The link between longevity and mitochondrial function has been documented; therefore, we suspect that the evolution of mitochondrial DNA (mtDNA) is linked to the evolution of longevity. We selected 128 fish species with a wide range of longevity and inhabiting habitats with differing temperatures and examined their association with dN/dS ratios of mtDNA genes. Our findings (i) rule out environmental temperature as a primary driver of longevity, (ii) confirm the negative relationship between synonymous substitution rate and longevity for four of the mitochondrial protein coding genes, (iii) reveal a correlation of the fish body length at maturity with the dN/dS ratio for ATP6, ND1 and ND4, and (iv) highlight for the first time to our knowledge, a link between high conservation of the three cytochrome c oxidase (COX) genes and adaptation to temperatures in fishes. By extending conclusions drawn from mtDNA to individual genes, our study opens new avenues for exploring the ageing process. Moreover, the specific link between the evolution of COX genes and habitat temperature confirms the importance of complex IV in temperature adaptation. Our findings also suggest a link between dN/dS in complex I genes and longevity, highlighting the need to examine the functional association between their encoded peptides and lifespan. This article is part of the theme issue 'Evolutionary genetics of mitochondria: on diverse and common evolutionary constraints across eukarya'.

Studying mitochondrial respiratory function is critical to understanding the plasticity of cellular energetics. Mitochondrial respiratory function is usually studied ex vivo and requires isolation of high-quality mitochondrial preparations. However, mitochondria are usually damaged by this process, and the degree of damage is typically assessed by measuring respiratory control ratios (RCRs) and the change in respiration rate mediated by exogenous cytochrome C addition to isolated mitochondrial preparations. The standard thresholds in the field for determining whether isolated mitochondria are “acceptable” are based on studies in common laboratory rodents and are entirely arbitrary. However, zoologists are increasingly employing nonstandard animal models in the study of mitochondrial respiratory function across a wide variety of fields and there is growing evidence that the canonical thresholds of acceptable RCRs and the cytochrome C response that have been used to identify healthy mitochondrial preparations may not be useful in other species. In this commentary, we discuss the limitations of using RCRs and cytochrome C-mediated changes in mitochondrial respiration in the study of nontraditional laboratory species and propose alternative means of evaluating mitochondrial integrity that may permit more accurate assessment of the quality of mitochondria isolated, and thus better support comparison of data across species and studies.

The theory of optimal cell size postulates that cell size imposes constraints on oxygen delivery in larger cells owing to their smaller surface-area-to-volume ratios. Smaller cells, with a higher surface-area-to-volume ratio, have an increased capacity to take up oxygen, which is therefore expected to increase their heat tolerance (CTmax). However, the precise mechanisms linking cell size, body size and heat tolerance remain unclear. We obtained contrasts in cell size by raising diploid and triploid juvenile Daphnia at different temperatures. Daphnia raised at lower temperatures had larger cells than those raised at higher temperatures. Triploid clones had larger cells than diploid clones at 16°C, 20°C and 24°C. CTmax increased with acclimation temperature and was negatively correlated to both cell and body size. Triploid clones had lower CTmax values than both subarctic and temperate diploid clones at 16°C and 20°C. Heat shock significantly increased the expression of Hsp70 and catalase, but these were not correlated with CTmax or ploidy, suggesting that heat tolerance was not directly linked to heat-shock proteins or oxidative stress responses. These findings highlight the role of cell size and polyploidy in shaping the heat tolerance and geographic distribution of ectotherms.

