Fishing down then up the food web of an invaded lake.

Analysis of commercial catches reveals a serial depletion of some oceanic fish stocks over time, resulting in fisheries focusing on increasingly smaller species closer to the base of the food chain. This effect, described as fishing down the marine food web, is observed when the trophic level of the catch declines over time, raising concerns about the ecosystem impacts of fishing. Freshwater systems also experience harvest, yet do not appear to commonly show the same fishing down response perhaps because time series are too short to witness early depletions, fishing is often recreational, or other factors like stocking and invasive species influence patterns. Here we make use of extensive catch records from Lake Simcoe dating back to the 1860s, to examine if fishing down effects are observed in this highly exploited Canadian inland lake. We measured 2 commonly used indicators from catch data, mean trophic level (MTL) and fishing-in-balance (FiB), and compared trends between a historical period dominated by commercial fishing and a contemporary period when commercial fishing ceased and recreational fishing effort increased. We found a striking difference between the 2 time periods, with MTL (and to some extent FiB) declining during commercial fishing but increasing during recreational fishing. However, indicators either increased or decreased due to invasive species and increased due to stocking. We show that while declining MTL can occur in a freshwater lake, the trajectory can be altered by a switch to recreational fishing, as well as stocking and invasive species.

Shifting trophic control of fishery-ecosystem dynamics following biological invasions.

Increasing human population size and mobility have accelerated the translocation of nonnative species globally, which has become a major threat to conservation of biodiversity and ecosystem services. Introduced species can disrupt species interactions of the recipient ecosystem, triggering system-wide events, and amplify or dampen effects of existing pressures. We show how two pervasive intercontinental invasive consumers in North American lakes, dreissenids (filter-feeding mussels) and Bythotrephes (carnivorous zooplankton), nonlinearly modify consumer-resource dynamics and undermine management interventions to rebuild cold-water predatory fish biomass. Synthesizing 30 yr (1986-2015) of lake-wide monitoring data with a dynamic mass-balance food-web model (consisting of 61 species and trophic groups), we reconstructed historical food-web dynamics of Lake Simcoe, a large, temperate lake in Ontario, Canada that has shifted from a turbid to clear-water state. We then analyzed patterns of biomass fluctuations of three recreationally harvested, ecologically connected populations; lake trout (Salvelinus namaycush, a piscivore), lake whitefish (Coregonus clupeaformis, a benthivore), and cisco (C. artedi, a planktivore) before and after the invasions by testing hypotheses on their delayed recoveries under management interventions-predator manipulations (fishery removal and stocking) and nutrient (phosphorus) load reduction. Analyses suggest that fishery harvest primarily regulated early recovery trajectories of the piscivore and planktivore, weakening top-down control prior to the establishment of the invasive consumers. By contrast, the benthivore biomass patterns were shaped, in part, by the invasive mussels (via diet shift), independently of management actions. Although improved water quality (with reduced hypoxia in deeper water) and, in turn, higher macrophyte production are projected to expand the predation refuge for young fish, intensified planktivory (by Bythotrephes) and herbivory (by dreissenids) have triggered shifts in community composition (from pelagic to demersal dominance). These system-wide shifts, in turn, have substantially diminished ecosystem productivity, thereby shrinking fishery yields. Novel consumers can rewire food webs, disrupt energy flows, and suppress predator recoveries, underscoring the need to account for altered ecological reality when sustainably managing fishery resources in invaded ecosystems.

Roles of density-dependent growth and life history evolution in accounting for fisheries-induced trait changes.

