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Morphological plasticity and continuous homeothermy of overwintering Sorex vagrans

Scott W. Gillihan The University of Montana

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Recommended Citation Gillihan, Scott W., "Morphological plasticity and continuous homeothermy of overwintering Sorex vagrans" (1992). Graduate Student Theses, Dissertations, & Professional Papers. 7020. https://scholarworks.umt.edu/etd/7020

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Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. MORPHOLOGICAL PLASTICITY AND CONTINUOUS HOMEOTHERMY OF OVERWINTERING SOREX VAGRANS

Scott W. Gillihan

B. S. Colorado State University, 1984

Presented in partial fulfillment of the requirements for the degree of

Master of Arts

University of Montana

1992

Approved by

ChairmanA Bd^rd of Examiners

Dean, Graduate

■ c2o. Date

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Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Gillihan, Scott W., M.A., June 1992 Zoology

Morphological Plasticity and Continuous Homeothermy of Overwintering Sorex vaarans (76 pp.)

Director: Kerry R. Foresman

Shrews are the smallest mammals to remain active all winter in North Temperate climates. Because their small size allows for minimal capacity for heat and energy storage, shrews experience rapid energetic turnover. This problem is exacerbated by the low ambient temperatures and reduced prey availability. To enhance overwinter survival, shrews employ a host of morphological, physiological, and behavioral strategies; this study examined the vagrant shrew (Sorex vaarans) for evidence of three of these strategies: winter weight depression, daily torpor, and reduced activity. Shrews were collected in western Montana throughout a 12- month period to provide a seasonal series of specimens. Total weight, total length, tail length, cranium height, and relative weights of the adrenals, liver, heart, testes, and interscapular brown adipose tissue were determined for each specimen. Additionally, winter-acclimatized shrews were housed in an environmental chamber under simulated natural photoperiod and temperature. The animals were placed on restricted diets and nest temperature was monitored for evidence of daily torpor. Data were collected concurrently on rest and activity periods, and compared with published data for summer-acclimatized S. vaarans. Most morphological values declined from the first summer to minimum values in winter, then increased to their highest values in the second spring and summer as sexual maturity was reached. Relative size of the heart and brown adipose tissue remained fairly constant. The winter weight loss is believed to serve to reduce absolute energy demands. Weight loss data from this study were graphed with similar data from the literature; the magnitude of the loss was seen to be greater in geographic areas with lower winter temperatures. No evidence of daily torpor was noted, although the possibility of very brief depressions of metabolism could not be eliminated. Analysis of activity patterns suggested that S. vaarans forages more frequently in winter, but for shorter periods, spending more time in the relative warmth of the nest.

11

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. ACKNOWLEDGEMENTS I am grateful to my advisor, Dr. Kerry Foresman, for his guidance in all phases of this study; Kerry's door was always open, and he never hesitated to set aside his work in order to discuss mine. I would also like to thank my committee members, Drs. Ken Dial and Dan Pletscher; their suggestions and criticisms greatly improved this thesis.

Dave Worthington's computer expertise was invaluable, as were his comments throughout the course of this project. Jon Gregg and Burl Williams provided skillful assistance in setting up the equipment for the torpor trials. Debbie Conway, Darla Sherrard, and Chuck Tomkiewicz cheerfully helped with the very unglamorous task of digging pitfall

traps. Steve Bell generously provided some of the shrews. Georgia Case assisted with field work but, more importantly, helped me to keep all of this in its proper

perspective. I am especially grateful to Brenda Martin for sharing the sacrifice, frustration, drudgery, stress, challenge,

accomplishment, triumph, and exultation that is graduate

school. I reserve my highest praise for my family, whose

unwavering support made everything possible.

This research was funded in part by the University of

Montana's Division of Biological Sciences, and by two

Grants-in-Aid of Research from Sigma Xi.

Ill

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. TABLE OF CONTENTS page ABSTRACT ...... Ü ACKNOWLEDGEMENTS...... iii LIST OF TABLES...... V LIST OF FIGURES...... vi INTRODUCTION...... 1

METHODS...... 9 Trapping...... 9 Morphological Measurements ...... 9 Torpor Trials...... 10 Activity Patterns...... 12 Analysis...... 12

RESULTS...... 15 Morphological Measurements...... 15

Torpor Trials...... 29

Activity Patterns...... 29 DISCUSSION...... 35

Morphological Measurements;...... 35

Torpor Trials...... 48 Activity Patterns...... 53

APPENDIX. STATISTICAL TESTS...... 56

LITERATURE CITED...... 68

IV

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. LIST OF TABLES

Table Page 1 Comparison of male body weight by season...... 56 2 Comparison of female body weight by season...... 57 3 Comparison of total length by season...... 58 4 Comparison of tail length by season...... 59 5 Comparison of body length by.season...... 60

6 Comparison of cranium height by season...... 61 7 Comparison of adrenal gland index by season...... 62 8 Comparison of liver index by.season...... 63

9 Comparison of heart index by.season...... 64 10 Comparison of brown adipose tissue index by season...... 65 11 Comparison of testes index by season...... 66

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. LIST OF FIGURES

Page 1 Body weight...... 16 2 Male length measurements...... 17 3 Female length measurements...... 18 4 Cranium height...... 19

5 Male adrenal gland weight and index...... 20 6 Female adrenal gland weight and index...... 21 7 Male liver weight and index...... 22

8 Female liver weight and index...... 23 9 Male heart weight and index...... 24 10 Female heart weight and index...... 25

11 Male brown adipose tissue weight and index...... 26 12 Female brown adipose tissue weight and index...... 27

13 Testes weight and index...... 28

14 Representative sleep period...... 30 15 Representative rest/activity period...... 31 16 Daily activity pattern of shrews on ad lib diet...... 33 17 Daily activity pattern of shrews on restricted diet...... 34 18 Mean monthly temperatures at Missoula...... 36

19 Mean monthly precipitation at Missoula...... 37 20 Winter weight change with latitude...... 44

21 Winter weight change with mean January temperature...... 46

VI

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. INTRODUCTION The small size and resultant high surface area-to-mass ratio of shrews places them near the minimum, theoretical size limit for endothermy (McNab, 1983; Pearson, 1948). Pearson (1948) calculated that an adult endotherm could not be any smaller than about 2.5 g, the size of the smallest

shrews; an animal any smaller would lose body heat faster than it could gather and assimilate food. This minimal body size equates with minimal capacity for heat and energy storage; the problem for shrews, therefore, is rapid energetic turnover (McNab, 1991). To offset rapid loss of

body heat shrews maintain a high metabolism, which

necessitates frequent foraging bouts (Saarikko, 1989). But

maintaining energy balance may be problematic for North Temperate shrews in winter, when ambient temperatures are

reduced and the insect prey base may be only one-eighth as large as during the summer (Randolph, 1973). These shrews employ a host of morphological, physiological, and

behavioral adaptations to enhance overwinter survival; this has been termed the "adaptive winter profile” for each

species (Merritt, 1986). Strategies utilized by some species

include nesting communally (Davis and Joeris, 1945), caching

food (Martin, 1984), supplementing the diet with plant

material (Dokuchaev, 1989) and carrion (Schluter, 1980), and

reducing body size to lower absolute energy requirements

(Mezhzherin, 1964).

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The phenomenon of winter reduction of certain morphological measurements has been well documented for Palearctic shrews in the subfamily Soricinae (Genoud, 1985; Hyvarinen, 1984; Z. Pucek, 1965). This so-called Dehnel's phenomenon is marked by a decline in the autumn and a subsecpient increase in the spring of the body weight and the

weights of some of the internal organs including the

kidneys, liver, spleen, adrenal glands, and brain (Hyvarinen, 1984; M. Pucek, 1965; Z. Pucek, 1965; Yaskin,

1984). Myrcha (1969) and Z. Pucek (1965) suggested that this weight reduction is a result of water loss. However, Churchfield (1981) determined that the amount of water lost

in winter, while considerable, was insufficient to account

for the total weight loss, and suggested it may also be a result of protein loss (Churchfield, 1990). Winter weight

loss has also been demonstrated in animals provided with food and water ad lib (Churchfield, 1982; WoIk, 1969). These

changes have been linked with changes in photoperiod (Dark,

et al., 1983; Ure, 1984) and hormonal activity (Siuda,

1964).