To engage undergraduate marine biology students and demonstrate the relevance of energy metabolism to their field, we developed laboratory activities that integrate cellular metabolism with the biology of marine invertebrates. Our approach has the potential to uncover specific adaptations in energy pathways associated with hypoxia tolerance. A key difference between marine invertebrates and vertebrates lies in their anaerobic metabolism. Whereas vertebrates typically utilize lactate dehydrogenase (LDH) to produce lactate as the end product of anaerobic glycolysis, marine invertebrates employ a variety of dehydrogenase pathways. This diversity enables efficient anaerobic energy production and reduces the accumulation of harmful by-products. We used two abundant polychaete species (Nephtys caeca and Alitta virens) found on the eastern Atlantic coast of Canada. Students measured the maximal activities of key enzymes of anaerobic (LDH, pyruvate kinase, and opine dehydrogenases) and aerobic (electron transport system, pyruvate kinase, malate dehydrogenase, and aspartate aminotransferase) metabolism. The presence of two opine dehydrogenases (strombine and alanopine) was observed in N. caeca, whereas LDH activity was marginal. Opine dehydrogenases are homologous to LDH and help buffer acidification during hypoxia. In A. virens, only LDH is present. As a general marker of aerobic capacity and hypoxia tolerance in invertebrates, malate dehydrogenase activity was high in both species. This laboratory activity introduces undergraduate students to metabolic adaptations and alternative energy pathways in marine life, particularly in the intertidal zone. This activity, conducted at the beginning of the semester, captured their interest and motivated them to study the key theoretical concepts governing animal energetic metabolism.NEW & NOTEWORTHY Polychaetes (bristle worms) are common in the marine coastal area of the North Atlantic. Some are active, and others are more sedentary, but most of them are regularly exposed to hypoxic conditions. To reveal potential adaptations that meet their bioenergetic requirements, students explored their cellular enzymatic machinery and compared two species in terms of their strategies for exploiting the habitat.

In fish, polyunsaturated fatty acids (PUFAs) are essential structural elements in cellular membranes, participate in pathway regulation and act as important energy storage sources for optimum growth performance. However, they are also highly susceptible to peroxidation and thus potential oxidative damage. Omega-3 fatty acid content can vary among individuals and populations of fish and can therefore modulate their health status or resistance to oxidative stress. Our objective was to modulate $ \Sigma $ omega-3 content in fish through different diets and estimate its impact on growth performance, overall fatty acid composition, oxidative stress parameters and antioxidant activity. We conducted experiments on juveniles (1+) of four salmonid groups: Arctic charr (Salvelinus alpinus), brook charr (Salvelinus fontinalis) and their reciprocal hybrids. We found that growth performance in the four groups was negatively affected by high dietary fatty acid content. The content of thiobarbituric acid reactive substances (TBARS, a marker of lipids peroxidation) significantly rose in Arctic charr when fed the omega-3-rich diet. It was also observed that individuals with high docosahexaenoic acid and low $ \Sigma $ omega-6 content had lower TBARS content. Consequently, high omega-3/omega-6 ratios were accompanied by lower oxidative stress levels. This supports the utilization of omega-3/omega-6 ratios as a marker of the ability of fish to modulate oxidative stress both in the wild and in an aquaculture context. This will further help to predict responses to environmental or nutritional modifications.

Environmental changes can influence species development, growth, size, distribution, and abundance, and when having a negative impact, they can potentially lead to a species' decline, and ultimately its local extinction. Consequently, evaluating the impacts of ocean global change drivers, in isolation and in combination, is particularly relevant for ecologically and economically important species which guarantee food security and income for coastal communities. This study aimed to determine the physiological responses of the northern shrimp Pandalus borealis to different combinations of ocean warming (OW), acidification (OA) and hypoxia at multiple levels of its biological organization (i.e. from the whole-organism to the cell), to help in predicting with greater accuracy the fate of this species in a rapidly changing ocean. To do so, shrimp were exposed for 30 d to different combinations of seawater temperature (2, 6 or 10°C), pH (7.75 or 7.40 pHT) and oxygen (100 or 35% relative to air saturation), and their survival, whole-organism aerobic performance, and cellular energetic capacity were characterized. Our results show that shrimp were overall tolerant to the isolated effects of OW, OA and hypoxia, but when exposed to combined drivers their survival and whole-organism aerobic performance severely decreased. Isolated and combined drivers had overall no effect on enzyme activity, suggesting a low capacity for metabolic reorganization. Nonetheless, under combined drivers, we observed an adjustment of the mitochondrial enzyme stoichiometry that might help cells to maintain their energy production efficiency. Overall, the northern shrimp's physiological status is compromised under combined ocean global change drivers, which together with the high mortality levels observed, point to a potential risk for local commercial collapse. Our results will be useful to refine mechanistic modelling for future abundance and distribution, in order to improve stock assessments, management and conservation of the northern shrimp under ongoing global changes.