The relative roles of density dependence and life history evolution in contributing to rapid fisheries-induced trait changes remain debated. In the 1930s, northeast Arctic cod (Gadus morhua), currently the world's largest cod stock, experienced a shift from a traditional spawning-ground fishery to an industrial trawl fishery with elevated exploitation in the stock's feeding grounds. Since then, age and length at maturation have declined dramatically, a trend paralleled in other exploited stocks worldwide. These trends can be explained by demographic truncation of the population's age structure, phenotypic plasticity in maturation arising through density-dependent growth, fisheries-induced evolution favoring faster-growing or earlier-maturing fish, or a combination of these processes. Here, we use a multitrait eco-evolutionary model to assess the capacity of these processes to reproduce 74 y of historical data on age and length at maturation in northeast Arctic cod, while mimicking the stock's historical harvesting regime. Our results show that model predictions critically depend on the assumed density dependence of growth: when this is weak, life history evolution might be necessary to prevent stock collapse, whereas when a stronger density dependence estimated from recent data is used, the role of evolution in explaining fisheries-induced trait changes is diminished. Our integrative analysis of density-dependent growth, multitrait evolution, and stock-specific time series data underscores the importance of jointly considering evolutionary and ecological processes, enabling a more comprehensive perspective on empirically observed stock dynamics than previous studies could provide.

Ecological change alters the evolutionary response to harvest in a freshwater fish.

Harvesting can induce rapid evolution in animal populations, yet the role of ecological change in buffering or enhancing that response is poorly understood. Here, we developed an eco-genetic model to examine how ecological changes brought about by two notorious invasive species, zebra and quagga mussels, influence harvest-induced evolution and resilience in a freshwater fish. Our study focused on lake whitefish (Coregonus clupeaformis) in the Laurentian Great Lakes, where the species supports valuable commercial and subsistence fisheries, and where the invasion of dreissenid (zebra and quagga) mussels caused drastic shifts in ecosystem productivity. Using our model system, we predicted faster rates of evolution of maturation reaction norms in lake whitefish under pre-invasion ecosystem conditions when growth and recruitment of young to the population were high. Slower growth rates that occurred under post-invasion conditions delayed when fish became vulnerable to the fishery, thus decreasing selection pressure and lessening the evolutionary response to harvest. Fishing with gill nets and traps nets generally selected for early maturation at small sizes, except when fishing at low levels with small mesh gill nets under pre-invasion conditions; in this latter case, evolution of delayed maturation was predicted. Overall, the invasion of dreissenid mussels lessened the evolutionary response to harvest, while also reducing the productivity and commercial yield potential of the stock. These results demonstrate how ecological conditions shape evolutionary outcomes and how invasive species can have a direct effect on evolutionary responses to harvest and sustainability.

Broad shifts in the resource use of a commercially harvested fish following the invasion of dreissenid mussels.

Dreissenid mussels, including the zebra (Dreissena polymorpha) and quagga (Dreissena rostiformus bugensis) mussel, are invasive species known for their capacity to act as ecosystem engineers. They have caused significant changes in the many freshwater systems they have invaded by increasing water clarity, reducing primary productivity, and altering zooplankton and benthic invertebrate assemblages. What is less clear is how their ecosystem engineering effects manifest up the food web to impact higher trophic levels, including fish. Here, we use a biological tracer (stable isotopes of carbon and nitrogen) to analyze long-term and broad-scale trends in the resource use of benthivorous lake whitefish (Coregonus clupeaformis) in the Laurentian Great Lakes, where dreissenid mussels have become established in each lake except Lake Superior. We measured stable isotope ratios from archived material (fish scale samples) collected over several decades by multiple agencies and from 14 locations around the Great Lakes. In the majority of locations, the δ13 C of lake whitefish increased following the establishment of dreissenid mussels. Trends in δ15 N were less clear, but significant breakpoints in the time series occurred within 5 yr of dreissenid establishment in several locations, followed by declines in δ15 N. In contrast, isotopic signatures in Lake Superior locations did not show these trends. Our results provide evidence that lake whitefish shifted toward greater reliance on nearshore benthic production, supporting the theory that fundamental energy pathways are changed when dreissenid mussels become established. Importantly, these effects were noted across multiple, large, and complex ecosystems spanning a broad geographic area. Our study underscores the potential for aquatic invasive species to alter key ecosystem services as demonstrated here through their impacts on energy pathways supporting a commercially harvested fish species.

