Energy allocation shifts from sperm production to self-maintenance at low temperatures in male bats

Abstract

The ability of animals to produce endogenous heat provides a buffer against environmental changes but also incurs high energetic costs. Especially small endothermic mammals have high energy demands. Some temperate-zone species (heterotherms) regularly use torpor, which slows down their entire metabolism but also potentially delays reproduction, to compensate for this. We used a unique experimental approach to test the consequences of extended low and high ambient temperatures on the trade-off in energy allocation to body mass maintenance, thermoregulation effort and seasonal sexual maturation in temperate zone male bats. We showed that long exposure to low ambient temperature shifts energy allocation away from sexual maturation to self-maintenance and results in a delay of sperm maturation by as much as an entire month. This effect was partially buffered by higher body mass. Heavier bats were able to afford more intensive thermoregulation and consequently speed up maturation. Interestingly, bats at constant high temperatures avoided deep torpor and matured faster than those at low temperatures, but sperm production was also slower than under natural conditions. Our results show that not only low, but also constant high ambient temperatures are detrimental during seasonal sexual maturation and the trade-off between investing into self-maintenance and fitness is a finely tuned compromise.

Life history consequences of climate change in hibernating mammals: a review

“…Higher reproductive success should track phenological match with key resources, as mothers face less severe tradeoffs between energetic investment in offspring versus their own pre-hibernation body condition when resources are plentifulduring reproduction. We hypothesized that early spring warming should lengthen growing seasons (Buermann et al 2018), giving more time for males to become seasonally sexually matureleading to higher fertility (Komar et al 2022). In addition, if warming leads to shorter hibernation durations, one would expect males and females to emerge in better condition, leading to a higher proportion of reproductively active individuals and larger, more successful litters.…”

Contrasting Torpor Use by Reproductive Male Common Noctule Bats in the Laboratory and in the Field

“…However, as we were not able to obtain T a directly from roosts, in which T a are often more stable compared to the outside, but can also increase drastically, for example, if the bat box faces the sun, we can only speculate about fluctuations in T a in the roost and their possible effects on torpor use. Generally, our data suggests that “early reproduction” bats still flexibly used torpor, most likely because conditions were not optimal for them in the laboratory ( Komar et al 2022 ).…”

“…Most research comparing torpor patterns between life history stages in free-ranging bats has been performed with females ( Lausen and Barclay 2003 ; Willis et al 2006 ; Dzal and Brigham 2013 ), as the cost of torpor, such as reduced fetal growth or milk production, has been long recognized ( Audet and Fenton 1988 ; Hamilton and Barclay 1994 ; Grinevitch et al 1995 ; Racey and Speakman 1987 ). However, it is becoming increasingly clear that in males, too, energetic costs increase during spermatogenesis ( Racey 1974 ; Kurta and Kunz 1988 ; Hałat et al 2020 ; Komar et al 2020 ; Komar et al 2022 ), during courtship, or when defending a harem ( Entwistle et al 1998 ; Speakman et al 2003 ; Becker et al 2013 ). This leads to reduced torpor use by males during these life history stages ( Kurta and Kunz 1988 ; Gebhard 2013 ).…”

The behavioural costs of overcrowding for gregarious cave‐dwelling bats

“…A similar correlation pattern was also observed in the relaxation behaviour, suggesting a potential connection between relaxation and energy conservation strategies (Luo et al., 2021). Furthermore, the positive correlation between relaxation and thermoregulation behaviour indicates that bats in aggregated colonies may alternate between cooling down and resting (Becker et al., 2012; Komar et al., 2022). Additionally, the positive correlation between relaxation behaviour and self‐maintenance, as well as positive social behaviour, implies that bats in non‐aggregated colonies might use relaxation to recharge and engage in social interactions during their active hours, which could enhance their overall fitness and well‐being (Hengjan et al., 2017).…”