Deciphering the molecular adaptation of the king scallop (Pecten maximus) to heat stress using transcriptomics and proteomics

Background The capacity of marine species to survive chronic heat stress underpins their ability to survive warming oceans as a result of climate change. In this study RNA-Seq and 2-DE proteomics were employed to decipher the molecular response of the sub-tidal bivalve Pecten maximus, to elevated temperatures. Results Individuals were maintained at three different temperatures (15, 21 and 25 °C) for 56 days, representing control conditions, maximum environmental temperature and extreme warming, with individuals sampled at seven time points. The scallops thrived at 21 °C, but suffered a reduction in condition at 25 °C. RNA-Seq analyses produced 26,064 assembled contigs, of which 531 were differentially expressed, with putative annotation assigned to 177 transcripts. The proteomic approach identified 24 differentially expressed proteins, with nine identified by mass spectrometry. Network analysis of these results indicated a pivotal role for GAPDH and AP-1 signalling pathways. Data also suggested a remodelling of the cell structure, as revealed by the differential expression of genes involved in the cytoskeleton and cell membrane and a reduction in DNA repair. They also indicated the diversion of energetic metabolism towards the mobilization of lipid energy reserves to fuel the increased metabolic rate at the higher temperature. Conclusions This work provides preliminary insights into the response of P. maximus to chronic heat stress and provides a basis for future studies examining the tipping points and energetic trade-offs of scallop culture in warming oceans

Les métamorphoses, entre fiction et notion

Centré sur la représentation des métamorphoses naturelles, ce volume se propose d’étudier des échanges croisés entre fiction et science, dans une perspective transséculaire et interdisciplinaire. Il développe une réflexion sur les potentialités épistémologiques et esthétiques de l’idée de métamorphose, et cherche à mettre en lumière les enjeux idéologiques, philosophiques ou religieux, qui se rattachent à cette notion du xvie au xxie siècle

Variabilité environnementale et adaptabilité énergétique de la coquille Saint-Jacques, Pecten Maximus, face au changement climatique

