- Email: [email protected]
Winter microclimate of field voles (Microtus agrestis) in SW Scotland
ARTICLE IN PRESS
Journal of Thermal Biology 28 (2003) 397–401
Winter microclimate of field voles (Microtus agrestis) in SW Scotland D.J. McCaffertya,*, J.B. Moncrieffb, I.R. Taylorc a b
Department of Adult and Continuing Education, University of Glasgow, St. Andrew’s Building, 11 Eldon Street, Glasgow G3 6NH, UK Institute of Ecology and Resource Management, University of Edinburgh, Darwin Building, Mayfield Road, Edinburgh EH9 3JU, UK c Applied Ornithology Group, Johnstone Centre, Charles Sturt University P.O. Box 789, Albury, NSW 2640, Australia Received 4 December 2002; accepted 21 February 2003
Abstract The microclimate of the field vole (Microtus agrestis) was measured in rough grassland in SW Scotland from February–April 1992. Measurements represented conditions experienced by voles when foraging. Air temperature in the grass tunnels used by voles was only 0.3 C greater than air temperature above the vegetation. On average, the change in temperature in grass tunnels and at feeding stations used by voles matched the diurnal increase in air temperature. However, snow cover was found to insulate vole habitat from large changes in air temperature. The grassland provided considerable shading from solar radiation and shelter from wind. Solar radiation and wind speed at the surface were closely coupled with conditions above the ground surface due to the short height of grassland at this season of the year. Although the winter temperatures experienced by field voles are well below their thermoneutral zone of metabolism, their sheltered microclimate means that they can remain active in wet and windy weather when predators may be less able to detect them. r 2003 Elsevier Science Ltd. All rights reserved. Keywords: Microclimate; Field vole; Microtus agrestis; Temperature; Wind speed; Solar radiation
1. Introduction The field vole (Microtus agrestis) is a widely distributed microtine rodent found in rough grassland throughout the Palearctic (Gipps and Alibhai, 1991). Field voles exhibit short-term and circadian rhythms of activity together with long-term seasonal changes in the timing of activity. They typically have a 2–4 h activity pattern of feeding followed by rest periods (Davis, 1933; Lehmann, 1976) and are more active at night, with peaks in activity around sunset and shortly before sunrise (Davis, 1933; Nygren, 1978). It also appears that these circadian rhythms shift seasonally such that voles
*Corresponding author. Tel.: +44-141-330-1803; fax: +44141-330-1835. E-mail address: [email protected] (D.J. McCafferty).
are more active during the day in winter (Baumler, 1975; Erkinaro 1961, 1970). The high metabolic rate associated with small body size suggests that avoidance of heat loss may be important in reducing overall energy demands for voles, especially in winter. The metabolic rate of field voles doubles between typical summer and winter temperatures (Hansson and Grodzinski, 1970). High wind speeds have also been shown to increase metabolic heat production of small mammals (Chappell and Holsclaw, 1984), indicating that other factors may strongly influence energy costs for field voles. It has been suggested that due to the shelter provided by vegetation within which voles live, weather conditions have relatively little importance in determining their activity patterns (Halle, 2000). Laboratory studies have indeed shown that field voles can avoid low temperatures by building well-insulated nests and by huddling to keep warm (Hayes et al., 1992; Redman et al., 1999).
0306-4565/03/$ - see front matter r 2003 Elsevier Science Ltd. All rights reserved. doi:10.1016/S0306-4565(03)00024-X
ARTICLE IN PRESS 398
D.J. McCafferty et al. / Journal of Thermal Biology 28 (2003) 397–401
Nevertheless, it is not known what temperatures are experienced by voles in the wild and if the habitat allows them to avoid the cooling effects of wind. The aim of this study was therefore to determine the microclimate of field voles in order to understand how weather may influence their behaviour.
