Water consumption by Red Tree Voles (Arborimus longicaudus).
Key words: Arborimus longicaudus, Arborimus pomo, Microtus, Myodes, Oregon, Red Tree Vole, water consumption
Studies of voles in the genera Microtus, Pitymys, and Myodes suggest that most species consume relatively large amounts of free water per day when kept in captivity and fed artificial diets of dry lab chow. Typical amounts of water consumed per day reported in the literature range from 0.25 to 0.60 ml/g of body mass (Chew 1951; Church 1966; Getz 1963; Pearson 1972; McManus 1974; Rhodes and Richmond 1981). These estimates suggest that many voles drink 40 to 60% of their mass in water each day. Although not all of these studies used the same methods or foods, they do suggest that availability of free water or plant foods with high water content may be important factors limiting the distribution of many species of voles (Pearson 1972). The water consumption studies cited previously also raise interesting questions regarding the adaptations that allow some species of voles like the Sagebrush Vole (Lemmiscus curtatus) to live in relatively xeric environments where free water is unavailable for long periods of time.
Tree Voles (Arborimus [Phenacomys] longicaudus, A. pomo) live in relatively mesic forest environments in western Oregon and northwestern California. They spend most of their time in the forest canopy, although they do occasionally descend to the ground to move between trees that are not interconnected by limbs (Swingle and Forsman 2009). Although it is generally assumed that Tree Voles obtain much of their water from their food, they also obtain free water by licking dew or rain from the needles of the conifers in which they live (Howell 1926; Maser 1966). This has led some observers to suggest that Tree Voles can only occur in areas where fog or dew is common in summer. This hypothesis has never been tested. An alternative hypothesis is that, although they will drink free water when it is available, Tree Voles are capable of persisting for long periods solely on the water obtained from their food, which consists of the needles and bark of conifers, especially Douglas-fir (Pseudotsuga menziesii; Howell 1926; Maser and others 1981). This hypothesis has not been tested, and, in fact, the only quantitative data on water consumption of Tree Voles was recorded by Howell (1926:54) who reported that 2 subadult females drank an average of 6 ml of water/d (approximately 0.25 ml/g/d). If true, this would be equivalent to a vole drinking approximately 25% of its body mass in water per day. We found this questionable because we (and others) have found many Tree Voles in comparatively dry upland forests where they do not have easy access to large amounts of free water during summer. Therefore, our objective was to mononitor the amount of free water consumed per day by captive Tree Voles that were fed a normal diet of Douglas-fir needles, with water provided only in meniscus style water tubes that could be weighed to estimate the amount of free water consumed per day. Herein we describe the results of our observations.
We measured water consumption by 7 adults, including 3 wild-caught voles (1 male, 2 female) and 4 captive-bred females from 20 April 2008 to 15 July 2010. Voles were individually housed in large (60 x 60 x 120 cm) wire cages in an unheated (ambient outdoor temperature) garage where they could build nests and harvest their own food from fresh branches of Douglasfir that we replaced every 1 to 3 d. Prior to being fed to voles, branches were stored upright in a bucket with the cut ends submerged in water to keep the needles hydrated, but branches were never sprayed with water. Water was provided in each cage in a glass water bottle with an L-shaped glass drinking tube. Water bottles were filled and reweighed to the nearest tenth of a gram at irregular intervals (2 to 26 d), as needed to maintain a continuous supply of water in each cage. In addition to the water bottles in each cage, we used 3 control bottles that we filled and measured on the same schedule as the water bottles in the vole cages. Estimates of evaporative water loss from the controls were used to adjust estimates of water consumed by the voles, assuming similar evaporative loss in control tubes and vole tubes. All tubes were weighed and measured at the same time so that sampling intervals were the same for voles and controls.
We estimated water consumption as the average of the means of all sampling intervals for each vole. All estimates were expressed in milliliters of water consumed per gram of body mass per day (ml/g/d), based on a mean body mass of 27 g for males and 30 g for females. These estimates of mean body mass were based on a sample of museum specimens (Forsman and Swingle unpubl, data), because we did not want to disturb the experimental voles by tearing their nests apart to capture and weigh them. Samples also were subdivided into seasonal periods to test the hypothesis that water consumption did not vary among seasons. Seasonal periods were: spring (March to May), summer (June to August), autumn (September to November), and winter (December to February). None of the voles were allowed to breed during the sampling period, so our results only applied to non-breeders. We used analysis of variance (ANOVA) to compare means. All animal handling procedures met the guidelines recommended by the American Society of Mammalogists Animal Care and Use Committee (Gannon and others 2007), and Oregon State University Animal Care and Use Permit 3091.
