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.

Blinded by the light? Nearshore energy pathway coupling and relative predator biomass increase with reduced water transparency across lakes.

Habitat coupling is a concept that refers to consumer integration of resources derived from different habitats. This coupling unites fundamental food web pathways (e.g., cross-habitat trophic linkages) that mediate key ecological processes such as biomass flows, nutrient cycling, and stability. We consider the influence of water transparency, an important environmental driver in aquatic ecosystems, on habitat coupling by a light-sensitive predator, walleye (Sander vitreus), and its prey in 33 Canadian lakes. Our large-scale, across-lake study shows that the contribution of nearshore carbon (δ13C) relative to offshore carbon (δ13C) to walleye is higher in less transparent lakes. To a lesser degree, the contribution of nearshore carbon increased with a greater proportion of prey in nearshore compared to offshore habitats. Interestingly, water transparency and habitat coupling predict among-lake variation in walleye relative biomass. These findings support the idea that predator responses to changing conditions (e.g., water transparency) can fundamentally alter carbon pathways, and predator biomass, in aquatic ecosystems. Identifying environmental factors that influence habitat coupling is an important step toward understanding spatial food web structure in a changing world.

Effects of differential habitat warming on complex communities.

Food webs unfold across a mosaic of micro and macro habitats, with each habitat coupled by mobile consumers that behave in response to local environmental conditions. Despite this fundamental characteristic of nature, research on how climate change will affect whole ecosystems has overlooked (i) that climate warming will generally affect habitats differently and (ii) that mobile consumers may respond to this differential change in a manner that may fundamentally alter the energy pathways that sustain ecosystems. This reasoning suggests a powerful, but largely unexplored, avenue for studying the impacts of climate change on ecosystem functioning. Here, we use lake ecosystems to show that predictable behavioral adjustments to local temperature differentials govern a fundamental structural shift across 54 food webs. Data show that the trophic pathways from basal resources to a cold-adapted predator shift toward greater reliance on a cold-water refuge habitat, and food chain length increases, as air temperatures rise. Notably, cold-adapted predator behavior may substantially drive this decoupling effect across the climatic range in our study independent of warmer-adapted species responses (for example, changes in near-shore species abundance and predator absence). Such modifications reflect a flexible food web architecture that requires more attention from climate change research. The trophic pathway restructuring documented here is expected to alter biomass accumulation, through the regulation of energy fluxes to predators, and thus potentially threatens ecosystem sustainability in times of rapid environmental change.

Life-history plasticity and sustainable exploitation: a theory of growth compensation applied to walleye management.

A simple population model was developed to evaluate the role of plastic and evolutionary life-history changes on sustainable exploitation rates. Plastic changes are embodied in density-dependent compensatory adjustments to somatic growth rate and larval/juvenile survival, which can compensate for the reductions in reproductive lifetime and mean population fecundity that accompany the higher adult mortality imposed by exploitation. Evolutionary changes are embodied in the selective pressures that higher adult mortality imposes on age at maturity, length at maturity, and reproductive investment. Analytical development, based on a biphasic growth model, led to simple equations that show explicitly how sustainable exploitation rates are bounded by each of these effects. We show that density-dependent growth combined with a fixed length at maturity and fixed reproductive investment can support exploitation-driven mortality that is 80% of the level supported by evolutionary changes in maturation and reproductive investment. Sustainable fishing mortality is proportional to natural mortality (M) times the degree of density-dependent growth, as modified by both the degree of density-dependent early survival and the minimum harvestable length. We applied this model to estimate sustainable exploitation rates for North American walleye populations (Sander vitreus). Our analysis of demographic data from walleye populations spread across a broad latitudinal range indicates that density-dependent variation in growth rate can vary by a factor of 2. Implications of this growth response are generally consistent with empirical studies suggesting that optimal fishing mortality is approximately 0.75M for teleosts. This approach can be adapted to the management of other species, particularly when significant exploitation is imposed on many, widely distributed, but geographically isolated populations.

Predator bioenergetics and the prey size spectrum: do foraging costs determine fish production?

Most models of fish growth and predation dynamics assume that food ingestion rate is the major component of the energy budget affected by prey availability, while active metabolism is invariant (here called constant activity hypothesis). However, increasing empirical evidence supports an opposing view: fish tend to adjust their foraging activity to maintain reasonably constant ingestion levels in the face of varying prey density and/or quality (the constant satiation hypothesis). In this paper, we use a simple but flexible model of fish bioenergetics to show that constant satiation is likely to occur in fish that optimize both net production rate and life history. The model includes swimming speed as an explicit measure of foraging activity leading to both energy gains (through prey ingestion) and losses (through active metabolism). The fish is assumed to be a particulate feeder that has to swim between consecutive individual prey captures, and that shifts its diet ontogenetically from smaller to larger prey. The prey community is represented by a negative power-law size spectrum. From these rules, we derive the net production of fish as a function of the size spectrum, and this in turn establishes a formal link between the optimal life history (i.e. maximum body size) and prey community structure. In most cases with realistic parameter values, optimization of life history ensures that: (i) a constantly satiated fish preying on a steep size spectrum will stop growing and invest all its surplus energy in reproduction before satiation becomes too costly; (ii) conversely, a fish preying on a shallow size spectrum will grow large enough for satiation to be present throughout most of its ontogeny. These results provide a mechanistic basis for previous empirical findings, and call for the inclusion of active metabolism as a major factor limiting growth potential and the numerical response of predators in theoretical studies of food webs.

Species compositions mediate biomass conservation: The case of lake fish communities.

