Spatiotemporal segregation by migratory phenotype indicates potential for assortative mating in lake sturgeon.

Migratory diversity can promote population differentiation if sympatric phenotypes become temporally, spatially, or behaviorally segregated during breeding. In this study, the potential for spatiotemporal segregation was tested among three migratory phenotypes of lake sturgeon (Acipenser fulvescens) that spawn in the St. Clair River of North America's Laurentian Great Lakes but differ in how often they migrate into the river and in which direction they move after spawning. Acoustic telemetry over 9 years monitored use of two major spawning sites by lake sturgeon that moved north to overwinter in Lake Huron or south to overwinter in Lake St. Clair. Lake St. Clair migrants were further distinguished by whether they migrated into the St. Clair River each year (annual migrants) or intermittently (intermittent migrants). Social network analyses indicated lake sturgeon generally co-occurred with individuals of the same migratory phenotype more often than with different migratory phenotypes. A direct test for differences in space use revealed one site was almost exclusively visited by Lake St. Clair migrants whereas the other site was visited by Lake Huron migrants, intermittent Lake St. Clair migrants, and, to a lesser extent, annual Lake St. Clair migrants. Analysis of arrival and departure dates indicated opportunity for co-occurrence at the site visited by all phenotypes but showed Lake Huron migrants arrived approximately 2 weeks before Lake St. Clair migrants. Taken together, our results indicated partial spatiotemporal segregation of migratory phenotypes that may generate assortative mating and promote population differentiation.

Small-scale intraspecific patterns of adaptive immunogenetic polymorphisms and neutral variation in Lake Superior lake trout.

Many fishes express high levels of intraspecific variability, often linked to resource partitioning. Several studies show that a species' evolutionary trajectory of adaptive divergence can undergo reversals caused by changes in its environment. Such a reversal in neutral genetic and morphological variation among lake trout Salvelinus namaycush ecomorphs appears to be underway in Lake Superior. However, a water depth gradient in neutral genetic divergence was found to be associated with intraspecific diversity in the lake. To investigate patterns of adaptive immunogenetic variation among lake trout ecomorphs, we used Illumina high-throughput sequencing. The population's genetic structure of the major histocompatibility complex (MHC Class IIß exon 2) and 18 microsatellite loci were compared to disentangle neutral and selective processes at a small geographic scale. Both MHC and microsatellite variation were partitioned more by water depth stratum than by ecomorph. Several metrics showed strong clustering by water depth in MHC alleles, but not microsatellites. We report a 75% increase in the number of MHC alleles shared between the predominant shallow and deep water ecomorphs since a previous lake trout MHC study at the same locale (c. 1990s data). This result is consistent with the reverse speciation hypothesis, although adaptive MHC polymorphisms persist along an ecological gradient. Finally, results suggested that the lake trout have multiple copies of the MHC II locus consistent with a historic genomic duplication event. Our findings indicated that conservation approaches for this species could focus on managing various ecological habitats by depth, in addition to regulating the fisheries specific to ecomorphs.

Divergent migration within lake sturgeon (Acipenser fulvescens) populations: Multiple distinct patterns exist across an unrestricted migration corridor.