Economic repercussions of fisheries-induced evolution.

Fish stocks experiencing high fishing mortality show a tendency to mature earlier and at a smaller size, which may have a genetic component and therefore long-lasting economic and biological effects. To date, the economic effects of such ecoevolutionary dynamics have not been empirically investigated. Using 70 y of data, we develop a bioeconomic model for Northeast Arctic cod to compare the economic yield in a model in which life-history traits can vary only through phenotypic plasticity with a model in which, in addition, genetic changes can occur. We find that evolutionary changes toward faster growth and earlier maturation occur consistently even if a stock is optimally managed. However, if a stock is managed optimally, the evolutionary changes actually increase economic yield because faster growth and earlier maturation raise the stock's productivity. The optimal fishing mortality is almost identical for the evolutionary and nonevolutionary model and substantially lower than what it has been historically. Therefore, the costs of ignoring evolution under optimal management regimes are negligible. However, if fishing mortality is as high as it has been historically, evolutionary changes may result in economic losses, but only if the fishery is selecting for medium-sized individuals. Because evolution facilitates growth, the fish are younger and still immature when they are susceptible to getting caught, which outweighs the increase in productivity due to fish spawning at an earlier age.

From genes to populations: how fisheries-induced evolution alters stock productivity.

By removing individuals with certain heritable characteristics such as large body size, harvesting may induce rapid evolutionary change in fish life history. There is controversy, however, as to the prevalence of fisheries-induced evolution (FIE) and to what extent it should be considered as part of sustainable resource management. Recent research has shown that FIE can be difficult to detect and its economic effects might not always be significant. Here, we show how population growth rate (r), a critical factor affecting sustainability and recovery, is affected by FIE through the analysis of a simulation model that demonstrates the link between individual-level genetic processes and stock dynamics. We examine how different levels of evolvability, fishing intensity, and density-dependence interact to influence r in three commercially harvested species: Atlantic cod (Gadus morhua), lake whitefish (Coregonus clupeaformis), and yellow perch (Perca flavescens). We demonstrate that at low harvest levels, evolution has minimal effect on r for all three species. However, at the harvest rates experienced by many fish stocks, evolution increases r and reduces the risk of collapse for cod and whitefish. During the initial stages of a harvest moratorium, a switch occurs, and r becomes reduced as a consequence of evolution. These results explain how evolution increases stock resilience, but also impedes recovery after periods of intense harvesting.

A bio-economic analysis of harvest control rules for the Northeast Arctic cod fishery.

Harvest control rules (HCRs) have been implemented for many fisheries worldwide. However, in most instances, those HCRs are not based on the explicit feedbacks between stock properties and economic considerations. This paper develops a bio-economic model that evaluates the HCR adopted in 2004 by the Joint Norwegian-Russian Fishery Commission to manage the world's largest cod stock, Northeast Arctic cod (NEA). The model considered here is biologically and economically detailed, and is the first to compare the performance of the stock's current HCR with that of alternative HCRs derived with optimality criteria. In particular, HCRs are optimized for economic objectives including fleet profits, economic welfare, and total yield and the emerging properties are analyzed. The performance of these optimal HCRs was compared with the currently used HCR. This paper show that the current HCR does in fact comes very close to maximizing profits. Furthermore, the results reveal that the HCR that maximizes profits is the most precautionary one among the considered HCRs. Finally, the HCR that maximizes yield leads to un-precautionary low levels of biomass. In these ways, the implementation of the HCR for NEA cod can be viewed as a success story that may provide valuable lessons for other fisheries.

Alternative migratory strategies related to life history differences in the Walleye (Sander vitreus).

