This file was created by scanning the printed publication.
Errors identified by the software have been corrected;
however, some errors may remain.
Environmental Stress Influences Aboveground
Pest Attack and Mycorrhizal Mutualism in
Pifton-Juni per Woodlands: Implications For
Management in the Event of Global Warming
Catherine Gehring and Thomas Whitham
1
Abstract.-In this paper, we summarize our findings on the relationships
between abiotic environmental stress, herbivory, mistletoe parasitism, and
mycorrhizal colonization in pinon pine and one-seeded juniper. We
compared trees growing in two very different environments - the nutrient
and water stressed ash and cinder fields of the San Francisco volcanic field
in northern Arizona, and the sandy loam soils of nearby areas. We found
that levels of moth herbivory in pinons (Pinus edulis) were 100-fold higher,
and levels of mistletoe parasitism in junipers (Juniperus monosperma) were
three-fold higher on trees growing in the stressful cinder soils than in the
sandy loam soils. Ectomycorrhizal colonization of pinon roots was two-fold
higher in trees growing in the cinder soils than in the sandy loam soils, but
was significantly reduced on cinder-site trees that experienced chronic
insect attack. Similar mycorrhizal reductions were observed in junipers that
experienced severe mistletoe infestation. Simulated moth herbivory
significantly reduced mycorrhizal colonization of pinons growing in the
cinder soils, but not of pinons in the sandy loam soils. These results
indicate that environmental stress influences three important parameters in
pinon-juniper woodlands: 1) the likelihood that a tree will experience
herbivore or parasite attack, 2) the abundance of mycorrhizal mutualists on
a plant, and. 3) the degree of mycorrhizal reductions that result from biotic
stresses such as herbivory. The importance of environmental stress in these
interactions suggests that global warming could cause significant increases
in pest attack and complex changes in levels of mycorrhizal mutualisms.
Furthermore, because these interactions in pinons are associated with host
plant genetics, pinon trees growing in stressful environments may possess
unique stress-tolerant genotypes that are important to conserve.
INTRODUCTION
environmental stress in this interaction is still
unclear (Gehring and Whitham 1994a). Pifton pines
(Pinus edulis) and one-seeded juniper Vuniperus
monosperma) grow in a variety of environments in
northern Arizona that vary markedly in
environmental stress. In particular, these tree
species are community dominants in many of the
nutrient and water-stressed cinder environments
that have resulted from geologically recent
eruptions of the San Francisco volcanic field.
The degree of environmental stress (e.g.
nutrient and water stress) experienced by plants
can have important effects on a plant's
susceptibility to herbivore attack (White 1969, 1974,
1976, 1984), and on the abundance of mycorrhizal
mutualists present on a plant's root system (Meyer
1973). Herbivores and mycorrhizae are also known
to interact with one· another, although the role of
1 Catherine Gehring is a postdoctoral research asSOCiate, and
Thomas Whitham is a Professor. Both are in the Department of
Biological SCiences, Northern Arizona University, Flagstaff, AZ.
30
By comparing levels of mycorrhizae and
herbivory in pifions and junipers in stressful cinder
environments to those growing in nearby less
stressful noncinder areas consisting of sandy loam
soils, we can better understand the effects of
environmental stress on this
widespread
vegetation type. In addition, because pmons and
junipers are attacked by different types of pests,
and have different types of mycorrhizal mutualists
(ectomycorrhizae in pmons and vesiculararbuscular mycorrhizae in junipers), it is of
particular interest to determine the effect of
environmental stress on these trees and their
associated taxa. This information could allow us to
make better predictions about the potential impacts
of human-caused stresses such as global warming
on pinon-juniper communities.