The mean sampling period for the 7 voles was 472 [+ or -] 114 d (range 112 to 816 d). The estimated mean water consumption per day was 0.016 [+ or -] 0.001 ml/g/d (Table 1). There was considerable variation among individuals, with 1 individual drinking approximately twice as much water as the others (Table 1; [F.sub.6,378] = 15.259, P < 0.001). Water consumption varied seasonally, primarily because of higher consumption in spring and summer than in autumn and winter (Table 2; [F.sub.3,20] = 5.153, P = 0.008). Although voles did commonly drink small amounts of water, they often went for long periods with little evidence of any free-water consumption (for example, water loss in vole tubes was [less than or equal to] controls). Of the time intervals measured for each vole, the percent of intervals with no water consumption averaged 29 [+ or -] 6% (range 11 to 50%). The mean duration of periods in which there was no measurable water consumption was 22 [+ or -] 3 d (range 1 to 70 d). Water consumption by the only male in our sample fell within the range of values observed for females (Table 1).
Our study indicates that non-breeding Tree Voles drink little free water, and can exist for long periods of time with almost no free water. Based on the average quantities of water consumed, they drank less free water per day than the Mongolian Gerbil (Meriones unguiculatus), a species known for its ability to persist exclusively on metabolic water (Table 3; Winklemann and Getz 1962). Presumably, the low nutrient value and high water content of conifer needles (Beaton and others 1965; Waring and others 1979; Camm 1993; Cross and Perakis 2011) allows Tree Voles to obtain virtually all of their water from their food. Rhodes and Richmond (1982) reached the same conclusion regarding free-ranging Pine Voles (Pitymys pinetorum), and Getz (1968) found that Redbacked Voles (Myodes gapperi) could persist for at least 2 wk on a diet of mushrooms without losing weight and with no access to free water. We suspect that the large amount of free water consumed by most species of voles in captivity (Table 3) is a response to an artificial diet of dry lab chow, oats, or sunflower seeds. Our results presumably explain how Tree Voles can exist in the forest canopy in relatively dry upland habitats where free water is often limited for weeks at a time during late summer. During hot and dry summer weather, Tree Voles also reduce evaporative water loss by remaining in their nests during the day when the ambient humidity is presumably lower than the humidity inside the nest. Our results may also explain why reproduction by Tree Voles declines in late summer, as it probably becomes increasingly difficult for females to maintain lactation during periods when little free water is available and the water content of conifer needles declines. Bradford (1974) suggested a similar response by Pinyon Mice (Peromyscus truei), which typically had reduced body mass and lower reproduction in late summer.
The physiological mechanisms that allow Tree Voles to exist with relatively little free water are unknown, but may include the ability to produce concentrated urine or to vary the amount of water in feces, as has been documented for other rodent species (Bradford 1974; but see Rhodes and Richmond 1982). Our results suggest the need for a more extensive experimental study of water consumption and metabolic rates in Tree Voles, including females with young. Studies of water consumption under controlled conditions of humidity and temperature would almost certainly reveal details we could not evaluate.
We thank J Swingle and N Hatch for helping us capture Tree Voles. Reviews by 2 anonymous reviewers helped to improve the manuscript.
BEATON JD, MOSS A, MACRAE I, KONKIN JW, MCGHEE WPT, KOS1CK R. 1965. Observations on foliage nutrient content of several coniferous tree species in British Columbia. The Forestry Chronicle 41: 222-236.
BRADFORD DF. 1974. Water stress of free-living Peromyscus truei. Ecology 55:1407-1414.
CAMM E. 1993. Photosynthetic responses in developing and year-old Douglas-fir needles during new shoot development. Trees 8:61-66.
CHEW RM. 1951. The water exchanges of some small mammals. Ecological Monographs 21:215-225.
CHURCH RL. 1966. Water exchanges of the California Vole, Microtus californicus. Physiological Zoology 39:326-340.
CROSS A, PERAKIS SS. 2011. Tree species and soil nutrient profiles in old-growth forests of the Oregon Coast Range. Canadian Journal of Forest Research 41:195-210.
GANNON WL, SIKES RS, ANIMAL CARE AND USE COMMITTEE. 2007. Guidelines of the American Society of Mammalogists for the use of wild mammals in research. Journal of Mammalogy 88: 809-823.
GETZ LL. 1963. A comparison of the water balance of the Prairie and Meadow Voles. Ecology 44:202-207.
GETZ LL. 1968. Influence of water balance and microclimate on the local distribution of the Redback Vole and White-footed Mouse. Ecology 49:276-286.
HOWELL AB. 1926. Voles of the genus Phenacomys. North American Fauna 48:1-66.
MASER CO. 1966. Life histories and ecology of Phenacomys albipes, Phenacomys longicaudus, Phenacomys silvicola [thesis]. Corvallis, OR: Oregon State University. 221 p.
MASER C, MATE BR, FRANKLIN JF, DYRNESS CT. 1981. Natural history of Oregon Coast mammals. USDA Forest Service General Technical Report PNW-133. 496 p.
