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Nordic Society Oikos
Role of Food in Hare Population Cycles
Author(s): Lloyd B. Keith
Source: Oikos, Vol. 40, No. 3, Herbivore-Plant Interactions at Northern Latitudes. Proceedings
of a Symposium Held 14-18 September, 1981, at Kevo, Finland (May, 1983), pp. 385-395
Published by: Blackwell Publishing on behalf of Nordic Society Oikos
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OIKOS 40: 385-395. Copenhagen 1983
Role of food in hare population cycles
Lloyd B. Keith
Keith, L. B. 1983. Role of food in hare population cycles. - Oikos 40: 385-395.
The snowshoe hare has a well-documented 10-yr cycle in North America's Boreal
Forest; the Arctic hare probably has cyclic fluctuations of comparable periodicity,
amplitude and geographic scope within the taiga of USSR. Arctic hare populations
have a 3- to 4-yr cycle in the forests of Norway and Sweden. Fluctuations of
black-tailed jackrabbits in Utah, near the species' northern limit, exhibit an approximate 10-yr periodicity. Cyclic declines in snowshoe and Arctic hare populations
having 10-yr cycles of abundance are likely initiated by food shortage over winter
which lowers reproduction and juvenile survival. Declines in Arctic hares having a 3to 4-yr cycle in Scandinavia appear to be linked to declines in microtine rodents
which cause markedly increased predation on hares and other alternative prey. Declines in the cyclic jackrabbit population of northern Utah are allegedly part of a
predator-prey oscillation with coyotes. In neither of the latter two fluctuations is food
shortage involved. Both cyclic and noncyclic hare populations may become food
short at high densities. It is proposed that the 10-yr cycle is dampened or replaced by
irregular fluctuations where snowshoe habitat is fragmented and insular because: (1)
the greater structural (niche) diversity of fragmented habitats increases prey species
diversity, and hence the stability and facultative nature of predator populations; and
(2) the resulting sustained predation on dispersing hares blocks potential increases in
distribution and density. Thus it may be the character of predation, as molded by
habitat factors, that primarily determines the regularity of snowshoe hare fluctuations. This is likely also true for other species of hares. Because snow cover effectively
protects vegetation from browsing by snowshoe and Arctic hares, the impact of
varying snow depth on overwinter food supplies may be highly significant to hare
populations at or near cyclic peaks.
L. B. Keith, Dept of Wildlife Ecology, Univ. of Wisconsin, Madison, WI 53706, USA.
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Accepted 11 October 1982
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385
1. Introduction
2.2. Arctichares
Certain mammals and birds of northern regions exhibit
marked multi-annual fluctuations that are both periodic
and synchronous over large geographic areas. Increasingly sophisticated analyses (Bulmer 1974, Finerty
1980) of long-available population indices have convincingly affirmed what seemed intuitively evident to
many earlier workers - a 3- to 4-yr cycle in microtine
rodents and a 10-yr cycle in the snowshoe hare Lepus
americanus. Each oscillation is tracked by a number of
largely obligate predators, and by tetraonids that are
ecologically linked through common predators, food
sources, etc. to microtine and hare populations.
The snowshoe hare cycle has stimulated discussion
and speculation among biologists for approximately 60
yr (Hewitt 1921, Elton 1924), and was recognized by
fur traders at least 100 yr earlier (Elton and Nicholson
1942). Numerous theories and hypotheses about the
cycle were reviewed by Keith (1963) and Finerty
(1980); there is currently no general agreement as to its
cause(s).
The specific aim of the present paper is to assess
whether food plays a role in generating cyclic fluctuations of snowshoe and/or other hare populations.
Three species of Arctic hares are currently recognized:
L. timidus (Arctic, blue, snow or mountain hare) of
northern Europe and Asia; L. othus (tundra hare) of
western Alaska; and L. arcticus (Arctic hare) of northern Canada and Greenland. These alleged species are
very closely related (Howell 1936, Ognev 1940) and are
here simply called Arctic hares. An important ecological distinction, however, is that timidus occupies both
tundra and forest habitats, whereas othus and arcticus
are restricted to tundra. L. timidus is thus the ecological
counterpart of North America's Arctic and snowshoe
hares.
There are no long-term indices to fluctuations of L.
timidus in Eurasia that compare with those available for
L. americanus in North America. Nevertheless, a multitude of field observations and some short-term indices
of abundance led Formozov (1935) to conclude that L.
timidus populations exhibit an approximate 9- to 10-yr
cycle in northern regions, but a shorter cycle of about 6
220
0
34 -
LEPUS TIMIDUS
(NORTHWESTERN U.S.S.R.)
U)
I
2. Occurrence of cyclic and noncyclic hare
populations
Implicit in the term "cycle", as applied to wildlife
populations, is the idea of regularity. While such cycles
are never perfectly regular, they are significantly more
so than are other fluctuations.
In this section I attempt to identify cyclic hare populations, and briefly describe their periodicity, amplitude
and synchrony.
180
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1920
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2.1. Snowshoehare
The snowshoe hare inhabits the Boreal Forest of North
America, and has long been considered a classic cyclic
species. Its periodicity is mainly 8 to 11 yr (Keith 1963);
measured amplitudes of change have exceeded 100-fold
within good habitat, and 10- to 30-fold changes are
common (Keith 1981). The cycle is broadly synchronized over a vast area from Alaska to Newfoundland, with regional peaks or lows rarely differing by
more than 3 yr (Keith 1963).
Cyclic fluctuations are dampened or disappear where
snowshoe habitat becomes fragmented through plant
succession or agricultural clearing (Buehler and Keith
1982). The fragmented habitats of mountainous regions
have apparently never supported cyclic populations
(Keith 1963).
386
60
F
40
I
20 1
0
cn
u. I
z
0
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1856
1866
1876
1886
1896
1906
Fig. 1. Fluctuationsof Arctichares(Lepustimidus)withinthe
taigaof the Soviet Union as depictedby annualharvests(Formozov 1935, Naumov1947, 1960); and fluctuationsof snowshoe hares(L. americanus)in the Boreal Forestnear Hudson
Bay, Canada(MacLulich1957).
OIKOS 40:3 (1983)
yr further south. Naumov (1947) supported this conclusion with additional population indices, and noted
that the shorter-term fluctuations to the south were
much less regular. He associated 8- to 12-yr fluctuations
with ". . . the taiga zones of Europe, Siberia, and the
Siberian forest-steppe . . .", and 4- to 9-yr fluctuations
with ". .. regions of the mixed and insular forest zones
and the European forest-steppe".