In this paper, we review some of our recent
research on the effects of environmental stress on
pmon pine and address the following questions: 1)
Do pmons and junipers growing in stressful cinder
environments and less stressful sandy loam
environments differ in herbivore or parasite
attack?,2) Do pmons growing in cinder and sandy
loam environments differ in mycorrhizal
colonization?, and 3) Do herbivores and parasites
interact with mycorrhizae, and is this'interaction
influenced by environmental stress? Although the
data we used to address these questions have
largely been published separately elsewhere, we
bring them together here to allow a more complete
synthesis of our results regarding environmental
stress, and to facilitate ~omparisons between
pmons and junipers growing in the same
environment. In spite of differences between
pmons and junipers in types of mycorrhizae
and
vesicular-arbuscular
(ectomycorrhizae
mycorrhizae, respectively), and major pests (insects
vs. mistletoes, respectively), we find that
environmental stress results in similar impacts on
these trees, mycorrhizal mutualists, and pests. We
use our data on patterns associated with
environmental stress to make predictions about the
potential effects of global warming on pest attack
rates and levels of mycorrhizal mutualism in
pmon-juniper woodlands, and to argue that pinons
growing in stressful environments possess unique
stress-tolerant genotypes that are important to
conserve.
Table 1 - Soil parameter COI1Y,)Clrisons between cinder and noncinder soils.1
~Vllue
Cinder
4.45
Nonclnder
12.20
.0001
5.61
9.39
.0001
Nitrite mineralization (ppm)
.60
5.86
.0001
Ammonium mlnerallzltlon (ppm)
-.84
2.47
PhosphIte (ppm)
Soli moisture (% water)
1 Values are the means of four cinder and four noncinder shes in northern Arizona.
.054
Data are
from Gehring and Whitham (1994b).
compared differed substantially in soil nutrient
and moisture levels (Gehring and Whitham
1994b)(Table 1). Soil from the cinder sites averaged
63% lower levels of phosphate, 40% lower levels of
soil moisture, and 70-90% lo~er nitrogen
mineralization rates than s~ils from the nearby
limestone-derived sandy loam sites. Two of the
same sites (one cinder and one noncinder) have
been shown to differ in the same nutrients
(Mopper et al. 1991), as well as many others (e.g.,
magnesium, potassium, calcium), with the cinder
sites always possessing the lower values (Cobb et
al., in review). The lower levels of soil nutrients
and moisture in the cinder soils have been
associated with a 23% reduction in pmon shoot
growth (Gehring and Whitham 1994b), a 66-90%
reduction in pmon cone production (Christensen
and Whitham 1991), and a 15% increase in tree
water potentials (Mopper et al. 1991) relative to
pmons growing in sandy loam soils.
HERBIVORY AND MISTLETOE PARASITISM
INCREASE WITH PLANT STRESS
Our results suggest that environmental stress
leads to increased susceptibility to moth herbivory
in pmon pines and to increased susceptibility to
mistletoe parasitism in one-seeded juniper. Piflon
pines growing in cinder soils from four different
sites in northern Arizona experienced an average
shoot mortality due to the stem- and cone-boring
moth (Dioryctria albovittella) of 7% while pmons at
four nearby sandy loam sites experienced less than
0.05% shoot mortality (Gehring and Whitham
1994b) (fig. 1A). Considering that these insects
selectively destroy a tree's terminal shoots thereby
turning trees into shrubs, even relatively low levels
of damage can have dramatic impacts on a tree's
architecture and cone production (Whitham and
Mopper 1985). A similar pattern was observed by
Mopper et al. (1991) for one cinder site and one
sandy loam site, and the data presented here
suggest that this pattern is a general one.
NUTRIENT AND MOISTURE STRESS
ACROSS EXTREME SOIL TYPES
The four stressful cinder environments and the
four less stressful noncinder environments that we
31
Piftons at Sunset Crater vary in susceptibility to
moth attack; resistant trees experience chronically
low levels of moth attack while susceptible trees
growing nearby experience chronically high levels
of moth herbivory (Whitham and Mopper 1985).
Furthermore, resistant and susceptible pi:ii.ons
differ genetically in both allelic frequency and
heterozygosity (Mopper et al. 1991). Our data
suggest that resistant and susceptible trees may
also be present at cinder sites other than Sunset
A.
o
Pinyon
10
~s
7.5
Crater. Although we have no genetic data for these
other sites, trees at these sites varied ten-fold or
more from one another in level of moth herbivory.
Based upon our genetic studies of other sites, these
findings suggest that some of these trees were
resistant while others were susceptible (Gehring
and Whitham, unpub. data).
