Novel energy savings to multiple stressors in birds: The ultradian regulation of body temperature

This study aimed to examine thermoregulatory responses in birds facing two commonly experienced stressors, cold and fasting. Logging devices allowing long-term and precise access to internal body temperature were placed within the gizzards of ducklings acclimated to cold (CA) (5°C) or thermoneutrality (TN) (25°C). The animals were then examined under three equal 4-day periods: ad libitum feeding, fasting and re-feeding. Through the analysis of daily as well as short-term, or ultradian, variations of body temperature, we showed that while ducklings at TN show only a modest decline in daily thermoregulatory parameters when fasted, they exhibit reduced surface temperatures from key sites of vascular heat exchange during fasting. The CA birds, on the other hand, significantly reduced their short-term variations of body temperature while increasing long-term variability when fasting. This phenomenon would allow the CA birds to reduce the energetic cost of body temperature maintenance under fasting. By analysing ultradian regulation of body temperature, we describe a means by which an endotherm appears to lower thermoregulatory costs in response to the combined stressors of cold and fasting

Male within-individual variability in a sexual signal component and its impact on female choice

International audienceA growing body of literature deals with the influence of physical or social environments on signal components over long time periods. Surprisingly, variations of signal quality over minutes or hours are less studied although most of the behavioral decisions of the receiver are taken at this time scale. Despite potentially strong implications on theoretical developments linked to sexual selection and communication, within-individual variability in a signal component and its possible consequence on accuracy of female choice has never been thoroughly investigated. Focusing on call dominant frequency (DF) in the European tree frog, Hyla arborea, we showed that frequency variability is due to a warm-up effect on the beginning of the call sequence but not to an exhaustion effect at the end of the sequence. Nevertheless, the great majority of male within-variability at the night scale is due to sudden discontinuities with independent temporal patterns from one individual to another. Secondly, we simulated female mate choice decisions with simple rules based on DF. Within-individual variability in DF the proportion of beneficial choice decreases up to 30% in the worst case. In addition, to overcome these temporary variations in male signal, we emphasize a weak advantage supplied by increasing sampling duration. The costs of being selective are assumed to increase with time sampling. We suggest that females may benefit from assessing several signal components simultaneously in short samples instead of disproportionately increasing sampling duration

The proximal costs of case construction in caddisflies: antioxidant and life history responses

International audienceAnimal construction allows organisms to cope with environmental variations but the physiological costs of such behaviour are still poorly understood. The aim of the present study was to measure the physiological cost of construction behaviour through the oxidative balance that is known to affect the ability of organs to function, stimulates senescence processes and ultimately impacts the fitness of the organism. We used larvae of caddisfly, Limnephilus rhombicus, by experimentally modifying the effort associated with case building. Larvae that were forced to build a new case showed a significant increase in both total antioxidant capacity and the specific activity of superoxide dismutase 48 and 72 h, respectively, after the initiation of the reconstruction. These results strongly suggest that the larval construction behaviour triggered the production of reactive oxygen species, but their effects were reversed 7 days after the reconstruction. In the animals that were forced to build a new case, oxidative stress appeared to be mitigated by a network of antioxidant defences because no oxidative damage was observed in proteins compared with the control larvae. At the adult stage, while longevity was not sex dependent and was not affected by the treatment, body mass and body size of adult males from the reconstruction treatment were significantly lower than the control values. This unexpected sex effect together with data on oxidative stress highlights the difficulty of determining the physiological cost associated with energy-demanding behaviours, implying a consideration of both their energetic and non-energetic components is required

Physiological actions of corticosterone and its modulation by an immune challenge in reptiles

International audienceHormones are an important interface between genome and environment, because of their ability to modulate the animal's phenotype. In particular, corticosterone, the stress hormone in lizards, is known to reallocate energy from non-essential functions to affect morphological, physiological and behavioral traits that help the organism to deal with acute or chronic stressors. However, the effects of corticosterone on life history stages are still unclear primarily because of the dependence of life history stages on both internal and external factors. Using a cross-design, we tested the effect of elevated levels of exogenous corticosterone on the physiology of pregnant females in different immune contexts in a wild population of common lizards (Lacerta vivipara). Immune challenge was induced by the injection of sheep red blood cells (SRBC) and corticosterone levels were increased using a transdermal administration of corticosterone. Thereafter, reproductive traits, metabolism and cellular immune responses were measured. The elevation of corticosterone in pregnant females significantly altered reproductive and physiological performance. The corticosterone treatment decreased clutch success, juvenile size and body condition, but enhanced measures of physiological performance, such as metabolism and catalase activity. These first results reinforce the understanding of the physiological actions of corticosterone in reptiles. The data also demonstrated different direct impacts of immune challenge by SRBC on inflammatory response and antioxidant activity. The injection of SRBC stimulated the SOD activity in larger females. Finally, we demonstrated experimentally the modulation of the corticosterone action by the immune challenge on stamina and hatching date. Copyright @ 2010 Elsevier Inc. All rights reserved

