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An Ecosystem-Centered View of Insect and
Disease Effects on Forest Health
T.D. Schowalter1
Abstract - Phytophagous insects and pathogens traditionally have been
blamed for' declines in forest health. Accumulating evidence, however,
supports an ecosystem-centered view that these organisms respond to
changes in forest condition in ways that contribute to maintenance or
recovery of forest functional equilibrium, i.e., forest health. Populations of
phytophagous insects and pathogens grow on abundant and/or susceptible
host species. Pruning and thinning reduce competition, enhance productivity
of survivors, and promote non-host plant species. Turnover of plant parts
through herbivory, mortality and decomposition maintains nutrient cycling
processes essential to soil fertility and permits reallocation of resources from
inefficient plant parts to younger tissues. Accumulated fuel increases the
likelihood of regular, low-intensity fires that mineralize litter and maintain
forest structure. Because tree species are adapted to different conditions
following disturbances, increased diversity promotes functional stability and
recovery of the forest ecosystem. Few studies have addressed integrated
or long-term effects. Contributions to the health and stability of forest
ecosystems should be addressed for balanced assessment of impact and
need for suppression of insects and pathogens.
INTRODUCTION
tree establishment, growth and survival cannot address
integrative and longer-tenn effects on ecosystem processes that
contribute to forest health; studies of integrated ecosystems that
do not monitor or manipulate insects and pathogens cannot
provide insight into feedback effects. Although non-confounding
experimental manipulation of insect or pathogen abundance in
mature forests is difficult, techniques have been developed for
manipulation of bark beetles (e.g., Schowalter and Turchin
1993). Defoliation often has been simulated by artificial clipping
of foliage, but this technique does not simulate all effects of
natural defoliation (Schowalter et al. 1986). Adequate replication
of randomly assigned treatment plots in integrated ecosystems
requires improved cooperation between scientists and resource
managers.
This paper describes an ecosystem-centered view of forest
insects and pathogens, not as "pests" but as indicators of forest
condition (health) and regulators of forest function. Although
some insect and pathogen effects may continue to intetfere with
some forest management goals, consideration of their potential
role in maintaining health is essential to balanced assessments
of impacts and need for suppression of these organisms and to
diagnosis and treatment of forest condition
phytophagous insects and pathogens are major components
of forest ecosystems, representing most of the biological
diversity and affecting virtually all forest processes and uses.
They have been viewed as detrimental to forest health and
commercial production of forest products and have been taIgets
of suppression efforts. However, accumulating evidence
indicates that many "pests" may be instrumental in maintaining
ecosystem processes critical to forest health.
Despite theoretical consideration of insect and pathogen
contnbutions to ecosystem stability through feedback effects on
ecosystem processes (Mattson and Addy 1975; Schowalter et al.
1981, 1986; Seastedt and Crossley 1984), few experimental
studies have evaluated insect and pathogen roles, especially in
forests. Advances in this area require an ecosystem framework
for experiments, with randomly replicated insect or pathogen
abundances, designed to evaluate effects on integrated ecosystem
processes. Narrowly-focused studies of effects on commercial
1 Tim Schowalter is professor of forest entomology and
ecosystem ecology in the Entomology Department at Oregon State
University, Corvallis.
189
ASSESSMENT OF FOREST HEALTH
Discussion of forest health requires definition and appropriate
measures of forest health. I will use an ecosystem-based
definition of forest health, i.e., the ability to maintain or recover
long-term functional equilibrium. Functional equilibrium
represents a dynamic balance between dissipative forces and
ecosystem processes that maintain suitable conditions for
sustained productivity (fig. 1).
1.0
1.0
1----..-
---_
.....
