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.

Joint temporal trends in river thermal and hydrological conditions can threaten the downstream migration of the critically endangered European eel.

Climate change is modifying the hydrological and thermal regimes of rivers worldwide, threatening the triggering of organisms' key life-cycle processes. European eel (Anguilla anguilla) is a critically endangered fish species that migrates over several thousand kilometres between its rearing habitats in continental waters of Europe and North Africa and its spawning area in the Sargasso Sea. Downstream migration of adult eels occurs during periods of decreasing river water temperature associated with high discharge but changes in these environmental cues may affected eel migratory conditions. An innovative multivariate method was developed to analyse long-term datasets of daily water temperature, discharge and eel passage in two European rivers. Over the past 50 years, water temperature and discharge increased in both rivers during the downstream migration period from August to November. Silver eels preferentially migrated at temperatures between 10 and 20 °C combined with high discharge. Environmental changes have resulted in the migration of silver eels under warmer water temperatures. This example illustrates how the changes in environmental cues have led to a growing mismatch between the migratory conditions preferentially selected and those actually used, which may threaten the completion of the eel's life cycle and ultimately the persistence of this already critically endangered species.

An innovative bivariate approach to detect joint temporal trends in environmental conditions: Application to large French rivers and diadromous fish.

Most key life-events of organisms are synchronized by complex interactions of several environmental cues to ensure optimal survival and growth of individuals and their offspring. However, global change is known to affect multiple components of ecosystems and cues at the same time. Therefore, detecting joint trends in covariate time series is a crucial challenge in global change ecology that has rarely been addressed so far. In this context, we designed an innovative combination of kernel density estimations and Mann-Kendall trend tests to detect joint temporal trends in a pair of environmental variables. This methodological framework was tested on >30 years (1976-2019) of water temperature and discharge data for 6 large French rivers (the Garonne, Dordogne, Rhône, Rhine, Loire and Vienne rivers). The implications of such trends in both temperature and discharge for diadromous species key life-cycle processes were then explored by checking if significant bivariate environmental changes occurred during seasons of upstream and downstream migration, and reproductive activities. Results were contrasted between rivers and seasons: many rivers displayed an increase in the number of days with high water temperature and low river discharge, but local discharge regulation measures could have mitigated the trend in discharge. Our findings showed that species migrating or spawning in spring were likely to be strongly impacted by the new environmental conditions in the Garonne, Loire and Rhône rivers, given the marked changes in water temperature and discharge associations detected by our new method. Conditions experienced by fall-running and spawning species have been strongly affected in all the rivers studied. This innovative methodology was implemented in a new R package, ChocR, for application to other environments and ecosystems.

EStimating Contaminants tRansfers Over Complex food webs (ESCROC): An innovative Bayesian method for estimating POP's biomagnification in aquatic food webs.

Pollution greatly impacts ecosystems health and associated ecological functions. Persistent Organic Pollutants (POPs) are among the most studied contaminants due to their persistence, bioaccumulation, and toxicity potential. Biomagnification is often described using the estimation of a Trophic Magnification Factor (TMF). This estimate is based on the relationship between contamination levels of the species and their trophic level. However, while the estimation can be significantly biased in relation to multiple sources of uncertainty (e.g. species physiology, measurement errors, food web complexity), usual TMF estimation methods typically do not allow accounting for these potential biases. More accurate and reliable assessment tool of TMFs and their associated uncertainty are therefore needed in order to appropriately guide chemical pollution management. The present work proposes a relevant and innovative TMF estimation method accounting for its many variability sources. The ESCROC model (EStimating Contaminants tRansfers Over Complex food webs), which is implemented in a Bayesian framework, allows for a more reliable and rigorous assessment of contaminants trophic magnification, in addition to accurate estimations of isotopes trophic enrichment factors and their associated uncertainties in food webs. Similar to classical mixing models used in food web investigations, ECSROC computes diet composition matrices using isotopic composition data while accounting for contamination data, leading to more robust food web descriptions. As a demonstration of the practical application of the model, ESCROC was implemented to revisit the trophic biomagnification of 5 polyfluoroalkyl substances (PFAS) in a complex estuarine food web (the Gironde, SW France). In addition to the TMF estimate and 95% confidence intervals, the model provided biomagnification probabilities associated to the investigated contaminants-for instance, 92% in the case of perfluorooctane sulfonate (PFOS)-that can be interpreted in terms of risk assessment in a precautionary approach, which should prove useful to environmental managers.

