Jacques Labonne

Assessing maternal effects on metabolic rate dynamics along early development in brown trout (Salmo trutta): an individual-based approach

Routine metabolic rate (oxygen consumption) of individual eggs and larvae of brown trout (Salmo trutta) originating from different families were monitored from fertilisation to the onset of emergence by means of flow through micro-respirometry. This measuring system revealed an accurate tool to measure oxygen consumption on small organisms at the individual level, and daily consumption proved to be very stable. The mass-specific metabolic rate remained low from fertilisation to hatching, and then increased quickly until the age of emergence. A Bayesian modelling approach was used to adequately infer maternal effects on metabolic rate dynamics all along the development period. Substantial differences were found between families, affecting average metabolic rate as well as intra-family variance. That is, offspring originating from different females may have different energetic needs at emergence from gravel. Moreover, between siblings, variability in metabolic rate is also under the influence of maternal effects. Implications of this metabolic rate variability are discussed with regard to life history strategies and early behaviours.

Female preference for male body size in brown trout, Salmo trutta: is big still fashionable?

The study of female preference for male traits is of primary importance for understanding the role of sexual selection in the evolution of natural populations. Female preference is usually investigated in controlled conditions to facilitate the manipulation of variables. However, such results are rarely confirmed in wild populations where many variables act together. Inferring the role of female preference in the outcome of reproduction thus requires field studies and a specific approach to behavioural data. We observed, over 2 years, the courtship behaviours of male and female brown trout in six populations distributed along a French watershed. We focused on behavioural items linked to female preference for male body size. We built a behavioural model describing the relationships between behaviour and female preference and estimated the parameters of the model using a Bayesian modelling approach. We found a significant preference for body size ratio: females tended to prefer males at least 1.45 times their own size. This preference varied between populations and was influenced by female size. Operational sex ratio had only a weak influence on female preference. Our model explained 44% of the observed variation in behaviour. Finally, because observed body size ratio at mating was generally greater than 1, we conclude that female preference plays a major role in the outcome of reproduction in wild populations of brown trout. These results are compared with existing knowledge and theory and their possible consequences at the population level are discussed.

The role of body size versus growth on the decision to migrate : a case study with Salmo trutta

In a population exhibiting partial migration (i.e. migration and residency tactics occur in the same population), the mechanisms underlying the tactical choice are still unclear. Empirical studies have highlighted a variety of factors that could influence the coexistence of resident and migratory individuals, with growth and body size considered to be key factors in the decision to migrate. Most studies suffer from at least one of the two following caveats: (1) survival and capture probabilities are not taken into account in the data analysis, and (2) body size is often used as a proxy for individual growth. We performed a capture–mark–recapture experiment to study partial migration among juvenile brown trout Salmo trutta at the end of their first year, when a portion of the population emigrate from the natal stream while others choose residency tactic. Bayesian multistate capture–recapture models accounting for survival and recaptures probabilities were used to investigate the relative role of body size and individual growth on survival and migration probabilities. Our results show that, despite an apparent effect of both size and growth on migration, growth is the better integrative parameter and acts directly on migration probability whereas body size acts more strongly on survival. Consequently, we recommend caution if size is used as a proxy for growth when studying the factors that drive partial migration in juvenile salmonid species.

The concentration of plasma metabolites varies throughout reproduction and affects offspring number in wild brown trout (Salmo trutta).

In wild populations, measuring energy invested in the reproduction and disentangling investment in gametes versus investment in reproductive behavior (such as intrasexual competition or intersexual preference) remain challenging. In this study, we investigated the energy expenditure in brown trout reproductive behavior by using two proxies: variation in weight and variation of plasma metabolites involved in energy production, over the course of reproductive season in a semi natural experimental river. We estimated overall reproductive success using genetic assignment at the end of the reproductive season. Results show that triglycerides and free fatty acid concentrations vary negatively during reproduction, while amino-acids and glucose concentrations remain stable. Decrease in triglyceride and free fatty acid concentrations during reproduction is not related to initial concentration levels or to weight variation. Both metabolite concentration variations and weight variations are correlated to the number of offspring produced, which could indicate that gametic and behavioral reproductive investments substantially contribute to reproductive success in wild brown trout. This study opens a path to further investigate variations in reproductive investment in wild populations.

Habitat selection in amphidromous Gobiidae of Reunion Island: Sicyopterus lagocephalus (Pallas, 1770) and Cotylopus acutipinnis (Guichenot, 1863)

Freshwater populations of the Indo-pacific region are characterized by a large proportion of amphidromous species. In this paper, we analyse habitat selection by two amphidromous sympatric Gobiidae: Sicyopterus lagocephalus and Cotylopus acutipinnis in Reunion Island. A sampling method using Point Abundance Sampling (PAS) was conducted in 12 rivers. We used mixed logistic models in order to examine the presence probability of species according to location, downstream-upstream gradient, microhabitat variables (depth, velocity and predominant substrata) and presence of conspecifics and sympatric species. Presence probabilities varied between the sampled rivers. We observed a positive attraction between identical developmental stages of both species, which suggests that social interactions or similar preferences for environmental cues influenced their distribution. The presence probabilities of both species’ juveniles decreased from downstream to upstream. We showed that traditional microhabitat variables weakly explained the spatial distribution of both S. lagocephalus and C. acutipinnis, in Reunion Island. We suggest that weak habitat selection for these species is consistent with the amphidromous life style because of the unpredictability of juvenile settlement and the extreme hydrological variations in tropical rivers.