TIME
Figure 2. - Hypothetical relationship between resource
demand:resource supply ratio (solid line) and
insect/pathogen abundance (dashed line). Stress resulting
from insufficient resources (demand/supply >1.0) triggers
insect and pathogen responses that suppress hosts (reduce
demand); nutrient subsidy resulting from demand/supply
<1.0 stimUlates productivity and tolerance to
insect/pathogen-enhanced
turnover;
balanced
demand/supply (= 1.0) limits resources for insects and
pathogens.
(feedback) processes. This view differs from a commercial, site
or stand based view that emphasizes persistence and maximum
growth of a particular forest community.
Impaired health reflects functional degradation, often
indicated by insect or pathogen responses to host stress resulting
from extreme climate fluctuation (or change), increased
crowding, and/or substmte deteriomtion (Lorio et al. 1993,
Mattson and Haack 1987). Stressed plants alter resource
allocation between growth, defense, and other metabolic
pathways, often becoming more susceptible to phytophagous
insects and pathogens (Bazzaz et al. 1987, Lorio et aI. 1993).
Rapidly growing plants also can become vulnerable as a result
of phenological or physiological processes that limit expression
of defensive ability (Lorio et al. 1993).
Closely spaced hosts are likely to trigger outbreaks of insects
and pathogens. In diverse forests, potential hosts can be
"hidden" among non-host vegetation; even vulnerable trees may
be relatively resistant to small numbers of insects or pathogen
propagules that find their way through surrounding non-hosts
(Hunter and Arssen 1988, Waring and Pitman 1983). Tree
turnover will be low and continuous in such forests. Conversely,
in monocultures tree defenses can be sunnounted quickly by
larger numbers of insects or pathogens dispersing from
surrounding conspecific trees, especially during vulnerable
periods. (Schowalter and Turchin 1993, Waring and Pitman
1983). Outbreaks of phytophagous insects and pathogens
abruptly reduce dense host populations (to levels incapable of
sustaining the outbreak) and promote resource turnover and
non-host productivity.
Figure 1. - Simplified ecosystem model showing pools (boxes)
and mediating processes (ovals). with arrows showing
direction of effect. Positive and negative feedbacks maintain
functional equilibrium and modify abiotic conditions.
Ecosystem development reflects the cumulative ability of the
community to modify environmental conditions. For example,
interception of incoming solar radiation, precipitation, and air
currents by vegetation reduces surface tempemture, erosion, and
wind speed. These processes maintain modemte tempemtures
and relative humidities, and facilitate acquisition, retention and
uptake of resources (e.g., Hobbie 1992, Lucas et al. 1993,
McCune and Boyce 1992). The massive structures characterizing
forests exemplify ecosystem regulation of climate and nutrient
fluxes (Dickinson 1987) and may buffer forests against
significant change in external conditions (Franklin et al. 1992).
Forest health depends on replacement of weak or intolerant
organisms by more tolemnt organisms and on turnover of
resources to prevent bottlenecks in fluxes of critical resources
(processes accelerated by insects and pathogens) as
environmental conditions change (fig. 2). At the same time,
species critical to recovery of internal environment and to
nutrient retention following disturbances depend on sufficiently
large canopy gaps (often created by insects and pathogens) for
survival. Accordingly, the shifting mosaic of successional
communities that compose the forest landscape represents a
healthy forest ecosystem in functional equilibrium with abiotic
conditions. Forest health can be represented by multiple
equilibrium states reflecting tradeoff's among various regulatory
190
dramatically. In an ecosystem (cybernetic) sense, these
organisms potentially function to regulate ecosystem processes,
including the timing and rate of plant growth, hydrology, carbon
and rutrient fluxes, and vegetation composition {Mattson and
Addy 1975, Seastedt and Crossley 1984).
Elevated insect or pathogen activity on stressed vegetation
reduces growth and hastens host decline and replacement.