2. Materials and methods 2.1. Field measurements The microclimate of the field vole was measured in rough grassland at an altitude of 300 m at Eskdalemuir in SW Scotland (55 190 N 3 140 W) from February to April 1992. The grassland was dominated by purple moor-grass (Molinia caerulea) and soft rush (Juncus effusus) which was within the forest ride of a sitka spruce (Picea sitchensis) plantation. The maximum height of grassland was approximately 0.45 m. Field vole runways were identified by the presence of faeces and caches of partially eaten vegetation at the entrance to grass tunnels (Gipps and Alibhai, 1991). Temperature (70.1 C) was measured using thermocouple junctions placed at the entrance and 10–20 cm inside five vole runways at the base of the vegetation. Thermocouples (0.2 mm welded tip type K thermocouples RS Ltd.) were weather-proofed with a thin covering of epoxy adhesive and wired in parallel to give a mean temperature for both entrance and tunnel sites. Solar radiation (71 W m2) was measured with a mini pyranometer (LI–200SZ, Li-cor Ltd.) at the entrance to a vole tunnel. Wind speed (70.01 m s1) was measured with a hot wire anemometer (AVM 501, Proster Scientific Instruments Ltd) at 1 cm above the ground surface at the entrance to a vole tunnel. Microclimate measurements were compared with wind speed, solar radiation and temperature above the ground surface. Wind speed (70.1 m s1) was recorded using cup anemometers (A100R, Vector Instruments Ltd.) at a height of 0.45 and 1.7 m (over grassland) and at 9 m (over the forest). Air temperature was recorded at 9 m using a shielded temperature sensor (Skye 103, Skye Inst. Ltd.). Measurements were recorded automatically and stored as 10 min averages on data loggers (CR10 and 21X, Campbell Scientific Instruments). Snowfall data were obtained from Eskdalemuir Meteorological Observatory which has similar climatic conditions (McCafferty, 1993) and is situated 7 km from the study site. 2.2. Instrument calibration Thermocouples were calibrated in an ethylene glycol temperature-controlled bath and the temperature sensor
was calibrated in a cooled incubator against a standard platinum resistance thermometer (Guildline Instruments Ltd.). Cup anemometers were calibrated (1–10 m s1) in an experimental wind tunnel where wind speed was measured using a pitot tube and atmospheric pressure readings. The flow regime was laminar, with a turbulent intensity of 1% in the empty tunnel at 4 m s1 (Grace, 1978). The hot wire anemometer was calibrated by mounting the anemometer on an aluminium trolley, which ran freely on bearings along a smooth rail. The trolley speed was controlled by computer (BBC microcomputer), which allowed speeds of 5–50 cm s1. A plastic enclosure was placed over the top of the apparatus to ensure still air conditions. The voltage output from the anemometer was recorded at an execution interval of 0.1 and 0.05 s for wind speeds >35 cm s1. Acceleration and deceleration readings were rejected from the start and the end of each calibration and a third-order polynomial was fitted to the mean voltage output at each wind speed. The effect of air temperature (1–20 C) on anemometer performance was examined by placing the anemometer inside a cooled incubator. The anemometer was clamped at the base of a vertically mounted plastic tube fitted with a 12 V electric fan (Micronel Ltd.) which was run from a stabilised power supply (L30B Farnell Ltd.) outside the incubator. The anemometer was found to have a mean temperature coefficient of 7 mV C1 (SE=0.21). The effect of supply voltage on anemometer output was also investigated by allowing the supply voltage provided by 9 V alkaline cells to fall with continuous use. The anemometer was mounted in airflow of approximately 10 cm s1 for 48 h. Voltage output from the anemometer fell rapidly with decreasing battery voltage within 24 h continuous operation. The anemometer was therefore powered in the field by a regulated supply from two 12 V, 24 A h1 lead acid batteries and all measurements were corrected for changes in air temperature. The manufacturer’s calibration was used for pyranometer measurements.
3. Results 3.1. Microclimate Continuous records of temperature and solar radiation were obtained for 34 days and wind speed for 26 days. Data were summarised as hourly averages and these were used to calculate daily averages and maximum and minimum hourly values of temperature, solar radiation and wind speed (Table 1). The temperature of vole habitat in the absence of snow cover exhibited a typical pattern of diurnal warming and nocturnal cooling similar to the change in air temperature above the vegetation (Fig. 1).
ARTICLE IN PRESS D.J. McCafferty et al. / Journal of Thermal Biology 28 (2003) 397–401
399
Table 1 Microclimate of field vole habitat from February to April 1992 Mean
SE
Min
Max 12.0 11.4 11.9
Air temperature ( C) Tunnel Entrance Above vegetation
5.1 4.5 4.8
0.23 0.26 0.21
2.8 5.4 3.1
Wind speed (ms1) 0.01 m 0.45 m 1.70 m 9.00 m
0.13 1.21 1.78 3.27
0.003 0.02 0.03 0.05
0.0 o0.1a o0.1a o0.1a
Solar radiation (W m2) (0700–1900 GMT) Entrance Above vegetation
8.6 101.1
1.6 19.7
0 0
0.29 2.88 3.99 7.58
40.0 463.8
Fig 2. Mean air temperature ( C) of field vole habitat during a period of snow cover (depth=0.05 m) from afternoon of 1 April to morning of 3 April 1992.
Data was summarised from mean hourly values. a The minimum wind speed recorded with cup anemometers was 0.1 ms1.
Fig 3. Mean wind speed (m s1) measured at the entrance to a vole tunnel (height=0.01 m) and above the vegetation (height=9 m) from February to April 1992.
Fig 1. Mean air temperature ( C) measured at the entrance and inside field vole tunnels from February to April 1992. These measurements are compared with mean air temperature above the vegetation. Time is given as Greenwich Mean Time (GMT).