Juniper trees showed a similar pattern with
regard to environmental stress - junipers growing
in the cinders of Sunset Crater had higher levels of
mistletoe parasitism than junipers growing at a
nearby noncinder site (Gehring and Whitham
1992) (fig. IB). The mistletoe, Phoradendron
juniperinum removes water, minerals, and carbon
from its host plant (Hull and Leonard 1964,
Ehleringer et al. 1985, Marshall and Ehleringer
1990) causing branch die-back and increased water
stress in heavily infested plants (Ferrell 1974,
Knutson 1983). The difference between sites in
mistletoe parasitism was largely due to higher
levels of mistletoe infestation in female treesfemale trees at Sunset Crater had three-fold higher
levels of mistletoe parasitism than male trees at
Sunset Crater or than male or female trees at the
noncinder site (Gehring and Whitham 1992) (fig.
IB).
The higher levels of mistletoe parasitism on
female junipers at the stressful site could be due to
a preference by avian mistletoe seed dispersal
agents for female trees (Gehring and Whitham
1992). Female junipers possess two potential food
resources -mistletoe berries and juniper berries,
and birds may thus spend more time on female
trees than male trees, and deposit more mistletoe
seeds there. However, our finding that male and
female junipers growing in the less stressful
environment did not differ in mistletoe parasitism,
even though they possessed a similar avifauna and
abundant berries, is not consistent with this
hypothesis.
A second hypothesis to explain the difference
between sexes in mistletoe parasitism is that
mistletoe growth and survival is greater on female
trees than male trees in the stressful cinder
environment (Gehring and Whitham 1992). Female
junipers may be less resistant to mistletoe attack
than male junipers if they are under greater stress
as are females of several other dioecious plant
species (Stark 1970, Hikmat et al. 1982, Freeman
and MacArthur 1982). The male-biased sex ratio
(1.56 males for every female) at the stressful site is
consistent both with the hypothesis that female
junipers are under greater stress in that
environment, and with studies of biased sex ratios
a
Q)
---e>=
~
CD
...
::J:
en
0
0
oJ::
0 ~
0
::E
5
.s:::.
en
-
2.5
b
0
B.
E
til
;:::
(f)
-;; E
...caca --en
a..
Juniper
1.5
1.0
Q)
0
CD Q )
0 ;::
a;
u;
:i
en
~
-
0.5
0
male female
Cinder
male
female
Noncinder
Figure 1A.-Level of stem- and cone-boring moth herbivory on
pinon pines growing in cinder and sandy loam soUs. Values
are means ± S.E. and represent the average of four cinder
and four sandy loam sites in northern Arizona. Different
~etters above the bars denote significant differences at p <
0.05 and were adapted from Gehring and Whitham (19Mb).
Figure 1 B.-Level of mistletoe parasitism on male and female
junipers at one cinder and one noncinder site. Data are means
± 1 S.E. and were adapted from Gehring and"Whltham (1992).
Different letters above the bars denote significant differences
atp < 0.05.
32
in junipers and other plant species (Freeman et al.
1976).
Experimental studies demonstrate that the
increased susceptibility of piftons to moth
herbivory described here is, at least in part, caused
by environmental stress. Moth-susceptible pinons
at the Sunset Crater site that received
supplemental
nutrients
and
water
to
experimentally reduce environmental stress,
prod uced significantly higher levels of defensive
resins (60% increase) and suffered significantly less
moth herbivory (9% reduction) relative to
untreated control trees (Cobb et al., in review).
These
results
provide
observational and
experimental support for the plant stress
hypothesis (White 1969, 1974, 1976, 1984) which
predicts that herbivore performance will be higher
on stressed plants.
Mutualistic Effects
of Ectomycorrhizae
1.25
§
...
1.00
.c
0)
~
'0
0
.c
c
=sCD
CD
en
Figure 3.-Shoot weight of pinon seedlings grown in cinder solis
with lower (80 or less) or higher (150 or more) numbers of
ectomycorrhizal roots. Data are means ± 1 S.E. and were
adapted from Gehring and Whitham (1994b). Different letters
above the bars denote significant differences at p < 0.05.
environments where soil fertility is low and the
need for enhanced nutrient and moisture uptake is
greatest (Meyer 1973). Although we do not have
comparable data for the vesicular-arbuscular
mycorrhizae of juniper, similar relationships
between soil fertility and vesicular-arbuscular
mycorrhizal colonization were found by Boerner
(1986) and Van Noordwijk and Hairiah (1986).