Body mass dependence of oxidative phosphorylation efficiency in liver mitochondria from mammals

International audienceIn 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

Comparison of the cold hardiness capacities of the oviparous and viviparous forms of Lacerta vivipara

The lizard Lacerta vivipara has allopatric oviparous and viviparous populations. The cold hardiness strategy of L. vivipara has previously been studied in viviparous populations, but never in oviparous ones. The present study reveals that both the oviparous and viviparous individuals of this species are able to survive in a supercooled state at -3 degrees C for at least one week when kept on dry substrates. The mean crystallisation temperatures of the body, around -4 degrees C on dry substrata and -2 degrees C on wet substrata, do not differ between oviparous and viviparous individuals. All the individuals are able to tolerate up to 48-50% of their body fluid converted into ice, but only viviparous individuals were able to stabilize their body ice content at 48%, and hence were able to survive even when frozen at -3 degrees C for times of up 24 hours. Ice contents higher than 51% have been constantly found lethal for oviparous individuals. This suggests that, in L. vivipara, the evolution towards a higher degree of freezing tolerance could parallel the evolution of the viviparous reproductive mode, a feature believed to be strongly selected under cold climatic conditions. This is the first report, among reptiles, of an intraspecific variation regarding the freeze tolerance capacities

Mean data set (Boel et al 2019)

Mean values of mitochondrial bioenergetics parameters for all of the species shown in the manuscript

David and Goliath: a mitochondrial coupling problem?

An organism's size, known to affect biological structures and processes from cellular metabolism to population dynamics, depends upon the duration and rate of growth. However, it is still poorly understood how mitochondrial function affects the energetic basis of growth, especially in ectotherms, which represent a huge majority of animal biodiversity. Here, we present an intraspecies comparison of neighboring populations of frogs (Rana temporaria) that have large differences in body mass even at the same age. By investigating liver mitochondrial bioenergetics, we find that frogs with high growth rates and large body sizes exhibit higher ATP synthesis rates and more efficient oxidative phosphorylation compared to the smaller frogs with low growth rates. This higher energy transduction efficiency is not associated with significant increased oxidative capacity or membrane potential values, but instead may rely on a higher mitochondrial phosphorylation system activity in combination with a lower inner membrane proton leakage. Overall, the present study introduces the mitochondrial energy transduction system as an important mechanism for balancing physiological and ecological trade-offs associated with body size. Whether phenotype differences in mitochondrial function result from local ecological constraints or reflect a natural genetic variability within wild populations of common frogs remains an open question. However, our findings highlight the need for closer consideration of all aspects of mitochondrial metabolism for a better understanding of the physiological basis of the link between size, metabolism, and energy production in wild-dwelling organisms

Data from: Allometry of mitochondrial efficiency is set by metabolic intensity

Metabolic activity sets the rates of individual resource uptake from the environment and resource allocations. For this reason, relationship with body size has been heavily documented from ecosystems to cells. Until now, most of the studies used the fluxes of oxygen as proxy of energy output without knowledge of the efficiency of biological systems to convert oxygen into ATP. The aim of this study was to examine the allometry of coupling efficiency (ATP/O) of skeletal muscle mitochondria isolated from twelve mammal species ranging from 6 g to 550 kg. Mitochondrial efficiencies were measured at different steady states of phosphorylation. The efficiencies increased sharply at higher metabolic rates. We have shown that body mass dependence of mitochondrial efficiency depends on metabolic intensity in skeletal muscles of mammals. Mitochondrial efficiency positively depends on body mass when mitochondria are close to the basal metabolic rate, however the efficiency is independent of body mass at the maximum metabolic rate. As a result, it follows that large mammals exhibit a faster dynamic increase in ATP/O than small species when mitochondria shift from basal to maximal activities. Finally, the invariant value of maximal coupling efficiency across mammal species could partly explain why scaling exponent values are very close to 1 at maximal metabolic rates