Population structure, distribution, abundance and dispersal arguably underpin the entire field of animal ecology, with consequences for regional species persistence, and provision of ecosystem services. Divergent migration behaviours among individuals or among populations are an important aspect of the ecology of highly mobile animals, allowing populations to exploit spatially or temporally distributed food and space resources. This study investigated the spatial ecology of lake sturgeon (Acipenser fulvescens) within the barrier free Huron-Erie Corridor (HEC), which connects Lake Huron and Lake Erie of the North American Laurentian Great Lakes. Over 6 years (2011-2016), movements of 268 lake sturgeon in the HEC were continuously monitored across the Great Lakes using acoustic telemetry (10 years battery life acoustic transmitters). Five distinct migration behaviours were identified with hierarchical cluster analysis, based on the phenology and duration of river and lake use. Lake sturgeon in the HEC were found to contain a high level of intraspecific divergent migration, including partial migration with the existence of residents. Specific behaviours included year-round river residency and multiple lake-migrant behaviours that involved movements between lakes and rivers. Over 85% of individuals were assigned to migration behaviours as movements were consistently repeated over the study, which suggested migration behaviours were consistent and persistent in lake sturgeon. Differential use of specific rivers or lakes by acoustic-tagged lake sturgeon further subdivided individuals into 14 "contingents" (spatiotemporally segregated subgroups). Contingents associated with one river (Detroit or St. Clair) were rarely detected in the other river, which confirmed that lake sturgeon in the Detroit and St. Clair represent two semi-independent populations that could require separate management consideration for their conservation. The distribution of migration behaviours did not vary between populations, sexes, body size or among release locations, which indicated that intrapopulation variability in migratory behaviour is a general feature of the spatial ecology of lake sturgeon in unfragmented landscapes.

Genetic and phenotypic variation along an ecological gradient in lake trout Salvelinus namaycush.

BACKGROUND: Adaptive radiation involving a colonizing phenotype that rapidly evolves into at least one other ecological variant, or ecotype, has been observed in a variety of freshwater fishes in post-glacial environments. However, few studies consider how phenotypic traits vary with regard to neutral genetic partitioning along ecological gradients. Here, we present the first detailed investigation of lake trout Salvelinus namaycush that considers variation as a cline rather than discriminatory among ecotypes. Genetic and phenotypic traits organized along common ecological gradients of water depth and geographic distance provide important insights into diversification processes in a lake with high levels of human disturbance from over-fishing. RESULTS: Four putative lake trout ecotypes could not be distinguished using population genetic methods, despite morphological differences. Neutral genetic partitioning in lake trout was stronger along a gradient of water depth, than by locality or ecotype. Contemporary genetic migration patterns were consistent with isolation-by-depth. Historical gene flow patterns indicated colonization from shallow to deep water. Comparison of phenotypic (Pst) and neutral genetic variation (Fst) revealed that morphological traits related to swimming performance (e.g., buoyancy, pelvic fin length) departed more strongly from neutral expectations along a depth gradient than craniofacial feeding traits. Elevated phenotypic variance with increasing water depth in pelvic fin length indicated possible ongoing character release and diversification. Finally, differences in early growth rate and asymptotic fish length across depth strata may be associated with limiting factors attributable to cold deep-water environments. CONCLUSION: We provide evidence of reductions in gene flow and divergent natural selection associated with water depth in Lake Superior. Such information is relevant for documenting intraspecific biodiversity in the largest freshwater lake in the world for a species that recently lost considerable genetic diversity and is now in recovery. Unknown is whether observed patterns are a result of an early stage of incipient speciation, gene flow-selection equilibrium, or reverse speciation causing formerly divergent ecotypes to collapse into a single gene pool.

Evaluating harvest-based control of invasive fish with telemetry: performance of sea lamprey traps in the Great Lakes.

Physical removal (e.g., harvest via traps or nets) of mature individuals may be a cost-effective or socially acceptable alternative to chemical control strategies for invasive species, but requires knowledge of the spatial distribution of a population over time. We used acoustic telemetry to determine the current and possible future role of traps to control and assess invasive sea lampreys, Petromyzon marinus, in the St. Marys River, the connecting channel between Lake Superior and Lake Huron. Exploitation rates (i.e., fractions of an adult sea lamprey population removed by traps) at two upstream locations were compared among three years and two points of entry to the system. Telemetry receivers throughout the drainage allowed trap performance (exploitation rate) to be partitioned into two components: proportion of migrating sea lampreys that visited trap sites (availability) and proportion of available sea lampreys that were caught by traps (local trap efficiency). Estimated exploitation rates were well below those needed to provide population control in the absence of lampricides and were limited by availability and local trap efficiency. Local trap efficiency estimates for acoustic-tagged sea lampreys were lower than analogous estimates regularly obtained using traditional mark-recapture methods, suggesting that abundance had been previously underestimated. Results suggested major changes would be required to substantially increase catch, including improvements to existing traps, installation of new traps, or other modifications to attract and retain more sea lampreys. This case study also shows how bias associated with telemetry tags can be estimated and incorporated in models to improve inferences about parameters that are directly relevant to fishery management.