However, other researchers have observed no
significant correlation between ectomycorrhizal
colonization and soil fertility (e.g., Lee and Lim
1989, McAfee and Fortin 1989), and the results of
studies that monitored changes in ectomycorrhizal
colonization following nutrient supplementation
are similarly variable, suggesting that other factors
are also important (e.g., Gagnon et al. 1987,
Arnebrant and Soederstroem 1990, MacFall et al.
1990, Termorshuizen and Ket 1990) .
Although cinder and noncinder site PIDons
differed in ectomycorrhizal colonization, data from
seedling studies in the greenhouse demonstrate
that ectomycorrhizae enhance seedling growth in
both soil types. We observed a significant positive
correlation between ectomycorrhizal abundance
(total # of ectomycorrhizal roots) and shoot weight
for seedlings grown in both cinder and noncinder
soil types (Gehring and Whitham 1994b). For
example, in cinder soils, the shoot weight of
seedlings with high numbers of ectomycorrhizae
60~---------------------'
50
40
"iii
N
:c
...
...o
g.
30
b
20
E
-e
w
10
o
Cinder
High
# of Ectomycorrhizae
Ectomycorrhizae on Pinyon
o
0.25
0
Environmental stress was also significantly
associated with ectomycorrhizal colonization in
pinon pines. Pinons growing in four cinder
environments had, on average, two-fold higher
levels of ectomycorrhizal colonization than pinons
growing in four sandy loam soil sites (Gehring and
Whitham 1994b) (fig. 2). This result is consistent
with the hypothesis that ectomycorrhizae are most
important to plants growing in stressful
(5
0.75
en 0.50
0)
ECTOMYCORRHIZAL COLONIZATION IN
PINON INCREASES WITH PLANT STRESS
c
o
~
N
"2
o
b
Noncinder
Figure 2.-Levels of ectomycorrhizal colonization of pinons
growing In cinder and sandy loam soils. Values are means ±
1 S.E. and represent the average of four .cinder and four
sandy loam sites. Different letter above the bars denote
significant differences at p < 0.05. Data were adapted from
Gehring and Whitham (1994b).
33
(150 or more) was approximately 44% higher than
the shoot weight of seedlings with lower numbers
of ectomycorrhizae (80 or less )(fig. 3). This positive
relationship between ectomycorrhizae and shoot
growth suggests that any environmental factor that
reduces ectomycorrhizae could negatively affect
pifton growth.
Ectomycorrhizae on Pinyon Pine
100
JS
:2 c
t:: "~
o
...
(,) JS
"-
~ C
E
A. Moth Herbivory
B. Scale Herbivory
Susceptible Susceptible
Control
Moth
Removal
Susceptible Susceptible
Control
Scale
Removal
75
50
0..2
~ 8 25
HERBIVORES AND MISTLETOE PARASITES
NEGATIVELY AFFECT MYCORRHIZAE IN
PINONS AND JUNIPERS
tft
o
In both piftons and junipers, we observed a
between
significant
negative
relationship
mycorrhizal colonization and pest attack In mature
piftons, ectomycorrhizal colonization of trees
resistant to moth attack was approximately 30%
greater than ectomycorrhizal colonization of mothsusceptible trees in the cinder soils of Sunset Crater
(Gehring and Whitham 1991). Removal of moths
from susceptible trees resulted in a rebound in
ectomycorrhizal colonization demonstrating that
the moth was responsible for the mycorrhizal
reductions in susceptible trees (fig. 4A). Younger
piftons that experienced severe herbivory by a
needle-feeding scale insect also suffered significant
reductions in ectomycorrhizal colonization that
were eliminated following insect removal (Del
Vecchio et al. 1993)(fig. 4B).
