricted seabird was highly sensitive to the relationship between prey availability and adult survival but was not sensitive to the relationship between prey and reproductive success. An adaptive biomass-limit harvest rule for forage fish resulted in substantially higher seabird abundance compared to constant fishing across all scenarios, with minimal trade-offs to the fishery (depending on fishery management objectives). However, mechanisms governing the impact of the forage fish fishery on the seabird varied by forage fish type. Therefore, tailoring forage fish management strategies to forage fish life history can lead to mutually acceptable outcomes for fisheries and seabirds. If data or time are limited, an adaptive control rule is likely a safe bet for meeting seabird conservation objectives with limited impacts to fisheries.

Direct and ancillary benefits of ecosystem-based fisheries management in forage fish fisheries.

Natural resource management is evolving toward holistic, ecosystem-based approaches to decision making. The ecosystem science underpinning these approaches needs to account for the complexity of multiple interacting components within and across coupled natural-human systems. In this research, we investigate the potential economic and ecological gains from adopting ecosystem-based approaches for the sardine and anchovy fisheries off of the coast of California, USA. Research has shown that while predators in this system are likely substituting one forage species for another, the assemblage of sardine and anchovy can be a significant driver of predator populations. Currently, the harvest control rules for sardine and anchovy fisheries align more with traditional single species framework. We ask what are the economic and ecological gains when jointly determining the harvest control rules for both forage fish stocks and their predators relative to the status quo? What are the implications of synchronous and anti-synchronous environmental recruitment variation between the anchovy and sardine stocks on optimal food-web management? To investigate these questions, we develop an economic-ecological model for sardine, anchovy, a harvested predator (halibut), and an endangered predator (Brown Pelican) that includes recruitment variability over time driven by changing environmental conditions. Utilizing large-scale numerical optimal control methods, we investigate how the multiple variants of integrated management of sardine, anchovy, and halibut impact the overall economic condition of the fisheries and Brown Pelican populations over time. We find significant gains in moving to integrated catch control rules both in terms of the economic gains of the fished stocks, and in terms of the impacts on the Brown Pelican populations. We also compare the relative performance of current stylized catch control rules to optimal single species and optimal ecosystem-based fisheries management (EBFM) across ecological and economic dimensions, where the former trade-off considerable economic value for ecological goals. More generally, we demonstrate how EBFM approaches introduce and integrate additional management levers for policymakers to achieve non-fishery objectives at lowest costs to the fishing sectors.

Evolution and connectivity influence the persistence and recovery of coral reefs under climate change in the Caribbean, Southwest Pacific, and Coral Triangle.

Corals are experiencing unprecedented decline from climate change-induced mass bleaching events. Dispersal not only contributes to coral reef persistence through demographic rescue but can also hinder or facilitate evolutionary adaptation. Locations of reefs that are likely to survive future warming therefore remain largely unknown, particularly within the context of both ecological and evolutionary processes across complex seascapes that differ in temperature range, strength of connectivity, network size, and other characteristics. Here, we used eco-evolutionary simulations to examine coral adaptation to warming across reef networks in the Caribbean, the Southwest Pacific, and the Coral Triangle. We assessed the factors associated with coral persistence in multiple reef systems to understand which results are general and which are sensitive to particular geographic contexts. We found that evolution can be critical in preventing extinction and facilitating the long-term recovery of coral communities in all regions. Furthermore, the strength of immigration to a reef (destination strength) and current sea surface temperature robustly predicted reef persistence across all reef networks and across temperature projections. However, we found higher initial coral cover, slower recovery, and more evolutionary lag in the Coral Triangle, which has a greater number of reefs and more larval settlement than the other regions. We also found the lowest projected future coral cover in the Caribbean. These findings suggest that coral reef persistence depends on ecology, evolution, and habitat network characteristics, and that, under an emissions stabilization scenario (RCP 4.5), recovery may be possible over multiple centuries.

Evolution reverses the effect of network structure on metapopulation persistence.

