Does global change increase the risk of maladaptation of Atlantic salmon migration through joint modifications of river temperature and discharge?

In freshwater ecosystems, water temperature and discharge are two intrinsically associated triggers of key events in the life cycle of aquatic organisms such as the migration of diadromous fishes. However, global changes have already profoundly altered the thermal and hydrological regimes of rivers, affecting the timing of fish migration as well as the environmental conditions under which it occurs. In this study, we focused on Atlantic salmon (Salmo salar), an iconic diadromous species whose individuals migrate between marine nursery areas and continental spawning grounds. An innovative multivariate method was developed to analyse long-term datasets of daily water temperature, discharge and both salmon juvenile downstream and adult upstream migrations in three French rivers (the Bresle, Oir and Nivelle rivers). While all three rivers have gradually warmed over the last 35 years, changes in discharge have been very heterogeneous. Juveniles more frequently used warmer temperatures to migrate. Adults migrating a few weeks before spawning more frequently used warm temperatures associated with high discharges. This has already led to modifications in preferential niches of both life stages and suggests a potential mismatch between these populations' ecological preference and changes in their local environment due to global change.

Spatial synchrony in the response of a long range migratory species (Salmo salar) to climate change in the North Atlantic Ocean.

A major challenge in understanding the response of populations to climate change is to separate the effects of local drivers acting independently on specific populations, from the effects of global drivers that impact multiple populations simultaneously and thereby synchronize their dynamics. We investigated the environmental drivers and the demographic mechanisms of the widespread decline in marine survival rates of Atlantic salmon (Salmo salar) over the last four decades. We developed a hierarchical Bayesian life cycle model to quantify the spatial synchrony in the marine survival of 13 large groups of populations (called stock units, SU) from two continental stock groups (CSG) in North America (NA) and Southern Europe (SE) over the period 1971-2014. We found strong coherence in the temporal variation in postsmolt marine survival among the 13 SU of NA and SE. A common North Atlantic trend explains 37% of the temporal variability of the survivals for the 13 SU and declines by a factor of 1.8 over the 1971-2014 time series. Synchrony in survival trends is stronger between SU within each CSG. The common trends at the scale of NA and SE capture 60% and 42% of the total variance of temporal variations, respectively. Temporal variations of the postsmolt survival are best explained by the temporal variations of sea surface temperature (SST, negative correlation) and net primary production indices (PP, positive correlation) encountered by salmon in common domains during their marine migration. Specifically, in the Labrador Sea/Grand Banks for populations from NA, 26% and 24% of variance is captured by SST and PP, respectively and in the Norwegian Sea for populations from SE, 21% and 12% of variance is captured by SST and PP, respectively. The findings support the hypothesis of a response of salmon populations to large climate-induced changes in the North Atlantic simultaneously impacting populations from distant continental habitats.

Abundance indices and biological traits of juvenile salmon (Salmo salar) sampled in three rivers on the Atlantic and Channel coasts (France).

BACKGROUND: Atlantic Salmon (Salmo salar) is an anadromous migratory species adapted to cool temperatures. It is protected by the Bern convention and by the European Habitats Directive. It has been listed as vulnerable by the French IUCN Red List. Salmon decline is the result of combined and cumulated, mainly anthropic, causes: climate change, increasingly high number of impoundments, degradation of water quality and habitat and over-exploitation by fisheries. Monitoring of this species has been carried out on three rivers in France (Southern part of the distribution area) to produce data and knowledge (growth, precocious maturity, survival) for stock management.For 24 years, a specific and standardised electric fishing protocol has been used to target young-of-the-year (0+ parr) Atlantic salmon. Sampling was restricted to areas with shallow running water that flows over a coarse bottom substrate, i.e. the preferred habitat of young salmon. This monitoring and inventory of growing areas thus allows assessment of juvenile recruitment and provides baseline data required to calculate total allowable catches (TACs). NEW INFORMATION: The dataset currently consists of 47,077 occurrence data points from 105 sites spanning up to 24 years in three different watersheds in France. Beyond our project, this dataset has a clear utility to research since it associates abundance measurements with the measurement of biological traits and the collection of tissue samples. It allows for current and retrospective characterisation of individuals or populations, according to life history traits and genetic features in relation to changes in environmental conditions. The fact that the monitoring takes place in France, the southern part of the distribution area, over 24 years, makes the dataset particularly relevant for climate change studies.

A hierarchical bayesian model to quantify uncertainty of stream water temperature forecasts.

Providing generic and cost effective modelling approaches to reconstruct and forecast freshwater temperature using predictors as air temperature and water discharge is a prerequisite to understanding ecological processes underlying the impact of water temperature and of global warming on continental aquatic ecosystems. Using air temperature as a simple linear predictor of water temperature can lead to significant bias in forecasts as it does not disentangle seasonality and long term trends in the signal. Here, we develop an alternative approach based on hierarchical Bayesian statistical time series modelling of water temperature, air temperature and water discharge using seasonal sinusoidal periodic signals and time varying means and amplitudes. Fitting and forecasting performances of this approach are compared with that of simple linear regression between water and air temperatures using i) an emotive simulated example, ii) application to three French coastal streams with contrasting bio-geographical conditions and sizes. The time series modelling approach better fit data and does not exhibit forecasting bias in long term trends contrary to the linear regression. This new model also allows for more accurate forecasts of water temperature than linear regression together with a fair assessment of the uncertainty around forecasting. Warming of water temperature forecast by our hierarchical Bayesian model was slower and more uncertain than that expected with the classical regression approach. These new forecasts are in a form that is readily usable in further ecological analyses and will allow weighting of outcomes from different scenarios to manage climate change impacts on freshwater wildlife.