A similar negative relationship between pest
attack and mycorrhizal colonization is found in
one-seeded juniper even t~ough junipers have a
different type of mycorrhizal mutualist and are
hypothesized to be better adapted to arid
conditions than pifton pines. Vesicular-arbuscular
mycorrhizal colonization of juniper roots was 30%
lower in trees with high mistletoe densities than in
trees with low mistletoe densities (Gehring and
Whitham 1992) (fig. 4C). The consistent nature of
these results suggests that even the mycorrhizae of
more dry-adapted species will decline following
pest attack
To assess the importance of environmental
stress to the interactions between mycorrhizae and
aboveground pests, we simulated herbivory at a
sandy loam site and compared the mycorrhizal
responses of trees at this site to trees experiencing
the same type of simulated herbivory at a cinder
site. Our results indicate that environmental stress
is an important component of the interactiontrees at the cinder site experienced declines in
ectomycorrhizal colonization while those at the
sandy loam site did not (Gehring and Whitham, in
prep.). These findings suggest that environmental
Vesicu lar-arbuscu lar Mycorrhizae
on Juniper
...
C
0
80
.5
0
60
~
(,)
as
~~
"2
U)
~o
C. Mistletoe Parasitism
b
a
as 1ii 40
'3 N
('):2
"r;; t:: 20
~
~oo
g
~
E
0
High Mistletoe
Low Mistletoe
Figure 4.-The relationship between moth (A) and scale (8)
herbivory and ectomycorrhizal colonization In pUlon pine, and
the relationship between mistletoe parasitism and vesiculararbuscular mycorrhizal colonization In juniper (C). Graphs A
and 8 demonstrate that ectomycorrhlzal levels Increased
following herbivore removal In pinons, while Graph C shows
that veslcular-arbuscular mycorrhizal colonization of juniper
roots Is lower In heavily mistletoe parasitized trees; Values
are means + 1 S.E. and different letters above the bars denote
significant differences at p < 0.05. Data were adapted from
Gehring and Whitham 1991, 1992, and Del Vecchio et aI.,
1993).
stress not only influences the responses of
mycorrhizae and herbivores individually, but also
influences the interactions between the two. Trees
growing in more benign environments may be able
to retain their mycorrhizae following herbivory or
other pest attacks while trees growing in more
stressful environments cannot.
MANAGEMENT IMPLICATIONS
Our findings, summarized in Table 2, have
several potential implications for the management
34
Table 2 - Summary of interactions among environmental stress, pest attack, and myconhizal colonization
in pinyons and junipers.
Higher Environmental Stress
Lower Environmental Stress
Factor
Pinyon
Juniper
Pinyon
Juniper
pest attack
high moth herbivory
high mistletoe
parasitism
( Q > d)
low moth herbivory
low mistletoe
parasitism
no data
low ectomycorrhizal
colonization
no data
hi~ levels of mislletoe
no elfec1 of simulated
herbivory on
ectomyconhizae
no data
myconflizae
mycon11izae·pest
Interaction
:!toonizalion
ectomycorrhizal
natural or simulated
herbivory causes
declines in
ectomycorrhizae
parasitism associated
with declines in
vesicular-arbuscutar
mycorrhizae
of pmon-juniper woodlands. First, our results
suggest that pmons and junipers are more likely to
experience attack by three different pests as
environmental stress increases. This finding is
especially noteworthy because these pests exhibit
the same patterns even though they have different
lifestyles and feeding modes; a parasitic mistletoe
that feeds from the xylem sap, a scale insect that
feeds from the mesophyll of needles from juvenile
plants, and a stem- and cone-boring moth that
attacks mature trees. These results have
implications for broad issues associated with global
climate change. For' example, if environmental
threats such as global warming cause soil in more
benign environments to become warmer and drier
(two characteristics of the stressful environments
we studied), our findings suggest that trees
growing in warmer conditions would experience
increased susceptibility to attack_by a variety of
pests and would, as a result, suffer reduced rates of
growth
and
reproduction.
Ayres'
(1993)
observation that the rate" of increase of moth
populations on mountain birch trees was 2.9-fold
higher on trees growing in a greenhouse warmed
by only one degree Celsius relative to controls
supports this hypothesis. Ayres (1993) predicted
that global warming of only 2 to 4 degrees would
lead to outbreaks of many insect herbivores if
insects are generally more sensitive to temperature
increases than their host plants. However, we
believe that plant-herbivore responses to global
warming are likely to be more complex than this.