Les recherches présentées dans cette thèse ont été menées au Laboratoire des sciences de l'environnement marin, Université de Bretagne occidentale (Plouzané, France), au Département de biologie théorique, Vrije Universiteit Amsterdam (Pays-Bas) et à l'Institut de recherche marine (Bergen, Norvège).The relationship between environmental conditions and life history has intrigued biologists for centuries. This thesis aims to better understand the variability of life history traits of the great scallop, Pecten maximus, facing environmental variability. This economically important species for French, English and Norwegian fisheries has a wide distribution range (from the Azores to Lofoten Islands). Growth and reproduction patterns are very variable within this area, potentially due to the environmental variability. Great scallops living at the head of Norway’s fjords are the biggest but grow slowly whereas individuals from lower latitudes have faster growth rates and reach a smaller ultimate size and those from the continental shelf display both low growth rates and a reduced size. The variability in biological traits might be attributed to a plasticity or genetic adaptation of the physiological response of individuals to the environment, to mechanistic causes related to energy fluxes that fuel the metabolism again with regard to environmental forcings or to a combination of these two mechanisms.The approach considered here to study the causes of this variability focuses on the dynamics of energy fluxes which allow us to deal with all the metabolic functions of the individual. The Dynamic Energy Budget (deb) theory provides a mechanistic framework that allows a quantitative description of feeding, assimilation, growth, reproduction, maturation and maintenance over the full life cycle, in relation to thermal and trophic conditions. The first part of this thesis is dedicated to the development of a deb model for P. maximus, with an emphasis on feeding implementation. The model makes use of the Synthesizing Units to provide the system with two substrates which quantifies food selection by the animal. We tested the model on the great scallop population from the Bay of Brest (France), with two proxies of trophic resource : phytoplankton cell counts and suspended organic particles.The second chapter expands on the integration of this individual bioenergetic model to a 3D biogeochemical model in the English Channel. This modeling system allows the mapping of growth and reproduction capacities according to environmental conditions. The individual model simulations enabled us to improve a spatialized model of population dynamics divided in age-classes and including the planktonic larval stage. We carried out predictions over a period of 30 years, thus providing a potential tool for exploited stock forecasting in the English Channel.In the third part of this thesis, we investigated the seasonality and diversity of the diet of this suspension-feeding bivalve in a coastal environment, with the aim to improve our knowledge on the seasonal dynamics of feeding in this species and better understand how we feed the bioenergetic model.We used the combination of three trophic markers (pigments, fatty acids and sterols), measured in the seawater and in two parts of the digestive tract. This study revealed five important pieces of information : (i) the unexpected importance of dinoflagellates in the diet of P. maximus ; (ii) the recurrent switch between ingestion of diatoms and dinoflagellates along with the succession of algae blooms ; (iii) the probable ingestion and assimilation of cyanobacteria and other bacteria, in particular during low microalgae densities ; (iv) the selection capacity of the great scallop, which can preferentially select some algae classes and neglect some others ; (v) trophic inputs from the water column proved to be more important than from the benthos except in early spring.In the two last chapters, we developed and applied a modeling approach consisting of the inversion of the deb model in order to reconstruct the functional response of food assimilation from growth data (obtained from the sclerochronological study of the shell) and temperature. Indeed, it is generally difficult to simply link the dynamics of trophic availability with the dynamics of assimilation and the method proposed here overcomes this issue. The process relies on a simplified equation of growth as described in deb theory.This, therefore, facilitates the inversion of the model while also allowing the reconstruction of state variables and some energy fluxes (reserve dynamics, maintenance costs). As for many organisms producing a carbonated skeleton, P. maximus’ shell grows by sequential increments. The analysis of the striae allows an accurate measurement of daily growth dynamics. We exploited these high frequency data in order to reconstruct the