Sex-specific plasticity in a trophic polymorphic aquatic predator: a modeling approach.

Phenotypic plasticity is common among animal taxa. While there are clearly limits and likely costs to plasticity, these costs are unknown for most organisms. Further, as plasticity is partially genetically determined, the potential magnitude of exhibited plasticity may vary among individuals. In addition to phenotypic plasticity, various animal taxa also display sexual size dimorphism, a feature ultimately thought to arise due to differential size-dependent fitness costs and benefits between sexes. We hypothesized that differential selection acting on males and females can indirectly select for unequal genetically defined plasticity potential between the sexes. We evaluate this possibility for Eurasian perch (Perca fluviatilis), a species that displays modest sexual size dimorphism and habitat-related morphological plasticity. Using 500-year simulations of an ecogenetic agent-based model, we demonstrate that genetically determined morphological plasticity potential may evolve differently for males and females, leading to greater realized morphological variation between habitats for one sex over the other. Genetically determined potential for plasticity evolved differently between sexes across (a) various sex-specific life-history differences and (b) a variety of assumed costs of plasticity acting on both growth and survival. Morphological analyses of Eurasian perch collected in situ were consistent with model predictions: realized morphological variation between habitats was greater for females than males. We suggest that due to sex-specific selective pressures, differences in male and female genetically defined potential for plasticity may be a common feature across organisms.

Movement rule selection through eco-genetic modeling: Application to diurnal vertical movement.

Agent-based, spatially-explicit models that incorporate movement rules are used across ecological disciplines for a variety of applications. However, appropriate movement rules may be difficult to implement due to the complexity of an individual's response to both proximate and ultimate cues, as well as the difficulty in directly assessing how organisms choose to move across their environment. Environmental cues may be complex and dynamic, and therefore, movement responses may require tradeoffs between preferred levels of different environmental variables (e.g., temperature, light level, and prey availability). Here, we present an approach to determine appropriate movement rules by setting them as heritable traits in an eco-genetic modeling framework and allowing movement rules to evolve during the model rather than setting them a priori. We modeled yellow perch, Perca flavescens, movement in a simulated environment and allowed perch to move in response to high-resolution vertical gradients in temperature, dissolved oxygen, light, predators, and prey. Evolving movement rules ultimately increased fish growth and survival over generations in our model, indicating that evolving movement rules led to improved individual performance. We found that emergent movement rules were consistent across trials, with evolved movement rules incorporating different weights of these environmental factors and the most rapid selection on temperature preference. This case study presents a flexible method using eco-genetic modeling to determine appropriate movement rules that can be applied to diverse scenarios in spatially-explicit ecological modeling.

Behavioral and physiological responses of yellow perch (Perca flavescens) to moderate hypoxia.

While severe hypoxia can be lethal and is usually avoided by mobile aquatic organisms, moderate hypoxic conditions are likely more prevalent and may affect organisms, such as fishes, in a variety of systems. However, fishes have the potential to adjust physiologically and behaviorally and thus reduce the negative effects of hypoxia. Quantifying such physiological responses may shed light on the ability of fishes to tolerate reduced oxygen concentrations. This study assessed how two different hatchery populations of yellow perch Perca flavescens, a fish that is likely to encounter moderate hypoxic conditions in a variety of systems, responded to moderate hypoxic exposure through three experiments: 1) a behavioral foraging experiment, 2) an acute exposure experiment, and 3) a chronic exposure experiment. No marked behavioral or physiological adjustments were observed in response to hypoxia (e.g., hemoglobin, feeding rate, movement frequency, gene expression did not change to a significant degree), possibly indicating a high tolerance level in this species. This may allow yellow perch to utilize areas of moderate hypoxia to continue foraging while avoiding predators that may be more sensitive to moderately low oxygen.

Fluctuating water temperatures affect development, physiological responses and cause sex reversal in fathead minnows.