Variations in environmental oxygen availability can induce oxidative stress in mammalian cells; episodes of hypoxia/re-oxygenation can be deleterious to cardiac function. Subterranean-living African naked mole-rats putatively experience repeated bouts of hypoxia/re-oxygenation in their natural habitat and are among the most hypoxia-tolerant mammals. To mitigate the potentially deleterious effects of frequent hypoxia/re-oxygenation exposure, naked mole-rats possess cardiac mitochondrial adaptations that may limit oxidative damage caused by fluctuating environmental oxygen levels. These include low respiratory flux through complex II (succinate dehydrogenase) of the mitochondrial electron transport system and robust cardiac reactive oxygen species (ROS) scavenging capacities. We hypothesized that these specializations are common traits in all hypoxia-tolerant African mole-rats. To test this hypothesis, we evaluated mitochondrial respiration and both ROS efflux and scavenging capabilities from naked mole-rats, six additional hypoxia-tolerant African mole-rat species, and hypoxia-intolerant mice (Mus musculus), rats (Rattus norvegicus; non-subterranean), and star-nosed moles (Condylura cristata; subterranean). We found a clear and inverse relationship between complex II-fuelled respiration of isolated mitochondria and hypoxia-tolerance across all species tested. Conversely, we found no relationship between hypoxia-tolerance and rates of complex I-fuelled respiration, H2O2 efflux (with any substrate), or mitochondrial H2O2 scavenging capacity. Our results suggest that downregulating the catalytic capacity of cardiac mitochondrial complex II may be an adaptation that supports systemic hypoxia-tolerance in African mole-rats.

In Northern Canada, pollution from mining discharges represents a significant environmental stressor for aquatic organisms. Variations in water temperature constitute another source of stress for fish. Although numerous studies have investigated the effects of environmental stressors on fish physiology, research specifically addressing their impact on energy metabolism pathways remains limited. In this study, we investigated the effects of manganese (Mn), thermal acclimation, and their combination on cellular energy metabolism pathways in Arctic charr, a cold-water stenotherm. Juvenile charr were acclimatized to two contrasting temperatures (7 degrees C and 16 degrees C) for two weeks. Thereafter, half of the specimens where exposed to Mn (1 mg/L) for eight weeks. After 56 days, mortality was higher in fish acclimatized to 16 degrees C compared to 7 degrees C. Trace metal analysis performed by ICP-AES showed that bioaccumulation of Mn in gills and kidney was higher at 7 degrees C than at 16 degrees C, while the bioaccumulation of Mn in liver and muscle was not affected by temperature. Enzyme assays performed in liver and muscle showed a decrease in aerobic capacity and an increase in glycolytic capacity caused by Mn combined with a high temperature. Hepatic cytochrome C oxidase activity was significantly lower in fish acclimatized at 16 degrees C and exposed to Mn compared to other treatments. Hepatic citrate synthase activity showed a decrease in fish from the 16 degrees C and Mn treatment compared to those at 7 degrees C without Mn exposure. In both tissues, phosphofructokinase activity increased in fish acclimatized at 16 degrees C and exposed to Mn compared to both treatments at 7 degrees C. Hepatic lactate dehydrogenase activity was lower at 16 degrees C than at 7 degrees C in fish from the control treatment. The activity of beta-hydroxyacyl-CoA dehydrogenase was unaffected by temperature or Mn. These results suggest that Mn, combined with high temperature, may affect mitochondrial function leading to a decrease in aerobic capacity. In response to the decline of cellular respiration capacity, metabolic pathways responded differently. Aerobic glycolysis was stimulated, while lipid metabolism showed no metabolic adjustment. This study represents one of the first steps towards understanding Mn toxicity in the context of climate change in a cold-water stenothermic species, and its impact on fish health and metabolism.