history of functional response along the growth trajectory. This method was applied in a study of the variability of growth patterns along latitudinal and bathymetric gradients. The highly fluctuating pattern of food availability seems to be a key factor in understanding the energy fluxes dynamics in northern and deep-sea populations.The combination of mild temperatures and low and varying food conditions on the continental shelf might lead to a local selection of smaller individuals which require limited maintenance costs. Moreover, this approach allowed us to explore the relationship between the functional response and various markers of trophic availability. It showed that chlorophyll-a measurements in the water column did well and truly explain the major part of the variability of assimilation, at least when phytoplanktonic production in the water column is important.This work shows that the modeling of energy fluxes provides a tool that helps understanding the origin and fate of various energy sources as well as the distribution patterns of individuals. This tool also provides a mechanistic explanation to intra-specific variability patterns. Nevertheless, some physio- logical traits such as the filtration rate are very likely to show some plasticity.Indeed, the simulation carried out in northern and deep-water populations using the parameter set that was estimated in the Bay of Brest provided less relevant results. Further investigations should be conducted on data from early stages and in contrasting environments, in order to better integrate the variability within this species, which would help refine the deb parameter set.The study of P. maximus physiological capacities, carried out on a spatial scale in this thesis, and the stepping to the population level could be useful tools for a better assessment and management of scallop fisheries (which fluctuating recruitment is still poorly understood). Finally, while the effects of global change are being investigated, the use of deb theory in this work could provide a powerful framework to evaluate the impact of changing environments on the energetics of the great scallop.Ces travaux de thèse ont été mené dans le but de mieux comprendre la variabilité des traits d’histoire de vie de la coquille Saint-Jacques, Pecten maximus, face à la variabilité de son environnement. Cette espèce économiquement importante pour les pêcheries françaises, anglaises et norvégiennes a une large aire de répartition (des Açores aux îles Lofoten). Les schémas de croissance et de reproduction sont très variables dans cette zone, ce qui peut être dû à la variabilité de l'environnement. Les grands pétoncles vivant à la tête des fjords norvégiens sont les plus gros mais leur croissance est lente, tandis que les individus des basses latitudes ont un taux de croissance plus rapide et atteignent une taille finale plus petite et ceux du plateau continental ont à la fois un taux de croissance faible et une taille réduite. La variabilité des caractéristiques biologiques pourrait être attribuée à une plasticité ou à une adaptation génétique de la réponse physiologique des individus à l'environnement, à des causes mécanistes liées aux flux d'énergie qui alimentent à nouveau le métabolisme en ce qui concerne les forçages environnementaux ou à une combinaison de ces deux mécanismes.L'approche envisagée ici pour étudier les causes de cette variabilité se concentre sur la dynamique des flux énergétiques qui permet de traiter l'ensemble des fonctions métaboliques de l'individu. La théorie du budget énergétique dynamique (deb) fournit un cadre mécaniste qui permet une description quantitative de l'alimentation, de l'assimilation, de la croissance, de la reproduction, de la maturation et du maintien sur l'ensemble du cycle de vie, en relation avec les conditions thermiques et trophiques. La première partie de cette thèse est consacrée au développement d'un modèle deb pour P. maximus, avec un accent sur la mise en œuvre de l'alimentation. Le modèle utilise les unités de synthèse pour fournir au système deux substrats qui quantifient la sélection de la nourriture par l'animal. Nous avons testé le modèle sur la population de coquilles Saint-Jacques de la baie de Brest (France), avec deux approximations de la ressource trophique : le nombre de cellules phytoplanctoniques et les particules organiques en suspension.Le second chapitre développe l'intégration de ce modèle bioénergétique individuel à un modèle biogéochimique 3D dans la Manche. Ce système de modélisation permet de cartographier les capacités de croissance et de reproduction en fonction des conditions environnementales. Les simulations des modèles individuels ont permis d'améliorer un modèle spatialisé de la dynamique des populations divisé en classes d'âge et incluant le stade larvaire planctonique. Nous avons effectué des prévisions sur une période de 30 