Yvon Le Maho

Relationships between lipid availability and protein utilization during prolonged fasting

SummaryMammals and birds adapt to prolonged fasting by mobilizing fat stores and minimizing protein loss. This strategy ends with an increase in protein utilization associated with behavioural changes promoting food foraging. Using the Zucker rat as a model, we have investigated the effect of severe obesity on this pattern of protein loss during long-term fasting. Two interactions between the initial adiposity and protein utilization were found. First, protein conservation was more effective in obese than in lean rats: fatty rats had a three times lower daily nitrogen excretion and proportion of energy expenditure deriving from proteins, and a lower daily protein loss in various muscles. This phase of protein sparing is moreover nine times longer in the fatty rats. Second, obese animals did not show the late increase in nitrogen excretion that occurred in their lean littermates. Total body protein loss during starvation was larger in fatty rats (57% versus 29%) and, accordingly, total protein loss was greater in their muscles. At the end of the experiment, lean and obese rats had lost 98% and 82%, respectively, of their initial lipid reserves, and fatty rats still had an obese body composition. These results support the hypothesis that in severely obese humans and animals a lethal cumulative protein loss is reached long before the exhaustion of fat stores, while the phase of protein conservation is still continuing. In contrast, in lean rats, survival of fasting seems to depend on the availability of lipid fuels. The data also suggest that accumulation of too much fat in wild animals is detrimental for survival, because it eliminates the late phase of increase in nitrogen excretion that is linked to a food foraging behaviour anticipating a lethal depletion of body reserves.

Marine animal behaviour: neglecting ocean currents can lead us up the wrong track

Tracks of marine animals in the wild, now increasingly acquired by electronic tagging of individuals, are of prime interest not only to identify habitats and high-risk areas, but also to gain detailed information about the behaviour of these animals. Using recent satellite-derived current estimates and leatherback turtle (Dermochelys coriacea) tracking data, we demonstrate that oceanic currents, usually neglected when analysing tracking data, can substantially distort the observed trajectories. Consequently, this will affect several important results deduced from the analysis of tracking data, such as the evaluation of the orientation skills and the energy budget of animals or the identification of foraging areas. We conclude that currents should be systematically taken into account to ensure the unbiased interpretation of tracking data, which now play a major role in marine conservation biology.

Reliability of flipper-banded penguins as indicators of climate change

In 2007, the Intergovernmental Panel on Climate Change highlighted an urgent need to assess the responses of marine ecosystems to climate change. Because they lie in a high-latitude region, the Southern Ocean ecosystems are expected to be strongly affected by global warming. Using top predators of this highly productive ocean (such as penguins) as integrative indicators may help us assess the impacts of climate change on marine ecosystems. Yet most available information on penguin population dynamics is based on the controversial use of flipper banding. Although some reports have found the effects of flipper bands to be deleterious, some short-term (one-year) studies have concluded otherwise, resulting in the continuation of extensive banding schemes and the use of data sets thus collected to predict climate impact on natural populations. Here we show that banding of free-ranging king penguins (Aptenodytes patagonicus) impairs both survival and reproduction, ultimately affecting population growth rate. Over the course of a 10-year longitudinal study, banded birds produced 39% fewer chicks and had a survival rate 16% lower than non-banded birds, demonstrating a massive long-term impact of banding and thus refuting the assumption that birds will ultimately adapt to being banded. Indeed, banded birds still arrived later for breeding at the study site and had longer foraging trips even after 10 years. One of our major findings is that responses of flipper-banded penguins to climate variability (that is, changes in sea surface temperature and in the Southern Oscillation index) differ from those of non-banded birds. We show that only long-term investigations may allow an evaluation of the impact of flipper bands and that every major life-history trait can be affected, calling into question the banding schemes still going on. In addition, our understanding of the effects of climate change on marine ecosystems based on flipper-band data should be reconsidered.

