Contrasting torpor use by reproductive male common noctule bats in the laboratory and in the field
2023, Keicher, Lara, Shipley, J. Ryan, Schaeffer, Paul J., Dechmann, Dina K. N.
Metabolic processes of animals are often studied in controlled laboratory settings. However, these laboratory settings often do not reflect the animals’ natural environment. Thus, results of metabolic measurements from laboratory studies must be cautiously applied to free-ranging animals. Recent technological advances in animal tracking allow detailed eco-physiological studies that reveal when, where and how physiological measurements from the field differ from those from the laboratory. We investigated torpor behavior of male common noctule bats (Nyctalus noctula) across different life history stages using two approaches: in controlled laboratory experiments and in the field using calibrated heart rate telemetry. We predicted that non-reproductive males would extensively use torpor to conserve energy, whereas reproductive males would reduce torpor use to promote spermatogenesis. We did not expect differences in torpor use between captive and wild animals as we simulated natural temperature conditions in the laboratory. We found that during the non-reproductive phase, both captive and free-ranging bats used torpor extensively. During reproduction, bats in captivity unexpectedly also used torpor throughout the day, while only free-ranging bats showed the expected reduction in torpor use. Thus, depending on life history stage, torpor behavior in the laboratory was markedly different from the wild. By implementing both approaches and at different life history stages, we were able to better explore the limitations of eco-physiological laboratory studies and make recommendations for when they are an appropriate proxy for natural behavior.
Metabolic rate in common shrews is unaffected by temperature, leading to lower energetic costs through seasonal size reduction
2020-04, Schaeffer, Paul J., O'Mara, Michael Teague, Breiholz, Japhet, Keicher, Lara, Lazaro, Javier, Muturi, Marion, Dechmann, Dina K. N.
Small endothermic mammals have high metabolisms, particularly at cold temperatures. In the light of this, some species have evolved a seemingly illogical strategy: they reduce the size of the brain and several organs to become even smaller in winter. To test how this morphological strategy affects energy consumption across seasonally shifting ambient temperatures, we measured oxygen consumption and behaviour in the three seasonal phenotypes of the common shrew (Sorex araneus), which differ in size by about 20%. Body mass was the main driver of oxygen consumption, not the reduction of metabolically expensive brain mass. Against our expectations, we found no change in relative oxygen consumption with low ambient temperature. Thus, smaller body size in winter resulted in significant absolute energy savings. This finding could only partly be explained by an increase of lower cost behaviours in the activity budgets. Our findings highlight that these shrews manage to avoid one of the most fundamental and intuitive rules of ecology, allowing them to subsist with lower resource availability and successfully survive the harsh conditions of winter.
Domestication effect of reduced brain size is reverted when mink become feral
2023, Pohle, Ann-Kathrin, Zalewski, Andrzej, Muturi, Marion, Dullin, Christian, Farková, Lucie, Keicher, Lara, Dechmann, Dina K. N.
A typical consequence of breeding animal species for domestication is a reduction in relative brain size. When domesticated animals escape from captivity and establish feral populations, the larger brain of the wild phenotype is usually not regained. In the American mink (Neovison vison), we found an exception to this rule. We confirmed the previously described reduction in relative braincase size and volume compared to their wild North American ancestors in mink bred for their fur in Poland, in a dataset of 292 skulls. We then also found a significant regrowth of these measures in well-established feral populations in Poland. Closely related, small mustelids are known for seasonal reversible changes in skull and brain size. It seems that these small mustelids are able to regain the brain size, which is adaptive for living in the wild, and flexibly respond to selection accordingly.
Stable carbon isotopes in breath reveal fast metabolic incorporation rates and seasonally variable but rapid fat turnover in the common shrew (Sorex araneus)
2017-08-02, Keicher, Lara, O'Mara, Michael Teague, Voigt, Christian C., Dechmann, Dina K. N.