Temperature inside the tunnels was on average only 0.3 C greater than the air temperature (paired t-test, t ¼ 19:7; d.f.=23, po0:0001). At the entrance to tunnels, the temperature was on average 0.3 C colder than air temperature (t ¼ 3:5; df=23, po0:01) and there was a clear pattern of surface cooling at night followed by surface heating during the day (Fig. 1). The effect of snow cover (approximate depth=0.05 m) was to insulate vole habitat from large changes in air temperature (Fig. 2). During this period, the temperature of vole habitat was relatively stable and remained greater than air temperature. In the grass tunnels, the temperature was found to be as much as 3 C above air temperature during the coldest period of the night.
Wind speed recorded at the entrance to the vole tunnel closely matched changes in wind speed above the vegetation, which showed a clear diurnal pattern (Fig. 3). Mean daily wind speed recorded at the entrance to the vole tunnel was 0.13 m s1 and the maximum wind speed was 0.29 m s1. This compared with a daily mean of 1.2 m s1 and a maximum hourly wind speed of 2.9 m s1 at 0.45 m above the surface. Solar radiation at the entrance to the vole tunnel showed a diurnal pattern corresponding to the flux above the vegetation and averaged 8.6 W m2 with a maximum flux of 40 W m2 (Fig. 4). This represented only 8% of that received above the vegetation.
4. Discussion 4.1. Microclimate This study provided data on the microclimate of field voles in late winter in an upland area of SW Scotland.
ARTICLE IN PRESS 400
D.J. McCafferty et al. / Journal of Thermal Biology 28 (2003) 397–401
Fig 4. Mean solar radiation (W m2) measured at the entrance to a field vole tunnel and above the vegetation from February to April 1992.
The data are insufficient to fully describe the thermal conditions of field voles. Nevertheless, it is possible to determine the extent to which certain environmental variables may be important to field voles in natural conditions. The air temperature experienced by field voles followed a pattern of diurnal warming and nocturnal cooling similar to air temperature measured above the vegetation. These findings were somewhat different from studies on other species of small mammals where burrow and nest temperatures remain relatively stable (Hayward, 1965; Stark, 1963). In this study, thermocouples recorded the temperature of feeding stations at the entrance to tunnels and inside the network of runways through the grass. The temperatures in these locations are likely to be considerably less than in well-insulated nests which are also heated by an animal’s own body heat. In the laboratory, local heating effects of 7 C have been recorded in field vole nests at 0 C and heating effects were even greater if there were more than one individual in the nest at any one time (Hayes et al., 1992; Redman et al., 1999). Measurements in this study were therefore thought to represent conditions experienced by voles when foraging. Snow cover protected field voles from cold conditions as the temperature remained 3 C higher than air temperature when there was a thin snow layer. Vegetation preserves a distinct airspace beneath snow where small mammals can live and where the temperature remains relatively stable (Coulianos and Johnels, 1963). Insulation provided by snow is likely to be more important for field voles if the temperature falls even lower than those recorded in this study. For example, Johnson (1951) found that red-backed voles (Clethrionomys rutilis) in Alaska used these subnivean locations (70–85 cm beneath the surface) where temperatures were 3 to 6 C when above snow temperatures ranged between 45 C and 10 C.
Both solar radiation and wind speed at the entrance to field vole tunnels had diurnal patterns corresponding to changes above the vegetation. Due to shading, the solar radiation at the entrance to the vole tunnel was less than 10% of that above the vegetation. Similarly, wind speed declined rapidly towards the surface, indicating that voles may experience wind speeds on average of around 0.1 m s1. It is expected that the growth of the vegetation in summer would further reduce solar radiation and wind speed experienced by field voles. Taller vegetation would also lead to less diurnal changes in temperature, humidity, wind speed and solar radiation (Oke, 1978). 4.2. Ecological implications Temperature is likely to have the greatest influence on field vole activity in SW Scotland as throughout the year voles experience temperatures well below their thermoneutral zone of metabolism which is around 25–35 C (Rigaudiere and Delost, 1964; McDevitt and Speakman, 1994). Field voles are less likely to be influenced by any thermal effects of solar radiation and wind because of the shelter provided by their tunnel systems within the vegetation. Studies of some small mammals have shown that there appears to be no correlation between activity and wind speed (Marten, 1973; Doucet and Bider, 1974). Although rainfall can potentially lead to increased energy costs by reducing pelage insulation (Webb and King, 1984), small mammals are often more active during rain (Doucet and Bider, 1974; Vickery and Bider, 1981; Gauthier and Bider, 1987). The runway systems and well-insulated nests used by field voles mean that they are unlikely to become wet, even in heavy rain. It may be advantageous for voles to be active during rain as predators may find it difficult to detect their scent or sound in wet and windy conditions (Vickery and Bider, 1981; Gauthier and Bider, 1987). The noise of wind and rain will interfere with detection of sounds and wetting of vegetation may reduce the sound of small mammals and wash away scent trails. Behavioural responses of field voles and other small mammals to weather may therefore be due to the fact that they live in a relatively sheltered microclimate and that they have evolved behaviours that balance energetic considerations with the risk of predation.