I have compared (Fig. 1) the 3 longest sets of population indices that are available for L. timidus (Formozov
1935, Naumov 1947, 1960) with those for L.
americanus (MacLulich 1957). The periodicity and regularity of these major fluctuations appear similar, and
strongly suggest that timidus, like americanus, has a
"10-yr cycle". The indices for L. timidus depict fluctuations that occurred within the taiga zone of northwestern and northeastern USSR. This apparent cycle of L.
timidus resembles that of L. americanus in two other
respects: the amplitude of change is reportedly marked
(20- to 50-fold, Formozov 1935); and population peaks
occur synchronously over large areas (Naumov 1947).
The long-term cycle of L. timidus contrasts sharply
with fluctuations recorded in the northern forests of
Scandinavia (Fig. 2). These peak at mostly 3- to 4-yr
intervals and, as discussed later, seem to be linked to the
existing microtine cycle. The 2- to 7-fold amplitudes of
change are probably less than for timidus in the USSR,
but neither this aspect nor the degree of inter-area synchrony is well documented (Hornfeldt 1978, Lindlof
and Lemnell 1981).
Indices to Arctic hare fluctuations elsewhere provide
little evidence of cyclic changes. Hunting-kill estimates
from two estates in Finland spanned about 80 yr, and
depicted irregular short-term fluctuations with mean
intervals between all apparent peaks of approximately 3
yr (Siivonen 1948). On the other hand, kill data from
Scotland (Middleton 1934, Hewson 1955, 1965, 1976)
showed major long-term fluctuations with little sugges250
25
200
20
.
Co
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tion of regularity or inter-area synchrony. Measured
amplitudes of fluctuation, 2 to 10-fold, were comparable to those in Scandinavia (Watson and Hewson 1973,
Hewson 1976). Characteristics of Arctic hare fluctuations in North America and Greenland are virtually unknown. A 42-yr record of pelt shipments from Alaska
(L. othus) suggests long-term fluctuations of high
amplitude (Buckley 1954). General observations of L.
arcticus point to large annual variations in density on
Canada's Arctic islands (Howell 1936, Bonnyman
1975).
2.3. Black-tailedjackrabbit
The black-tailed jackrabbit occupies arid and semi-arid
deserts and grasslands of the western United States and
Mexico. Its fluctuations have often been marked
(Palmer 1897, Nelson 1909), and recent studies indicate a regularity within northern sections of its range.
Thus Gross et al. (1974) concluded:
"... there is variationin synchronybetweenlocalizedareas
... yet, there has been sufficientsimilarityover this broad
region[UtahandsouthernIdaho]to stampthe early1950's,
the late 1950's, and the late 1960's or early 1970's as the
highdensityyears.The amplitudeof variation[9-fold]during our study has evidentlybeen less than that commonly
reportedfor the snowshoehare."
I have compared jackrabbit population trends on an
intensive study area in Utah during 1963-1980 with
those of a cyclic snowshoe hare population in Alberta
during 1961-77 (Fig. 3). This comparison, together
with the general historical trend cited above, suggests
that the Utah jackrabbit population is also cyclic.
2.4. Otherhares
The European hare (L. europaeus) is the only other
species for which indices are adequate to classify fluctuations. These were reviewed by Keith (1981) and interpreted as indicating irregular and short-term (2-4 yr)
changes in numbers. The white-tailed jackrabbit
occupies much of the northern prairies of the United
States and Canada. Nothing is known of its population
fluctuations, and very little of other aspects of demography.
2.5. Synopsis
0
I
Cyclic fluctuations of mainly 8 to 11 yr occur among
snowshoe hares occupying more or less continuous
(nonfragmented) habitat within the Boreal Forest
,
I
I
1945
1950
1955
960
1965
1
1
(taiga) of North America. A cycle of similar length
1945
1950
1955
1960
1965
1970
1975
probably occurs among Arctic hares in the taiga of the
Fig. 2. Fluctuationsof Arctic hares (Lepus timidus) in the Soviet Union. In each case fluctuations are of high
northerntaigaof Norway(solidline) andSweden(dashedline)
as depicted by annual harvests (Moksnes 1972, Hornfeldt amplitude (> 10-fold) and broadly synchronized within
1978). Arrowsindicatereportedyearsof peak microtinenum- large geographic regions. In the northern forests of
bers.
Norway and Sweden, Arctic hare fluctuations are much
z
50
OIKOS 40:3 (1983)
387
Vaughan and Keith 1981), together with other field
studies of shorter duration (see Keith and Windberg
1978: 50-52, Wolff 1980), disclosed that the cyclic
pattern is generated by a predictable sequence of birthand survival-rate changes.
The decline from peak autumn densities is initiated
by sharply lower overwinter survival of juveniles; adult
survival is not notably reduced until 1 or 2 yr later. A
major decrease in the birth rate immediately precedes
and/or follows that in juvenile survival, and accentuates
the population decline. Both juvenile survival and reproductive rates remain low for 2 or 3 yr, then recover
over a period of 2 or 3 yr; reproduction improves more
rapidly than juvenile survival. Onset of the next cyclic
increase in numbers is evoked by marked rises in both
juvenile and adult survival, reproduction having already
fully recovered.
600
LEPUS AMERICANUS
500
:
z
y
400
UJ
L
300
I
,
a
0
n
200
100
o
z
0
1960
1965
1970
1975
300
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a:
|
LEPUS CALIFORNICUS
250
3.1.2. A conceptual model
In 1971 I presented a conceptual model of the snowshoe hare cycle which was later summarized by Keith
and Windberg (1978):
z
x
o
200
z
Q
150
Z
< 100
oc
y
II
50
0
1965
1970
1975
1980
"... the cycleis repeatedlygeneratedintrinsicallythrougha
hare-vegetationinteraction(dominantherbivorevs. winter
food supply)that triggersthe populationdecline.This elevates the predator-hareratio,therebyintensifyinga second
interactionthat extendsthe periodof declineanddrivesthe
hare populationstill lower. The grouse are cyclic due to
varyingratesof predatorinducedmortality- a spin-offfrom
the hare-predatorinteraction.Interregionalsynchronyis
causedbasicallyby mildwintersthat moderatemortalityin
peakharepopulations,andpermitothersthatarelaggingto
attainpeakdensities.Suchsynchronyis reinforcedby highly
mobile predatorpopulations."
Fig. 3. Fluctuationsof snowshoehares(Lepusamericanus)on
intensivestudy areasnear Rochester,Alberta,Canada(Keith
et al. 1977, L. B. Keith, unpubl.)and black-tailedjackrabbits
(L. californicus)in CurlewValley,Utah, USA (L. C. Stoddart,
unpubl.).