Small non-migratory mammals with Northern distribution ranges apply a variety of behavioural and physiological wintering strategies. A rare energy-saving strategy is Dehnel's phenomenon, involving a reduction and later regrowth of the body size, several organs and parts of the skeleton in red-toothed shrews (Soricidae). The size extremes coincide with major life stages. However, the physiological consequences for the shrew's metabolism remain poorly understood. In keeping with the energetic limitations that may induce the size changes, we hypothesised that metabolic incorporation rates should remain the same across the shrews' lifetimes. In contrast, fat turnover rates should be faster in smaller subadults than in large juveniles and regrown adults, as the metabolic activity of fat tissue increases in winter individuals (subadults). Measuring the changes in the ratio of exhaled stable carbon isotopes, we found that the baseline diet of shrews changed across the season. A diet switch experiment showed that incorporation rates were consistently rapid (t50=38.2±21.1-69.3±53.5 min) and did not change between seasons. As predicted, fat turnover rates were faster in size-reduced subadults (t50=2.1±1.3 h) compared with larger juveniles (t50=5.5±1.7 h) and regrown adults (t50=5.0±4.4 h). In all three age/size classes, all body fat was turned over after 9-24 h. These results show that high levels of nutrient uptake are independent of body size, whereas fat turnover rates are negatively correlated with body size. Thus, the shrews might be under higher pressure to save energy in winter and this may have supported the evolution of Dehnel's phenomenon.
Flexible energy-saving strategies in female temperate-zone bats
2022-11, Keicher, Lara, Shipley, J. Ryan, Komar, Ewa, Ruczyński, Ireneusz, Schaeffer, Paul J., Dechmann, Dina K. N.
Torpor is characterized by an extreme reduction in metabolism and a common energy-saving strategy of heterothermic animals. Torpor is often associated with cold temperatures, but in the last decades, more diverse and flexible forms of torpor have been described. For example, tropical bat species maintain a low metabolism and heart rate at high ambient and body temperatures. We investigated whether bats (Nyctalus noctula) from the cooler temperate European regions also show this form of torpor with metabolic inhibition at high body temperatures, and whether this would be as pronounced in reproductive as in non-reproductive bats. We simultaneously measured metabolic rate, heart rate, and skin temperature in non-reproductive and pregnant females at a range of ambient temperatures. We found that they can decouple metabolic rate and heart rate from body temperature: they maintained an extremely low metabolism and heart rate when exposed to ambient temperatures changing from 0 to 32.5 °C, irrespective of reproductive status. When we simulated natural temperature conditions, all non-reproductive bats used torpor throughout the experiment. Pregnant bats used variable strategies from torpor, to maintaining normothermy, or a combination of both. Even a short torpor bout during the day saved up to 33% of the bats' total energy expenditure. Especially at higher temperatures, heart rate was a much better predictor of metabolic rate than skin temperature. We suggest that the capability to flexibly save energy across a range of ambient temperatures within and between reproductive states may be an important ability of these bats and possibly other temperate-zone heterotherms.
Growth overshoot and seasonal size changes in the skulls of two weasel species
2017-01-25, LaPoint, Scott, Keicher, Lara, Wikelski, Martin, Zub, Karol, Dechmann, Dina K. N.
Ontogenetic changes in mammalian skulls are complex. For a very few species (i.e. some Sorex shrews), these also include seasonally driven, bidirectional size changes within individuals, presumably to reduce energy requirements during low resource availabilities. These patterns are poorly understood, but are likely most pronounced in high-metabolic species with limited means for energy conservation. We used generalized additive models to quantify the effect of location, Julian day, age and sex on the length and depth of 512 and 847 skulls of stoat (Mustela erminea) and weasel (M. nivalis) specimens collected throughout the northern hemisphere. Skull length of both species varies between sexes and geographically, with stoat skull length positively correlated with latitude. Both species demonstrate seasonal and ontogenetic patterns, including a rare, absolute growth overshoot in juvenile braincase depth. Standardized braincase depths of both species peak in their first summer, then decrease in their first winter, followed by a remarkable regrowth that peaks again during their second summer. This seasonal pattern varies in magnitude and timing between geographical regions and the sexes, matching predictions of Dehnel's phenomenon. This suggests implications for the evolution of over-wintering strategies in mammals, justifying further research on their mechanisms and value, with implications for applied osteology research.