Freshwater fishes are one of the most threatened animal taxa in North America. In Canada, roughly 30% of the occurring species are currently listed and under protection, including redhorses. This review covers Moxostoma spp. ecology, biology, conservation efforts, and highlights challenges to galvanize actions and outcomes through research. The threats to their survival are strongly associated to increasing anthropogenic pressures, superimposed by climate change effects. In Canada, recovery plans for the copper and the black redhorse, and a management plan for the river redhorse, are operational. The recovery strategy for the copper redhorse relies on stocking campaigns of 0+ juveniles, which was exclusively based on artificial breeding of captured wild broodstock. A conservation aquaculture program that includes genetic diversity and adaptation considerations was recently initiated, and the areas of refinement identified are the following: broodstock and early-life rearing protocols and environmental and physical enrichment protocols to improve juveniles’ post-release fitness. Research through the prism of conservation physiology is proposed in the identification welfare and health bioindicators and adaptability/response to climatic change. Concurrently, aquatic ecosystem protection/restoration, control of invasive species, eDNA detection/telemetry tracking, and post-release monitoring efforts should also be reinforced.

Identification of physiological processes setting thermal tolerance limits is essential to describing adaptive response to temperature changes. We used the North American Daphnia pulex complex, which makes a remarkable model for comparative physiology as it is composed of clones differing in heat tolerance and ploidies, and with a wide geographic distribution. The fatty acid composition of 18 diploid and triploid D. pulex clones acclimated to 16 degrees C and 24 degrees C was measured and compared with their tolerance to extreme high and low temperatures (CTmax and CTmin, respectively). Eicosapentaenoic acid (EPA) relative content showed a strong negative relationship with CTmax and a clear association with CTmin. Higher unsaturation and peroxidation indices were associated with better cold tolerance, whereas saturated fatty acids and monounsaturated fatty acids were associated with lower cold tolerance. Triploid D. pulex clones accumulated more EPA and had lower CTmin than diploid clones (better cold tolerance). Triploid clones retained more omega-6 polyunsaturated fatty acids at high temperature. CTmax was positively correlated with CTmin, suggesting the existence of important constraints in temperature tolerance caused by fatty acid composition.

Mitochondria play a key role in aging. Here, we measured integrated mitochondrial functions in experimentally evolved lines of the seed beetle Acanthoscelides obtectus that were selected for early (E) or late (L) reproduction for nearly 4 decades. The 2 lines have markedly different lifespans (8 days and 13 days in the E and L lines, respectively). The contribution of the NADH pathway to maximal flux was lower in the L compared to the E beetles at young stages, associated with increased control by complex I. In contrast, the contribution of the Succinate pathway was higher in the L than in the E line, whereas the Proline pathway showed no differences between the lines. Our data suggest that selection of age at reproduction leads to a modulation of complex I activity in mitochondria and that mitochondria are a functional link between evolutionary and mechanistic theories of aging.