The Dehnel's phenomenon is marked by seasonal skeletal

changes as well. The height of the skull decreases in

winter, then increases again in the spring (Pucek, 1963).

These changes are not due to seasonal differences in mineral

content (e.g., calcium deficiency), but to resorption and

subsequent rebuilding of material at the sutura saaittalis

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 3 and sutura lambdoides (Hyvarinen, 1968; Pucek and Markov, 1964). These changes occur without corresponding changes in

other skull measurements such as condylobasa1 length (Pucek and Markov, 1964). The total body length also decreases, due to flattening of the intervertébral discs as a result of

decreasing fluid content in the nucleus oulposus (Hyvarinen,

1969; Saure and Hyvarinen, 1965). These morphological changes are believed to serve to

reduce absolute energy demands (Mezhzherin, 1964). This energy savings has been demonstrated in captive Sorex araneus kept outdoors under natural conditions (Churchfield,

1982; Wolk, 1969). Even though food was provided ad lib, these animals ate significantly less in winter than in summer, measured in absolute terms. Genoud (1985) estimated

that the 0.5 g winter weight loss of Sorex coronatus led to a 10% reduction in the daily energy budget. Evidence of the Dehnel's phenomenon among Nearctic soricines, however, is inconsistent (Connor, 1960; Hooven, et al., 1975; Merritt,

1986; Rudd, 1955). Brown adipose tissue (BAT) is an important source of

endogenous heat for overwintering small mammals (Rothwell

and Stock, 1985). It is generally accepted as the primary

site of nonshivering thermogenesis (NST), the principal

source of increased heat produced during cold stress (Foster

and Frydman, 1978). It is especially critical for shrews

since they are nearly always below their thermoneutral

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 4

zones, which extend from approximately 30 to 34 C (Genoud, 1985; McNab, 1991). The relative weight of BAT in shrews is reported to be 3 to 6 times as great as in sympatric rodents

(Hissa and Tarkkonen, 1969). While some workers suggest that relative BAT mass in shrews peaks in the spring (Buchalczyk and Korybska, 1964; Pasanen, 1969, 1971), other studies have

shown a peak in winter (Churchfield, 1981; Merritt, 1986: Myrcha, 1969; Z. Pucek, 1965). The per-gram thermogenic capacity of BAT also peaks in winter (Merritt, 1986;

Pasanen, 1971).

Some endothermie animals survive periods of energetic stress by employing daily torpor, which is a short-term

depression of body temperature and metabolic rate (Hudson, 1978). In contrast to hibernation, which involves a deep depression of metabolism as a strategy to survive months of

energetic stress, daily torpor is a shallow depression of

metabolism when shorter periods of energetic stress occur.

While body temperature in hibernating animals can be as low

as 2-5 C, in torpid animals it only decreases to 10-20 C,

and only to 30-34 C in some birds (Wang, 1989). Daily energy

savings of 5-30% have been reported (Hill, 1975).

Photoperiod is believed to be the environmental cue that

triggers daily torpor in winter (Steinlechner, et al.,

1986), while ambient temperature exerts some influence over

its depth and frequency (Gaertner, et al., 1973). Examples

include insectivorous bats, which utilize torpor during the

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. daylight hours when they are unable to forage, and

hummingbirds, which utilize torpor at night for the same reason (Lyman, 1982). Merritt (1986) suggested that shrews might utilize

daily torpor as a means of avoiding the energetic cost of maintaining a high metabolism during winter. McNab (1969)

had earlier postulated that shrews did not enter torpor due

to their opportunity for continous foraging, which contrasts with the temporal constraints faced by bats and

hummingbirds. Once torpor was documented in the

Crocidurinae, but not the Soricinae, subfamily of the Soricidae (Frey and Vogel, 1979; Gebczynski, 1971; Nagel,

1977; Vogel, 1974), Vogel (1980) suggested that soricines

were incapable of entering torpor due to their higher body temperature and metabolism. At about the same time, torpor

was demonstrated in the soricine Notiosorex crawfordi. which

has the lowest body temperature reported for this subfamily

(Lindstedt, 1980). McNab (1983) then formulated the "minimal

boundary curve for endothermy", which separates animals that

enter torpor from those that do not, based on the

relationship between body size and basal metabolic rate. To

offset the high rate of energy turnover, a small animal must

maintain a high level of energy intake or resort to torpor

to conserve energy (McNab, 1989). Genoud (1988) plotted BMR

values for shrews against body mass and confirmed that the

boundary curve separated the two subfamilies, with soricines

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above the line, on the "non-torpor" side. There were, however, three exceptions: N. crawfordi. which had

demonstrated torpor, Sorex sinuosus (= S . ornatus; Junge and

Hoffmann, 1981), which fell just below the line and had demonstrated "torpor-like" behavior in response to energetic

stress (Newman and Rudd, 1978), and S. vaarans. which could

be expected to utilize torpor based on its position below the line, but had not been subjected to torpor trials.

The lack of demonstrated torpor in other soricines may be due to improper study design. The frequency and duration

of torpor has been found to be greater during winter than

other seasons in heteromyid rodents (French, 1989; Lynch, et al., 1978) and hummingbirds (Carpenter, 1974). This pattern appeared unrelated to food availability or ambient

temperatures. If this annual rhythm is present in soricines, winter-acclimatized individuals should be more likely to

exhibit torpor than summer-acclimatized individuals; in many

studies this seasonality was not considered (Hanski, 1984;

Morrison, et. al., 1959; Vogel, 1976). Even when utilizing

winter-acclimatized animals, it may be necessary to expose

them to the low temperatures found in the field to induce

torpor (Lynch, et al., 1978). However, most metabolic trials

with soricines have been conducted at 2 3-30 C, well above

winter ambient temperatures (Hanski, 1984 ; Merritt, 1986;

Morrison and Pearson, 1946; Morrison, et al., 1959; Tomasi,

1985; Vogel, 1976). Aitchison (1987), in a review of the

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literature on shrew metabolism, stressed a need for data

from low-temperature trials. Previous attempts to elicit torpor in soricines have

not adequately considered the role of food availability. Hudson (1978) recommended that animals in torpor trials

undergo a progressive restriction of available food.

However, some researchers have assumed that starvation will

trigger torpor, and have conducted trials with unfed animals (Gebczynski, 1971, 1977; Morrison and Pearson, 1946), while

others have conducted trials with animals fed ad lib

(Gebczynski, 1977; Hanski, 1984). Lindstedt (1980) elicited torpor in the soricine N. crawfordi only when individuals

were on diets restricted to maintenance levels; animals fed ad lib never entered torpor. Laboratory conditions to which shrews have been exposed

in these studies varied. Animals have been held for up to 6 months before metabolic trials (Genoud, 1985; Hanski, 1984);

results from these studies should be examined critically

since levels of fat, which play a key role in

thermoregulation, are much higher in captive shrews

(Churchfield, 1981). Even recently-caught animals may not be

suitable test subjects if they have not been maintained at

the temperatures found in the field. Short-term exposure to

warm temperatures has been shown to result in a decrease in

the capacity for nonshivering thermogenesis in Peromyscus

spp. (Zegers and Merritt, 1988).

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 8

A final problem apparent in these previous studies has to do with sample sizes. Since not all individuals in a

population will enter torpor (Hudson, 1978), sample sizes should be relatively large to increase the likelihood of

capturing individuals predisposed to torpor. However, studies with winter-caught soricines have relied on small sample sizes (n < 5) (Gebczynski, 1971, 1977; Genoud, 1985;

Morrison and Pearson, 1946).

