Assimilation of shrimp farm sediment by Holothuria scabra: a coupled fatty acid and stable isotope approach

Deposit-feeding sea cucumbers are efficient nutrient recyclers and have the potential to contribute to the limitation of organic matter load in polyculture or integrated aquaculture systems. Assessing how they assimilate organic matter originating from other farmed species is therefore important for the development of such multi-species farming systems. Here, a coupled stable isotope − fatty acid approach was used to characterize the assimilation of organic matter from shrimp (Penaeus stylirostris) farming by Holothuria scabra in an experimental culture system. H. scabra were reared in mesocosms on shrimp farming-originating sediment with and without additional food sources (maize and fish meals). Although fatty acid results did indicate that shrimp-farming sediment was assimilated by holothurids, we found no evidence of maize waste and fish meal contribution to H. scabra organic carbon (no effect on δ13C, no accumulation of meal-specific fatty acids). However, a strong effect of fish meal on H. scabra δ15N was observed, suggesting that this additional food source could represent an alternative source of nitrogen for holothurids. Finally, this study supports the culture of H. scabra as a perspective to reduce sedimentary organic matter excess associated with shrimp farms, and suggest that the addition of selected food sources might contribute to increasing the content in some nitrogen organic compounds in holothurid tissues

Trophic ecophysiology of Nodipecten subnodosus and Spondylus crassisquama bivalves submitted to environmental variability in the lagoon of Ojo de Liebre (Baja California, Mexico)

Les lagunes côtières sont des écosystèmes semi-fermés à l'interface de la terre et des océans et sous l'influence de ces deux compartiments. De par ces caractéristiques, elles sont soumises à de fortes variations spatiales et saisonnières de leurs ressources trophiques. De par leur nature fermée et peu profonde, elles vont amplifier la force des processus qui conditionnent la disponibilité des ressources alimentaires et par conséquent l'écophysiologie des organismes benthiques qui composent les assemblages associés. Ce travail de thèse se propose de caractériser l'écophysiologie trophique de deux espèces de bivalves filtreurs (Nodipecten subnodosus et Spondylus crassisquama) au sein d'une lagune du Pacifique Nord-est (Basse Californie, Mexique). Une approche mufti-tissus et multi-traceurs (isotopes stables, acides gras, stérols et analyse isotopique sur acides gras) a été adoptée afin de pouvoir caractériser l'écologie trophique des espèces, mais aussi leurs régulations physiologiques face aux variations environnementales. Deux facteurs clés se sont révélés largement explicatifs de la variabilité spatio-temporelle observée dans le régime alimentaire : la période (hiver vs été) et la localisation dans la lagune par rapport à l'embouchure. L'importance des apports de phytoplancton océanique a été démontrée dans l'ensemble de la lagune, avec une contribution plus importante de diatomées océaniques notamment en période estivale pour les individus à proximité de l'embouchure. Par ailleurs, les bivalves en fond de lagune semblaient davantage dépendre de la matière organique locale, en particulier issue du recyclage bactérien, voire de la production des herbiers de phanérogames. Ces contrastes spatiaux se reflétaient également dans la composition des membranes cellulaires, mettant en évidence les interactions entre apports trophiques et régulations métaboliques des compositions en acides gras chez ces deux bivalves. Cette thèse présente une approche intégrée dédiée à la compréhension des variations spatiales et saisonnières des ressources trophiques d'un écosystème lagunaire, ainsi que leurs répercutions trophiques et physiologiques sur les assemblages benthiques.Coastal lagoons are semi-enclosed ecosystems at the interface between land and ocean and under the influence of these two compartments. Owing to these characteristics these ecosystems are submitted to spatial and seasonal variations in their trophic resources. Because of their enclosed and shallow nature, lagoons amplify the intensity of processes conditioning the availability of food resources and consequently the ecophysiology of the benthic organisms which compose associated assemblages. This thesis aims to characterize the trophic ecophysiology of two species of suspension feeding bivalves (Nodipecten subnodosus and Spondylus crussisquomo) within a lagoon of Northeast Pacific (Baja California, Mexico). A mufti-tissue and multi-tracer approach (stable isotopes, fatty acids, sterols, and isotope analysis on fatty acids) was used in order to characterise the trophic ecology of both species, as well as their physiological regulations against environmental variations. Two key factors have been found to explain the observed spatio-temporal variability: the period (winter vs summer), and the location in the lagoon with respect to the distance from the mouth. The importance of oceanic phytoplankton inputs has been highlighted throughout the lagoon, with a greater contribution of oceanic diatoms particularly during the summer period for individuals near the mouth. Bivalves from the inner lagoon seemed more dependent of local organic matter, in particular resulting from bacterial recycling, or even from the production of eelgrass. These spatial contrasts were also reflected in the composition of cell membranes, highlighting the interactions between trophic contributions and metabolic regulation of fatty acid composition in both bivalves. This thesis presents an integrated approach to understand spatial and seasonal variations of the trophic resources of a lagoon ecosystem, as well as their trophic and physiological repercussions on benthic assemblages