A moving target--incorporating knowledge of the spatial ecology of fish into the assessment and management of freshwater fish populations.

Freshwater fish move vertically and horizontally through the aquatic landscape for a variety of reasons, such as to find and exploit patchy resources or to locate essential habitats (e.g., for spawning). Inherent challenges exist with the assessment of fish populations because they are moving targets. We submit that quantifying and describing the spatial ecology of fish and their habitat is an important component of freshwater fishery assessment and management. With a growing number of tools available for studying the spatial ecology of fishes (e.g., telemetry, population genetics, hydroacoustics, otolith microchemistry, stable isotope analysis), new knowledge can now be generated and incorporated into biological assessment and fishery management. For example, knowing when, where, and how to deploy assessment gears is essential to inform, refine, or calibrate assessment protocols. Such information is also useful for quantifying or avoiding bycatch of imperiled species. Knowledge of habitat connectivity and usage can identify critically important migration corridors and habitats and can be used to improve our understanding of variables that influence spatial structuring of fish populations. Similarly, demographic processes are partly driven by the behavior of fish and mediated by environmental drivers. Information on these processes is critical to the development and application of realistic population dynamics models. Collectively, biological assessment, when informed by knowledge of spatial ecology, can provide managers with the ability to understand how and when fish and their habitats may be exposed to different threats. Naturally, this knowledge helps to better evaluate or develop strategies to protect the long-term viability of fishery production. Failure to understand the spatial ecology of fishes and to incorporate spatiotemporal data can bias population assessments and forecasts and potentially lead to ineffective or counterproductive management actions.

Seasonal thermal ecology of adult walleye (Sander vitreus) in Lake Huron and Lake Erie.

The purpose of this study was to characterize thermal patterns and generate occupancy models for adult walleye from lakes Erie and Huron with internally implanted biologgers coupled with a telemetry study to assess the effects of sex, fish size, diel periods, and lake. Sex, size, and diel periods had no effect on thermal occupancy of adult walleye in either lake. Thermal occupancy differed between lakes and seasons. Walleye from Lake Erie generally experienced higher temperatures throughout the spring and summer months than did walleye in Lake Huron, due to limnological differences between the lakes. Tagged walleye that remained in Saginaw Bay, Lake Huron (i.e., adjacent to the release location), as opposed to those migrating to the main basin of Lake Huron, experienced higher temperatures, and thus accumulated more thermal units (the amount of temperature units amassed over time) throughout the year. Walleye that migrated toward the southern end of Lake Huron occupied higher temperatures than those that moved toward the north. Consequently, walleye that emigrated from Saginaw Bay experienced thermal environments that were more favorable for growth as they spent more time within their thermal optimas than those that remained in Saginaw Bay. Results presented in this paper provide information on the thermal experience of wild fish in a large lake, and could be used to refine sex- and lake-specific bioenergetics models of walleye in the Great Lakes to enable the testing of ecological hypotheses.

Temporal instability of lake charr phenotypes: Synchronicity of growth rates and morphology linked to environmental variables?