In addition to morphological and physiological changes, shrews in winter may adopt a behavioral shift. They may

spend more time in their nests, possibly as a result of reduced absolute energy demands brought about by the reduction in body mass, or to reduce the energetic costs of

activity incurred in the cold environment (Buchalczyk, 1972; Churchfield, 1982). In order to contribute to the knowledge of winter

survival ecology of Nearctic soricines; including development of an adaptive winter profile for S . vaorans. the following questions were examined:

1) Does s. vaarans exhibit the same seasonal variation

in morphological indices as Palearctic soricines,

specifically organ weights, BAT deposition, body length, and

skull height?

2) Will winter-acclimatized S. vaarans enter torpor

when energetically stressed?

3) Does S . vaarans exhibit reduced activity in winter?

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. METHODS Shrews were caught in pitfall traps (number 10 cans buried flush with the soil surface) and unbaited Sherman live-traps. Traps were set within 15 m of streams; at all

sites vegetation was dominated by douglas-fir fPseudotsuaa

menziesii) and western larch (Larlx occidentalis), with lodgepole pine (Pinus contorta) and willow (Salix spp.) also

present. Most shrews were captured in the Lolo Cree)c

drainage west of Missoula, Montana. Additional specimens

were collected from similar habitat in the Bitterroot River

drainage south of Missoula, the Blackfoot River drainage

east of Missoula, and the University of Montana Biological Station at Flathead La)ce. The sites were trapped on a

rotating schedule, with each site visited for 2-10 days followed by at least a 2-month hiatus. To provide a seasonal

series of specimens for the morphological studies, shrews

were collected from April 1990 to March 1991, with

additional animals collected in September 1991 and January 1992. Live animals used in the torpor trials were captured

in February and April 1991, and January and February 1992.

Morphological data were gathered from trap mortalities

collected throughout the year. In most cases, measurements

were taken on animals within 18 hours of death. On rare

occasions, more shrews were collected than could be

processed in one day, and some specimens were frozen until

the next day. Tota1-body measurements were made before

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 10 dissection, then the adrenal glands, liver, heart, and interscapular brown fat masses were excised and weighed to 0.0001 g on a Mettier balance. To adjust for differences in body size, each weight was expressed as a percentage of the body weight after subtracting the weight of the tissue or organ from the total body weight; this value was referred to as the index for that organ or tissue. Weight measurements

from pregnant females were not included in any analysis. Skulls were cleaned of tissue by dermestid beetles, and cranium height measurements were made with a dissecting

microscope fitted with an ocular micrometer. Live shrews brought back to the lab were housed individually in cages in an environmental chamber,

maintained under simulated natural photoperiod (9L:15D) and temperature (5 ± 2 C), and provided water and food ad lib. The cages were opaque plastic buckets with 530 cm2 of floor

space, lined with a thin layer of fiqe dirt. The animals

were fed at approximately 1720 h each day; the food was commercial dry cat food, moistened with water and mixed with

canned cat food (2 parts dry:1 part canned). Additionally, two live meal worms were supplied to each shrew daily. The

weight of the food was checked daily to determine the amount

eaten; this was assumed to be the amount required for

maintaining body weight. Following a two-day period of

adjustment to the laboratory conditions, the food was

reduced stepwise over a 3-day period to 70% (1991 trials) or

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 11

80% (1992 trials) of maintenance levels. A foam tube closed at one end (length 7 cm, inside diameter 2.5 cm) served as

nest chamber. A copper-constantan thermocouple was

positioned in the floor of the tube so that approximately 1 mm of the thermocouple was exposed. Preliminary trials were

conducted to determine optimum placement of the thermocouple

to ensure that the shrew's venter would be in contact with it whenever the animal was in the nest. A Honeywell

recording potentiometer (Model 6400) provided a record of

the nest temperature every 40 seconds. An unoccupied cage/nest served as a control to monitor ambient temperature

in the environmental chamber. Animals were monitored for 1-7

days after the adjustment period.

Interpretation of the potentiometer charts was based on

previous studies of shrews and small mammals, which used

similar experimental protocol (Brown and Bartholomew, 1969; Frey, 1980; Frey and Vogel, 1979; Genoud, 1985; Lindstedt,

1980; Vogel, 1974). In those studies, torpor was

characterized by a distinctive pattern of temperature change

in the nest chamber. Entry into torpor was manifested as a

gradual decline in nest temperature requiring an hour or

more. This was followed by steady temperature readings

approximately 10 C lower than when an animal was merely

sleeping in the nest. Individual torpor bouts lasted as long

as 10 hours (Lindstedt, 1980). The period of arousal from

torpor was generally shorter, requiring 10-60 min as the

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 12 animal rewarmed itself, as reflected in increasing nest temperatures. Winter activity periods were quantified in a manner consistent with that of Ingles (1960) to allow comparison with his summer-acclimatized animals. After the adjustment period, some shrews were fed ad lib for an additional 2 days

while nest temperature was recorded. Periods of activity were identified on the potentiometer strip charts by a rapid decline in nest temperature when an animal left the nest. Rest and sleep periods in the nest were marked by steady

temperature readings, 20-25 C above ambient temperature. Each day was divided into 144, 10-minute periods. The number of periods during which any activity occurred was tallied

for each 24-hour period. As an alternative method of analysis, the duration of each rest or activity period for

one individual was determined during one 48-hour period of

ad lib feeding. Because S. vaarans has a maximum lifespan in the wild

of only about 16 months (Clothier, 1955; Rudd, 1955), two

age classes were recognized (Young of the Year and Overwintered Adult), based on amount of tooth wear. For

statistical analyses and graphing, animals were separated by

age class and sex. Monthly means of morphological

measurements were calculated and graphed for comparison with

previous studies, and to allow examination of trends.

However, due to the arbitrary nature of monthly divisions.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 13 and because of small sample sizes in some months, the age class and date of capture were used to pool individual morphological measurements into 6 seasons for statistical analyses. Dates of separation between seasons were 15 May, 18 August, 16 November, 19 February, 15 May, 13 August, and

1 December; these dates were selected to coincide with gaps in the collecting periods and inflection points in the data.

Seasonal means for each morphological variable were

calculated to test for differences between seasons. As an initial step, Bartlett's test of homogeneity of variances was employed. Variables with sufficiently homogeneous variances (at the 0.05 level), were then analyzed with one­ way analysis of variance (ANOVA) with the Scheffe procedure

used to identify the groups that were significantly different. Variables with heterogeneous variances were subjected to square root transformation, then re-submitted to the Bartlett test. Transformed variables with homogeneous

variances were tested with one-way ANOVA as above. Variables that still had heterogeneous variances were tested for equal

means by the nonparametric Mann-Whitney U-test, with the

Bonferroni adjustment of significance level employed to

account for the number of tests.

The morphological indexes were first normalized with

arcsine transformation (Sokal and Rohlf, 1981), then tested

for homogeneity of variance. Those that had sufficiently

homogeneous variances were tested for equal means by one-way

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 14

ANOVA. Those that did not were tested with the Mann-Whitney

U-test as untransformed values.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. RESULTS

Morphological data were collected from 189 S. vaarans. Monthly means for each of the morphological measurements and

indexes are plotted in Figures 1-13. Measurements from

specimens were plotted based on month of capture and age

class, regardless of calendar year. Each plot then essentially tracks a cohort through its life cycle, i.e.,

the plot begins in May, when the first Young of the Year

(YOY) was captured, and ends the following November, when

the last Overwintered Adult (OA) was captured.

A general pattern of change can be identified in most of the graphs. There was a slight increase from May to June, followed by a steady decline from June to September, which

was mostly reversed in October. Another decline into the

winter months of December and January followed, when minimum values for most of the measurements were recorded. Both

sexes grew rapidly in the spring, when many of the

measurements reached their highest values. Values for males began to rise in the January/February period, at least one

month before females. Values remained fairly constant from

April through August, then declined gradually through the

fall months. An exception to the general pattern was found in the

values for the adrenal glands. For both sexes, the adrenal

gland weight and index fluctuated very little during the

first year, and did not exhibit the winter weight reduction.

