Journal of Mammalogy, 82(1):1–21, 2001

IMPORTANCE OF BIOGEOGRAPHY AND ONTOGENY OF WOODY

PLANTS IN WINTER HERBIVORY BY MAMMALS

ROBERT K. SWIHART* AND JOHN P. BRYANT

Department of Forestry and Natural Resources, Purdue University,

West Lafayette, IN 47907-1159 (RKS)
Institute of Arctic Biology, University of Alaska, Fairbanks, AK 99775 (JPB)

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Mammals can influence growth, reproduction, competitive ability, and survival of woody
plants by virtue of selective browsing and gnawing of dormant shoots during winter. Ap-
parently in response to this type of herbivory, plants have evolved chemical and mechanical
deterrents to mammalian herbivores. We report on plant ontogeny and biogeography, which
exert their influence on herbivory at different spatiotemporal scales. To evaluate how plant
ontogeny influences herbivory, we conducted a meta-analysis of 128 studies, encompassing
37 plant and 10 mammal species, in which juvenile and mature growth stages of conspecific
plants were made available to mammals during winter in temperate and northern latitudes.
Mammals ate more of the mature-stage growth in 96% of the studies, and stage-specific
differences in consumption were very large (d1 5 2.16). Plants characterized by rapid
growth rates or low tolerances to resource limitation elicited the greatest degree of stage-
specific discrimination by mammals, consistent with existing theories regarding tradeoffs
governing plant growth and defense. The influence of a plant’s growth rate and tolerance
to resource limitation was dependent on climatic regime; plants grown in areas with harsh
winter conditions tended to elicit greater discrimination of juvenile- and mature-stage
growth by mammals than plants grown in more moderate climates. Further evidence for
biogeographical variation in mammalian consumption came from 14 feeding studies, in-
cluding 6 plant and 6 mammal species, that compared conspecific plants of the juvenile
growth stage either grown or collected at different localities. In 86% of the studies, extent
of herbivory by mammals varied inversely with latitude, and this yielded a moderate effect
(Z1 5 20.46, r1 5 20.53). We discuss potential roles of life history, climate, and historical
association of plants and mammals in shaping these biogeographical patterns.

Key words: biogeography, development, herbivory, latitude, mammals, secondary chemistry, win-
ter, woody plants

In terrestrial ecosystems from temperate riculture and forestry as a consequence of

to polar latitudes, mammals are the domi-
nant group of herbivores during winter.
Several orders of mammals depend upon
woody plants as important sources of en-
ergy and nutrition in winter, relying on fer-
mentation systems in the digestive tract to
process roots, cambium, shoots, or buds
(Robbins 1993; Van Soest 1982). Of prac-
tical concern is the damage incurred in ag-
* Correspondent: rswihart@fnr.purdue.edu
winter herbivory by mammals (Conover et
al. 1995; Gill 1992; Swihart and Conover
1990). Winter herbivory by mammals also
is of interest because mammals can alter
growth, reproduction, competitive ability,
survival, and perhaps other fitness compo-
nents of woody plants (Buckley et al. 1998;
Healy 1997; Kielland and Bryant 1998;
Tilghman 1989). Ultimately, feeding by
mammals can alter the composition and
successional trajectories of plant commu-

1
2 JOURNAL OF MAMMALOGY
nities (Bryant and Chapin 1986; Kielland
and Bryant 1998; Pastor and Naiman 1992;
Ritchie et al. 1998).
Browsing mammals during winter tend
to be polyphagous, yet they exhibit clear
preference and avoidance of certain plants,
that is, they are selective generalists (Bry-
ant and Kuropat 1980; Swihart and Yahner
1983). Most descriptive studies of winter
diets of mammalian herbivores have ex-
amined variation in consumption of several
species of plants from a single locality. In
those studies relating dietary choices to
chemical characteristics of plants, differen-
tial consumption of plants seldom seems to
be based solely on energy or nutrient con-
tent (Basey et al. 1990; Rousi 1990). More-
over, mammals often respond negatively to
secondary metabolites when making dietary
choices (Bryant and Kuropat 1980; Palo
and Robbins 1991).
In light of the potential impacts of mam-
malian herbivory, an important goal of
managers and ecologists is to identify fac-
tors that influence dietary choices. These
factors typically function as constraints, ei-
ther on use of plants by herbivores or on
defense of plants from herbivory. Con-
straints are manifested as genetic tradeoffs
resulting from physiologic, ecologic, and
evolutionary processes (Herms and Mattson
1992). These processes span an array of
scales in space (e.g., microclimate, geo-
graphic range) and time (e.g., bite rate, his-
tory of species associations). Mammals
seem capable of exerting considerable se-
lective pressure on woody plants to evolve
defenses to deter winter herbivory. Indeed,
heritable, intraspecific variation in deterrent
capabilities has been documented for sev-
eral mammal–woody plant interactions
(Chiba and Nagata 1976; Dimock et al.
1976; Rousi 1990; Rousi et al. 1991, 1997;
Silen et al. 1986). We examined the impor-
tance of plant ontogeny and biogeography,
which exert their influence on herbivory at
different spatiotemporal scales.
Ontogeny as used here refers to tightly
regulated developmental changes that take
Vol. 82, No. 1
place during a plant’s life. Maturation or
phase change refers to relatively rapid and
predictable ontogenetic changes occurring
early in the life cycle of a woody plant and
characterizing its transition to a sexually re-
producing adult (Kozlowski 1971). A sim-
ilar but slightly broader concept that incor-
porates physiologic alterations during plant
development has been termed the develop-
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mental stream (Kearsley and Whitham
1998). Developmentally based changes in
plant–herbivore interactions have received
relatively little attention from ecologists,
but results in well-studied systems indicate
the need for closer examination. Experi-
ments have demonstrated strong effects of
plant development on insect herbivores of
cotton (Gossypium hirsutum—Karban and
Thaler 1999) and cottonwoods (Populus
sp.—Kearsley and Whitham 1989, 1998).
Other studies have demonstrated strong,
chemically based effects of plant develop-
ment on winter herbivory of hares (Lepus)
in subarctic taiga (Bryant 1981a, 1981b;
Bryant et al. 1985).
Basic life-history considerations and em-
pirical studies of plant population dynamics
suggest that selection for plant defense
against herbivores is greatest in the juvenile
(pre–sexually reproductive, sensu Kozlows-
ki 1971) stage (Watkinson 1986). Although
the notion is not new that plant develop-
mental stage may influence investment in
defense (Bryant 1981a; Bryant et al.
1983a), the generality and strength of its
effect on mammalian herbivory has not
been examined. We reviewed published
comparisons of stage-specific differences in
consumption of winter-dormant shoots by
mammals, combined these with results
from our unpublished work over the last
several years, and used meta-analysis to test
the null hypothesis that plant ontogeny has
no influence on patterns of consumption of
woody plants. We also tested whether se-
lected physiologic, morphologic, and life-
history attributes explain additional varia-
tion in consumption by mammals.
Even less is known about geographic
February 2001 SWIHART AND BRYANT—WINTER HERBIVORY
ecology of mammalian herbivory. Attempts
to generalize findings on winter dietary
choices of mammals from 1 locality to an-
other have met with limited success (Swi-
hart and Yahner 1983; Wolff 1978). In ad-
dition to obvious effects due to differences
in relative availability of plants at different
localities, we believe that constraints oper-
ating on resident plants and mammals could
differ across large spatial scales. We ex-
plored this possibility in 2 ways. First, we
tested whether geographic differences in or-
igins of woody plants, categorized accord-
ing to classes of winter severity, explained
significant levels of variation in discrimi-
nation by mammals when offered shoots
from plants at different stages of ontogeny.
Second, we reviewed published studies of
feeding experiments in which juvenile-
stage growth was offered from conspecific
plants either growing in different geograph-
ic areas or grown in a common environment
from seed collected in different areas. We
then tested for a latitudinal trend in those
data using meta-analysis and proposed pos-
sible explanations for patterns that we ob-
served.
MATERIALS AND METHODS
Sources of data.—Data for testing patterns of
consumption as related to plant ontogeny were
derived from studies in which mammalian her-
bivores were provided with a choice of winter-
dormant juvenile- and mature-stage growth, and
consumption of each type was measured subse-
quently. Although details varied among studies,
2 general protocols were followed. In some stud-
ies, juvenile and mature growth forms were pre-
sented in equal (or nearly equal) amounts to
mammals in cafeteria-style feeding trials involv-
ing several plant species simultaneously (e.g.,
Klein 1977). In other studies, juvenile and ma-
ture growth were presented simultaneously to
mammals in trials involving a single plant spe-
cies (e.g., Bryant et al. 1985). Of the 2 protocols,
the latter provided a less variable assay of dis-
crimination by mammals as a function of plant
ontogeny because interspecific influences on
consumption were absent. Studies also differed
in whether they relied upon captive or free-rang-
3
ing test subjects. When captive subjects were
used, each usually received its own plant mate-
rial, and consumption thus reflected per capita
use, subject to the constraints of interpreting re-
sults from trials with captive mammals. When
free-ranging mammals were used, .1 individual
could potentially visit any given test station pro-
visioned with juvenile- and mature-stage
growth. Under free-ranging conditions, con-
sumption values did not necessarily reflect per
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capita use. Moreover, independence of stations
cannot be assured under free-ranging conditions,
although most studies spaced stations far enough
apart to minimize the likelihood that a single
mammal would visit .1 station during a test pe-
riod (e.g., Bryant 1981b).
Our review of the literature provided suitable
data from 19 published studies on relative con-
sumption of juvenile- and mature-stage growth
of winter-dormant woody plants by mammals;
those studies included feeding trials involving
82 combinations of mammals and woody plants
(Table 1). We supplemented those data with pre-
viously unpublished feeding trials with which
we have been involved over the past 2 decades.
Those trials involved 46 combinations of mam-
mals and woody plants; most of those trials test-
ed plant species singly. Thus, our total database
for examining patterns of consumption related
to plant ontogeny included 128 sets of trials,
conducted with 37 different species of plants
and 10 species of mammals (Table 1).
For each set of feeding trials, we also cate-
gorized woody plants according to growth rate
(slow, medium, fast), tolerance to resource lim-
itation (principally to limitation of light: low,
medium, high), growth form (shrub ,2 m tall,
shrub .2 m tall, tree), and leaf type (deciduous,
evergreen). Classifications were made after con-
sulting Fowells (1965), Harlow and Harrar
(1969), Loehle (1988), Tutin et al. (1964, 1968),
and Viereck and Little (1972). For species not
covered by those sources (usually shrubs or trees
of little commercial value), levels of categories
were assigned based on our personal knowledge
or after consulting forest ecologists from the re-
gion where the species of plant was tested. We
further categorized sets of trials according to the
digestive strategy of the herbivore involved
(foregut or hindgut fermentation). Finally, for
each feeding experiment, we classified the geo-
graphic locality from which the plant material
was collected according to severity of winter
 4

