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METABOLISM, FOOD CAPACITY, AND FEEDING BEHAVIOR
IN FOUR SPECIES OF SHREWS'
CHARLES H. BUCKNER2
Forest Entomology and Pathology Branch, Canada Department of Forestry, Ottawa, Canada
Received May 23, 1963
Abstract
The metabolic rates of Sorex cinereus, Sorex arcticus, Alicrosorex hoyi, and
Blarina brevicauda were calculated from oxygen consumption, carbon dioxide
production, and urinary nitrogen excretion and found to be 6.1, 6.9, 6.7, and
9.7 Calories per animal per day respectively. The resting rate of oxygen consumption was lower for S. cinereus than values reported by previous authors and was
probably close to the basal level. Respiratory quotients were higher than expected for carnivorous animals, averaging 0.83 for all species. Protein catabolism
accounted for about half the daily caloric output. Metabolic rate increased with
increasing population densities.
The minimum numbers of larch sawfly eonymphs required to support the daily
metabolic requirements, including fecal wastage, for S. cinereus, S. arcticus,
M. hoyi, and B. brevicauda were 87, 123, 98, and 150 respectively. Because of
digestive inefficiency and wasteful feeding habits the approximate numbers of
eonymphs destroyed dail y could be as high as 663, 570, 711, and 150, and if hoarding is considered, 833, 790, 891, and 410 respectivel y could be taken. Excepting
B. brevicauda, the larch sawfly is a preferred food of the group and, when available in abundance, comprises over 70% of the diet. It was estimated that shrews
have the capacity to consume numbers of cocoons in excess of naturally occurring
populations, but the likelihood of complete destruction of populations is remote.
Of the species studied, S. cinereus appeared to be the most likely to provide effective control of larch sawfly populations.
Introduction
The importance of shrews as predators of forest sawflies is well established
(2, 9). Previous studies by the writer (3) have indicated predation of from 14
to 88Y0 of cocoon populations of the larch sawfiy, Pristiphora erichsonii (Htg.),
in southeastern Manitoba. Despite their importance, relatively little has been
published on the feeding behavior, food preferences, and metabolism of these
animals. This may be due in part to the peculiar difficulties encountered in
working with shrews as experimental animals. Intolerance of artificial rearing
conditions and a highly nervous and aggressive disposition call for unusual
care in laboratory maintenance. Continuous trapping is required to replace
stocks of test animals. The extraordinarily high rate of food consumption and
the restricted natural diet of these insectivores pose difficult problems in obtaining adequate fresh stocks of natural foods for studies of food preferences.
Identification of food items in the stomach contents of shrews is more difficult
than in the case of rodents, apparently because of more thorough mastication.
The food preference trials described in this paper are based on somewhat
scanty data but are included because of the paucity of such information in
the literature (7). The term "basal metabolic rate" (BMR) is used throughout
the text, with the realization that the measurement of the BMR of animals so
'Contribution No. 965.
?Address: Forest Entomology Laboratory, Box 6300, Winnipeg 1, Manitoba.
Canadian Journal of Zoology. Volume 42 (1964)
260
CANADIAN JOURNAL OF ZOOLOGY. VOL. 42, 1964
voracious and mobile presents a very difficult if not impossible technical
problem. The term "standard metabolism", meaning the metabolism at minimum motor activity, might be more appropriate, but the term BMR is retained in order to equate more readily the results of this study with those
published by other authors (1, 12-15).
Four species of shrews were used in this study: Sorex cinereus cinereus Kerr,
the cinereus or masked shrew; S. arcticus laricorum Jackson. the arctic or
saddle-backed shrew; Microsorex hoyi hoyi (Baird), the American pigmy shrew;
and Blarina brevicauda manitobensis Anderson, the Manitoba short-tailed
shrew. All may, at times, be regarded as important predators of larch sawfly
cocoons. Data on metabolism were obtained from a total of 60 animals. Of
these, 33 were S. arcticus, for which no previous physiological information
could be found in the literature.
The study of shrews and other small mammals as predators of the larch
sawily has been undertaken as an integral part of a long-term investigation
of the ecology and outbreak dynamics of this forest pest in Manitoba (10). The
work described in the present paper was carried out from 1955 to 1957 in the
Whiteshell Forest Reserve in southeastern Manitoba, and is based on part of
a Ph. D. thesis presented to the Zoology Department, University of Western
Ontario, London, October, 1959.
Nletabolism
Apparatus and ilfethods
The metabolism of an animal can be determined in precise terms on the
basis of measurements of oxygen consumption, carbon dioxide production,
and urinary nitrogen excretion. The apparatus was a modification of the closedsy stem automatic respirometer described by Morrison (13). The test cages
were the same as those used for food-preference tests and arc described later
in this paper. The important features with respect to metabolic measurements
were (a) a screen mesh floor, beneath which was suspended (b) a funnel to
collect urine. The carbon dioxide of respiration was absorbed in a solution of
potassium hydroxide and barium chloride, which was located beneath the
funnel beside the urine-collecting receptacle. Oxygen consumption was recorded automatically; carbon dioxide was measured by titrating an acid against
the hydroxide bath (1); and urinary nitrogen was determined by the microKjeldahl technique (S). Constant temperature baths were not available, but
temperature changes within the system were minimized by immersing the
respiration chamber in a water bath containing ice chips and covered with
sphagnum. Temperatures ranged from 9 to 14° C. Carbon dioxide in the
respiration chamber remained below 1% as determined by samples extracted
from the respiration chamber and analyzed by the Van Slyke manometric
technique (8). Caloric utilization in the metabolic process was calculated
according to Brody (1). Table I gives a sample calculation for an adult female
hoyi.
