Heterothermy is associated with reduced fitness in wild rabbits.
ABSTRACT: An increase in variation in the 24 h pattern of body temperature (heterothermy) in mammals can be induced by energy and water deficits. Since performance traits such as growth and reproduction also are impacted by energy and water balance, we investigated whether the characteristics of the body temperature rhythm provide an indication of the reproductive success of an individual. We show that the amplitude of the daily rhythm of body temperature in wild rabbits (Oryctolagus cuniculus) prior to breeding is inversely related to the number of pregnancies in the subsequent seven months, while the minimum daily body temperature is positively correlated to the number of pregnancies. Because reproductive output could be predicted from characteristics of the core body temperature rhythm prior to the breeding season, we propose that the pattern of the 24 h body temperature rhythm could provide an index of animal fitness in a given environment.
Project description:Abstract Animals have adapted behavioral and physiological strategies to conserve energy during periods of adverse conditions. Heterothermy is one such adaptation used by endotherms. While heterothermy—fluctuations in body temperature and metabolic rate—has been shown in large vertebrates, little is known of the costs and benefits of this strategy, both in terms of energy and in terms of fitness. Hence, our objective was to model the energetics of seasonal heterothermy in the largest Arctic ungulate, the muskox (Ovibos moschatus), using an individual?based energy budget model of metabolic physiology. We found that the empirically based drop in body temperature (winter max ~?0.8°C) overwinter in adult females resulted in substantial fitness benefits in terms of reduced daily energy expenditure and body mass loss. Body mass and energy reserves were 8.98% and 14.46% greater in modeled heterotherms compared to normotherms by end of winter. Based on environmental simulations, we show that seasonal heterothermy can, to some extent, buffer the negative consequences of poor prewinter body condition or reduced winter food accessibility, leading to greater winter survival (+20%–30%) and spring energy reserves (+10%–30%), and thus increased probability of future reproductive success. These results indicate substantial adaptive short?term benefits of seasonal heterothermy at the individual level, with potential implications for long?term population dynamics in highly seasonal environments. Animals use seasonal heterothermy to conserve energy during periods of adverse environmental conditions. Our energy budget model of muskoxen reveals considerable fitness benefits of overwinter heterothermy in the form of conserved body mass, energy reserves, and increased survival, relative to simulated normothermic individuals. Individual energetics and fitness consequences of heterothermy could have implications for population dynamics. Photo credit: Lars Holst Hansen.
Project description:Environmental and biotic pressures impose homeostatic costs on all organisms. The energetic costs of maintaining high body temperatures (T<sub>b</sub>) render endotherms sensitive to pressures that increase foraging costs. In response, some mammals become more heterothermic to conserve energy. We measured T<sub>b</sub> in banner-tailed kangaroo rats (Dipodomys spectabilis) to test and disentangle the effects of air temperature and moonlight (a proxy for predation risk) on thermoregulatory homeostasis. We further perturbed homeostasis in some animals with chronic corticosterone (CORT) via silastic implants. Heterothermy increased across summer, consistent with the predicted effect of lunar illumination (and predation), and in the direction opposite to the predicted effect of environmental temperatures. The effect of lunar illumination was also evident within nights as animals maintained low T<sub>b</sub> when the moon was above the horizon. The pattern was accentuated in CORT-treated animals, suggesting they adopted an even further heightened risk-avoidance strategy that might impose reduced foraging and energy intake. Still, CORT-treatment did not affect body condition over the entire study, indicating kangaroo rats offset decreases in energy intake through energy savings associated with heterothermy. Environmental conditions receive the most attention in studies of thermoregulatory homeostasis, but we demonstrated here that biotic factors can be more important and should be considered in future studies.