Ecophysiologie trophique des bivalves Nodipecten subnodosus et Spondylus crassisquama soumis à la variabilité environnementale dans la lagune d'Ojo de Liebre (Basse Californie, Mexique)

Coastal lagoons are semi-enclosed ecosystems at the interface between land and ocean and under the influence of these two compartments. Owing to these characteristics these ecosystems are submitted to spatial and seasonal variations in their trophic resources. Because of their enclosed and shallow nature, lagoons amplify the intensity of processes conditioning the availability of food resources and consequently the ecophysiology of the benthic organisms which compose associated assemblages. This thesis aims to characterize the trophic ecophysiology of two species of suspension feeding bivalves (Nodipecten subnodosus and Spondylus crussisquomo) within a lagoon of Northeast Pacific (Baja California, Mexico). A mufti-tissue and multi-tracer approach (stable isotopes, fatty acids, sterols, and isotope analysis on fatty acids) was used in order to characterise the trophic ecology of both species, as well as their physiological regulations against environmental variations. Two key factors have been found to explain the observed spatio-temporal variability: the period (winter vs summer), and the location in the lagoon with respect to the distance from the mouth. The importance of oceanic phytoplankton inputs has been highlighted throughout the lagoon, with a greater contribution of oceanic diatoms particularly during the summer period for individuals near the mouth. Bivalves from the inner lagoon seemed more dependent of local organic matter, in particular resulting from bacterial recycling, or even from the production of eelgrass. These spatial contrasts were also reflected in the composition of cell membranes, highlighting the interactions between trophic contributions and metabolic regulation of fatty acid composition in both bivalves. This thesis presents an integrated approach to understand spatial and seasonal variations of the trophic resources of a lagoon ecosystem, as well as their trophic and physiological repercussions on benthic assemblages.Les lagunes côtières sont des écosystèmes semi-fermés à l'interface de la terre et des océans et sous l'influence de ces deux compartiments. De par ces caractéristiques, elles sont soumises à de fortes variations spatiales et saisonnières de leurs ressources trophiques. De par leur nature fermée et peu profonde, elles vont amplifier la force des processus qui conditionnent la disponibilité des ressources alimentaires et par conséquent l'écophysiologie des organismes benthiques qui composent les assemblages associés. Ce travail de thèse se propose de caractériser l'écophysiologie trophique de deux espèces de bivalves filtreurs (Nodipecten subnodosus et Spondylus crassisquama) au sein d'une lagune du Pacifique Nord-est (Basse Californie, Mexique). Une approche mufti-tissus et multi-traceurs (isotopes stables, acides gras, stérols et analyse isotopique sur acides gras) a été adoptée afin de pouvoir caractériser l'écologie trophique des espèces, mais aussi leurs régulations physiologiques face aux variations environnementales. Deux facteurs clés se sont révélés largement explicatifs de la variabilité spatio-temporelle observée dans le régime alimentaire : la période (hiver vs été) et la localisation dans la lagune par rapport à l'embouchure. L'importance des apports de phytoplancton océanique a été démontrée dans l'ensemble de la lagune, avec une contribution plus importante de diatomées océaniques notamment en période estivale pour les individus à proximité de l'embouchure. Par ailleurs, les bivalves en fond de lagune semblaient davantage dépendre de la matière organique locale, en particulier issue du recyclage bactérien, voire de la production des herbiers de phanérogames. Ces contrastes spatiaux se reflétaient également dans la composition des membranes cellulaires, mettant en évidence les interactions entre apports trophiques et régulations métaboliques des compositions en acides gras chez ces deux bivalves. Cette thèse présente une approche intégrée dédiée à la compréhension des variations spatiales et saisonnières des ressources trophiques d'un écosystème lagunaire, ainsi que leurs répercutions trophiques et physiologiques sur les assemblages benthiques