Pathways through which phenotypic variation among individuals arise can be complex. One assumption often made in relation to intraspecific diversity is that the stability or predictability of the environment will interact with expression of the underlying phenotypic variation. To address biological complexity below the species level, we investigated variability across years in morphology and annual growth increments between and within two sympatric lake charr Salvelinus namaycush ecotypes in Rush Lake, USA. A rapid phenotypic shift in body and head shape was found within a decade. The magnitude and direction of the observed phenotypic change were consistent in both ecotypes, which suggests similar pathways caused the variation over time. Over the same time period, annual growth increments declined for both lake charr ecotypes and corresponded with a consistent phenotypic shift of each ecotype. Despite ecotype-specific annual growth changes in response to winter conditions, the observed annual growth shift for both ecotypes was linked, to some degree, with variation in the environment. Particularly, a declining trend in regional cloud cover was associated with an increase of early-stage (ages 1-3) annual growth for lake charr of Rush Lake. Underlying mechanisms causing changes in growth rates and constrained morphological modulation are not fully understood. An improved knowledge of the biology hidden within the expression of phenotypic variation promises to clarify our understanding of temporal morphological diversity and instability.

Among-individual diet variation within a lake trout ecotype: Lack of stability of niche use.

In a polyphenic species, differences in resource use are expected among ecotypes, and homogeneity in resource use is expected within an ecotype. Yet, using a broad resource spectrum has been identified as a strategy for fishes living in unproductive northern environments, where food is patchily distributed and ephemeral. We investigated whether specialization of trophic resources by individuals occurred within the generalist piscivore ecotype of lake trout from Great Bear Lake, Canada, reflective of a form of diversity. Four distinct dietary patterns of resource use within this lake trout ecotype were detected from fatty acid composition, with some variation linked to spatial patterns within Great Bear Lake. Feeding habits of different groups within the ecotype were not associated with detectable morphological or genetic differentiation, suggesting that behavioral plasticity caused the trophic differences. A low level of genetic differentiation was detected between exceptionally large-sized individuals and other piscivore individuals. We demonstrated that individual trophic specialization can occur within an ecotype inhabiting a geologically young system (8,000-10,000 yr BP), a lake that sustains high levels of phenotypic diversity of lake trout overall. The characterization of niche use among individuals, as done in this study, is necessary to understand the role that individual variation can play at the beginning of differentiation processes.

From top to bottom: Do Lake Trout diversify along a depth gradient in Great Bear Lake, NT, Canada?

Depth is usually considered the main driver of Lake Trout intraspecific diversity across lakes in North America. Given that Great Bear Lake is one of the largest and deepest freshwater systems in North America, we predicted that Lake Trout intraspecific diversity to be organized along a depth axis within this system. Thus, we investigated whether a deep-water morph of Lake Trout co-existed with four shallow-water morphs previously described in Great Bear Lake. Morphology, neutral genetic variation, isotopic niches, and life-history traits of Lake Trout across depths (0-150 m) were compared among morphs. Due to the propensity of Lake Trout with high levels of morphological diversity to occupy multiple habitat niches, a novel multivariate grouping method using a suite of composite variables was applied in addition to two other commonly used grouping methods to classify individuals. Depth alone did not explain Lake Trout diversity in Great Bear Lake; a distinct fifth deep-water morph was not found. Rather, Lake Trout diversity followed an ecological continuum, with some evidence for adaptation to local conditions in deep-water habitat. Overall, trout caught from deep-water showed low levels of genetic and phenotypic differentiation from shallow-water trout, and displayed higher lipid content (C:N ratio) and occupied a higher trophic level that suggested an potential increase of piscivory (including cannibalism) than the previously described four morphs. Why phenotypic divergence between shallow- and deep-water Lake Trout was low is unknown, especially when the potential for phenotypic variation should be high in deep and large Great Bear Lake. Given that variation in complexity of freshwater environments has dramatic consequences for divergence, variation in the complexity in Great Bear Lake (i.e., shallow being more complex than deep), may explain the observed dichotomy in the expression of intraspecific phenotypic diversity between shallow- vs. deep-water habitats. The ambiguity surrounding mechanisms driving divergence of Lake Trout in Great Bear Lake should be seen as reflective of the highly variable nature of ecological opportunity and divergent natural selection itself.