ans, fournissant ainsi un outil potentiel pour la prévision des stocks exploités dans la Manche.Dans la troisième partie de cette thèse, nous avons étudié la saisonnalité et la diversité du régime alimentaire de ce bivalve se nourrissant en suspension dans un environnement côtier, dans le but d'améliorer nos connaissances sur la dynamique saisonnière de l'alimentation de cette espèce et de mieux comprendre comment nous alimentons le modèle bioénergétique.Nous avons utilisé la combinaison de trois marqueurs trophiques (pigments, acides gras et stérols), mesurés dans l'eau de mer et dans deux parties du tube digestif. Cette étude a révélé cinq informations importantes : (i) l'importance inattendue des dinoflagellés dans le régime alimentaire de P. maximus ; (ii) le changement récurrent entre l'ingestion de diatomées et de dinoflagellés au cours de la succession des proliférations d'algues ; (iii) l'ingestion et l'assimilation probables de cyanobactéries et d'autres bactéries, en particulier lors de faibles densités de microalgues ; (iv) la capacité de sélection de la grande coquille Saint-Jacques, qui peut sélectionner de préférence certaines classes d'algues et en négliger d'autres ; (v) les apports trophiques de la colonne d'eau se sont avérés plus importants que ceux du benthos, sauf au début du printemps.Dans les deux derniers chapitres, nous avons développé et appliqué une approche de modélisation consistant en l'inversion du modèle deb afin de reconstruire la réponse fonctionnelle de l'assimilation alimentaire à partir des données de croissance (obtenues par l'étude sclérochronologique de la coquille) et de la température. En effet, il est généralement difficile de relier simplement la dynamique de la disponibilité trophique à la dynamique de l'assimilation et la méthode proposée ici permet de surmonter cette difficulté. Le processus s'appuie sur une équation simplifiée de la croissance telle que décrite dans la théorie de Deb.Cela facilite donc l'inversion du modèle tout en permettant la reconstruction des variables d'état et de certains flux d'énergie (dynamique de réserve, coûts de maintenance). Comme pour de nombreux organismes produisant un squelette carbonaté, la coquille de P. maximus se développe par incréments séquentiels. L'analyse des stries permet une mesure précise de la dynamique de croissance quotidienne. Nous avons exploité ces données à haute fréquence afin de reconstituer l'historique de la réponse fonctionnelle le long de la trajectoire de croissance. Cette méthode a été appliquée dans une étude de la variabilité des schémas de croissance le long des gradients latitudinaux et bathymétriques. Le modèle très fluctuant de la disponibilité alimentaire semble être un facteur clé pour comprendre la dynamique des flux d'énergie dans les populations du nord et des grands fonds marins.La combinaison de températures douces et de conditions alimentaires basses et variables sur le plateau continental pourrait conduire à une sélection locale d'individus plus petits qui nécessitent des coûts d'entretien limités. De plus, cette approche nous a permis d'explorer la relation entre la réponse fonctionnelle et divers marqueurs de la disponibilité trophique. Elle a montré que les mesures de la chlorophylle-a dans la colonne d'eau expliquaient bien et véritablement la majeure partie de la variabilité de l'assimilation, du moins lorsque la production phytoplanctonique dans la colonne d'eau est importante.Ce travail montre que la modélisation des flux d'énergie fournit un outil qui aide à comprendre l'origine et le devenir de diverses sources d'énergie ainsi que les schémas de distribution des individus. Cet outil fournit également une explication mécaniste aux modèles de variabilité intraspécifiques. Néanmoins, certains traits physio-logiques tels que le taux de filtration sont très susceptibles de présenter une certaine plasticité.En effet, la simulation réalisée dans les populations du nord et des eaux profondes à l'aide de l'ensemble des paramètres estimés en baie de Brest a donné des résultats moins pertinents. Des recherches supplémentaires devraient être menées sur les données des premiers stades et dans des environnements contrastés, afin de mieux intégrer la variabilité au sein de cette espèce, ce qui permettrait d'affiner le jeu de paramètres deb.L'étude des capacités physiologiques de P. maximus, menée à l'échelle spatiale dans le cadre de cette thèse, et le passage au niveau de la population pourraient être des outils utiles pour une meilleure évaluation et gestion des pêcheries de coquilles Saint-Jacques (dont la fluctuation du recrutement est encore mal comprise). Enfin, alors que les effets du changement global sont étudiés, l'utilisation de la théorie deb dans ce travail pourrait fournir un cadre puissant pour évaluer l'impact des environnements changeants sur l'énergétique de la coquille Saint-Jacques

