Assessing conservation status with extensive but low-resolution data: Application of frequentist and Bayesian models to endangered Athabasca River rainbow trout.

Use of extensive but low-resolution abundance data is common in the assessment of species at-risk status based on quantitative decline criteria under International Union for Conservation of Nature (IUCN) and national endangered species legislation. Such data can be problematic for 3 reasons. First, statistical power to reject the null hypothesis of no change is often low because of small sample size and high sampling uncertainty leading to a high frequency of type II errors. Second, range-wide assessments composed of multiple site-specific observations do not effectively weight site-specific trends into global trends. Third, uncertainty in site-specific temporal trends and relative abundance are not propagated at the appropriate spatial scale. A common result is the propensity to underestimate the magnitude of declines and therefore fail to identify the appropriate at-risk status for a species. We used 3 statistical approaches, from simple to more complex, to estimate temporal decline rates for a designatable unit (DU) of rainbow trout in the Athabasca River watershed in western Canada. This DU is considered a native species for purposes of listing because of its genetic composition characterized as >0.95 indigenous origin in the face of continuing introgressive hybridization with introduced populations in the watershed. Analysis of abundance trends from 57 time series with a fixed-effects model identified 33 sites with negative trends, but only 2 were statistically significant. By contrast, a hierarchical linear mixed model weighted by site-specific abundance provided a DU-wide decline estimate of 16.4% per year and a 3-generation decline of 93.2%. A hierarchical Bayesian mixed model yielded a similar 3-generation decline trend of 91.3% and the posterior distribution showed that the estimate had a >99% probability of exceeding thresholds for an endangered listing. We conclude that the Bayesian approach was the most useful because it provided a probabilistic statement of threshold exceedance in support of an at-risk status recommendation.

El uso de datos extensivos, pero de baja resolución, de la abundancia es una práctica común en la evaluación del estado de riesgo de una especie con base en los criterios cuantitativos de declinación establecidos por la Unión Internacional para la Conservación de la Naturaleza (UICN) y la legislación nacional sobre especies en peligro extinción. Dicha información puede ser problemática por tres razones: primero, el poder estadístico para rechazar la hipótesis nula de ningún cambio es frecuentemente bajo debido a un tamaño pequeño de la muestra y a la elevada incertidumbre del muestreo, lo que resulta en una frecuencia elevada de errores de tipo II; segundo, las evaluaciones de amplia variedad compuestas de varias observaciones específicas de sitio no sopesan efectivamente las tendencias específicas de sitio dentro de las tendencias globales; y tercero, la incertidumbre en las tendencias temporales específicas de sitio y en la abundancia relativa no se propagan a la escala espacial apropiada. Un resultado común del uso de esta información es la propensión a subestimar la magnitud de las declinaciones, y por lo tanto equivocarse en la identificación del estado de riesgo apropiado para la especie. Usamos tres estrategias estadísticas, de simples a más complejas, para estimar las tasas de declinación temporal para una unidad designable (UD) de trucha arcoíris en la cuenca del río Athabasca al oeste de Canadá. Esta UD es considerada una especie nativa por razones de listado debido a su composición genética, caracterizada como >0-95 de origen nativo de frente a la continua hibridación introgresiva con poblaciones introducidas a la cuenca. El análisis de las tendencias de abundancia de 57 series de tiempo con un modelo de efectos fijos identificó 33 sitios con tendencias negativas, pero sólo dos fueron estadísticamente significativas. En contraste, un modelo lineal mixto de jerarquías sopesado por abundancia específica de sitio proporcionó una estimación de declinación en toda la UD de 16.4% año−1 y una declinación a tres generaciones de 93.2%. Un modelo bayesiano de jerarquías produjo una tendencia de declinación a tres generaciones de 91.3% y la distribución posterior mostró que el estimado tuvo una probabilidad >99% de exceder los umbrales para la categorización como especie en peligro. Concluimos que la estrategia bayesiana fue la más útil porque proporcionó una afirmación probabilística de la superación del umbral a favor de una recomendación de categorizar el estado como en riesgo.

Life-history variation along environmental and harvest clines of a northern freshwater fish: Plasticity and adaptation.

