(Miller) and Other Woodland Mice Author(S): James E

Home , Canyon mouse, Jaculus (rodent), Pitymys, Woodland jumping mouse

Ecology and Physiology of Napaeozapus Insignis (Miller) and Other Woodland Mice Author(s): James E. Brower and Tom J. Cade Reviewed work(s): Source: Ecology, Vol. 47, No. 1 (Jan., 1966), pp. 46-63 Published by: Ecological Society of America Stable URL: http://www.jstor.org/stable/1935743 . Accessed: 24/12/2011 11:58

Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at . http://www.jstor.org/page/info/about/policies/terms.jsp

JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact [email protected].

Ecological Society of America is collaborating with JSTOR to digitize, preserve and extend access to Ecology.

http://www.jstor.org ECOLOGY AND PHYSIOLOGY OF NAPAEOZAPUS INSIGNIS (MtILLL,"R)AND OTHER WOODLAND MICE J.AMESE. BROWER AND ToM J. CADE Deparhimlcilt of Zoology, Syracuse University, Syracuse, Nczv York

-11bstract. The distribution and ecology of the woodland jumping mouse, Napacoz-aplus uisuipliis, were studied in the light of its behavior in the field, its physiology in the laboratory, and by comparison with other species of small rodents. Data from 36 traplines show that jumping mice have no preference for habitats near water. Shrubby ground cover appears to be the most important factor affecting their local abundance. Napaeozaputs has probably been associated so often with streams because these areas favor growth of good ground cover. Woodlan(1 jumping mice were found in nonwooded areas where shrubby ground cover was found. In one nonwooded area it replaced the meadow jumping mouse, Zapus hudsomins. Removal of the population of woodland jumping mice in the fall was followed by the establishment of the meadow species the next spring. Woodland jumping mice and redback voles seldom occurred together in abundant numbers. This separation was partly the result of distinct habitat differences, but in some areas of mixed woods having ground cover, the presence of voles was accompanied by an absence of jumping mice. When jumping mice were present, redback voles were few or absent. This pattern of distribution could not be explained by differences in habitat selection or by competition. Some form of interference could be involved. Woodland jumping mice show a tendency to be more active on colder nights. This behavior contrasts with o1)servations on deer mice by other workers who state that these mice are more active onI warm, cloudy nights. The high population densities of Napavozaputs found in this study were in an area of New York State having boreal elements. The lower densities reported for western and southern areas of the northeastern United States indicate that its overall distribution is affected by the presence of horeal vegetation. Ad libitiml. water consumption shows that redback voles drink more than twice as much as their predicted weight-relative value. Woodland jumping mice drank normal weight-relative amounts, but deer mice drank less. The rate of evaporation in Napaeozapus was considerably lower than that found in sympatric Peromyscus inaniculatus. Its rate of evaporation was closer to values found for some populations of mice from drier climates. These results suggest that moisture is not a critical limiting factor in the distribution of woodland jumping mice. The low rate of evaporation in Napaeozapus could be an adaptation against desiccation during hibernation. The spreading of saliva by the deer mice is an important cooling device. At 37?C deer mice lost 72% of their heat production through evaporation. At this same ambient temperature, jumping mice lost only 38% of their heat by evaporation. Deer mice were able to withstand 39' with no ill effects, but few jumping mice survived 37?C. Hyperthermia associated with low metabolism was observed in the deer mice. This could be the result of vasoconstriction in nonvital organs, thereby limiting substrates and 09 to the cells of these organs. Such an adjustment would not only limit the rate of metabolism but would also increase the body temperature by limiting transfer of heat by the blood. The decreased metabolic rate and the increased rate of evaporation by spreading saliva would increase the efficiency of cooling at high ambient temperatures. Basal metabolic values of deer mice and jumping mice are near their predicted weight- relative values. The high lower critical temperatures in jumping mice are consistent with the idea that hibernators have high rates of heat loss. Jumping mice appear to have more precise thermoregulation over a wider range of ambient temperatures than do deer mice during the summer period. Metabolic patterns of several small rodents are compared. These patterns show little association with specific climatic conditions among distantly related, sympatric forms. The deer mouse complex, the jumping mice, the voles, and the pocket mice seem to have their own distinctive metabolic and thermoregulatory patterns, which may be associated with phy- logeny. Some physiological adaptation to climate seems to be indicated within these phylogenetic patterns, as exemplified by populations of Peromyscus, while some of the more specialized phylogenetic patterns, such as the one which characterizes the genus Perognathus, seem to have evolved in the ancestral populations to suit specific climatic conditions.

