Biological invasions are a major driver of biodiversity erosion mainly because invasive species show greater trophic impact than their non-invasive counterparts. The experimental paradigm for assessing this trophic impact is the functional response (FR) test that describes the relationship between per capita consumption rate and resource density. Two key parameters are then assessable and comparable between populations and species: the space clearance rate (attack rate, a) measuring predatory efficiency at low prey densities, and handling time (h) representing the time required to capture, handle and digest prey. This test is frequently conducted to compare non-invasive and invasive species and shows that invasive species have a higher FR than non-invasive species (characterized by higher space clearance rates and lower handling times) which would explain both their invasion success and their ecological impact. However, it appears that whether FR parameters differ between invasive species sampled in their native versus invasion range has never been tested, implicitly assuming that FR measures can be extrapolated to the entire range of distribution. Using a phylogenetically corrected comparative analysis of 269 FR observations from 45 freshwater fish species (23 non-invasive species and 22 invasive species), we confirm that invasive species exhibited higher FR than non-invasive species. However, this pattern holds true only when considering invasive species sampled in their native range. Invasive species studied in their invasion range displayed functional responses comparable to non-invasive species, with similar space clearance rates and handling times. Additionally, space clearance rates decreased with temperature in non-invasive species but tended to increase in invasive species from invasive introduction ranges, suggesting that climate warming may exacerbate competitive asymmetries. Together, these results indicate that high FR predispose species to invasiveness, but also challenge the assumption that FRs measured in the native range of a species can be directly extrapolated to predict its trophic impacts elsewhere. Our findings call for greater consideration of biogeographic context when using functional responses to assess invasion risk and ecological impact.
Environmental stochasticity in abiotic factors is inherent to ecosystems and is exacerbated by global change. However, experimental protocols typically cancel this factor by using cyclic or constant conditions, limiting the study of environmental variations. This simplification highlights the need for better methodological tools to control fluctuating environmental variables. We present here a guidance and solution for generating and implementing stochastic environmental conditions through our Raspberry Pi System for environmental Stoch asticity (PiStoch). This low‐cost, low‐tech and scalable method for mesocosm experiments also has the potential to replicate any other form of variability, including cyclic patterns. This system successfully reproduced stochastic time series in temperature and oxygen manipulation experiments. Testing with two biological case studies (macrophyte biomass and freshwater fish oxygen consumption), it demonstrated that thermal stochasticity had stronger effects than mean temperature, highlighting the importance of studying fluctuating conditions. Developing accessible methods to study organismal responses to environmental stochasticity is essential for improving the realism of laboratory experiments and enhancing the accuracy of physiological and ecological predictions.
Heat stress events will be more frequent and intense in the future. These events will challenge the capacity of organisms to exhibit sufficient metabolic flexibility to adapt to such variations. To better understand the acclimation processes implemented in response to acute warming, with an integrative approach we examined in vivo metabolic rate and cardiac mitochondrial respiration in the Rhône streber, during and after a heat stress on a precise time line. The temperature was raised from 13°C to 18°C (+1°C per hour) and maintained at 18°C for 5 days, before returning to 13°C at the same rate. We repeatedly measured, during the heat stress and 5 days after the end of the event, in vivo metabolic rate in the same individuals and cardiac mitochondrial respiration from different individuals. At the organismal level, oxygen consumption increased in line with warming, and was followed by a return to pre-acclimated levels just after the end of the heat stress. Conversely, cardiac mitochondrial respiration decreased during the heat stress, especially 24 h in, and recovered at the end of the event. Our results suggest that the heat stress was responsible for a metabolic mismatch in the strebers. Indeed, we observed (i) a strong thermodynamic effect without any acclimation process, suggesting that the range of temperatures chosen was not stressful for the fish, and (ii) the establishment of a transitory energy saving process. Our results underline the need for more integrative studies to understand how organisms will adapt to climate change.
Here, we investigate whether the elevated mitochondrial H2O2 release in small mammals arises from a tradeoff between NAD-dependent enzymes, which synthesizes NADH to support high oxidative phosphorylation, and NADP-dependent enzymes, which generates NADPH to detoxify H2O2 within the matrix. We measured the activities of NAD- and NADP-dependent enzymes in skeletal muscle mitochondria from mammal species ranging from 4 g to 600 kg. The activities of the two most active NADPH-producing enzymes increased, whereas NAD-dependent enzyme activities declined with body mass. Therefore, small mammals prioritize NADH synthesis at the expense of NADPH, increasing the oxidative cost of mitochondrial metabolism.
