Badger setts provide thermal refugia, buffering changeable surface weather conditions
Introduction
Mammals can occupy a range of bioclimatic zones due to homeothermy; however, regulating core temperature to stay within a narrow range (Crompton et al., 1978) requires potentially costly energy expenditure, particularly in cold or variable environments (Boyles et al., 2011, Lowell and Spiegelman, 2000). These costs can be especially high for neonatal and developing juvenile mammals that are less able to regulate core temperature, often have sparse fur, and are more prone to heat loss than adults due to scale laws in relation to their small body size (McNab, 1988; see Noonan et al., 2015b).
As a consequence, mammals supplement physiological thermoregulatory mechanisms with behavioural strategies (Terrien et al., 2011). One key strategy employed by many rodents and carnivores for mitigating inclement weather is the use of subterranean refugia, especially while nursing young (Noonan et al., 2015b). Underground dens and burrows tend to have stable (or more stable) microclimates, which buffer changes in surface conditions (Boutros et al., 2007, Johnson and Pelton, 1980, Magoun and Copeland, 1998). Furthermore, dens offer complete protection against rain and snow (Blix and Lentfer, 1979), and even forest fire (Thompson and Purcell, 2016). Nevertheless, fossorial animals must leave their dens to forage, and engage in other activities, resulting in a trade-off between the proportions of time individuals can spend underground versus other essential activities (Noonan et al., 2014). The insulating quality of burrows and the ability of species to reduce activity during inclement above-ground conditions (e.g. torpor, hibernation; Humphries et al., 2002) can thus be critically important. This may be especially important during cold winter, or unusually aberrant conditions (Smith et al., 2009, Smith, 2011), when food availability may be low, but foraging incurs substantial heat loss.
Since the mid- 20th century, anthropogenic greenhouse gas concentrations have contributed substantially to increasing global average temperatures and extreme weather events (IPCC, 2014a). This rapid climate warming can affect animal ecology in two ways; either indirectly, through impacts on food resources, reducing available energy inputs (Tuomainen and Candolin, 2010), or directly, by costing the animal more energy to thermoregulate (Beever et al., 2017, Huey and Tewksbury, 2009, Sih, 2013). A decline in population survival rate will, however, only become apparent once conditions exceed the thermal tolerance range of the species examined (Scheffers et al., 2014, Silva et al., 2017) and their ability to adapt their daily and seasonal routines (see Newman et al., 2017). It is therefore important to better understand how animals actually respond and adapt to the range of weather conditions they experience in order to project how they may cope with changed climatic conditions in the future (Beever et al., 2017, Scheffers et al., 2014, Noonan et al., 2015a).
Here we establish the conditions in fossorial dens (termed ‘setts’) used by the European badger (Meles meles; henceforth ‘badger’) in relation to prevailing weather. In the UK, badgers live mainly in agricultural mosaic habitats, locating setts in wooded areas (Macdonald et al., 2015). They are nocturnal, resting underground for on average 12.3 ± 1.69 SD hours per diem (same study population; Noonan et al., 2015c). Badgers are widely distributed across Europe, and have been established to achieve their highest densities where earthworms provide a major proportion of their diet, such as in Britain (Johnson et al., 2002); with congeneric Meles spp. across Asia (Zhou et al., 2017). Because microclimate affects the availability of earthworms (Jiménez and Decaëns, 2000), badger population dynamics are governed strongly by weather conditions (see Macdonald et al., 2010; Macdonald and Newman, 2002; Newman et al., 2017; Nouvellet et al., 2013).
At high density, badgers form social groups (Macdonald et al., 2015) with each group sharing a sett (Noonan et al., 2014, Roper, 1992). Over winter, when food resources are in short supply, badgers can conserve energy by staying within their setts (Noonan et al., 2014, Noonan et al., 2015a) and use periods of light torpor to conserve metabolic expenditure (Fowler and Racey, 1988; see also Newman et al., 2011)-strategies used predominantly by fatter badgers that are less desperate to feed (Noonan et al., 2014). Notably, in Scotland (Silva et al., 2017) and Ireland (Byrne et al., 2015) badgers prefer warmer sites.