INTRODUCTION which are distributed through the temperate and The woodlandjuumping mouse -Napaeozapus in- boreal regions of the Northern Hemisphere. Only signis (Miller) belongs to a small family of hiber- recently have physiologists (Johansen and Krog nating rodents, the Zapodidae, the members of 1959; Morrison and Ryser 1962a; and Neumann Winter 1966 ECOLOGY AND PHYSIOLOGY OF WOODLAND MICE 47 and Cade 1964) begun to study the members of areas were sampled in the summers of 1961, 1962, this phylogenetically old family, which is repre- and 1963, but the bulk of the data was collected sented by fossil forms possibly as far back as the in 1962. Two types of Sherman live-traps were Eocene (Wood 1955). used, the larger spring-floor box traps and the Napaeozapus is found generally over a wide smaller folding traps. Rolled oats were used in range in northeastern North America from the the small traps and a mixture of peanut butter and limits of the boreal forest in Quebec and Labrador, rolled oats in the larger. Traps were set at the south through the Appalachian system to Georgia, bases of stumps and trees, near logs, holes in the and westward from the Atlantic coast to Minnesota ground, and at any other spots where a small and Saskatchewan (Hall and Kelson 1959). Often mammal might pass. All mice were removed from rare within this range, woodland jumping mice the sites and were not released. We obtained may be quite abundant locally (Sheldon 1934, records from a total of 4,024 trap-nights. Trap- 1938; Hamilton 1935; Preble 1956). E. A. Preble lines were set for 3 to 5 days in one place. Results (1899), Hamilton (1935), N. A. Preble (1956) are expressed in number of mice trapped per 100 and others have emphasized a preference by this trap nights. We designate the animals as 1) species for cool, moist, wooded habitats along abundant if 5 or more; 2) common, if 2.5 to 5; streams or other bodies of water, implying a strong 3) few, if at least 1.0, and 4) rare, if less than 1.0 association with water. Connor (1960) and were caught per 100 trap-nights. Whitaker (1963a), on the other hand, feel that The general habitat of the trapping areas was surface water is not an essential part of the habitat recorded in terms of dominant vegetation, amount for these mice. Snyder (1924) and Whitaker of brushy ground cover, and approximate distance (1963a) believe that ground cover is the most from water. The dominant types of vegetation important component of their habitat. were classified as coniferous woods, deciduous We have tried to gain some insight into the woods, mixed woods, shrub community, or field factors which govern the geographic and ecological community. Cover, in the form of shrubs or small distribution of Napaeozapus by studying its be- trees (up to 6 or 8 feet above the ground) was havior in the field and by examining its metabolic rated as dense (difficult to walk through), inter- and thermoregulatory characteristics in the labo- mediate (vegetation close but easy to maneuver ratory. To assess the distributional significance through), or sparse (little or no shrub-like vege- of our findings on Napaeozapus, we have made tation present). Distance from water was divided extensive comparisons with other species of small into three categories: adjacent to water (less than rodents. 200 ft), close to water (200 to 600 ft), and far from water (estimated greater than 600 ft). All METHODS AND MATERIALS water bodies were streams or brooks. Field study The second portion of the field work entailed Whiteface Mountain, in the northern Adiron- maintaining a grid from August 10, 1962 to Sep- dack Mountains of New York State, was selected tember 13, 1962, on an old, abandoned ski slope, for a field study for several reasons. Preliminary on Marble Mountain at an elevation of 1,900 ft. trapping during the summer of 1961 revealed This area proved almost ideal. It had an abundant jumping mice to be abundant in a number of lo- population of jumping mice, four contrasting but calities. A mountain highway and chair lift made closely situated habitats, was easily accessible, numerous areas accessible. The State University of New York Atmospheric Sciences Research Center located there provided a convenient source for information on weather (1963). The Adirondack region lies in a pocket of the coniferous forest biome. Lower elevations are chiefly a mixture of coniferous and deciduous woods, whereas the higher elevations consist mainly of spruce-fir complexes. Most of the work was done at the lower elevations in the mixed woods. The field study consisted of two parts: (1) trapping in as many areas and habitats as time permitted and (2) selecting an area in which to capture and release jumping mice to study the movements of individuals in detail. Thirty-six FIG. 1. A photograph of the grid study area. 48 JAMES E. BROWER AND TOM J. CADE Ecology, Vol. 47, No. 1 and had been relatively undisturbed by man for L-shaped tubes attached. Animals were given 5 years. The grid area (Figs. 1 and 3) had an distilled water, sunflower seeds, and small amounts old field and shrub community forming a 90-ft of rolled oats. They were kept in 15 X 9 X 9-inch wide middle strip. A small, dense, shrub commu- wire cages. Measurements were made to the near- nity, consisting of smooth alder (Alnus serrulate), est milliliter and were made over periods of 5 to was located in the lower corner of this north-facing 10 days. An extra drinking tube was used to slope. The base of this slope was bordered by measure the rate of evaporation. Light, tempera- bare soil. On both sides of the old ski trail, the ture, and humidity were as stated above. grid extended into woods consisting mostly of Evaporative water loss and metabolism were measured white and gray birch (Betula papyrifera and B. with the Haldane open-system respirometer (Brody populifolia), maple (Acer saccharum), black 1945). Ambient temperature was controlled within spruce (Picea mariana) and hemlock (Tsuga +0.50C by two methods, a constant-temperature water bath or a constant-temperature room. Animals were re- canadensis). At the base of the slope both woods moved from cages and food 4 to 5 hours before measure- were alike, containing a dense ground cover of ments were made. Desiccators, 150 mm in diameter (air striped maple (Acer pennsylvanicum). The woods volume, 2 liters) with paraffin oil in the bottom, were on the east side of the trail had virtually no ground used for respiration chambers. Granular magnesium in the upper portion of the grid, whereas in perchlorate was used as desiccant and sodium hydroxide cover for absorption of carbon dioxide. A constant air flow the woods on the west side, cover was abundant of 400 ml/min was used. The absorbing tubes for water though less so than at the base. The woods and and CO2 were weighed to the nearest 1/10 mg. To cir- grid on the west side were bordered by another cumvent the problem of animal activity, short time periods trail. On the east side of the grid, the nearest of 4 to 6 minutes were used for measurement as recom- ski trail was about 50 ft from the upper east corner. 160 * X.,. I I Forty-eight traps set 30 ft apart formed a pre- NAPAEOZAPUS / After 6 days, it was enlarged to INSIGNIS /7X liminary grid. 140 - 20'C / 72 traps set 30 ft apart so that a larger area could / be covered. Only the larger Sherman box traps were used in the grid. A 30-ft spacing was used 8l20 7 7 in order to sample sufficiently the small commu- 0 10 7~~~~~~~~~~~~~~~~~~~~~~017 2 22 2 nities composing this area. Animals were toe- 07. clipped for identification and released at the site ~100 7 .7 o of capture. Activity was measured in terms of catches and is expressed as the percentage of total resident captures and recaptures. A mouse was classified as a resident after three captures in different traps. WEIGHT IN GRAMS Criticisms of trapping methods used in studying * I ' lo ' small mammal populations are too numerous to 01 be discussed here. It is sufficient to say that our 80 - PEROMYSCUSMANICULATUS /- trapline data are a coarse index of populations. 300C o Stickel (194&, 1954) recommends the use of capture-release grid techniques. These could not be used for extensive sampling because of time limitations. An index of relative abundance given by data was useful for an evaluation of trap-night - habitats, while the grid capture-release technique 60 1 12 permitted us to obtain more quantitative data in one optimum area within the limitations of trapping. Physiological study Mice used in physiological experiments were 20WIGH IN GRAM trapped at Whiteface Mountain in June and August of 1963. They were kept at about 230C FIG. 2. The relationship of metabolism to body weight and 50-60% relative humidity with 12 hr of light on a double logarithm scale showing the method of ana- lyzing data for Peromyscus maniculatus and Napaeozapus and 12 hr of dark. Water consumption was mea- insignia. The solid line is a regression line with a slope sured using either L-shaped, graduated drinking of 0.7; dotted lines bound approximately 80% of the tubes or 100-ml graduated cylinders inverted with values. Open circles represent discarded values. Winter 1966 ECOLOGY AND PHYSIOLOGY OF WOODLAND MICE 49 mended by Pearson (1962); however, to lessen weighing paeozapus was common to abundant, averaging errors, longer periods of 8 to 12 minutes were used when 8.4 per 100 trap-nights. the animal remained quiet. At the conclusion of the ex- periment, deep rectal temperatures were taken when pos- In 13 areas of intermediate cover, populations sible using a Yellow Springs telethermometer and ther- were variable. Eight traplines gave 5 mice from mistor probe. Temperatures were estimated to the nearest 956 trap-nights or 0.5 per 100 trap-nights. Five 1/10C. The use of a water bath for most of the experi- of these 13 areas, on the other hand, had common ments on jumping mice prevented temperature measure- to abundant numbers, averaging 5.3 per 100( ments after these runs. trap- Two methods were used to compute metabolic values. nights. Fifteen sparsely covered areas were less The minimum value of a series of runs on one animal was variable. Twelve of the 15 areas gave only 3 mice considered as standard. This selection, however, does not from 1,408 trap-nights (0.21 per 100 trap-night), eliminate a number of possible experimental errors, such whereas 3 areas produced 28 per 283 trap-nights as unnoticed activity, weighing errors resulting from short runs, CO2 washout, and weight bias caused by fat animals. (7.2 per 100 trap-nights). One of these three Minimum CO2 values were then plotted against weight areas was near a dump providing an unusual and on double logarithmic paper (Fig. 2). Since metabolism abundant source of food. A second was along a is proportional to weight (W) to a power (b), M = kWb woodland stream adjacent to cover, but a third (Brody 1945; Kleiber 1961), an arbitrary line with a area lacked cover or any other obvious reason for slope of 0.7 was drawn by inspection to fit the points. The value 0.7 is recommended by Brody (1945). Parallel this abundance. lines were then drawn equidistant from this line to include Jumping mice showed no association with spe- approximately four-fifths of the values. Values outside cific kinds of woody plant cover. They were these lines were discarded. Only minimal weights of trapped equally in stands of yew (Taxus canaden- water loss from a series of runs on one animal were selected for use. sis), hobble bush (Viburnum alnifolium), birch Oxygen consumption was measured with a closed-system saplings (Betula sp.), mountain and striped maple "minute oxygen uptake spirometer" (Aloe Scientific (Acer pennsylvanicum and A. spicaturn), and Co.). RQ was calculated as 0.68 for Napaeozapus, but smooth alder (Alnus an RQ of 0.7 was used in computations. An RQ of 0.7 serrulata). applied to our CO2 data gave values 02 for P. maniculatus Table I shows the abundance of Clethrionomys in rela- quite similar to those determined for this species by tion to ground cover, vegetation type, and water. Red- McNab and Morrison (1963), who measured oxygen up- back voles showed no special association with dense take in a closed system. shrubby cover when the three cover types are compared. The species was, however, abundant in 1 of the 9 areas of dense cover, where 7 voles were taken in 72 trap-nights, RESULTS or 9.7 per 100 trap-nights. This one area contained Field study mixed woods. The other 8 areas of dense cover averaged only 0.9 voles per 100 trap-nights (8 per 869 trap-nights). Data from 36 traplines emphasize 2 points about Thirty-eight voles were taken from 697 trap-nights (5.2 the habitats utilized by jumping mice at Whiteface per 100 trap-nights) in 7 areas of coniferous woods and Mountain. First, there was no special association 50 voles, from 2,131 trap-nights (2.4 per 100 trap-nights) in mixed woods. These catches reflect the association of with habitats adjacent or close to water. Napaeo- redback voles with boreal elements. Although voles were zapus was found equally abundantly far from almost common in mixed woods, they were only common streams as near (Table I). Second, jumping mice to abundant in 6 of 18 areas. Jumping mice, on the other were trapped most frequently in areas with sub- hand, were rare in coniferous woods (0.7 per 100 trap- nights), but since only one area had sufficient shrubby stantial ground cover. In all 8 areas of dense cover, the relative use of coniferous areas by these mice shrubs or stands of sapling and small trees, Na- cannot be estimated.

TABLE I. The abundance of woodland mice in relation to various components of habitat

Number of mice per 100 trap-nights Total Number number of Napaeozapus Peromyscus Clethrionomys Components of areas trap-nights insignia maniculatus gapperi Total Adjacent to water 9 1182 3.6 3.8 1.4 8.8 Close to water .9 9 823 3.6 1.8 2.8 8.2 Far from water. 18 2019 3.2 2.4 2.6 8.2 Dense cover ...... 8 941 8.4 3.4 1.6 13.4 Intermediate cover . . 1 . ...13 1292 2.2 2.11 2.8 7.1 Sparse cover .15 1791 1.7 2.9 2.2 6.8 Coniferous woods 7 697 0.7 3.5 5.2 9.4 Mixed woods ...... 18 2131 5.0 3.7 2.4 11.1 Open shrub.3 3 290 7.9 0.7 0.3 8.9 Field ...... 6 556 0.4 1.1 0.2 1.7 50 JAMES E. BROWER AND TOM J. CADE Ecology, Vol. 47, No. 1

TABLE II. The distribution of activity by mice on a 1.5-acre plot

Percentage of total captures Total Number of number of Dense to Species resident resident West side intermediate Woods mice captures of plot ground cover Napaeozapus insignia...... 12 70 87 94 44 Peromyscus maniculatus.8 39 61 64 70 Clethrionomysgapperi .8 41 41 90 85

