The Role of Drought in Outbreaks of Plant-Eating Insects

Author(s): William J. Mattson and Robert A. Haack

Source: BioScience, Vol. 37, No. 2 (Feb., 1987), pp. 110-118
Published by: Oxford University Press on behalf of the American Institute of Biological
Sciences
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 The Role of Drought in
Outbreaks of Plant-eating Insects
Drought's physiological effects on plants can predict its
influence on insect populations

William J. Mattson and Robert A. Haack

ubstantial evidence indicates increases to an optimum, and thereaf-

We
that drought stress promotes present here a more ter decreases. Thus, severe and pro-
outbreaks of plant-eating (phy- longed drought can become debilitat-
holistic conceptual model ing to phytophagous insects, just as it
tophagous) fungi and insects. Obser-
vations and experiments show that
to explain how drought is to plants.
colonization success and prevalence
of such fungi as root and stalk rots, may provoke Drought stress affects
stem cankers, and sometimes wilts
insect outbreaks plant traits
and foliar diseases are much higher
on water-stressed plants than on nor- I Gene expression and genomic change.
mal plants (Schoeneweiss 1986). The Drought affects virtually every plant
evidence associating insectshere anda more holistic conceptual model process; the magnitude of the effect
drought is more circumstantial, tocon-
better explain how drought may depends on the drought's severity and
sisting largely of observations provoke
that insect outbreaks. Unlike ar- duration as well as the plant's devel-
outbreaks around the world of such guments by Schoeneweiss (1986) that opmental stage (Kramer 1983).
insects as bark beetles and leaf feeders plant susceptibility and suitability Drought stress includes aspects of wa-
(see Table 1) are typically preceded byto pathogens increase continuously ter, temperature, and nutrient stress.
unusually warm, dry weather. Therewith stress, our hypotheses assume At the molecular level, drought can
is also a consistent, positive correla-that insect responses to drought ef- have a significant impact on gene
tion between insect outbreaks and fects are nonlinear; that is, the suit- expression and genomic change
dry, nutrient-poor sites (Mattson andability of conditions for insect coloni- (McClintock 1984, Walbot and Cullis
Haack 1987). zation and reproduction first 1985). For example, water stress
To explain these phenomena, the
following hypotheses have been pro-
Table 1. Selected genera of forest and range insects that historically have reached
posed both separately and in combi-outbreak proportions following drought. Source: Mattson and Haack (1987).
nation. Drought increases pathogen
and insect survival and growth Insect
through elevated plant nutrient levels,
especially nitrogen (Rhoades 1983, Order Family Genus Genera of woody hosts
White 1984); lowered plant defenses
(Rhoades 1983, 1985); and a more Coleoptera Buprestidae Agrilus Betula, Populus, Quercus
Cerambycidae Tetropium Abies
suitable physical environment (Begon Acer
Scolytidae Corthylus
1983, Rhoades 1983). We present Dendroctonus Picea, Pinus
Ips Picea, Pinus
Scolytus Abies, Carya
William J. Mattson is an insect ecologist Homoptera Aphididae Aphis Crataegus
and Robert A. Haack is a research ento- Psyllidae Cardiaspina Eucalyptus
Hymenoptera Diprionidae Neodiprion Pinus
mologist with the United States Depart-
Lepidoptera Geometridae Bupalus Pinus
ment of Agriculture, Forest Service,
located at the North Central Forest
Lambdina Abies, Picea
Selidosema Pinus
Experiment Station at the Pesticide Lymantriidae Lymantria Picea, several hardwoods
Research Center, Department of Ento- Tortricidae Choristoneura Abies, Picea, Pinus
mology, Michigan State University, East
Orthoptera Acrididae Several genera Many grasses and range plants
Lansing, MI 48824.

110 BioScience Vol. 37 No. 2

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 ?e w -- lr ..... i i ! .j

The pine sawfly, Diprion similis (above), introd

eastern North America. Young larvae feed greg
white pine but also jack, Scotch, and red pines.
result in tree death. The forest tent caterpillar (r
most of the US and Canada. Larvae often feed
quaking aspen, oaks, and water tupelo. Outbreak
areas, causing reduced growth and some tree mo
preceded by consecutive years of unusually cold