BACKGROUND: While Pace of Life Syndrome predicts behavioural differences between individuals with differential growth and survival, testing these predictions in nature is challenging due to difficulties with measuring individual behaviour in the field. However, recent advances in acoustic telemetry technology have facilitated measurements of individual behaviour at scales not previously possible in aquatic ecosystems. METHODS: Using a Walleye (Sander vitreus) population inhabiting Black Bay, Lake Superior, we examine whether life history characteristics differ between more and less mobile individuals as predicted by Pace of Life Syndrome. We tracked the movement of 192 individuals from 2016 to 2019 using an acoustic telemetry study, relating patterns in annual migratory behaviour to individual growth, and seasonal changes in optimal thermal-optical habitat. RESULTS: We observed two consistent movement patterns in our study population-migratory individuals left Black Bay during late summer to early fall before returning to the bay, whereas residents remained within the bay year-round. The average maximum length of migrant Walleye was 5.5 cm longer than residents, and the sex ratios of Walleye caught during fall surveys was increasingly female-biased towards the mouth of Black Bay, suggesting that a majority of migrants were females. Further, Walleye occupancy outside of Black Bay was positively associated with increasing thermal-optical habitat. CONCLUSIONS: Walleye in Black Bay appear to conform to Pace of Life Syndrome, with migrant individuals gaining increased fitness through increased maximum size, which, given size-dependent fecundity in this species, likely results in greater reproductive success (via greater egg deposition vs. non-migrants). Further, apparent environmental (thermal) controls on migration suggest that migratory Walleye (more so than residents) may be more sensitive to changing environmental conditions (e.g., warming climate) than residents.

Eco-genetic modeling of contemporary life-history evolution.

We present eco-genetic modeling as a flexible tool for exploring the course and rates of multi-trait life-history evolution in natural populations. We build on existing modeling approaches by combining features that facilitate studying the ecological and evolutionary dynamics of realistically structured populations. In particular, the joint consideration of age and size structure enables the analysis of phenotypically plastic populations with more than a single growth trajectory, and ecological feedback is readily included in the form of density dependence and frequency dependence. Stochasticity and life-history trade-offs can also be implemented. Critically, eco-genetic models permit the incorporation of salient genetic detail such as a population's genetic variances and covariances and the corresponding heritabilities, as well as the probabilistic inheritance and phenotypic expression of quantitative traits. These inclusions are crucial for predicting rates of evolutionary change on both contemporary and longer timescales. An eco-genetic model can be tightly coupled with empirical data and therefore may have considerable practical relevance, in terms of generating testable predictions and evaluating alternative management measures. To illustrate the utility of these models, we present as an example an eco-genetic model used to study harvest-induced evolution of multiple traits in Atlantic cod. The predictions of our model (most notably that harvesting induces a genetic reduction in age and size at maturation, an increase or decrease in growth capacity depending on the minimum-length limit, and an increase in reproductive investment) are corroborated by patterns observed in wild populations. The predicted genetic changes occur together with plastic changes that could phenotypically mask the former. Importantly, our analysis predicts that evolutionary changes show little signs of reversal following a harvest moratorium. This illustrates how predictions offered by eco-genetic models can enable and guide evolutionarily sustainable resource management.

Rapid resistance to pesticide control is predicted to evolve in an invasive fish.

Xenobiotic resistance is commonly found in species with short generation times such as bacteria, annual plants, and insects. Nevertheless, the fundamental evolutionary principles that govern the spread of resistance alleles hold true for species with longer generation times. One such example could occur with sea lamprey (Petromyzon marinus), a parasitic invasive species in the Laurentian Great Lakes that decimated native fish populations prior to its control with the pesticide 3-trifluoromethyl-4-nitrophenol (TFM). Since the 1950s, tributaries have been treated annually with TFM, where treatments effectively remove most, but not all, larval sea lamprey. We developed an eco-genetic model of sea lamprey to examine factors affecting the evolution of resistance and found that resistance alleles rapidly rise to fixation after 40-80 years of treatment, despite the species' relatively long generation time (4-7 years). The absence of natal homing allows resistant individuals to spread quickly throughout the entire system, but also makes the early detection of resistance challenging. High costs of resistance and density independent reproduction can delay, but not prevent, the onset of resistance. These results illustrate that sea lamprey have the potential to evolve resistance to their primary control agent in the near future, highlighting the urgent need for alternative controls.