Acknowledgements Thanks to Tillhill Economic Forestry who allowed field work to be carried out at the study site, to all staff and colleagues at IERM for assistance throughout the study. This work was supported by a Chalmers Research Scholarship (University of Edinburgh).
ARTICLE IN PRESS D.J. McCafferty et al. / Journal of Thermal Biology 28 (2003) 397–401
References Baumler, W., 1975. Activity of some mammals in the field. Acta Theriol. 20, 365–377. Chappell, M.A., Holsclaw, D.S., 1984. Effects of wind on thermoregulation and energy balance in deer mice (Peromyscus maniculatus). J. Comp. Physiol. B 154, 619–625. Coulianos, C.C., Johnels, A.G., 1963. Notes on the subnivean environment of small mammals. Ark. Zool. Stockholm 15, 363–370. Davis, D.H.S., 1933. Rhythmic activity in the short tailed-tailed vole Microtus. J. Anim. Ecol. 2, 232–238. Doucet, G.J., Bider, J.R., 1974. The effects of weather on the activity of the masked shrew. J. Mammal. 55, 348–363. Erkinaro, E., 1961. The seasonal change of the activity of Microtus agrestis. Oikos 12, 157–163. Erkinaro, E., 1970. Der Phasenwechsel der lokomotorischen aktivitat bei Microtus agrestis (L.), M. arvalis (Pall.) und M. oeconomus (Pall.). Aquilo (Zool.) 8, 1–29. Gauthier, R., Bider, R., 1987. The effects of weather on runway use by rodents. Can. J. Zool. 65, 2035–2038. Gipps, J.H.W., Alibhai, S.K., 1991. Field vole Microtus agrestis. In: Corbet, G.B., Harris, S. (Eds.), Handbook of British Mammals, 3rd Edition. Blackwell, Oxford. Grace, J., 1978. The turbulent boundary layer over a flapping Populus leaf. Plant Cell Environ. 1, 35–38. Halle, S., 2000. Voles—small graminivores with polyphasic patterns. In: Halle, S., Stenseth, N.C. (Eds.), Activity Patterns in Small Mammals. Ecological Studies., Vol. 141. Springer, Berlin. Hansson, L., Grodzinski, W., 1970. Bioenergetic parameters of the field vole Microtus agrestis L. Oikos 21, 76–82. Hayes, J.P., Speakman, J.R., Racey, P.A., 1992. The contributions of local heating and reducing exposed surface area to the energetic benefits of huddling by short-tailed field voles (Microtus agrestis). Physiol. Zool. 65, 742–762.
401
Hayward, J.S., 1965. Microclimate temperature and its adaptive significance in 6 geographic races of Peromyscus maniculatus. Can. J. Zool. 43, 341–350. Johnson, H.M., 1951. Preliminary ecological studies of the microclimates inhabited by the smaller arctic and subarctic mammals. Proceedings of the Second Alaskan Science Conference (Alaska Div. AAAS), Vol. 2, pp. 125–131. Lehmann, U., 1976. Short term and circadian rhythms in the behaviour of the vole, Microtus agrestis (L.). Oecologia 23, 185–199. Marten, G.G., 1973. Time patterns of Peromyscus activity and their correlations with weather. J. Mammal. 54, 169–188. McCafferty, D.J., 1993. Biophysical ecology of the barn owl (Tyto alba Scopoli). Ph.D. Thesis, University of Edinburgh. McDevitt, R.M., Speakman, J.R., 1994. Limits to sustainable metabolic rate during transient exposure to low temperatures in short tailed field voles (Microtus agrestis). Physiol. Zool. 67, 1103–1116. Nygren, J., 1978. Interindividual influence on diurnal rhythms of activity in cycling and noncycling populations of the field vole, Microtus agrestis L. Oecologia 35, 231–239. Oke, T.R., 1978. Boundary Layer Climates. Methuen, London. Redman, P., Selman, C., Speakman, J.R., 1999. Male shorttailed voles (Microtus agrestis) build better insulated nests than females. J. Comp. Physiol. B 169, 581–587. Rigaudiere, N., Delost, P., 1964. Point de neutralite thermique et metabolisme de base chez les Campagnols. J. Physiol. Paris 56, 431–432. Stark, H.E., 1963. Nesting habits of the California vole, Microtus californicus and microclimatic factors affecting its nests. Ecology 44, 663–669. Vickery, W.L., Bider, J.R., 1981. The influence of weather on rodent activity. J. Mammal. 62, 140–145. Webb, D.R., King, J.R., 1984. Effects of wetting on insulation of bird and mammal coats. J. Therm. Biol. 9, 189–191.