Project description:Invasive species present a major conservation threat globally and nowhere are their affects more pronounced than in island ecosystems. Determining how native island populations respond demographically to invasive species can provide information to mitigate the negative effects of invasive species. Using 20 years of mark-recapture data from three sympatric species of albatrosses (black-browed Thalassarche melanophris, grey-headed T. chrysostoma, and light-mantled albatrosses Phoebetria palpebrata), we quantified the influence of invasive European rabbits Oryctolagus cuniculus and extreme weather patterns on breeding probability and success. Temporal variability in rabbit density explained 33-76% of the variability in breeding probability for all three species, with severe decreases in breeding probability observed after a lag period following highest rabbit numbers. For black-browed albatrosses, the combination of extreme rainfall and high rabbit density explained 33% of total trait variability and dramatically reduced breeding success. We showed that invasive rabbits and extreme weather events reduce reproductive output in albatrosses and that eliminating rabbits had a positive effect on albatross reproduction. This illustrates how active animal management at a local breeding site can result in positive population outcomes even for wide ranging animals like albatrosses where influencing vital rates during their at-sea migrations is more challenging.
Project description:African mole-rats are strictly subterranean mammals that live in extensive burrow systems. High humidity levels in the burrows prevent mole-rats from thermoregulating using evaporative cooling. However, the relatively stable environment of the burrows promotes moderate temperatures and small daily temperature fluctuations. Mole-rats therefore display a relatively wide range of thermoregulation abilities. Some species cannot maintain their body temperatures at a constant level, whereas others employ behavioural thermoregulation. Here we test the effect of ambient temperature on locomotor activity and body temperature, and the relationship between the two parameters, in the highveld mole-rat. We exposed mole-rats to a 12L:12D and a DD light cycle at ambient temperatures of 30°C, 25°C and 20°C while locomotor activity and body temperature were measured simultaneously. In addition, we investigated the endogenous rhythms of locomotor activity and body temperature at different ambient temperatures. Mole-rats displayed nocturnal activity at all three ambient temperatures and were most active at 20°C, but least active at 30°C. Body temperature was highest at 30°C and lowest at 20°C, and the daily cycle was highly correlated with locomotor activity. We show that the mole-rats have endogenous rhythms for both locomotor activity and body temperature. However, the endogenous body temperature rhythm appears to be less robust compared to the locomotor activity rhythm. Female mole-rats appear to be more sensitive to temperature changes than males, increased heterothermy is evident at lower ambient temperatures, whilst males show smaller variation in their body temperatures with changing ambient temperatures. Mole-rats may rely more heavily on behavioural thermoregulation as it is more energy efficient in an already challenging environment.
Project description:Aardvarks (Orycteropus afer) are elusive burrowing mammals, predominantly nocturnal and distributed widely throughout Africa except for arid deserts. Their survival may be threatened by climate change via direct and indirect effects of increasing heat and aridity. To measure their current physiological plasticity, we implanted biologgers into six adult aardvarks resident in the semi-arid Kalahari. Following a particularly dry and hot summer, five of the study aardvarks and 11 other aardvarks at the study site died. Body temperature records revealed homeothermy (35.4-37.2°C) initially, but heterothermy increased progressively through the summer, with declining troughs in the nychthemeral rhythm of body temperature reaching as low as 25°C before death, likely due to starvation. Activity patterns shifted from the normal nocturnal to a diurnal mode. Our results do not bode well for the future of aardvarks facing climate change. Extirpation of aardvarks, which play a key role as ecosystem engineers, may disrupt stability of African ecosystems.