The relative abundance of deer mice was not clearly associated with any of the observed parameters of habitat (Table I). They were most common in mixed woods where, on 10 of the 18 traplines, they were common to WV '~ ~~~~VV abundant. Deer mice did not average abundant in any of the habitat groupings. They were abundant on 6 of the total of 36 traplines, and common on 8. Deer mice showed no particular avoidance of or preference for areas occupied by jumping mice or redback voles. In the 13 areas of intermediate cover, the absence of Napaeozapus seemed to be complemented by the presence of Clethrionomys gapperi and vice versa. In eight of these areas, jumping mice were scarce, and in five of these eight areas, redback voles were common to abundant. On these traplines, the voles also outnumbered the deer mice. E + W Two of these five areas populated by voles were coniferous SCALE0 FL woods. In the three areas of intermediate cover where H~~~~~~ jumping mice were abundant, redback voles were rare or absent. Jumping mice were abundant, but the voles un- common, in three areas of sparsely covered woods. In FIG. 3. A map of the grid study area showing captures one sparsely covered nonconiferous habitat where the voles of resident mice. Dashed line is the grid outline (270 were abundant, no jumping mice were present. On 10 X 240 ft) ; slanted lines represent open woods; crossed traplines in mixed woods, there was no difference in com- lines represent woods with abundant to dense under- position of local habitats which could explain why the growth; vertical lines represent an alder patch; stippling voles were found in good numbers in four areas, but were is bare soil; three dark, radiating lines represent bushes; scarce in another six. five light, radiating lines represent grasses and composites. Grid trapping for one month revealed patterns similar Each circle, triangle or X represents a single capture of to those noticed in the trapline data. Table II shows the N. insignis, P. aniculatus, or C. gapperi respectively. importance of cover. Ninety-four per cent of 70 catches The compass orientation is as in Fig. 1. of 12 resident jumping mice and 64% of 47 transients were associated with ground cover. Preference for woods was less than for cover. Only 44% of the resident catches rodents. Deer mice showed about equal activity on either were in the woods, whereas 56% were on the old ski side. slope. Traplines were set 150 to 200 ft to the east and west As in the trapline data, redback voles tended to show sides of the grid to determine the small mammals present. a complementary pattern on the grid. Table II and Both areas had a little mountain maple cover. Twenty- Figure 3 show greater activity by jumping mice on the five traps were set in the eastern line for three nights, west side of the grid, even though woodland cover was catching five redback voles, one deer mouse, one chip- the same on the lower east side as in the woods on the munk(Talias striates), and no jumping mice. The west west. Of the total catches, 87% were on the west side line consisted of 20 traps set for 3 nights. The west woods (the middle row of traps is included in the west side). was a thin strip 60 to 100 ft wide. A ski slope separated these Greater activity by the voles was observed on the east woods from the woods in the grid. Two jumping mice, one and three deer mice side where 6 of the 8 resident voles were trapped 24 of vole, were trapped. The ski to be 30 times (71%). Most of the vole activity noticed on slope appeared good habitat for the meadow jumping mouse but the west side was produced by only 2 animals which were (Zapus hudsonius), only two were trapped on the plot during the caught on that side 10 of 11 times. Six of eight transient August-September period of trapping; one was trapped once and the other voles were trapped on the east side. Resident and non- three times. No catches were made in te alders or woods. resident voles were fairly restricted to woods with cover. On June 2 and3o 1963, 24 traps were set at the grid sta- Deer mice showed less avoidance of the sparsely covered tions in the lower west quarter of the plot. Nine Zapus woods and the area of high vole activity than did jumping wese woods fo the alders and surrounding bushes, but mice. They were more strongly associated with the woods only four vapaeolapes, in the woods and alders. All mice than jumping mice, but were less restricted to the woods captured the previous year (1962) on September 12 and than the voles. Fewer catches of deer mice were asso- 13 were removed, including 14 Napaeozapus. ciated with ground cover than of either of the other two The meadow vole (Microtus pennsylvanicus) was Winter 1966 ECOLOGY AND PHYSIOLOGY OF WOODLAND MICE 51 2.2 times the predicted weight-relative value. ' Jumping mice drank near the predicted amount, 'JBo /r*?'-*%% O % %% p0 and deer mice drank less than the predicted 60 ~ . 0 I i IIV I I I amount. Jumping mice, redback voles, and deer ~40 mice were trapped commonly in what appeared to the eye to be moist habitats. These three moist- '-.- 4 0* - forest inhabitants were at times syntopic. 2 20 Evaporative water losses are shown for Pero- myscus and Napcaeozapmsin Figure 5. Deer mice at 250C and above had higher evaporative losses W0.4 less water Z , I I m II than jumping mice. They evaporated Cr!0.2 than the jumping mice at 20'C, but at 10'C both species evaporated about the same amount. Be- 14 16 18 20 27 29 31 3 5 7 10 la tween TA 200 and 31'C, jumping mice showed a AUGUST1962 SEPTEMBER1962 slight but significant decrease in evaporation. At FIG. 4. The relation of jumping mouse activity on the grid to weather conditions. Dashed line on the tempera- 350C deer mice began to salivate and spread the ture scale represents the maximum daily temperature; saliva over their fur. Evaporative loss increased solid line is the minimum daily temperature; plain bars sharply at this point. Deer mice evaporated 1.7 represent precipitation records from the base of the moun- times more than jumping mice at 350 and 370C. tain; solid bars represent precipitation records from the summit. The center chart represents catches of jumping Jumping mice evaporated almost the same amount mice. of water at 370C as deer mice did at 350C. plentiful in 1962. Five of these voles were captured 3 or more times, 2 twice, and 13 only once. There was a 40 - PEROMYSCUS MANICULATUS high mortality of Microtus in the traps, since they were checked only once a day. These voles were trapped in 30 _ equal numbers on the open slope and in berry patches. Microtus and Clethrionomys had distinct areas of activity with little overlap. There was some spatial overlap among x 20 4 individuals of Napaeozapus and Microtus. Three times during the 1962 trapping, two jumping mice were found together in the same trap. Twice deer mice 10 16 8 79 10 ] were found in pairs, and once a deer mouse and a jumping mouse were found together. No such incidents occurred with redback voles. NAPAEOZAPUS INSIGNIS Figure 4 compares temperature and precipitation with the catches of jumping mice on the grid. Often when 1 nights were warm, catches were low. The three highest 15 + 13 7 1l 5 catches were on cool nights. There seemed to be no clear effect of rain or wind on the activity of jumping mice. l10 20 30 40 Data are too few to show any trends with the other spe- AMBIENTTEMPERATURE *C cies of mice. FIG. 5. Evaporative loss in Napaeozapus insignis and Peromyscus maniculatus in relation to ambient tempera- Physiological study ture. The horizontal lines represent mean values, vertical Table III compares ad libitum drinking of 7 lines, the ranges and the open rectangles, +2 standard redback voles, 8 deer mice, and 10 jumping mice. errors. Numbers represent the sample size. Water vapor in the animal chamber ranged from 3.5 mg/liter air at TA The mean consumption for the jumping mice was 100C to 5.7 mg/liter air at TA 370C for Napaeozapus and almost twice that of the deer mice. Redback voles 6.7 mg/liter air at 100C to 23 mg/liter air at 390C for drank 2.4 times as much as jumping mice and Peromyscus.

TABLE III. Ad libitumn water consumption of Clethriornomys gapperi, Napaeozapus insignis, and Peromyscus maniculatus. Each value is the mean of 5- to 10-day measurements at 230C and relative humidity of 50 to 60%

Weight (g) ml H20/g day Predicted Species N Avg 2 SE Avg Range 2 SE weight-relative, H20 consumption

C. gapper .7 23.9 2.3 0.38 0.35-0.39 0.01 0.16 N. insign.s. 10 20.9 1.5 0.16 0.09-0.24 0.03 0.17 P. maniculatus ...... 8| 17.9 1.5 0.08 0.04-0.12 0.02 0.17

a(mlH20/g day) = 0.24W(g) -0. 12, fromHudson (1962) modified from Adolph (1949). 52 JAMES E. BROWER AND TOM J. CADE Ecology, Vol. 47, No. 1 Jumping mice showed signs of heat stress at Figures 6 and 7 compare body temperatures ot 370C but were not observed spreading saliva. The Napaeozapus and Peromyscus after 2 to 3 hours' more active mice showed more pronounced signs exposure at a given TA. The samples of tempera- of stress. Their eyes bulged, appendages were ture taken between 5 and 33.5?C show precise extended, and breathing was rapid as they lay thermal regulation in woodland jumping mice. sprawled on their bellies. One Animalvibrated its The deep body temperature of these mice did not sparsely haired tail rapidly in the air. This mouse deviate significantly from 370C. Deer mice had was removed after a 2-hour exposure at 370C to labile body temperatures, which were lower at prevent death but was found dead in its cage the 10'C and higher at 33.50C than those of jumping next morning. Two died during the experiments, mice. An approximate TB of 370C was recorded and within 1 week after these experiments at 370 C, at TA 25 and 300C. A rise in TB began above only 4 of the 12 mice tested remained alive. No TA 30'C in Peromyscus but not until 33.50C in experiments were made on jumping mice at 390C. Napaeozapus. Deer mice showed different responses at higher Figures 8 and 9 illustrate the effect of TA on ambient temperatures. Aside from higher water metabolism. The thermal neutral zones of the losses, they tolerated 390C with no ill effects. At 39?C deer mice were practically soaked from PEROMYSCUSMANICULATUS spreading saliva, and evaporated 2.9 times more \ CALCULATED02 CONSUMPTION water than at 370C. The white portion of the tail CoD PRODUCTION 6C FOR 10'-29C Ma6.-0.165T appeared pink. On two occasions, high mortality was noted in Microtus, Clethrionomys, Zapus, and Napaeozapus when they were accidentally exposed to heat; however, Peromyscus showed no ill effects 04- on these same occasions. 41 2

40- NAPAEOZAPUSINSIGNIS V 39 6 O10 20 30 40 38- AMBIENT TEMPERATURE*C 1I FIG. 8. The relationship between metabolism and ambient temperaturein N. insignis. The' dark solid regres- 34 4 7 sion line is computed using CO2 values from 10 to 30'C. Least squares equation, M = 5.8 - 0.14T; the light solid regression line was computed using CO2 values from 20 35- to 300C. Least squares equation, M = 6.8 - 0.18T; X = measured 02 consumption; dashed line is 02 con- 34. sumption calculated from the light line assuming an RQ 0 10 20 30 40 of 0.7. Sample size under each symbol. Other symbols AMBIENT TEMPERATURE'C as in Figure 5. FIG. 6. Body temperaturesof Napaeozapus insignia in relation to ambient temperature. Symbols as in Figure 8 5. Sample size is under symbols. NAPAEOZAPUSINSIGNIS -- CALCULATED02 CONSUMPTION 41 CO2. PRODUCTION - FOR 200-300C Ms 6.79 0.179 T \- CO2 PRODUCTION 40 PEROMYSCUS MANICULATUS FOR 10 - 30*C M. 5.78-0.141T