One for all and all for one: the energetic benefits of huddling in endotherms

Huddling can be defined as “an active and close aggregation of animals”. It is a cooperative group behaviour, permitting individuals involved in social thermoregulation to minimize heat loss and thereby lower their energy expenditure, and possibly allowing them to reallocate the saved energy to other functions such as growth or reproduction. Huddling is especially important in the case of animals faced with high heat loss due to a high surface‐to‐volume ratio, poor insulation, or living in cold environments. Although numerous experimental studies have focused on the huddling behaviour of a wide range of species, to our knowledge, this is the first attempt to review the various implications of this widely used behavioural strategy.

King penguin population threatened by Southern Ocean warming

Seabirds are sensitive indicators of changes in marine ecosystems and might integrate and/or amplify the effects of climate forcing on lower levels in food chains. Current knowledge on the impact of climate changes on penguins is primarily based on Antarctic birds identified by using flipper bands. Although flipper bands have helped to answer many questions about penguin biology, they were shown in some penguin species to have a detrimental effect. Here, we present for a Subantarctic species, king penguin (Aptenodytes patagonicus), reliable results on the effect of climate on survival and breeding based on unbanded birds but instead marked by subcutaneous electronic tags. We show that warm events negatively affect both breeding success and adult survival of this seabird. However, the observed effect is complex because it affects penguins at several spatio/temporal levels. Breeding reveals an immediate response to forcing during warm phases of El Niño Southern Oscillation affecting food availability close to the colony. Conversely, adult survival decreases with a remote sea-surface temperature forcing (i.e., a 2-year lag warming taking place at the northern boundary of pack ice, their winter foraging place). We suggest that this time lag may be explained by the delay between the recruitment and abundance of their prey, adjusted to the particular 1-year breeding cycle of the king penguin. The derived population dynamic model suggests a 9% decline in adult survival for a 0.26°C warming. Our findings suggest that king penguin populations are at heavy extinction risk under the current global warming predictions.

Recurrent evolution of host-specialized races in a globally distributed parasite

The outcome of coevolutionary interactions is predicted to vary across landscapes depending on local conditions and levels of gene flow, with some populations evolving more extreme specializations than others. Using a globally distributed parasite of colonial seabirds, the tick Ixodes uriae, we examined how host availability and geographic isolation influences this process. In particular, we sampled ticks from 30 populations of six different seabird host species, three in the Southern Hemisphere and three in the Northern Hemisphere. We show that parasite races have evolved independently on hosts of both hemispheres. Moreover, the degree of differentiation between tick races varied spatially within each region and suggests that the divergence of tick races is an ongoing process that has occurred multiple times across isolated areas. As I. uriae is vector to the bacterium responsible for Lyme disease Borrelia burgdorferi sensu lato, these results may have important consequence for the epidemiology of this disease. With the increased occurrence of novel interspecific interactions due to global change, these results also stress the importance of the combined effects of gene flow and selection for parasite diversification.

Hypothalamic gene expression in long-term fasted rats: relationship with body fat.

Many hypothalamic neuropeptides are involved in the regulation of energy homeostasis and feeding behavior. We have investigated whether and to what extent neuropeptide Y (NPY), agouti-related protein (AGRP), melanin-concentrating hormone (MCH), and prepro-orexin (prepro-OX) as well as pro-opiomelanocortin (POMC) and cocaine and amphetamine-regulated transcript (CART) mRNA levels are affected in rat hypothalamus. An experimental model of long-term fasting rat characterized by three metabolic phases from changes in lipid and protein utilization was used. Except for prepro-OX and compared to fed group, starvation induced an increase in the orexigenic gene expressions that was much more marked in phase 3 (by 2.5-, 8.1-, and 13.5-fold for MCH, AGRP, and NPY, respectively) than in phase 2 (by about 1.5-2.2-fold as an average) of fasting. AGRP and NPY mRNA levels were inversely related to body fat content. Anorexigenic gene expression was only slightly affected at both fasting stages. We conclude that the regulation of NPY and AGRP gene expression is primarily involved during late fasting and could mediate the concomitant enhanced drive for refeeding.