Fish morphometric body condition indices reflect energy reserves but other physiological processes matter

Morphometric indices of body condition are assumed to reflect an animal’s health and ultimately its fitness, but their physiological significance remains a matter of debate. These indices are indeed usually considered as proxies of energy reserves, ignoring other physiological processes involved in animal health such as nutritional, immune and hormonal states. Given the wide variety of ecological processes investigated through morphometric body condition indices in marine sciences, there is a clear need to determine whether morphometric indices reflect primarily individuals’ energy reserves or their broader integrated physiological status. To address this issue, we used morphometric and physiological data (cortisol level, oxidative stress, digestive enzymes activity, and both fatty acids percentage and total amount) collected in three stocks of the European sardine (Sardina pilchardus) presenting contrasted patterns of growth and body condition. We found that morphometric body condition indices are indeed mainly and consistently linked to a proxy of the amount of lipid reserves (i.e., fatty acids amount), but also significantly to quality of lipid reserves (i.e., fatty acids percentage) and fish chronic stress (scale cortisol levels). We found no significant relationship between morphometric indices of body condition and both oxidative stress proxies and variables measuring digestive enzymes activity. Our study confirmed that morphometric body condition indices primarily reflect the variance in individuals’ lipid reserves and to a lesser extent the actual composition of these reserves (linked to differences in fish diet) and scale cortisol levels (indicating fish metabolism and/or their chronic stress levels). Therefore, some non-energetic aspects should be considered when studying individuals’ responses to environmental changes and other key physiological processes (oxidative stress proxies, activity of digestive enzymes) should be investigated directly to support scientific-based decision-making in the context of climate change

The relationship between membrane fatty acid content and mitochondrial efficiency differs within- and between- omega-3 dietary treatments

An important, but underappreciated, consequence of climate change is the reduction in crucial nutrient production at the base of the marine food chain: the long-chain omega-3 highly unsaturated fatty acids (n-3 HUFA). This can have dramatic consequences on consumers, such as fish as they have limited capacity to synthesise n-3 HUFA de novo. The n-3 HUFA, such as docosahexaenoic acid (DHA, 22:6n-3) and eicosapentaenoic acid (EPA, 20:5n-3), are critical for the structure and function of all biological membranes. There is increasing evidence that fish will be badly affected by reductions in n-3 HUFA dietary availability, however the underlying mechanisms remain obscure. Hypotheses for how mitochondrial function should change with dietary n-3 HUFA availability have generally ignored ATP production, despite its importance to a cell's total energetics capacity, and in turn, whole-animal performance. Here we (i) quantified individual variation in mitochondrial efficiency (ATP/O ratio) of muscle and (ii) examined its relationship with content in EPA and DHA in muscle membrane of a primary consumer fish, the golden grey mullet Chelon auratus, receiving either a high or low n-3 HUFA diet. Mitochondria of fish fed on the low n-3 HUFA diet had higher ATP/O ratio than those of fish maintained on the high n-3 HUFA diet. Yet, mitochondrial efficiency varied up about 2-fold among individuals on the same dietary treatment, resulting in some fish consuming half the oxygen and energy substrate to produce the similar amount of ATP than conspecific on similar diet. This variation in mitochondrial efficiency among individuals from the same diet treatment was related to individual differences in fatty acid composition of the membranes: a high ATP/O ratio was associated with a high content in EPA and DHA in biological membranes. Our results highlight the existence of interindividual differences in mitochondrial efficiency and its potential importance in explaining intraspecific variation in response to food chain changes