Test animals were taken from permanent sample plots where monthly
estimates were made of shrew population levels. Population assessment involved recapture techniques to be described in a subsequent paper. Thus it
was possible to relate the metabolism of each animal to the density of the
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BUCKNER: METABOLISM OF SHREWS TABLE I
Calculation of the Calories of metabolism of an adult female of M. hoyi weighing 3.5 g
Grams urinary nitrogen excreted per hr
Liters oxygen associated with protein oxidation (.0036 X 5.94)*
Liters carbon dioxide associated with protein oxidation (.0036 X 4.76)*
Total liters carbon dioxide exhaled per hr
Total liters oxygen consumed per hr
Liters non-protein carbon dioxide (.0499—.0171)
Liters non-protein oxygen (.0587—.0214)
Overall respiratory quotient
Non-protein respiratory quotient
Caloric value of liter of oxygen at respiratory quotient .879
Non-protein Cal per hr (4.899 X .0373)
Protein Cal per hr (.0036 X 26.5)*
Total Cal per hr
Metabolic Cal in 24 hr
.0036
.0214
.0171
.0499
.0587
.0328
.0373
.850
.879
4.899
.1827
.0954
.2781
6.67
g urinary nitrogen represents the metabolism of 6.25 g protein, the absorption of 5.94 I. of oxygen, the production of 4.76 I. of carbon dioxide, and the liberation of 26.5 Cal.
population from which it was taken. Fresh test animals were held in the respiration chambers at temperatures of 9 to 14° C for an acclimation period of
3 days. Preliminary trials on oxygen consumption indicated a stabilization of
behavior after 2 days: hence the 3-day period was deemed sufficient. Food in
the form of commercial canned dog food and water were available ad libitum
during the acclimation period and the subsequent metabolic trial because the
animals would die if deprived of them, even for short periods. The diet was
supplemented with some natural foods, especially during the first few hours of
captivity, and occasionally thereafter. Each animal was tested once for a
continuous 24-hour period.
Results
Oxygen consumption was highest per unit body weight in M. hoyi, followed
in order b y S. cinereus, S. arcticus, and B. brevicauda (Table II). This is in accordance with measurements made by other authors, • showing that oxygen
consumption per unit of weight increases with decreasing body weight, and
that it is higher for shrews than expected from values calculated by the general
formula postulated for mammalian metabolism. Minimum and maximum
values of the oxygen consumption of S. cinereus are lower and higher respectivel y than values hitherto published, possibly resulting from (a) the relatively
long periods over which measurements were made in the current study and
(b) the comparatively short term of individual measurements (the automatic
oxygen record recycled after approximately 10 ml was consumed). Minimal
values recorded herein are a close approximation of "standard metabolism", but
their relationship to BMR is subject to the limitations mentioned earlier.
The objection to accepting minimal values as close approximations of BM R is
that, by definition, BMR must be measured during the postabsorptive state
and in the zone of thermoneutrality. Each minimum value of this stud y was
taken during a relatively long period of inactivity, so that it is likel y that the
postabsorptive state was approached. However, the experimental temperatures under which these experiments were conducted were apparentl y well
below thermoneutrality (15), which would tend to overestimate BMR to a
considerable degree.
z
TABLE II
Oxygen consumption, carbon dioxide production, urinary nitrogen excretion, and Calories of metabolism in four species of shrews at 9-14° C
Species
Number of
measurements
S. cinereus
S. arcticus
.111. hoyi
B. brevicauda
*95% confidence interval.
15
33
1
11
02 consumption ml/g hr
Mean
weight
Ay.
Max.
3.6
5.4
3.5
20.1
15.4±2.1*
10.9±1.8*
16.7
4.6±0.8*
28.9
19.7
25.4
5.4
Min.
Av. CO2
production
ml/g hr
Av. urinary
N excretion
mg/g hr
Av. Cal
/animal
per day
7.9
7.5
11.2
4.2
13.6+1.9*
8.8+0.6*
14.2
3.6+0.6*
0.87
1.08
1.02
0.27
6.09±0.26*
6.94±0.33*
6.67
9.69±0.88*
z
z
0
N
0
0
0
0
rr
BUCKNER: METABOLISM OF SHREWS
263
Variation in oxygen consumption within the range of temperature experienced during these experiments was relatively slight. The mean value of
oxygen consumption for S. cinereus was 15.9 +3.6 ml/g hr at 9° C and 15.1 ±
4.1 ml/g hr at 14° C, a difference of only 5%. Comparable results were obtained
for the other species. The temperature regime selected for these studies approximated field temperatures at the time of major cocoon predation.