Both the hare-vegetation and predator-hare interactions have the strong delayed-density-dependent attributes that can promote and sustain oscillations. The
shorter-termed and of lower amplitude: prominent cyc- successive population changes and the relative biolic peaks occur at chiefly 3- to 4-yr intervals, as do those masses involved are outlined in Fig. 4.
in associated microtine populations. Black-tailed jackrabbits probably have a cycle of around 7 to 10 yr in 3.1.3. Role of food
The cornerstone of the foregoing model is a hare-winter
Utah near the northern limit of their range.
in
marked
food interaction, evidence of which will now be
fluctuations
sometimes
be
may
Although
other hare species, and in other populations of the examined. In this and later sections I use the term
"food" in a strictly quantitative sense - as something
above-mentioned cyclic species, they are either noncyclic (e.g. European hare, Arctic hare in Scotland) or providing hares with energy.
The overwinter (6-8 month) diet of cyclic snowshoe
there are insufficient data on which to make a judgement (e.g. white-tailed jackrabbit, Arctic hares in North hare populations is predominantly woody vegetation the terminal twigs of various shrubs and small trees. In
America and Greenland).
November 1970, at the outset of a winter of peak hare
densities, we began to measure food supplies on study
3. Cause(s) of cyclic fluctuations
areas in central Alberta. Food was insufficient to suphare populations in this peak winter and the winter
port
3.1. Snowshoe hare
following, and there was probably also food shortage
3.1.1. General demography
during the third winter (Pease et al. 1979). This was the
Cyclic snowshoe hare populations in central Alberta, first quantification of food shortage during a cyclic peak
and decline. Subsequently, Wolff (1980) showed that
Canada, were studied intensively for 17 yr (1961-77).
This work (Keith et al. 1977, Keith and Windberg 1978,
snowshoe populations in interior Alaska had also ex388
OIKOS 40:3 (1983)
250
little evidence of a density effect on any demographic
attribute of these experimental populations.
In summary, there is good evidence - direct, indirect,
and experimental - that peak snowshoe hare populations become short of food over winter; and that this
produces the characteristic sequence of demographic
responses which initiates cyclic declines.
100
3.2. Arctichares
0Sooo
26000
-
25>0
-
/
WOODYBROWSE
(WINTER
FOODFOR HARES)
1 ooo
500
-j
HARES
SNOWSHOE
SO
3.2.1. Soviet Union
As noted earlier, available indices suggest that Arctic
25
hare populations within the Russian taiga have cyclic
RUFFEDGROUSE
fluctuations comparable in periodicity, amplitude and
synchrony to those of snowshoe hares in Canada. It is
thus logical to anticipate that other aspects of their
population dynamics are similar, including the role of
winter food shortage in triggering cyclic declines.
1.00
Both Formozov (1935) and Naumov (1947) largely
PFEDATORS
0.50
discounted the idea that cyclic Arctic hare populations
usually declined from food shortage. Instead, they re025
peatedly emphasized the role of "epizootics", especially
parasitic, as primary causes of mortality. This seems
6
7
9
10
11
12
4
8
5
1
2
0
3
-1
questionable to me because it is often malnutrition that
YEARS
predisposes mammals to conspicuous losses from
Fig. 4. Fluctuationsin relativebiomassof majorcomponentsof parasitic disease. Furthermore, obvious and widespread
the 10-yr cycle as observednear Rochester,Alberta,Canada
destruction of woody vegetation by high Arctic hare
(Keith et al. 1977, Pease et al. 1979, L. B. Keith, unpubl.).
populations is apparently common (Formozov 1935):
ceeded their food supplies during 2-3 peak and postpeak winters.
Annual midwinter-to-spring weight losses among
hares were interpreted as providing strong indirect evidence of periodic food shortage in Alberta (Keith and
Windberg 1978). Such weight losses were greater during the 3 successive winters of known food shortage and
population decline than during the next 3 winters when
food was ample (8.5-10.3% vs. 3.0-5.8%). There was
an apparent cyclic trend in such weight losses during
1963-76, and a significant correlation with reproduction and juvenile growth rates.
To test the hypothesis that midwinter-to-spring
weight losses, reproduction, and juvenile growth reflected overwinter nutrition, Vaughan and Keith (1981)
experimentally manipulated winter food supplies of
captive snowshoe populations. The results of this experiment were wholly consistent with the above-stated
hypothesis: hares in food-scarce treatments exhibited
greater overwinter weight loss, and markedly lower reproduction during the subsequent breeding season.
Growth rates of young born to parents from food-scarce
treatments were also lower. Parameter values in all 3
cases closely approximated those previously observed in
declining wild populations. Adult survival was only
slightly reduced by food scarcity, but juvenile survival
dropped sharply - a situation comparable to that noted
during the first year or two of a cyclic decline. There was
24
OIKOS 40:3 (1983)
"Therewere so manyof them [hares]that there was not a
singlebushwithoutone in it. Aspens,birchesandwillowsup
to a centimetreand a half thick have been completelydevoured."
"... in years in which the white hare is few in number,
willowthickets,youngaspens,aldersand bircheshave time
to grow and re-establishthemselves,after being generally
completelydestroyedby haresin yearsin whichtheirnumbersare at a maximum(I tracedthis re-establishment
of the
winter food base of the white hare very thoroughlyin
SharinskDistrictoverthe years1930-34, afterall the young
shoots of edible specieshad been destroyedby the animals
in 1927-28.)."
These accounts are reminiscent of early descriptions of
severe browsing by peak snowshoe hare populations
(Seton 1911, Soper 1921, MacLulich 1937, etc.). But as
pointed out by Grange (1965) and Pease et al. (1979),
food shortage may exist without such conspicuous damage because it is the most inconspicuous parts of the
browsable vegetation that comprise the essential food
resource, i.e. the small terminal twigs produced largely
during the previous growing season.
Popov (1960) measured the quantity of browse available to Arctic hares in Yakutia, and concluded:
"A comparisonof food requirementsand reservesshows
that at the onset of hare populationdecline in 1954, there
was no lack of food, such that would have led directlyto
hare deaths due to starvation,but food reserveswere limited, which rendereddifficult any possibilityof further
growthof the snow hare population."
389
Hornfeldt (1978) modified Keith's (1974) conceptual
model of the snowshoe hare cycle to fit the Swedish
ecosystem: thus voles replaced snowshoes as the dominant herbivore in successive herbivore-winter food
and herbivore-predator interactions, and the Arctic
hare was added to the tetraonids as a species suffering
higher predation rates (predator shift) and hence declining after the dominant herbivore (i.e. voles) had
crashed due to food shortage.