A hidden Markov movement model for rapidly identifying behavioral states from animal tracks.

Electronic telemetry is frequently used to document animal movement through time. Methods that can identify underlying behaviors driving specific movement patterns can help us understand how and why animals use available space, thereby aiding conservation and management efforts. For aquatic animal tracking data with significant measurement error, a Bayesian state-space model called the first-Difference Correlated Random Walk with Switching (DCRWS) has often been used for this purpose. However, for aquatic animals, highly accurate tracking data are now becoming more common. We developed a new hidden Markov model (HMM) for identifying behavioral states from animal tracks with negligible error, called the hidden Markov movement model (HMMM). We implemented as the basis for the HMMM the process equation of the DCRWS, but we used the method of maximum likelihood and the R package TMB for rapid model fitting. The HMMM was compared to a modified version of the DCRWS for highly accurate tracks, the DCRWSNOME, and to a common HMM for animal tracks fitted with the R package moveHMM. We show that the HMMM is both accurate and suitable for multiple species by fitting it to real tracks from a grey seal, lake trout, and blue shark, as well as to simulated data. The HMMM is a fast and reliable tool for making meaningful inference from animal movement data that is ideally suited for ecologists who want to use the popular DCRWS implementation and have highly accurate tracking data. It additionally provides a groundwork for development of more complex modeling of animal movement with TMB. To facilitate its uptake, we make it available through the R package swim.

Temporal constraints on the potential role of fry odors as cues of past reproductive success for spawning lake trout.

Deciding where to reproduce is a major challenge for most animals. Many select habitats based upon cues of successful reproduction by conspecifics, such as the presence of offspring from past reproductive events. For example, some fishes select spawning habitat following odors released by juveniles whose rearing habitat overlaps with spawning habitat. However, juveniles may emigrate before adults begin to search for spawning habitat; hence, the efficacy of juvenile cues could be constrained by degradation or dissipation rates. In lake trout (Salvelinus namaycush), odors deposited by the previous year's offspring have been hypothesized to guide adults to spawning reefs. However, in most extant populations, lake trout fry emigrate from spawning reefs during the spring and adults spawn during the fall. Therefore, we postulated that the role of fry odors in guiding habitat selection might be constrained by the time between fry emigration and adult spawning. Time course chemical, physiological, and behavioral assays indicated that the odors deposited by fry likely degrade or dissipate before adults select spawning habitats. Furthermore, fry feces did not attract wild lake trout to constructed spawning reefs in Lake Huron. Taken together, our results indicate fry odors are unlikely to act as cues for lake trout searching for spawning reefs in populations whose juveniles emigrate before the spawning season, and underscore the importance of environmental constraints on social cues.

Use of navigation channels by Lake Sturgeon: Does channelization increase vulnerability of fish to ship strikes?

Channelization for navigation and flood control has altered the hydrology and bathymetry of many large rivers with unknown consequences for fish species that undergo riverine migrations. In this study, we investigated whether altered flow distributions and bathymetry associated with channelization attracted migrating Lake Sturgeon (Acipenser fulvescens) into commercial navigation channels, potentially increasing their exposure to ship strikes. To address this question, we quantified and compared Lake Sturgeon selection for navigation channels vs. alternative pathways in two multi-channel rivers differentially affected by channelization, but free of barriers to sturgeon movement. Acoustic telemetry was used to quantify Lake Sturgeon movements. Under the assumption that Lake Sturgeon navigate by following primary flow paths, acoustic-tagged Lake Sturgeon in the more-channelized lower Detroit River were expected to choose navigation channels over alternative pathways and to exhibit greater selection for navigation channels than conspecifics in the less-channelized lower St. Clair River. Consistent with these predictions, acoustic-tagged Lake Sturgeon in the more-channelized lower Detroit River selected the higher-flow and deeper navigation channels over alternative migration pathways, whereas in the less-channelized lower St. Clair River, individuals primarily used pathways alternative to navigation channels. Lake Sturgeon selection for navigation channels as migratory pathways also was significantly higher in the more-channelized lower Detroit River than in the less-channelized lower St. Clair River. We speculated that use of navigation channels over alternative pathways would increase the spatial overlap of commercial vessels and migrating Lake Sturgeon, potentially enhancing their vulnerability to ship strikes. Results of our study thus demonstrated an association between channelization and the path use of migrating Lake Sturgeon that could prove important for predicting sturgeon-vessel interactions in navigable rivers as well as for understanding how fish interact with their habitat in landscapes altered by human activity.