Carbon dioxide production was surprisingly high (Table II). Respiratory
quotients (RQ), calculated from the mean oxygen consumption and carbon
dioxide production, were 0.SS for S. cinereus, 0.81 for S. arcticzts, 0.S5 for ill.
hoyi, and 0.7S for B. brevicauda. These are relatively high for carnivorous
species, particularly so because the group feeds almost exclusively on a protein
diet.
Urinary nitrogen measurements varied considerably between species (Table
S. cinereus, S. arcticus, 11I. hoyi, and B. brevicauda excreted 75, 140, 85,
and 130 mg nitrogen per day respectively, the equivalent of 1.99, 3.71, 2.25,
and 3.45 kcal. This represented the daily protein catabolism and showed that
one-third to one-half of the entire daily heat production of each species was
attributable to the oxidation of protein.
The daily caloric heat production, recorded in the final column (Table II),
is a combination of basal and active metabolism. If it is assumed that metabolic rate is proportional to oxygen consumption, minimal metabolic rates in
terms of Calories may be estimated using the minimal figures for oxygen consumption. These are 3.1, 4.7, 4.5, and 8.8 kcal per day respectively.
Although the objective of this study was primarily to determine the caloric
requirements of the principal shrews inhabiting tamarack bogs and to relate
these to feeding capacities, sufficient data are available to elucidate the position of these species in relation to general theories of metabolism. According
to Brody (1), the relationship between metabolism and body weight in mammals may be expressed by the equation
111=a TV'
where 31=
R,
IV= bod y weight,
a = specific metabolism = kcal/Bb,
and
b= a power transforming weight into "metabolically active weight".
The accepted values for a and b are 70.5 and 0.73 respectively when W is
expressed in kilograms; hence the equation becomes
BAIR = 70.5 'V.".
The mean weight of each species (Table II) may be substituted in the equation
to calculate an expected BAIR (Table III). As Morrison et al. (15) have pointed
out, basal metabolism is confounded by the specific dynamic action (SDA) of
protein, amounting to 40% of the Calories derived from protein catabolism.
Values for the Calories of protein catabolism have been presented already
(Table II), so corrections for SDA of protein can be made from these (Table
Thus, what at first appeared to be a wide discrepancy between observed
and expected values of the BMR is reduced to insignificant proportions by
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CANADIAN JOURNAL OF ZOOLOGY. VOL. 42, 1964
TABLE III
Comparison of the minimum metabolic rate, minimum metabolic rate corrected for the SDA
of protein, and the theoretical BMR of four species of shrews
Species
Min. metabolic
rate (kcal/day)
Min. metabolic rate
corrected for SDA
of protein
Calculated
BNIR
S. cinereus
S. arcticus
if. hoyi
B. brevicauda
3.1
4.7
4.5
8.8
2.3
3.8
3.1
7.4
2.5
1.9
1.9
6.9
correcting for SDA. The slight differences between observed and expected
values of BMR may have been further reduced had the measurements been
taken in the zone of thermoneutrality. These data lend considerable support
to the views of Morrison et al. (15) that no specific properties, other than high
protein catabolism, need be invoked to explain the exceptionally high metabolic
rates of shrews.
Records maintained in connection with extensive trapping programs carried out in the areas where the shrews were obtained provided information on
the life history of each animal used for the metabolic tests. No significant differences were found in the metabolic rate due to age, sex, season (May to
October), or extent of the cruising radius, but with S. cinercus and S. arcticus,
oxygen consumption was significantly higher in animals taken from higher
population densities (Table IV). B. brevicauda was not available for study from
populations of high density, and a sufficient range of population densities of
11. hoyi was not encountered. The data provide experimental support for the
view held by Chitty (6) that certain physiological changes are associated
with population densit y . Chitty compares such changes in the ph ysiology of
mammals with those observed by Wellington (17) on insects, these changes
being associated with heredity. The differences observed herein are likely the
effects of more frequent physical contact and competition for space and hence
are due to high density per se.
Food Preferences and Daily Activity
Apparatus and Methods
Food-preference tests were complicated by the impossibility of securing
sufficient quantities of insect food other than larch sawfly, and b y the habit of
the animals of removing and hoarding all uneaten food irrespective of preference. Thus a method was adopted whereby preferences might be indicated
without the animals having free access to the food. Small cages similar to those
described by Mann and Stinson (11) were constructed with four openings,
which allowed access to four wire screen runways. The runways were pivoted
and counterbalanced in such a way that the animals would tilt them when they
were entered. The common pivot for the four runways was a metal bar connected by bell wire to the common return terminal of an Esterline-Angus operation recorder. Each runway, when tilted, allowed a wire to touch an individual
mercury cup, which in turn was connected by bell wire to a pen terminal of the
recorder. Thus, when a shrew left its cage and entered a runway, a record was
made of the place, time, and duration of the visit.