8'939 9 ~4. ! 38 -

37 - 14/

FIG36 Bd 7 2~~~~~~~~~~~~~~~~~~~1 I0 35- 13 0 o 10 20 30 40 34 II 0 tO 20 30 4 AMBIENT TEMPERATURE*C AMBIENTTEMPERATURE "C FIG. 9. The relationship between metabolism and am- FIG. 7. Body temperature of Peromyscus maniculatus bient temperature in P. maniculatus. Legend as in Figure in relation to ambient temperature. Symbols as in Figure 8. Least squares regression from 10 to 290C, M = 6.0 5. Sample size is under symbols. - 0.17T. Winter 1966 ECOLOGY AND PHYSIOLOGY OF WOODLAND MICE 53 two species were different. Under our conditions, of water, mentioned by many writers, becomes Peromyscus had an 80 zone (29 to 370C), whereas clearer when good accounts of vegetation are given. Napaeozapus had a 2.50 zone (31 to 33.50C). In such accounts (Hamilton 1935; Jameson Basal metabolism for both species was about the 1949; Preble 1956), undergrowth was present and same as that predicted by the equation M - usually abundant. Napaeozapus has probably been 3.8W-0.27 (Morrison, Ryser and Dawe 1959). associated so often with streams because they The average minimum metabolism for 11 jumping favor the growth of shrubby cover. mice at TA 310C (avg wt - 21.6 g, RQ of 0.7) Our results indicate that the species of woody was 1.8 cc O2/g hr (1.3 cc C02/g hr). Minimum plant cover is unimportant. Connor (1960) and metabolism for seven deer mice at TA 290C (avg Whitaker (1963a) found jumping mice in a variety wt 17.0 g) was 1.8 cc 02/g hr (1.3 cc C02/g hr). of vegetation types, and Townsend (1935) and Although metabolic rate was not constant for deer Connor (1960) have trapped them outside wooded mice between 290 and 370C, no sharp rise in their habitats. Most reports have attributed catches metabolism occurred. outside wooded areas to occasional wanderings. Thermal conductance can be calculated from At Marble Mountain, 56% of the resident catches the formula M - C(TB- TA), where M equals of Napaeozapus were on the abandoned ski slope. the metabolism at ambient temperature TA; TB is This figure is too large to be attributed to occa- body temperature, and C is the cooling constant sional wanderings, even though all catches were or thermal conductance. Between 20 and 300C, taken within 45 ft of the woods (Fig. 3). Only thermal conductance in jumping mice was 0.27 cc 3 of the 70 resident catches were made in open O2/g hr 'C. The deer mice, by comparison, had field, and 2 of these were on the border of the a value of 0.23 cc O2/g hr 'C. At 100C, metabo- woods. Thirty-six of the captures on the ski lism of jumping mice was lower than predicted slope were in dense or intermediate shrubby cover. from thermal conductance. If one were to include In another alder patch which lies in the fork of this value in the calculation of the regression line, 2 roads, 9 woodland jumping mice were taken this line would extrapolate to TA 40.60C (Fig. 8). from 30 trap-nights. In the woods on one side When these values at 10?C are excluded, the line of the fork, the mice were rare; on the other side extrapolates to 36.60C, as does the regression line they were few. Three Zapus were also caught in for deer mice. The extrapolation to this tempera- these alders. It therefore seems that in nonwooded ture, which is fairly close to the body temperatures areas, populations of Napaeozapus are found, not of these mice, is in agreement with Newton's law because of proximity to woods, but because of of cooling as applied to homeotherms. abundant shrub cover. These findings support Townsend's idea (1935) that Napaeozapus is a DISCUSSION "forest-edge" species. hudsonius has different habitat associa- Utilization of habitat Zaputs tions which are discussed by Sheldon (1934), There are many conflicting statements about the Hamilton (1935), Quimby (1951), Getz (1961a), habitats utilized by jumping mice. In a large and Whitaker (1963b). Getz, Quimby, and Ham- number of reports, woodland jumping mice are ilton felt that water is significant in the distribution said to prefer cool, moist woods along mountain of Zapus. Whitaker (1963b) concluded that her- streams (Preble 1899; Miller 1899; Hamilton baceous cover is preferred, with water as a factor 1935; Osgood 1938; Preble 1956). Snyder affecting vegetation. Overlap of Zapus and Na- (1924) stated that undergrowth was essential for paeozapus has been reported (Hamilton 1935; Napaeozapus. Whitaker (1963a) concluded that Townsend 1935; Connor 1960). Only two areas herbaceous cover is preferred. Townsend (1935) of overlap were observed at Whiteface Mountain. found a preference for "low, moist woods" in Habitat moisture, cover, and food preferences of central New York and stated that Napaeozapus the two species are similar, but their occupancy is a "forest-edge" mammal. Connor (1960) found of habitats is different. At Whiteface Mountain, that Napaeozapus in a variety of areas preferred field communities, with substantial shrubby cover cool hardwoods and hemlock woods. In his study, located at the margins of forests, allow opportuni- most areas supporting Napaeozapus had a ground ties for the ranges of the two species to overlap. cover of ferns and sedges. Connor (1960) and Whitaker (1963a) found no preference for habi- Competition tats near water. Our results, unlike Connor's and Peromyscus maniculatus did not complement Whitaker's, indicate low, woody undergrowth to either Clethrionomys or Napaeozapus in habitats be important, but we agree that there is a lack around Whiteface Mountain. Manville (1949), of close association with water. The significance however, observed a complementary pattern be- 54 JAMES E. BROWER AND TOM J. CADE Ecology, Vol. 47, No. 1 tween Peromyscus maniculatus and Clethrionomys Overlapping ranges between individuals of gacpperiin northern Michigan. To our knowledge, Zapus and Napaeozapus have already been men- no writer has called attention to a complementary tioned. Whitaker (1963b) claims that the species pattern between Napaeozapus and Clethrionomys, are ecologically isolated and that they therefore but a number of papers bear indications of it. cannot compete. He found that the absence of Hamilton (1935), in one area of central New York, Napaeozapms in the woods did not lead to an caught 51 woodland jumping mice but only 2 red- establishment of Zcapus, and Napcaeozapus was back voles. Townsend (1935) found Napaeo- not present in the fields in the absence of Zapuss. zapus common in two areas in central New York, Townsend (1935) speculated that Napaeozapus but a scarcity of Clethrionomys. In the one area may tend to drive Zapus out from an area where where he found Clethrionomys abundant, Napaeo- the latter could have been present. Hamilton zapus was rare. Blair (1941) captured 52 wood- (1935) and Preble (1956) stated that Zapus is land jumping mice and only 9 redback voles in found in Napaeozapus territory but never the re- 28 days of trapping in northern Michigan. Man- verse. Connor (1960) found 10 Napaeozapus and ville (1949) found these voles common in northern 5 Zapus in Zapus-type territory, but in another Michigan, but captured only two woodland jump- similar habitat he trapped 14 Zapus and no Na- ing mice in three years of trapping. Jameson paeozapus. Our findings resemble Connor's. (1949) found Clethrionomys in fair numbers in From the actual replacement of Napaeozapus by two areas of central New York but seldom caught Zapus in the grid area after the former was re- Napaeozapus. Three other areas yielded good moved, it appears that they are not as ecologically numbers of jumping mice with redback voles taken isolated as Whitaker feels. We agree that these in fewer numbers. two species at present have little overall influence Distinct habitat associations undoubtedly play on their respective distributions, but this conclu- an important role in this complementary pattern. sion probably does not apply in local fringe areas At Whiteface Mountain, the preference of Napaeo- where good shrubby cover extends into field habi- zapus for dense woody undergrowth is contrasted tats. In these areas, competition may well play a by a lack of such preference in Clethrionomys. role in their local distribution. The abundance of Clethrionomys on sparsely covered floors of coniferous woods contrasts with A bundance the absence of Napaeozapus in such areas (Table The density of Napaeozapus on Whiteface I). It is in the mixed forest-edge communities Mountain during our study was high by compari- with abundant to sparse ground cover, where both son with other areas which have been studied. species may occur, that this complementary dis- In 3 of Whitaker's (1963a) study areas which tribution appears to be unexplained in terms of contained Napaeozapus in any numbers, 23 mice differences in utilization of habitat. were taken from 11,166 trap-nights (0.21 per 100 The complementary pattern of these two species trap-nights). Its local abundance in the Adiron- in mixed forest-edge habitats may be explained dack Mountains has been reported previously by by contrasting their behavioral characteristics. Merriam (1884), Miller (1899), and Harper Clethrionomys is aggressive, nervous, and gen- (1929). Napaeozapus was found to be abundant erally intolerant of other individual mice (Hatt in the Presidential Range of New Hampshire 1930; Manville 1949; and personal observation). (Preble 1956), not very abundant in east central In captivity we have often observed them fighting New York (Connor 1960), not numerous in cen- among themselves. Redback voles do not form tral New York (Townsend 1935; Jameson 1949), colonies and are not gregarious (Jackson 1961). and locally abundant in one area of central New Jumping mice are docile, but nervous, and they York (Hamilton 1935). Blair (1941) trapped a retreat with leaps and bounds from threatening local population of 52 in northern Michigan over situations (Snyder 1924; Sheldon 1934; and per- a period of 28 days on an 18.5-acre plot (2.7 mice sonal observation). These behavioral differences per acre), but only 32 of these were caught 5 or could conceivably restrict jumping mice from areas more times. Burt (1946) calculated a fall popula- occupied by voles but not the converse. This hy- tion of three per acre in northern Michigan, while pothesis appears to be consistent with the pattern Manville (1949) found 0.26 per acre in northern found in nature. The kind of interaction existing Michigan. In our study 59 woodland jumping between these two species may be of the disruptive mice were trapped on a 1.5-acre plot in 1 month, sort rather than direct competition for resources averaging 39 per acre; however, only 12 mice were in short supply. Therefore, competition in the trapped 3 or more times, and only 8 residents were strict sense (Birch 1957; Milne 1961) may not be taken during a particular trapping period. On involved. the basis of the latter, we calculate 5.2 resident Winter 1966 ECOLOGY AND PHYSIOLOGY OF WOODLAND MICE 55 woodland jumping mice per acre. This population rowiez (1960) found rain to be the strongest factor level was remarkably high and constant during the affecting rodent activity in Poland. Moderate 4 weeks of trapping. This high density of jumping temperatures favored his catches. mice was undoubtedly affected by the abundance Hamilton (1935) caught more woodland jump- on the plot of raspberries, blackberries, alder fruits, ing mice on cold (380 to 40'F), disagreeable and birch seeds. nights than on warm nights. Likewise, our study According to Miller (1899), farming practices indicates reduced jumping mouse catches on warm seem to have restricted the range of Napaeozapus nights with the highest totals on cold nights. Cloud while enlarging that of Zapus. The relatively low cover or rain seemed to have no effect on Napaeo- catches in central New York, which is largely zapus. Whitaker (1963b) found no effect of rain agricultural, contrast with its abundance in the on Zapus hudsonius activity. Only one instance wilder Adirondacks; however, the favoring of of a decreased catch of woodland jumping mice on boreal elements by Napaeozapus is probably more a clear night at full moon was noted; this night was important in restricting its overall distribution than also warm. If Napaeozapus is more active on cold farming practices, as suggested by Miller (1899). nights, and if Peromyscus, as some writers have Altitude may affect the southern distribution of indicated, is more active on warm, cloudy nights, Napaeozapus because of its influence on vegetation. then one can better understand how they inhabit The westward distribution of this genus is limited the same areas while eating similar food. The by the prairie. behavioral response of a species to weather is an important aspect of the animals' niche and is often Weather overlooked. Surprisingly few studies have been made on the There are, then, a number of complex ecological effects of weather on small mammal activity. A relationships affecting the distributional pattern of few of the more recent works include Gentry and Napaeozapus. Foremost, its overall distribution Odum (1957), Sidorowiez (1960), and Getz is limited to northeastern North America and is (1961b). The relation between weather and associated with boreal elements. Hibernation, an activity of small mammals depends on the season aspect of its niche, is very important to its survival and species. Gentry and Odum (1957) observed in a cool climate. With a low reproductive poten- that in winter, individuals of Peromyscus poliono- tial, this mouse would probably be at an ecological tus were more active on warm, cloudy nights than disadvantage in a warmer climate. At Whiteface on cool, clear nights. Summer-caught individuals Mountain at least, its local distribution and abun- of P. maniculatus behave in a similar manner (Hat- dance appear affected by the density of shrubby field 1938). Tappe (1941), Pruitt (1959), and cover, abundance of food (especially seeds and Blair (1951) have shown that moonlight reduces fruits), interaction with redback voles, and pos- the activity of various nocturnal rodents. Sido- sibly by competition with Zapus. Specific vegeta-