15

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 10

8 o> 6 X o 111 4

2

0 MJJASONDJ FMAMJJASON MONTH

10

8

6 11 14 14 X o 18 üi 4

2

0 MJJASONDJ FMAMJJASON MONTH Fig. 1. Total body weight of male (above) and female (below) Sorex vagrans by month (mean ± SD).

16

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 130

E 120 - 10 E 110 -■ O z 100 - LU 90

5 80

70 MJJASONDJ FMAMJJASON MONTH 55

E 50 E § UJ 40

35

30 MJJASONDJ FMAMJJASON MONTH 80

70 ,10 7 E E 60 10 9

UJ 50 - >

8CD 40 -

30

MONTH

Fig. 2. Total length, tail length, and body length of male soyex vaarans by month (mean ± SD).

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 120 - £ & 110 - g ï C5 100 H Ul I ï l i t ' ï f i i —I 90 - < 6 80 -

70 1 I— I— I— UJL j I I. i,,.l I I— I I I I I I MJ J ASONOJ FMAMJ J ASON MONTH

60

11 Z I 40 - -IUJ 30 -

20

MONTH 80

70 - E £ X 60 o z UJ 50 - o s 40 -

30 MJJASONDJ FMAMJJASON

MONTH Fig. 3, Total lengthy tail length, and body length of female Sorex vaarans by month (mean ± SD).

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 7

E E 6 X O z 5

3 Z 4 < OC o 3 MJ J ASONDJ FMAMJ J ASON MONTH

6.5

E E 6.0 -

Ë 5.5 i Z 5.0-

< OC 4.5- o 4.0 MJ J ASONDJ FMAMJ J ASON MONTH

Fig. 4. cranium height of male (above) and female (below) sorex vaçgana by month (mean ± SD).

19

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 0.020

" 10 s I °"" UJ 5 0.010 -J < z UJ K 0.005 <Û

MJ J ASONOJ FMAMJ J ASON MONTH

6 6

0.2 0 - X oUJ z

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0 QQ ' ' ' I ' ' ' ' '__ I__ I__ I I I .1.1 II. I. I. I.. I-- 1. MJJASONDJ FMAMJJASON

MONTH

Fig. 5. Adrenal gland weight (above) and index (below) of male SOXfiX vaarans by month (mean ± SD).

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Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 0.02

en

X O

0.01 -

0.00 MJ J ASONOJ FMAMJ J ASON MONTH

0.3

0.2

—I < 2 Ul OC o <

0.0 MJ J ASONDJ FMAMJ J ASON

MONTH

Fig. 6. Adrenal gland weight (above) and index (below) of female Sorex vaarans by month (mean ± SD).

21

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 0.8 -

o 0.6 - üi S 0.4 - QC UJ > 0.2 -

0.0 MJJASONDJ FMAMJJASON MONTH

12. 0 -

10.0 X 10 8 o 8.0

CE Ul > 6.0

4.0

2.0 MJ J ASONOJ FMAMJ J ASON MONTH

Fig. 7. Liver weight (above) and index (below) of male sorex vaarans by month (mean ± SD).

22

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Ot) 0.6 - f— X 0.5 0.4 - 0.3- UJ 0.2

0.0 MJJASONDJ FMAMJJASON MONTH

10

8 14 I oc 6 s:

4

2 MJ J ASONDJ FMAMJ J ASON

MONTH

Fig. 8. Liver weight (above) and index (below) of female Sûisx Yaarans by month (mean ± SD).

23

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O)

0.10 - o üj $ -4 QC 0.05- < UJ

0.00 MJJASONDJ FMAMJJASON MONTH

2.0

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0.0

MONTH

Pig. 9. Heart weight (above) and index (below) of male sorex vaqrans by month (mean ± SO).

24

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O) 0.10 -

X 0.08 - 0 14 1 0.06-1 oc 0.04 - < Ul X 0 .0 2 -

0.00 MJJ ASONDJ FMAMJ J ASON MONTH

2.0

1.5-

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0.0 MJ J ASONDJ FMAMJ J ASON MONTH

Fig. 10. Heart weight (above) and index (below) of female Sorex vaarans by month (mean ± SD).

2 5

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3 0.120 - X 0.100 - o UJ 0.080 - 10 s 0.060 - T 10 < m 0.040- 0,020 0.000 MJ J ASONDJ FMAMJ J ASON MONTH

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Fig. 11. Bro%m adipose tissue weight (above) and index (below) of male SSüZSK vaarans by month (mean ± SD).

26

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0.06- O) 14

LU 0.04 -

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0.00 MJJASONDJ FMAMJJASON MONTH

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Fig. 12. Brown adipose tissue weight (above) and index (below) of female Sorex vaarans by month (mean ± SD).

2 7

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Fig. 13. Testes weight (above) and index (below) of Sorex vaarans by month (mean ± SD).

28

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With the onset of spring and the sexual maturation of the animals, however, the adrenals increased markedly. Results of the statistical analyses comparing seasonal means are presented in the Appendix, in Tables 1-11. Again, certain general trends are apparent. Females exhibited a

significant decline for most measurements between summer and winter, followed by a significant increase the second

summer. Most values for males showed no significant difference between first summer and winter, but then a significant increase the second summer.

Nine animals were used in the torpor trials. Two of the

three animals used during the 1991 trails died, probably as a result of overly severe food restrictions. Data from those animals on the day of death were not used in analysis of

activity patterns. Potentiometer strip charts representing 168 hours of trials with shrews fed ad lib and 602 hours of trials with animals on restricted diets were examined.

Extended sleep and activity periods were readily distinguished (Figs. 14-15). However, the particular pattern of temperature change that would indicate a torpor bout, as

described above, was never evident. Three shrews were fed ad lib for a total of 7 days.

These animals were active during an average of 100.7 of the

144 daily 10-minute periods, or 70%. Six shrews were on

restricted diets for a total of 21 days. These animals were

active during an average of 102.2 of the 144 10-minute

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 20 - S

s i

0 20 40 60 80 100 TIME (m in )

Pig, 14. Representative section of potentiometer strip chart during typical sleep period of Sorex vaqrans♦

3 0

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 20 - 5 i : 10 -

m

0 20 40 60 80 TIME (min)

Fig. 15. Representative section of potentiometer strip chart during typical rest/activity cycles of Sorex vagrans.

3 1

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 32

periods, or 71%. The average duration of an activity period was 55 min during the day and 73 min at night. For these

shrews on restricted diets, the average rest period was 25 min during the day and 31 min at night. The longest activity period during the day was 3 hr 50 min, and at night, 6 hr 10

min. The longest rest periods were 1 hr 10 min and 2 hr 10

min for day and night, respectively. The daily activity patterns for shrews on the different feeding regimes are presented in Figures 16 and 17.

The duration of individual rest and activity periods

were determined for a single shrew over a 48-hour period.

This method of tabulation revealed average activity periods

of 2 min 20 sec during the day and 4 min at night. Average rest periods were 11 min 36 sec during the day and 9 min 20

sec at night. This animal was active for 26% of each 24-hour

period.

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3 4

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. DISCUSSION Morphological Measurements

The results indicate that the Nearctic S . vaarans undergoes seasonal morphological changes similar to

Palearctic shrew species. The observed pattern of winter

decline in most measurements, with subsequent growth the second year, is consistent with the Dehnel's phenomenon.