However, surviving trees may show compensatory growth if
defoliation alleviates stressful conditions (Schowalter et al. 1986,
Trumble et al. 1993). Wickman (1980) and Alfaro and
MacDonald (1988) found that, following the expected short-tenn
growth depression dUring the period of conifer defoliation,
defoliated trees grew faster during the next 2-3 decades, more
than replacing the lost growth (fig. 3). In fact, Alfaro and
MacDonald (1988) found that the magnitude of this
compensatory growth following defoliation was inversely
proportional to the severity of defoliation Schowalter et al.
(1991) reported that manipulated levels of defoliation (up to
20%) by lepidopteran 13.IVae did -not reduce growth or nutrient
content of young Douglas-fir. All saplings doubled in size over
the 3-year period, indicating compensation by the defoliated
saplings. Compensatory growth may reflect improved water or
rutrient conditions, as described below.
Insect and pathogen effects on canopy structure affect
interception of precipitation and evapotranspiration Reduced
canopy coverage increases precipitation penetration through the
canopy and reduces evapotranspiration (Klock and Wickman
1978, Leuschner and Berck 1985, Schowalter et al. 1991, Swank
et al. 1981). Schowalter et al. (1991) reported that 20% foliage
removal by native defoliators doubled the amount of
precipitation reaching the forest floor under Douglas-fir saplings
during the relatively dry spring and summer in western Oregon
Increased soil temperature and moisture, as well as nutrients
and, perhaps, herbivore products, improves the lifter
environment for saprophagous organisms, especially during drier
Insects and pathogens (along with fire) traditiona1ly have been
considered to impair forest health. Howeve~ moderate pruning,
thinning and litter mineralization resulting from interaction
among insects, pathogens, and fire in unmanaged forests are
important processes that facilitate rutrient turnover (especially
in arid regions) and maintain vegetation structure and diversity
(e.g., Schowalter et al. 1981). Outbreaks and catastrophic fire
result from impaired litter decomposition and nutrient cycling
in dense managed forests protected from frequent, low intensity
fires (Hagle and Schmitz 1993, Schowalter et al. 1981).
Maintenance or restoration of .forest health will require
attention to ecosystem processes and natural regulatory
mechanisms. Measures of forest health include a) balanced
vs. resource supply
resource accumulation in biotic
through input and turnover processes, as this balance affects
forest productivity, b) community ability (through species
interactions) to regulate nutrient flow rates and lag times and
thereby minimize variation, and c) community regulation of
internal climate and substrate conditions essential for continuous
resource turnover and availability. Bottlenecks in
biogeochemical cycling result from excessive tree density and
resource accumulation in slow turnover sinks such as wood and
from inhibition of critical control processes (such as nitrogen
fixation and establishment of species that maintain key processes
following distuIbances). Insect and pathogen outbreaks can be
viewed as triggered responses that indicate and alleviate
imbalances in nutrient turnover or other processes (fig. 2).
sinks
INSECT AND PATHOGEN EFFECTS ON
FOREST FUNCTION
phytophagous and saprophagous invertebrates and pathogens
are capable of rapid responses to changing conditions and can
affect vegetation composition and turnover processes
2
;;
...
Q)
(J
Q)
Co
)(
w
:c
Defoliation
Q)
>
Q;
II)
.c
Q.
1
X
w
C
- - Severe Defoliation
~
J:
• • • • • •• Moderate Defoliation
~
~
0
- • - • - No Defoliation
a:
CJ
0
0
5
10
15
20
25
30
35
40
45
50
TIME (Years)
Figure 3. - Long-term trends in tree growth index following defoliation. Note initial reduction in growth followed by long-term
compensatory growth. Adapted from Alfaro and MacDonald (1988) and Wickman (1980).
191
periods (Schowalter and Sabin 1991, Seastedt and Crossley
1983). These OIganisms are critical to litter decomposition and
to porosity (water stomge) of woody litter and soil. Improved
water balance enhances plant SUIVival during drought.
Catbon flux is affected by changes in canopy structure and
plant metabolism, such as caused by insects or pathogens. Oaks,
maples and birches showed increased carbon dioxide
assimilation by residual and regrowth foliage following artificial
defoliation (Heichel and Thmer 1983, Prudhomme 1983).