Natural and human activities can result in both high temporal and spatial variability in water temperature. Rapid temperature changes have the potential to dramatically affect physiological processes in aquatic organisms and, due to their limited mobility, fish early life stages are particularly vulnerable to ambient temperature fluctuations. In this study, we examined how the magnitude and frequency of temperature fluctuations affect survival, growth, development, expression of thermoresponsive genes, and gonadal differentiation in fathead minnows, Pimephales promelas. We exposed individuals (0 to 4 days post fertilization) of known genotypic sex to fluctuations of Δ4 °C over 12-h, Δ8 °C over 12- and 24-h, and three stable temperatures (21, 25, and 29 °C) for up to 45 d. Expression of hsp70 in fish exposed to the highest-magnitude, highest-frequency fluctuating treatment cycled in concert with temperature and was upregulated initially during exposure, and may have contributed to temperature fluctuations having little effect on time to and size at hatching (whole-organism responses). This treatment also caused fish to undergo nondirectional sex reversal. These results indicate that hsp70 may be involved in mediating thermal stress from subdaily temperature fluctuations and that sex determination in fathead minnows can be influenced by cycling temperatures.

Nearshore energy subsidies support Lake Michigan fishes and invertebrates following major changes in food web structure.

Aquatic food webs that incorporate multiple energy channels (e.g., nearshore benthic and pelagic) with varying productivity and turnover rates convey stability to biological communities by providing independent energy sources. Within the Lake Michigan food web, invasive dreissenid mussels have caused rapid changes to food web structure and potentially altered the channels through which consumers acquire energy. We used stable C and N isotopes to determine how Lake Michigan food web structure has changed in the past decade, coincident with the expansion of dreissenid mussels, decreased pelagic phytoplankton production, and increased nearshore benthic algal production. Fish and invertebrate samples collected from sites around Lake Michigan were analyzed to determine taxa-specific 13C:12C (delta13C) and 15N:14N (delta15N) ratios. Sampling took place during two distinct periods, 2002-2003 and 2010-2012, that spanned the period of dreissenid expansion, and included nearshore, pelagic and profundal fish and invertebrate taxa. The magnitude and direction of the delta13C shift indicated significantly greater reliance upon nearshore benthic energy sources among nearly all fish taxa as well as profundal invertebrates following dreissenid expansion. Although the mechanisms underlying this delta13C shift likely varied among species, possible causes include the transport of benthic algal production to offshore waters and increased feeding on nearshore prey items by pelagic and profundal species. delta15N shifts were more variable and of smaller magnitude across taxa, although declines in delta15N among some pelagic fishes suggest a shift to alternative prey resources. Lake Michigan fishes and invertebrates appear to have responded to dreissenid-induced changes in nutrient and energy pathways by switching from pelagic to alternative nearshore energy subsidies. Although large shifts in energy allocation (i.e., pelagic to nearshore benthic) resulting from invasive species appear to affect total production at upper trophic levels, changes in trophic structure and utilization of novel energy pathways may help to stabilize food webs following species invasions.

Microplastics impact simple aquatic food web dynamics through reduced zooplankton feeding and potentially releasing algae from consumer control.

Concentrations of microplastics in aquatic environments continue to rise due to industrial production and pollution. While there are various concerns regarding potential deleterious effects of microplastics on ecosystems, several knowledge gaps remain, including the potential for microplastics to directly and indirectly affect biotic interactions and food web dynamics. We explored the effects of environmentally relevant microplastic concentrations on two co-exposed species of herbaceous freshwater crustaceous zooplankton, filter feeding Daphnia dentifera and selective phytoplankton grazers Arctodiaptomus dorsalis. Study organisms were exposed to different concentrations of microplastics (plastic polyethylene microspheres; low = 2.38 × 10-8 mg/L, medium = 0.023 mg/L, high = 162 mg/L), phytoplankton prey, and predator cues, simulating a simple freshwater food web. Microplastic uptake was greater by D. dentifera, but both species were characterized by decreased algal consumption in the highest microplastic concentration treatment. Importantly, aqueous chlorophyll-a concentrations at the conclusion of the experiment were greater for the high microplastic treatment than all controls and other microplastic treatments. Finally, a predator effect was only apparent for D. dentifera, with greater microplastic uptake in the presence of a predator. We conclude that microplastics may adversely impact the ability of zooplankton to feed on algae and potentially release algae from consumptive control by herbivorous zooplankton. SYNOPSIS: This research aimed to better understand the broader food web effects of environmentally relevant microplastic concentrations on aquatic communities.