For example, 75% of the 450 studies reviewed by
Waring and Cobb (1992) reported significant
herbivore responses to plant stress.
These
responses varied from positive to negative to
nonlinear and depended upon the types of plants
(e.g., flowering plants vs. conifers) and "the resource
requirements of the herbivores involved (Waring
and Cobb 1992).
( Q
= d)
Second, our data suggest that the mycorrhizae
of pifton-juniper woodlands are also likely to be
affected by global climate change, although the
response of mycorrhizae is less clear. Our finding
that pmons growing in stressful cinder
environments have higher ectomycorrhizal levels
than piftons growing in sandy loam soils leads us
to predict that mycorrhizal colonization would
increase with global warming. We found that
pmons growing in sandy loam soils had 33%
higher levels of ectomycorrhizal colonization
during a drier year than a moister year, supporting
this hypothesis (Gehring and Whitham, unpub
data).
However, we have shown that pests such as
herbivores and mistletoes have a negative effect on
mycorrhizae and have hypothesized that the
densities of these pests were likely to increase with
global warming. Therefore, any increases in
mycorrhizae observed in response to the increased
abiotic stress of warmer, drier soil could be offset by
decreases in mycorrhizal colonization in response
to increased pest attack The mycorrhizae of some
herbaceous species, especially grasses, have been
shown to be reduced· by herbivory (e.g.,
Bethlenfalvay et al., 1988, reviewed by Gehring and
Whitham 1994a) suggesting that pifton-juniper
community understory species may exhibit similar
complicated relationships with environmental
stress and parasite attack
Third, the negative association we observed
between aboveground pests and belowground
mutualists emphasizes the importance of stud~g
both components of the plant (shoot and root
systems) in concert. Assessment of damage to
aboveground tissues alone does not give us a
complete understanding of the impacts of
aboveground
pest
attack
For
example,
aboveground herbivory has negative effects on
pifton ectomycorrhizae in cinder soils, but not in
35
Second, because plant genetics plays a role in
pifton drought tolerance and resistance to insect
herbivory, environmentally stressful areas such as
Sunset Crater are important to conserve because of
the unique plant genotypes they possess. For
example, Sunset Crater and other cinder sites may
contain some of the most drought-tolerant and
insect-resistant pifton genotypes. These stresstolerant genotypes could be commercially
important for outplanting in arid areas, and could
serve as adapted gene pools in the event of global
warming and pifton die-back Thus, although it is
important to preserve the center of a species
distribution, where its growth and reproduction is
greatest, the conservation of more extreme
boundary populations under greater biotic and
abiotic stress may be of equal importance.
sand y loam soils, s ugges ting that the effects of
aboveground herbivory on belowground processes
can vary with environmental stress and may not be
easily predicted. The same is likely to be true for
other aboveground stressors such as grazing, some
fires, etc.
Finally, the patterns of increasing herbivory
and mycorrhizal reductions on trees growing in
cinder soils have additional management
implications because they are associated with host
plant genetics. Mopper at al. (1991) found genetic
differences both between pinons growing in cinder
and noncinder soils, and between moth-resistant
and moth-susceptible piftons growing in the
cinders. Furthermore, Cobb and Whitham (1994)
observed an association between growth and
genotype in piftons growing in the cinders, and
found that the slowest growing genotypes were
significantly less abundant in mature trees than
juvenile trees suggesting that selection had favored
the fastest growing genotype. These differences
suggest that the abilities of pinons at Sunset Crater
to survive and to resist herbivory are likely to be
genetically based.
These results have two
additional implications for the management of
pifton-juniper woodlands.
First, these genetic data combined with data on
the associations between pinon community
members and pinon insect resistance, argue that
there is a genetic basis to pifton community
structure that links community members. We have
already described linkages between mycorrhizal
mutualists and insect-resistant and insectsusceptible piftons. In addition, Christensen and
Whitham (1991, 1993) found that moth herbivory
on insect-susceptible trees had significant impacts
on the birds and mammals dependent upon pifton
seeds for food. Thus, through its negative effect on
the cone production of genetically susceptible
trees, moth herbivory caused a shift in the balance
between birds and mammals. At stressed sites with
high levels of moth herbivory, the majority of the
pifton crop was harvested by mammals, who act as
seed predators, rather than by birds who are
important seed dispersers (Christensen and
Whitham 1991, 1993). Such plant genetics-based
linkages between diverse taxa in pifton-juniper
woodlands may make this community more
susceptible to environmental perturbations than
other communities where members are less tightly
linked or are loose assemblages of species.