Defoliation can mobilize carbon from starch reserves in older
foliage and wood for productiop of new foliage (Webb 1980).
Canopy opening increases soil tempemture and moisture,
conditions that promote decomposition and catbon dioxide flux
to the atmosphere. Effects on carbon flux influence carbon
tmnsformation and turnover processes, hence ecosystem
energetics.
Phytophagous insects and pathogens stimulate nutrient
cycling in several ways. These organisms can concentrate major
cations several orders of magtritude over plant and soilllitter
concentrations (Cromack et al. 1975, Schowalter and Crossley
1983). For example, defoliators are particularly rich sources of
potassium, calcium and magnesium (Schowalter and Crossley
1983). The elemental pools represented by these organisms are
nonnally small relative to plant and soilllitter pools but could
become important short-turnover pools during outbreaks
(Schowalter and Crossley 1983).
Insects and pathogens are major regulators of nutrient
turnover from plant biomass. Pruning and/or thinning stimulate
plant growth by reducing competition for limited plant resources
(Velazquez-Martinez et al. 1992). Folivorous insects and
pathogens typically remove less than 10% of foliage and shoots,
apparently functioning as natum1 pruning agents (Schowalter et
al. 1986). Removal of these plant parts reduces plant metabolic
demands and facilitates reallocation of plant resources.
Turnover of plant parts throughout the growing season
provides more constant tnltrient input to litter, compared to
seasonal littetfall (fig. 4), thereby contributing to forest floor
processes and soil fertility (Risley 1993). Kimmins (1972)
reported that experimentally elevated sawfly populations
increased cesium-134 turnover from young red pine, primarily
through leaching from chewed leaf surfaces. Schowalter et al.
(1991) and Seastedt et a!. (1983), manipulated folivore
abundance in yotmg coniferous forest and deciduous forest,
respectively, and found that phytophagous arthropods
significantly increased turnover of biomass, nitrogen,
phosphorus and potassium from foliage to litter (fig. 4).
Schowalter et al. (1991), but not Seastedt et al. (1983), also
found that phytophagous arthropods significantly increased
calcium turnover from young conifers. Calcium generally is
considered a relatively immobile element, but enhanced turnover
to the acidic soils under conifers could promote soil fertility and
biological activity. Insects and pathogens can improve quality
of litter detoxified during digestion (Zlotin and Khodashova
1980) but may reduce quality of residual and regrowth foliage
with high content of induced inhibitory compounds (Rhoades
1983, Schultz and Baldwin 1982). Defoliation also can stimulate
nitrogen ftxationand nitrification processes on the forest floor,
reflected in increased export by streams (Swank et al. 1981).
Xylophagous insects and root pathogens are instrumental in
initiating decomposition and nutrient turnover from dying trees
and woody litter. Beetles, especially, penetmte bark and inoculate
wood with saprophytic and nitrogen-fIxing microorganisms
0.014
0.012
U
01
.!!!
~
Exclusion
•
Sap-suckers
•
Defoliators
0.01
:2
01
D
0.008
en
en
<
:E 0.006
a:
w
~
:::; 0.004
0.002
0
Jan-Mar
Apr-Jun
Jul-Sep
Oct-Dec
SEASON
Figure 4. - Seasonal litterfall of young Douglas-fir in western Oregon during 1983-1986, as affected by sap-sucking insects feeding
April-September, defoliating insects feeding September-June (peak in April-June), and insect exclusion. Defoliation significantly (P
< 0.0005) increased litterfall and turnover of nitrogen, potassium and calcium during April-June, compared to other treatments.
Data from Schowalter et al. (1991).
192
CONCLUSIONS
(Ausmus 1977, Bridges 1981, Dowding 1984, Schowalter et al.