TABLE 1.—Feeding experiments used to test hypotheses regarding effects of plant ontogeny on mammalian herbivory during winter. Acronyms
for categories of plant attributes are listed sequentially as follows: growth rate (F 5 fast, M 5 medium, S 5 slow)–tolerance to stress (L 5 low,
M 5 medium, H 5 high)–leaf type (D 5 deciduous, E 5 evergreen)–growth form (T 5 tree, H 5 shrub .2 m, L 5 shrub ,2 m)–severity of
winter temperatures (V 5 very severe, S 5 severe, M 5 moderate, Mi 5 mild). See text for discussion of variables used in meta-analysis. NA 5
not available.

Categories of Xj/(Xj
Plant Mammal plant attributes di 1 Xm) nj nm Source
Acer rubrum Lepus americanus M-L-D-T-M 0.81 0.43 6 6 Current study
A. rubrum Odocoileus virginianus M-L-D-T-M 0.49 0.35 4 4 Current studya
Alnus crispa Clethrionomys rutilus M-H-D-H-V 1.91 0.15 10 10 Current studyb
A. crispa Dicrostonyx groenlandicus M-H-D-H-V 4.27 0.11 10 10 Current studyb
A. crispa L. americanus M-H-D-H-V 2.73 0.03 5 5 Bryant (1981b)
A. crispa L. americanus M-H-D-H-V 1.56 0.19 25 25 Bryant et al. (1983b)
A. crispa L. americanus M-H-D-H-V 14.82 0.19 30 30 Current study
A. crispa L. americanus M-H-D-H-V NA 0.48 5 5 Clausen et al. (1986)
A. crispa L. americanus M-H-D-H-V NA 0.19 10 10 Clausen et al. (1986)
A. crispa L. americanus M-H-D-H-V 3.63 0.20 4 4 Klein (1977)
A. crispa Microtus pennsylvanicus M-H-D-H-V 1.52 0.21 10 10 Current studyb
Alnus incana L. americanus M-H-D-H-V 11.64 0.17 30 30 Current study
Betula alleghaniensis L. americanus M-M-D-T-M 0.08 0.49 7 7 Swihart et al. (1994)
B. alleghaniensis L. americanus M-M-D-T-M 1.16 0.39 10 10 Swihart et al. (1994)
B. alleghaniensis L. americanus M-M-D-T-M 20.04 0.50 8 8 Swihart et al. (1994)
B. alleghaniensis L. americanusc M-M-D-T-M 3.98 0.31 8 8 Current study
JOURNAL OF MAMMALOGY

Betula glandulosad L. americanus M-H-D-L-V 4.18 0.10 30 30 Current study

Betula lenta L. americanus F-M-D-T-M 0.16 0.47 7 7 Swihart et al. (1994)
B. lenta L. americanus F-M-D-T-M 0.38 0.48 5 5 Swihart et al. (1994)
B. lenta L. americanus F-M-D-T-M 20.12 0.52 7 7 Swihart et al. (1994)
B. lenta L. americanusc F-M-D-T-M 2.22 0.39 8 8 Current study
B. lenta O. virginianus F-M-D-T-M 10.97 0.00 2 2 Current studya
Betula papyrifera L. americanus F-L-D-T-M 1.14 0.44 5 5 Swihart et al. (1994)
B. papyrifera L. americanus F-L-D-T-M 1.69 0.09 7 7 Swihart et al. (1994)
B. papyrifera L. americanus F-L-D-T-M 0.98 0.33 9 9 Swihart et al. (1994)
B. papyrifera L. americanusc F-L-D-T-M 14.38 0.05 8 8 Current study
Betula pendula Alces alces M-M-D-T-M 1.43 0.20 13 17 Danell et al. (1990)
B. pendula Lepus timidus M-M-D-T-S 6.38 0.13 10 10 Bryant et al. (1991)
B. pendula L. timidus M-M-D-T-S 3.65 0.18 10 10 Bryant et al. (1989)
B. pendula Microtus agrestis M-M-D-T-M 0.61 0.38 12 12 Danell et al. (1987)
Betula pubescens A. alces M-M-D-T-M 0.60 0.29 12 15 Danell et al. (1990)
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 TABLE 1.—Continued.