Abstract Both in their natural habitat (estuaries, marine coastal environment, ocean depths and freshwater lakes) or in captivity conditions (land‐based, open‐sea aquaculture and aquariums), exposure to hypoxia can have direct detrimental effects on fish growth, reproduction, behaviour and health. The objective of this study was to investigate the effects of chronic exposure of spotted wolffish (Anarhichas minor) (∼1.4 kg) and the interspecific hybrid (A. minor × A. lupus) (∼600 g) to moderate hypoxia levels (dissolved oxygen [DO]: 40%, 50% and 60% saturation) in comparison to a normoxia group (control 100%) over a period of 14 weeks at ∼7.5°C. The trials were conducted as a common‐garden experiment (both fish groups reared together) in quadruplicate (4 tanks per DO level = 16 tanks). Fish performance (specific growth rate, feed intake [FI]) and physiological status (condition factor [K] and hepatosomatic index, haematocrit) were monitored at different intervals. The metabolic enzyme activity of citrate synthase (CS), lactate dehydrogenase (LDH) and pyruvate kinase (PK) was measured as well as antioxidant enzymes glutathione reductase and catalase. Oxidative stress indices were assessed by the quantification of thiobarbituric acid reactive substances (TBARS) and the measurement of the enzymatic activity level of aconitase. Significant reduction in growth rate occurred at DO 40%. DO was identified as a major driver of FI. Our results indicate a very strong adaptation to hypoxia as (1) exposures to DO 40% were not severe enough to affect aerobic or anaerobic metabolism capacity or to significantly induce oxidative stress and (2) metabolic organization of the muscle tissue, as expressed by LDH, CS and PK is not affected by DO levels down to 40%. However, at the lowest DO levels (40% and 50%), hybrid fish displayed significantly better growth than the spotted wolffish.

Although a mechanism accounting for hyperthermic death at critical temperatures remains elusive, the mitochondria of crucial active excitable tissues (i.e. heart and brain) may well be key to this process. Mitochondria produce ∼90% of the ATP required by cells to maintain cellular integrity and function. They also integrate into biosynthetic pathways that support metabolism as a whole, allow communication within the cell, and regulate cellular health and death pathways. We have previously shown that cardiac and brain mitochondria demonstrate decreases in the efficiency of, and absolute capacity for ATP synthesis as temperatures rise, until ultimately there is too little ATP to support cellular demands, and organ failure follows. Importantly, substantial decreases in ATP synthesis occur at temperatures immediately below the temperature of heart failure, and this suggests a causal role of mitochondria in hyperthermic death. However, what causes mitochondria to fail? Here, we consider the answers to this question. Mitochondrial dysfunction at high temperature has classically been attributed to elevated leak respiration suspected to result from increased movement of protons (H+) through the inner mitochondrial membrane (IMM), thereby bypassing the ATP synthases. In this Commentary, we introduce some alternative explanations for elevated leak respiration. We first consider respiratory complex I and then propose that a loss of IMM structure occurs as temperatures rise. The loss of the cristae folds of the IMM may affect the efficiency of H+ transport, increasing H+ conductance either through the IMM or into the bulk water phases of mitochondria. In either case, O2 consumption increases while ATP synthesis decreases.

Heart failure is among the first major consequences of heat stress in aquatic ectotherms. Mitochondria produce most of the ATP used by the heart and represent almost half of the volume in cardiac cells. It has therefore been hypothesized that mitochondrial dysfunction may be a major cause of heart failure associated with heat stress. The present study aims to investigate if CT max is linked to the thermal sensitivity of cardiac mitochondria in the three-spined stickleback ( Gasterosteus aculeatus), and if it is influenced by heart fatty acid composition and age. To do so, we measured the CT max of 30 fish. The cardiac mitochondrial oxygen consumption was measured by high resolution respirometry at three temperatures and heart lipid profiles were obtained by gas chromatography (GC) coupled with a flame ionization detector (FID). Fish age was estimated via otolith readings. Fatty acid profiles showed no correlation with CTmax, but EPA levels were higher in older individuals. Mitochondrial respiration was measured in 35 fish using high-resolution respirometry. It was strongly affected by temperature and showed a drastic drop in OXPHOS respiration fed by complex I and complex I+complex II, while uncoupled respiration plateaued at CT max temperature. Our results suggest that complex I is an important modulator of the impact of temperature on mitochondrial respiration at high temperatures but is not the main limiting factor in physiological conditions (maximal OXPHOS). Mitochondrial respiration was also affected by fish age, showing a general decrease in older individuals.