alone has been found

chemical toin induce
changes that occur matur- quan-
titative ing cells
changes in and patterns
the ensuing morphologi-
of protein
synthesis in cal changes) is not
barley as sensitive lowing
(Jacobsen to (Kramer
et1983).al.
1986) both and
drought as arequantitative
the growth processes.Even more importantly,anddrought-
Differentiation may
qualitative changes inactually
maize be en- seedlings
stressed plants are consistently warm-
(Heikkila et al.
hanced1984).
during moderate High tempera-
er than
stress, be- well-watered plants. This ef-
ture or heat cause
shock is inknown
with the decline growth therefect is to
due to upset
stomatal closure
are abundant
normal patterns of photosynthates
protein to fuel
reducing
synthesisthe transpirational cooling.
the maturation
in favor of novel heat processes (LorioAlthough
shock proteins
temperature differences are
(Walbot and1986).Cullis
The net result1985).
is thicker cell The
usually 2?-4? C, full
differences as great
walls, more
impact of these abundant fiber and
changes on as 15?
con- a C have been is
plant recorded (Matt-
largely unknown. Nevertheless,
ducting elements, and higher concen- son and Haackthe 1987). In fact, the
wide distribution of
trations of such these
secondary measurement
products responses of plant temperature
in prokaryoticas terpenes,
and alkaloids, and waxes
eukaryotic has become orga- an important and simple
nisms (Lorio
suggests 1986, Sharpe
that they et al. 1985).
are index
an of the degree of stress a plant is
impor-
tant and ancient developmental
However, severe stress eventually cur- experiencing (Reicosky et al. 1985).
mechanism (Kurtz et process
tails the differentiation al.when
1986).
During the gradual dehydration of
levels of photosynthates and other plants caused by prolonged water
Plant growth raw
and materials become limiting
differentiation. stress, there is
Onea breaking, or cavita-
of the most sensitive and immediate (Sharpe et al. 1985). Temperature tion, of the water columns in the
plant responses to water stress at thestress can inhibit both plant growth conducting xylem tissue of leaves and
cellular level is a reduction in the and differentiation. stems (Pena and Grace 1986). The
growth processes-cell division and cavitations cause acoustic emissions
enlargement (Kramer 1983). The net Spectral qualities, temperature, and that are believed to be vibrations
acoustic emissions. The spectral and coming from single cells. The fre-
result is smaller plants and plant parts
(e.g., leaves, buds, reproductive or- thermal qualities of plants change sig- quencies of such vibrations may be in
gans, and xylem growth rings). Pho- nificantly with increasing drought the audible range for large water-
stress. Leaf reflectance increases in
tosynthesis itself is not as sensitive, conducting cells (vessels) but are pri-
declining only slowly until water both visible and infrared wavelengths marily ultrasonic (80-2000 kHz) for
stress becomes moderate to severe smaller cells such as fibers and tra-
(Drake 1976). For example, severe
(Kramer 1983, Sharpe et al. 1985).drought stress inhibits chlorophyllcheids (Sandford and Grace 1985).
Cavitation apparently occurs first in
production and thus induces leaf yel-
The process of differentiation (the