Categories of Xj/(Xj
Plant Mammal plant attributes di 1 Xm) nj nm Source
February 2001

B. pubescens L. timidus M-M-D-T-S 1.82 0.29 10 10 Bryant et al. (1991)

B. pubescens M. agrestis M-M-D-T-M 2.76 0.16 10 10 Danell et al. (1987)
Betula resinifera L. timidus F-L-D-T-V 6.45 0.00 10 10 Bryant et al. (1989)
B. resinifera A. alces F-L-D-T-V NA 0.07 20 20 Reichardt et al. (1984)
B. resinifera C. rutilus F-L-D-T-V 1.70 0.02 10 10 Current studyb
B. resinifera D. groenlandicus F-L-D-T-V 371.90 0.00 10 10 Current studyb
B. resinifera L. americanus F-L-D-T-V 19.11 0.08 5 5 Bryant (1981b)
B. resinifera L. americanus F-L-D-T-V 339.54 0.03 30 30 Current study
B. resinifera L. americanus F-L-D-T-V 8.22 0.07 5 3 Klein (1977)
B. resinifera L. americanus F-L-D-T-V 2.35 0.01 10 10 Reichardt et al. (1984)
B. resinifera L. americanus F-L-D-T-V 8.40 0.02 10 10 Reichardt et al. (1984)
B. resinifera L. americanus F-L-D-T-V 46.71 0.01 100 100 Reichardt et al. (1984)
B. resinifera L. americanus F-L-D-T-V 11.63 0.12 4 8 Current studye
B. resinifera L. americanus F-L-D-T-V 1.82 0.00 8 8 Current study
B. resinifera M. pennsylvanicus F-L-D-T-V 2.50 0.02 10 10 Current studyb
B. resinifera 3 glandulosa L. americanus F-L-D-H-V 9.38 0.05 30 30 Current study
Juniperus virginiana O. virginianus S-L-E-T-M 2.26 0.18 7 7 Swihart and Picone (1998)
Kalmia latifolia L. americanus S-M-E-H-M 0.07 0.49 6 6 Current study
Larix laricinad L. americanus M-H-D-T-V 11.05 0.38 30 30 Current study
Picea glauca L. americanus M-H-E-T-V NA 0.18 5 5 Bryant (1981b)
P. glauca L. americanus M-H-E-T-V 7.26 0.19 30 30 Current study
P. glauca L. americanus M-H-E-T-V 1.92 0.24 4 4 Klein (1977)
P. glauca L. americanus M-H-E-T-V 10.72 0.06 3 3 Sinclair and Smith (1984)
P. glauca L. americanus M-H-E-T-V 16.64 0.04 3 3 Sinclair and Smith (1984)
P. glauca L. americanus M-H-E-T-V 1.95 0.10 6 8 Current studye
SWIHART AND BRYANT—WINTER HERBIVORY

P. glauca L. americanus M-H-E-T-V 7.60 0.10 3 2 Current studye

P. glauca L. americanus M-H-E-T-V 1.92 0.11 4 4 Current studye
Picea mariana L. americanus S-H-E-T-V 2.51 0.39 5 5 Bryant (1981b)
P. mariana L. americanus S-H-E-T-V 2.43 0.32 30 30 Current study
P. mariana L. americanus S-H-E-T-V 1.42 0.18 4 4 Klein (1977)
Pinus radiata Lepus californicus F-M-E-T-Mi NA 0.14 49 49 Libby and Hood (1976)
Pinus sylvestris L. timidus M-M-E-T-S NA 0.00 5f 5f Rousi et al. (1987)
Populus balsamifera C. rutilus F-L-D-T-V 2.37 0.02 10 10 Current studyb
P. balsamifera D. groenlandicus F-L-D-T-V 1.71 0.03 10 10 Current studyb
P. balsamifera L. americanus F-L-D-T-V 4.86 0.02 5 5 Bryant (1981b)
5

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 6

TABLE 1.—Continued.

Categories of Xj/(Xj
Plant Mammal plant attributes di 1 Xm) nj nm Source
P. balsamifera L. americanus F-L-D-T-V 12.42 0.05 30 30 Current study
P. balsamifera L. americanus F-L-D-T-V 0.01 0.48 4 4 Klein (1977)
B. balsamifera L. americanus F-L-D-T-V 11.06 0.04 6 6 Reichardt et al. (1990)
B. balsamifera L. americanus F-L-D-T-V 6.28 0.01 3 3 Sinclair and Smith (1984)
B. balsamifera L. americanus F-L-D-T-V 7.72 0.02 3 3 Sinclair and Smith (1984)
B. balsamifera L. americanus F-L-D-T-V 2.46 0.16 5 6 Current studye
B. balsamifera M. Pennsylvanicus F-L-D-T-V 0.75 0.02 10 10 Current studyb
Populus grandidentata L. americanus F-L-D-T-M 20.44 0.58 8 8 Swihart et al. (1994)
P. grandidentata L. americanus F-L-D-T-M 20.56 0.58 5 5 Swihart et al. (1994)
P. grandidentata L. americanus F-L-D-T-M 1.04 0.28 5 5 Swihart et al. (1994)
P. grandidentata L. americanus F-L-D-T-M 20.31 0.55 7 7 Swihart et al. (1994)
Populus tremuloides L. americanus F-L-D-T-V 7.24 0.03 5 5 Bryant (1981b)
P. tremuloides L. americanus F-L-D-T-V 41.20 0.21 30 30 Current study
P. tremuloides L. americanus F-L-D-T-V 13.28 0.15 5 3 Klein (1977)
P. tremuloides L. americanus F-L-D-T-M 0.75 0.34 7 7 Swihart et al. (1994)
P. tremuloides L. americanus F-L-D-T-M 2.68 0.05 4 4 Swihart et al. (1994)
P. tremuloides L. americanus F-L-D-T-M 0.30 0.44 9 9 Swihart et al. (1994)
P. tremuloides L. americanus F-L-D-T-M 2.06 0.17 5 5 Swihart et al. (1994)
P. tremuloides L. americanus F-L-D-T-V 2.41 0.25 2 3 Current studye
Pseudotsuga menziesii Odocoileus hemionus F-M-E-T-S 1.53 0.01 4 4 Dawson et al. (1990)
P. menziesii O. hemionus columbianus F-M-E-T-Mi NA 0.34 8 8 Silen et al. (1986)
JOURNAL OF MAMMALOGY

Salix alaxensis C. rutilus F-L-D-H-V 12.05 0.13 10 10 Current studyb

S. alaxensis D. groenlandicus F-L-D-H-V 1.92 0.34 10 10 Current studyb
S. alaxensis L. americanus F-L-D-H-V 3.49 0.10 10 10 Bryant et al. (1985)
S. alaxensis L. americanus F-L-D-H-V 21.93 0.04 10 10 Bryant et al. (1985)
S. alaxensis L. americanus F-L-D-H-V 7.60 0.32 5 5 Bryant et al. (1985)
S. alaxensis L. americanus F-L-D-H-V 3.43 0.02 9 9 Bryant et al. (1989)
S. alaxensis L. americanus F-L-D-H-V 20.18 0.25 30 30 Current study
S. alaxensis L. americanus F-L-D-H-V 17.29 0.06 3 3 Sinclair and Smith (1984)
S. alaxensis L. americanus F-L-D-H-V 11.81 0.11 3 3 Sinclair and Smith (1984)
S. alaxensis L. americanus F-L-D-H-V 0.00 0.20 7 8 Current studye
S. alaxensis L. americanus F-L-D-H-V 7.09 0.06 10 8 Current studye
S. alaxensis L. timidus F-L-D-H-V 1.42 0.50 10 10 Bryant et al. (1989)
S. alaxensis M. pennsylvanicus F-L-D-H-V 4.49 0.29 10 10 Current studyb
Salix arbusculoides L. americanus M-M-D-H-V 0.27 0.35 3 3 Current studye
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 TABLE 1.—Continued.

Categories of Xj/(Xj
Plant Mammal plant attributes di 1 Xm) nj nm Source
February 2001