TABLE IV. A comparison of ad libitum water consumptiDn in small rodents

Measured Predicted Ratio of ml H20/ ml H20/ measured Species Number TACC Weight g daya g daya to Authority predicted

Napaeozapus insignia 10 23 20.9 0.157 0.167 0.94 This study Clethrionomysgapperi 7 23 23.9 0.375 0.168 2.2 This study Clethrionomysgapperi 5 25 0.399 Getz (1962) Microtus pennsylvanicus 22 25 29.0 0.282 0.160 1.8 Getz (1963) Microtus pennsylvanicus 6 20-25 34.7 0.209 0.157 1.3 Lindeborg (1952) Microtus ochrogaster 27 25 32.0 0.206 0.158 1 .3 Getz (1963) Peromyscus maniculatus osgoodi 26 17-23 21.0 0.16 0.167 0.97 Williams (1949b) Peromyscus maniculatus bairdii 60 20-25 18.5 0.155 0.169 0.92 Lindeborgb (1952) Peromyscus maniculatus gracilis 20 20-25 21.0 0.099 0.167 0.59 Lindeborgb (1952) Peromyscus maniculatus gracilis 8 23 17.9 0.079 0.170 0.47 This study Peromyscus leucopus noveboracensis 40 20-25 21.5 0.116 0.167 0.70 Lindeborgb (1952) Peromyscus leucopus tornillo 40 20-25 29.4 0.064 0.160 0.40 Lindeborgb (1952)

aI=0.24W -0.12, Hudson(1962), modified from Adolph (1949). bAveragescomputed from data. 56 JAMES E. BROWER AND TOM J. CADE Ecology, Vol. 47, No. 1 tional types and surface water have no direct woods, the jumping mice showed no significant bearing on its local distribution. In summer it increase in ad libitum water consumption over the appears to be most active on cool nights. predicted weight-relative value (Table III). On the other hand, Clethrionomys showed a greater Water consumption water consumption than predicted. Our values Ad libitum water consumption has been used to for redback voles are nearly the same as Getz's relate animal distribution to environmental mois- (1962). He found that high consumption is re- ture (Odum 1944; Lindeborg 1952). Lindeborg lated to a high urine output. We did not measure (1952), Hudson (1962), and Lee (1963) caution urine output for jumping mice, but when litter against using this method alone to indicate adapta- in the cages was changed, it was obvious from the tion to specific habitats. Since no measurements degree of wetting that jumping mice had a lower of the minimum requirements for water were made, urine output than redback voles. By this criterion, we can only make indirect statements relating the deer mice showed a generally lower urine output water economy of Napaceozapusto its habitat. than jumping mice. In spite of their association with cool, moist Ad libitum water consumption in P. manicu-

TABLE V. A comparison of evaporative water loss in various small rodents

Air flow Average Water Water Water Water rate weight loss loss loss loss Species Number TA?C (ml/min) (g) (mg/hr) (mg/g/lir) (mg/cm3 hra) (mg/ml 02 hr) Authority

Microtus pennsylvanicus 5 28 250 2.1 Getz (1963) Clethrionomysgapperi 1 28 250 2.0 Getz (1962) 1 25 250 2.1 Microtus ochrogaster 5 28 250 1.5 Getz ( 963) 5 28 60-250 42.6 120 2.9 1.4 Chew (1951)

5 28 20.6 140 6.9 2.1 Chew Peromyscus leucopus 60-250 (1951) noesboracensis 5 25 120 Lindeborg (1955)

Peromyscus leucopus 14 25 29.3 97 3.3 1.1 Lindeborg (1955) tornillo

Peromyscus maniculatus 7 29 400 17.0 85 5.2 1.4 2.47 This study gracilis 8 25 400 15.9 95 6.1 1.7 2.34

Peromyscus maniculatus 9-11 27 500 17.2 69 4.0 1.2 0.91 Chew (1955) sonoriensis

Peromyscus crinitus 2 28 300 22.0 34 1.6 0.48 0.54 Schmidt- N e!,ens (1950)

Napaeozapus insignia 7 29 400 20.8 65 3.2 0.95 1.45 This study 13 25 400 24.9 79 4.2 1.1 1.31

Perognathus penicillatus 2 29 400 17.7 29 1.6 0.48 0.88 Brower and Cade 4 25 400 14.9 28 1.9 0.51 0.66 (unpublished) 14 25 ? 17.4 33 1.9 0.56 1 Lindeborg (1955)

Perognathus baileyi 6 28 300 25.2 40 1.6 0.52 0.50 Schmidt- Nielsens (1950)

Dipodomys meriami 18 28 300 36.1 44 0.44 0.54 Schmidt- Nielsens (1950)

Dipodomysspectabilis 7 28 300 100.1 80 0.8 0.41 0.57 Schmidt- Nielsens (1950)

Cricetus aureus 10 28 300 95.1 95 1.0 0.51 0.59 Schmidt- (Mesocricetusauratus) Nielsens(1950)

MuS musculus 3 28 300 27.3 58 2.1 0.64 0.59 Schmidt- (wild) Nielsens (1950)

Mus muscusus 5 28 300 29.2 90 3.1 1.05 0.85 Schmidt- (albino) Nielsens (1950)

Rattusnorregicus 12 28 300 102.0 186 1.8 0.96 0.94 Schmidt- (albino) (1950) INielsens

aS = 7W2/3 for voles (Pearson 1947) S = 9W2/3 for other species (Chew 1951) Winter 1966 ECOLOGY AND PHYSIOLOGY OF WOODLAND MICE 57 latus gracilis was considerably lower than the free water nor atmospheric moisture are impor- predicted weight-relative value and lower than in tant in directly controlling the present-day distri- other subspecies (Table IV). Lindeborg's (1952) bution of Napaeozapus during its active phase of values for field-caught P. m. gracilis are not sig- life. Atmospheric moisture, however, may be nificantly different from ours. One of his labora- important during hibernation. Differences in ad tory stocks of P. m. gracilis had higher values, libitum water consumption and evaporative water but they were below those predicted. He found loss do not reveal a consistent physiological adap- that P. m. gracilis survived longer and lost less tation specific for a given environment among weight on restricted water rations than either P. unrelated groups of rodents; but closely related leucopus noveboracensis or P. m. bairdii, which species and subspecies may show some adaptive also drank more. One field-caught stock of P. m. modifications of these processes. gracilis drank less than P. m. bairdii, but had similar patterns of survival and weight loss. Metabolism and thermoregulation When evaporative water loss, body tempera- Evaporative water loss ture, and metabolism are compared, a difference Shelford (1913) and Chenoweth (1917) impli- in physiological adjustment is shown between two cated the evaporating power of air as an important unrelated rodents living in the same climate and factor in animal distribution. Chew (1951) pre- habitat. Peromyscus has an increase in body sented some evidence for a correlation between temperature between 10 and 250C and an increase rate of evaporation in small mammals and the in evaporative water loss. There is a narrow zone habitat of a species, and Getz (1963) found a of TA, within which its TB is regulated near 370C, similar relationship in Microtus ochrogaster and and which extends slightly into the zone of mini- M. pennsylvanicus. mum metabolism. By contrast, the hibernator Table V compares our results with those of Napaeozapus shows a relatively constant body tem- Chew, Getz, Schmidt-Nielsen and Schmidt-Niel- perature of 370C between 10 and 33.5?C, and sen (1950), and Lindeborg (1955). There is between 20 and 310C it has a slightly decreasing slight difference in the evaporative water loss per rate of evaporation. The high lower critical tem- gram body weight in P. maniculatus gracilis and perature and high metabolism in Napaeozapus P. leucopus noveboracensis. Napaeozapus evapo- below 310C suggest an insulation value which is rates less water than P. 1. noveboracensis, P. m. less than that of Peromyscus. gracilis or Microtus pennsylvanicus, but it does Johansen and Krog (1959) noted high meta- not differ much from M. ochrogaster and P. 1. bolic rates at lower ambient temperatures in the tornillo, forms which occupy more arid regions. zapodid Sicista betulina. At 200C four animals Lee (1963) found no difference in evaporative ranged from about 3.5 to 5.7 cc 02/g hr. Napaeo- water loss between desert and coastal wood zapus averaged 4.4 cc 02/g hr. Three meadow rats; the desert species had a higher evaporation jumping mice at the same TA had a metabolic rate than other desert rodents. Schmidt-Nielsen and of 3.5 to 4.0 cc O2/gm hr (Morrison and Ryser Schmidt-Nielsen (1950) found that desert het- 1962a), but these animals were fat. Zapus, unlike eromyids have lower evaporation than albino mice, Napaeozapus and Sicista, kept increasing its me- but are not different from wild house mice, ham- tabolism with declining temperatures from 15 to sters, or the canyon mouse Peromyscus crinitus. 30 C. The latter two showed a lowering of That a- moist-forest-dwelling rodent such as metabolism at or below 100C. Hibernators gen- Napaeozapus should have such a low evaporative erally have higher lower critical temperatures and water loss is seemingly inconsistent with ideas higher peak metabolic rates than nonhibernators about climatic adaptation (Schmidt-Nielsen and (Kayser 1961). Schmidt-Nielsen 1950; Chew 1951; Lindeborg Unlike the hibernators Perognathus longimem- 1955; Getz 1962, 1963). This reduced evapora- bris (Bartholomew and Cade 1957), P. californi- tion, however, may be important to the survival cus (Tucker 1962), and Sicista betulina (Johansen of a hibernator. Kayser (1961) has reviewed the and Krog 1959), woodland jumping mice did not problem of desiccation during hibernation. Bats, show labile body temperatures or sporadic or daily for instance, are very sensitive to moisture losses torpidity between TA 5 and 33.5?C. In the field, during torpidity, and a relative of Napaeozapus, however, we h~ve found torpid jumping mice Sicista betulina, leaves its dry summer den to trapped on cold, summer nights. Zapus also shows hibernate in a damp place. Sicista has been shown a constant TB down to 100C, but then TB becomes to dehydrate during hibernation when placed in a more variable (Morrison and Ryser 1962a). dry atmosphere (Gottlieb 1951). It is a common practice to extrapolate the As a result of these findings, we feel that neither metabolism curve to the ambient temperature that 58 JAMES E. BROWER AND TOM J. CADE Ecology, Vol. 47, No. 1 equals the body temperature. This presumably of homeotherms. According to Brody (1945) the represents Newton's law of cooling as applied to exponent b generally varies from 0.67 to 0.75. homeotherms: cooling is proportional to the sur- These values appear to hold true for ambient tem- face area and to the temperature difference be- peratures outside the thermal neutral zone (Pear- tween the cooling body and its environment. Scho- son 1962). The slope for Clethrionowmysglareolus lander, Hock, Walters, Johnson and Irving (Pearson 1962) varied from 0.64 to 0.78 over TA (1950), McNab and Morrison (1963), and others from 4 to 28'C. Kayser (1950), however, found have tried to fit their experimental results to this that metabolism in animals varied directly with formulation. Kleiber (1961) has discussed its body weight during hibernation, but was normal misinterpretation and doubts whether it should when they were not in hibernation. Values for be applied to homeotherms. Higher metabolism Peromyscus maniculatus, although few, tend to caused by a decrease in environmental tempera- follow a normal pattern over a range of TA from ture is a thermostatic process in homeotherms, not 10 to 390C like those which Pearson found for a cooling process. Figure 8 is an example of the Clethrionomys. Napaeozapus shows a close rela- danger of assuming the application of Newton's tionship to the weight-metabolism law down to law to Napaeozapus at all ambient temperatures. 200C (Fig. 2). At 100C, however, a slope of There are some animals that do not have metabolic 1.3, instead of the usual 0.7, appears to fit the curves which extrapolate to body temperature. points better. At this temperature, the average Examples among rodents are: the kangaroo mouse minimal metabolism was below the value predicted Microdipodops pallidus (Bartholomew and Mac- from Newton's law of cooling (Fig. 8). The low Millen 1961), the harvest mouse Reithrodontomys metabolism, normal deep body temperature, de- megalotis (Pearson 1960) and the desert pocket creased evaporative heat loss, and change in the mouse Perognathus penicillatus (Brower and slope of the weight-metabolism curve indicate a Cade, unpublished results). significant change in the physiological heat regu- Figure 10 shows a deviation of Napaeozapus lation of Napaeozapuzsat 100C. from the predicted metabolism-weight relationship Most mammals have a similar tolerance for maximum body temperature (Fisher 1958). The 2.5 * , efficiency with which a mammal can regulate its NAPAEOZAPUSINSIGNIS body temperature below the lethal temperature is more important to its survival. There are a number of factors involved in temperature regulation TA 10'C under heat stress: heat production, vascular transfer of heat to the surface, hyperthermia, 2.4 - convection, conduction, radiation, and evaporative M kWk3 cooling. The method and effectiveness of thermoregulation at high ambient temperatures are dif- o ~~~~~~~/ ferent in jumping mice and deer mice. Peromyscus has labile body temperatures and utilizes vasodilation, evaporative cooling, and low metabolism al: 2.3 /S W - for heat tolerance. Peromyscus begins to increase body temperature at 33.50C, water loss sharply at 350C, and metabolism above 370C. Even though /~~ body temperature increases steadily, metabolism remains low but is higher than basal. This fact e~J ~2.11~k02.2 / is difficult to reconcile with Van't Hoff's law as / applied to homeotherms. Peromyscus is more successful in heat than Napaeozapus, since it tol- erates 390C with no ill effects. Napaeozapus is a more precise thermoregulator than Peromyscus, but failing to use evaporative *1.2 1.3 1.4 1.5 cooling, it has less tolerance for heat. At ambient LOG WEIGHT temperatures above 33.50C the jumping mouse FIG. 10. The relation between CO2 productionand body shows a rise in metabolism with a rise in ambient weight in Napaeozapus at 10'C. Closed circles are values temperature. Above 33.5 ?C Napaeozapus becomes used in metabolism calculation, open circles are discarded hyperthermic, increases its metabolism, and main- values. Solid line has a slope of 0.7 and is fitted by eye. Broken line is the best fit by eye to the points. Its slope tains lower evaporative water loss than Pero- is estimated as 1.3. myscus. Winter 1966 ECOLOGY AND PHYSIOLOGY OF WOODLAND MICE 59