The seasonal weight changes are the result of both extrinsic factors (environmental conditions) and intrinsic factors (maturation, Dehnel's phenomenon). The May to June

increase in body weight, and most of the other measurements, was a result of growth of YOY animals to adult size. The June-September decrease may have been due to dry conditions

in the shrews' habitat. The presence of water has been shown

to play a key role in the local distribution of shrews, presumably because of the higher abundance of prey items

found in moist areas (Getz, 1961) and because of the relatively high evaporative water loss experienced by shrews

(Chew, 1951). Dessication was believed to be the cause of a

similar late-smnmer decline in the body weights of S.

vaarans captured in an area of Oregon where warm, dry summers were common (Hooven, et al., 1975). The same pattern

was also found for S. trowbridaii in the Sierra Nevada

Mountains of California (Jameson, 1955). In western Montana,

May through July is a period of increasing temperatures

(Fig. 18) and decreasing precipitation (Fig. 19). The drop

35

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 25 n 20 wu I I - 5 :

Jan Feb lia r Apr May Jun Jul Aug Sep Oct Nov Dec

Fig. 18. Mean monthly temperatures at Missoula, Montana (U.S. Department of Commerce, 1988).

3 6

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! 4

< 3 t: & I 2

Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec

Fig. 19. Mean monthly precipitation at Missoula, Montana (U.S. Department of Commerce, 1988).

3 7

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 38 and subsequent rise in body weight parallels the changes in precipitation, with a one-month lag. This lag time could be a result of gradual drying of the habitat and resultant dessication of shrews, or it could be due to a lag in responses of invertebrates to the drying conditions.

Although a similar decline is not apparent in an earlier study from this same area (Clothier, 1950), those results were confounded by the inclusion of pregnant females and the generally larger Sorex monticolus. Confirmation of dessication as the cause of this decline would require detailed examination of habitat conditions, prey

availability, and analysis of shrew body composition. Finally, although values were low during this period, the

lowest values for most measurements were recorded in winter;

this is consistent with the Dehnel's phenomenon. Month to month changes in total length for both sexes failed to follow the general pattern described earlier, and

statistical analysis revealed no significant reduction

between first summer and winter. However when tail length,

which did not change significantly during the shrews'

lifespans, was subtracted from each specimen, yielding body length, the general pattern did emerge. That the winter

decline in length was found in the body but not the tail

supports previous work (Hyvarinen, 1969; Saure and

Hyvarinen, 1965), which implicated the intervertébral disks

of the spinal column as the site of the shrinkage

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 39

responsible for the winter decline in total length.

Changes in cranium height followed the general pattern of change, with one difference. The values were highest the

first summer rather than the second; there was a secondary peak during the second summer. This pattern is similar to the pattern of change for other Sorex species (Pucek, 1963).

Changes in brain weight in S. araneus follow a parallel pattern, but the magnitude of the change is greater (Pucek

and Markov, 1964), suggesting that seasonal change in

cranium height is a secondary phenomenon in response to changes in the brain (Bielak and Pucek, 1960). Adrenal values for males remained elevated throughout

the breeding season, while values for females appeared to return to first-year values by June. The longer duration of adrenal enlargement for males is probably related to the

breeding strategy of shrews. Shrews are polygynous, and the

normally solitary males expand their ranges in spring as

they search for females with which to mate (Churchfield,

1990; Hawes, 1977). The increase in adrenal size is related

both to sexual maturation and to the stress brought about by

the increase in agonistic encounters with other individuals

(Pankakoski and Tahka, 1982 ; Z. Pucek, 1965). As breeding

season winds down in late summer, those encounters diminish

in number, and adrenal weights decline as well.

Previous research has shown a different pattern of

change in adrenal weights for immature Sorex minutus and S_a_

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 40 araneus (Hyvarinen, 1984; Pankakoski and Tahka, 1982; Z. Pucek, 1965). The adrenal glands of animals in those studies were as large during the first summer as during the second. Because those species very rarely attain sexual maturity during the first summer (Pucek, 1960), the large size of the immature animals' adrenals was attributed to the stress of social interactions. An autumnal decline was interpreted as

being a consequence of decreasing social interactions after young animals had established territories for overwinter survival. It is not clear why there was not a comparable

pattern of change of adrenal glands in this study, since

immature S . vaarans also establish territories in the fall (Hawes, 1977).

Values for liver weight and index for both sexes followed the general pattern of seasonal change. There was an especially pronounced decline in value in late summer to the minimum in September. This decline was apparent in both

sexes the first summer, and in males the second summer. That it is not apparent for females the second summer is possibly

due to the small sample sizes. As stated above, this decline is believed to be related to the warm, dry conditions in the

habitat. Low winter weights are possibly due in part to the

low liver glycogen content recorded during that season

(Hyvarinen, 1984). The heart weight of both sexes followed the general

pattern of a May to June increase, a decline to September,

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 41 then an increase in October. There was no clear reduction in winter. Male heart weight increased appreciably in spring, but this did not appear to be the case for females. The

heart index showed no statistically significant changes for males through the seasons, although females exhibited a

significant increase between summer and winter. The absence of marked fluctuations of the heart weight and heart index is believed to be due to the importance of maintaining high cardiac output throughout the year (Z. Pucek, 1965), which is especially critical for shrews, with their high mass- specific metabolism and rapid heart rate.

Because of the extreme variability of the values, it was difficult to draw conclusions regarding seasonal changes in BAT. The May to September general pattern was apparent in BAT weight for males but not females. There was no clear winter increase in absolute and relative weights as has been found for S . araneus in Poland (Myrcha; 1969; Z. Pucek,

1965). Instead, these results are similar to results for S_^

araneus in England, where a seasonal change in BAT of only 2% was recorded (Churchfield, 1981).

Although there were no clear seasonal changes in the

amount of BAT present, its condition did change. No

qualitative analysis of the BAT was attempted, but

differences between summer and winter were apparent from

casual observation. In summer, the BAT appeared pink or

brown, and its gelatinous texture allowed easy removal from

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 42

the interscapular region. In winter, the BAT was a darker, redder color, and was more difficult to remove intact because of its slightly more liquid nature. The darker color is indicative of greater blood perfusion and higher

concentration of high cytochrome-content mitochondria (Rothwell and Stock, 1985). BAT with this appearance is considered to be in the "active" state, i.e., actively

involved in maintaining metabolism via nonshivering thermogenes is while the animal is below its thermoneutral

zone (Rothwell and Stock, 1985). Thus, BAT clearly plays an

important role in the overwintering strategy of S. vaarans. The testes of sexually immature males showed a steady

decline into winter. Minimum values were recorded in

October-November, and in winter were significantly smaller than summer. This result is consistent with the Dehnel's

phenomenon. Maturation and a surge of growth began in late January; Clothier (1950) found that spermatogenesis begins

in late February for this species in western Montana. The testes remained enlarged throughout the second summer until

October, as would be expected in light of the extended breeding season (Clothier, 1955; Hawes, 1977; Hooven, et

al., 1975; Newman, 1976). Analysis of some of the morphological measurements was

complicated by the amount of variability present in the

measurements, which no doubt was responsible for the failure

to find statistically significant differences in some

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 43

comparisons. There are several possible sources of this

variability. The first involves the difficulty in obtaining

an accurate measurement of the mass of very small organs, such as adrenal glands. This is due primarily to the difficulty of removing all extraneous tissue; even a small

amount could represent a relatively large increase in the measured mass of the organ. Also, more than one person

performed the dissections and took the measurements. Subtle differences in technique could have translated into relatively large differences in measurements. Finally, because specimens for each month (or season) often came from

different localities, some variation could be due to

morphological differences between populations. Variation of some cranial measurements has been found among western

Montana S . vaarans populations (Hennings, 1970), and could exist for other morphological measurements, as well. It was not possible to test this, however, as sample sizes were

quite small (n < 5 in most cases) once the samples were

split by sex, age class, season, and location.