S. arbusculoides L. americanus M-M-D-H-V 8.39 0.07 30 30 Current study

S. arbusculoides L. americanus M-M-D-H-V 1.66 0.17 2 2 Klein (1977)
Salix bebbiana L. americanus M-L-D-H-V NA 0.04 5 5 Bryant (1981b)
S. bebbiana L. americanus M-L-D-H-V 44.30 0.05 30 30 Current study
S. bebbiana L. americanus M-L-D-H-V 17.12 0.10 2 2 Klein (1977)
Salix brachycarpa L. americanus M-M-D-H-V 10.22 0.06 30 30 Current study
Salix caprea L. americanus F-L-D-T-S 8.08 0.22 9 9 Bryant et al. (1989)
S. caprea L. timidus F-L-D-T-S 2.01 0.34 2 2 Bryant et al. (1991)
S. caprea L. timidus F-L-D-T-S 9.12 0.25 10 10 Bryant et al. (1989)
S. caprea L. timidus F-L-D-T-S 16.86 0.18 3 3 Tahvanainen et al. (1985)
Salix glauca L. americanus M-M-D-H-V 11.32 0.08 3 3 Sinclair and Smith (1984)
S. glauca L. americanus M-M-D-H-V 6.02 0.26 3 3 Sinclair and Smith (1984)
Salix lasiandra L. americanus F-L-D-H-V 14.16 0.09 30 30 Current study
Salix myrsinifolia phylicifolia M. agrestis F-L-D-H-M 1.77 0.21 9 9 Danell et al. (1987)
Salix nigricans L. timidus F-L-D-H-S 8.26 0.10 3 3 Tahvanainen et al. (1985)
S. nigricans L. timidus F-L-D-H-S 1.81 0.41 2 2 Tahvanainen et al. (1985)
Salix novae-anglieae L. americanus M-M-D-H-V 12.60 0.07 30 30 Current study
Salix pentandra L. timidus F-L-D-T-S 10.49 0.06 3 3 Tahvanainen et al. (1985)
S. pentandra M. agrestis F-L-D-T-M 1.23 0.32 10 10 Danell et al. (1987)
Salix phylicifolia L. americanus M-L-D-L-S 1.06 0.40 9 9 Bryant et al. (1989)
S. phylicifolia L. timidus M-L-D-L-S 3.20 0.14 10 10 Bryant et al. (1989)
S. phylicifolia L. timidus M-L-D-L-S 10.49 0.11 3 3 Tahvanainen et al. (1985)
S. phylicifolia L. timidus M-L-D-L-S 5.43 0.15 2 2 Tahvanainen et al. (1985)
Salix planifolia L. americanus M-M-D-L-V 15.84 0.15 30 30 Current study
SWIHART AND BRYANT—WINTER HERBIVORY

Sorbus aucuparia M. agrestis M-M-D-T-M 0.47 0.43 20 20 Danell et al. (1987)

Tsuga canadensis L. americanus S-H-E-T-M 3.01 0.14 6 6 Current study
T. canadensis O. virginianus S-H-E-T-M 1.56 0.23 6 6 Swihart and Picone (1998)
a
Trials conducted in conjunction with P. Picone.
b
Trials conducted in conjunction with H. Henttenon.
c Trials conducted using hares in Alaska.

d Tolerance ratings to stress were based on nutrients for B. glandulosa and L. laricina, and to light for all other species.

e Trials conducted in conjunction with J. Cary and C. Krebs.

f Approximate number of hares present.

7

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8 JOURNAL OF MAMMALOGY Vol. 82, No. 1

TABLE 2.—Summary of studies reporting winter herbivory by mammals on woody plants origi-
nating from .1 geographic locality. Data from $3 localities were required for a study to be included
in the meta-analysis testing overall strength of the correlation between latitude and extent of herbiv-
ory, and $4 localities were required for inclusion in the meta-analysis using Fisher’s Z-transformation.
In some studies, it was not possible to calculate r (or Z); for those studies, we merely report authors’
tests of significant differences for consumption of conspecific plants from different localities. NS 5
not significant.

Plant Mammal ri Zi n Source

Betula pendula Lepus timidus 20.54 20.60 4 Rousi et al. (1989)
20.94

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B. pendula L. timidus 1.74 4 Rousi et al. (1989)
B. pendula L. timidus 20.85 21.26 4 Rousi et al. (1989)
B. pendula L. timidus 20.86 21.29 4 Rousi et al. (1991)
B. pendula Microtus agrestis NS 2 Rousi (1988)
Pinus contorta M. agrestis 20.44 20.47 25 Hansson (1985)
P. contorta Alces alces P , 0.01 35 Hansson (1985)
P. contorta A. alces P ø 0.10 16 Hansson (1985)
Pinus ponderosa Lepus 20.36 20.38 10 Squillace and Silen (1962)
P. ponderosa Odocoileus 20.62 20.72 10 Squillace and Silen (1962)
P. ponderosa Lepus californicus 0.38 0.40 17 Read (1971)
Pinus sylvestris Alces alces 20.63 20.74 29 Niemelä et al. (1989)
P. sylvestris A. alces 20.51 20.56 30 Niemelä et al. (1989)
Populus grandidentata Lepus americanus 20.93 3 Swihart et al. (1994)
Populus tremuloides L. americanus 20.99 3 Swihart et al. (1994)
P. tremuloides L. americanus 20.99 3 Bryant et al. (1994)
P. tremuloides L. americanus 20.99 3 Bryant et al. (1994)

temperatures (very severe, severe, moderate, Meta-analysis.—Meta-analysis refers to a set