TABLE VI. A comparison of the heat budgets of Napaeozapus and Peromyscus

Evaporative Heat Evaporative TA heat lossa Boby heatb production heat loss/ Species (0C) (cal/g hr) (cal/g) (cal/g hr) heat produced (%) Napaeozapus ...... 10 2.2 30.6 27.7 7.9 Peromyscus ...... 10 2.4 30.0 28.7 8.4 Napaeozapus ...... 20 3.7 30.8 21.0 17.6 Peromyscus...... 20 1.9 30.2 17.1 11.1 Napaeozapus ...... 25 2.4 15.4 15.6 Peromyscus...... 25 3.5 30.8 11.7 29.9 Napaeozapus ...... 29 1.8 - 10.5 17.2 Peromyscus...... 29 3.0 8.5 35.3 Napaeozapus ...... 30 1.8 30.8 9.4 19.2 Peromyscus ...... 30 3.5 30.6 8.8 39.8 Napaeozapus ...... 31 1.5 8.5 17.6 Peromyscus ...... 31 Napaeozapus ...... 33.5 2.9 30.6 8.1 35.8 Peromyscus...... 33.5 2.7 31.4 10.4 25.9

Napaeozapus ...... 35 2.3 31.5 10.0 23.0 Peromyscus...... 35 3.8 32.2 9.8 37.8

Napaeozapus ...... 37 4.1 32.5 10.6 38.7 Peromyscus ...... 37 7.0 32.5 9.7 72.2 Napaeozapus ...... 39 - Peromyscus...... 39 21.0 33.0 18.2 115.0

aH = 576W (W = weight of water loss) bH = 0.83T (T = body temperature; fHart 1951) cH = 6.6V (V = volume of C02)

Table VI compares the heat budgets of deer and limiting the rate of cellular metabolism. The mice and jumping mice and illustrates the impor- core body temperature would therefore increase tance of evaporative cooling for the deer mouse. as a result of decreasing the transport of heat by Heat loss per gram body weight at TA 37?C circulation. Thermoregulation in Napaeozapus is is 1.7 times that of the jumping mouse. Heat primarily achieved by ventilation of the respiratory lost by evaporation is calculated to be 72% of tract and by vasodilation. The long, sparsely the heat produced. At TA 370C jumping mice haired tail may be a thermoregulatory organ. lost only 39% of their heat by evaporation. At Johansen (1962) found the muskrat tail to be an 390C deer mice were calculated to evaporate 115% indispensable heat exchanger, which regulated heat of their heat production. This value may b2 high loss in cold environments and overheating in warm as a result of waste caused by spreading of saliva environments. and evaporation of saliva from the desiccator and its wire floor. At their respective lower critical Physiology and climatic adaptation temperatures, deer mice were losing 35% of heat Scholander et al. (1950) state that arctic homeo- production by evaporation, whereas jumping mice therms have lower critical temperatures and there- lost only 18%. Such a high heat loss in deer mice fore wider thermal neutral zones than tropical undoubtedly affects the lower critical temperature. species. They concluded that climatic adaptation This factor has been overlooked by many physi- in homeotherms is associated with insulation and ologists when they computed fur insulation values peripheral vascular control rather than with ad- based on metabolic measurements. justments of basal metabolic rate or deep body We noted maintenance of a low metabolism temperature. Such a broad generalization based during hyperthermia in P. maniculatus similar to on data from a few, distantly related species of that reported by Hudson (1962) for Ammosper- diverse sizes fails to recognize possible phyloge- mophilus leucurus. This paradox may result from netic differences in thermoregulation and metabo- vasoconstriction in nonvital organs by regulating lism. Furthermore, as the body size of an animal the passage of oxygen and substrates to the cells becomes smaller, fur insulation reaches a limiting 60 JAMES E. BROWER AND TOM J. CADE Ecology, Vol. 47, No. 1

TABLE VII. A comparison of metabolic patterns in small rodents

Average Basal redicteda Lower Thermal UTpper Air flow Species weight metabol's-e metabolism critical neutral lethal ambient rate Climate and general Authority (g) (ml 02/g hr) (ml 02/g hr) temperature zone temperature (ml/min) region ______~~~~~(OC) (OC ) (OC )______Zapus hudsonius...... 30.0 1.5 1.5 30 - - 0 Temperate N. Am. Morrison and Ryser (1962a) Napae.szapus insignia ...... 21.6 1.8 1.7 31 2.5 37 400 Temperate E. N. Am. This study Peromyscus maniculatus gracilis ...... 17.0 1.8 1.8 29 8.0 39c 400 Temperate N. Am. This study Peromyscus maniculatus gambeli...... 19.1 1.9(1.7b) 1.7 29 5.5 - 0 Temperate W. N. Am. NcMab and Morrison (1963) Peromyscus californicus insignis ...... 45.5 1.0(0.9b) 1.3 28 6.5 - 0 Mountain W. N. Am. McNab and Morrison (1963) Peromyscus crintus stephensi. 15.9 1.6(I.4b) 1.8 28.5 6.5 - 0 Desert W. N. Am. McNab and Morrison (1963) Reithrodontomysmegalotis.... 9.0 2.5 2.1 33 none 37 0 Mesic-arid W. N. Am. Pearson (1962) Perognathus penicillatus ... . 16.0 1.4 1.8 31 4-6 39c 400 Desert W. N. Am. Brower and Cade (unpublished) Perognathus californicus ..... 20.9 1 0 1.7 32.5 none - - Chaparral W. N. Am. Tucker (1962) Microdipodops pallidus...... 15.2 1.3 1.8 35 none 39 250 Desert W. N. Am. Bartholomew and Mae- Millen (1961) Dipodomys seerriami...... 34.7 1.2 1.4 31 3 39c 600 Desert W. N. Am. Dawson (1955) Dipodomys panamintinus .... 56.9 1.2 1.3 33 1 39 600 Desert W. N. Am. Dawson (1955) Meriones unguiculatus...... 61-80 1.4 - 30 10 40c 0 Temperate desert Asia Robinson (1959) Cerbillus pyramidum...... 72-145 0.8 - _ 0 none 40 0 Equatorial desert Robinson (1961) Africa Dipus aejyptius Equatorial desert Kirmiz (1962) (Jaculus jaculus) ...... 149 0.8 1 .0 29 2 45 - Africa Clethrionsmysrufocanus. .. . 27.5 2.2 1.6 25 - - - Arctic Ecrope Pearson (1962) Clethrionomysglare lus ...... 20.4 2.4 i.7 26 _ - - Subarctic Europe Pearsosi (1962) Clethrionomysqlare-lus ...... 18.0 2.5 1.7 26 none _ - Temperate Europe Jansky (1959) Microtus renns.,slanicus .... 30.0 3.2 1.5 25 4 34-39 0 Temperate N. Am. Wiegert (1961) Micr~;tusarealis ...... 18.0 3.0 1.7 20 10(c - Temperate Ecrope Jansky (1959)