Dispersive currents explain patterns of population connectivity in an ecologically and economically important fish.

How to identify the drivers of population connectivity remains a fundamental question in ecology and evolution. Answering this question can be challenging in aquatic environments where dynamic lake and ocean currents coupled with high levels of dispersal and gene flow can decrease the utility of modern population genetic tools. To address this challenge, we used RAD-Seq to genotype 959 yellow perch (Perca flavescens), a species with an ~40-day pelagic larval duration (PLD), collected from 20 sites circumscribing Lake Michigan. We also developed a novel, integrative approach that couples detailed biophysical models with eco-genetic agent-based models to generate "predictive" values of genetic differentiation. By comparing predictive and empirical values of genetic differentiation, we estimated the relative contributions for known drivers of population connectivity (e.g., currents, behavior, PLD). For the main basin populations (i.e., the largest contiguous portion of the lake), we found that high gene flow led to low overall levels of genetic differentiation among populations (F ST = 0.003). By far the best predictors of genetic differentiation were connectivity matrices that were derived from periods of time when there were strong and highly dispersive currents. Thus, these highly dispersive currents are driving the patterns of population connectivity in the main basin. We also found that populations from the northern and southern main basin are slightly divergent from one another, while those from Green Bay and the main basin are highly divergent (F ST = 0.11). By integrating biophysical and eco-genetic models with genome-wide data, we illustrate that the drivers of population connectivity can be identified in high gene flow systems.

Yellow perch genetic structure and habitat use among connected habitats in eastern Lake Michigan.

Maintenance of genetic and phenotypic diversity is widely recognized as an important conservation priority, yet managers often lack basic information about spatial patterns of population structure and its relationship with habitat heterogeneity and species movement within it. To address this knowledge gap, we focused on the economically and ecologically prominent yellow perch (Perca flavescens). In the Lake Michigan basin, yellow perch reside in nearshore Lake Michigan, including drowned river mouths (DRMs)-protected, lake-like habitats that link tributaries to Lake Michigan. The goal of this study was to examine the extent that population structure is associated with Great Lakes connected habitats (i.e., DRMs) in a mobile fish species using yellow perch as a model. Specifically, we tested whether DRMs and eastern Lake Michigan constitute distinct genetic stocks of yellow perch, and if so, whether those stocks migrate between the two connected habitats throughout the year. To do so, we genotyped yellow perch at 14 microsatellite loci collected from 10 DRMs in both deep and littoral habitats during spring, summer, and autumn and two nearshore sites in Lake Michigan (spring and autumn) during 2015-2016 and supplemented our sampling with fish collected in 2013. We found that yellow perch from littoral-DRM habitats were genetically distinct from fish captured in nearshore Lake Michigan. Our data also suggested that Lake Michigan yellow perch likely use deep-DRM habitats during autumn. Further, we found genetic structuring among DRMs. These patterns support hypotheses of fishery managers that yellow perch seasonally migrate to and from Lake Michigan, yet, interestingly, these fish do not appear to interbreed with littoral fish despite occupying the same DRM. We recommend that fisheries managers account for this complex population structure and movement when setting fishing regulations and assessing the effects of harvest in Lake Michigan.

No evidence of microplastic impacts on consumption or growth of larval Pimephales promelas.