A wave of studies has recently emphasized the influence of sex chromosomes on both lifespan and actuarial senescence patterns across vertebrates and invertebrates. Basically, the heterogametic sex (XY males in XX/XY systems or ZW females in ZW/ZZ systems) typically displays a lower lifespan and a steeper rate of actuarial senescence than the homogametic sex. However, whether these effects extend to the senescence patterns of other phenotypic traits or physiological functions is yet to be determined. Here, we investigated whether sex chromosomes modulate reproductive senescence using females from the African pygmy mouse (Mus minutoides). This biological model exhibits an odd sex determining system with a third, feminizing sex chromosome, X*, resulting in three distinct female genotypes (XX, X*X, or X*Y) that coexist in natural populations. We found that the rate of senescence in litter size at birth is much more pronounced in heterogametic X*Y females than in homogametic XX or X*X females that may support the unguarded X or toxic Y hypotheses and can be directly linked to the complex and unique X*Y phenotype. A decrease in neonatal survival with mother's age has also been found, but this decline is not different between the three female genotypes.
Thermoregulation is a major challenge for extremely small mammals such as the African pygmy mice Mus mattheyi and Mus minutoides, weighing less than 12g. A previous study showed that these tiny mice exhibit different mitochondrial energy efficiency for ATP synthesis, with a higher efficiency in M. mattheyi (∼6 g) than in M. minutoides (∼10 g). This result suggests a lower mitochondrial heat production at rest in M. mattheyi, despite its lower body weight and inevitably greater heat loss from its body surface, than in M. minutoides. Consequently, a compensatory thermoregulatory strategy should exist in M. mattheyi to maintain homeothermy. The present study aimed to assess whether M. mattheyi uses non-shivering thermogenesis in brown adipose tissue (BAT) and/or activity-thermoregulatory heat substitution. For this purpose, multidisciplinary approaches involving behavioral, physiological, biochemical and molecular analyses were used. Mus mattheyi showed higher daily mass-specific energy expenditure and food intake per unit weight and allocated more daily energy to vital function, spent less time moving in their cage during daytime but exhibited higher non-locomotor activity and higher movement-related energy cost compared to M. minutoides. BAT of M. mattheyi, was metabolically more active, exhibiting higher mitochondrial respiration rates and citrate synthase activity than in M. minutoides, but lower uncoupling protein 1 content. Altogether, these results suggest that the tiny M. mattheyi mainly uses non-exercise activity thermogenesis, increased cost of movement, and to a lesser extent BAT non-shivering thermogenesis for remaining warm.
The primary objective of this study was to assess whether adenine nucleotide translocase (ANT) content could be associated with phylogenetic disparities in mitochondrial coupling efficiency, within liver mitochondria obtained from rats, crocodiles, and ducklings. Our measurements included mitochondrial membrane conductance, ANT content, and oxidative phosphorylation fluxes at various steady-state rates. We observed significant variations in liver mitochondrial coupling efficiency across the three species. These variations correlated with interspecific differences in mitochondrial oxidative capacity and, to a lesser extent, the ANT content of liver mitochondria. These findings expand upon previous research by highlighting the pivotal role of oxidative capacity and ANT in modulating mitochondrial efficiency on an interspecific scale.
Despite a number of studies showing a negative relationship between age and telomere length, the universality of this pattern has been recently challenged, mainly in ectothermic animals exhibiting diverse effects of age on telomere shortening. However, data on ectotherms may be strongly affected by the thermal history of the individuals. We thus investigated the age-related changes in relative telomere length in the skin of a small but long-lived amphibian living naturally in a stable thermal environment over its entire life, allowing comparison with other homeothermic animals like birds and mammals. The present data showed a positive relation between telomere length and individual age, independent of sex and body size. A segmented analysis highlighted a breakpoint in the telomere length-age relationship, suggesting that telomere length reached a plateau at the age of 25 years. Further studies focusing on the biology of animals that live much longer than expected based on body mass will contribute to our better understanding of how ageing processes evolved and may also bring innovation for extending human health span.
In eukaryotes, the performances of an organism are dependent on body mass and chemically supported by the mitochondrial production of ATP. Although the relationship between body mass and mitochondrial oxygen consumption is well described, the allometry of the transduction efficiency from oxygen to ATP production (ATP/O) is still poorly understood. Using a comparative approach, we investigated the oxygen consumption and ATP production of liver mitochondria from twelve species of mammals ranging from 5 g to 600 kg. We found that both oxygen consumption and ATP production are mass dependent but not the ATP/O at the maximal phosphorylating state. The results also showed that for sub-maximal phosphorylating states the ATP/O value positively correlated with body mass, irrespective of the metabolic intensity. This result contrasts with previous data obtained in mammalian muscles, suggesting a tissue-dependence of the body mass effect on mitochondrial efficiency.