Therefore, management decisions that affect one
community member (e.g., pifton pine) may have
repercussions on the entire community dependent
upon that species.
ACKNOWLEDGEMENTS
The work reviewed here was supported by
USDA grants 91-37302-6224 and 92-37302-7854,
DOE grant DE-FG03-94ER61849, and NSF grant
BSR-9107042. The authors thank the U.S. Forest
Service for access to the study sites.
LITERATURE CITED
Arnebrant, K., Soederstroem, B. 1990. The influence of
nitrogen fertilization on ecotmycorrhizal mycelial
colonization and infection. Agriculture Ecosystems
and Environment 28: 21-25.
Ayres, M.P. 1993. Plant defense, herbivory, and climate
change. In: Biotic Interactions and Global Change.
P.M. Kareiva, J.G. Kingsolver, and R.B. Huey, eds.,
Sinauer Associates Inc., Sunderland, MA, pp. 75-94.
Bethlenfalvay, G.J., Thomas, R.S., Dakessian, 5., Brown,
M.S., Ames, R.N. 1988. Mycorrhizae in stressed
environments: effects on growth, endophyte
development, soil stability, and soil water. In: Arid
Lands Today and Tomorrow. E.A. Whitehead, C.R
Hutchinson, B.N. Tunmerman, and R. G. Varady,
eds., Westview Press, Boulder, CO, pp. 1015-1029.
Boerner, R.E.J. 1986. Seasonal nutrient dynamics,
nutrient resorption, and mycorrhizal infection
intensity of two perennial forest herbs. American
Journal of Botany 73: 1249-1257.
Christensen, K.M., Whitham, T.G. 1993. Herbivore
impact on competition between birds and mammals
for pinyon seeds. Ecology 74: 2270-2278.
Christensen, K.M., Whitham, T.G. 1991. Indirect
herbivore mediation of avian seed dispersal in
pinyon pine. Ecology 72: 534-542.
36
Mistletoes. D. Calder, and P. Bernhardt, eds.,
Academic Press, Sydney, pp. 295-316.
Lee, S.S., Lim, K.L. 1989. Mycorrhizal infection and foliar
phosphorous content of seedlings of three
dipterocarp species growing in a selectively logged
forest and a forest plantation. Plant and Soil 117: 237241.
MacFall, J.S., Iyer, J., Slack, S., Berbee, J. 1990.
Mycorrhizal-phosphorous interaction on red pine
(Pinus resinosa Ait). Agriculture Ecosystems and
Environment 28: 321-324.
Marshall, J.D., Ehleringer, J.R. 1990. Are xylem-tapping
mistletoes partially heterotrophic? Oecologia 84: 244248.
McAfee, B.J., Fortin J.A. 1989. Ectomycorrhizal
colonization on black spruce and jack pine seedlings
outplanted in reforestation sites. Plant and Soil 116: 917.
Meyer, RH. 1973. Distribution of ectomycorrhizae in
native and man-made forests. In: Ectomycorrhizae:
Their Ecology and Physiology. J.C. Marks and T. T.
Kozlowski, eds., Academic Press, New York, NY, pp.
79-106.
Mopper, S., Mitton, J., Whitham, T.G., Cobb, N.,
Christensen, K.M. 1991. Genetic differentiation and
heterozygosity in pinyon pine associated with
herbivory and environmental stress. Evolution 45:
989-999.
Stark, N. 1970. Water balance of some warm desert
plants in a wet year. Journal of Hydrology 10: 113126.
Termorshuizen, A.J., Ket, P.C. 1990. The effects of
fertilization with ammonium and nitrate on
mycorrhizal seedlings of Pinus sylvestris. Agriculture
Ecosystems and Environment 28: 497-501.
Van Noordwijk, M., Hairiah, K. 1986. Mycorrhizal
infection in relation to soil pH and soil phosphorous
content in a rain forest of northern Sumatra. Plant
and Soil 96: 299-302.