'FABLE IV
Average oxygen consumption in three species of shrews at three population levels
Population level
2-4/acre
Less than 2/acre
More than 4/acre
Species
No.
measurements
ml 02 /g hr
No.
measurements
ml 02 ,/g hr
No.
measurements
ml 02/g hr
S. cincreus
S. arcticus
B. brevicauda
8
13
9
15.3+1.4
10.9±1.1
4.6+1.0
5
11
2
15.5+1.9
10.9+1.3
4.5 + 0
5
9
0
19.6+:2.1*
13.3+2.6*
*Difference significant at 5% level.
IF
266
CANADIAN JOURNAL OF ZOOLOGY. VOL. 42. 1064
Test animals were acclimated for a period of 3 days. The food items being
tested were then enclosed in wire containers and suspended at the ends of the
runways. An index of preference for a particular food as compared to the preference for larch sawfly eonymphs was calculated by dividing the minutes of
activit y spent in the runway with the test food by the minutes of activity
spent in the runway containing larch sawfly eonymphs.
The tilting runwa y s also provided a means of comparing the activity of
shrews. Each record of an animal in one of the runwa y s designated an activity
period. The frequency and duration of these activity periods were studied for
15 S. cinereus, 33 S. arcticus, 1 if. hoyi, and 9 B. brevicauda.
Results
The amount of time spent in each runway was assumed to provide an index
of preference for food in the runway. This was confirmed by tests using unparasitized cocoons of the larch sawfly, and cocoons parasitized b y the tachinid
Bessa harveyi (Tnsd.), for which other estimates of preference are available
(3). Four categories of cocoons were placed in the runways, one to each runwa y , and the runway location for each category was chosen at random for
every trial. The categories were:
unparasitized cocoons, exposed for feeding;
unparasitized cocoons, enclosed in wire containers;
cocoons parasitized by B. harveyi, exposed for feeding;
cocoons parasitized by B. harveyi, enclosed in wire containers.
The numbers of unparasitized cocoons opened by S. cinereus greatly exceeded
the numbers of parasitized cocoons opened by this species, whereas the numbers opened by S. arcticus were more nearly equal (Table V). Similarl y , more
time was spent by S. eineretts in the runways containing caged, unparasitized
cocoons than in the runways containing caged, parasitized cocoons, whereas
S. arcticus spent almost equal time in each. The same relative ability to discriminate between parasitized and unparasitized cocoons was noted for these
species in the observations cited previously (3).
Because of the limited availability of many of the prey species, it was necessary in most cases to limit preference trials to one individual of a shrew species.
However, the prolonged period of each trial provided a relatively long series
of data, and the consistenc y of results within individual trials and between
trials of the three long-tailed species add to the confidence in conclusions.
Preferences exhibited by S. cinereus, S. arcticus, and ..11. hoyi were similar.
All showed a decided preference over all other choices for a hepialid larva,
Sthenopsis argentiomaculatus (Harr.), next to the larch sawfly the most abundant food insect available during the years in which these experiments were
conducted. A slight but consistent preference for grasshoppers over larch
sawfly eon y mphs was also exhibited. Slightly less preferred than larch sawfly
eonymphs were elaterid larvae and adults, large lepidopterous larvae, larch
sawfly adults, and dipterous larvae. Tenebrionid and carabid adults, larch
sawfly larvae, spiders, and silphid adults were accepted in decreasing order of
preference, and ants appeared to be avoided entirely. To a degree, the preference exhibited by these three species appeared to be related to the abundance
of the prey species in the bog habitat. In contrast, preferences exhibited by
TABLE, V
Numbers of parasitized and unparasitized cocoons opened by two species of shrews, compared to time devoted to investigating each food
category. Total of 500 cocoons in each category presented to 20 shrews of each species. Parasitized cocoons were reared from larvae bearing
eggs of B. h3rveyi (Tnsd.)
Minutes activity
No. cocoons opened
Species
Unparasitized
S. cinercus
S. arairus
256
451
Parasitized
Ratio u/p
Unparasitized
Parasitized
Ratio u/p
63
4.06
3.19
1 . 03
2 ,469
106
774
439
998
1
11
IF
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CANADIAN JOURNAL OF ZOOLOGY. VOL. 42, 1964
10-
S• cinereus
5
FtG. 1. The daily activity of three species of shrews. Bars represent the average activity
in half-hour intervals over a 24-hour period for 15 S. cinereus, 9 S. arclicus, and 7 13.
brct'icauda.
B. brevicauda appeared to be related to prey size rather than abundance,
viz. large lepidopterous larvae, grasshoppers, adult beetles, sawfly adults,
sawflY eonymphs, and smaller insects were accepted in decreasing order of
preference. This shrew also avoided ants.
The average total daily activity in minutes was 217 for S. cinercus, 115 for
S. arcticus, 239 for M. hoyi, and 94 for B. brevicauda. Activity occurred in short
periods, lasting on the average 2.1, 3.3, 2.9, and 4.5 minutes respectively.
S. cinereus was active for short periods throughout all hours of the day, with
about 19 peaks of activity throughout a 24-hour period and the greatest
activity during the hours of darkness (Fig. 1). About 14 activity peaks were
recorded for S. arcticus, and although these again were distributed throughout
the entire 24-hour period, a more pronounced nocturnal trend was evident.
Periods between activity peaks of B. brevicauda were still longer, with about 11
active periods in 24 hours and a major peak during the hours of darkness.