We focused here on the autumn period leading into winter, when variation in weather can have a significant effect on badger survival (Macdonald et al., 2010). Note: after delayed implantation, badger gestation commences around late-December / early January, and maternal condition is known to affect embryonic development, litter size and neonatal mortality rate (Woodroffe, 1995, Macdonald and Newman, 2002). Specifically we tested whether:
- i)
microclimatic conditions within setts differed from prevailing above-ground weather conditions, and investigated how stable temperatures were within setts.
- ii)
the soil type in which the sett was dug, or its aspect were associated with the sett's thermal properties.
- iii)
sett temperature changed through the 24 h cycle in relation to badger occupancy
- iv)
autumn-winter sett temperature influenced the contemporaneous body-condition and weight of sett residents (cubs/adults), and the weight and body-condition achieved among natal cubs and resident adults in the subsequent spring.
We conclude by evaluating how our findings on subterranean refugia conditions and usage may enhance the ability of fossorial species to cope with more extreme weather conditions, as predicted by climate change scenario IPCC AR5 (IPCC, 2014a).
Section snippets
Study site
Wytham Woods, located 5 km north-west of the City of Oxford, comprise 424 ha of semi-natural woodland with areas of open grassland (for details see: Savill et al., 2010). Taylor et al. (2010) give mean annual temperature as 10 °C (1993–2007) with mean annual rainfall of 717 mm, recorded at the top of Wytham Hill at an elevation of 160 m by the Environmental Change Network. Due to unique ecological circumstances, Wytham Woods have the highest published density of badgers in the world, at > 40/km2
Sett temperature and humidity compared to exterior conditions
Weekly spot measures of interior sett temperature (n = 924; taken by day, when badgers were in residence) averaged 10.64 ± 2.53 °C (range: 3.90–16.60 °C, median = 10.8 °C) over the study period, versus a contemporaneous exterior sett temperature average of 10.78 ± 4.06 °C (range: 2.60–24.00 °C, median = 10.3 °C). From OLS tests, interior sett temperature followed the same patterns of increase and decrease as exterior sett temperature (t = 17.97, p < 0.0001), with a negative effect of date
Discussion
With regard to our first study aim, from logging daily sett interior temperature in a single entrance, we found that setts were generally warmer than exterior conditions. However, from weekly spot measurements over multiple entrances, we found that daytime (afternoon) sett temperatures (i.e., while badger were present and benefitted from the sett's thermal properties) were in actuality cooler than exterior conditions in the autumn (Sept-Oct), and warmer than exterior conditions once ambient air
Conclusion
Maintaining homeothermic regulation is crucial for mammals, but incurs considerable energetic costs (Weiner, 1989). For animals exposed to prevailing weather conditions, the more extreme the environmental temperature (and other contributors such as soaking by rain; Webb and King, 1984) departs from the normative range to which that species is adapted, the more energy an animal has to commit to maintaining its constant body temperature (Terrien et al., 2011). Consequently, den use can be crucial
Acknowledgements
We are grateful to the badger trapping team, past and present. We thank Ms. Nadine Adrianna Sugianto, a DPhil student atWildCRU, for supporting the surveys, and Prof. Andrew Markham, of Oxford University's Department of Computer Science, for loaning us data loggers We also thank Dr. Masayuki U. Saito, of Yamagata University's Faculty of Agriculture, for statistical advice in R. We thank the National Meteorological Library and Archive - Met Office, UK for the provision of meteorological data.
Conflict of interest
The authors declare no conflicts of interest.
Funding
This work was supported by Grant-in Aid for Scientific Research (JSPS KAKENHI Grant Number JP26257404).
Animal ethics statement
All work was evaluated by the University Oxford Animal Welfare and Ethical Review Board. Interventions at badger setts were performed under UK government Natural England licence numbers 2016–18558-SCI-SCI and 2017–27589-SCI-SCI. All animal trapping and handling procedures were performed under UK Animals (Scientific Procedures) Act, 1986 licence PPL
References (68)
- et al.
The effects of disturbance on the emergence of Eurosialn badgers in winter
Biol. Conserv.
(1985) - et al.
Does mean annual insolation have the potential to change the climate?
Earth Planet. Sci. Lett.
(2004) - et al.
Estimating metabolic heat loss in birds and mammals by combining infrared thermography with biophysical modelling
Comp. Biochem. Physiol. A. Mol. Integr. Physiol.
(2011) - et al.