How membrane fatty acids influence sardine size across diverse marine environments

Differences in diet quality and quantity may influence trophodynamic processes in small pelagic fish. Yet, we currently lack direct and comprehensive information on how large-scale areas differ in dietary resources and the degree to which these differences influence fish physiological performances (i.e., growth), ultimately influencing entire fish stocks. Fatty acid composition is one of the bioindicator that can provide insights on how dietary provisions of essential lipids influence the structure of the membrane fatty acids and subsequently fish growth among contrasted habitats. To address this issue, we conducted a large-scale sampling of European sardine (Sardina pilchardus) a species with major socio-economic importance that plays a key role as an energy pathway linking lower and upper trophic levels in pelagic ecosystems. We sampled individuals from the Gulf of Lions (Mediterranean Sea), the Bay of Biscay, and the English Channel (Atlantic Ocean) of age-0 to -3+and found clear spatial differences in the quantity and quality of dietary lipids. Sardines from the Gulf of Lions fed on trophic food web based on dinoflagellates, with greater proportions of DHA (22:6n-3; docosahexaenoic acid) in reserve lipids. Sardines’ reserve lipids had important proportions of zooplankton biomarkers in the English Channel (e.g., 20:1n-9 and 20:1n-11), and diatoms biomarkers such as 16C fatty acids and EPA (20:5n-3; eicosapentaenoic acid) in the Bay of Biscay. The relationship between sardines’ membrane fatty acid composition and individuals’ length changed progressively with individuals’ age, a result consistent across areas, indicating ontogenetic abilities between largest and smallest individuals. Before maturity, largest sardines had higher DHA proportions, followed after maturity by higher proportions of ARA (20:4n-6; arachidonic acid), EPA and DPA (22:5n-3; docosapentaenoic acid). Finally, the study highlights the importance of considering the quality and diversity of dietary resources to better understand how individuals cope with their physiological needs. It is thus important to consider combined aspects (e.g., diet quality and diversity, influence of particular nutrients on length) to better understand the underlying mechanistic processes influencing fish physiology, likely cascading to different expression of their life history traits and affecting fisheries stocks

Red muscle of small pelagic fishes? fillets are high-quality sources of essential fatty acids

International audienceSmall pelagic fishes such as sardine and anchovy are among the richest species in essential fatty acids that are eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA), whose bioavailability may depend on its esterification to polar or neutral lipids. The EPA and DHA quantities in neutral and polar lipids were compared in sardine (from the English Channel) and anchovy (from the Bay of Biscay) fillets, and in red and white muscle separately. Sardine fillets had the highest EPA+DHA content (760 ± 670 vs 370 ± 510 mg/100 g in anchovy fillets), mainly because of their largest proportion of lipid-rich red muscle and its relatively high lipid content. However, DHA esterified to polar lipids was higher in anchovy than in sardine fillet (270 ± 60 vs 230 ± 30 mg/100 g). EPA+DHA content were higher in red than white muscle for both species. This study highlights the nutritional interest of red muscle to provide essential dietary fatty acids to consumers, and the necessity to consider its importance in nutrition studies

How membrane fatty acids influence sardine size across diverse marine environments