Project description:The hibernator's heart functions continuously and avoids damage across the wide temperature range of winter heterothermy. To define the molecular basis of this phenotype, we quantified proteomic changes in the 13-lined ground squirrel heart among eight distinct physiological states encompassing the hibernator's year. Unsupervised clustering revealed a prominent seasonal separation between the summer homeotherms and winter heterotherms, whereas within-season state separation was limited. Further, animals torpid in the fall were intermediate to summer and winter, consistent with the transitional nature of this phase. A seasonal analysis revealed that the relative abundances of protein spots were mainly winter-increased. The winter-elevated proteins were involved in fatty acid catabolism and protein folding, whereas the winter-depleted proteins included those that degrade branched-chain amino acids. To identify further state-dependent changes, protein spots were re-evaluated with respect to specific physiological state, confirming the predominance of seasonal differences. Additionally, chaperone and heat shock proteins increased in winter, including HSPA4, HSPB6, and HSP90AB1, which have known roles in protecting against ischemia-reperfusion injury and apoptosis. The most significant and greatest fold change observed was a disappearance of phospho-cofilin 2 at low body temperature, likely a strategy to preserve ATP. The robust summer-to-winter seasonal proteomic shift implies that a winter-protected state is orchestrated before prolonged torpor ensues. Additionally, the general preservation of the proteome during winter hibernation and an increase of stress response proteins, together with dephosphorylation of cofilin 2, highlight the importance of ATP-conserving mechanisms for winter cardioprotection.
Project description:The analysis of introgression of genomic regions between divergent populations provides an excellent opportunity to determine the genetic basis of reproductive isolation during the early stages of speciation. However, hybridization and subsequent gene flow must be relatively common in order to localize individual loci that resist introgression. In this study, we used next-generation sequencing to study genome-wide patterns of genetic differentiation between two hybridizing subspecies of rabbits (Oryctolagus cuniculus algirus and O. c. cuniculus) that are known to undergo high rates of gene exchange. Our primary objective was to identify specific genes or genomic regions that have resisted introgression and are likely to confer reproductive barriers in natural conditions. On the basis of 326,000 polymorphisms, we found low to moderate overall levels of differentiation between subspecies, and fewer than 200 genomic regions dispersed throughout the genome showing high differentiation consistent with a signature of reduced gene flow. Most differentiated regions were smaller than 200 Kb and contained very few genes. Remarkably, 30 regions were each found to contain a single gene, facilitating the identification of candidate genes underlying reproductive isolation. This gene-level resolution yielded several insights into the genetic basis and architecture of reproductive isolation in rabbits. Regions of high differentiation were enriched on the X-chromosome and near centromeres. Genes lying within differentiated regions were often associated with transcription and epigenetic activities, including chromatin organization, regulation of transcription, and DNA binding. Overall, our results from a naturally hybridizing system share important commonalities with hybrid incompatibility genes identified using laboratory crosses in mice and flies, highlighting general mechanisms underlying the maintenance of reproductive barriers.
Project description:<h4>Background</h4>Predation may potentially lead to negative effects on both prey (directly via predators) and predators (indirectly via human persecution). Predation pressure studies are, therefore, of major interest in the fields of theoretical knowledge and conservation of prey or predator species, with wide ramifications and profound implications in human-wildlife conflicts. However, detailed works on this issue in highly valuable--in conservation terms--Mediterranean ecosystems are virtually absent. This paper explores the predator-hunting conflict by examining a paradigmatic, Mediterranean-wide (endangered) predator-two prey (small game) system.<h4>Methodology/principal findings</h4>We estimated the predation impact ('kill rate' and 'predation rate', i.e., number of prey and proportion of the prey population eaten, respectively) of Bonelli's eagle Aquila fasciata on rabbit Oryctolagus cuniculus and red-legged partridge Alectoris rufa populations in two seasons (the eagle's breeding and non-breeding periods, 100 days each) in SE Spain. The mean estimated kill rate by the seven eagle reproductive units in the study area was c. 304 rabbits and c. 262 partridges in the breeding season, and c. 237 rabbits and c. 121 partridges in the non-breeding period. This resulted in very low predation rates (range: 0.3-2.5%) for both prey and seasons.<h4>Conclusions/significance</h4>The potential role of Bonelli's eagles as a limiting factor for rabbits and partridges at the population scale was very poor. The conflict between game profitability and conservation interest of either prey or predators is apparently very localised, and eagles, quarry species and game interests seem compatible in most of the study area. Currently, both the persecution and negative perception of Bonelli's eagle (the 'partridge-eating eagle' in Spanish) have a null theoretical basis in most of this area.