Multiple generalist morphs of Lake Trout: Avoiding constraints on the evolution of intraspecific divergence?

A generalist strategy, as an adaptation to environmental heterogeneity, is common in Arctic freshwater systems, often accompanied, however, by intraspecific divergence that promotes specialization in niche use. To better understand how resources may be partitioned in a northern system that supports intraspecific diversity of Lake Trout, trophic niches were compared among four shallow-water morphotypes in Great Bear Lake (N65° 56' 39″, W120° 50' 59″). Bayesian mixing model analyses of stable isotopes of carbon and nitrogen were conducted on adult Lake Trout. Major niche overlap in resource use among four Lake Trout morphotypes was found within littoral and pelagic zones, which raises the question of how such polymorphism can be sustained among opportunistic generalist morphotypes. Covariances of our morphological datasets were tested against δ13C and δ15N values. Patterns among morphotypes were mainly observed for δ15N. This link between ecological and morphological differentiation suggested that selection pressure(s) operate at the trophic level (δ15N), independent of habitat, rather than along the habitat-foraging opportunity axis (δ13C). The spatial and temporal variability of resources in Arctic lakes, such as Great Bear Lake, may have favored the presence of multiple generalists showing different degrees of omnivory along a weak benthic-pelagic gradient. Morphs 1-3 had more generalist feeding habits using both benthic and pelagic habitats than Morph 4, which was a top-predator specialist in the pelagic habitat. Evidence for frequent cannibalism in Great Bear Lake was found across all four morphotypes and may also contribute to polymorphism. We suggest that the multiple generalist morphs described here from Great Bear Lake are a unique expression of diversity due to the presumed constraints on the evolution of generalists and contrast with the development of multiple specialists, the standard response to intraspecific divergence.

Acoustic telemetry reveals large-scale migration patterns of walleye in Lake Huron.

Fish migration in large freshwater lacustrine systems such as the Laurentian Great Lakes is not well understood. The walleye (Sander vitreus) is an economically and ecologically important native fish species throughout the Great Lakes. In Lake Huron walleye has recently undergone a population expansion as a result of recovery of the primary stock, stemming from changing food web dynamics. During 2011 and 2012, we used acoustic telemetry to document the timing and spatial scale of walleye migration in Lake Huron and Saginaw Bay. Spawning walleye (n = 199) collected from a tributary of Saginaw Bay were implanted with acoustic tags and their migrations were documented using acoustic receivers (n = 140) deployed throughout U.S. nearshore waters of Lake Huron. Three migration pathways were described using multistate mark-recapture models. Models were evaluated using the Akaike Information Criterion. Fish sex did not influence migratory behavior but did affect migration rate and walleye were detected on all acoustic receiver lines. Most (95%) tagged fish migrated downstream from the riverine tagging and release location to Saginaw Bay, and 37% of these fish emigrated from Saginaw Bay into Lake Huron. Remarkably, 8% of walleye that emigrated from Saginaw Bay were detected at the acoustic receiver line located farthest from the release location more than 350 km away. Most (64%) walleye returned to the Saginaw River in 2012, presumably for spawning. Our findings reveal that fish from this stock use virtually the entirety of U.S. nearshore waters of Lake Huron.