Journal of Thermal Biology 28 (2003) 397–401
Winter microclimate of field voles (Microtus agrestis) in SW Scotland D.J. McCaffertya,*, J.B. Moncrieffb, I.R. Taylorc a b
Department of Adult and Continuing Education, University of Glasgow, St. Andrew’s Building, 11 Eldon Street, Glasgow G3 6NH, UK Institute of Ecology and Resource Management, University of Edinburgh, Darwin Building, Mayfield Road, Edinburgh EH9 3JU, UK c Applied Ornithology Group, Johnstone Centre, Charles Sturt University P.O. Box 789, Albury, NSW 2640, Australia Received 4 December 2002; accepted 21 February 2003
Abstract The microclimate of the field vole (Microtus agrestis) was measured in rough grassland in SW Scotland from February–April 1992. Measurements represented conditions experienced by voles when foraging. Air temperature in the grass tunnels used by voles was only 0.3 C greater than air temperature above the vegetation. On average, the change in temperature in grass tunnels and at feeding stations used by voles matched the diurnal increase in air temperature. However, snow cover was found to insulate vole habitat from large changes in air temperature. The grassland provided considerable shading from solar radiation and shelter from wind. Solar radiation and wind speed at the surface were closely coupled with conditions above the ground surface due to the short height of grassland at this season of the year. Although the winter temperatures experienced by field voles are well below their thermoneutral zone of metabolism, their sheltered microclimate means that they can remain active in wet and windy weather when predators may be less able to detect them. r 2003 Elsevier Science Ltd. All rights reserved. Keywords: Microclimate; Field vole; Microtus agrestis; Temperature; Wind speed; Solar radiation
1. Introduction The field vole (Microtus agrestis) is a widely distributed microtine rodent found in rough grassland throughout the Palearctic (Gipps and Alibhai, 1991). Field voles exhibit short-term and circadian rhythms of activity together with long-term seasonal changes in the timing of activity. They typically have a 2–4 h activity pattern of feeding followed by rest periods (Davis, 1933; Lehmann, 1976) and are more active at night, with peaks in activity around sunset and shortly before sunrise (Davis, 1933; Nygren, 1978). It also appears that these circadian rhythms shift seasonally such that voles
*Corresponding author. Tel.: +44-141-330-1803; fax: +44141-330-1835. E-mail address: [email protected] (D.J. McCafferty).
are more active during the day in winter (Baumler, 1975; Erkinaro 1961, 1970). The high metabolic rate associated with small body size suggests that avoidance of heat loss may be important in reducing overall energy demands for voles, especially in winter. The metabolic rate of field voles doubles between typical summer and winter temperatures (Hansson and Grodzinski, 1970). High wind speeds have also been shown to increase metabolic heat production of small mammals (Chappell and Holsclaw, 1984), indicating that other factors may strongly influence energy costs for field voles. It has been suggested that due to the shelter provided by vegetation within which voles live, weather conditions have relatively little importance in determining their activity patterns (Halle, 2000). Laboratory studies have indeed shown that field voles can avoid low temperatures by building well-insulated nests and by huddling to keep warm (Hayes et al., 1992; Redman et al., 1999).
0306-4565/03/$ - see front matter r 2003 Elsevier Science Ltd. All rights reserved. doi:10.1016/S0306-4565(03)00024-X
ARTICLE IN PRESS 398
D.J. McCafferty et al. / Journal of Thermal Biology 28 (2003) 397–401
Nevertheless, it is not known what temperatures are experienced by voles in the wild and if the habitat allows them to avoid the cooling effects of wind. The aim of this study was therefore to determine the microclimate of field voles in order to understand how weather may influence their behaviour.