Reconstructing physiological history from growth, a method to invert DEB models

Dynamic Energy Budget (DEB) models rely on measurements of food availability to describe the rates at which organisms assimilate and use energy from food for maintenance, growth, maturation and reproduction. Although crucial, the determination of appropriate and accurate energy input variables can be problematic. We developed an inverted DEB model to reconstruct the food intake from temperature and growth trajectories. The method makes use of a reformulation of the DEB model dynamics into a second order linear equation. This formula not only allows the reconstruction of the scaled functional response but also gives access to reserve dynamics, mobilization, and somatic maintenance fluxes. The shell of the great scallop, Pecten maximus, providing high resolution records of incremental growth, was used to explore the potential of this approach to reconstruct the functional response from daily shell growth rates data. In a theoretical case, we investigated the resolution and sensitivity limits of the method. In a validation process, predictions were used to re-simulate growth that was compared to the initial growth trajectory. Moreover, as growth data used in the reconstruction process usually show high-frequency variability, we also developed a smoothing method, based on DEB theory assumptions, to filter growth data time series

New insights into the reproductive cycle of two Great Scallop populations in Brittany (France) using a DEB modelling approach

The present study aimed to improve understanding of the environmental conditions influencing the reproductive cycle of the great scallop Pecten maximus in two locations in Brittany (France). We also evaluated potential consequences of future climate change for reproductive success in each site. We simulated reproductive traits (spawning occurrences and synchronicity among individuals) of P. maximus, using an existing Dynamic Energy Budget (DEB) model. To validate and test the model, we used biological and environmental datasets available for the Bay of Brest (West Brittany, France) between 1998 and 2003. We also applied the scallop DEB model in the Bay of Saint-Brieuc (North Brittany, France) for the same period (1998–2003) to compare the reproductive cycle in different environmental conditions. In order to accurately model the P. maximus reproductive cycle we improved the scallop DEB model in two ways: through (1) energy acquisition, by incorporating microphytobenthos as a new food source; and (2) the reproductive process, by adding a new state variable dedicated to the gamete production. Finally, we explored the effects of two contrasting IPCC climate scenarios (RCP2.6 and RCP8.5) on the reproductive cycle of P. maximus in these two areas at the 2100 horizon. In the Bay of Brest, the simulated reproductive cycle was in agreement with field observations. The model reproduced three main spawning events every year (between May and September) and asynchronicity in the timing of spawning between individuals. In the Bay of Saint-Brieuc, only two summer spawning events (in July and August) were simulated, with a higher synchronicity between individuals. Environmental conditions (temperature and food sources) were sufficient to explain this well-known geographic difference in the reproductive strategy of P. maximus. Regarding the forecasting approach, the model showed that, under a warm scenario (RCP8.5), autumnal spawning would be enhanced at the 2100 horizon with an increase of seawater temperature in the Bay of Brest, whatever the food source conditions. In the Bay of Saint-Brieuc, warmer temperatures may impact reproductive phenology through an earlier onset of spawning by 20 to 44 days depending on the year

Modeling the Growth of Sugar Kelp (Saccharina latissima) in Aquaculture Systems using Dynamic Energy Budget Theory

Aquaculture is an industry with the capacity for further growth that can contribute to sustainable food systems to feed an increasing global population. Sugar kelp (Saccharina latissima) is of particular interest for farmers as a fast-growing species that benefits ecosystems as a primary producer. However, as a new industry in the U.S., farmers interested in growing S. latissima lack data on growth dynamics. To address this gap, we calibrated a Dynamic Energy Budget (DEB) model to data from the literature and field-based growth experiments in Rhode Island (U.S.A.). Environmental variables forcing model dynamics include temperature, irradiance, dissolved inorganic carbon concentration, and nitrate and nitrite concentration. The modeled estimates for field S. latissima blade length were accurate despite underestimation of early season growth. In some simulations, winter growth was limited by the rate at which the light-dependent reaction of photosynthesis, the first step of carbon assimilation, was performed. Nitrogen (N) reserves were also an important limiting factor especially later in the spring season as irradiance increased, although the low resolution of N forcing concentrations might restrict the model accuracy. Since this model is focused on S. latissima grown in an aquaculture setting with winter and spring growth, no specific assumptions were made to include summer growth patterns such as tissue loss or reproduction. The results indicate that this mechanistic model for S. latissima captures growth dynamics and blade length at the time of harvest, thus it could be used for spatial predictions of S. latissima aquaculture production across a range of environmental conditions and locations. The model could be a particularly useful tool for further development of sustainable ocean food production systems involving seaweed

Production potential of seaweed and shellfish integrated aquaculture in Narragansett Bay (Rhode Island, U.S.) using an ecosystem model

Integrated aquaculture systems combining macroalgae with traditional fish and shellfish production represent an ecologically sound and economically attractive solution for farmers. To evaluate the potential of growing sugar kelp (Saccharina latissima) at existing oyster (Crassostrea virginica) farms in Narragansett Bay (NB; Rhode Island, U.S.), we developed an ecosystem model based on individual Dynamic Energy Budget models for kelp and oysters forced offline by a coupled 3D hydrodynamic-water quality model. Kelp growth during the cold winter months provides ecosystem services through the removal of nutrients in the bay as well as serving as an additional source of revenue for farmers. Locations with the most nutrient-rich waters at the northern end of the bay seem most suitable for kelp aquaculture, with oyster growth also reaching maxima at the same locations. Predictions of kelp biomass grown on lines ranged from 0.97 kgWW m–1 at the easternmost site at the Bay Entrance to 2.03 kgWW m–1 at the northernmost site in the Upper Bay, or 1.6 and 3.4 tons ha–1 on 6 m spaced line-farms, respectively. For denser production in 1.5 m spaced line-farms, estimates ranged between 6.5 and 13.5 tons ha–1. Depending on the different farm setups, we estimated the potential profits (based on delivered cost for consumer product) at $4,468 for a 6 m spaced line-farm of 1 ha and$17,872 for a 1.5 m spaced line-farm. The N and C fixation of kelp ranged depending on spacing of longlines and time of harvest but reached maximum values of 1117 and 6184 kg ha−1, respectively. These estimates offer valuable information that should help producers and managers in their decision to direct efforts and investments into this developing activity in the U.S