Field studies at Grims6, which began in 1974, were
designed to test this same model of population change.
According to Lindlof (1980) amplitudes of change in
both vole and hare populations are less pronounced at
Grimso than further north in Sweden, and the
chronological relationship between their fluctuations
was not clear. Angelstam et al. (in press) and Lindstrom
et al. (unpubl.) also reported a low-amplitude fluctuation at Grims6, but noted that hare density changes
followed the vole cycle with a lag of 1 yr. Lindstrom et
"'Everynow and then incursionsof haresoccuron such a al.
(unpubl.) further concluded that hare mortality rates
large scale that they attractattentionby destroyingshrubs
vegetationandeven the grass.Thisoccurred,for instance,in decreased when vole numbers rose, and increased when
1914 when vast tractsof willows,poplarsand aspenswere voles declined. The same 1-yr lag that occurred in the
destroyedin VerkhoyanskDistrict ... from the mouth of hare decline likewise occurred among foxes (Vulpes
the river Yana to the Aldan [1000 km] I saw trees and
shrubsin some placesthat had been strippedby these vor- vulpes) - the hares' chief predator (Lindstrom unpubl.).
The credibility of the above model in explaining the
aciousrodents."'
short-cyclic fluctuations of these hares is further enPredation has likewise been stressed as a mortality fac- hanced by their reported densities of only 1-4 ind km-2
tor by Soviet workers (Formozov 1935, Naumov 1947),
(Lindlof and Lemnell 1981, Lindstrom et al. unpubl.),
or less than 10 hares per fox (Lindstrom unpubl.).
mainly concomitant with epizootics. The delayed-denLindlof and Lemnell (1981) pointed out that hare
sity-dependence, or lag, in predator population redensities at Grimso were 1/100 of those on an island off
sponse to snowshoe hare declines (Keith et al. 1977)
also occurs among the chief predators of Arctic hares the Swedish west coast, where food resources were evi(Labutin 1960, Naumov 1972).
dently poorer. They suggested that food was, therefore,
The only solid demographic data that I have seen not likely limiting the growth of the hare population at
published on Arctic hares in the Soviet Union deal with Grimso. I am inclined to agree with them.
reproduction (Naumov 1947). Mean litter size varies
with the stage of the cycle, decreasing during the peak
3.3. Black-tailedjackrabbit
year or year following, and remaining low throughout
most of the period of population decline. This relation- The cyclic black-tailed jackrabbit population in Curlew
ship is also typical of snowshoe hares (Keith and Valley, Utah (Fig. 3), has been studied intensively since
Windberg 1978: 50-52, Cary and Keith 1979), and has 1962, and much is known of its demography and inbeen interpreted by me as reflecting the food shortage teraction with food and predators.
A demographic summary covering the period
that besets peak and declining populations. Naumov
(1947) likewise ascribed such reproductive variation to 1962-70 (Gross et al. 1974) revealed two characterisnutrition, but in a qualitative (vitamin) rather than tics of this jackrabbit population which indicate to me
that food shortage likely played no significant role in its
quantitative (energy) sense.
The obvious parallels between cyclic fluctuations of population dynamics: (1) annual variations in natality
Arctic hares in USSR and snowshoe hares in North were small (< 20% of the 8-year mean); and (2) both
America suggest that their cyclic declines have a com- annual survival of juveniles and variation in annual survival were similar to that of adults. As I described earmon basis - food shortage.
lier, snowshoe hares respond to food shortage with
3.2.2. Norway and Sweden
major decreases in reproduction and highly differential
The largely 3- to 4-yr cyclic fluctuations of Arctic hares losses of young.
in Norway and Sweden have been investigated at
Clark (1981) and Clark and Innis (unpubl.) examined
Grimso in central Sweden, but not to my knowledge the interaction between jackrabbits and their food reelsewhere. The most evident ecological correlate with sources in Curlew Valley. The general conclusion from
this hare cycle is a periodic fluctuation among mic- a simulation of this interaction (Clark and Innis unrotines occupying these same northern forests (Fig. 2). publ.) was that "... the observed declines from populaPopov's (1960) data indicated that the total biomass of
browse available at the hare peak might have barely
supported the population if about equally apportioned
among all individuals - a highly improbable event. That
the interaction between the hare populations and its
winter food supply became critical was seen in Popov's
report that by spring 1954 90% of the hares were in
poor nutritional condition. Over this same winter, the
population allegedly declined more than 90% from 60
km-2 in autumn to 5.4 km-2 by spring.
Frequent reports of mass movements of Arctic hares
during years of high population provide additional evidence of food shortage. This association is well
documented among other species (Lack 1954); and in
referring to a peak year, Formozov (1935) stated: "In
winter when hares are as abundant as this, food begins
to get short and the animals begin to move and undertake migrations." He also cited an observer who wrote:
390
OIKOS 40:3 (1983)
tion peaks, characteristic of this oscillatory population,
must be caused by some ecological mechanism other
than food resource depletion." In all but the poorest
production years jackrabbits consumed less than 5% of
available net primary production (Clark 1981).
On the other hand, Wagner and Stoddart (1972) reported that year-to-year changes in mortality (which
accounted for 85% of the variation in rates of population growth) were largely a function of coyote (Canis
latrans) predation. And, more recently, Stoddart (1978)
concluded ". .. with the observed functional and numerical response of the coyote population to jackrabbit
density, and with jackrabbit behavioral changes, the
general trend of the observed jackrabbit 'cycle' can be
accounted for by coyote predation." If Stoddart's appraisal is correct, this jackrabbit-coyote interaction
would appear to be the first documented example of a
classic predator-prey oscillation in wild vertebrates.
3.4. Synopsis
A predictable syndrome of birth- and survival-rate
changes, resulting from overwinter food shortage, initiates cyclic declines of snowshow hares in North
America. There is strong circumstantial evidence that
declines of Arctic hare populations having a 10-yr cycle
in the Soviet Union are also triggered by food shortage.
Predation becomes the dominant mortality factor
among snowshoes only after their initial food-related
decline has greatly increased predator-hare ratios; the
same is likely also true for Arctic hares.
The much shorter 3- to 4-yr cycle of Arctic hares in
Norway and Sweden is probably due to varying rates of
predator-caused mortality. The short-cyclic fluctuations
of microtines control predator numbers and diet, and
the relatively low-density hare populations are especially sensitive to such factors. There is no evidence that
food shortage plays a significant role in this hare cycle.