Plasticity, local adaptation and evolutionary trade-offs drive clinal variation in traits associated with lifetime growth. Disentangling the processes and determinants that cause these traits to vary helps to understand species' responses to changing environments. This is particularly urgent for exploited populations, where size-selective harvest can induce life-history evolution. Lake trout (Salvelinus namaycush) are an exploited fish with a life history adapted to low-productivity freshwaters of northern North America, which makes them highly vulnerable to ecosystem changes and overfishing. We characterized life-history variation across a broad and diverse landscape for this iconic northern freshwater fish and evaluated whether clinal variation was consistent with hypotheses for local adaptation or growth plasticity. We estimated growth-associated traits for 90 populations exposed to a diversity of environments using a Bayesian multivariate hierarchical model. We tested for clinal variation in their somatic growth, size at maturity and reproductive allocation along environmental gradients of lake productivity, climate, prey and exploitation clines under competing hypotheses of plasticity and local adaptation. Clinal life-history variation was consistent with growth plasticity and local adaptations but not harvest-induced evolution. Variation in somatic growth was explained by exploitation, climate and prey fish occurrence. Increased exploitation, from pristine to fully exploited conditions, led to increased somatic growth (from 32 to 45 mm/year) and adult life spans, and reduced age at maturity (from 11 to 8 years). Variation in size at maturity was explained by climate and, less certainly, prey fish occurrence, while reproductive allocation was explained by evolutionary trade-offs with mortality and other traits, but not environment. Lake trout life-history variation within this range was as wide as that observed across dozens of other freshwater species. Lake trout life histories resulted from evolutionary trade-offs, growth plasticity and local adaptations along several environmental clines. Presuming a plastic response, we documented ~1.4-fold growth compensation to exploitation-lower growth compensation than observed in many freshwater fishes. These results suggest that harvested species exposed to spatially structured and diverse environments may have substantial clinal variation on different traits, but due to different processes, and this has implications for their resilience and successful management.

Metabolic Scope as a Proximate Constraint on Individual Behavioral Variation: Effects on Personality, Plasticity, and Predictability.

Behavioral ecologists have hypothesized that among-individual differences in resting metabolic rate (RMR) may predict consistent individual differences in mean values for costly behaviors or for behaviors that affect energy intake rate. This hypothesis has empirical support and presently attracts considerable attention, but, notably, it does not provide predictions for individual differences in (a) behavioral plasticity or (b) unexplained variation (residual variation from mean individual behavior, here termed predictability). We outline how consideration of aerobic maximum metabolic rate (MMR) and particularly aerobic scope (= MMR - RMR) can be used to simultaneously make predictions about mean and among- and within-individual variation in behavior. We predict that while RMR should be proportional to an individual's mean level of sustained behavioral activity (one aspect of its personality), individuals with greater aerobic scope will also have greater scope to express behavioral plasticity and/or greater unpredictability in behavior (=greater residual variation). As a first step toward testing these predictions, we analyze existing activity data from selectively bred lines of mice that differ in both daily activity and aerobic scope. We find that replicate high-scope mice are more active on average and show greater among-individual variation in activity, greater among-individual variation in plasticity, and greater unpredictability. These data provide some tentative first support for our hypothesis, suggesting that further research on this topic would be valuable.

Habitat availability and ontogenetic shifts alter bottlenecks in size-structured fish populations.

For species that utilize different habitats throughout their life cycle, the habitat limitation at a given stage can act as a bottleneck on population abundance, impacting density-dependent processes such as individual growth and survival. We explore the influence of habitat limitation on population dynamics by developing a multi-stage population model based on lake-dwelling rainbow trout (Oncorhynchus mykiss) populations where adults occupy the lake habitat but use tributaries for spawning and juvenile rearing. The model details density-dependent ecological processes and ontogenetic habitat shifts, harvest mortality, and the impact of climate on growth. We ran model simulations using a range of early life stage habitat availabilities and climatic conditions representative of the native range of rainbow trout in Canada and compared the results to empirical data. The results suggest that (1) increases in early life stage habitat leads to increases in population abundance but, due to density-dependent processes, also results in slower growing stunted populations; (2) population bottlenecks can occur at any life stage, even at the adult stage if spawning and rearing habitats are abundant; (3) when the level of competition for early life stages is increased, inter-cohort competition can lead to population cycles. The model's conclusions are further reinforced by empirical data showing a similar trend in the relationship between fish density and maximum size and providing evidence that limited early life stage habitat leads to lower fish densities and larger fish size. We provide a model that links environmental conditions to population dynamics and is useful for fisheries management and habitat conservation decisions.