Waring, G.L., Cobb, N.S. 1992. The impact of plant stress
on herbivore population dynamics. In: Plant-Insect
Interactions., E. A. Bernays, ed., CRC Press, Boca
Raton, FL, pp 167-226.
White, T.C.R. 1984. The abundance of invertebrate
herbivores in relation to the availability of nitrogen in
stressed food plants. Oecologia 63: 90-105.
White, T.C.R. 1976. Weather, food, and plagues of locusts.
Oecologia 22: 119-134.
White, T.C.R. 1974. A hypothesis to explain outbreaks of
looper caterpillars with special reference to
populations of Selidosema suavis in a plantation of
Pinus radiata in New Zealand. Oecologia 16: 279-301.
White, T.C.R. 1969. An index to measure weatherinduced stress of trees associated with outbreaks of
psyUids in Australia. Ecology 50: 905-909.
Whitham, T.G~, Mopper, S. 1985. Chronic herbjvory:
impacts on architecture and sex expression of pinyon
pine. Science 227: 1089-1091.
Cobb, N.S., Whitham, T.G. 1994. Genetic variation
associated with chronic water and nutrient stress in
pinyon pine. American Journal of Botany 81: 936940.
Cobb, N .S., Mopper, S., Gehring, C., Caouette, M.,
Christensen, K.M., Whitham, T.G. Herbivore response
to stress and experimental stress release in pinyon
pine. Submitted to Ecology.
Del Vecchio, 'I, Gehring, C.A., Cobb, N.5., Whitham, T.G.
1993. Negative effects of scale insect (Matsucoccus
acalyptus) herbivory on the ectomycorrhizae of
pinyon pine. Ecology 74: 2297-2302.
Ehleringer, J.R., Schulze, E-D, Ziegler, H., Lange, O.L.,
Farquhar, G.D., Cowan, I.R. 1985. Xylem-tapping
mistletoes: water or nutrient parasites? Science 227:
1479-1481.
Ferrel, G.T. 1974. Moisture stress and fir engraver
(Coleoptera: Scolytidae) attack in white fir infected
by true mistletoe. The Canadian Entomologist 106:
315-318.
Freeman, D.C., McArthur, E.D. 1982. A comparison of
twig water stress between males and females of six
species of desert shrubs. Forest Science 28: 304-308.
Freeman, D.C., Kllkoff, L.G., Harper, K.T. 1976.
Differential resource utilization by the sexes of
dioecious plants. Science 193: 597-599.
Gagnon, J., Langois, C.G., Fortin, J.A. 1987. Growth of
containerized jack pine seedlings inoculated with
different ectomycorrhizal fungi under a controlled
fertilization schedule. Canadian Journal of Forest
Research 17: 58-62.
Gehring, C.A., Whitham, T.G. 1994a. Interactions
between aboveground
herbivores and
the
mycorrhizal mutualists of plants. Trends in Ecology
and Evolution 9: 251-254.
Gehring, C.A., Whitham, T.G. 1994b. Comparisons of
ectomycorrhizae on pinyot:\s pines (Pinus edulis;
Pinaceae) across extremes of soil type and herbivory.
American Journal of Botany, in press.
Gehring, C.A., Whitham, T.G. 1992. Reduced
mycorrhizae on Juniperus monosperma with mistletoe:
the influence of environmental stress and tree gender
on a plant parasite and a plant-fungal mutualism.
Oecologia 89: 298-303.
Gehring, C.A., Whitham, T.G. 1991. Herbivore-driven
mycorrhizal mutualism in insect-susceptible pinyon
pine. Nature 353: 556-557.
Hikmat, A.A.A., Strain, B.R., Mooney, H.A. 1972. The
physiological ecology of diverse populations of the
Journal of
desert shrub, Simmondsia chinensis.
Ecology 60: 41-57.
Hull, R. J., Leonard, O.A. 1964. Physiological aspects of
(Arceuthobium
and
parasitism in
mistletoes
Phoradendron) I. The carbohydrate nutrition of
mistletoes. Plant Physiology 39: 996-1007.
Knutson, D.M. 1983. Physiology of mistletoe parasitism
and disease responses in the host. In: The Biology of
37