The approximate 10-yr cycle of black-tailed jackrabbits in northern Utah, USA, is generated demographically by cyclic changes in annual mortality. These
changes are not caused by nutrition but allegedly by
predation, with coyotes and jackrabbits interacting to
produce a predator-prey oscillation.
4. Discussion
4.1. The basis of food shortageamonghares
I earlier cited evidence that the quantity or biomass of
available browse has been inadequate to support peak
populations of snowshoe and Arctic hares overwinter.
There are two other aspects of hare browse - species
diversity and chemical composition - that must also be
considered because they influence hare nutrition and
hence conclusions about the adequacy of natural food
supplies. Feeding trials have established that neither
snowshoe nor Arctic hares can long survive on a single24* OIKOS 40:3 (1983)
species diet (Bookhout 1965, Pehrson 1980, J. P.
Bryant, pers. comm.). A mix of two or more woody
browse species is evidently essential; and a large
biomass of browse, if consisting largely of one species,
may not indicate food abundance. Thus hares may
starve in the midst of apparent plenty if browse-species
diversity is lacking. Such diversity tends to be low within
extensive willow (Salix) and black spruce (Picea
mariana) monotypes in North America, and likewise
within birch (Betula) and larch (Larix) forests of
Eurasia. Selective feeding by hares during population
highs may likewise reduce browse diversity.
Chemical responses by woody plants to browsing by
both snowshoe and Arctic hares are well documented
(Pehrson 1980, Bryant 1981a). Bryant (1981a,b) demonstrated that adventitious shoots produced after severe browsing contain elevated levels of terpene and
phenolic resins which make them extremely unpalatable
to snowshoe hares. He also suggested that because such
resins repel even food-short hares, browsing-induced
chemical defenses may play a role in the 10-yr cycle.
The most likely effect would be to reduce supplies of
usable browse during the population decline (following
severe browsing which occurs at cyclic peaks), and
thereby extend the period of food shortage.
4.2. The problemof noncyclicfluctuations
Noncyclic snowshoe hare populations occur where
suitable habitat (i.e. a dense understory of woody
shrubs and saplings) is highly fragmented. This fragmentation exists naturally in mountain ranges, and
along the southern limit of snowshoe distribution. It
may also develop where fire suppression has permitted
forests to mature beyond the successional stage at which
hare habitat is more or less continuous (Buehler and
Keith 1982). Agricultural clearing, which physically
fragments habitat, markedly reduces the amplitude of
cyclic fluctuations relative to that occurring on adjacent
uncleared land (Windberg and Keith 1978).
Buehler and Keith (1982) hypothesized that:
". .. cyclicfluctuationsof snowshoeharesarenot generated
where forest cover may be extensiveif areas of low dense
woody vegetation therein are widely separated and island-like.This is because dispersersfrom these islandsof
favorablehabitatareremovedby a relativelystationaryand
abundantcomplexof facultativepredators,thus effectively
negatingboth expandeddistributionand local increasesin
density. Such hare populationsare therebyprimarilyregulatedwithincomparativelynarrowlimitsby the interaction
of habitat,dispersalandpredation.On the otherhand,large
blocks of favorablehabitatprovide a matrixof food and
cover which is more conduciveto survivalof dispersers.
This, coupled with recurrentscarcityof predatorswhose
markedfluctuationsstem from their dependencyon hares,
permitsthe scatteredpocketsof snowshoesremainingafter
a cyclic decline to expand and coalesce as numbersbuild
towardanotherpeak. The next significanthare-predation
interactionoccursonly after food shortagehas greatlyreduced haresfrom peak abundance."
391
Tab. 1. Peakseasonaldensitiesof snowshoeharesin cyclicandnoncyclicpopulationsas determinedfromestimatorsthatrequired
trappingand markingof individualson intensivestudyareas.
Studyarea location
CentralAlberta (continoushabitat) ..
InteriorAlaska ....................
InteriorAlaska ....................
CentralAlberta(fragmentedhabitat)
NorthernNew York ...............
WesternOregon...................
NorthernMinnesota ...............
WesternMontana .................
New Brunswick ...................
CentralColorado..................
NorthernMichigan ................
NorthernUtah ....................
Haresper km2
Type of long-term
of habitat
fluctuations
exhibitedby hare
Autumn
Spring
population*
cyclic
cyclic
cyclic
cyclic
noncyclic
noncyclic
cyclic
noncyclic
noncyclic
noncyclic
cyclic
noncylic
1288 (Nov)**
609 (Aug)**
592 (Oct)
554 (Nov)**
454 (Sep)***
395 (Oct)
163 (Sep)
479 (Apr)
192 (Apr)
294 (Apr)
230 (Mar)
184 (Feb)
161 (Mar)
159 (Apr)
73 (Apr)
62 (Apr)
46 (Apr)
Reference
Keith and Windberg(1978)
Ernest(1974)
Trapp(1962)
Windbergand Keith (1978)
Crisseyand Darrow(1949)
Black (1965)
Green and Evans (1940)
Adams (1959)
Wood and Munroe(1977)
Dolbeer and Clark(1975)
Bookhout(1965)
Dolbeer and Clark(1975)
* There are sufficientlong-termindicesto establishthat populationshere designatedas cyclicare, or have been so, up to the
time of the study;populationshere designatedas noncycliclack long-termindices,but on the basisof generalobservations,
have been long considerednoncyclic.
** Populationknownto have become shortof food overwinter(Pease et al. 1979, Wolff 1980, Windbergand Keith 1978).
*** Descriptionof impactof harepopulationon woodyvegetationoverwinter(Cook and Robeson 1945) stronglysuggeststhat
food shortagebroughtabout the populationdecline.
A similar view of habitat structure, dispersal, and predation interacting to prevent cyclic fluctuations of
snowshoe hares was recently outlined by Wolff (1980,
1981), and discussed at length by Finerty (1980).
Lidicker's (1975) conception of "presaturation dispersal" and of a "dispersal sink" are obviously highly relevant to this model.
Wagner (1981) indicated that fluctuations of blacktailed jackrabbits decrease in amplitude and regularity
from northern Utah to southern Arizona. This he ascribed to increased biotic diversity - in particular, a
predator complex that has more species, is largely
facultative, and fluctuates less. These changes greatly
reduce the interdependency between rate of jackrabbit
increase and state (level) of predator population, and
vice versa, that Wagner believed necessary to generate
cycles. The altered character of predation in cyclic vs.
noncyclic jackrabbit populations, as described by
Wagner, clearly parallels that deemed significant also in
dampening snowshoe fluctuations.
Although sustained facultative predation seems to be
the paramount limitation on noncyclic snowshoe hare
populations, one cannot rule out recurrent food shortage within occupied islands of habitat. Field data (Tab.