mild). Categories reflected a gradient from long,
cold winters (very severe) to short, warm win-
ters (mild). Generally, sites with more severe
winter temperatures occurred at higher latitudes,
with reductions in winter severity associated
with lower latitudes and maritime climates.
Additional information on geographic varia-
tion in palatability of woody plants to mammals
was obtained from studies that monitored con-
sumption of a single growth stage (juvenile) col-
lected from conspecific plants at .1 source.
Those studies varied somewhat in terms of de-
sign and sampling procedures, but generally
they took 1 of 2 forms. In some feeding trials,
mammals were presented with shoots of plants
collected from different geographic localities
and hence exposed to different environmental
regimes during development (e.g., Bryant et al.
1994). In the remaining trials, mammals chose
among plants of different geographic origins but
grown from seed in a common environment
(e.g., Niemelä et al. 1989). Both captive and
free-ranging mammals were used as test sub-
jects. Our review of the literature provided data
from 9 published studies, including trials involv-
ing 6 plant and 6 mammalian species (Table 2).
of statistical methods that enables comparison
and synthesis of results of multiple studies (Gel-
ber and Goldhirsch 1991; Gelber et al. 1992;
Hedges 1992). Ecologic and evolutionary stud-
ies have begun to use meta-analytic techniques
(Bender et al. 1998; Côté and Poulin 1995; Gur-
evitch et al. 1992; Hamilton and Poulin 1997;
Møller and Thornhill 1998), and meta-analysis
can improve rigor of reviews and syntheses
(Arnqvist and Wooster 1995; Gurevitch and
Hedges 1993). Meta-analysis was chosen be-
cause data were compiled from multiple sources
that used similar techniques but analyzed data
and reported results differently (Rosenberg et al.
1997). We were interested in whether regulari-
ties existed in the direction of differences re-
ported for multiple sets of trials that collectively
indicated a strong underlying process.
Procedures for meta-analysis are covered
elsewhere (Gurevitch and Hedges 1993; Gure-
vitch et al. 1992; Hedges and Olkin 1985). After
gathering data from multiple studies that address
a common question, meta-analysis tends to ad-
vance sequentially (Arnqvist and Wooster 1995).
First, results of studies were transformed to a
common scale, called effect size, which repre-
February 2001 SWIHART AND BRYANT—WINTER HERBIVORY
sented the magnitude and sign of the effect of
interest. By necessity, studies of the effect of
plant ontogeny on mammalian herbivory in-
volve a comparison of consumption of 2 growth
stages (j 5 juvenile, m 5 mature). To test wheth-
er mammals discriminate between conspecific
juvenile- and mature-stage growth of plants, we
computed an effect size, d (Hedges and Olkin
1985), for each study in which it was possible
to obtain information on mean consumption of
each growth stage, standard deviations about
each mean, and sample sizes (Table 1). The ef-
fect size, di, for the ith set of trials was given by
J(Xm 2 Xj)/s, where Xm was the mean measure
of consumption of mature-stage growth, Xj was
the mean consumption of juvenile-stage growth,
and s was the pooled standard deviation of the
juvenile and mature groups (Hamilton and Pou-
lin 1997; Rosenberg et al. 1997). J was used to
correct for bias caused by small samples and
was given by Hedges and Olkin (1985) as J 5
1 2(3/[4k 2 1]), where k 5 nj 1 nm 2 2, and
nj and nm represented the samples for juvenile-
and mature-stage growth, respectively. Effect
size was considered small if di , 0.2, moderate
if di 5 0.5, large if di . 0.8, and very large if
di . 1.0 (Cohen 1969). The variance in di was
vi 5 [(nj 1 nm)/njnm] 1 [di2/2(nj 1 nm)].
Next, we combined effect sizes from individ-
ual sets of trials into an overall effect size. To
compute a mean effect size across all t sets of
trials (i 5 1, . . . , t), we computed d1 5 Swidi/
Sdi, where wi was the weight of the reciprocal
of vi, which gave greater weight to sets of trials
with larger samples and, presumably, more pre-
cise results (Gurevitch et al. 1992; Hedges and
Olkin 1985). The variance of d1 was v1 5 1/
Swi. Confidence intervals (95%) for d1 were d1
6 1.96v1.
To test for differences in effect sizes among
sets of trials grouped by plant growth rate, tol-
erance to limiting resources (hereafter termed
stress tolerance), growth form, leaf type, mam-
malian digestive strategy, or winter severity, we
used MetaWin (Rosenberg et al. 1997). We ex-
pressed the result of each set of trials for this
part of the analysis as a response ratio, RR,
where RR 5 Xj/Xm. In meta-analysis, effect size
typically is computed for ln(RR) rather than RR.
An advantage of ln(RR) as a measure of effect
size was that, when combined with resampling
tests (see below), it did not require knowledge
of intraclass variation in resampling (Rosenberg
9
et al. 1997), which permitted us to increase the
number of studies used in some comparisons
(Table 1). Thus, ln(RR) was used in statistical
analyses. Each set of trials received a nonpara-
metric weighting, wi 5 njnm/(nj 1 nm) (Adams et
al. 1997; Rosenberg et al. 1997). We used
mixed-model analyses because they do not re-
quire that all sets of trials within a particular
category (e.g., fast-growing plant species) share
a common, true effect size (Rosenberg et al.
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1997). For each analysis, we computed a mea-
sure of the variation in mean effect size between
categories (e.g., between sets of trials conducted
using evergreen and deciduous leaf types),
termed QB* (Rosenberg et al. 1997). Larger val-
ues of QB* reflect greater differences in mean
effect sizes between categories. Adams et al.
(1997) urged ecologists to use resampling meth-
ods when evaluating the significance of main ef-
fects in meta-analysis studies, thereby avoiding
problems associated with distributional assump-
tions of parametric tests. To test the null hy-
pothesis that effect sizes did not differ among
categories, randomization tests consisting of
4,999 iterations were used to derive a null dis-
tribution for QB*, from which a P-value was ob-
tained. We also used MetaWin to calculate bias-
corrected bootstrap confidence intervals (95%)
to facilitate comparisons (Adams et al. 1997;
Dixon 1993; Rosenberg et al. 1997).
Because some of our main effects for plant
ontogeny were correlated traits (e.g., growth rate
and leaf type), we conducted our tests according
to the following criteria. First, each main effect
was tested as described above. Main effects
yielding at least marginally significant differenc-
es (P # 0.15) in ln(RR1) among categories were
subsequently subjected to fine-scale analysis by
cross-classifying pairs of categories and repeat-
ing the meta-analysis. No category was included
in an analysis if it contained #5 sets of trials.
When samples were sufficient, we also exam-
ined cross-classified pairs of categories for in-
dividual genera of woody plants (Betula, Popu-
lus, Salix).
A slightly different form of meta-analysis was
used to examine whether geographically based
differences in mammalian herbivory existed
among juvenile-stage growth of conspecific
woody plants (Table 2). Based on previous work
(Swihart et al. 1994), we hypothesized that lat-
itudinal gradients in palatability would exist,
with northern plants being less palatable than
10 JOURNAL OF MAMMALOGY
more southern conspecifics. To test that hypoth-
esis, we used procedures described by Côté and
Poulin (1995). For study i, we computed the cor-
relation, ri, between the latitude from which a
plant originated and the extent of herbivory.
Next, we computed an overall correlation coef-
ficient, r1, which weighted each ri by its sample
size, Ni: r1 5 SNiri/SNi. Observed population
variance was computed as vr 5 S[Ni(ri 2 r1)2]/
SNi. Observed variance was partitioned into the
true population variance and variance due to
sampling error. Variance due to sampling error,
ve, was approximated as ve 5 (1 2 r12)2/(N 2 1),
where N is the average sample size across stud-
ies. The true population standard deviation, s,
was then estimated as (vr 2 ve)½. If the ri are
normally distributed, then a test of the null hy-
pothesis that r1 5 0 can be made using Z 5 r1/
s. Because the correlation coefficient can exhibit
undesirable statistical properties, particularly
when samples are small, we also conducted a
second meta-analysis on these data after apply-
ing Fisher’s Z-transformation (Rosenberg et al.
1997): Zi 5 {ln[(1 1 ri)/(1 2 ri)]}/2. We used
Zi as effect sizes, with weights of Ni 2 3 (Ro-
senberg et al. 1997), to derive an overall effect
size, Z1.
Meta-analysis has many advantages over
qualitative summaries and ‘‘vote counting’’ pro-
cedures (Arnqvist and Wooster 1995; Hedges
and Olkin 1985; Hunter et al. 1982). In partic-
ular, meta-analysis is useful because it provides
an estimate of the magnitude of an effect that
takes into account differences in sample size
among studies, and it provides greatly improved
control of type II error rates (Arnqvist and Woo-
ster 1995). However, meta-analysis is not with-
out its limitations. One concern is that the prob-
ability of a type I error could increase if studies
with nonsignificant results were published less
frequently than studies with significant results.
A plot of sample size versus effect size failed to
suggest that selective reporting occurred in our
data (Palmer 1999). We doubt that a publication
bias exists because data that formed the basis for
our analyses usually represented only a fraction