February 1987 111

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the largest conducting cells and then stress metabolites. Tissue concentra- Drought provides a more favorable
in smaller and smaller ones as stress tions of several classes of allelochemi-
thermal environment for growth of
intensifies (Tyree et al. 1984). cals (secondary compounds that stim- phytophagous insects. Because insects
ulate or inhibit other organisms) tendhave limited thermoregulatory capac-
Plant osmolytes, minerals, nitrogen, to increase during drought, including ity, the higher air and host plant
and carbohydrates. Most plants low- cyanogenic glycosides, glucosinolatestemperatures associated with drought
er their osmotic potential during and other sulfur compounds, terpen- may enable them to grow and repro-
drought by accumulating such com- oids, and alkaloids (Gershenzon duce in a more nearly optimal tem-
pounds (osmolytes) as inorganic ions, 1984, Mattson and Haack 1987). perature regime. Mattson and Scriber
amino acids, sugars, sugar alcohols, However, the relationship between (1987) proposed that insects that feed
and organic acids (Kramer 1983, drought stress and foliar phenolic lev- on grasses and leaves of woody plants
Mattson and Haack 1987). Mineral els has not been clearly demonstrated may have unusual enzyme and mem-
nutrient uptake from soil is altered (Gershenzon 1984). Secondary brane systems with relatively high
during drought because soil tempera- metabolites may accumulate during thermal optima. Small changes in
tures increase, soil water decreases, mild to moderate drought because temperature may evoke large respons-
ion movement and root growth are their synthesis is enhanced by the es by the insect (Begon 1983, Wagner
reduced, and roots become more su- increased levels of available carbon et al. 1984). For example, Martin et
berized, or corky (Kramer 1983). Sev- and nitrogen (Lorio 1986, Sharpe al. et (1980) reported that activity of the
eral minerals (calcium, chlorine, po- al. 1985). In stressed mint (Mentha) midgut proteases of Tipula abdomin-
tassium, magnesium, nitrogen, plants, for example, foliar terpenoid alis increased seven- to tenfold for
sodium) can accumulate to higher levels increase because the terpenoid- each 10? C increment over the range
than normal levels in the above- containing trichomes are more dense- of 4?-37? C. Growth rates of the
ly packed on smaller than normal
ground tissues of drought-stressed whole insect typically increase in a
leaves (Gershenzon 1984). Likewise,
plants (Mattson and Haack 1987). sigmoidal fashion in relation to tem-
Viets (1972) reported that a plant's perature (Wagner et al. 1984). Surviv-
in moderately stressed conifers, levels
of low molecular weight terpenoids
depth of rooting influences its mineral al and fecundity usually exhibit an S-
increase (Sharpe et al. 1985). Xero-
content. During drought, for exam- or a dome-shaped relation to tem-
phytes allocate extremely largeperature (Morris and Fulton 1970).
ple, deep-rooted plants draw water
amounts of energy and carbonMany
mainly from deep soil where nutrients to studies have shown that merely
are scarce. As a result, the diluted
allelochemical production (Hoffmann
providing insects with optimal tem-
et al. 1984).
tissue nutrients limit plant function perature regimes, without changes in
Plant allelochemical concentrations
before water does. On the other hand, food quality, will permit them to
in shallow-rooted plants, nutrients
appear to exhibit a dome-shaped rela-grow faster and larger, suffer less
may become concentrated in plant tionship to drought stress. Severemortality, and lay more eggs per unit
tissue, and water becomes limitingdrought stress in conifers, for exam-of ingested food (Mattson and Haack
long before nutrients do. ple, lowers oleoresin production (and 1987).
During drought, concentrations also
ofexudation pressure, flow rate,
such nitrogenous compounds asviscosity,
ami- and rate of crystallization)Drought-stressed plants are behavior-
no acids (especially proline), nitrate,
and induces compositional changes inally more attractive or acceptable for
and betaine often increase in plant
the resin acid and monoterpene frac-insects. The leaf yellowing, higher
tissues (Kramer 1983, Mattsontions and(Hodges and Lorio 1975, Matt- temperatures, and greater infrared re-
son et al. 1987). Similarly, severe flectance of drought-stressed plants
Haack 1987). Although soluble nitro-
gen generally increases during drought in rubber (Hevea) trees re- may make them more attractive or
duces the production and flow rate ofacceptable to insects. The insects may
drought, the effects on total nitrogen
are tissue and stress dependent. latex
Dur-(Buttery and Boatman 1976). detect thermal, acoustic, biochemical,
Many environmental stresses com-and electromagnetic properties. Elec-
ing mild to moderate water stress, for
example, total nitrogen concentra- monly induce production of several tromagnetic cues include those per-
tions decline in roots and older volatile compounds (e.g., ethylene,ceived with normal vision and with
above-ground tissues, but increase ethanol,
in ethane, acetaldehyde) (Kim-infrared receptors (Evans and Kuster
younger above-ground tissues (Matt-merer and Kozlowski 1982). These 1980). Many insects are attracted to
son and Haack 1987). compounds, along with abscisic acid,yellow hues (Prokopy and Owens
Likewise, as stress intensifies, are often considered to be stress
con- 1983), and several others have heat
centrations of sugars and sugar metabolites,
alco- but their effects atand theinfrared receptors (Altner and
level of the whole plant are poorly
hols (e.g., inositol) typically increase, Loftus 1985). For example, the bu-
while complex carbohydrates understood
(e.g., (Ayers 1984). prestid beetle Melanophila acuminata
starch) decrease (Kramer 1983). Total has infrared receptors that apparently
carbohydrate concentrations are of- assist it in finding fire-scorched coni-
ten high in foliage of drought-stressed
Implications for insects fers, in which it oviposits (Evans and
plants (Kramer 1983, MattsonWe
andwill consider six major mecha-
Kuster 1980). Although evidence ex-
Haack 1987). nisms by which drought may affectists that some insects use color and
infrared perception in host finding,
aspects of insect behavior and physi-
Plant allelochemicals and volatile ology (Figure 1). much research is still needed.