Microplastics are an abundant pollutant in aquatic systems, but little is known regarding their effects on larval fish. We conducted foraging and growth experiments to observe how increasing densities of microplastics (polyethylene microspheres) impact the foraging and growth of Pimephales promelas larvae. We found minimal impacts on larval consumption of Artemia nauplii in the consumption study, as well as little impact on total length after 30 d of the growth experiment. Environ Toxicol Chem 2018;37:2912-2918. © 2018 SETAC.

A meta-analysis of the effects of exposure to microplastics on fish and aquatic invertebrates.

Microplastics are present in aquatic ecosystems the world over and may influence the feeding, growth, reproduction, and survival of freshwater and marine biota; however, the extent and magnitude of potential effects of microplastics on aquatic organisms is poorly understood. In the current study, we conducted a meta-analysis of published literature to examine impacts of exposure to microplastics on consumption (and feeding), growth, reproduction, and survival of fish and aquatic invertebrates. While we did observe within-taxa negative effects for all four categories of responses, many of the effects summarized in our study were neutral, indicating that the effects of exposure to microplastics are highly variable across taxa. The most consistent effect was a reduction in consumption of natural prey when microplastics were present. For some taxa, negative effects on growth, reproduction and even survival were also evident. Organisms that serve as prey to larger predators, e.g., zooplankton, may be particularly susceptible to negative impacts of exposure to microplastic pollution, with potential for ramifications throughout the food web. Future work should focus on whether microplastics may be affecting aquatic organisms more subtly, e.g., by influencing exposure to contaminants and pathogens, or by acting at a molecular level.

Species identity matters when interpreting trophic markers in aquatic food webs.

In aquatic systems, food web linkages are often assessed using diet contents, stable isotope ratios, and, increasingly, fatty acid composition of organisms. Some correlations between different trophic metrics are assumed to be well-supported; for example, particular stable isotope ratios and fatty acids seem to reflect reliance on benthic or pelagic energy pathways. However, understanding whether the assumed correlations between different trophic metrics are coherent and consistent across species represents a key step toward their effective use in food web studies. To assess links among trophic markers, we compared relationships between major diet components, fatty acids, and stable isotope ratios in three fishes: yellow perch (Perca flavescens), round goby (Neogobius melanostomus), and spottail shiner (Notropis hudsonius) collected from nearshore Lake Michigan. Yellow perch and spottail shiner are native in this system, while round goby are a relatively recent invader. We found some evidence for agreement between different trophic metrics, especially between diet components, n-3:n-6 fatty acid ratios, and stable isotope ratios (δ13C and δ15N). However, we also observed significant variation in observed relationships among markers and species, potentially due to taxonomic variation in the specific diet items consumed (e.g., chydorid microcrustaceans and Dreissena mussels) and species-specific biochemical processes. In many of these latter cases, the invasive species differed from the native species. Understanding the effects of taxonomic variation on prey and predator signatures could significantly improve the usefulness of fatty acids in food web studies, whereas diet contents and stable isotopes appear to be reliable indicators of trophic niche in aquatic food webs.

Performance Benchmarks for Scholarly Metrics Associated with Fisheries and Wildlife Faculty.