Only one measurement was made for M. hoyi, which appears to have an activity
pattern resembling that of S. cinereus. Thus S. cinereus and if hoyi are apparently the most active species, S. arcticus about half as active as these, and
B. brevicauda the least active.
Food Utilization
Methods
In calculating the caloric content of food or fecal samples, the material was
first dried to constant weight under partial vacuum. The fat content was then
extracted in ether in a Soxhlet apparatus and the residue dried to constant
weight again, the fat content being represented by the difference in weight
before and after treatment. The fat-free sample was then divided into two approximately equal portions. One was digested in concentrated sulphuric acid,
TABLE VI
Caloric values of preferred insect foods of shrews and the numbers required to satisfy metabolism
Food insect
thenopsis argenteomaculahts
lenicera spinosus (larva)
. spinosus (adult)
'enebrio picipes (adult)
gonum sinuatus (adult)
abanus sp. (larva)
ristiphora erichsonii (et/nymph)
No.
measurements
Mean Cal
per insect
10
2
3
5
4
3
25
.12 (.00-.14)
.09 (.08-. 10)
.11 (.10-.12)
.13 (.11-.14)
. 14 ( . 13- . 15)
.11 (.10-.12)
.07 (.06-.09)
Representative nos. of prey required to satisfy metabolism
S. cinereus
51
68
55
47
44
55
87
S. arclicus
58
77
63
53
50
63
99
M. hoyi
B. brevicauda
56
74
61
51
48
61
95
81
108
88
75
69
88
138
IF
270
CANADIAN JOURNAL OF ZOOLOGY. VOL. 42. 1964
the nitrogen content determined b y the micro-Kjeldahl distillation technique,
and the protein estimated as a multiple, 6.25, of the weight of nitrogen (8).
The second portion was boiled under reflux in 70% alcohol and 10% hydrochloric acid to hydrolyze and extract all utilizable carbohydrates. The supernatant was cleared of proteins by combining it with boric lead acetate, centrifuging, and filtering. It was then subjected to the Hane analysis for reducing
sugars (8). These analyses provide a measurement of the fat, protein, and carboh ydrate and can be converted to Calories by applying the factors 9.3, 4.3, and
4.1 respectively (1). Equivalents for the larch sawfly eonymph may be expressed as follows:
66 . 33 + 5 .54
average eonymph weight (mg)
(hence 1 g is equivalent to approximately 15 eonymphs),
4.04+0.36,
average protein content (mg) 6.09+0.75,
average lipid content (mg)
0.10+0.02,
average carbohydrate content (mg) 0 . 074,
caloric value of one eonymph
1 .2.
caloric value of 1 g of eonymphs
Caloric Values of Preferred Foods
The caloric values of certain abundant preferred foods were determined as
outlined and are listed in Table VI. Representative numbers of individual
insects of each group that would be required to satisfy the metabolic requirements of the four species of shrews are given. Metabolic requirements were
determined by dividing the mean metabolic rate of each species (Table II) by
the caloric value of each food.
Stomach .1nalvses
The stomach contents of shrews killed in snap-back traps were preserved in
70% alcohol and later examined under low-power binocular magnification.
Components of the diet were classified as: remains of larch sawfly eonymphs,
remains of other insects, plant material. The percentage by volume of each of
these classes was estimated ocularly with the aid of a grid underlying the slide.
The stomach contents were analyzed chemically to determine the proportions
of fats, proteins, and carbohydrates in the same manner as described earlier
for food and fecal analysis.
From the gross stomach analyses, the diet of S. cinereus was evidently almost exclusivel y insects. Plant fragments occurred in a number of stomachs
but never amounted to more than 5% of the total amount, and as these were
usually sticks and moss, they were probably ingested accidentally with prey
insects. Fragments of adult larch sawflies occurred occasionally in the stomachs
of S. cinereus from mid-May until the latter part of August (Fig. 2, top). The
balance of the contents was almost exclusivel y "other insects". Towards the
end of August the numbers of larch sawfly larvae rose abruptly, and by midSeptember "other insects" had declined to the level observed for the larch
sawfly earlier in the season. Because of the infrequency of occurrence of any
stage except eonymphs, it is unlikely that S. cinereus is an important predator
during any other stage in the life history of this insect. The predation period
lasts from late August until well into November, amounting to about 90 days
of active predation.
pr-
BUCKNER: METABOLISM OF SHREWS
271
Analyses of stomach contents of S. arcticits gave results similar to those for
S. cinereits (Fig. 2, center), the chief difference being the extent of larch sawfly
utilization during the period of heavy predation. Whereas S. cinereits fed on
larch sawfly almost exclusively, this component amounted to about
7oc,--c of the
100
80
60
40
20
Sores cinereus
70
60
40
20
Sores orcticus
15
10
MAY
JUNE JULY
AUG.
SEPT OCT NOV
FIG. 2. The seasonal occurrence of larch sawfly in the diet of three species of shrews,
based upon stomach analyses performed on 122 S. cineretts, 62 S. arcticus, and 9 B.
brevicauda.