Interaction of ecological and angler processes: experimental stocking in an open access, spatially structured fishery.

Effective management of socioecological systems requires an understanding of the complex interactions between people and the environment. In recreational fisheries, which are prime examples of socioecological systems, anglers are analogous to mobile predators in natural predator-prey systems, and individual fisheries in lakes across a region are analogous to a spatially structured landscape of prey patches. Hence, effective management of recreational fisheries across large spatial scales requires an understanding of the dynamic interactions among ecological density dependent processes, landscape-level characteristics, and angler behaviors. We focused on the stocked component of the open access rainbow trout (Oncorhynchus mykiss) fishery in British Columbia (BC), and we used an experimental approach wherein we manipulated stocking densities in a subset of 34 lakes in which we monitored angler effort, fish abundance, and fish size for up to seven consecutive years. We used an empirically derived relationship between fish abundance and fish size across rainbow trout populations in BC to provide a measure of catch-based fishing quality that accounts for the size-abundance trade off in this system. We replicated our experimental manipulation in two regions known to have different angler populations and broad-scale access costs. We hypothesized that angler effort would respond to variation in stocking density, resulting in spatial heterogeneity in angler effort but homogeneity in catch-based fishing quality within regions. We found that there is an intermediate stocking density for a given lake or region at which angler effort is maximized (i.e., an optimal stocking density), and that this stocking density depends on latent effort and lake accessibility. Furthermore, we found no clear effect of stocking density on our measure of catch-based fishing quality, suggesting that angler effort homogenizes catch-related attributes leading to an eroded relationship between stocking density and catch-based fishing quality at the timescale of annual surveys. We conclude that declines in fishing quality resulting from understocking (due to declines in catch rate with low fish abundance) and overstocking (due to suppressed growth and limited recruitment at high density) give an optimal stocking rate that depends on accessibility and latent effort.

Supply-demand equilibria and the size-number trade-off in spatially structured recreational fisheries.

Recreational fishing effort varies across complex inland landscapes (e.g., lake-districts) and appears influenced by both angler preferences and qualities of the fishery resource, like fish size and abundance. However, fish size and abundance have an ecological trade-off within a population, thereby structuring equal-quality isopleths expressing this trade-off across the fishing landscape. Since expressed preferences of recreational anglers (i.e., site-selection of high-quality fishing opportunities among many lakes) can be analogous to optimal foraging strategies of natural predators, adopting such concepts can aid in understanding scale-dependence in fish-angler interactions and impacts of fishing across broad landscapes. Here, we assumed a fish supply-angler demand equilibria and adapted a novel bivariate measure of fishing quality based on fish size and catch rates to assess how recreational anglers influence fishing quality among a complex inland landscape. We then applied this metric to evaluate (1) angler preferences for caught and released fish compared to harvested fish, (2) the nonlinear size-numbers trade-off with uncertainty in both traits, and (3) the spatial-scale of the equilibria across 62 lakes and four independent management regions in British Columbia's (BC) rainbow trout Oncorhynchus mykiss fishery. We found anglers had low preference for caught and released fish (~10% of the value compared to harvested fish), which modified anglers' perception of fishing quality. Hence, fishing quality and angler effort was not influenced simply by total fish caught, but largely by harvested fish catch rates. Fishing quality varied from BC's northern regions (larger fish and more abundant) compared to southern regions (smaller fish and less abundant) directly associated with a 2.5 times increase in annual fishing effort in southern regions, suggesting that latent fishing pressure can structure the size-numbers trade-off in rainbow trout populations. The presence of two different equal-quality isopleths suggests at least two effective landscapes support co-occurring ideal free distributions of recreational fishing effort in BC's rainbow fishery. Anglers' expressed preferences among lakes interacted with density dependent growth and survival within lakes to structure a size-numbers trade-off influencing how anglers perceive fishing quality and, ultimately, distribute across complex inland landscapes.

Energy allocation strategy modifies growth-survival trade-offs in juvenile fish across ecological and environmental gradients.