1) do not, in fact, support the widespread supposition
that maximum densities attained by noncyclic populations are well below those at cyclic peaks. There has
been, for example, considerable overlap in highest
spring densities of noncyclic (46-230 km-2) and cyclic
(62-479 km-2) populations; and, the autumn density of
at least one noncyclic population (395 km-2) approached that of two cyclic populations (554 and 609
392
km-2) in which overwinter food shortage was measured.
Furthermore, snowshoes on Valcour Island, New York,
rose to a peak of 454 km-2 in September 1943, following 3 yr of intensive predator control (Tab. 1). Destruction of woody vegetation on Valcour overwinter
1943-44 (Cook and Robeson 1945), and the occurrence of only 17 predator kills among 112 hare carcasses found in spring 1944 (Crissey and Darrow 1949),
suggests to me that acute food shortage was responsible
for the population crash.
The role of food in noncyclic fluctuations of Arctic
hares is even more difficult to assess because: (1) density estimates for noncyclic populations are unavailable,
other than in Scotland; and (2) evident high-amplitude
fluctuations outside the taiga in the Soviet Union and in
Alaska may or may not be cyclic - the data are insufficient to be certain. In any case, there are strong indications that where high densities are attained food shortages sometimes occur: Scotland (Hewson 1965, Moss
and Miller 1976); Baltic Islands (Hakkinen and Jokinen
1981); Soviet Union (Formozov 1935); and perhaps
Alaska (Grauvogel 1981). Weather conditions affecting
food quality and accessibility reportedly aggravate or
precipitate shortages of food at high densities in Scotland.
The above-cited snowshoe and Arctic hare data suggest that noncyclic populations may also suffer densitydependent food shortages; hence, the occurrence of a
hare-food interaction does not in itself guarantee cyclic
fluctuations. An obvious major difference between cyclic and noncyclic populations lies in the character of
predation, as dictated by habitat structure and species
diversity.
OIKOS 40:3 (1983)
Finerty (1980) apparently reached a similar conclusion through loop analysis (italics mine);
DEC
NOV
JAN
FEB
MAR
APR
1963-64
20
"Biological information and community structure ...
suggest that the role of predatorsis to create the type of
3
process."
zO
functional dispersal sink that sets the stage for the cyclic
r,
mh
--
i
(0
0
C)
4.3. Significanceof snow to winterfood supply
Snow is an integral part of northern environments, and
hindfoot size and coat-color change in the snowshoe
and Arctic hare are obviously adaptations to snow. In
some regions Arctic hares burrow into snow for shelter
(Ognev 1940, Flux 1970, Hakkinen and Jokinen 1974);
my impression is that this is less common in forest
habitats than on the tundra or other open landscapes.
Burrowing by snowshoe hares, a forest dweller, is extremely rare.
Although Arctic hares may dig and gnaw through
crusted snow to obtain food (Manniche 1910), there is a
strong inference in the literature that most vegetation
covered by snow is largely unavailable to them (Hewson
1965, 1976, Pulliainen 1972, Bonnyman 1975). I have
never seen snowshoes dig for food, nor have I encountered reports of such behavior. If Arctic and snowshoe
hares are primarily dependent upon exposed browse, it
then seems important to examine the impact of snow
depth on overwinter food supply. This question becomes especially significant where snowfall varies markedly from year to year, and cyclic declines in hare
populations are initiated by winter food shortages - i.e.
in the Boreal Forest or taiga.
Accounts of snowfall providing new sources of
browse by elevating hares or weighing down vegetation
are common (Bider 1961, Pruitt 1970, Pulliainen
1972). To assess the net effect of increasing snow depth,
however, one must also know how much food becomes
buried and hence unavailable. This will depend importantly on the vertical profile of browse biomass. We
were able to estimate this variable from field measurements of hare browse in central Alberta, and then
model effects of between-year variations in snow depth
on relative availability of browse overwinter. In that
largely-deciduous sector of the Boreal Forest, typical of
prime snowshoe habitat and characterized by strongly
cyclic populations, hare browse was so concentrated
near ground level that as little as 50 cm of snow reduced
available biomass by 60%. According to our model,
annual extremes in snow accumulation alone could have
produced a 2-fold difference in the amount of browse
available to hares overwinter (Fig. 5).
Such variation might easily determine the nutritional
status of near-peak hare populations and thus whether
or not they begin to decline. Where total annual snowfall tends to be similar over large geographic regions, as
for example within the Boreal Forest of North America,
comparatively snow-free winters occurring during the
OIKOS 40:3 (1983)
40
20
0.8-
0.3.
W
&!'>?
0.5
0.5-
o0I
cI
-
i
o.4-
0.3
I
.
196364
.
.
. --- I
. I.
.
196869
.
197374
III
.
.
.
Fig. 5. Extremes in winter snow depths observed near
Rochester,Alberta,Canada,1961-77; and the calculatedeffect of snow depth on overwinteravailabilityof browse(hare
food) presentin autumn(J. R. Cary,unpubl.).
increase phase of a hare cycle may promote inter-area
synchrony by permitting already high populations to
persist while lagging ones continue to grow toward a
critical food shortage.
There is certainly a need to determine how food
availability for hares is affected elsewhere by changing
snow depth.
Acknowledgements - I am very grateful to those persons who
generouslypermittedme to cite their unpublisheddata and
manuscripts. Especially notable in this regard were E.
Lindstromand L. C. Stoddart.The translationsby S. Postupalskyof papersin Russianon Lepustimiduswere extremely
useful.
References
Adams, L. 1959. An analysisof a populationof snowshoe
hares in northwesternMontana. - Ecol. Monogr. 29:
141-170.
Angelstam,P., Lindstrom,E. and Widen,P. Cyclicshiftingof
predation and other interrelationshipsin a south taiga
small game community. - Trans. Int. Congr. Game
Biologists14: (in press).
Bider, J. R. 1961. An ecological study of the hare Lepus
americanus. - Can. J. Zool. 39: 81-103.
393
Black, H. C. 1965. An analysisof a populationof snowshoe
- and Jokinen,M. 1981. Populationdynamicsof the mountain hare (Lepus timidus) on an island in the outer arOregon.- Ph.D. thesis, OregonState Univ.
chipelagoof SWFinland.- In: Myers,K. andMaclnnes,C.
D. (eds), Proc.WorldLagomorphConf.,Univ. of Guelph,
Bonnyman,S. G. 1975. Behaviouralecologyof Lepusarcticus.
- M.S. thesis, CarletonUniv.
pp. 469-477.