The link between longevity and mitochondrial function has been documented for years. Since mitochondrial DNA (mtDNA) encodes for electron transport system (ETS) proteins, we could suspect that its evolution is linked with that of longevity. A negative relationship has been documented between the synonymous substitution rate and lifespan when analyzing the whole mitochondrial genome in animals. In this study, we aimed to confirm this negative correlation for each of the mitochondrial protein coding genes (mtPCGs) and explore potential relationships between adaptation to extreme temperatures and the evolution of mtDNA. To this end, we selected 112 species of fish with a wide range of longevity as well as divergences in environmental temperature, which is a good proxy for energy metabolism in these animals. Our results 1) challenge the “rate of living” theory by not showing any correlation between longevity and environmental temperature, 2) confirm the negative relationship between substitution rate and longevity for each of the 13 mtPCGs, and 3) highlight for the first time a link between high conservation of the three COX genes and adaptation to warmer temperatures in fish. By challenging a paradigm and extending the conclusions made for mtDNA to individual genes, our study opens a wide field to be explored concerning study of the aging process. Moreover, the specific link between the evolution of COX genes and temperature tolerance confirms the importance of complex IV in adaptation to extreme temperatures and, more generally, the importance of distinguishing gene families when studying mtDNA evolution in animals.### Competing Interest StatementThe authors have declared no competing interest.

Overwinter feed restriction followed by spring refeeding is proposed as a strategy to improve productivity and sustainability of Arctic charr production. A 257-day experiment was conducted with different feeding regimes to evaluate compensatory growth response in growth and physiological state of juvenile fish (150-200 g) reared under seasonal temperature and photoperiod. Five experimental groups in replicates were created based on frequency (C = continuous and P = periodic) and feed restriction level (0, 50 and 100%): C100%, P50%, C50%, P0% and C0%. After a period of acclimation of one month, two distinct phases of the growth trial were conceived: a restriction period (102 days) followed by a refeeding period (126 days). The growth (SGR's, organ indexes (HSI, CSI, ISI and VSI), FCE and FI) and pyloric caeca digestive (TRYP, CHY) and metabolic (LDH and CS) enzyme activity, stress levels (cortisol, HSP70 and hematocrit), morphometric traits (body mass, length and K) and muscle proximate composition were evaluated at different intervals. Our results indicate that 1) a limited period of food restriction (P0%) or a prolonged starving (C0%) enabled the observation of a complete growth compensation after 86 and 126 days post-refeeding respectively with improved feed conversion efficiency (FCE of 1.20 for P0% and C0% compared to 1.06 for the control); 2) Arctic charr under a fair level of food reduction applied either periodically (P50%) or continuously (C50%) can achieve similar growth than un-restricted fish; 3) during the refeeding period, lower variability in growth was successfully induced (C100% > P50% > C50% > P0% > C0%); 4) rapid size or mass adjustment of key digestive organs such as pyloric caeca and intestine is associated with feed restriction and refeeding (reduction and increase in relative size respectively); 5) enzymatic activities of TRY, LDH and CS measured at the last sampling of the restriction phase indicate some level of adjustments that quickly receded to levels similar to the control group (9 days post-refeeding); 6) lipid content value was significantly higher in fish from the C100% group in comparison to C50%, P0% and C0% groups at the end of the restriction phase, indicating that lipid depletion is a prerequisite to compensatory growth induction and 7) in comparison to the control un-restricted fish, the stress levels, as estimated by stress markers (cortisol, HSP70 or hematocrit) were not affected by the level of feed restriction. Feed restriction has been successfully used to promote compensatory and catch-up growth. Here we suggest that studies are however required to further explore to which extent feed-restriction could induce vulnerability of Arctic charr, during sub-optimal growth conditions. Finally, defining the best sequence of feed restriction and refeeding should ensure imple-mentation of production and benefit while maintaining optimal health conditions.