Global environmental change is challenging species with novel conditions, such that demographic and evolutionary trajectories of populations are often shaped by the exchange of organisms and alleles across landscapes. Current ecological theory predicts that random networks with dispersal shortcuts connecting distant sites can promote persistence when there is no capacity for evolution. Here, we show with an eco-evolutionary model that dispersal shortcuts across environmental gradients instead hinder persistence for populations that can evolve because long-distance migrants bring extreme trait values that are often maladaptive, short-circuiting the adaptive response of populations to directional change. Our results demonstrate that incorporating evolution and environmental heterogeneity fundamentally alters theoretical predictions regarding persistence in ecological networks.

Unexpected food web responses to low dissolved oxygen in an estuarine fjord.

In coastal marine ecosystems, the depletion of dissolved oxygen can cause behavioral and distributional shifts of organisms and thereby alter ecological processes. We used the spatiotemporal variation in the onset and intensity of low dissolved oxygen in Hood Canal, Washington, USA, to investigate consequences of seasonally reduced oxygen on fish-zooplankton predator-prey interactions. By simultaneously monitoring densities of zooplankton (primarily the euphausiid; Euphausia pacifica) and zooplanktivorous fish (Pacific herring, Clupea pallasii, and Pacific hake, Mercluccius productus), and the feeding of zooplanktivorous fish, we could separate the effects of dissolved oxygen on fish-zooplankton interactions from other seasonal changes. We expected that fish predators (especially Pacific herring) would be less abundant and have lower feeding rates when oxygen levels declined below biological thresholds, and that this would result in increased zooplankton abundance in areas with lowest dissolved oxygen. However, these expectations were not borne out. Overall, there was mixed evidence for an effect of dissolved oxygen on many of our response variables, and when effects were detected, they were frequently in the opposite direction of our expectations. Specifically, the pelagic fish community became more abundant (as measured by increasing acoustic backscatter), which was particularly pronounced for Pacific herring. Zooplankton had weak evidence for a response to dissolved oxygen, but the direction was negative instead of positive. Although predator feeding composition was unrelated to dissolved oxygen, stomach fullness (an index of feeding intensity) of Pacific herring declined, as per our expectations. These unexpected findings highlight the importance of in situ measurements of multiple aspects of predator-prey linkages in response to environmental stress to enhance our ability to predict ecological consequences of declining oxygen.

Limited evidence for sardine and anchovy asynchrony: re-examining an old story.

Asynchronous fluctuations in abundance between species with similar ecological roles can stabilize food webs and support coexistence. Sardine (Sardinops spp.) and anchovy (Engraulis spp.) have long been used as an example of this pattern because low-frequency variation in catches of these species appears to occur out of phase, suggesting that fisheries and generalist predators could be buffered against shifts in productivity of a single species. Using landings data and biomass and recruitment estimates from five regions, we find that species do not have equivalent peak abundances, suggesting that high abundance in one species does not compensate for low abundance in the other. We find that globally there is a stronger pattern of asynchrony in landings compared to biomass, such that landings data have exaggerated the patterns of asynchrony. Finally, we show that power to detect decadal asynchrony is poor, requiring a time series more than twice the length of the period of fluctuation. These results indicate that it is unlikely that the dynamics of these two species are compensatory enough to buffer fisheries and predators from changes in abundance, and that the measurements of asynchrony have largely been a statistical artefact of using short time series and landings data to infer ecology.

Resurgence of an apex marine predator and the decline in prey body size.

In light of recent recoveries of marine mammal populations worldwide and heightened concern about their impacts on marine food webs and global fisheries, it has become increasingly important to understand the potential impacts of large marine mammal predators on prey populations and their life-history traits. In coastal waters of the northeast Pacific Ocean, marine mammals have increased in abundance over the past 40 to 50 y, including fish-eating killer whales that feed primarily on Chinook salmon. Chinook salmon, a species of high cultural and economic value, have exhibited marked declines in average size and age throughout most of their North American range. This raises the question of whether size-selective predation by marine mammals is generating these trends in life-history characteristics. Here we show that increased predation since the 1970s, but not fishery selection alone, can explain the changes in age and size structure observed for Chinook salmon populations along the west coast of North America. Simulations suggest that the decline in mean size results from the selective removal of large fish and an evolutionary shift toward faster growth and earlier maturation caused by selection. Our conclusion that intensifying predation by fish-eating killer whales contributes to the continuing decline in Chinook salmon body size points to conflicting management and conservation objectives for these two iconic species.