ABSTRACT Body mass is known to be a fundamental driver of many biological traits, including metabolism. However, the effect of body mass on mitochondrial energy transduction is still poorly understood and has mainly been described in mammals. Using 13 species of birds ranging from 15 g (finches) to 160 kg (ostrich), we report here that the mitochondrial production of ATP, and the corresponding oxygen consumption, are negatively dependent on body mass in skeletal muscles but not in the heart. Results also showed that mitochondrial efficiency was positively correlated with body mass at sub-maximal phosphorylating states in the skeletal muscle, but not in the heart. This difference between muscle tissues is potentially linked to the difference in energetic demand expandability and the heavy involvement of skeletal muscle in thermoregulation.
Both birds and mammals have important thermogenic capacities allowing them to maintain high body temperatures, i.e., 37 °C and 40 °C on average in mammals and birds, respectively. However, during periods of high locomotor activity, the energy released during muscular contraction can lead to muscle temperature reaching up to 43-44 °C. Mitochondria are responsible for producing the majority of ATP through cellular respiration and metabolizing different substrates, including carbohydrates and lipids, to generate ATP. A limited number of studies comparing avian and mammalian species showed preferential utilization of specific substrates for mitochondrial energy at different metabolic intensities, but authors always measured at body temperature. The present study evaluated mitochondrial respiration rates and OXPHOS coupling efficiencies at 37 °C, 40 °C and 43 °C associated with pyruvate/malate (carbohydrate metabolism) or palmitoyl-carnitine/malate (lipid metabolism) as substrates in pigeons (Columba livia) and rats (Rattus norvegicus), a well-known pair in scientific literature and for their similar body mass. The data show different hyperthermia-induced responses between the two species with (i) skeletal muscle mitochondria from rats being more sensitive to rising temperatures than in pigeons, and (ii) the two species having different substrate preferences during hyperthermia, with rats oxidizing preferentially carbohydrates and pigeons lipids. By analyzing the interplay between temperature and substrate utilization, we describe a means by which endotherms deal with extreme muscular temperatures to provide enough ATP to support energy demands.
Spatial and temporal variations of oxygen environments affect the behaviors of various cells and are involved in physiological and pathological events. Our previous studies with Dictyostelium discoideum as a model of cell motility have demonstrated that aerotaxis toward an oxygen-rich region occurs below 2% O2. However, while the aerotaxis of Dictyostelium seems to be an effective strategy to search for what is essential for survival, the mechanism underlying this phenomenon is still largely unclear. One hypothesis is that an oxygen concentration gradient generates a secondary oxidative stress gradient that would direct cell migration towards higher oxygen concentration. Such mechanism was inferred but not fully demonstrated to explain the aerotaxis of human tumor cells. Here, we investigated the role on aerotaxis of flavohemoglobins, proteins that can both act as potential oxygen sensors and modulators of nitric oxide and oxidative stress. The migratory behaviors of Dictyostelium cells were observed under both self-generated and imposed oxygen gradients. Furthermore, their changes by chemicals generating or preventing oxidative stress were tested. The trajectories of the cells were then analyzed through time-lapse phase-contrast microscopic images. The results indicate that both oxidative and nitrosative stresses are not involved in the aerotaxis of Dictyostelium but cause cytotoxic effects that are enhanced upon hypoxia.
Stress hormones and their impacts on whole organism metabolic rates are usually considered as appropriate proxies for animal energy budget that is the foundation of numerous concepts and models aiming at predicting individual and population responses to environmental stress. However, the dynamics of energy re-allocation under stress make the link between metabolism and corticosterone complex and still unclear. Using ectopic application of corticosterone for 3, 11 and 21 days, we estimated a time effect of stress in a lizard (Zootoca vivipara). We then investigated whole organism metabolism, muscle cellular O-2 consumption and liver mitochondrial oxidative phosphorylation processes (O-2 consumption and ATP production) and ROS production. The data showed that while skeletal muscle is not impacted, stress regulates the liver mitochondrial functionality in a time-dependent manner with opposing pictures between the different time expositions to corticosterone. While 3 days exposition is characterized by lower ATP synthesis rate and high H2O2 release with no change in the rate of oxygen consumption, the 11 days exposition reduced all three fluxes of about 50%. Oxidative phosphorylation capacities in liver mitochondria of lizard treated with corticosterone for 21 days was similar to the hepatic mitochondrial capacities in lizards that received no corticosterone treatment but with 40% decrease in H2O2 production. This new mitochondrial functioning allows a better capacity to respond to the energetic demands imposed by the environment but do not influence whole organism metabolism. In conclusion, global mitochondrial functioning has to be considered to better understand the proximal causes of the energy budget under stressful periods.