aM = 3.8W -0-27 modified from Brody (1945) (Morrison et al. 1959) b"Minimal" values higher than

value (Scholander et al. 1950; Hart 1957). Thus gracilis is 2 to 30C higher than recorded for other small mammals are faced with special problems in mesic species (P. californicus insignis, P. c. para- colder climates. Small size also presents special siticus, P. truei gilberti, and P. maniculatus gain- problems in hot, arid regions (Schmidt-Nielsen beli). Significant differences in the lower critical 1964). It is not always easy to distinguish among temperatures do not occur. Figure 9 shows an those physiological characteristics which have a increase in metabolism for P. m. gracilis at 33.50C general relationship with body size or which repre- significantly higher than the basal value at 29GC. sent broad phylogenetic patterns, and those which Body temperature at 33.50C was also higher (Fig. are specifically a climatic adaptation. 7). At 370C metabolism showed a slight decrease Table V7II compares basal metabolism, critical over 33.50C, but this decrease was not statistically temperatures, and thermal neutral zones of several significant; however, deer mice were cooling by small rodents from various climates and ecological evaporation of saliva. zones. The information is by no means exhaustive Thermoregulatory and metabolic differences but is a sample from the more complete studies on among three unrelated rodents which exist in the small rodents. A number of these rodents appear same region may reflect underlying phylogenetic to have metabolic patterns following no climatic patterns. The field vole Microtus pennsylvanicus rationale. Some differences in the range of the (Wiegert 1961), the deer mouse Peromyscus thermal neutral zone (Table VII) probably result maniculatus gracilis, and the woodland jumping from different techniques. The air flow in an mouse Napaeozapus insignia have lower critical open-system respirometer may affect the critical. temperatures of 250, 290 and 31'C, respectively. temperatures in rodents, especially those which The basal metabolic rates of the deer mouse and cool by evaporation. The low air flow rates of jumping mouse are close to the predicted weight- 250 cc/min used by Bartholomew and MacMillen relative values, but the metabolic rate of the vole (1961) and 400 cc/min used in this study seem to is higher. have had little effect on the species which do not The differences in physiology of these rodents cool by spreading saliva, but a difference is appar- may follow patterns common to generic and supra-- ent when our study on P. niculatus is compared generic groupings of species. Several workers with that of McNab and Morrison (1963). The have found high metabolic rates and low lower upper critical temperature for P. maniculatus critical temperatures in a number of microtines: Winter 1966 ECOLOGY AND PHYSIOLOGY OF WOODLAND MICE 61 Dicrostonyx groenlandicus (Hart and Heroux of the voles, hibernation in the jumping mice, and 1955), Clethrionomys glareolus (Jansky 1959; a poor tolerance of heat in both probably represent A. M. Pearson 1962), C. rufocanns (A. M. Pear- phylogenetic characters which evolved under the son 1962), Microtus pennsylvanicus (Wiegert influence of a cold climate. In the genus Pero- 1961), and M. arvalis (Jansky 1959). 0. P. myscus, on the other hand, the high lower critical Pearson (1947) also noted high minimum me- temperature, labile body temperature, survival at tabolism in the vole Pitymys pinetorum. Morrison a high TA by the spreading of saliva, and tolerance (1948), who also found high metabolic rates in to hypothermia may be reminiscent of a basic voles, felt that these high values result from short adaptation evolved by the ancestral population in resting periods interspersed with activity; how- response to a warm, arid climate as found in the ever, A. M. Pearson (1962) used short measuring Southwest. The physiological pattern which is periods of 4 minutes to eliminate activity. Micro- found in Peromyscus shows some similarities to tines also have a limited tolerance for heat (Wie- the more specialized one found in Perognathus. gert 1961; Hart and Heroux 1955; and personal We agree that physiological adaptations to cli- observation) and for hypothermia (Neumann mate may be found in closely related populations of 1962; Cade, unpublished). small rodents, but among distantly related groups, Species of Peromyscus seem to be characterized we see few uniformly consistent adaptations which physiologically by labile body temperatures, mod- are specific for a given climate. Close parallelism erately high lower critical temperatures between in physiological adaptation is most likely to occur 27 and 300 C, tolerance for hypothermia and tol- among groups of small mammals subject to ex- erance of high ambient temperatures (Sealander treme environmental conditions such as occur in 1951; Morrison and Ryser 1959; Murie 1961; deserts. The jerboas (family Dipodidae), ger- McNab and Morrison 1963; Cade 1964). A bils (family Cricetidae), and kangaroo rats (family related genus, Baiomys, shows similar features Heteromyidae) are examples of such uniformity. (Hudson 1963). Since small mammals, such as rodents, may have Two zapodinine genera, Zapus and Napaeo- important ancestral differences in their physiologi- zapus, have the following related physiological cal constitutions, one can not expect all groups to attributes: deep seasonal hibernation, high lower follow one pattern in adapting to a particular set critical temperatures, precise thermoregulation in of environmental conditions. It is likely that the nonhibernating period, poor tolerance for high adaptive variations on physiological themes in ambient temperatures, and tolerance for hypo- closely related populations will appear as more is thermia (Morrison and Ryser 1962a; Neumann learned of physiological regulation in rodents. The 1962; Cade 1964; and this study). work of Murie (1961) and McNab and Morrison Another example of phylogenetic uniformity is (1963) is certainly indicative, but we would like apparent. Species of the genus Perognathus to emphasize that the interpretation of differences (family Heteromyidae) seem generally to be char- and similarities in physiological characters should acterized by a low basal metabolism, labile body also consider broader phylogenetic patterns and, temperatures, sporadic torpidity and tolerance for when possible, past evolutionary history. Only high ambient temperatures (Bartholomew and when these larger patterns have been identified Cade 1957; Morrison and Ryser 1962b; Tucker can one begin to appreciate the specific adaptive 1962; Cade 1964; Brower and Cade, unpublished). significance of subtle shifts in physiology. The physiological patterns of three groups of rodents, voles, deer mice, and jumping mice, some ACKNOWLEDGMENTS members of which are sympatric, may reflect their We wish to thank the Adirondack Mountain Authority and the State University of New York Atmospheric area of origin and ancestry rather than their Sciences Research Center for their co-operation in the present-day distribution. According to Hooper field study. The field work was supported in part by a (1949) and Krutzsch (1954), the centers of evo- New York State Museum Graduate Student Honorarium. lution and dispersal for the Zapodinae are in north- Other aspects of the study were supportedby NSF grant eastern North America. The microtines are boreal G-21912. in their origin (Hooper 1949) and are probably LITERATURE CITED invaders from Eurasia (Clark, Dawson and Wood Adolph, E. F. 1949. Quantitative relations in the 1964). Peromyscus appears to have had its origin physiological constitutions of mammals. Science 109: in southwestern United States (Hooper 1949; 575-585. Clark et al. 1964). Although the subfamilies Atmospheric Sci. Res. Center, State Univ. of N. Y., Mountain Microtinae and Zapodinae show distinct physio- Albany. 1963. A report of Whiteface activities, Summer, 1962. logical patterns, both patterns are adaptive for a Bartholomew, G. A. and T. J. Cade. 1957. Tempera- cool climate. The low lower critical temperature ture regulation, hibernation, and aestivation in the 62 JAMES E. BROWER AND TOM J. CADE Ecology, Vol. 47, No. 1 little pocket mouse, Perognathus longimembris. J. in the energetics of homeotherms. Rev. Can. de Biolo- Mammal. 38: 60-72. gie 16: 133-174. , and R. E. MacMillen. 1961. Oxygen consump- , and 0. Heroux. 1955. Exercise and tempera- tion, estivation and hibernation in the kangaroo mouse, ture regulation in lemmings and rabbits. Can. J. Microdipodops pallidus. Physiol. Zool. 34: 177-183. Biochem. Physiol. 33: 428-432. Birch, L. C. 1957. The meanings of competition. Amer. Hatfield, D. M. 1938. Studies on rodent populations Nat. 91: 5-18. in a forested area. J. Mammal. 19: 207-211. Blair, W. F. 1941. Some data on the home ranges and Hatt, R. T. 1930. The biology of the voles of New general life history of the short-tailed shrew, red- York. Roosevelt Wild Life Bull. 5: 513-623. backed vole, and woodland jumping mouse in north- Hooper, E. T. 1949. Faunal relationships of recent ern Michigan. Amer. Midland Nat. 25: 681-685. North American rodents. Misc. Publ. Mus. Zool. . 