of the data reported in any given publication,
and they often were presented ancillary to a pa-
per’s central theme. In addition, 36% of the data
sets in Table 1 represented unpublished work
that clearly had not been subjected to such bias.
A 2nd concern is that researchers might select
subjects for study because they anticipate deriv-
Vol. 82, No. 1
ing significant results (Adams et al. 1997). Re-
search bias did not likely play a role in the ma-
jority of studies used in our meta-analyses be-
cause choice of species often was governed by
factors, such as economic importance or avail-
ability, that are unrelated to hypotheses we test-
ed. Another concern is a possible lack of inde-
pendence of sets of trials included in a meta-
analysis, which could result when multiple tests
are reported from single studies (Arnqvist and
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Wooster 1995). We could not rule out that pos-
sibility because several studies provided .1 ef-
fect size for use in our analyses and some spe-
cies were represented disproportionately often.
However, all effect sizes were independent in
the sense that they were derived from different
combinations of test subjects, plant species, and
localities.
RESULTS
Plant selection based on ontogeny.—If
mammals do not discriminate between ju-
venile and mature growth stages of conspe-
cific plants during winter, then each growth
stage should be eaten in equal proportion.
However, relative consumption nearly al-
ways favored mature-stage growth; juve-
nile-stage growth comprised ,50% of the
average total consumption by mammals in
123 of 128 trials (96%). In the majority of
feeding experiments, consumption of juve-
nile-stage growth comprised ,20% of the
total (Fig. 1). Effect sizes showed a similar
pattern; di was ‘‘very large’’ (Cohen 1969)
for 99 of the 120 experiments (82%) for
which it could be calculated (Fig. 1). The
overall effect size for the studies was d1 5
2.16, with a 95% CI of 2.03–2.29. When
presented with a choice between juvenile-
and mature-stage winter-dormant growth,
mammals avoid the juvenile stage.
When feeding experiments were catego-
rized by plant growth rate, there was a ten-
dency for differential discrimination to oc-
cur between juvenile and mature growth
stages (QB* 5 6.27, P 5 0.062). Overall
response ratios exhibited a gradient, with
the greatest level of discrimination by
mammals occurring between juvenile and
mature growth stages of fast-growing plants
February 2001 SWIHART AND BRYANT—WINTER HERBIVORY
FIG. 1.—A) Distributions illustrating the pro-
portion of total consumption of juvenile-stage
growth in trials in which mammalian herbivores
were presented with approximately equal
amounts of juvenile- and mature-stage growth;
note the preponderance of studies for which
,50% of total consumption consisted of juve-
nile-stage growth. B) Distribution of effect sizes,
d, from Table 1; designations regarding effect
sizes follow Cohen (1969).
(RR1 5 0.11, n 5 72, CI 5 0.07–0.16), an
intermediate amount occurring for plants
with medium growth rates (RR1 5 0.19, n
5 49, CI 5 0.12–0.25), and the least dis-
crimination between ontogenetic stages oc-
curring for slow-growing plants (RR1 5
0.36, n 5 7, CI 5 0.24–0.56). An analo-
gous pattern was seen for experiments in-
volving Betula (QB* 5 12.94, P 5 0.004),
with mammals exhibiting greater discrimi-
nation between ontogenetic stages when of-
fered fast-growing species (RR1 5 0.04, n
5 22, CI 5 0.02–0.09) than when offered
species with medium growth rates (RR1 5
11
0.35, n 5 12, CI 5 0.14–0.87). Discrimi-
nation of ontogenetic stages by mammals
did not differ as a function of growth rate
when Salix was presented in feeding exper-
iments (QB* 5 2.72, P 5 0.12).
When experiments were categorized ac-
cording to stress tolerance of the plants in-
volved, a marginal tendency for differential
discrimination occurred (QB* 5 5.18, P 5
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0.108). Plants with low tolerance ratings
elicited the greatest discrimination in their
juvenile and mature growth stages when
presented to mammals (RR1 5 0.11, n 5
74, CI 5 0.07–0.16), whereas proportion-
ately twice as much juvenile-stage growth
was consumed by mammals offered plants
with medium (RR1 5 0.21, n 5 30, CI 5
0.10–0.35) or high (RR1 5 0.20, n 5 24,
CI 5 0.14–0.27) tolerance ratings.
Mammals did not discriminate between
ontogenetic stages as a function of either
leaf type (QB* 5 0.04, P 5 0.832) or plant
growth form (QB* 5 1.94, P 5 0.582). Cat-
egorizing mammals by type of fermentation
system also failed to reveal any additional
variation in response ratios (QB* 5 0.17, P
5 0.693), although only 9 feeding experi-
ments involved mammals with foregut fer-
mentation (Table 1).
Interactive effects of winter severity and
plant life history.—To examine more close-
ly how mammalian herbivory varies as a
function of plant ontogeny, we partitioned
feeding experiments according to winter se-
verity and plant growth rate. When mam-
mals were presented with juvenile and ma-
ture growth stages of fast-growing plants,
they discriminated differentially as a func-
tion of winter severity (QB* 5 16.04, P 5
0.001). Fast-growing plants from areas of
moderate winter temperatures elicited less
discrimination between juvenile and mature
growth stages than fast-growing plants from
areas of severe or very severe winter tem-
peratures (Fig. 2). A similar pattern of dis-
crimination was evident when mammals
were presented with plants characterized by
medium growth rates (QB* 5 15.57, P 5
0.003), except that the lowest RR1 occurred
12 JOURNAL OF MAMMALOGY
FIG. 2.—Response ratios (RR1 5 J/M) mea-
suring the discrimination exhibited by mamma-
lian herbivores between juvenile- and mature-
stage growth of winter-dormant woody plants.
Response ratios are categorized by plant growth
rate and severity of winter temperatures; colder
winters elicit greater discrimination against ju-
venile-stage growth by mammals. Vertical lines
are 95% bias-corrected bootstrap confidence in-
tervals based on 4,999 samples.
for feeding trials of plants from areas with
severe winter temperatures (Fig. 2). Quali-
tatively, mammals did not seem to discrim-
inate among ontogenetic stages of slow-
growing plants on the basis of winter se-
verity (moderate, RR1 5 0.41, n 5 5; very
severe, RR1 5 0.43, n 5 3).
We also partitioned feeding experiments
according to winter severity and stress tol-
erance of plants. Insufficient samples were
available to permit analysis of experiments
on plants from areas with mild or severe
winter temperatures, or for plants charac-
terized by high stress tolerance (Table 1).
Mammals exhibited differential discrimi-
nation of juvenile and mature growth stages
Vol. 82, No. 1
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FIG. 3.—Response ratios (RR1 5 J/M) mea-
suring discrimination exhibited by mammalian
herbivores between juvenile- and mature-stage
growth of winter-dormant woody plants. Re-
sponse ratios are categorized by plant tolerance
to limiting resources and severity of winter tem-
peratures; colder winters elicit greater discrimi-
nation against juvenile-stage growth by mam-
mals. Vertical lines are 95% bias-corrected boot-
strap confidence intervals based on 4,999 sam-
ples.
when presented with plants of low (QB* 5
18.14, P 5 0.0002) and medium stress tol-
erance (QB* 5 11.32, P 5 0.011). For both
tolerance classes of plants, mammals dis-
criminated between ontogenetic stages to
the greatest extent when plants were grown
in areas with very severe winter tempera-
tures (Fig. 3).
Biogeographic patterns of mammalian
herbivory.—Categorizing plants according
to severity of winter temperatures where
they were grown revealed strong differen-
tial discrimination in consumption of juve-
nile-stage and mature-stage growth (QB* 5
24.59, P 5 0.0002). Overall response ratios
February 2001 SWIHART AND BRYANT—WINTER HERBIVORY
exhibited a gradient with respect to winter
severity. Mammals discriminated greatly
between juvenile and mature growth stages
from areas with very severe (RR1 5 0.09,
n 5 76, CI 5 0.06–0.13) and severe winter
temperatures (RR1 5 0.13, n 5 16, CI 5
0.04–0.26). However, a nearly 4-fold in-
crease in relative consumption of juvenile-
stage growth occurred in areas experiencing
moderate winter temperatures (RR1 5 0.40,
n 5 34, CI 5 0.25–0.55). Although an in-
sufficient number of experiments (n 5 2)
were conducted in mild localities to warrant
inclusion in the analysis, they exhibited
qualitative agreement with our other results
(RR1 5 0.28). Betula (QB* 5 39.06, P 5
0.0002) and Populus (QB* 5 16.90, P 5
0.0008) followed that pattern, although
only plants from areas with moderate and
very cold winters were subjected to testing.
When mammals were offered Betula from
areas with very severe winter temperatures,
they were more discriminating (RR1 5
0.02, n 5 14, CI 5 0.01–0.04) than when
offered Betula from areas with moderate
winters (RR1 5 0.34, n 5 17, CI 5 0.15–
0.58). Similarly, when mammals were of-
fered Populus from areas with very severe
winter temperatures, they were much more
discriminating (RR1 5 0.06, n 5 14, CI 5
0.03–0.12) than when offered Populus from
areas with moderate winters (RR1 5 0.53,
n 5 8, CI 5 0.23–0.93). Experiments with
Salix were conducted only using plants
from areas with very severe and severe
winter temperatures, and no difference in
discrimination of ontogenetic stages was
noted (QB* 5 0.92, P 5 0.34).
Intensity of browsing was negatively cor-
related with latitude in 12 (86%) of the 14
studies (Table 2). Overall correlation be-