Based on results from Poland, England, and Finland,

Churchfield (1990) pointed out an apparent relationship

between the extent of winter weight loss and latitude, with

shrews in more northern areas exhibiting the greatest weight

loss. A graph of the magnitude of weight change with

latitude, using data from the literature, reveals a weak

correlation (r-squared = -0.55; Fig. 20); a slightly better

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 2 0 -1 o r-squared = - 0 . 5 5 1 0 - 0 1 , j - » ^raneus o + wn eM us - 1 0 - b. nninuius ■ a S. coronatus a I □ - 2 0 ■ S. funieus % o ' ‘ A 3. irowbridoi) nt - 3 0 - % O - 4 0 - r ' ■ ' ^ ' 1 ' 1 ■ ' ' 30 40 50 60 70 LATITUDE

Fig. 20. Magnitude of summer to winter weight change with latitude for immature Sar&K araneus (Gebczynski, 1965, 1977; Heikura, 1984; Hyvarinen, 1969, 1984; Malzahn, 1974 ; Michielsen, 1966; Myrcha, 1969; Niethammer, 1956; Z. Pucek, 1965; Roben, 1969; Schubarth, 1958), S . coronatus (Genoud, 1985), s. fumeus (Hamilton, 1940), S. minutus (Gebczynski, 1971, 1977; Michielsen, 1966; Myrcha, 1 9 6 9 ) , S . ornatus (Rudd, 1955), s. trowbridgii (Jameson, 1955), and s. vaarans (Clothier, 1950; Hooven, et al., 1975; this study).

4 4

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 45

correlation is found by graphing weight change with mean January temperatures, using data from the recording stations nearest the study sites (r-squared = 0.65; Fig. 21). The two

studies in which shrews gained weight were conducted in areas with mild winters, while the studies which recorded the greatest relative weight loss were in Finland, which

experiences harsh winter conditions. Further support for the influence of temperature comes from Michielsen (1966), who documented significantly greater weight loss in S . araneus during the colder of the two winters of her study. Information from a broader range of latitudes, together with detailed climatic data, could help clarify the nature of

this relationship. There is some confusion regarding the source of the weight loss. Some workers have held that the decline in

total body weight is a result of water loss (Myrcha, 1969; Z. Pucek, 1965), while Churchfield (1981) disputed this. She

contended that, because the proportion of water in the body

declines only slightly, water loss alone cannot be responsible. The results from these studies are similar; the

confusion seems to arise from differences in interpretation.

It is clear that soricine shrews lose weight in winter; it

is also clear that this weight loss is not a result of loss

of fat as body fat levels actually increase, presumably a

result of increasing BAT levels (Churchfield, 1981).

Although it is not known which tissues are being eliminated

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. r-sciuared = 0.65 w a S. vaarans < ♦ S. araneus S + S. ornatus H o S. minutus m S coronatus i a 5. furneus H A S. trowbridaii * - 3 0 -

-4 0 -1 5 -10 ■5 0 5 10 MEAN JANUARY TEMPERATURE (C)

Fig. 21. Magnitude of summer to winter weight change with mean January temperature, as reported by the recording station closest to the study site (U.S. Department of Commerce, 1989); references as per Fig. 20.

4 6

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 47

to reduce total weight, they presumably have a water content comparable to the whole-body water content, i.e., 60-70% (Churchfield, 1981); this would account for the relatively

constant whole-body water content. Therefore, both views are correct in a sense, because tissues are being eliminated, and those tissues are composed primarily of water.

Identification of the tissues involved would be the next

logical step, as it would provide valuable insight into the nature of this phenomenon; this could be accomplished with

compositional analysis of a seasonal series of organs and muscle masses. The idea that winter is an energetically stressful period for shrews is a fundamental assumption that underlies

the research in this area of study. However, if energetic stress is reflected in the mortality rate, then the

available data tend to refute this assumption. The highest

seasonal mortality rates for small mammals have been found at other times of the year, reportedly coinciding with the

spring thaw and autumn freeze (Merritt and Merritt, 1978,

1980). For S. vaarans also, the highest mortality rates

occur during spring and autumn, while the lowest mortality

rates of the year are exhibited during winter (Newman,

1976). Although I collected no data on mortality rates, the

late summer declines in values for most morphological

measurements suggest that this period of hot, dry conditions

may also be an energetically stressful period in this study

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 48 area.

Torpor

Several possible scenarios can explain the failure of S . vaarans to become torpid during these trials. First, the

conditions of captivity may have precluded torpor bouts.

Hudson (1978) felt that the unnatural conditions of captivity typically interfered with the natural responses of

animals in studies of winter dormancy. The very unnatural

changes in diet, food availability, and activity begin to affect an animal's thermoregulation and metabolism

immediately after capture; this has been termed the

"captivity effect" (Studier and Wilson, 1979). Specific problem areas might have included the diet, since a link between dietary protein and torpor has been demonstrated in

certain rodents (Montoya, et al., 1979), and the temperature of the environmental chamber, since animals will resist

entering torpor if ambient temperature is too low (Hudson,

1978) or too high (Lynch, et al., 1978). Another possibility is that the shrews entered a very

shallow torpor that was not recognizeable on the

potentiometer strip charts. Studies of shrews and other

animals that enter torpor reveal a marked depression of

temperature of 10-20 C, and no mention is made of shallower

depressions (Frey and Vogel, 1979; Nagel, 1977; Vogel,

1974) . Shrews in this study never exhibited this drastic

depression or the gradual decline that leads into it.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 49

However, it has been proposed that torpor is (functionally if not biochemically) part of a continuum from sleep to

hibernation, with successive points along the continuum simply deeper depressions of metabolism (Heller, et al., 1978). Brief periods of unusually low rates of oxygen

consumption have been noted for S . ornatus (Newman and Rudd, 1978) and the short-tailed shrew, Blarina brevicauda (Martinsen, 1969). It is possible that brief periods of

depressed metabolism occurred in my study as well. However, no evidence of this was noted. Instead of gradually declining temperatures, which would be associated with

declining metabolism, each sleep period consisted of steady temperature readings interrupted only occasionally by a

sudden shift to either a higher or lower level, where the

steady temperatures continued. These sudden changes were interpreted as shifts in the animal's body posture and

position relative to the thermocouple (Fig. 14). However, a

brief depression of metabolism might not yield a noticeable

decline in body surface temperature; in order to satisfactorily determine if S . vaarans utilizes these brief

respites, monitoring of oxygen consumption may be a more

appropriate method of investigation.

A final explanation is that S. vaarans does not

naturally utilize daily torpor. Based on the basal metabolic

rate (BMR) determined by Tomasi (1985), S . vaqrans falls

well below McNab's (1983) "minimal boundary curve for

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 50

endothermy”, suggesting strongly that this species should

utilize daily torpor to conserve energy (Genoud, 1988). But McNab (1991) has suggested that Tomasi's correction for the

specific dynamic action of food consumed by animals in his trials was unnecessary. McNab fed varying numbers of mealworms to Crvptotis parva individuals before metabolic

trials, without significant differences in the measured metabolic rates. After removing the correction factor from the BMR, S. vaarans falls just above the boundary curve.

This position makes S . vaarans seem a much less likely

candidate for torpor. The position of S . vaarans in relation to the boundary

curve can be further altered by changes in its conductance (McNab, 1983). Measurements of S. araneus indicate higher insulating values for winter pelage (Gebczynski and

Olszewski, 1963), due at least in part to the decrease in

body size as a result of the Dehnel's phenomenon, which

results in an increase in the density of hair follicles

(Borowski, 1958). The use of nests can further improve an

animal's insulation by acting, in effect, as an extension of

the animal's pelage. This advantage can be seen in the

resting metabolic rate (RMR) of S. coronatus; at 2 C, the

RMR of an animal with a nest was 20% lower than the RMR of

an exposed animal (Genoud, 1985). S . vaarans in summer uses

an open cup nest, but in winter constructs a spherical nest

with an inner chamber (Hooven, et al., 1975); this winter

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 51

nest would clearly offer better insulation. Differential use of the available microclimates could

also reduce the energy demands of S. vaarans. The thermal stability and relative warmth of the subnivean microclimate

has been we11-documented (Fuller, et al., 1969; Heikura,

1984; Merritt and Merritt, 1978). The snowcover in western Montana would provide S . vaarans with a thermal advantage.