Influence of energetic status on ontogenetic niche shifts: emergence from the redd is linked to metabolic rate in brown trout.

Ontogenetic niche shift should occur when the ratio of growth opportunities to mortality risk becomes higher in the subsequent habitat. While most studies have focused on size to understand the timing of these shifts, an endogenous factor like energetic status (interaction between energy available and energy requirements) appears as a natural candidate to integrate and analyze the growth trade-off between habitats. In this study, we measure energetic content and metabolic rate of individual brown trout (Salmo trutta) fry at emergence from gravel to investigate the influence of energetic status on the timing of this critical ontogenetic niche shift. In addition, as offspring energetic status is subject to parental effects, we examine how females could maximize their own fitness by influencing offspring emergence timing. Our results demonstrate that emergence from gravel is influenced by energetic status. Individuals that emerge first have a higher energetic content but deplete it faster because of a higher metabolic rate. We also find that female fecundity is positively related to emergence period duration. Moreover, our results suggest that females may decrease kin competition during the critical period of emergence by influencing the energetic status of offspring, thus, maximizing their own fitness. Our results help elucidate the mechanisms underlying early ontogenetic niche shifts in juvenile fish and suggest reasons why maternal investment can be so variable within populations.

Female Effects on Offspring Energetic Status and Consequences on Early Development in Yolk Feeding Brown Trout (Salmo trutta)

Energetic status can be defined as the interaction between energy stores and metabolic rate. In salmonids, it is variable and influences the timing of emergence, and therefore may have strong effects on both juvenile and maternal fitness. The aim of this study is to (i) describe the ontogeny of energy use for different brown trout clutches to understand how such a variability of energetic status is developed at the end of incubation and (ii) to estimate maternal influences over offspring physiological processes. Using individual measures of total mass and metabolism throughout ontogeny combined with a hierarchical Bayesian modeling approach, we successfully described clutch-specific (i) metabolic trajectories, (ii) use of yolk resources and the building of new tissues throughout ontogeny. Our results show that females laying large eggs have offspring with lower metabolic costs and higher yolk conversion efficiencies. Females also influence within clutch variance of metabolic and yolk consumption rates leading to potential developmental variations. These results are discussed with regard to their consequences on early life history through the critical period of emergence.

Experimental evidence of population differences in reproductive investment conditional on environmental stochasticity.

Environmental stochasticity is expected to shape life histories of species, wherein organisms subjected to strong environmental variation should display adaptive response by being able to tune their reproductive investment. For riverine ecosystems, climate models forecast an increase in the frequency and intensity of extreme events such as floods and droughts. The speed and the mechanisms by which organisms may adapt their reproductive investment are therefore of primary importance to understand how species will cope with such radical environmental changes. In the present study, we sampled spawners from two different populations of wild brown trout, originating from two environments with contrasting levels of flow stochasticity. We placed them in sympatry within an experimental channel during reproductive season. In one modality, water flow was maintained constant, whereas in another modality, water flow was highly variable. Reproductive investment of all individuals was monitored using weight and energetic plasma metabolite variation throughout the reproductive season. Only the populations originating from the most variable environment showed a plastic response to experimental manipulation of water flow, the females being able to reduce their weight variation (from 19.2% to 13.1%) and metabolites variations (from 84.2% to 18.6% for triglycerides for instance) under variable flow conditions. These results imply that mechanisms to cope with environmental stochasticity can differ between populations of the same species, where some populations can be plastic whereas other cannot.

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 1950s 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.

No early gender effects on energetic status and life history in a salmonid

Throughout an organisms early development, variations in physiology and behaviours may have long lasting consequences on individual life histories. While a large part of variation in critical life-history transitions remains unexplained, a significant proportion may be caused by early gender effects as part of gender-specific life histories shaped by sexual selection. In this study, we investigated the presence of early gender effects on the timing of emergence from gravel and the energetic status of brown trout (Salmo trutta) early stages. To investigate this question, individual measures of emergence timing, metabolic rate and energetic content were coupled for the first time with the use of a recent genetic marker for sdY (sexually dimorphic on the Y-chromosome), a master sex-determining gene. Our results show that gender does not influence the energetic content of emerging juveniles or their emergence timing. These findings suggest that gender differences may appear later throughout salmonid life history and that selective pressures associated with the critical period of emergence from gravel may shape early life-history traits similarly in both males and females.