In young temperate zone fishes, conflicting energy demands lead to variability in growing season and winter survival. Growing season survival is driven by size-dependent predation risk whereas winter survival is constrained by autumn body size, energy storage and winter duration. We developed a model of the seasonality of energetics coupled to empirical measures of resource availability, size-dependent predation and temperature seasonality for rainbow trout (Oncorhynchus mykiss) in two sets of lakes in British Columbia, Canada, representing endpoints of a gradient of temperature, growing season duration and winter duration. This model was used to determine the energy allocation strategy which maximized first-year survival across these gradients. Survival was sensitive to the timing of the switch from somatic to storage strategies in cold, short growing season, low resource environments. A broader range of energy allocation strategies were viable in warmer, longer growing season and higher resource lakes. We used empirical observations of autumn energy storage and our modeled values for size-dependent minimal lipid levels needed to survive winter in each system to estimate winter survival for juvenile rainbow trout. Winter survival estimates were 6% in cold lakes with low resources, 82% in warm, lakes with low resources and 100% in warm lakes with high resources. Fish in warm lakes with ample resources allocated substantially more to storage than the minimum required to survive winter generated from our model, suggesting additional selection pressures for increased storage when there was ample surplus energy. We concluded that growth-survival trade-offs, modified by seasonality of the environment, influenced the growing season energy allocation strategies for young-of-the-year fish, and suggested this may be important for understanding population viability across environmental gradients.

Neutral and adaptive drivers of genomic change in introduced brook trout (Salvelinus fontinalis) populations revealed by pooled sequencing.

Understanding the drivers of successful species invasions is important for conserving native biodiversity and for mitigating the economic impacts of introduced species. However, whole-genome resolution investigations of the underlying contributions of neutral and adaptive genetic variation in successful introductions are rare. Increased propagule pressure should result in greater neutral genetic variation, while environmental differences should elicit selective pressures on introduced populations, leading to adaptive differentiation. We investigated neutral and adaptive variation among nine introduced brook trout (Salvelinus fontinalis) populations using whole-genome pooled sequencing. The populations inhabit isolated alpine lakes in western Canada and descend from a common source, with an average of ~19 (range of 7-41) generations since introduction. We found some evidence of bottlenecks without recovery, no strong evidence of purifying selection, and little support that varying propagule pressure or differences in local environments shaped observed neutral genetic variation differences. Putative adaptive loci analysis revealed nonconvergent patterns of adaptive differentiation among lakes with minimal putatively adaptive loci (0.001%-0.15%) that did not correspond with tested environmental variables. Our results suggest that (i) introduction success is not always strongly influenced by genetic load; (ii) observed differentiation among introduced populations can be idiosyncratic, population-specific, or stochastic; and (iii) conservatively, in some introduced species, colonization barriers may be overcome by support through one aspect of propagule pressure or benign environmental conditions.

Rapid depletion of genotypes with fast growth and bold personality traits from harvested fish populations.

The possibility for fishery-induced evolution of life history traits is an important but unresolved issue for exploited fish populations. Because fisheries tend to select and remove the largest individuals, there is the evolutionary potential for lasting effects on fish production and productivity. Size selection represents an indirect mechanism of selection against rapid growth rate, because individual fish may be large because of rapid growth or because of slow growth but old age. The possibility for direct selection on growth rate, whereby fast-growing genotypes are more vulnerable to fishing irrespective of their size, is unexplored. In this scenario, faster-growing genotypes may be more vulnerable to fishing because of greater appetite and correspondingly greater feeding-related activity rates and boldness that could increase encounter with fishing gear and vulnerability to it. In a realistic whole-lake experiment, we show that fast-growing fish genotypes are harvested at three times the rate of the slow-growing genotypes within two replicate lake populations. Overall, 50% of fast-growing individuals were harvested compared with 30% of slow-growing individuals, independent of body size. Greater harvest of fast-growing genotypes was attributable to their greater behavioral vulnerability, being more active and bold. Given that growth is heritable in fishes, we speculate that evolution of slower growth rates attributable to behavioral vulnerability may be widespread in harvested fish populations. Our results indicate that commonly used minimum size-limits will not prevent overexploitation of fast-growing genotypes and individuals because of size-independent growth-rate selection by fishing.

Density-dependent life-history compensation of an iteroparous salmonid.