2. Materials and methods 2.1. Field measurements The microclimate of the field vole was measured in rough grassland at an altitude of 300 m at Eskdalemuir in SW Scotland (55 190 N 3 140 W) from February to April 1992. The grassland was dominated by purple moor-grass (Molinia caerulea) and soft rush (Juncus effusus) which was within the forest ride of a sitka spruce (Picea sitchensis) plantation. The maximum height of grassland was approximately 0.45 m. Field vole runways were identified by the presence of faeces and caches of partially eaten vegetation at the entrance to grass tunnels (Gipps and Alibhai, 1991). Temperature (70.1 C) was measured using thermocouple junctions placed at the entrance and 10–20 cm inside five vole runways at the base of the vegetation. Thermocouples (0.2 mm welded tip type K thermocouples RS Ltd.) were weather-proofed with a thin covering of epoxy adhesive and wired in parallel to give a mean temperature for both entrance and tunnel sites. Solar radiation (71 W m2) was measured with a mini pyranometer (LI–200SZ, Li-cor Ltd.) at the entrance to a vole tunnel. Wind speed (70.01 m s1) was measured with a hot wire anemometer (AVM 501, Proster Scientific Instruments Ltd) at 1 cm above the ground surface at the entrance to a vole tunnel. Microclimate measurements were compared with wind speed, solar radiation and temperature above the ground surface. Wind speed (70.1 m s1) was recorded using cup anemometers (A100R, Vector Instruments Ltd.) at a height of 0.45 and 1.7 m (over grassland) and at 9 m (over the forest). Air temperature was recorded at 9 m using a shielded temperature sensor (Skye 103, Skye Inst. Ltd.). Measurements were recorded automatically and stored as 10 min averages on data loggers (CR10 and 21X, Campbell Scientific Instruments). Snowfall data were obtained from Eskdalemuir Meteorological Observatory which has similar climatic conditions (McCafferty, 1993) and is situated 7 km from the study site. 2.2. Instrument calibration Thermocouples were calibrated in an ethylene glycol temperature-controlled bath and the temperature sensor
was calibrated in a cooled incubator against a standard platinum resistance thermometer (Guildline Instruments Ltd.). Cup anemometers were calibrated (1–10 m s1) in an experimental wind tunnel where wind speed was measured using a pitot tube and atmospheric pressure readings. The flow regime was laminar, with a turbulent intensity of 1% in the empty tunnel at 4 m s1 (Grace, 1978). The hot wire anemometer was calibrated by mounting the anemometer on an aluminium trolley, which ran freely on bearings along a smooth rail. The trolley speed was controlled by computer (BBC microcomputer), which allowed speeds of 5–50 cm s1. A plastic enclosure was placed over the top of the apparatus to ensure still air conditions. The voltage output from the anemometer was recorded at an execution interval of 0.1 and 0.05 s for wind speeds >35 cm s1. Acceleration and deceleration readings were rejected from the start and the end of each calibration and a third-order polynomial was fitted to the mean voltage output at each wind speed. The effect of air temperature (1–20 C) on anemometer performance was examined by placing the anemometer inside a cooled incubator. The anemometer was clamped at the base of a vertically mounted plastic tube fitted with a 12 V electric fan (Micronel Ltd.) which was run from a stabilised power supply (L30B Farnell Ltd.) outside the incubator. The anemometer was found to have a mean temperature coefficient of 7 mV C1 (SE=0.21). The effect of supply voltage on anemometer output was also investigated by allowing the supply voltage provided by 9 V alkaline cells to fall with continuous use. The anemometer was mounted in airflow of approximately 10 cm s1 for 48 h. Voltage output from the anemometer fell rapidly with decreasing battery voltage within 24 h continuous operation. The anemometer was therefore powered in the field by a regulated supply from two 12 V, 24 A h1 lead acid batteries and all measurements were corrected for changes in air temperature. The manufacturer’s calibration was used for pyranometer measurements.
3. Results 3.1. Microclimate Continuous records of temperature and solar radiation were obtained for 34 days and wind speed for 26 days. Data were summarised as hourly averages and these were used to calculate daily averages and maximum and minimum hourly values of temperature, solar radiation and wind speed (Table 1). The temperature of vole habitat in the absence of snow cover exhibited a typical pattern of diurnal warming and nocturnal cooling similar to the change in air temperature above the vegetation (Fig. 1).
ARTICLE IN PRESS D.J. McCafferty et al. / Journal of Thermal Biology 28 (2003) 397–401
399
Table 1 Microclimate of field vole habitat from February to April 1992 Mean
SE
Min
Max 12.0 11.4 11.9
Air temperature ( C) Tunnel Entrance Above vegetation
5.1 4.5 4.8
0.23 0.26 0.21
2.8 5.4 3.1
Wind speed (ms1) 0.01 m 0.45 m 1.70 m 9.00 m
0.13 1.21 1.78 3.27
0.003 0.02 0.03 0.05
0.0 o0.1a o0.1a o0.1a
Solar radiation (W m2) (0700–1900 GMT) Entrance Above vegetation
8.6 101.1
1.6 19.7
0 0
0.29 2.88 3.99 7.58
40.0 463.8
Fig 2. Mean air temperature ( C) of field vole habitat during a period of snow cover (depth=0.05 m) from afternoon of 1 April to morning of 3 April 1992.
Data was summarised from mean hourly values. a The minimum wind speed recorded with cup anemometers was 0.1 ms1.
Fig 3. Mean wind speed (m s1) measured at the entrance to a vole tunnel (height=0.01 m) and above the vegetation (height=9 m) from February to April 1992.
Fig 1. Mean air temperature ( C) measured at the entrance and inside field vole tunnels from February to April 1992. These measurements are compared with mean air temperature above the vegetation. Time is given as Greenwich Mean Time (GMT).