1951. Population structure, social behavior, and Univ. Mich. 72: 1-72. environmental relations in a natural population of the Hudson, J. W. 1962. The role of water in the biology beach mouse (Peromyscus polionotus leucocephalus). of the antelope ground squirrel Citellus leucurus. Univ. Contrib. Lab. Vert. Biol. Univ. Mich. 48: 1-47. Calif. Publ. Zool. 64: 1-56. Brody, S. 1945. Bioenergetics and growth. Reinhold, 1963. Daily torpor and aestivation in the pigmy New York. 1023 p. mouse, Baiomys taylori. Amer. Zool. 3: 520. Burt, W. H. 1946. The mammals of Michigan. Univ. Jackson, H. H. T. 1961. Mammals of Wisconsin. Mich. Press, Ann Arbor. 288 p. Univ. of Wisconsin Press, Madison. 504 p. Cade, T. J. 1964. The evolution of torpidity in rodents. Jameson, E. W. 1949. Some factors influencing the Ann. Acad. Sci. Fenn. Series A. IV. Biologica 71: local distribution and abundance of woodland small 79-112. mammals in central New York. J. Mammal. 30: 221- Chenoweth, H. E. 1917. Reactions of certain moist 235. forest mammals to air conditions, and its bearing on Jansky, L. 1959. Working oxygen consumption in two problems of mammalian distribution. Biol. Bull. 32: species of wild rodents (Microtus arvalis, Clethriono- 183-201. mys glareolus). Physiol. Bohemoslov. 8: 472-478. Chew, R. M. 1951. The water exchanges of some mam- Johansen, K. 1962. Heat exchanges through the musk- mals. Ecol. Monogr. 21: 215-225. rat tail. Evidence for vasodilator nerves to the skin. . 1955. Skin and respiratory losses of Peromyscus Acta Physiol. Scand. 55: 160-169. maniculatus sonoriensis. Ecology 36: 463-467. , and J. Krog. 1959. Diurnal body temperature Clark, J. B., M. R. Dawson and A. E. Wood. 1964. variations and hibernation in the birchmouse, Sicista Fossil mammals from the Lower Pliocene of Fish betulina. Amer. J. Physiol. 196: 1200-1204. Lake Valley, Nevada. Bull. Mus. Comp. Zool. Har- Kayser, C. 1950. Le problem de la loi des surfaces et vard Univ. 131: 29-63. de la loi des tailles tel qu'il apparait dans l'etude des Connor, P. F. 1960. The small mammals of Otsego Batraciens et Reptiles et des Mammiferes hibernants. and Schoharie Counties, New York. N. Y. State Arch. Sci. Physiol. 4: 361-378. Mus. and Science Service Bull. 382: 1-84. . 1961. The physiology of natural hibernation. Dawson, W. R. 1955. The relation of oxygen con- Pergamon Press, New York. 325 p. sumption to temperature in desert rodents. J. Mam- Kirmiz, J. P. 1962. Adaptation de la gerboise Dipus mal. 36: 543-553. aegyptius au milieu desertique. Soc. de Publ. Egyp- Fisher, K. C. 1958. An approach to the organ and tiennes S. A. E., p. 1-154. cellular physiology of adaptation to temperature in Kleiber, M. 1961. The fire of life: an introduction to fish and small mammals, p. 3-49. In C. L. Prosser, animal energetics. John Wiley and Sons, New York. (ed.) Physiological adaptation. Amer. Physiol. Soc. 454 p. Gentry, J. B. and E. P. Odum. 1957. The effect of Krutzsch, P. H. 1954. North American jumping mice weather on the winter activity of old-field rodents. (genus Zapus). Univ. Kansas Publ. Mus. Nat. Hist. J. Mammal. 38: 72-77. 7: 349-372. Getz, L. L. 1961a. Notes on the local distribution Lee, A. K. 1963. The adaptation to arid environments of Peromyscus leucopus and Zapus hudsonius. Amer. in wood rats of the genus Neotoma. Univ. Calif. Publ. Midland Nat. 65: 486-500. Zool. 64: 57-96. . 1961b. Responses of small mammals to live Lindeborg, R. G. 1952. Water requirements of certain traps and weather conditions. Amer. Midland Nat. rodents from xeric and mesic habitats. Contrib. Lab. 66: 160-170. Vert. Biol. 58: 1-32. . 1962. Notes on the water balance of the red- . 1955. Water conservation in Perognathus and back vole. Ecology 43: 565-566. Peromyscus. Ecology 36: 338-339. -. 1963. A comparison of the water balance of Manville, R. H. 1949. A study of small mammal popu- the prairie and meadow voles. Ecology 44: 202-207. lations in northern Michigan. Misc. Publ. Mus. Zool. Gottlieb, G. 0. 1951. Zur Kenntnis der Birkenmaus Univ. Mich. 73: 1-83. (Sicista betulina). Zool. Jahrb. Abt. System. Okol. McNab, B. K. and P. R. Morrison. 1963. Body tem- Georgr. Tiere 79: 93-113. perature and metabolism in subspecies of Peromyscus Hall, E. R. and K. R. Kelson. 1959. The mammals of from arid and mesic environments. Ecol. Monogr. North America. Vol. 2. Ronald Press, New York. 33: 63-82. Hamilton, W. J., Jr. 1935. Habits of jumping mice. Merriam, C. H. 1884. The vertebrates of the Adiron- Amer. Midland Nat. 16: 187-200. dack region, northeastern New York (Mammalia). Harper, F. 1929. Notes on mammals of the Adiron- Linnaean Soc. N. Y. Trans. 2: 5-214. dacks. N. Y. State Mus. Handbook 8: 51-118. Miller, G. S. 1899. A preliminary list of New York Hart, J. S. 1951. Average body temperature in mice. State mammals. N. Y. State Mus. Bull. 6: 271-390. Science 113: 325-326. Milne, A. 1961. Definition of competition among ani- . 1957. Climatic and temperature induced changes mals. Symp. Soc. Exptl. Biol. 15: 40-71. Winter 1966 ECOLOGY AND PHYSIOLOGY OF WOODLAND MICE 63 Morrison, P. R. 1948. Oxygen consumption in several Schmidt-Nielsen, K. 1964. Desert animals; physiologi- mammals under basal conditions. J. Cell. and Comp. cal problems of heat and water. Oxford Univ. Press. Physiol. 31: 281-292. 277 p. , and F. A. Ryser. 1959. Body temperatures in Schmidt-Nielsen, B. and K. Schmidt-Nielsen. 1950. the white-footed mouse, Peromyscus leucopus novebora- Pulmonary water loss in desert rodents. Amer. J. censis. Physiol. Zool. 32: 256-271. Physiol. 162: 31-36. , and . 1962a. Metabolism and body tem- Scholander, P. F., R. Hock, V. Walters, F. Johnson and perature in a small hibernator, the meadow jumping L. Irving. 1950. Heat regulation in some arctic and mouse, Zapus hudsonius. J. Cell. and Comp. Physiol. tropical mammals and birds. Biol. Bull. 99: 237-258. 60: 169-180. Sealander, J. A. 1951. Survival in Peromyscus in re- , and . 1962b. Hypothermic behavior in lation to environmental temperatures and acclima- the hispid pocket mouse. J. Mammal. 43: 529-532. tion at high and low temperatures. Amer. Midland 1 ~-, and A. R. Dawe. 1959. Studies on the Nat. 46: 257-311. physiology of the masked shrew Sorex cinereus. Sheldon, C. 1934. Studies on the life histories of Physiol. Zool. 32: 256-271. Zapus and Napaeozapus in Nova Scotia. J. Mammal. Murie, M. 1961. Metabolic characteristics of moun- 15: 290-300. tain, desert and coastal populations of Peromyscus. . 1938. Vermont jumping mice of the genus Ecology 42: 723-740. Napaeozcpuus. J. Mammal. 19: 444-453. Neumann, R. L. 1962. Hibernation and hypothermia in Shelford, V. E. 1913. The reaction of certain animals jumping mice of the genera, Napaeozapus and Zapus. to gradients of evaporating power of air. A study in UnpublishedM.Sc. Thesis, Syracuse U., Syracuse, New experimental ecology. Biol. Bull. 25: 79-120. York. 81 p. Sidorowiez, J. 1960. The influence of weather on the , and T. J. Cade. 1964. Photoperiodic influence capture of micromammalia. Acta. Therialogica 4: on the hibernation of jumping mice. Ecology 45: 139-158. 382-384. Snyder, L. L. 1924. Some details on the life history Odum, E. P. 1944. 'Water consumption of certain mice and behavior of Napaeozapus insignis arbietorum in relation to habitat selection. J. Mammal. 25: 404- (Preble). J. Mammal. 5: 233-237. 405. Stickel, L. F. 1948. The trapline as a measure of Osgood, F. L. 1938. The mammals of Vermont. J. small mammal populations. J. Wildl. Mgt. 12: 153- Mammal. 19: 435-441. 161. Pearson, A. M. 1962. Activity patterns, energy metabo- .1954. A comparison of certain methods of lism, and growth rate of the voles Clethrionomysrufo- measuring ranges of small mammals. J. Mammal. 35: canus and C. glareolus in Finland. Ann. Zool. Soc. 1-15. "Vanamo" 24: 1-58. Tappe, D. T. 1941. A natural history of the Tulare Pearson, 0. P. 1947. The rate of metabolism of some kangaroo rat. J. Mammal. 22: 117-148. small mammals. Ecology 28: 127-145. Townsend, M. T. 1935. Studies on some small mam- . 1960. The oxygen consumption and bioener- mals of central New York. Roosevelt Wild Life getics of harvest mice. Physiol. Zool. 33: 152-160. Annals 4: 1-120. Preble, E. A. 1899. Revision of the jumping mice of Tucker, V. A. 1962. Diurnal torpidity in the Cali- the genus Zapus. N. Amer. Fauna 15: 1-43. fornia pocket mouse. Science 136: 380-381. Preble, N. A. 1956. Notes on the life history of Napaeo- Wiegert, R. G. 1961. Respiratory energy loss and penn- zapus. Mammal. 37: 196-200. activity patterns in the meadow vole, Microtus J. Ecology 42: 245-253. 0. local distribu- sylvanicus pennsylvanicus. Pruitt, W. 1959. Microclimates and Whitaker, J. 0. 1963a. Food, habitat and parasites of tion of small mammals on the George Reserve, Michi- the woodland jumping mouse in central New York. gan. Misc. Publ. Mus. Zool. Univ. Mich. 109: 5-25. J. Mammal. 44: 316-321. Quimby, D. C. 1951. The life history and ecology of 1. 963b. A study of the meadow jumping mouse, the meadow jumping mouse, Zapus hudsonius. Ecol. Zapus hudson'ius (Zimmerman) in central New York. Monogr. 21: 61-95. Ecol. Monogr. 33: 215-254. Robinson, P. F. 1959. Metabolism of the gerbil, Williams, 0. 1959. Water intake in the deer mouse. Meriones unguiculatus. Science 130: 502-503. J. Mammal. 40: 602-606. . 1961. Metabolism of Gerbillus pyramidum. Na- Wood, A. E. 1955. A revised classification of the ro- ture 190: 637-638. dents. J. Mammal. 36: 165-187.