Reaction norm analysis reveals rapid shifts toward delayed maturation in harvested Lake Erie yellow perch (Perca flavescens).

Harvested marine fish stocks often show a rapid and substantial decline in the age and size at maturation. Such changes can arise from multiple processes including fisheries-induced evolution, phenotypic plasticity, and responses to environmental factors other than harvest. The relative importance of these processes could differ systematically between marine and freshwater systems. We tested for temporal shifts in the mean and within-cohort variability of age- and size-based maturation probabilities of female yellow perch (Perca flavescens Mitchill) from four management units (MUs) in Lake Erie. Lake Erie yellow perch have been commercially harvested for more than a century, and age and size at maturation have varied since sampling began in the 1980s. Our analysis compared probabilistic maturation reaction norms (PMRNs) for cohorts when abundance was lower and harvest higher (1993-1998) to cohorts when abundance was higher and harvest lower (2005-2010). PMRNs have been used in previous studies to detect signs of evolutionary change in response to harvest. Maturation size threshold increased between the early and late cohorts, and the increases were statistically significant for the youngest age in the western MU1 and for older ages in the eastern MU3. Maturation envelope widths, a measure of the variability in maturation among individuals in a cohort, also increased between early and late cohorts in the western MUs where harvest was highest. The highest rates of change in size at maturation for a given age were as large or larger than rates reported for harvested marine fishes where declines in age and size at maturation have been observed. Contrary to the general observation of earlier maturation evolving in harvested stocks, female yellow perch in Lake Erie may be rapidly evolving delayed maturation since harvest was relaxed in the late 1990s, providing a rare example of possible evolutionary recovery.

The evolution of spawning migrations: state dependence and fishing-induced changes.

Individuals migrate to exploit heterogeneities between spatially separated environments to modulate growth, survival, or reproduction. We devised a bioenergetics model to investigate the evolution of migration distance and its dependence on individual states. Atlantic cod Gadus morhua ranges from sedentary populations to stocks that migrate several thousand kilometers annually. We focused on the Northeast Arctic cod stock, which migrates south to spawn. A linear relationship between migration distance and the expected survival of offspring was assumed, here understood as the prospects for future survival and development that a fertilized egg faces at a particular spawning location. Reasons for why it may increase southward include warmer water that increases development rates, and thereby survival, along the pelagic drift trajectory. In the model, ingested energy can either be allocated to growth or stored for migration and reproduction. When migrating, individuals forgo foraging opportunities and expend energy. Optimal energy allocation and migration strategies were found using state-dependent optimization, with body length, age, condition, and current food availability as individual states. For both a historical and contemporary fishing regime we modeled two behaviors: (1) homing cod returning to the same spawning site each year and (2) roaming cod with no such constraints. The model predicted distinct regions of locally high spawning stock biomass. Large individuals in good condition migrated farthest, and these also tended to mature later in life. The roaming cod spread farther south as they grew larger and older. Homing cod did not have this freedom, and spawning was generally concentrated along a narrower stretch of the coastline. Under contemporary fishing, individuals matured earlier at a smaller size, had shorter migrations, spawned over a contracted geographical range, and tended to be in poorer condition. The effects were most pronounced for the homing behavior.

Evolutionary impact assessment: accounting for evolutionary consequences of fishing in an ecosystem approach to fisheries management.