MCMANUS JJ. 1974. Bioenergetics and water requirements of the Redback Vole, Clethrionomys gapperi. Journal of Mammalogy 55:30-44.
PEARSON JP. 1972. The influence of behavior and water requirements on the distribution and habitat selection of the Gray-tailed Vole (Microtus canicaudus) with notes on Microtus townsendii [dissertation]. Corvallis, OR: Oregon State University. 56 p.
RHODES DH, RICHMOND ME. 1981. Water metabolism in the Pine Vole Pitymys pinetorum. Eastern Pine and Meadow Vole Symposia. Lincoln, NB: University of Nebraska. p 127-130. (available online at http://digitalcommons.unl.edu/voles).
RHODES DH, RICHMOND ME. 1982. Water metabolism in laboratory-maintained and free-ranging Pine Voles (Microtus pinetorum). Eastern Pine and Meadow Vole Symposia. Lincoln, NE: University of Nebraska. p 112-116. (available online at http:// digitalcommons.unl.edu/voles).
SWINGLE JK, FORSMAN ED. 2009. Home range areas and activity patterns of Red Tree Voles (Arborimus longicaudus) in western Oregon. Northwest Science 83:273-286
WARING RH, WHITEHEAD D, JARVIS PC. 1979. The contribution of stored water to transpiration in Scots pine. Plant, Cell and Environment 2:309-317.
WINKLEMANN JR, GETZ LL. 1962. Water balance in the Mongolian Gerbil. Journal of Mammalogy 43:150154.
Submitted 10 September 2010, accepted 9 December 2010. Corresponding Editor: Paul Cryan.
ERIC D FORSMAN
USDA Forest Service, Pacific Northwest Research Station, 3200 SW Jefferson Way, Corvallis, OR 97331
AMY L PRICE
Department of Fisheries and Wildlife, Oregon State University, Corvallis, OR 97331
TABLE 1. Consumption of free water by 7 Red Tree Voles (Arborimus longicaudus) maintained in captivity and fed a natural diet of Douglas-fir (Pseudotsuga nienziesii) branches. No. Vole ID Sex Observation period No. days intervals (1) 1 M 2 Nov 2008-15 Jul 2010 621 37 2 F 28 Apr 2008-2 Jul 2010 795 79 3 F 20 Apr 2008-10 Aug 2008 112 33 4 F 20 Apr 2008-2 Dec 2008 226 46 5 F 20 Apr 2008-15 Jul 2010 816 81 6 F 20 Apr 2008-29 Sep 2008 162 42 7 F 20 Apr 2008-15 Nov 2009 574 67 Mean Water consumption (ml/g/d) Vole ID Mean SE Range 1 0.017 0.002 0-0.049 2 0.011 0.002 0-0.066 3 0.039 0.006 0-0.136 4 0.006 0.001 0-0.039 5 0.024 0.003 0-0.108 6 0.016 0.003 0-0.068 7 0.007 0.002 0-0.081 Mean 0.016 0.001 (1) Mean length of sampling intervals was 8.0--0.4 d (range 110 d). TABLE 2. Seasonal variation in consumption of free water by Red Tree Voles (Arborimus longicaudus) maintained in captivity and fed a natural diet of Douglas fir (Pseudotsuga menziesii) branches. Free water consumption ml/g/d Season (1) No. voles Mean SE Range Spring 7 0.027 0.006 0.010-0.059 Summer 7 0.013 0.004 0.004-0.028 Autumn 6 0.006 0.001 0.002-0.010 Winter 4 0.006 0.002 0.000-0.014 (1) Spring--Mar-May, Summer = Jun-Aug, Fall = Sep-Nov, Winter = Dec-Feb. TABLE 3. Published data on mean consumption of free water by selected small mammals. nd = not determined. Source Species n This study Arborimus longicaudus 7 Winkleman and Getz 1962 Meriones unguiculatus 4 Getz 1963 Microtus ochrogaster 27 Church 1966 Microtus californicus 47 Getz 1963 Microtus pennsylvanicus 22 Getz 1968 Clethrionomys gapperi 6 McManus 1974 Clethrionomys gapperi 5 Rhodes and Richmond 1981 Pitymys pinetorutn (2) 10 Rhodes and Richmond 1981 Pitymys pinetortim (3) 10 Free water consumption Source ml/g/d ml/d This study 0.016 [+ or -] 0.01 0.5 Winkleman and Getz 1962 0.039 nd Getz 1963 0.206 6.6 Church 1966 0.246 [+ or -] 0.66 nd Getz 1963 0.282 8.2 Getz 1968 0.315 7.23 McManus 1974 0.679 [+ or -] 0.536 (1) nd Rhodes and Richmond 1981 0.71 14.8 Rhodes and Richmond 1981 0.77 15.5 (1) Mean is the grand mean of 5 groups that were tested at different ambient temperatures. (2) Maintained at 30[degrees]C. (3) Maintained at 15[degrees]C.