Production dynamics reveal hidden overharvest of inland recreational fisheries.

Recreational fisheries are valued at $190B globally and constitute the predominant way in which people use wild fish stocks in developed countries, with inland systems contributing the main fraction of recreational fisheries. Although inland recreational fisheries are thought to be highly resilient and self-regulating, the rapid pace of environmental change is increasing the vulnerability of these fisheries to overharvest and collapse. Here we directly evaluate angler harvest relative to the biomass production of individual stocks for a major inland recreational fishery. Using an extensive 28-y dataset of the walleye (Sander vitreus) fisheries in northern Wisconsin, United States, we compare empirical biomass harvest (Y) and calculated production (P) and biomass (B) for 390 lake year combinations. Production overharvest occurs when harvest exceeds production in that year. Biomass and biomass turnover (P/B) declined by ∼30 and ∼20%, respectively, over time, while biomass harvest did not change, causing overharvest to increase. Our analysis revealed that ∼40% of populations were production-overharvested, a rate >10× higher than estimates based on population thresholds often used by fisheries managers. Our study highlights the need to adapt harvest to changes in production due to environmental change.

Correction: Eco-Label Conveys Reliable Information on Fish Stock Health to Seafood Consumers.

[This corrects the article DOI: 10.1371/journal.pone.0043765.].

Spawning and emergence phenology of bull trout Salvelinus confluentus under differing thermal regimes.

Median bull trout Salvelinus confluentus breeding was 2 weeks earlier in a cool stream than in a proximate warmer stream, aligning with expectations for salmonids, followed by emergence timing calculated to be 6 weeks later in the cool stream than the warm stream. This pattern is consistent with both site-specific adaptation and thermal spawning threshold hypotheses for life-history event timing in this threatened species.

Somatic growth contributes to population variation in marine fishes.

Understanding population fluctuations is a major goal of population ecology. In unpredictable marine environments, population variation is thought to be caused primarily by varying survival rates through a critical early life-history stage. However, there is increasing evidence that somatic growth variation is common and causes population fluctuations. We examine the relative effects of empirically validated variability in somatic growth and recruitment on two response metrics across eight different life-history archetypes of marine fish. We evaluate how much variation is propagated into mature biomass (MB), a proxy for population resilience, and population production, a measure of population rebuilding capacity. Production is defined as the biomass produced by the stock above what is needed to sustain the population at a constant level. We used empirical estimates of reproductive success and somatic growth rate, coupled with a population model, to evaluate the relative role of both types of variation in population fluctuations. The effects of this variation on population production and MB were examined across three variation scenarios, in which somatic growth only, reproduction only or both processes varied temporally. We also examined three levels of age truncation to explore whether modified population age structure altered these dynamics. The contribution of somatic growth to biomass variability exceeded that of recruitment for some species (2/8), while in others (5/8 species), recruitment variation was more influential. When population production was examined, somatic growth variation contributed more to population variation for three species. The relative importance of the two processes was not clearly correlated with key life-history traits (i.e., growth and mortality rates), but instead was determined by time-series characteristics of growth and recruitment variation. Increasing age truncation slightly increased the relative effect of recruitment variation on MB variation for three species. These results suggest somatic growth variation can be as important as early life-history survival in driving population fluctuations in some marine fish species. This analysis provides a counterexample to the commonly held assumption of many marine population dynamics models: That population variability is induced primarily through variation in reproductive success.

Economic value of ecological information in ecosystem-based natural resource management depends on exploitation history.

Ecosystem approaches to natural resource management are seen as a way to provide better outcomes for ecosystems and for people, yet the nature and strength of interactions among ecosystem components is usually unknown. Here we characterize the economic benefits of ecological knowledge through a simple model of fisheries that target a predator (piscivore) and its prey. We solve for the management (harvest) trajectory that maximizes net present value (NPV) for different ecological interactions and initial conditions that represent different levels of exploitation history. Optimal management trajectories generally approached similar harvest levels, but the pathways toward those levels varied considerably by ecological scenario. Application of the wrong harvest trajectory, which would happen if one type of ecological interaction were assumed but in fact another were occurring, generally led to only modest reductions in NPV. However, the risks were not equal across fleets: risks of incurring large losses of NPV and missing management targets were much higher in the fishery targeting piscivores, especially when piscivores were heavily depleted. Our findings suggest that the ecosystem approach might provide the greatest benefits when used to identify system states where management performs poorly with imperfect knowledge of system linkages so that management strategies can be adopted to avoid those states.