Contrasting effects of climate change in continental vs. oceanic environments on population persistence and microevolution of Atlantic salmon.

Facing climate change (CC), species are prone to multiple modifications in their environment that can lead to extinction, migration or adaptation. Identifying the role and interplay of different potential stressors becomes a key question. Anadromous fishes will be exposed to both river and oceanic habitat changes. For Atlantic salmon, the river water temperature, river flow and oceanic growth conditions appear as three main stressing factors. They could act on population dynamics or as selective forces on life-history pathways. Using an individual-based demo-genetic model, we assessed the effects of these factors (1) to compare risks of extinction resulting from CC in river and ocean, and (2) to assess CC effects on life-history pathways including the evolution of underlying genetic control of phenotypic plasticity. We focused on Atlantic salmon populations from Southern Europe for a time horizon of three decades. We showed that CC in river alone should not lead to extinction of Southern European salmon populations. In contrast, the reduced oceanic growth appeared as a significant threat for population persistence. An increase in river flow amplitude increased the risk of local extinction in synergy with the oceanic effects, but river temperature rise reduced this risk. In terms of life-history modifications, the reduced oceanic growth increased the age of return of individuals through plastic and genetic responses. The river temperature rise increased the proportion of sexually mature parr, but the genetic evolution of the maturation threshold lowered the maturation rate of male parr. This was identified as a case of environmentally driven plastic response that masked an underlying evolutionary response of plasticity going in the opposite direction. We concluded that to counteract oceanic effects, river flow management represented the sole potential force to reduce the extinction probability of Atlantic salmon populations in Southern Europe, although this might not impede changes in migration life history.

Invasion dynamics of a fish-free landscape by brown trout (Salmo trutta).

Metapopulation dynamics over the course of an invasion are usually difficult to grasp because they require large and reliable data collection, often unavailable. The invasion of the fish-free freshwater ecosystems of the remote sub-Antarctic Kerguelen Islands following man-made introductions of brown trout (Salmo trutta) in the 1950's is an exception to this rule. Benefiting from a full long term environmental research monitoring of the invasion, we built a Bayesian dynamic metapopulation model to analyze the invasion dynamics of 85 river systems over 51 years. The model accounted for patch size (river length and connections to lakes), alternative dispersal pathways between rivers, temporal trends in dynamics, and uncertainty in colonization date. The results show that the model correctly represents the observed pattern of invasion, especially if we assume a coastal dispersal pathway between patches. Landscape attributes such as patch size influenced the colonization function, but had no effect on propagule pressure. Independently from patch size and distance between patches, propagule pressure and colonization function were not constant through time. Propagule pressure increased over the course of colonization, whereas the colonization function decreased, conditional on propagule pressure. The resulting pattern of this antagonistic interplay is an initial rapid invasion phase followed by a strong decrease in the invasion rate. These temporal trends may be due to either adaptive processes or environmental gradients encountered along the colonization front. It was not possible to distinguish these two hypotheses. Because invasibility of Kerguelen Is. freshwater ecosystems is very high due to the lack of a pre-existing fish fauna and minimal human interference, our estimates of invasion dynamics represent a blueprint for the potential of brown trout invasiveness in pristine environments. Our conclusions shed light on the future of polar regions where, because of climate change, fish-free ecosystems become increasingly accessible to invasion by fish species.

Assessing adaptive phenotypic plasticity by means of conditional strategies from empirical data: the latent environmental threshold model.

Conditional strategies are the most common form of discrete phenotypic plasticity. In a conditional strategy, the phenotype expressed by an organism is determined by the difference between an environmental cue and a threshold, both of which may vary among individuals. The environmental threshold model (ETM) has been proposed as a mean to understand the evolution of conditional strategies, but has been surprisingly seldom applied to empirical studies. A hindrance for the application of the ETM is that often, the proximate cue triggering the phenotypic expression and the individual threshold are not measurable, and can only be assessed using a related observable cue. We describe a new statistical model that can be applied in this common situation. The Latent ETM (LETM) allows for a measurement error in the phenotypic expression of the individual environmental cue and a purely genetically determined threshold. We show that coupling our model with quantitative genetic methods allows an evolutionary approach including an estimation of the heritability of conditional strategies. We evaluate the performance of the LETM with a simulation study and illustrate its utility by applying it to empirical data on the size-dependent smolting process for stream-dwelling Atlantic salmon juveniles.

Investigating evolutionary trade-offs in wild populations of atlantic salmon (salmo salar): incorporating detection probabilities and individual heterogeneity.

Evolutionary trade-offs among demographic parameters are important determinants of life-history evolution. Investigating such trade-offs under natural conditions has been limited by inappropriate analytical methods that fail to address the bias in demographic estimates that can result when issues of detection (uncertain detection of individual) are ignored. We propose a new statistical approach to quantify evolutionary trade-offs in wild populations. Our method is based on a state-space modeling framework that focuses on both the demographic process of interest as well as the observation process. As a case study, we used individual mark-recapture data for stream-dwelling Atlantic salmon juveniles in the Scorff River (Southern Brittany, France). In freshwater, juveniles face two life-history choices: migration to the ocean and sexual maturation (for males). Trade-offs may appear with these life-history choices and survival, because all are energy dependent. We found a cost of reproduction on survival for fish staying in freshwater and a survival advantage associated with the "decision" to migrate. Our modeling framework opens up promising prospects for the study of evolutionary trade-offs when some life-history traits are not, or only partially, observable.