Research productivity and impact are often considered in professional evaluations of academics, and performance metrics based on publications and citations increasingly are used in such evaluations. To promote evidence-based and informed use of these metrics, we collected publication and citation data for 437 tenure-track faculty members at 33 research-extensive universities in the United States belonging to the National Association of University Fisheries and Wildlife Programs. For each faculty member, we computed 8 commonly used performance metrics based on numbers of publications and citations, and recorded covariates including academic age (time since Ph.D.), sex, percentage of appointment devoted to research, and the sub-disciplinary research focus. Standardized deviance residuals from regression models were used to compare faculty after accounting for variation in performance due to these covariates. We also aggregated residuals to enable comparison across universities. Finally, we tested for temporal trends in citation practices to assess whether the "law of constant ratios", used to enable comparison of performance metrics between disciplines that differ in citation and publication practices, applied to fisheries and wildlife sub-disciplines when mapped to Web of Science Journal Citation Report categories. Our regression models reduced deviance by » to ½. Standardized residuals for each faculty member, when combined across metrics as a simple average or weighted via factor analysis, produced similar results in terms of performance based on percentile rankings. Significant variation was observed in scholarly performance across universities, after accounting for the influence of covariates. In contrast to findings for other disciplines, normalized citation ratios for fisheries and wildlife sub-disciplines increased across years. Increases were comparable for all sub-disciplines except ecology. We discuss the advantages and limitations of our methods, illustrate their use when applied to new data, and suggest future improvements. Our benchmarking approach may provide a useful tool to augment detailed, qualitative assessment of performance.

The re-eutrophication of Lake Erie: Harmful algal blooms and hypoxia.

Lake Erie supplies drinking water to more than 11 million consumers, processes millions of gallons of wastewater, provides important species habitat and supports a substantial industrial sector, with >$50 billion annual income to tourism, recreational boating, shipping, fisheries, and other industries. These and other key ecosystem services are currently threatened by an excess supply of nutrients, manifested in particular by increases in the magnitude and extent of harmful planktonic and benthic algal blooms (HABs) and hypoxia. Widespread concern for this important international waterbody has been manifested in a strong focus of scientific and public material on the subject, and commitments for Canada-US remedial actions in recent agreements among Federal, Provincial and State agencies. This review provides a retrospective synthesis of past and current nutrient inputs, impairments by planktonic and benthic HABs and hypoxia, modelling and Best Management Practices in the Lake Erie basin. The results demonstrate that phosphorus reduction is of primary importance, but the effects of climate, nitrogen and other factors should also be considered in the context of adaptive management. Actions to reduce nutrient levels by targeted Best Management Practices will likely need to be tailored for soil types, topography, and farming practices.

Rapidly shifting maturation schedules following reduced commercial harvest in a freshwater fish.

Size-selective harvest of fish stocks can lead to maturation at smaller sizes and younger ages, which may depress stock productivity and recovery. Such changes in maturation may be very slow to reverse, even following complete fisheries closures. We evaluated temporal trends in maturation of five Great Lakes stocks of yellow perch (Perca flavescens Mitchill) using indices that attempt to disentangle plastic and evolutionary changes in maturation: age at 50% maturity and probabilistic maturation reaction norms (PMRNs). Four populations were fished commercially throughout the time series, while the Lake Michigan fishery was closed following a stock collapse. We documented rapid increases in PMRNs of the Lake Michigan stock coincident with the commercial fishery closure. Saginaw Bay and Lake Huron PMRNs also increased following reduced harvest, while Lake Erie populations were continuously fished and showed little change. The rapid response of maturation may have been enhanced by the short generation time of yellow perch and potential gene flow between northern and southern Lake Michigan, in addition to potential reverse adaptation following the fishing moratorium. These results suggest that some fish stocks may retain the ability to recover from fisheries-induced life history shifts following fishing moratoria.

Elucidating causes of Diporeia decline in the Great Lakes via metabolomics: physiological responses after exposure to different stressors.