But S. vaqrans may further escape the low winter

temperatures by taking advantage of the additional insulation offered by logs and the litter layer, where temperatures fluctuate even less (Merritt and Merritt,

1978). Tracking of S. vaarans and S. cinereus marked with phosphorescent powder revealed that, although both species

make extensive use of the space under logs, that space may

be more important to S. vaarans as log density was significantly higher in areas where it was captured (McCracken, 1990). Also, Clothier (1955) found remains of

annelids in 63 of 137 S . vaarans stomachs collected throughout the year, and studies that compared diets of

sympatric shrew species showed S. vaarans had the highest

intake of annelids (McCracken, 1990; Whitaker and Maser, 1976). These data suggest that this species may be more

hypogeal than is commonly believed. Other studies have shown

a strong negative correlation between population densities

of s . vaarans and S. trowbridgii. a species known to burrow

(Dalquest, 1941; Newman, 1976; Terry, 1981) . Although S_^

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 52

vaarans probably does not burrow per se (Terry, 1981), it is known to utilize the burrows of moles (Scheffer, 1945), and

it is common to habitats with a thick organic layer in which

it could forage (Hawes, 1977; Newman, 1976; Terry, 1981). These improvements in the pelage and the microhabitat insulation could moderate the effects of winter ambient

temperatures and reduce the energy expenditure of s. vaarans. thereby shifting the relative positions of the

animal and the boundary curve, moving S. vaarans even

further above the line and presumably reducing the necessity to utilize torpor to conserve energy.

In a broader ecological context, an examination of

continental patterns of distribution revealed that the highest percentages of animals that undergo some period of

dormancy are found in the hot, dry regions (Hagmeir and

Stults, 1964); the authors suggested that dormancy is more

likely a response to drought conditions, not reduced

temperatures. Torpor in shrews may likewise be restricted to

species inhabiting desert or tropical areas where food

distribution is clumped and supplies unpredictable (Genoud,

1988; McNab, 1991); given the limited capacity for energy

storage by shrews, the ability to reduce energy consumption

by entering torpor would be clearly advantageous in that

environment. The ability of crocidurines to enter torpor

could then be seen as a result of their tropical evolution,

in contrast with the north temperate evolution of soricines

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 53 (Genoud, 1988; Vogel, 1980).

Activity Patterns The winter-acclimatized shrews in this study exhibited longer activity periods and shorter rest periods than

Ingles' (i960) summer-acclimatized shrews. This result was unexpected in light of the findings of Churchfield (1982) for S . araneus. which indicated an average activity period

during winter only half as long as during summer, and much longer rest periods during winter than summer. However, while reviewing the potentiometer strip charts, it was

evident that the activity period was often much shorter than 10 minutes, yet each 10-minute period during which any activity occurred was counted as an activity period, as per Ingles (1960). This clearly overestimated the total amount of daily activity. The alternative method was used to

determine the length of each rest and activity period for a

single shrew during a 48-hour period. These results present a more accurate picture of the timing of winter activity periods of s. vaarans. These data can be compared to

observations of captive summer-acclimatized S . vaarans,

which indicated activity periods of 5-10 min, followed by

slightly longer rest periods (Eisenberg, 1964). It therefore

appears that s . vaarans in winter has a slightly shorter

rest/activity cycle than in summer, as was also found for S_^

araneus (Gebczynski, 1965).

Activity patterns for the shrews in this study do not

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 54

show the clear daily rhythm of activity of summer- acclimatized shrews (Ingles, 1960). In that study, although

shrews were active around the clock, they were clearly more active at night, with peaks of activity around 2130 h and

0300 h, and lowest activity between 1500 h and 1700 h.

Shrews in my study, however, exhibited a fairly constant and high level of activity throughout the 24-hour cycle, without clear peak periods of activity. The only obvious lull

occurred during the hour immediately after food was provided; shrews typically sleep for an extended period

after successful foraging (Saarikko and Hanski, 1990).

Assuming that this high level of continous activity is a genuine phenomenon, and not an artifact of captivity or

the tabulation process, several possible explanations

present themselves. Ingles (1960) felt that the high levels of summer nighttime activity might be due in part to

avoidance of certain diurnal predators. While the protective

screen of the winter snow cover clearly does not preclude predation by a subnivean predator (Aldous and Manweiler,

1942), it would allow shrews to remain more active

throughout the day and night because of reduced threat from

birds of prey, the principal predators of shrews (Korpimaki

and Norrdahl, 1989). Ingles also felt that daily

fluctuations in temperature, and possibly their effects on

invertebrates, were linked to shrew activity; he noted that

the low point of activity coincided with the warmest part of

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 55

the day. However, temperature fluctuations may not be a factor in winter since they are dampened in the subnivean space. Thus, shrews could be expected to remain active

throughout the day in winter. Finally, it may be that the lower ambient temperatures in winter place such an energetic

tax on shrews that they reduce their exposure time out of

the nest on foraging bouts; they could compensate for the shorter duration of each bout by increasing the total number

of bouts.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. APPENDIX

STATISTICAL TESTS

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Summer Fall Winter Spring Summer II Summer 4.75 + 0.48 (25) Fall 4.66 + 0.76 (14) n. s. Winter 4.63 + 0.85 (19) n. s. n.s. Spring 7.26 ± 1.52 (11) *** *** *** Summer II 8.00 ± 1.17 (16) *** *** *** n.s. Fall II 6.47 + 0.94 (3) n. s. n.s. n.s. n.s. n.s.

Table 1. Comparison of total body weight of male Sorex vaarans among seasons using ANOVA (Scheffe procedure); 'n.s.' indicates no significant difference, *** indicates a significant difference at the 0.05 level, at the 0.01 level, and ***** at the 0.001 level. Values reported are means (in grams) ± SD (n).

56

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Summer Fall Winter Spring Summer II Summer 5.10 + 0.49 (28) Fall 4.75 + 0.79 n . s. (25) Winter 4.07 + 0.20 ** (28) Spring 6.25 n.s. n.s. n.s. (1) Summer II 6.75 + 1.83 n.s. n.s. * n.s. (3) Fall II 1 6.12 ± 0.18 * ** n.s. n.s. U ( 4 ) Table 2. Comparison of total body weight of female Sorex vaarans among seasons using the Mann-Whitney U-test; indicates a significant difference at the 0.05 level (as modified by the Bonferroni correction), 'n.s.' indicates no significant difference. Values reported are means (in grams) ± SD (n).

57

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Summer Fall Winter Spring Summer II Summer 97 + 5 (27) 100 + 5 (28) Fall 101 + 5 (14) n.s. 98 ± 4 (27) n.s. Winter 98 + 4 (21) n.s. n.s. 96 + 4 (29) n.s. n.s. - Spring 104 + 7 (12) * n.s. n.s. 103 (1) n.s. n.s. n.s. Summer II 108 + 6 (20) *** ** *** n.s. 106 + 4 (3) n.s. n.s. * n.s. Fall II 104 + 2 (3) ri • s • n.s. n.s. n.s. n.s. 112 ± 6 (4) *** *** *** n.s. n.s.

Table 3. Comparison of total length of Sorex vaqrans among seasons using ANOVA (Scheffe procedure); 'n.s.' indicates no significant difference, '*' indicates a significant difference at the 0.05 level, '**' at the O.Ol level, and '***' at the 0.001 level. Values reported are means (in millimeters) + SD (n), with males listed above females in each row.

58

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Summer Fall Winter Spring Summer II Summer 44 + 2 (27) 43 ± 2 (28) Fall 44 ± 2 (14) n.s. 43 ± 3 (27) . s. Winter 44 ± 2 (21) n.s. n.s. 43 ± 2 (29) n.s. n.s. ■ ■ Spring 44 ± 2 (12) n.s. n.s. n.s. 44 : : : : (1) n.s. n.s. n.s. Summer II 44 + 3 (20) n.s. n.s. n.s. n.s. 44 + 2 (3) n.s. n.s. n.s. n.s. Fall II 44 ± 1 (3) n.s. n.s. n. s. n.s. n.s. 45 + 1 (4) n.s. n.s. n.s. n.s. n.s.