tween browsing intensity and latitude was
20.53, yielding a Z of 21.53 (P 5 0.066).
For Fisher’s Z-transformed correlations, we
obtained a moderate (Cohen 1969) effect
size of 20.46, which differed from the zero
predicted by the null hypothesis of no re-
lationship (CI 5 20.62 to 20.30).
13
DISCUSSION
Plant ontogeny and cost of herbivory.—
In the absence of herbivory, competition
between plants is the major factor deter-
mining resource allocation patterns in a giv-
en environment (Tilman 1990). Relative
costs of herbivory are magnified in the ju-
venile stage of ontogeny for woody plants
because a given level of herbivory removes
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a proportionately greater amount of a ju-
venile plant’s biomass and growing points
compared with a larger, reproductively ma-
ture conspecific. Herbivory also can have a
greater impact on a plant’s fitness if it oc-
curs in the juvenile stage and subsequently
diminishes (or precludes) lifetime reproduc-
tive success via, for example, mortality be-
fore maturation, a delay in age at 1st repro-
duction, or a decline in competitive ability
(Bulmer 1994; Prins and Nell 1990; Rough-
garden 1998; Stearns 1992). As a conse-
quence of the potentially greater cost of
herbivory in the prereproductive stage,
plants should invest relatively more in de-
fense of this growth stage. For woody
plants in which the chemical basis of pal-
atability to mammals has been determined,
juvenile-stage growth is more heavily de-
fended than mature-stage growth, usually
by lipid-soluble secondary metabolites of
low molecular weight (Bryant 1981a; Clau-
sen et al. 1986; Reichardt et al. 1984,
1990). In our analysis, mammals strongly
and consistently chose mature-stage growth
over juvenile-stage growth. Mammals dis-
criminate among plants on the basis of plant
chemistry, morphology, and texture and
avoid ingestion of plants or plant parts that
contain high levels of defensive substances
(Palo and Robbins 1991). Our analysis pro-
vides overwhelming support for the idea
that palatability of plants to mammals dif-
fers as a function of ontogenetic stage in a
manner consistent with an evolutionary re-
sponse of plants to stage-specific differenc-
es in costs of herbivory (Fig. 1). Moreover,
because those experiments were conducted
on winter-dormant woody plants, it seems
14 JOURNAL OF MAMMALOGY
highly unlikely that insects or pathogens
could have caused the response we ob-
served. Rather, mammals likely are the evo-
lutionary force generating these stage-spe-
cific differences.
Effects of plant life history.—Mammalian
discrimination between juvenile- and ma-
ture-stage growth varied somewhat as a
function of plant growth rate and tolerance
to resource stress. We suspect that these
patterns are a consequence of differences in
responses to resource-rich and resource-
poor environments. In resource-rich envi-
ronments, competition among plants is in-
tense, and success is dependent on rapid ac-
quisition of resources and on allocation of
these resources to vegetative structures
needed for subsequent acquisition of addi-
tional resources (Coley et al. 1985; Herms
and Mattson 1992). As a result, plants
adapted to resource-rich environments typ-
ically exhibit fast rates of growth (Herms
and Mattson 1992). In resource-poor envi-
ronments, competition among plants may
be less intense, and success is dependent on
efficient use and retention of resources
(Chapin 1980; Tilman 1990; Vitousek
1982). Consequently, plants adapted to re-
source-poor environments exhibit inherent-
ly slow rates of growth (Chapin et al. 1989;
Coley et al. 1985). Not surprisingly, plant
growth rate is correlated inversely with tol-
erance to resource limitation (Shipley and
Keddy 1988).
Plants adapted to resource-rich environ-
ments typically are more nutritious and thus
are more valuable to mammalian herbivores
than plants from resource-poor environ-
ments (Bryant and Kuropat 1980; Coley et
al. 1985). Herbivory presents an added di-
lemma for growth-dominated plants in rich
environments because beyond the direct
costs associated with lost tissue and nutri-
ents, reduced competitive ability in the ju-
venile stage could reduce future reproduc-
tive success. Moreover, growth-dominated
plants exhibit considerably greater pheno-
typic flexibility than stress-tolerant plants
(Herms and Mattson 1992). We suspect that
Vol. 82, No. 1
plants characterized by fast growth rates
and low tolerances to resource limitation
(i.e., plants facing intense competition in re-
source-rich environments) should invest
relatively more in defense of the juvenile
stage than slow-growing, stress-tolerant
plants. Consistent with this expectation,
when feeding experiments were categorized
by plant growth rate, mammals exhibited
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the greatest degree of ontogenetic discrim-
ination for fast growers and the least dis-
crimination for slow growers. Similarly,
when feeding experiments were categorized
by plant tolerance rating, mammals were
most discriminating when presented with
juvenile and mature growth stages of low-
tolerance plants and least discriminating
when offered ontogenetic stages of plants
with either medium or high tolerance rat-
ings. Overall differences in discrimination
between ontogenetic stages, as measured
using RR1, indicated a 2- to 3-fold change
for the extreme classes of growth rate and
tolerance rating.
Constraints of winter severity.—Discrim-
ination of ontogenetic stages by mammals
varied as a function of winter severity, even
after correcting for differences in plant
growth rate (Fig. 2) or tolerance rating (Fig.
3). Mammals tended to consume relatively
less juvenile-stage growth when occurring
in areas with severe or very severe winter
temperatures.
Greater discrimination in colder climates
may result from more stringent constraints
for mammals faced with a trade-off be-
tween energetic needs and detoxification
capabilities for ingested toxins. Energetic
costs of thermoregulation during winter
typically increase for a mammal of a given
size as temperature declines (Lindstedt and
Boyce 1985; Moen 1973; Robbins 1993).
Although costs can be partially offset by
changes in behavior (e.g., movement, hud-
dling), insulative quality of pelage, or re-
duced metabolism, it seems likely that in
many instances increased costs also must be
offset by increased food intake. An excep-
tion may be larger species that can rely to
February 2001 SWIHART AND BRYANT—WINTER HERBIVORY
a greater degree on fat reserves during win-
ter. Nonetheless, sites with colder winter
temperatures in temperate and northern lat-
itudes are associated with shorter growing
seasons; thus, mammalian herbivores from
these areas are forced to rely on dormant
woody plants as a primary food source for
a longer period each year. Finally, herbi-
vores from northern latitudes typically must
rely on a food base that is less diverse than
at more southern latitudes, which can limit
dietary breadth.
Juvenile-stage growth of woody plants
often contains elevated concentrations of
secondary metabolites that can elicit acute,
subacute, or chronic toxicosis (Bryant et al.
1992; Harju 1996a, 1996b; MacArthur et al.
1991; Reichardt et al. 1984). Detoxification
of plant secondary metabolites is essential
to maintenance of acid–base homeostasis in
mammals, but it is a saturable process (Fo-
ley et al. 1995). If intake of secondary me-
tabolites is great enough to saturate a mam-
mal’s system for excretion of organic an-
ions, deleterious effects on protein metab-
olism and sodium balance result (Foley et
al. 1995; Iason and Palo 1991; Illius and
Jessop 1995). Increases in dietary energy
and protein apparently can ameliorate ef-
fects of toxins, at least in ruminants (Burritt
et al. 2000; Wang and Provenza 1997).
When faced with few plant species from
which to choose, such nutrient supplemen-
tation seems unlikely for herbivores in
northern latitudes.
We suggest that mammals in harsh cli-
mates have 2 options for dealing with con-
straints imposed by their greater rate of
food intake and need to avoid toxicosis.
They must either forage more selectively
with respect to plant secondary metabolites
or evolve more effective means of detoxi-
fication. Our results are consistent with the
former prediction, although discrimination
in our analysis also might result from cli-
matic constraints on plants. Additional,
stronger support for the influence of winter
climate on discrimination comes from 3
feeding experiments in which reciprocal
15
feeding trials were conducted, and 3 species
of Betula grown in a moderate climate were
provided to snowshoe hares (Lepus ameri-
canus) inhabiting interior Alaska (Table 1).
In all cases, overall level of discrimination
by hares in Alaska was greater than any of
9 sets of trials for the same plant species
provided to hares inhabiting the more mod-
erate climate of Connecticut (Swihart et al.
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1994).
Mammals are equipped with genetic,
physiologic, and neurologic capabilities for
learning and remembering quality of poten-
tial food items (Provenza 1995, 1996).
Moreover, they prefer the flavor or odor of
nutritious foods (Villabla and Provenza
1996), yet they limit their intake of nutri-
tious but toxic foods and thereby avoid sat-
urating their detoxification system (Pfister
et al. 1997; Wang and Provenza 1996a,
1996b, 1997). Our data do not permit us to
assess whether mammals in harsher cli-
mates have developed more effective detox-
ification mechanisms. However, evidence
exists for Lepus that physiologic capabili-