Over the course of a decade, the bull trout (Salvelinus confluentus) population in Lower Kananaskis Lake, Alberta, Canada, recovered from a heavily overexploited state, experiencing a 28-fold increase in adult abundance after the implementation of zero-harvest regulations. This system provided a unique opportunity to monitor the changes in life-history characteristics in a natural population throughout the recovery process. The purpose of this study was to examine the degree to which life-history traits were able to compensate for harvest-induced changes and the implications of this for management. Density-dependent changes in growth, survival, and reproductive life-history characteristics were observed. As density increased, maturation was delayed, and the frequency of skipped reproductive events, primarily by individuals of poor condition, increased. However, size at maturation and the proportion of fish skipping reproduction differed between the sexes, suggesting that life-history trade-offs differ between the sexes. The rapid response of these life-history traits to changes in density suggests that these changes were primarily due to phenotypic plasticity, although the importance of natural and artificial selection should not be discounted. The magnitude of the variation in the traits represents the degree to which the population was able to compensate for overharvest, although the overexploited state of the population at the beginning of the study demonstrates it was not able to fully compensate for this mortality. However, no evidence of depensatory processes was found. This, in combination with the plasticity of the life-history traits, has important implications for the resilience of the population to overharvest. Furthermore, density-dependent growth may have the unintended result of making size-based regulations less conservative at low levels of population abundance, as younger fish, perhaps even immature fish, become vulnerable to harvest. Finally, the variation in life-history traits in relation to evolutionary change is discussed. Results from this study demonstrate the importance of considering not only survival, but also changes in life-history characteristics for management and conservation.

Ontogeny of energy allocation reveals selective pressure promoting risk-taking behaviour in young fish cohorts.

Given limited food, prey fishes in a temperate climate must take risks to acquire sufficient reserves for winter and/or to outgrow vulnerability to predation. However, how can we distinguish which selective pressure promotes risk-taking when larger body size is always beneficial? To address this question, we examined patterns of energy allocation in populations of age-0 trout to determine if greater risk-taking corresponds with energy allocation to lipids or to somatic growth. Trout achieved maximum growth rates in all lakes and allocated nearly all of their acquired energy to somatic growth when small in early summer. However, trout in low-food lakes took greater risks to achieve this maximal growth, and therefore incurred high mortality. By late summer, age-0 trout allocated considerable energy to lipids and used previously risky habitats in all lakes. These results indicate that: (i) the size-dependent risk of predation (which is independent of behaviour) promotes risk-taking behaviour of age-0 trout to increase growth and minimize time spent in vulnerable sizes; and (ii) the physiology of energy allocation and behaviour interact to mediate growth/mortality trade-offs for young animals at risk of predation and starvation.

Rainbow trout in seasonal environments: phenotypic trade-offs across a gradient in winter duration.

Survival through periods of resource scarcity depends on the balance between metabolic demands and energy storage. The opposing effects of predation and starvation mortality are predicted to result in trade-offs between traits that optimize fitness during periods of resource plenty (e.g., during the growing season) and those that optimize fitness during periods of resource scarcity (e.g., during the winter). We conducted a common environment experiment with two genetically distinct strains of rainbow trout to investigate trade-offs due to (1) the balance of growth and predation risk related to foraging rate during the growing season and (2) the allocation of energy to body size prior to the winter. Fry (age 0) from both strains were stocked into replicate natural lakes at low and high elevation that differed in winter duration (i.e., ice cover) by 59 days. Overwinter survival was lowest in the high-elevation lakes for both strains. Activity rate and growth rate were highest at high elevation, but growing season survival did not differ between strains or between environments. Hence, we did not observe a trade-off between growth and predation risk related to foraging rate. Growth rate also differed significantly between the strains across both environments, which suggests that growth rate is involved in local adaptation. There was not, however, a difference between strains or between environments in energy storage. Hence, we did not observe a trade-off between growth and storage. Our findings suggest that intrinsic metabolic rate, which affects a trade-off between growth rate and overwinter survival, may influence local adaptation in organisms that experience particularly harsh winter conditions (e.g., extended periods trapped beneath the ice in high-elevation lakes) in some parts of their range.

Predators select against high growth rates and risk-taking behaviour in domestic trout populations.