Old-Growth Fishes Become Scarce under Fishing.

Researchers have long recognized the importance of ecological differences at the species level in structuring natural communities yet until recently have often overlooked the influence of intraspecific trait variation, which can profoundly alter community dynamics [1]. Human extraction of living resources can reduce intraspecific trait variation by, for example, causing truncation of age and size structure of populations, where numbers of older individuals decline far more with exploitation than younger individuals. Age truncation can negatively affect population and community stability, increasing variability in population and community biomass [2-6], reducing productivity [7-10] and life-history diversity in traits such as the spatial and temporal pattern of reproduction and migration [4, 11-16]. Here, we quantified the extent of age truncation in 63 fished populations across five ocean regions, as measured by how much the proportions of fish in the oldest age groups declined over time. The proportion of individuals in the oldest age classes decreased significantly in 79% to 97% of populations (compared to historical or unfished values, respectively), and the magnitude of decline was greater than 90% in 32% to 41% of populations. The pervasiveness and intensity of age truncation indicates that fishing is likely reducing the stability of many marine communities. Our findings suggest that more emphasis should be given to management measures that reduce the impact of fishing on age truncation, including no-take areas, slot limits that prohibit fishing on all except a narrow range of fish sizes, and rotational harvesting.

Density dependence governs when population responses to multiple stressors are magnified or mitigated.

Population endangerment typically arises from multiple, potentially interacting anthropogenic stressors. Extensive research has investigated the consequences of multiple stressors on organisms, frequently focusing on individual life stages. Less is known about population-level consequences of exposure to multiple stressors, especially when exposure varies through life. We provide the first theoretical basis for identifying species at risk of magnified effects from multiple stressors across life history. By applying a population modeling framework, we reveal conditions under which population responses from stressors applied to distinct life stages are either magnified (synergistic) or mitigated. We find that magnification or mitigation critically depends on the shape of density dependence, but not the life stage in which it occurs. Stressors are always magnified when density dependence is linear or concave, and magnified or mitigated when it is convex. Using Bayesian numerical methods, we estimated the shape of density dependence for eight species across diverse taxa, finding support for all three shapes.

Risks of ocean acidification in the California Current food web and fisheries: ecosystem model projections.

The benefits and ecosystem services that humans derive from the oceans are threatened by numerous global change stressors, one of which is ocean acidification. Here, we describe the effects of ocean acidification on an upwelling system that already experiences inherently low pH conditions, the California Current. We used an end-to-end ecosystem model (Atlantis), forced by downscaled global climate models and informed by a meta-analysis of the pH sensitivities of local taxa, to investigate the direct and indirect effects of future pH on biomass and fisheries revenues. Our model projects a 0.2-unit drop in pH during the summer upwelling season from 2013 to 2063, which results in wide-ranging magnitudes of effects across guilds and functional groups. The most dramatic direct effects of future pH may be expected on epibenthic invertebrates (crabs, shrimps, benthic grazers, benthic detritivores, bivalves), and strong indirect effects expected on some demersal fish, sharks, and epibenthic invertebrates (Dungeness crab) because they consume species known to be sensitive to changing pH. The model's pelagic community, including marine mammals and seabirds, was much less influenced by future pH. Some functional groups were less affected to changing pH in the model than might be expected from experimental studies in the empirical literature due to high population productivity (e.g., copepods, pteropods). Model results suggest strong effects of reduced pH on nearshore state-managed invertebrate fisheries, but modest effects on the groundfish fishery because individual groundfish species exhibited diverse responses to changing pH. Our results provide a set of projections that generally support and build upon previous findings and set the stage for hypotheses to guide future modeling and experimental analysis on the effects of OA on marine ecosystems and fisheries.