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CANADIAN JOURNAL OF ZOOLOGY. VOL. 42. 1964
diet of S. arcticus. Duration of the predation period was about the same for
both species.
Analyses of stomach contents of the limited numbers of B. brevicauda (Fig. 2,
lower) showed that the sawfly comprised only a small portion of the diet of this
insectivore. Predation on the immature stages of the insect began much earlier
in the season than it did with the previous two species, suggesting that B. brevicauda may prey to a greater extent upon newly-fallen larvae before they have
spun cocoons. In addition, more adult sawflies were found in the stomachs of
the few specimens of B. brevicauda than in the larger series of the other two
species. The predation period of this species was of about the same duration
as the others but began and terminated earlier in the season.
Chemical analyses of the stomach contents were conducted to determine the
proteins, carbohydrates, and fats ingested b y shrews (Table VII). Protein
was the dominant component in the stomachs of the three species upon which
analyses were performed. Lipid contents were somewhat lower, but because the
caloric value of fat is more than double that of protein or carbohydrate, the
fat component amounted to 50 to 60% of the total energy value of the stomach
contents. Carbohydrates were the lowest component in the diet, comprising
14 to 18% of the bulk and 8 to 11% of the energy value. The ratio of protein:
carbohydrate:fat in the stomachs was about the same for all species and was
similar to the ratio of these components in insects. This lends further support
to the conclusion that insects form the major portion of the diet of shrews.
The highest caloric values in the stomachs of S. cinereus, S. arcticus, and
B. brevicauda were 0.46, 0.65, and 1.80 respectively and ma y be regarded as
near the capacity for each species. These were 7.5, 9.5, and 18.8% of the total
daily metabolic requirements respectively (Table II), or, alternatively, the
respective species would be required to feed to near capacity 13, 11, and 5
times daily in order to meet their normal metabolic requirements.
TABLE VII
Distribution of the primary food classes and the caloric values of the
contents of shrew stomachs
Mean weight of food class in
stomach (mg)
Species
S. cinereus
S. arcticus
B. brevicauda
No.
stomachs
analyzed
122
62
9
Protein
Carbo-
hydrate
Fat
Mean kcal
content of
stomach
11
17
89
4
6
27
8
12
78
0.13
0.44
1.21
Waste Due to Incomplete Digestion
In order to meet its metabolic requirements, an animal must ingest a larger
amount of food, in terms of caloric value, than its minimum needs because
potentially utilizable material is lost in the feces. The efficiency of digestion
may be determined experimentally by calculating the caloric equivalent of
food consumed and fecal excrement. After an acclimation period of 3 days during which the diet of the experimental animal was converted completely to
TABLE VIII
Daily food consumption by weight and caloric equivalent, and digestive efficiency of four species of shrews
Species
S. cinereus
S.
arclicus
M. hoyi
B.
brevicauda
Av. daily
caloric
equivalent
consumption
Ay. caloric
value of
feces
Cal
metabolized
per day
Percent
efficiency
Food
No. trials*
Av. daily
consumption
Larch sawfly
Dog food
5
5
5.8 (87)t
2.4
6.9
6.3
0.5
0.3
6.4
Larch sawfly
3
1.2
8.6
88
1
2
5
8.2 (123)t
6.5 (98)t
10.0 (150)t
4.2
9.8
Larch sawfly
Larch sawfly
Dog food
7.8
12.01
10.8
1.3
2.6
0 9
6.5
9.4
9.9
83
78
92
*Each trial performed on a separate animal.
1-Figures in parentheses indicate approximate numbers of whole larch sawfly eonymph equivalents.
6.0
93
95
-
274
CANADIAN JOURNAL OF ZOOLOGY. VOL. 42, 1964
test food, the daily food consumption was measured and the daily fecal production was collected and preserved in 70% alcohol for analysis. Two foods were
used: larch sawfly eonymphs with a caloric value of 1.2 per gram, and a commercial canned dog food with a caloric value of 2.6 per gram.
The caloric waste in the feces of the four species of shrews varied considerabl y (Table VIII). Calories metabolized per day were calculated by subtracting the caloric value of the feces from the caloric equivalent consumption
and are in reasonable agreement for three of the four species when compared
with determinations presented earlier (Table II). S. cinereus and B. brevicauda were tested with both larch sawfly eonvmphs and dog food, and in both
cases more efficient use was made of the dog food, although with S. cinereus
the difference was not great. The daily food consumption of larch sawffies by
S. cinereus was about one and one-half times the body weight, whereas with
dog food, consumption was approximately two-thirds the body weight. The
caloric value of the dog food is somewhat higher than that of the larch sawfly,
so it appears that the shrews, under the conditions of this experiment, consumed
only what they required for metabolism. This conclusion was also reached by
Morrison et al. (14) from studies on B. brevicauda. It is of interest to note, however, that S. cinereus under certain conditions ma y consume an amount in
excess of its essential metabolic needs, because when the species was reared at
temperatures between 18 and 24° C, a deposition of fat began accumulating
in the mesentery after about 3 days of captivity.
The efficiency of food assimilation varied from about 78 to 95(,.'," (Table VIII).