1992). The winding galleries of xylophagous beetles and
tennites ensure rapid inoculation of microorganisms throughout
logs (Dowding 1984, Schowalter et al. 1992). Basidiomycete
fungi (including facultative or obligate pathogens) typically are
the major degraders of lignin and cellulose, but a variety of
ascomycete and deuteromycete fungi and bacteria provide
vitamins and fIxed nitrogen essential to fuel wood decay and,
in turn, further transform breakdown products of lignin and
cellulose (Blanchette and Shaw 1978).
Nitrogen fixation and nutrient accumulation in decomposing
wood create nutrient" hot spots" that facilitate germination of
some trees (Schowalter 1992). Soil under decomposing logs may
receive considerably greater nutriell1 input than does soil under
leaf litter. Accordingly, mycorrhizal fungi and tree roots infuse
decomposing logs, transporting essential nutrients to living trees.
In nitrogen-limited forests, tennite colonies in living trees might
provide nitrogen to the host trees.;
The process of ecosystem ~very from distuIbance, as
affected by insects and pathogens, also contributes to nutrient
balance in forest ecosystems. Nutrients, especially nitrogen, are
more available in canopy gaps as a result of reduced uptake and
storage in tree tissues and increased turnover and mineralization,
as above (Schowalter et al. 1992, Waring et al. 1987). Recovery
of ecosystem function within the "gap" is essential to prevent
loss of sediment and resources.
Recovery is facilitated by fast-growing early successional
species that incorporate nutrients into biomass. Nitrogen-fIXation
during this stage is particularly important to succeeding forest
stages that may largely depend on· stored nitrogen Pruning,
thinning and enhanced nutrient turnover by phytophagous
insects and pathogens may initially stimulate rapid growth by
hosts flourishing under optimal resource conditions. As these
species grow and later successional species become established,
increasing biomass leads to competitive stress, eventually
triggering insect and pathogen outbreaks. Functional equilibrium
(but not appearance) is maintained by a rapid successional
transition to more tolerant, nutrient-conserving species. This
transition is facilitated by the successive colonization of
predisposed hosts by insect and pathogen species that accelerate
host decline and replacement. Self-thinning might eventually
produce this transition but at increased risk to critical ecosystem
processes.
Unfortunately, rapidly-growing early-successional trees most
valued for commercial timber and fIber production also are most
likely to suffer from resource limitation and insect/pathogen
response. Recognizing insects and pathogens as indicators of
forest health will facilitate development of management practices
that remedy the underlying imbalances, rather than simply
treating symptoms. In forests managed for sustainable uses,
consideration of insect and pathogen roles in integrated
ecosystems is essential to balanced assessment of impacts and
protection of natural mechanisms for maintaining functional
equilibrium (health).
Forest health, defined as maintenance of functional
equilibrium, can be evaluated as the degree to which the forest
maintains balance between vegetative demand for resources and
long-term resource availability and maintains moderate internal
environmental conditions suitable for survival of critical
functional elements. Impaired health is indicated by species
decline, resource bottlenecks, and insect or pathogen responses
to host stress. This view of forest health requires greater attention
to ecosystem processes underlying forest condition
Accumulating data suggest that forest insects and pathogens
not only respond to changing host condition, but may represent
regulatory mechanisms for controlling dominance by intolerant
vegetation and alleviating bottlenecks in biogeochemical cycling
processes fundamental to forest health. These roles appear to
promote functional equilibrium and capacity to recover
functional equilibrium following distuIbances. Accordingly,
insect and pathogen effects may become more pronounced as
ecosystems respond to global change. The limited evidence for
insect and pathogen contributions to forest health should
encourage a broader experimental approach to studying and
managing these organisms. Longer-term studies of integrated
effects of insects and pathogens on ecosystem function are
necessary to quantify the importance of these roles and to
provide more balanced assessments of impacts and need for
suppression of these organisms.
ACKNOWLEDGMENT
Critical comments were provided by R.A. Haack and v.P.
Gutschick.
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