Skeletal muscle mitochondria of the African pygmy mouse Mus mattheyi exhibit markedly reduced oxygen consumption and ATP synthesis rates but a higher mitochondrial efficiency than what would be expected from allometric trends. In the present study, we assessed whether such reduction of mitochondrial activity in M. mattheyi can limit the oxidative stress associated with an increased generation of mitochondrial reactive oxygen species. We conducted a comparative study of mitochondrial oxygen consumption, H2O2 release, and electron leak (%H2O2/O) in skeletal muscle mitochondria isolated from the extremely small African pygmy mouse (M. mattheyi, ~5 g) and Mus musculus, which is a larger Mus species (~25 g). Mitochondria were energized with pyruvate, malate, and succinate, after which fluxes were measured at different steady-state rates of oxidative phosphorylation. Overall, M. mattheyi exhibited lower oxidative activity and higher electron leak than M. musculus, while the H2O2 release did not differ significantly between these two Mus species. We further found that the high coupling efficiency of skeletal muscle mitochondria from M. mattheyi was associated with high electron leak. Nevertheless, data also show that, despite the higher electron leak, the lower mitochondrial respiratory capacity of M. mattheyi limits the cost of a net increase in H2O2 release, which is lower than that expected for a mammals of this size.
Heat waves are extreme thermal events whose frequency and intensity will increase with global warming. As metabolic responses to temperature are time-dependent, we explored the effects of an exposure to several heat waves on the mitochondrial metabolism of zebrafish Danio rerio. For this purpose, zebrafish were acclimated at 26 °C or 31 °C for 4 weeks and some fish acclimated at 26 °C underwent 2 types of heat waves: 2 periods of 5 days at 31 °C or 10 days at 31 °C. After this acclimation period, mitochondrial respiration of red muscle fibres was measured at 26 °C and 31 °C for each fish, with the phosphorylation (OXPHOS) and basal (LEAK) respirations obtained with activation of complex I, complex II or complexes I and II. The respiratory control ratio (RCR) and the mitochondrial aerobic scope (CAS) were also calculated at both temperatures after the activation of complexes I and II. Under our conditions, heat waves did not result in variations in any mitochondrial parameters, suggesting a high tolerance of zebrafish to environmental temperature fluctuations. However, an acute in vitro warming led to an increase in the LEAK respiration together with a higher temperature effect on complex II than complex I, inducing a decrease of mitochondrial efficiency to produce energy at high temperatures. Increased interindividual variability for some parameters at 26 °C or 31 °C also suggests that each individual has its own ability to cope with temperature fluctuations.
In ectotherms, it is well described that thermal acclimation induces compensatory adjustments maintaining mitochondrial functions across large shifts in temperature. However, until now, studies mostly focused on fluxes of oxygen without knowing whether mitochondrial efficiency to produce ATP (ATP/O ratio) is also dependent on temperature acclimation. We thus measured thermal reaction norms of oxidative phosphorylation activity and efficiency in isolated mitochondria from skeletal muscle of sea bass (Dicentrarchus labrax) juveniles acclimated at optimal (22°C), low (18°C), and high (26°C) temperatures. The mitochondrial fluxes (oxygen consumption and ATP synthesis) increased with increasing assay temperatures and were on the whole higher in fishes acclimated at 18°C than in the other two groups. However, these mitochondrial rates were not significantly different between experimental groups when they were compared at the acclimation temperature. In contrast, we show that acclimation to high, and not low, temperature improved mitochondrial efficiency (on average >15%). This higher efficiency in high-temperature-acclimated fishes is also apparent when compared at respective acclimation temperatures. This mitochondrial phenotype would favor an economical management of oxygen in response to harsh energetic constraints associated with warming water.
The aim of the study was to evaluate the interplay between mitochondrial respiration and H2O2 release during the transition from basal non-phosphorylating to maximal phosphorylating states. We conducted a large scale comparative study of mitochondrial oxygen consumption, H2O2 release and electron leak (% H2O2/O) in skeletal muscle mitochondria isolated from mammal species ranging from 7 g to 500 kg. Mitochondrial fluxes were measured at different steady state rates in presence of pyruvate, malate, and succinate as respiratory substrates. Every species exhibited a burst of H2O2 release from skeletal muscle mitochondria at a low rate of oxidative phosphorylation, essentially once the activity of mitochondrial oxidative phosphorylation reached 26% of the maximal respiration. This threshold for ROS generation thus appears as a general characteristic of skeletal muscle mitochondria in mammals. These findings may have implications in situations promoting succinate accumulation within mitochondria, such as ischemia or hypoxia.