Temperature inside the tunnels was on average only 0.3 C greater than the air temperature (paired t-test, t ¼ 19:7; d.f.=23, po0:0001). At the entrance to tunnels, the temperature was on average 0.3 C colder than air temperature (t ¼ 3:5; df=23, po0:01) and there was a clear pattern of surface cooling at night followed by surface heating during the day (Fig. 1). The effect of snow cover (approximate depth=0.05 m) was to insulate vole habitat from large changes in air temperature (Fig. 2). During this period, the temperature of vole habitat was relatively stable and remained greater than air temperature. In the grass tunnels, the temperature was found to be as much as 3 C above air temperature during the coldest period of the night.
Wind speed recorded at the entrance to the vole tunnel closely matched changes in wind speed above the vegetation, which showed a clear diurnal pattern (Fig. 3). Mean daily wind speed recorded at the entrance to the vole tunnel was 0.13 m s1 and the maximum wind speed was 0.29 m s1. This compared with a daily mean of 1.2 m s1 and a maximum hourly wind speed of 2.9 m s1 at 0.45 m above the surface. Solar radiation at the entrance to the vole tunnel showed a diurnal pattern corresponding to the flux above the vegetation and averaged 8.6 W m2 with a maximum flux of 40 W m2 (Fig. 4). This represented only 8% of that received above the vegetation.
4. Discussion 4.1. Microclimate This study provided data on the microclimate of field voles in late winter in an upland area of SW Scotland.
ARTICLE IN PRESS 400
D.J. McCafferty et al. / Journal of Thermal Biology 28 (2003) 397–401
Fig 4. Mean solar radiation (W m2) measured at the entrance to a field vole tunnel and above the vegetation from February to April 1992.
The data are insufficient to fully describe the thermal conditions of field voles. Nevertheless, it is possible to determine the extent to which certain environmental variables may be important to field voles in natural conditions. The air temperature experienced by field voles followed a pattern of diurnal warming and nocturnal cooling similar to air temperature measured above the vegetation. These findings were somewhat different from studies on other species of small mammals where burrow and nest temperatures remain relatively stable (Hayward, 1965; Stark, 1963). In this study, thermocouples recorded the temperature of feeding stations at the entrance to tunnels and inside the network of runways through the grass. The temperatures in these locations are likely to be considerably less than in well-insulated nests which are also heated by an animal’s own body heat. In the laboratory, local heating effects of 7 C have been recorded in field vole nests at 0 C and heating effects were even greater if there were more than one individual in the nest at any one time (Hayes et al., 1992; Redman et al., 1999). Measurements in this study were therefore thought to represent conditions experienced by voles when foraging. Snow cover protected field voles from cold conditions as the temperature remained 3 C higher than air temperature when there was a thin snow layer. Vegetation preserves a distinct airspace beneath snow where small mammals can live and where the temperature remains relatively stable (Coulianos and Johnels, 1963). Insulation provided by snow is likely to be more important for field voles if the temperature falls even lower than those recorded in this study. For example, Johnson (1951) found that red-backed voles (Clethrionomys rutilis) in Alaska used these subnivean locations (70–85 cm beneath the surface) where temperatures were 3 to 6 C when above snow temperatures ranged between 45 C and 10 C.
Both solar radiation and wind speed at the entrance to field vole tunnels had diurnal patterns corresponding to changes above the vegetation. Due to shading, the solar radiation at the entrance to the vole tunnel was less than 10% of that above the vegetation. Similarly, wind speed declined rapidly towards the surface, indicating that voles may experience wind speeds on average of around 0.1 m s1. It is expected that the growth of the vegetation in summer would further reduce solar radiation and wind speed experienced by field voles. Taller vegetation would also lead to less diurnal changes in temperature, humidity, wind speed and solar radiation (Oke, 1978). 4.2. Ecological implications Temperature is likely to have the greatest influence on field vole activity in SW Scotland as throughout the year voles experience temperatures well below their thermoneutral zone of metabolism which is around 25–35 C (Rigaudiere and Delost, 1964; McDevitt and Speakman, 1994). Field voles are less likely to be influenced by any thermal effects of solar radiation and wind because of the shelter provided by their tunnel systems within the vegetation. Studies of some small mammals have shown that there appears to be no correlation between activity and wind speed (Marten, 1973; Doucet and Bider, 1974). Although rainfall can potentially lead to increased energy costs by reducing pelage insulation (Webb and King, 1984), small mammals are often more active during rain (Doucet and Bider, 1974; Vickery and Bider, 1981; Gauthier and Bider, 1987). The runway systems and well-insulated nests used by field voles mean that they are unlikely to become wet, even in heavy rain. It may be advantageous for voles to be active during rain as predators may find it difficult to detect their scent or sound in wet and windy conditions (Vickery and Bider, 1981; Gauthier and Bider, 1987). The noise of wind and rain will interfere with detection of sounds and wetting of vegetation may reduce the sound of small mammals and wash away scent trails. Behavioural responses of field voles and other small mammals to weather may therefore be due to the fact that they live in a relatively sheltered microclimate and that they have evolved behaviours that balance energetic considerations with the risk of predation.