Catching‐up but telomere loss: half‐opening the black box of growth and ageing trade‐off in wild king penguin chicks

One of the reasons for animals not to grow as fast as they potentially could is that fast growth has been shown to be associated with reduced lifespan. However, we are still lacking a clear description of the reality of growth‐dependent modulation of ageing mechanisms in wild animals. Using the particular growth trajectory of small king penguin chicks naturally exhibiting higher‐than‐normal growth rate to compensate for the winter break, we tested whether oxidative stress and telomere shortening are related to growth trajectories. Plasma antioxidant defences, oxidative damage levels and telomere length were measured at the beginning and at the end of the post‐winter growth period in three groups of chicks (small chicks, which either passed away or survived the growth period, and large chicks). Small chicks that died early during the growth period had the highest level of oxidative damage and the shortest telomere lengths prior to death. Here, we show that small chicks that grew faster did it at the detriment of body maintenance mechanisms as shown by (i) higher oxidative damage and (ii) accelerated telomere loss. Our study provides the first evidence for a mechanistic link between growth and ageing rates under natural conditions.

Restoration of the jejunal mucosa in rats refed after prolonged fasting.

To investigate the importance of body fuel depletion on gut rehabilitation after food deprivation, we compared the kinetics of jejunal mucosa alteration and restoration in rats that were refed after reaching different stages in body fuel depletion. Rats (P2) were refed while still in the so-called phase II, where body protein utilization is minimized, whereas rats (P3) were refed when they had reached the stage of increasing protein utilization (phase III). There was a significant decrease in total mass of intestine (P2, -30%; P3, -40%) and jejunal mucosa (P2, -52%; P3, -60%), as well in the size of the crypts (P2, -15%; P3, -36%) and villi (P2, -37%; P3, -55%). Structural changes of the mucosa included disappearance of some villi and a reduction in the size and number of crypts. Despite the larger morphological alterations in P3, the restoration of mucosa was as fast and complete after only 3 days of refeeding for both P2 and P3 rats. The respective roles of the mitosis pressure and of the lamina propria dynamics were studied. The rapid reversibility of the gut mucosal alterations due to fasting might constitute an integrative process.

Intestinal gluconeogenesis and glucose transport according to body fuel availability in rats.

Intestinal hexose absorption and gluconeogenesis have been studied in relation to refeeding after two different fasting phases: a long period of protein sparing during which energy expenditure is derived from lipid oxidation (phase II), and a later phase characterized by a rise in plasma corticosterone triggering protein catabolism (phase III). Such a switch in body fuel uses, leading to changes in body reserves and gluconeogenic precursors, could modulate intestinal gluconeogenesis and glucose transport. The gene and protein levels, and the cellular localization of the sodium–glucose cotransporter SGLT1, and of GLUT5 and GLUT2, as well as that of the key gluconeogenic enzymes phosphoenolpyruvate carboxykinase (PEPCK) and glucose‐6‐phosphatase (Glc6Pase) were measured. PEPCK and Glc6Pase activities were also determined. In phase III fasted rats, SGLT1 was up‐regulated and intestinal glucose uptake rates were higher than in phase II fasted and fed rats. PEPCK and Glc6Pase mRNA, protein levels and activities also increased in phase III. GLUT5 and GLUT2 were down‐regulated throughout the fast, but increased after refeeding, with GLUT2 recruited to the apical membrane. The increase in SGLT1 expression during phase III may allow glucose absorption at low concentrations as soon as food is available. Furthermore, an increased epithelial permeability due to fasting may induce a paracellular movement of glucose. In the absence of intestinal GLUT2 during fasting, Glc6Pase could be involved in glucose release to the bloodstream via membrane trafficking. Finally, refeeding triggered GLUT2 and GLUT5 synthesis and apical recruitment of GLUT2, to absorb larger amounts of hexoses.