Environmental and geographical factors are known to influence the number, distribution, and combination of species that coexist within ecological communities. This, in turn, should influence ecosystem functions such as biomass conservation, or the ability of a community to sustain biomass from small to large organisms. We tested this hypothesis by assessing the role of environmental factors in determining how biomass is conserved in over 600 limnetic fish communities spread across a broad geographic gradient in Canada. Comprehensive and accurate information on water conditions and community characteristics such as taxonomy, abundance, biomass, and size distributions were used in our assessment. Results showed that species combinations emerge as one of the main predictors of biomass conservation among the effects of individual species and abiotic factors. Our study highlights the strong role that geographic patterns in the distribution of species can play in shaping key ecosystem functions, with consequences for ecosystem services such as the provision of harvestable fish biomass.

Biphasic growth in fish I: theoretical foundations.

We develop the theory of biphasic somatic growth in fish using models based on the distinction between pre- and post-maturation growth and an explicit description of energy allocation within a growing season. We define a 'generic biphasic' (GB) model that assumes post-maturation growth has a von Bertalanffy (vB) form. For this model we derive an explicit expression for the gonad weight/somatic weight ratio (g) which may either remain fixed or vary with size. Optimal biphasic models are then developed with reproductive strategies that maximise lifetime reproductive output. We consider two optimal growth models. In the first (fixed g optimal), gonad weight is constrained to be proportional to somatic weight. In the second (variable g optimal) model, allocation to reproduction is unconstrained and g increases with size. For the first of these two models, adult growth in a scaled measure of length has the exact vB form. When there are no constraints on allocation, growth is vB to a very good approximation. In both models, pre-maturation growth is linear. In a companion paper we use growth data from lake trout (Salvelinus namaycush) to test the bioenergetics assumptions used to develop these models, and demonstrate that they have advantages over the vB model, both in quality of fit, and in the information contained in the fitted parameters.

Biphasic growth in fish II: empirical assessment.

In [Quince, et al., 2008. Biphasic growth in fish I: Theoretical foundations. J. Theor. Biol., doi:10.1016/j.jtbi.2008.05.029], we developed a set of biphasic somatic growth models, where maturation is accompanied by a deceleration of growth due to allocation of energy to reproduction. Here, we use growth data from both hatchery-raised and wild populations of a large freshwater fish (lake trout, Salvelinus namaycush) to test these models. We show that a generic biphasic model provides a better fit to these data than the von Bertalanffy model. We show that the observed deceleration of somatic growth in females varies directly with gonad weight at spawning, with observed egg volumes roughly 50% of the egg volumes predicted under the unrealistic assumption of perfectly efficient energy transfer from somatic lipids to egg lipids. We develop a Bayesian procedure to jointly fit a biphasic model to observed growth and maturity data. We show that two variants of the generic biphasic model, both of which assume that annual allocation to reproduction is adjusted to maximise lifetime reproductive output, provide complementary fits to wild population data: maturation time and early adult growth are best described by a model with no constraints on annual reproductive investment, while the growth of older fish is best described by a model that is constrained so that the ratio of gonad size to somatic weight (g) is fixed. This behaviour is consistent with the additional observation that g increases with size and age among younger, smaller breeding females but reaches a plateau among older, larger females. We then fit both of these optimal models to growth and maturation data from nineteen wild populations to generate population-specific estimates of 'adapted mortality' rate: the adult mortality consistent with observed growth and maturation schedules, given that both schedules are adapted to maximise lifetime reproductive output. We show that these estimates are strongly correlated with independent estimates of the adult mortality experienced by these populations.

Supplementation stocking of Lake Trout (Salvelinus namaycush) in small boreal lakes: Ecotypes influence on growth and condition.

Supplementation stocking is a commonly used management tool to sustain exploited fish populations. Possible negative consequences of supplementation on local stocks are a concern for the conservation of wild fish populations. However, the direct impacts of supplementation on life history traits of local populations have rarely been investigated. In addition, intraspecific hybridization between contrasting ecotypes (planktivorous and piscivorous) has been seldom considered in supplementation plans. Here, we combined genetic (genotype-by-sequencing analysis) and life history traits to document the effects of supplementation on maximum length, growth rates, body condition and genetic admixture in stocked populations of two Lake Trout ecotypes from small boreal lakes in Quebec and Ontario, Canada. In both ecotypes, the length of stocked individuals was greater than local individuals and, in planktivorous-stocked populations, most stocked fish exhibited a planktivorous-like growth while 20% of fish exhibited piscivorous-like growth. The body condition index was positively related to the proportion of local genetic background, but this pattern was only observed in stocked planktivorous populations. We conclude that interactions and hybridization between contrasting ecotypes is a risk that could result in deleterious impacts and possible outbreeding depression. We discuss the implications of these findings for supplementation stocking.

Food web expansion and contraction in response to changing environmental conditions.

Macroscopic ecosystem properties, such as major material pathways and community biomass structure, underlie the ecosystem services on which humans rely. While ecologists have long sought to identify the determinants of the trophic height of food webs (food chain length), it is somewhat surprising how little research effort is invested in understanding changes among other food web properties across environmental conditions. Here we theoretically and empirically show how a suite of fundamental macroscopic food web structures respond, in concert, to changes in habitat accessibility using post-glacial lakes as model ecosystems. We argue that as resource accessibility increases in coupled food webs, food chain length contracts (that is, reduced predator trophic position), habitat coupling expands (that is, increasingly coupled macrohabitats) and biomass pyramid structure becomes more top heavy. Our results further support an emerging theoretical view of flexible food webs that provides a foundation for generally understanding ecosystem responses to changing environmental conditions.