Turcek (16), using similar techniques, found that the rodent Apodemus flavicollis (Melch.) assimilated about 90% of its food intake.
The daily metabolic requirements of the animals tested, including fecal
waste, ranged from 87 to 150 larch sawtly eonymphs (Table VI II). 1 lolling
(9) estimated that caged S. cinereus open a maximum of about 100 cocoons of
the European pine sawfly, Neodiprion sertifer (Geoff.), per day.
Food Waste and hoarding in Relation to Prey Density
Exclusive of fecal waste, metabolically utilizable food may also be rejected.
When cocoons of the larch sawfly were presented to shrews, the following
categories of waste were recognized: (a) uneaten fragments, often including the
head capsule, legs, and parts of the thorax; (b) cocoons opened and the
eonvmphs bitten but uneaten; and (c) cocoons containing eonymphs parasitized by B. harveyi. Onl y the first two of these categories will be considered,
as the rejection of parasitized cocoons has been reported previously (3).
Each experimental animal was provided with an excess of larch sawfly cocoons for 3 days prior to each trial. All food was then removed from the cage
and replaced by known quantities of experimental cocoons. Records were made
of wastage in categories (a) and (b), and hoarding. A complete trial consisted
of a series of 24-hour tests at various cocoon densities, the densit y of each test
being chosen at random.
At cocoon concentrations ranging from 100 to 200, waste occurred in category (a) almost exclusively and amounted to a minimum of about 8% of the
total consumption. This remained relatively constant over the entire range of
cocoon abundance and may therefore be considered normal waste for this
-
TABLE IX
Relation between larch sawfly cocoon abundance and wastage and hoarding in four species of shrews.
Data show average number of cocoons wasted and hoarded over a 24-hour period
Species
No. animals
tested
at each
density
S. cinereus
10
S. arcticus
5
M. hoyi
2
B. brevicauda
5
No. cocoons available
Utilization
200
400
600
Wasted
Boarded
Wasted
Boarded
Wasted
Hoarded
\Vasted
Hoarded
14.3
9.7
16.2
0
14.0
5.5
0.6
0
98.1
84.9
104.2
75.2
112.5
62.0
10.8
0
193.4
146.2
200.4
134.2
163.0
63.8
1000
1200
209.6 7 53.6
150.5 156.2
392.6 427.4
172.0 195.6
281.0
120.5
395.4 561.4
189.8 214.0
368.5
164.0
50 7 . 7
209.2
678.2
262.8
800
2000
4000
6000
8000
421.2 591.4
164.8 172.8
515.4 521.8
215.6 219.4
- 486.5
180.0
586.5
165.6
513.4
217.2
573.2
172.3
612.2
223.4
592.9
173.7
589.2
217.4
1500
-
-
276
CANADIAN JOURNAL OF ZOOLOGY. VOL. 42. 1964
ty pe of food. At cocoon quantities in excess of 200, cocoons were opened and
the contents mutilated, but not eaten, more regularly. Thus a progressive
increase in wastage with increasing cocoon densities occurred, so that at
maximum cocoon abundance, wastage was about six times greater than the
metabolic requirements of S. cincreus and over five times that of S. arcticus,
species for which complete data over a wide range were obtained (Table IX).
Incomplete data for the other two species suggest a similar relationship.
Hoarding followed the same general relationship but started later and was
less pronounced.
Discussion
Respiration metabolism studies are usually confined to measurements of
oxygen consumption, occasionally carbon dioxide production, and rarely both,
under the assumption that protein catabolism introduces a negligible error.
Because of the high protein content in the diet of insectivores, care was taken
in these experiments to include an assessment of protein catabolism by means
of urinary nitrogen analysis. The data permit a comparison of the two methods
of calorimetr y . In every case, estimates of the metabolic rate based upon oxygen consumption and carbon dioxide production were higher than estimates
made by including the correction for protein catabolism. However, as the
discrepancies were rarely over 5%, the error involved is generally less than
the variability in metabolism between individuals. For many purposes the
approximation is sufficient, but the more precise values obtained in considering
the entire metabolism are to he favored in studies of metabolic capacities.
The relationship between metabolic rate and population density is interesting. Chitty (6) postulates that a ph y siological density-related mechanism may
operate as a self-governing check on overpopulation. It is possible that increased contact between individuals may cause an increase in metabolic rate
b y overstimulating the adrenaline system, and that this may contribute to the
collapse of unusually high shrew populations. In the autumn of 1957, the rate
of oxygen consumption of resting S. cincreus from areas of unprecedented
populations (over nine shrews per acre) was fully one-third higher than that of
individuals from lower populations, under otherwise identical experimental
situations. Several hundred animals were captured in live traps, and almost
half were dead in the traps although the traps were examined at 2-hour intervals. Only five individuals of the remainder survived over 48 hours in captivity.
Normally, trap survival of the species was about 85%, even when the traps
were visited only once daily, and about sog survived at least a week in
captivity.