Bookhout,T. A. 1965. The snowshoeharein upperMichigan. Hewitt,C. G. 1921. The conservationof wild life in Canada.- Mich.Conserv.Dep., Res. and Develop, Report 38.
Schribner's,New York.
Bryant,J. P. 1981a. The regulationof snowshoehare feeding Hewson, R. 1955. The mountainhare in Scotlandin 1951. behaviorduringwinterby plantantiherbivorechemistry.Scott. Nat. 66: 70-88.
- 1965. Populationchanges in the mountainhare, Lepus
In: Myers, K. and Maclnnes, C. D. (eds), Proc. World
timidus L. - J. Anim. Ecol. 34: 587-600.
LagomorphConf., Univ. of Guelph,pp. 720-731.
- 1981b. Phytochemical deterrence of snowshoe hare
- 1976. A population study of mountain hares (Lepus
browsingby adventitiousshoots of four Alaskantrees. timidus) in north-east Scotland from 1956-1969. - J.
Science213: 889-890.
Anim. Ecol. 45: 395-414.
Buckley,J. L. 1954. Animalpopulationfluctuationsin Alaska Hornfeldt,B. 1978. Synchronouspopulationfluctuationsin
- a history.- Trans.N. Am. Wildl.Conf. 19: 338-357.
voles, smallgame,owls, andtularemiain northernSweden.
- Oecologia(Berl.) 32: 141-152.
Buehler,D. andKeith,L. B. 1982. Snowshoeharedistribution
and habitatuse in Wisconsin.- Can. Field-Naturalist96: Howell,A. B. 1936. A revisionof the AmericanArctichares.
- J. Mammal.17: 315-337.
19-29.
Bulmer,M. G. 1974. A statisticalanalysisof the 10-yearcycle Keith,L. B. 1963. Wildlife'sten-yearcycle.- Univ. Wisconsin
in Canada.- J. Anim. Ecol. 43: 701-718.
Press,Madison.
- 1974. Some featuresof populationdynamicsin mammals.
Cary,J. R. and Keith,L. B. 1979. Reproductivechangein the
- Proc. Int. Congr.Game Biol. 11: 17-58.
10-year cycle of snowshoe hares. - Can. J. Zool. 57:
- 1981. Populationdynamicsof hares.- In: Myers,K. and
375-390.
Clark,W. R. 1981. Role of black-tailedjackrabbitsin a North
Maclnnes, C. D. (eds), Proc. World LagomorphConf.,
Americanshrub-steppeecosystem.- In: Myers, K. and
Univ. of Guelph,pp. 395-440.
- andWindberg,L. A. 1978. A demographicanalysisof the
Maclnnes, C. D. (eds), Proc. World LagomorphConf.,
Univ. of Guelph,pp. 706-719.
snowshoehare cycle. - Wildl.Monogr.No. 58.
- , Todd,A. W., Brand,C. J., Adamcik,R. S. andRusch,D.
- andInnis,G. S. Forageinteractionsandjackrabbitpopulation dynamics:a simulationmodel.- Submittedto J. Wildl.
H. 1977. An analysisof predationduringa cyclicfluctuation of snowshoehares.- Proc.Int. Congr.GameBiol. 13:
Manage.
151-175.
Cook, D. B. and Robeson,S. B. 1945. Varyinghareandforest
succession.- Ecology 26: 406-410.
Labutin,Y. V. 1960. Predatorsas a factorin snow harepopulation changes.- In: Naumov,S. P. (ed.), Investigations
Crissey,W. F. and Darrow,R. W. 1949. A studyof predator
controlon ValcourIsland.- New YorkStateConservation
into the causes and regularitiesof snow hare population
Dep., Div. Fish Game, Res. Ser. No. 1.
dynamicsin Yakutia.Acad. SciencesU.S.S.R., Yukatian
Branchof SiberianSection:Acad. SciencesPress,Moscow.
Dolbeer, R. A. and Clark,W. R. 1975. Populationecologyof
snowshoeharesin the centralRockyMountains.- J. Wildl.
(In Russian.Translationby S. Postupalsky,for Dept of
WildlifeEcology,Univ. of Wisconsin,Madison).
Manage.39: 535-549.
Elton, C. 1924. Periodicfluctuationsin the numbersof ani- Lack, D. 1954. The naturalregulationof animalnumbers.mals: their causes and effects. - Brit. J. Exper. Biol. 2:
OxfordUniv. Press,Oxford.
119-163.
Lidicker,W. S. 1975. The role of dispersalin the demography
- andNicholson,M. 1942. The ten-yearcycle in numbersof
of smallmammals.- In: Golley, F. (ed.), Smallmammals:
the lynx in Canada.- J. Anim. Ecol. 11: 215-244.
their productivityand population dynamics.Cambridge
Univ. Press,Cambridge.
Ernest,J. 1974. Snowshoeharestudies.- FinalReport,Alaska
FederalAid in Wildl.Restoration,Proj.W-17-4,5,6.
Lindlof,B. 1980. Someaspectsof ecologyin hares.- Summary
of Ph. D. thesis, Univ. of Stockholm.
Finerty,J. P. 1980. The populationecology of cyclesin small
- and Lemnell,P. A. 1981. Differencesin islandand mainmammals.- Yale Univ. Press,New Haven.
land populationsof mountainhare. - In: Myers,K. and
Flux,J. E. C. 1970. Life historyof the mountainhare (Lepus
timidus scoticus) in north-east Scotland. - J. Zool. 161:
MacInnes,C. D. (eds), Proc. World LagomorphConf.,
75-123.
Univ. Guelph,pp. 478-485.
Formozov, A. N. 1935. Fluctuations in the numbers of MacLulich,D. A. 1937. Fluctuationsin the numbersof the
economicallyexploited animals.- All-Union Coop. Unvarying hare (Lepus americanus). - Univ. Toronto Stud.,
ified Publ. House, Moscow and Leningrad,108 pp. (In
Biol. Ser. No. 43.
- 1957. The place of chance in populationprocesses.- J.
Russian.Translationby J. D. Jackson,for Bureauof Animal Population,OxfordUniv., England.).
Wildl.Manage.21: 293-299.
Grange, W. B. 1965. Fire and tree growth relationshipsto Manniche,A. L. V. 1910. The terrestrialmammalsand birds
snowshoerabbits.- Proc. AnnualTall TimbersFire Ecol.
of north-eastGreenland.- Meddr.Gronland45: 1-200.
Conf. 4: 110-125.