The benthic macroinvertebrate Diporeia spp. have been extirpated from many areas of the Laurentian Great Lakes, but the mechanisms underlying such declines are not fully understood. Diporeia declines coinciding with the invasion of exotic dreissenid mussels (zebra and quagga) have led to the hypothesis that Diporeia declines are a result of decreased food availability from increasing competition with dreissenids for diatoms. There is additional evidence that Diporeia are negatively affected when in close proximity to dreissenids, probably because of exposure to toxins present in the mussels' pseudofeces. Diporeia are also known to be sensitive to anthropogenic contaminants (such as polychlorinated biphenyls [PCBs]) present in Great Lakes sediments. To better understand the physiological responses of Diporeia to diverse stressors, we conducted three 28-d experiments evaluating changes in the metabolomes of Diporeia (1) fed diatoms (Cyclotella meneghiniana) versus starved, (2) exposed (from Lake Michigan and Cayuga Lake) to quagga mussels (Dreissena bugensis), and (3) exposed to sediments contaminated with PCBs. The metabolomes of samples were examined using both two-dimensional gas and liquid chromatography coupled with mass spectrometry. Each stressor elicited a unique metabolome response characterized by enhanced citric acid cycle, fatty acid biosynthesis, and protein metabolism in diatom-fed Diporeia; impaired glycolysis, protein catabolism, and folate metabolism in Diporeia from Lake Michigan irrespective of quagga mussel exposure, suggesting lake-specific adaptation mechanisms; and altered cysteine and phospholipid metabolism during PCB exposure. Subsequent comparisons of these stressor-specific metabolic responses with metabolomes of a feral Diporeia population would help identify stressors affecting Diporeia populations throughout the Great Lakes.

Starvation causes disturbance in amino acid and fatty acid metabolism in Diporeia.

The benthic amphipod Diporeia spp. was once the predominant macroinvertebrate in deep, offshore regions of the Laurentian Great Lakes. However, since the early 1990s, Diporeia populations have steadily declined across the area. It has been hypothesized that this decline is due to starvation from increasing competition for food with invasive dreissenid mussels. In order to gain a better understanding of the changes in Diporeia physiology during starvation, we applied two-dimensional gas chromatography coupled with time of flight mass spectrometry (GCXGC/TOF-MS) for investigating the responses in Diporeia metabolome during starvation. We starved Diporeia for 60 days and collected five organisms every 12 days for metabolome analyses. Upon arrival to the laboratory, organisms were flash frozen and served as control (day 0). We observed an increase in lipid oxidation and protein catabolism with subsequent declines of essential amino acids (proline, glutamine, and phenylalanine), down-regulation of glycerophospholipid and sphingolipid metabolism, and decreased polyunsaturated fatty acid abundance in nutritionally stressed Diporeia. Abundance of 1-Iodo-2-methylundecane, a metabolite closely related to insect pheromones, also declined with starvation. This research has further substantiated the applicability of GCXGC/TOF-MS as a research tool in the field of environmental metabolomics. The next step is to apply this new knowledge for evaluating nutritional status of feral Diporeia to elucidate the underlying cause(s) responsible for their decline in the Great Lakes.

Eco-genetic model to explore fishing-induced ecological and evolutionary effects on growth and maturation schedules.

Eco-genetic individual-based models involve tracking the ecological dynamics of simulated individual organisms that are in part characterized by heritable parameters. We developed an eco-genetic individual-based model to explore ecological and evolutionary interactions of fish growth and maturation schedules. Our model is flexible and allows for exploration of the effects of heritable growth rates (based on von Bertalanffy and biphasic growth patterns), heritable maturation schedules (based on maturation reaction norm concepts), or both on individual- and population-level traits. In baseline simulations with rather simple ecological trade-offs and over a relatively short time period (<200 simulation years), simulated male and female fish evolve differential genetic growth and maturation. Further, resulting patterns of genetically determined growth and maturation are influenced by mortality rate and density-dependent processes, and maturation and growth parameters interact to mediate the evolution of one another. Subsequent to baseline simulations, we conducted experimental simulations to mimic fisheries harvest with two size-limits (targeting large or small fish), an array of fishing mortality rates, and assuming a deterministic or stochastic environment. Our results suggest that fishing with either size-limit may induce considerable changes in life-history trait expression (maturation schedules and growth rates), recruitment, and population abundance and structure. However, targeting large fish would cause more adverse genetic effects and may lead to a population less resilient to environmental stochasticity.