The importance of shrews in the natural control of the larch sawfly ma y be
assessed in a manner similar to that used for determining the importance of
birds as predators of this insect (5). Attributes of the predators to be considered
are: (a) the daily metabolic requirements; (b) the caloric equivalent of the
metabolic need, in terms of sawflies; (c) waste due to inefficienc y of digestion,
and to rejection; (d) the percentage of larch sawfly in the natural diet; and
(e) functional responses in wastage and hoarding. The first three of these have
been determined in precise terms in this study (Table VIII). The estimates of
(d) (Fig. 2) were taken during a period of relatively high pre y density and are
TABLE X
Potential utilization of larch sawfly cocoons by shrews on two plots in 1957, calculated from the metabolic requirements in terms of larch
sawfly eonymphs; the relative utilization of larch sawflies in the diet, wastage, hoarding, and predator population
S. cinereus
Metabolic requirement (eonymphs/day)
Fecal waste (eonymphs/day)
Feeding waste (eonymphs/day)
Minimum daily requirement (eonymphs/day)
Percentage larch sawflies in diet
Minimum potential utilization (eonymphs/day)
Waste at high prey density (eonymphs/day)
Hoarding at high prey density (eonymphs/day)
Maximum potential utilization (eonymphs/day)
Minimum potential utilization over 90-day predation
period (eonymphs)
Maximum potential seasonal utilization (eonymphs)
Shrew population/acre, plot I, 1057
Shrew population/acre, plot II, 1957
Potential range of utilization of larch sawfly
cocoons/acre, plot I (eonymphs)
Potential range of utilization of larch sawfly
cocoons/acre, plot II (conymplc;)
82
5
8
95
98%
93
570
170
833
S. arcticus
93
30
10
133
70%
J11. hovi
89
9
9
107
95%
B. brevicauda
131
19
13
163
15%
95
-175
220
790
101
610
180
891
25
125
260
410
8,400
75,000
5.5
9.3
8,600
71,000
1.6
0.2
9,100
80,000
0.3
0.5
2,300
37,000
0.7
0
46,000-413,500
13,700-113,600
2,700-24,000
1,600-25,000
77,800 697,500
1,700-14,200
4,500-40,000
0
273
CANADIAN JOURNAL OF ZOOLOGY. VOL. 42, 1964
probably maximum and subject to revision to account for functional responses
at low prey densities. Measurements on (e) were confined to laboratory studies
(Table IX) and have not yet been related directly to field situations for technical reasons. The 90-day predation period on larch sawfly cocoons (Fig. 2)
was adopted for all predator species as a realistic estimate of the seasonal duration of predation. It is assumed that, in dealing with the hoarding functional
response, all cocoons hoarded are eventually eaten or destroyed, an assumption
based upon empirical data of an earlier study (4).
I have chosen, as an example of the effectiveness of shrews as predators of
larch sawfly cocoons, records obtained in 1957 on the same two plots that were
used in the bird studies. These data are useful for purposes of illustration as
they include significant populations of all species of shrews, and widely divergent prey populations on the two plots. The potential of the various shrews,
shown in Table X, was calculated as outlined.
Estimates of cocoon populations and potential and actual destruction by
shrews per acre on the two plots in 1957 are s y nopsized as follows:
Cocoon population/acre
Potential destruction by shrews/acre Actual destruction by shrews/acre
Plot I
553,000
64,000 -577,000
248,000
Plot II
17,000
84,000-752,000
16,000
Actual destruction of cocoons by shrews falls within the expected range in the
plot with high prey density, but far short in the one with low prey densities.
Obviously shrews could not reach their full potential on the plot with low
numbers of cocoons because there were insufficient cocoons for them to do
so, but the fact that they did not destroy larger numbers reveals a functional
response at low prey densities. Of the four shrew species, S. cinereus exhibited
the highest potential for destroying larch sawfly cocoons, realized a greater
portion of the potential, and maintained higher seasonal and annual
populations.
The role of shrews as predators of the larch sawfly may be compared with
that of birds. Predation of the two groups is additive, because birds prey upon
adults and larvae, whereas shrews prey chiefly on eonymphs. Avian predation
begins early, and shrew predation late in the season, each period coinciding
with seasonal peaks in the prey and predator populations. Shrews are potentially the more effective predators because of their greater individual capacities and their longer predation period. The extent to which their potential is
realized is dependent upon their abundance. Population data obtained over
several years in tamarack bogs in southeastern Manitoba indicate that
shrews, on the average, are less than one-third as abundant as birds. Despite
their lower numbers on the study plots, however, shrews have usually destroyed greater total numbers of sawflies than birds. Although certain avian
species have exhibited a limited numerical response to increasing sawfly
populations, their proportional effectiveness becomes low at even moderate
prey densities. Shrews, on the other hand, have not exhibited a measureable
numerical response to a gradient of prey densities, and the various species
may be abundant, scarce, or absent in tamarack bogs, irrespective of prey
densities. Although shrews have never been totally absent from the study
plots to date, there is a possibility that this could happen, whereas it is un-
BUCKNER: METABOLISM OF SHREWS
279
likely that this could occur with birds. Because of this and the apparent lack
of a density relationship between shrew and sawfly populations, the effectiveness of shrews in the natural control of this forest pest tends to be somewhat
erratic.
BRODY, S. 1945.
BUCKNER, C. H.
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BUCKNER,