112 BioScience Vol. 37 No. 2

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 Acoustical cues may serve as short-
range attractants or arrestants for DROUGHT
some phytophagous insects. As plants
dehydrate, cavitations of the water Increased: Air temperature
columns in xylem tissue produce Insolation
acoustical, usually ultrasonic, emis- Soil temperature
sions. Many branch- and trunk-in-
festing bark beetles and buprestids Decreased: Rainfall
have well-developed acoustical senses
Humidity
(Barr 1969, Carlson and Knight
1969). Several insect species are capa- . ,

ble of detecting ultrasonic sound, at

least up to 100 kHz (Prosser 1973).
Therefore, we can speculate that HOST PLANT
NATURAL
acoustical emissions influence the be- ENEMIES
havior of such insects as wood borers. Increased:
(including
As they find and accept host plants, Temperature
most insects appear to respond to pathogens)
Acoustic emissions
blends of plant compounds (Miller Stress metabolites
and Strickler 1984). Because drought Decreased:
Osmolytes Numbers
stress alters the biochemical composi-
Soluble N Virulence
tion of plants, qualitative and quanti-
tative changes in these chemical Soluble sugars
blends could make stressed plants Secondary compounds
more attractive and acceptable to
phytophages. In fact, the insect's che- Decreased:
moreceptors appear to be especially Growth
sensitive to such changes. Resistance mechanisms
Phytophagous insects, for example, Water content
commonly have contact chemorecep-
tors that are sensitive to plant water, Altered:
amino acids, sugars, salts, and allelo-
Genomic expression
chemicals (Stadler 1984, Visser
Electromagnetic spectra
1986). The amino acid and salt recep-
tors are necessary to phytophages be- Plant morphology
cause their foods often contain only
small amounts of these nutrients
\
(Haack and Slansky 1987, Mattson
-

and Scriber 1987). However, it is not PHYTOPHAGOUS INSECT

clear why proline and inositol, which
are not essential nutrients for insects, Improved:
are feeding stimulants for so many Nutrition
species (Mattson and Haack 1987, Thermal environment
Stadler 1984). We hypothesize that
Immunocompetence
because proline and inositol are com-
Detoxication
mon plant osmolytes that accumulate
Developmental rates
during drought, they may aid insects
in detecting stressed plants. Host finding
Phytophagous insects appear to Host accepting
have the necessary sensory apparatus- Host utilization
es to detect common plant osmolytes Escape from natural enemies
and moreover they exhibit positive Growth of symbionts
feeding responses to most of these
compounds (Mattson and Haack Altered:
1987, Stadler 1984). As osmolytes Genomic expression
increase during drought, they may Natural selection

Figure 1. Hypothetical representation of

how drought influences host plants, phy-
INSECT OUTBR
tophagous insects, and their natural ene-
mies to provoke insect outbreaks.