The use and assessment of ketamine-medetomidine-butorphanol combinations for field anaesthesia in wild European badgers (Meles meles)
Vet. Anaesth. Analg.
(2005) - et al.
Soil heat flux and temperature variation with vegetation, soil type and climate
Agric. For. Meteorol.
(1987) Understanding variation in behavioural responses to human-induced rapid environmental change: a conceptual overview
Anim. Behav.
(2013)- et al.
Conditions inside fisher dens during prescribed fires; what is the risk posed by spring underburns?
For. Ecol. Manag.
(2016) - et al.
Effects of wetting of insulation of bird and mammal coats
J. Therm. Biol.
(1984) - et al.
Behavioral flexibility as a mechanism for coping with climate change
Front. Ecol. Environ.
(2017) - et al.
Microclimate in burrows of subterranean rodents—revisited
Temporal variance reverses the impact of high mean intensity of stress in climate change experiments
Ecology
Models of thermal protection in polar bear cubs-at birth and on emergence from the den
Am. J. Physiol. - Regul. Integr. Comp. Physiol.
Characterisation of Eurasian lynx Lynx lynx den sites and kitten survival
Wildl. Biol.
Adaptive thermoregulation in endotherms may alter responses to climate change
Integr. Comp. Biol.
In situ adaptive response to climate and habitat quality variation: spatial and temporal variation in European badger (Meles meles) body weight
Glob. Change Biol.
The influence of mean climate trends and climate variance on beaver survival and recruitment dynamics
Glob. Change Biol.
Population-level zoogeomorphology: the case of the Eurasian badger (Meles meles L.)
Phys. Geogr. Y.
Evolution of homeothermy in mammals
Nature
Why do European stoats Mustela erminea not follow Bergmann's Rule?
Ecography
Overwintering strategies of the badger, Meles meles, at 57°N
J. Zool.
Can behaviour douse the fire of climate warming?
Proc. Natl. Acad. Sci. Usa.
Climate-mediated energetic constraints on the distribution of hibernating mammals
Nature
Climate Change 2014: synthesis Report
Impacts, adaptation, and vulnerability. Part A: global and sectoral aspects
Vertical distribution of earthworms in grassland soils of the Colombian Llanos
Biol. Fertil. Soils
Environmental correlates of badger social spacing across Europe
J. Biogeogr.
Environmental relationships and the denning period of black bears in Tennessee
J. Mammal.
Variations in badger (Meles meles) sett microclimate: Differential cub survival between main and subsidiary setts, with implications for artificial sett construction
Int. J. Ecol.
Towards a molecular understanding of adaptive thermogenesis
Nature
Predicting badger sett numbers: evaluating methods in East Sussex
J. Biogeogr.
Badgers Meles meles population dynamics in Oxfordshire, UK, numbers, density and cohort life histories, and a possible role of climate change in population growth
J. Zool.
Badgers in the rural landscape - conservation paragon or farmland pariah? Lessons from the Wytham Badger Project
Are badgers ‘Under The weather’? Direct and indirect impacts of climate variation on European badger (Meles meles) population dynamics
Glob. Change Biol.
The distribution of Eurasian badger, Meles meles, setts in a high-density area: field observations contradict the sett dispersion hypothesis
Oikos
Cited by (15)
Extrinsic factors affecting cub development contribute to sexual size dimorphism in the European badger (Meles meles)
2019, ZoologyCitation Excerpt :In terms of weather, high rainfall during their first summer and winter had the most severe effects on both sexes, while effects of high rainfall during their second summer were less severe, due to cubs being closer to reaching their final somatic size. Persistently wet conditions expose cubs to greater hypothermic stress (Kaneko et al., 2010; Nouvellet et al., 2013; Tsunoda et al., 2018), where survival probability and recruitment are lower in years that are wetter than normal (Newman et al., 2001; Nouvellet et al., 2013; Macdonald et al., 2015), particularly when summer flooding occurs (Macdonald and Newman 2002; Macdonald et al., 2010). Weather conditions, especially during the first spring, do not only affect cubs directly, however, but also lactating mothers.
Influence of abiotic factors on habitat selection of sympatric ocelots and bobcats: testing the interactive range-limit theory
2023, Frontiers in Ecology and EvolutionEarly-life seasonal, weather and social effects on telomere length in a wild mammal
2022, Molecular Ecology