Evidence for the Trophic Transfer of Perfluoroalkylated Substances in a Temperate Macrotidal Estuary.

The present survey examines the trophodynamics of a suite of 19 perfluoroalkyl substances (PFASs) in a temperate macrotidal estuary (Gironde, SW France). Across the 147 biota samples (18 taxa) collected, perfluorooctane sulfonate (PFOS), perfluorooctane sulfonamide (FOSA), and C8-C14 perfluoroalkyl carboxylates (PFCAs) were the most-recurrent analytes. ΣPFASs ranged between 0.66-45 ng per g of wet weight of the whole body. Benthic organisms had relatively high ΣPFASs compared to demersal organisms and displayed specific composition profiles with higher relative abundances of C8 and C9 PFCAs. Trophic magnification factors (TMFs) were determined through the use of linear mixed effect models including censored data, thereby considering data below detection limits as well as the interspecific variability of δ15N and PFAS levels (random effects). TMFs were almost consistently >1 in the benthic food web as well as when considering all data pooled together, providing evidence for the biomagnification of several PFASs in estuarine environments. In addition, in contrast with previous observations, TMFs determined in the estuarine benthic web were found to significantly decrease with increasing chain length for C8-C14 PFCAs and C6-C8 perfluoroalkyl sulfonates. This suggests that PFAS chemical structure might not be necessarily predictive of TMFs, which are also influenced by the trophic web characteristics.

Toward a phenological mismatch in estuarine pelagic food web?

Alterations of species phenology in response to climate change are now unquestionable. Until now, most studies have reported precocious occurrence of life cycle events as a major phenological response. Desynchronizations of biotic interactions, in particular predator-prey relationships, are however assumed to strongly impact ecosystems' functioning, as formalized by the Match-Mismatch Hypothesis (MMH). Temporal synchronicity between juvenile fish and zooplankton in estuaries is therefore of essential interest since estuaries are major nursery grounds for many commercial fish species. The Gironde estuary (SW France) has suffered significant alterations over the last three decades, including two Abrupt Ecosystem Shifts (AES), and three contrasted intershift periods. The main objective of this study was to depict modifications in fish and zooplankton phenology among inter-shift periods and discuss the potential effects of the resulting mismatches at a community scale. A flexible Bayesian method was used to estimate and compare yearly patterns of species abundance in the estuary among the three pre-defined periods. Results highlighted (1) an earlier peak of zooplankton production and entrance of fish species in the estuary and (2) a decrease in residence time of both groups in the estuary. Such species-specific phenological changes led to changes in temporal overlap between juvenile fish and their zooplanktonic prey. This situation questions the efficiency and potentially the viability of nursery function of the Gironde estuary, with potential implications for coastal marine fisheries of the Bay of Biscay.

The Combined Use of Correlative and Mechanistic Species Distribution Models Benefits Low Conservation Status Species.

Species can respond to climate change by tracking appropriate environmental conditions in space, resulting in a range shift. Species Distribution Models (SDMs) can help forecast such range shift responses. For few species, both correlative and mechanistic SDMs were built, but allis shad (Alosa alosa), an endangered anadromous fish species, is one of them. The main purpose of this study was to provide a framework for joint analyses of correlative and mechanistic SDMs projections in order to strengthen conservation measures for species of conservation concern. Guidelines for joint representation and subsequent interpretation of models outputs were defined and applied. The present joint analysis was based on the novel mechanistic model GR3D (Global Repositioning Dynamics of Diadromous fish Distribution) which was parameterized on allis shad and then used to predict its future distribution along the European Atlantic coast under different climate change scenarios (RCP 4.5 and RCP 8.5). We then used a correlative SDM for this species to forecast its distribution across the same geographic area and under the same climate change scenarios. First, projections from correlative and mechanistic models provided congruent trends in probability of habitat suitability and population dynamics. This agreement was preferentially interpreted as referring to the species vulnerability to climate change. Climate change could not be accordingly listed as a major threat for allis shad. The congruence in predicted range limits between SDMs projections was the next point of interest. The difference, when noticed, required to deepen our understanding of the niche modelled by each approach. In this respect, the relative position of the northern range limit between the two methods strongly suggested here that a key biological process related to intraspecific variability was potentially lacking in the mechanistic SDM. Based on our knowledge, we hypothesized that local adaptations to cold temperatures deserved more attention in terms of modelling, but further in conservation planning as well.