ties for detoxification vary (Iason and Palo
1991).
Latitudinal trends and evolution of plant
defense.—Although constraints imposed by
geographic variation in winter severity
seem to influence levels of ontogenetically
based discrimination of woody plants by
mammals, this explanation is insufficient to
explain geographic variation in patterns of
consumption of conspecific, juvenile-stage
growth (Table 2). In these studies, mam-
mals at a single locality were either pre-
sented with plants grown on site from seed
collected at several different localities, or
offered plants that had been collected as ju-
veniles from several localities. Yet our anal-
ysis indicates a moderate effect size for lat-
itude, with mammals consuming propor-
tionately more biomass of plants of south-
ern origin. This effect likely has a
substantial genetic component, because
plants were grown in common environ-
ments for 67% of the studies exhibiting in-
verse relationships between latitude and
16 JOURNAL OF MAMMALOGY
palatability. Moreover, comparison of her-
bivory by snowshoe hares on juvenile-stage
growth of closely related species (Populus
grandidentata, P. tremuloides) grown in
common environments repeatedly has
shown that hares consume less of P. tre-
muloides, the species with the more north-
ern geographic range (Swihart et al. 1994).
Large-scale clinal variation in palatability
could result from evolutionary responses of
plants to $2 selective forces associated
with cold climates. Although numerous ex-
ceptions exist, soil temperatures in northern
latitudes generally are colder than in south-
ern latitudes of the same altitude. Colder
soils reduce the rate at which nutrients are
mineralized from organic matter and hence
made available for uptake by plants (Chap-
in and Shaver 1985). Consequently, cold-
soil plants growing in otherwise compara-
ble conditions could become more nutrient
limited (Swihart et al. 1994). Nutrient lim-
itation constrains rate of plant growth and
thus simultaneously serves to increase cost
of a unit of herbivory (Bryant et al. 1983a;
Coley et al. 1985) and diminish opportunity
costs associated with investing in defenses
at the expense of growth (Chapin 1989;
Herms and Mattson 1992). Greater levels of
defense against herbivory could evolve,
then, as a consequence of nutrient limitation
associated with cold soils. Although harsh
winter conditions also can lead to physio-
logic changes in plant responses to dessi-
cation and winter hardening, these changes
do not explain patterns of herbivory that we
observed (Swihart et al. 1994).
Growing seasons are shorter at more
northern latitudes, which forces northern
herbivorous mammals to rely on dormant
plants as sources of food for longer periods
of time than their southern counterparts. For
an identical complement of mammals, then,
plants in northern latitudes will experience
more herbivore-days of browsing pressure
during winter. Greater productivity in the
more southern latitudes of the temperate
zone could ameliorate this selective force
by yielding greater densities of herbivores.
Vol. 82, No. 1
However, the lower species richness and
productivity of woody plant communities
typifying taiga and subarctic regions pre-
sumably would elevate selective pressure
exerted on any given plant. Moreover, in
northern latitudes with long winters, popu-
lations of arvicoline rodents and lago-
morphs associated with specialized preda-
tors and relatively unfragmented habitat
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seem more prone to cyclical dynamics of
high amplitude (Bjørnstad et al. 1995; Han-
ski and Korpimaki 1995; Keith 1990; Keith
et al. 1993). During peak years, herbivory
can cause widespread mortality of seedlings
and saplings (Wolff 1980). Thus, some ev-
idence exists that latitudinal variation in
plant defense could arise as a direct con-
sequence of latitudinal variation in intensity
of winter herbivory.
Geographic variation in defense.—Effect
sizes for latitude were not large, and other
factors unrelated to latitude clearly influ-
ence geographic variation in mammalian
herbivory and plant defense. We were un-
able to examine effects of altitude in our
analysis, but we suspect that plants adapted
to montane environments exhibit defensive
characteristics similar to plants grown in
northern latitudes. Indirect evidence is con-
sistent with this notion. Hansson (1985) rat-
ed damage by field voles (Microtus agres-
tis) in Sweden to lodgepole pine (Pinus
contorta) collected from a variety of local-
ities in western North America. For plants
from 25 localities, our rank correlation of
latitude and damage was 20.44 (Table 2).
Hansson (1985) noted that northern prove-
nances were less damaged than southern
ones, with 1 dramatic exception. Voles only
weakly damaged the most southern prove-
nance, which came from a high-altitude lo-
cality. Removal of this locality from the
analysis strengthened the latitudinal corre-
lation by 41%, to 20.62.
Geographic variation in the historical in-
tensity of herbivory also may be unrelated
to latitude. Bryant et al. (1989) documented
dramatically different responses of hares to
congeneric woody plants; plants from an
February 2001 SWIHART AND BRYANT—WINTER HERBIVORY
area with no history of browsing mammals
were least defended chemically and con-
sumed in greatest quantities by hares, plants
from an area with a long history of brows-
ing mammals but hare populations that did
not cycle were intermediate in defense and
palatability, and plants from areas with a
long history of browsing mammals and
populations of hares with high-amplitude
cycles were least palatable and exhibited
the greatest levels of chemical defense. In-
traspecifically, only 2 studies in our analy-
sis failed to show an inverse relation be-
tween extent of mammalian herbivory and
latitude (Table 2). In 1 of these, Read
(1971) recorded browsing by black-tailed
jackrabbits (Lepus californicus) in Nebras-
ka on ponderosa pine (Pinus ponderosa)
seedlings originating from 17 localities
throughout the western United States. He
documented a significant difference in her-
bivory as a function of longitude of origin;
plants with origins west of the Continental
Divide were browsed more severely. Inter-
estingly, the intermountain area west of the
Divide has no history of intense herbivory
by large mammalian herbivores, in contrast
to land east of the Divide (Mack and
Thompson 1982). Thus, even though
Read’s (1971) study did not yield an inverse
latitudinal gradient in herbivory, its findings
are consistent with mammalian herbivory
as a force influencing geographic patterns
of defense in woody plants.
CONCLUSIONS
We reviewed the literature and docu-
mented patterns in the consumption of win-
ter-dormant woody plants by mammalian
herbivores that reflected small- and large-
scale variation in mammal–plant interac-
tions. Only by examination of a broader
spectrum of mammalian herbivores and
woody plants will the generality of our
findings be determined. In particular, com-
parative studies of ruminants are needed.
Based on available information, at any par-
ticular locality mammals perceive signifi-
cant intraspecific and intraplant differences
17
in palatability. These differences are onto-
genetically based, they often are large com-
pared with many of the interspecific differ-
ences that we and others have observed for
plants of the same ontogenetic stage, and
they seem to have evolved principally as
defensive responses of plants to mammalian
herbivory during winter.
The degree to which our findings gener-
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alize to other seasons, biomes, and taxa re-
mains to be seen. Few studies have exam-
ined effects of plant developmental stage on
herbivorous birds in northern latitudes
(Muller 1995; Ryala 1966; Svoboda and
Gullion 1972), but results thus far have
been consistent with our findings. Insect
herbivores also seem sensitive to develop-
mental differences in plants during the
growing season, but their responses vary in-
terspecifically and the number of studies is
small (Karban and Thaler 1999; Kearsley
and Whitham 1989, 1998; Waltz and Whi-
tham 1997).
Large-scale spatial variation also is evi-
dent and seems to be driven largely by win-
ter severity. Physiologic and ecologic con-
straints imposed by harsh environments in
northern latitudes seem to have resulted in
evolution of plants with better defenses and
mammalian herbivores with more discrim-
inating palates than their counterparts from
more moderate latitudes. Moreover, these
selective forces have generated a latitudinal
pattern that seems to differ from patterns of
geographic variation reported for insect
(Coley and Aide 1991; Levin 1976) and
aquatic (but see Steinberg 1986; Targett et
al. 1992) systems. Thus, any general theory
formulated to predict large-scale patterns in
plant defense against herbivory will have to
reconcile these disparate findings.
ACKNOWLEDGMENTS
We thank F. S. Chapin III, W. J. Foley, S. H.
Jenkins, L. K. Page, F. D. Provenza, K. Raffa,
K. Schwaegerle, H. P. Weeks, Jr., and an anon-
ymous reviewer for helpful comments on the
manuscript. K. Danell and L. Ericson provided
rankings of life-history categories for several
18 JOURNAL OF MAMMALOGY
species of European plants. Support was provid-
ed by Purdue University and the Institute of Arc-
tic Biology, University of Alaska. This is Purdue
University Agricultural Research Programs
manuscript 15811.
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Submitted 30 September 1999. Accepted 15 April
2000.
Associate Editor was Joseph A. Cook.