Decreased productivity in long-lived bird species is linked to prey depletion in marine ecosystems. Seabirds, however, exhibit behavioral flexibility at individual level to prevent this outcome. One such strategy to alleviate any impact on fitness would be to divorce from their partners. Although changing mates and increasing foraging effort have been shown to increase or maintain reproductive success, how the behavioral flexibility affects fundamental physiological parameters remains to be elucidated. Here, we compared physiological components (nutritional status, muscle damage and oxidative stress) of northern gannets ( Morus bassanus ) in relation to their partnership status and foraging effort. Specifically, we used a cross-sectional data set (at the population level) of three contrasted years to compare retained and changed mates. We predicted that mate change is a stressful event with impacts on health condition and those effects are higher during unfavorable years with food depletion. Our study showed that gannets changing mate increase parental effort only during years of low food abundance, with consequences on health condition (increased body mass loss, higher protein catabolism and higher oxidative damage during chick rearing period). Ultimately, our study suggests that partnership decision is not likely to reduce the long-term quality and the fitness of parents. Reproduction during harsh conditions would however likely be one of the primary causes of individual quality loss and fitness decline in this long-lived bird species.

Researchers from diverse disciplines, including organismal and cellular physiology, sports science, human nutrition, evolution and ecology, have sought to understand the causes and consequences of the surprising variation in metabolic rate found among and within individual animals of the same species. Research in this area has been hampered by differences in approach, terminology and methodology, and the context in which measurements are made. Recent advances provide important opportunities to identify and address the key questions in the field. By bringing together researchers from different areas of biology and biomedicine, we describe and evaluate these developments and the insights they could yield, highlighting the need for more standardisation across disciplines. We conclude with a list of important questions that can now be addressed by developing a common conceptual and methodological toolkit for studies on metabolic variation in animals.

Background Life history theory predicts trade-offs between reproduction and survival in species like the northern gannet (Morus bassanus). During breeding, demanding foraging conditions lead them to expand their foraging range and diversify their diet, increasing the risk of reproductive failure. Changing partners may enhance breeding success but lead to more physiological costs. Methods To investigate the physiological costs of reproduction upon partner changes, we measured and compared 21 biomarkers related to telomere dynamics, oxidative stress, inflammation, hematology, nutritional status, and muscle damage. We used a longitudinal approach with gannets (n = 38) over three contrasting years (2017, 2018 and 2019). Results Our results suggest that annual breeding conditions exert a greater influence on physiological changes than partnership status. Individuals that changed partner experienced greater short-term stress than retained partners. This transient increase in stress was marked by short-term increases in oxidative lipid damage, lower antioxidant capacity, signs of inflammation, and greater weight loss than individuals that retained partners. During favorable conditions, individuals that changed mates had stabilized telomere length, decreased antioxidant capacity, glucose concentration, and muscle damage, along with increased oxygen transport capacity. Conversely, unfavorable breeding conditions led to increased telomere attrition, stabilized antioxidant capacity, decreased inflammation susceptibility, diminished oxygen transport capacity, and increased muscle damage. In the cases where partners were retained, distinct physiological changes were observed depending on the year’s conditions, yet the telomere dynamics remained consistent across both partnership status categories. During the favorable year, there was an increase in unsaturated fatty acids and oxygen transport capacity in the blood, coupled with a reduction in inflammation potential and protein catabolism. In contrast, during the unfavorable year in the retained mates, we observed an increase in oxidative DNA damage, antioxidant capacity, weight loss, but a decrease in inflammation susceptibility as observed in changed mates. Discussion Our study shows that behavioral flexibility such as mate switching can help seabirds cope with the challenges of food scarcity during reproduction, but these coping strategies may have a negative impact on physiological status at the individual level. In addition, the marked reduction in telomere length observed during harsh conditions, coupled with the stabilization of telomere length in favorable conditions, highlights the long-term physiological impact of annual breeding conditions on seabirds. These findings underscore the effect on their potential survival and fitness, emphasizing that the influence of annual breeding conditions is greater than that of partnership status.