Acknowledgements Thanks to Tillhill Economic Forestry who allowed field work to be carried out at the study site, to all staff and colleagues at IERM for assistance throughout the study. This work was supported by a Chalmers Research Scholarship (University of Edinburgh).
ARTICLE IN PRESS D.J. McCafferty et al. / Journal of Thermal Biology 28 (2003) 397–401
References Baumler, W., 1975. Activity of some mammals in the field. Acta Theriol. 20, 365–377. Chappell, M.A., Holsclaw, D.S., 1984. Effects of wind on thermoregulation and energy balance in deer mice (Peromyscus maniculatus). J. Comp. Physiol. B 154, 619–625. Coulianos, C.C., Johnels, A.G., 1963. Notes on the subnivean environment of small mammals. Ark. Zool. Stockholm 15, 363–370. Davis, D.H.S., 1933. Rhythmic activity in the short tailed-tailed vole Microtus. J. Anim. Ecol. 2, 232–238. Doucet, G.J., Bider, J.R., 1974. The effects of weather on the activity of the masked shrew. J. Mammal. 55, 348–363. Erkinaro, E., 1961. The seasonal change of the activity of Microtus agrestis. Oikos 12, 157–163. Erkinaro, E., 1970. Der Phasenwechsel der lokomotorischen aktivitat bei Microtus agrestis (L.), M. arvalis (Pall.) und M. oeconomus (Pall.). Aquilo (Zool.) 8, 1–29. Gauthier, R., Bider, R., 1987. The effects of weather on runway use by rodents. Can. J. Zool. 65, 2035–2038. Gipps, J.H.W., Alibhai, S.K., 1991. Field vole Microtus agrestis. In: Corbet, G.B., Harris, S. (Eds.), Handbook of British Mammals, 3rd Edition. Blackwell, Oxford. Grace, J., 1978. The turbulent boundary layer over a flapping Populus leaf. Plant Cell Environ. 1, 35–38. Halle, S., 2000. Voles—small graminivores with polyphasic patterns. In: Halle, S., Stenseth, N.C. (Eds.), Activity Patterns in Small Mammals. Ecological Studies., Vol. 141. Springer, Berlin. Hansson, L., Grodzinski, W., 1970. Bioenergetic parameters of the field vole Microtus agrestis L. Oikos 21, 76–82. Hayes, J.P., Speakman, J.R., Racey, P.A., 1992. The contributions of local heating and reducing exposed surface area to the energetic benefits of huddling by short-tailed field voles (Microtus agrestis). Physiol. Zool. 65, 742–762.
401
Hayward, J.S., 1965. Microclimate temperature and its adaptive significance in 6 geographic races of Peromyscus maniculatus. Can. J. Zool. 43, 341–350. Johnson, H.M., 1951. Preliminary ecological studies of the microclimates inhabited by the smaller arctic and subarctic mammals. Proceedings of the Second Alaskan Science Conference (Alaska Div. AAAS), Vol. 2, pp. 125–131. Lehmann, U., 1976. Short term and circadian rhythms in the behaviour of the vole, Microtus agrestis (L.). Oecologia 23, 185–199. Marten, G.G., 1973. Time patterns of Peromyscus activity and their correlations with weather. J. Mammal. 54, 169–188. McCafferty, D.J., 1993. Biophysical ecology of the barn owl (Tyto alba Scopoli). Ph.D. Thesis, University of Edinburgh. McDevitt, R.M., Speakman, J.R., 1994. Limits to sustainable metabolic rate during transient exposure to low temperatures in short tailed field voles (Microtus agrestis). Physiol. Zool. 67, 1103–1116. Nygren, J., 1978. Interindividual influence on diurnal rhythms of activity in cycling and noncycling populations of the field vole, Microtus agrestis L. Oecologia 35, 231–239. Oke, T.R., 1978. Boundary Layer Climates. Methuen, London. Redman, P., Selman, C., Speakman, J.R., 1999. Male shorttailed voles (Microtus agrestis) build better insulated nests than females. J. Comp. Physiol. B 169, 581–587. Rigaudiere, N., Delost, P., 1964. Point de neutralite thermique et metabolisme de base chez les Campagnols. J. Physiol. Paris 56, 431–432. Stark, H.E., 1963. Nesting habits of the California vole, Microtus californicus and microclimatic factors affecting its nests. Ecology 44, 663–669. Vickery, W.L., Bider, J.R., 1981. The influence of weather on rodent activity. J. Mammal. 62, 140–145. Webb, D.R., King, J.R., 1984. Effects of wetting on insulation of bird and mammal coats. J. Therm. Biol. 9, 189–191.