International audienceDifferences in diet quality and quantity may influence trophodynamic processes in small pelagic fish. Yet, we currently lack direct and comprehensive information on how large-scale areas differ in dietary resources and the degree to which these differences influence fish physiological performances (i.e., growth), ultimately influencing entire fish stocks. Fatty acid composition is one of the bioindicator that can provide insights on how dietary provisions of essential lipids influence the structure of the membrane fatty acids and subsequently fish growth among contrasted habitats. To address this issue, we conducted a large-scale sampling of European sardine (Sardina pilchardus) a species with major socioeconomic importance that plays a key role as an energy pathway linking lower and upper trophic levels in pelagic ecosystems. We sampled individuals from the Gulf of Lions (Mediterranean Sea), the Bay of Biscay, and the English Channel (Atlantic Ocean) of age-0 to-3 + and found clear spatial differences in the quantity and quality of dietary lipids. Sardines from the Gulf of Lions fed on trophic food web based on dinoflagellates, with greater proportions of DHA (22:6n-3; docosahexaenoic acid) in reserve lipids. Sardines' reserve lipids had important proportions of zooplankton biomarkers in the English Channel (e.g., 20:1n-9 and 20:1n-11), and diatoms biomarkers such as 16C fatty acids and EPA (20:5n-3; eicosapentaenoic acid) in the Bay of Biscay. The relationship between sardines' membrane fatty acid composition and individuals' length changed progressively with individuals' age, a result consistent across areas, indicating ontogenetic abilities between largest and smallest individuals. Before maturity, largest sardines had higher DHA proportions, followed after maturity by higher proportions of ARA (20:4n-6; arachidonic acid), EPA and DPA (22:5n-3; docosapentaenoic acid). Finally, the study highlights the importance of considering the quality and diversity of dietary resources to better understand how individuals cope with their physiological needs. It is thus important to consider combined aspects (e.g., diet quality and diversity, influence of particular nutrients on length) to better understand the underlying mechanistic processes influencing fish physiology, likely cascading to different expression of their life history traits and affecting fisheries stocks

Common carp (Cyprinus carpio) obtain omega-3 long-chain polyunsaturated fatty acids via dietary supply and endogenous bioconversion in semi-intensive aquaculture ponds

Omega-3 long-chain polyunsaturated fatty acids (n-3 LC-PUFA) are essential micronutrients for aquatic consumers. Synthesized by aquatic primary producers, n-3 LC-PUFA are transferred across trophic levels and may eventually end up accumulating in fish. However, if short in dietary supply, fish may also biosynthesize n-3 LC-PUFA from dietary precursors (i.e., n-3 C18-PUFA). We applied compound-specific hydrogen stable isotope analysis (CSIA) of fatty acids to investigate sources and metabolic processes of n-3 LC-PUFA, and in particular of docosahexaenoic acid (22:6n-3, DHA), in Common Carp (Cyprinus carpio) raised in semi-intensive aquaculture ponds. Carp were feeding on natural pond zooplankton and benthic macroinvertebrates rich in n-3 LC-PUFA and cereal-based pellet feeds rich in C18-PUFA. Results provide isotopic evidence that carp obtained a significant amount of dietary lipids and nitrogen from added cereal-based feeds, while n-3 LC-PUFA were generally acquired by feeding on benthic macroinvertebrates and zooplankton. However, DHA retained in carp was also generated endogenously via bioconversion from dietary PUFA precursors, such as EPA. DHA was isotopically lighter than EPA and likely not supplied in sufficient quantities to meet the physiological requirements for DHA in carp. Our data show that depending on the natural abundance of dietary DHA in these eutrophic ponds, farmed carp can obtain DHA by two different pathways; i.e., directly via dietary uptake and indirectly via bioconversion. This field study highlights the importance of dietary LC-PUFA supply in eutrophic aquatic ecosystems and the ability of carp to biosynthesize highly valuable LC-PUFA, eventually also benefiting human health

Red muscle of small pelagic fishes’ fillets are high-quality sources of essential fatty acids

Small pelagic fishes such as sardine and anchovy are among the richest species in essential fatty acids that are eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA), whose bioavailability may depend on its esterification to polar or neutral lipids. The EPA and DHA quantities in neutral and polar lipids were compared in sardine (from the English Channel) and anchovy (from the Bay of Biscay) fillets, and in red and white muscle separately. Sardine fillets had the highest EPA+DHA content (760±670 vs 370±510 mg/100 g in anchovy fillets), mainly because of their largest proportion of lipid-rich red muscle and its relatively high lipid content. However, DHA esterified to polar lipids was higher in anchovy than in sardine fillet (270±60 vs 230±30 mg/100 g). EPA+DHA content were higher in red than white muscle for both species. This study highlights the nutritional interest of red muscle to provide essential dietary fatty acids to consumers, and the necessity to consider its importance in nutrition studies