Table 4. Comparison of tail length of Sorex vaqrans among seasons using ANOVA (Scheffe procedure); 'n.s.' indicates no significant difference, indicates a significant difference at the 0.05 level, '**' at the 0.01 level, and '***' at the 0.001 level. Values reported are means (in millimeters) ± SD (n), with males listed above females in each row.

59

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Summer Fall winter Spring Summer II Summer 53 + 5 (27) 56 + 5 (28) Fall 56 ± 4 (14) n.s. 55 + 4 (27) n.s. Winter 54 + 4 (21) n.s. n.s. 52 ± 3 (29) * n.s. Spring 60 + 7 (12) ** n.s. * 59 (1) n.s. n.s. n.s. Summer II 65 + 4 (20) *** *** *** n.s. 62 ± 6 (3) n.s. n.s. * n.s. Fall II 60 + 2 (3) n.s. n • s • n . s. n.s. n.s. 67 + 5 (4) ** *** *** n.s. n.s.

Table 5. Comparison of body length of Sorex vaqrans among seasons using ANOVA (Scheffe procedure); 'n.s.' indicates no significant difference, '*' indicates a significant difference at the 0.05 level, '**' at the 0.01 level, and '***' at the 0.001 level. Values reported are means (in millimeters) + SD (n), with males listed above females in each row.

60

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Summer Fall Winter Spring Summer II Summer 5.6 + 0.2 (13) 5.6 + 0.2 (14) Fall 5.3 + 0.2 n.s. (10) 5.3 4- 0.1 ** (22) Winter 5.1 + 0.1 n.s. n.s. (19) 5,0 + 0.2 *** *** (28) Spring 5.0 + 0.2 ** n.s. * (5)

Summer II 5.4 + 0.1 *** *** *** n.s. (9) 5.5 + 0.4 n.s. . s . ** n.s. (2) Fall II 5.4 + 0.1 n.s. n.s. n.s. n.s. n.s. (2) 5.2 + 0.1 n.s. n.s. # s # n. s. n.s. (2)

Table 6. Comparison of cranium height of Sorex vaqrans among seasons using ANOVA (Scheffe procedure); 'n.s.' indicates no significant difference, '*' indicates a significant difference at the 0.05 level, '**' at the 0.01 level, and '***' at the 0.001 level. Values reported are means (in millimeters) ± SD (n), with males listed above females in each row.

61

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Summer Fall Winter Spring Summer II Summer 0.0476 + 0.0118 (24) 0.0447 + 0.0086 (28) Fall 0.0444 + 0.0102 n.s. (14) 0.0396 + 0.0150 n.s. (25) Winter 0.0521 + 0.0197 n.s. n.s. (19) 0.0468 + 0.0116 n.s. n.s. (25) Spring 0.1571 + 0.0672 * * * (10) 0.2695 n.s. n . s. n . s . (1) Summer II 0.1487 + 0.0441 * * * n.s. (16) 0.0534 + 0.0020 n.s. n.s. n. s. n . s . (3) Fall II 0.0821 + 0.0112 * n.s. n.s. n.s. n.s. (3) 0.0444 + 0.0176 n.s. n.s. n.s. n.s. n.s. (4)

Table 7. Comparison of adrenal gland index of Sorex among seasons using the Mann-Whitney U-test; indicates a significant difference at the 0.05 level (as modified by the Bonferroni correction), 'n.s.' indicates no significant difference. Values reported are means ± SD (n), with males listed above females in each row.

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Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Summer Fall Winter Spring Summer II Summer 7.7650 + 1.4569 (25) 8.1581 + 0.7585 (28) Fall 6.4321 + 1.0834 * (14) 6.7677 + 0.9292 *** (25) Winter 6.8597 + 0.7602 n.s. n.s. (19) 6.7429 + 0.6061 *** n.s. (26) Spring 7.8550 + 1.3155 n.s. n.s. n.s. (11) 8.0343 n.s. n.s. n.s. (1) Summer II 9.1602 + 1.3073 ** *** *** n.s. (16) 7.8228 + 1.3840 n.s. n.s. n.s. n.s. (3) Fall II 6.0317 + 0.7492 n.s. n.s. n.s. n.s. ** (3) 7.9380 + 1.2026 n.s. n.s. n.s. n.s. n.s. 1 (4)

Table 8. Comparison of liver index of Sorex vaqrans among seasons using ANOVA (Scheffe procedure); 'n.s.' indicates no significant difference, '*' indicates a significant difference at the 0.05 level, '**' at the 0.01 level, and '***' at the 0.001 level. Values reported are means ± SD (n), with males listed above females in each row.

63

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Summer Fall Winter Spring Summer II Summer 1.1874 + 0.1518 (25) 1.2427 + 0.1545 (28) Fall 1.1502 + 0.1444 n.s. (14) 1.2064 + 0.1591 n.s. (25) Winter 1.2726 + 0.1278 n.s. n.s. (19) 1.4655 + 0.2132 ** *** (27) Spring 1.2641 + 0.1683 n.s. n.s. n.s. (11) 1.1998 n.s. n.s. n.s. (1) Summer 11 1.2908 + 0.1986 n.s. n.s. n.s. n.s. (16) 1.1609 + 0.2007 n.s. n.s. n.s. n.s. (3) Fall II 1.2853 + 0.1194 n.s. n.s. n.s. n.s. n.s. (3) 1.3277 + 0.2648 n.s. n.s. n.s. n.s. n.s. (4)

Table 9. Comparison of heart index of Sorex vaqrans among seasons using ANOVA (Scheffe procedure); 'n.s.' indicates no significant difference, '*' indicates a significant difference at the 0.05 level, '**' at the 0.01 level, and '***' at the 0.001 level. Values reported are means + SD (n), with males listed above females in each row.

64

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Summer Fall Winter Spring Summer II Summer 0.8025 + 0.2943 (25) 0.8493 + 0.3290 (28) Fall 1.0336 + 0.6666 n.s. (14) 0.7779 + 0.2677 n.s. (25) Winter 0.9285 + 0.4372 n.s. n.s. (19) 0.9231 4- 0.3391 n.s. n.s. (27) Spring 0.9789 + 0.4009 n.s. n.s. n.s. (11) 0,9628 n.s. n.s. n.s. (1) Summer II 1.0068 + 0.5017 n.s. n.s. n.s. n.s. (16) 0.6739 + 0.2758 n.s. n.s. n.s. n.s. (3) Fall II 0.7906 + 0.1479 n.s. n.s. n.s. n * s * n.s. (3) 0.9150 + 0.3671 n.s. n.s. n.s. n.s. n.s. (4)

Table 10. Comparison of brown adipose tissue (BAT) index of Sorex vaarans among seasons using ANOVA (Scheffe procedure); 'n.s.' indicates no significant difference, '*' indicates a significant difference at the 0.05 level, '**' at the 0.01 level, and '***' at the 0.001 level. Values reported are means + SD (n), with males listed above females in each row.

65

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Summer Fall Winter Spring Summer II Summer 0.0518 + 0.0319 (25) Fall 0.0337 + 0.0227 n. s. (14) Winter 0.3604 + 0.4130 ** (19) Spring 1.3988 + 0.3962 ** * (8) Summer II 0.9973 + 0.2430 * He * n. s. (16) Fall II 1.2849 + 0.1871 * n. S. n. s. n. s. n. s. II (3) Table 11. Comparison of testes index of male Sorex vaarans among seasons using the Mann-Whitney U-test; indicates a significant difference at the 0.05 level (as modified by the Bonferroni correction), 'n.s.' indicates no significant difference. Values reported are means + SD (n).

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Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. LITERATURE CITED

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68

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Academic Press, New York, 715 pp. Hennings, D.N. 1970. Systematics of the Sorex vaarans- obscurus complex, revisited. M.A. Thesis, University of Montana, Missoula, 118 pp.

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