Middleton,A. D. 1934. Periodicfluctuationsin Britishgame
progress
Grauvogel,C. A. 1981. Smallgamesurvey-inventory
populations.- J. Anim. Ecol. 3: 231-249.
hos smaviltarteri
report,GMU 22. - In: Hinman,R. A. (ed.), AnnualRe- Moksnes,A. A. 1972. Bestandsvingninger
- Naturen5: 315-319.
Activities.AlaskaFederalAid in
Trollheimsomradet.
portof Survey-Inventory
Wildl. Restoration,Proj.W-17-12.
Moss, R. and Miller, G. R. 1976. Production,dieback and
Green, R. G. and Evans,C. A. 1940. Studieson a population
grazingof heather(Callunavulgaris)in relationto numbers of red grouse (Lagopus 1. scoticus) and mountain
cycle of snowshoehareson the Lake Alexanderarea.- J.
Wildl.Manage.4: 220-238.
hares (Lepus timidus) in north-east Scotland. - J. appl.
Ecol. 13: 369-377.
Gross,J. E., Stoddart,L. C. and Wagner,F. H. 1974. Demographicanalysisof a northernUtah jackrabbitpopulation. Naumov, S. P. 1947. Ecology of the snow-hare.- Moscow
- Wildl. Monogr. No. 40.
Societyof Naturalists'Press,Moscow.(In Russian.Translation by S. Postupalsky,for Dept of Wildlife Ecology,
Hikkinen, I. and Jokinen,M. 1974. On the winterecology of
the snow hare (Lepustimidus)in the outer archipelago.Univ. of Wisconsin,Madison).
SuomenRiista 25: 5-14.
hares, Lepus americanus washingtonii Baird, in western
394
OIKOS 40:3 (1983)
- 1960. Generalregularitiesof the species' populationand
its dynamics.- In: Naumov,S. P. (ed.), Investigationsinto
the causes and regularities of snow hare population
dynamicsin Yakutia.Acad. SciencesU.S.S.R., Yakutian
Branchof SiberianSection:Acad.SciencesPress,Moscow.
(In Russian. Translationby S. Postupalsky,for Dept of
WildlifeEcology,Univ. of Wisconsin,Madison).
- 1972. The ecology of animals.- Univ. IllinoisPress, Urbana.
Nelson, E. W. 1909. The rabbitsof North America.- U.S.
Dept. Agric., Bur. Biol. Surv.,No. Am. Fauna29.
Newson, R. and DeVos, A. 1964. Populationstructureand
body weights of snowshoe hares on ManitoulinIsland,
Ontario. - Can. J. Zool. 42: 975-986.
Ognev, S. I. 1940. Mammalsof the U.S.S.R and adjacent
countries.- Vol. 4, Rodents. (In Russian.Translationby
the Israel programfor scientific translations,Jerusalem,
1966).
Palmer,T. S. 1897. The jackrabbitsof the United States. U.S. Dept. Agric., Div. Biol. Serv.
Pease,J. L., Vowles, R. H. and Keith,L. B. 1979. Interaction
of snowshoeharesandwoodyvegetation.- J. Wildl.Manage. 43: 43-60.
Pehrson,A. 1980. Intakeand utilizationof winterfood in the
mountain hare (Lepus timidlu L.) - a laboratory investiga-
tion. - Summaryof Ph.D. thesis, Univ. of Stockholm.
Popov, M. V. 1960. Food conditionsand their significanceto
populationdynamics.- In: Naumov,S. P. (ed.), Investigations into the causesand regularitiesof snow harepopulation dynamics in Yakutia. Acad. Sciences (U.S.S.R.,
Yakutian Branch of Siberian Section: Acad. Sciences
Press,Moscow.(In Russian.Translationby S. Postupalsky,
for Dept of WildlifeEcology, Univ. of Wisconsin,Madison).
Pruitt,W. 0. 1970. Some ecologicalaspectsof snow. - Proc.
HelsinkiSymposium(UNESCO),Ecologyof the Subarctic
Regions,pp. 83-99.
Pulliainen, E. 1972. Nutrition of the arctic hare (Lepus
timidus)in NortheasternLapland.- Ann. Zool. Fennici9:
17-22.
Seton, E. T. 1911. The Arcticprairies.- Int. Univ. Press,New
York.
OIKOS 40:3 (1983)
Siivonen, L. 1948. Structureof short-cyclicfluctuationsin
numbersof mammalsandbirdsin the northernpartsof the
northern hemisphere.- Finnish Foundationfor Game
Preservation,Paperson Game ResearchNo. 1.
Soper,J. D. 1921. Notes on the snowshoerabbit.-J. Mammal.
2: 101-108.
Stoddart,L. C. 1978. Populationdynamics,movementsand
homerangeof black-tailedjackrabbits(Lepuscalifornicus)
in Curlew Valley, northernUtah. - Final Report U.S.
Dept. Energy.ContractNo. E11-1-1229.
Trapp,G. R. 1962. Snowshoeharesin Alaska;II, home range
and ecology duringan early populationincrease.- M.S.
thesis, Univ. of Alaska.
Vaughan,M. R. andKeith,L. B. 1981. Demographicresponse
of experimentalsnowshoehare populationsto overwinter
food shortage.- J. Wildl.Manage.45: 354-380.
Vozeh, G. E. and Cumming,H. G. 1962. A moose population
census and winter browse survey in Gogama District,
Ontario.- Report,Ont. Dept. Landsand Forests.
Wagner,F. H. 1981. Role of lagomorphsin ecosystems.- In:
Myers, K. and Maclnnes, C. D. (eds), Proc. World
LagomorphConf., Univ. of Guelph,pp. 668-694.
- andStoddart,L. C. 1972. Influenceof coyote predationon
black-tailedjackrabbitpopulationsin Utah. - J. Wildl.
Manage.36: 329-342.
Watson, A. and Hewson, R. 1973. Populationdensities of
mountainhares (Lepus timidus)on westernScottishand
Irishmoorsandon Scottishhills.-J. Zool. 170: 151-159.
Windberg,L. A. and Keith,L. B. 1978. Snowshoeharepopulationsin woodlothabitat.- Can.J. Zool. 56: 1071-1080.
Wolff,J. 0. 1980. The role of habitatpathcinessin the population dynamicsof snowshoehares. - Ecol. Monogr.50:
111-130.
- 1981. Refugia, dispersal, and geographic variation in
snowshoeharecycles.- In: Myers,K. andMaclnnes,C. D.
(eds), Proc.WorldLagomorphConf.,Univ. of Guelph,pp.
441-449.
Wood, T. J. and Munroe,S. A., 1977. Dynamicsof snowshoe
harepopulationsin the MaritimeProvinces.- Can. Wildl.
Serv., OccasionalPaperNo. 30.
395