Managing fisheries resources to maintain healthy ecosystems is one of the main goals of the ecosystem approach to fisheries (EAF). While a number of international treaties call for the implementation of EAF, there are still gaps in the underlying methodology. One aspect that has received substantial scientific attention recently is fisheries-induced evolution (FIE). Increasing evidence indicates that intensive fishing has the potential to exert strong directional selection on life-history traits, behaviour, physiology, and morphology of exploited fish. Of particular concern is that reversing evolutionary responses to fishing can be much more difficult than reversing demographic or phenotypically plastic responses. Furthermore, like climate change, multiple agents cause FIE, with effects accumulating over time. Consequently, FIE may alter the utility derived from fish stocks, which in turn can modify the monetary value living aquatic resources provide to society. Quantifying and predicting the evolutionary effects of fishing is therefore important for both ecological and economic reasons. An important reason this is not happening is the lack of an appropriate assessment framework. We therefore describe the evolutionary impact assessment (EvoIA) as a structured approach for assessing the evolutionary consequences of fishing and evaluating the predicted evolutionary outcomes of alternative management options. EvoIA can contribute to EAF by clarifying how evolution may alter stock properties and ecological relations, support the precautionary approach to fisheries management by addressing a previously overlooked source of uncertainty and risk, and thus contribute to sustainable fisheries.

Toward Darwinian fisheries management.

There is increasing evidence that fishing may cause rapid contemporary evolution in freshwater and marine fish populations. This has led to growing concern about the possible consequences such evolutionary change might have for aquatic ecosystems and the utility of those ecosystems to society. This special issue contains contributions from a symposium on fisheries-induced evolution held at the American Fisheries Society Annual Meeting in August 2008. Contributions include primary studies and reviews of field-based and experimental evidence, and several theoretical modeling studies advancing life-history theory and investigating potential management options. In this introduction we review the state of research in the field, discuss current controversies, and identify contributions made by the papers in this issue to the knowledge of fisheries-induced evolution. We end by suggesting directions for future research.

Propensity of marine reserves to reduce the evolutionary effects of fishing in a migratory species.

Evolutionary effects of fishing can have unwanted consequences diminishing a fishery's value and sustainability. Reserves, or no-take areas, have been proposed as a management tool for reducing fisheries-induced selection, but their effectiveness for migratory species has remained unexplored. Here we develop an eco-genetic model to predict the effects of marine reserves on fisheries-induced evolution under migration. To represent a stock that undergoes an annual migration between feeding and spawning grounds, we draw model parameters from Atlantic cod (Gadus morhua) in the northern part of its range. Our analysis leads to the following conclusions: (i) a reserve in a stock's feeding grounds, protecting immature and mature fish alike, reduces fisheries-induced evolution, even though protected and unprotected population components mix on the spawning grounds; (ii) in contrast, a reserve in a stock's spawning grounds, protecting only mature fish, has little mitigating effects on fisheries-induced evolution and can sometimes even exacerbate its magnitude; (iii) evolutionary changes that are already underway may be difficult to reverse with a reserve; (iv) directly after a reserve is created or enlarged, most reserve scenarios result in yield losses; and (v) timescale is very important: short-term yield losses immediately after a reserve's creation can give way to long-term gains.

Implications of fisheries-induced evolution for stock rebuilding and recovery.

Worldwide depletion of fish stocks has led fisheries managers to become increasingly concerned about rebuilding and recovery planning. To succeed, factors affecting recovery dynamics need to be understood, including the role of fisheries-induced evolution. Here we investigate a stock's response to fishing followed by a harvest moratorium by analyzing an individual-based evolutionary model parameterized for Atlantic cod Gadus morhua from its northern range, representative of long-lived, late-maturing species. The model allows evolution of life-history processes including maturation, reproduction, and growth. It also incorporates environmental variability, phenotypic plasticity, and density-dependent feedbacks. Fisheries-induced evolution affects recovery in several ways. The first decades of recovery were dominated by demographic and density-dependent processes. Biomass rebuilding was only lightly influenced by fisheries-induced evolution, whereas other stock characteristics such as maturation age, spawning stock biomass, and recruitment were substantially affected, recovering to new demographic equilibria below their preharvest levels. This is because genetic traits took thousands of years to evolve back to preharvest levels, indicating that natural selection driving recovery of these traits is weaker than fisheries-induced selection was. Our results strengthen the case for proactive management of fisheries-induced evolution, as the restoration of genetic traits altered by fishing is slow and may even be impractical.