Domesticated (farm) salmonid fishes display an increased willingness to accept risk while foraging, and achieve high growth rates not observed in nature. Theory predicts that elevated growth rates in domestic salmonids will result in greater risk-taking to access abundant food, but low survival in the presence of predators. In replicated whole-lake experiments, we observed that domestic trout (selected for high growth rates) took greater risks while foraging and grew faster than a wild strain. However, survival consequences for greater growth rates depended upon the predation environment. Domestic trout experienced greater survival when risk was low, but lower survival when risk was high. This suggests that animals with high intrinsic growth rates are selected against in populations with abundant predators, explaining the absence of such phenotypes in nature. This is, to our knowledge, the first large-scale field experiment to directly test this theory and simultaneously quantify the initial invasibility of domestic salmonid strains that escape into the wild from aquaculture operations, and the ecological conditions affecting their survival.

Density-dependent mortality is mediated by foraging activity for prey fish in whole-lake experiments.

Whereas the effects of density-dependent growth and survival on population dynamics are well-known, mechanisms that give rise to density dependence in animal populations are not well understood. We tested the hypothesis that the trade-off between growth and mortality rates is mediated by foraging activity and habitat use. Thus, if depletion of food by prey is density-dependent, and leads to greater foraging activity and risky habitat use, then visibility and encounter rates with predators must also increase. We tested this hypothesis by experimentally manipulating the density of young rainbow trout (Oncorhynchus mykiss) at risk of cannibalism, in a replicated single-factor experiment using eight small lakes, during an entire growing season. We found no evidence for density-dependent depletion of daphnid food in the nearshore refuge where most age-0 trout resided. Nonetheless, the proportion of time spent moving by individual age-0 trout, the proportion of individuals continuously active, and use of deeper habitats was greater in high density populations than in low density populations. Differences in food abundance among lakes had no effect on measures of activity or habitat use. Mortality of age-0 trout over the growing season was higher in high density populations, and in lakes with lower daphnid food abundance. Therefore, population-level mortality of age-0 trout is linked to greater activity and use of risky habitats by individuals at high densities. We suspect that food resources were depleted at small spatial and temporal scales not detected by our plankton sampling in the high density treatment, because food-dependent activity and habitat use by age-0 trout occurs in our lakes when food abundance is experimentally manipulated (Biro, Post & Parkinson, in press).

Mechanisms for climate-induced mortality of fish populations in whole-lake experiments.

The effects of climate change on plant and animal populations are widespread and documented for many species in many areas of the world. However, projections of climate impacts will require a better mechanistic understanding of ecological and behavioral responses to climate change and climate variation. For vertebrate animals, there is an absence of whole-system manipulative experiments that express natural variation in predator and prey behaviors. Here we investigate the effect of elevated water temperature on the physiology, behavior, growth, and survival of fish populations in a multiple whole-lake experiment, by using 17 lake-years of data collected over 2 years with differing average temperatures. We found that elevated temperatures in excess of the optimum reduced the scope for growth through reduced maximum consumption and increased metabolism in young rainbow trout, Oncorhynchus mykiss. Increased metabolism at high temperatures resulted in increased feeding activity (consumption) by individuals to compensate and maintain growth rates similar to that observed at cooler (optimum) temperatures. However, greater feeding activity rates resulted in greater vulnerability to predators that reduced survival to only half that of the cooler year. Our work therefore identifies temperature-dependent physiology and compensatory feeding behavior as proximate mechanisms for substantial climate-induced mortality in fish populations at the scale of entire populations and waterbodies.

Behavioural trade-offs between growth and mortality explain evolution of submaximal growth rates.

1. The importance of body size and growth rate in ecological interactions is widely recognized, and both are frequently used as surrogates for fitness. However, if there are significant costs associated with rapid growth rates then its fitness benefits may be questioned. 2. In replicated whole-lake experiments, we show that a domestic strain of rainbow trout (artificially selected for maximum intrinsic growth rate) use productive but risky habitats more than wild trout. Consequently, domestic trout grow faster in all situations, experience greater survival in the absence of predators, but have lower survival in the presence of predators. Therefore, rapid growth rates are selected against due to increased foraging effort (or conversely, lower antipredator behaviour) that increases vulnerability to predators. In other words, there is a behaviourally mediated trade-off between growth and mortality rates. 3. Whereas rapid growth is beneficial in many ecological interactions, our results show the mortality costs of achieving it are large in the presence of predators, which can help explain the absence of an average phenotype with maximized growth rates in nature.