What can the shell tell about the scallop? Using growth trajectories along latitudinal and bathymetric gradients to reconstruct physiological history with DEB theory

The great scallop, Pecten maximus, presents a strong variability of growth and reproductive patterns along its spatial distribution range. Such differences in life history traits result from complex interactions between organisms and environmental conditions that can be apprehended through the study of energy dynamics. As the determination of accurate food proxy can be a limitation for modeling bioenergetic, recent work by Lavaud et al. (accepted, this issue), based on the DEB theory, provided a new approach consisting of using temperature and growth time series to reconstruct the required assimilated energy to support observed growth. In this study we present an application of this method to growth trajectories of the great scallop P. maxims used to elucidate: (1) life history traits patterns and (2) the choice of food availability proxies. The inverted DEB model was used to reconstruct the functional response (f) for different age classes of P. maximus in 10 locations of its spatial distribution range. We especially explored the patterns of reconstructed f along latitudinal and bathymetric gradients. Average reconstructed f as well as its maximum value were found to increase with latitude. The variability off, although increasing, did not show a significant relationship with the geographical position. Along the bathymetric gradient strong positive relationships were found between the mean f or its variability and depth. Ontogeny had low effect on the reconstructed f. Furthermore, as the inverted DEB model allows the reconstruction of physiological variables and energy fluxes, we explored the potential differences in reserve and maintenance fluxes dynamics from great scallops living in these contrasting environments. For one of the study sites, comparisons of f with field measurements of 11 food indicators (chlorophyll-a from the pelagic/benthic domains, phytoplankton cell counts, etc.) highlighted the complexity of the functional response and the diet of P. maximus. Pelagic or benthic phytoplankton biovolume, diatoms and dinoflagellates counts and chlorophyll-a were found to be the major contributors to the variability of f. Results suggest that although assimilation is best described by a combination of indicators, chlorophyll-a remains a good enough indicator of food availability for great scallops and bivalves in general

Ocean acidification and molluscan shell taphonomy: Can elevated seawater pCO2 influence taphonomy in a naticid predator–prey system?

The size and frequency of gastropod drill holes in shells of their prey are common indicators of predator-prey ecology in the fossil record. Taphonomic processes occurring after predation, however, can influence the preservation of shells in a given fossil assemblage and can thus influence ecological inferences based on preserved shells. To determine if ocean acidification (OA) has the capacity to influence prey shell taphonomy in a gastropod drilling predation system, we tested for effects of elevated pCO2 on dissolution rates, breakage force, and drill hole diameters in non-fragmented shells of two prey species of the cannibalistic naticid gastropod, Euspira heros. Drilled and non-drilled shells of Littorina littorea and E. heros were exposed to control (~300 μatm) and elevated (~800 and 4000 μatm) pCO2 treatments for five weeks. Dry shell weight and drill hole diameter (outer and inner) were recorded for individual shells before and after exposure; the force required for shell breakage was recorded at the end of the exposure period. Shell mass loss in 800 and 4000 μatm, respectively, were ~1 and 7% for E. heros, and ~0 and 4% for L. littorea, compared to ~0% in the control for both species. Shell breakage force was unaffected by elevated pCO2, but was affected by species and drill hole presence, with E. heros shells requiring a force of ~220 and 269 Newtons in drilled and non-drilled shells, respectively, compared to ~294 and 415 Newtons in L. littorea. At 4000 μatm, outer drill hole diameter significantly increased by ~12% for E. heros, while inner drill hole diameter significantly increased by ~13% in E. heros and ~10% in L. littorea. Ultimately, this study provides the first documentation of molluscan shell taphonomy in the context of OA for a gastropod drilling predation system and sets the stage for future research