February 1987 13

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simultaneously stimulate greater host explain in part why alpha-pinene is (Mattson and Haack 1987). Drought
acceptance and feeding by insects. such a common attractant and arres- may lower the inducible defense sys-
This hypothesis assumes that levels of tant for bark beetles that attack livingtems that some plants possess. For
these stimulatory compounds in un- but stressed conifers. example, expression of the genes con-
stressed plants are below the insect's Chararas (1979) suggested thatferring resistance of wheat to stem
optimal response level. drought stress lowers the relative con-and leaf rusts and to the Hessian fly
In the spruce budworm Choristo- centrations of most terpenes from aMayetiola destructor appear to be
neura fumiferana, for example, the repellent to an attractant level for
very temperature sensitive; resistance
many bark beetles. Such trees may
larva's peak feeding response occurs usually declines with increases in tem-
between 0.01 and 0.05 M sucrose not only be more attractive to barkperature, but for some traits the op-
beetles, but they may be less toxic asposite may occur (Gousseau et al.
(Albert et al. 1982), whereas sucrose
0.011For example, alpha-pinene, 1985, Sosa 1979). Likewise, the rate
levels range between 0.004 and well.
M in unstressed balsam fir (Abies
which increases in concentration with of generalized wound healing in
balsamea) foliage (Mattson and
stress, is one of the least toxic mono-
grand fir Abies grandis declines dur-
Haack 1987). Hence, drought stress
terpenes, whereas myrcene and limo-ing drought (Puritch and Mullick 1975).
nene,
would likely increase the level of thiswhich decrease in amount, are
among the most toxic monoterpenesDrought enhances insect detoxication
stimulant and thus promote greater
to bark beetles (Cates and Alexandersystems and immunocompetence. Be-
feeding. The same is true for some
1982, Mattson and Haack 1987). cause levels of many insect-resistance
other insects, such as the grasshopper
Locusta migratoria and several lepi- allelochemicals increase during
Drought-stressed plants are physio-drought, it would seem that stress
dopterans, that have peak responses
logically more suitable for insects.may actually fortify rather than
to relatively high sucrose levels (Matt-
son and Haack 1987). In addition,
Drought-stressed plants may be moreweaken plant defenses against some
suitable for insect growth, survival,classes of consuming insects. How
the varying levels of osmolytes proba-
and reproduction because plant nutri-then can outbreaks of these consum-
bly interact synergistically to further
promote host acceptance and feedingents are either more concentrated or ers be explained? It may be that
(Visser 1986). better balanced. This may be of par- drought somehow enhances the her-
The increased levels of foliar allelo- bivore's detoxication systems more
ticular importance to insects that feed
chemicals in moderately stressed
on woody plants because amounts of than the plant's defenses. One possi-
nitrogen, sugar, and minerals are of- bility is that the increased tempera-
plants would seemingly be detrimen-
tal to insects. However, these tenin- less than optimal (Haack and tures associated with drought in-
creases may not be substantial Slansky 1987, Mattson and Scriber crease the insect's ability to
enough to exceed the tolerance or White 1984). Logically, in- detoxicate some plant allelochemi-
1987,
creasing and/or improving the bal- cals. For example, Hinks (1985) re-
detoxication capacities of specialized
insects. Moreover, such increasesance
mayof these nutrients should favor ported that increasing temperatures
insect performance (Haack and reduce susceptibility of the grasshop-
actually benefit the specialists that
Slansky 1987, House 1974).
utilize allelochemicals as host finding per Melanoplus sanquinipes to pyre-
Several investigators have shown throid insecticides. Similar relation-
and accepting cues (Mattson and
Haack 1987, Visser 1986). that feeding on drought-stressed ships have been reported for other
Increased production of ethylene, plants led to improved growth, sur- insects exposed to pyrethroids, DDT,
ethane, acetaldehyde, and ethanol fol-or reproduction of various Ho- and some carbamates (Hinks 1985,
vival,
lowing stress (Kimmerer and moptera, Koz- Lepidoptera, Orthoptera, Mattson and Haack 1987).
lowski 1982) may likewise stimulate and mites (Mattson and Haack The altered chemical composition
greater host finding and accepting. 1987). In some cases, however, of drought-stressed plants could also
Ethanol serves as an attractant for growth and survival of aphids andenhance an insect's ability to detoxi-
many bark- and wood-inhabiting sco- mites declined on severely stressed cate compounds. Many studies indi-
plants, probably reflecting supraopti-cate that pesticide efficacy varies with
lytid and cerambycid beetles (Dunn et
mal temperatures, lowered turgorthe plant cultivar or species consumed
al. 1986, Haack and Slansky 1987),
but little information is available on pressure, or increased cell-sap viscosi-by insects prior to pesticide exposure
the attraction of the other three ty (Mattson and Haack 1987). The (Mattson and Haack 1987). De-
compounds. latter two factors are known to limit creased pesticide sensitivity as a result
On the other hand, severe drought feeding by sap-sucking arthropodsof dietary experience has been ex-
stress can reduce terpene emissions (Auclair 1963). plained in two ways. First, the insect's
from conifer needles due to stomatal Some plants clearly become more diet may contain inducers, such as
closure (Cates and Alexander 1982, susceptible to certain insects duringsome nontoxic allelochemicals, that
Chararas 1979). Not all terpenes are severe drought owing strictly to astimulate production of the insect's
equally reduced, and the concentra- decline in ongoing defenses. For ex- detoxicating enzymes (Terriere 1984);
tions of some, such as alpha-pinene, ample, drought-induced reduction in for example, the southern armyworm
may increase (Cates and Alexander oleoresin exudation pressure in coni- Spodoptera eridania was twice as tol-
1982), resulting in their increased fers is closely linked to the coloniza-erant to nicotine when its diet con-
dominance in the stressed plant's gas- tion success of bark beetles and larvae tained the inducer alpha-pinene
eous atmosphere. This increase may of some needle-feeding Lepidoptera (Brattsten 1979). Second, nutrient

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concentrations may be more nearly to insecticides. Hence, a stronger im-hood of resin exudation by conifer
optimal in those plants where insects mune system might indirectly allow hosts and thus favor colonization by
show reduced pesticide sensitivity. more potent detoxication or vice bark beetles. Future research must
Nutrient imbalances can lower the versa. address the influence of changing en-
production and sensitivity of detoxi- The immune system of vironments
insects ison insect-symbiont
cation mechanisms, such as the less complex than that of interactions.
vertebrates
mixed-function oxidase system (Dunn 1986, Gotz and Bowman During drought, high temperatures
(Campbell and Hayes 1974, Nutri- 1985). However, most research on
may allow phytophagous insects to
tion Reviews 1985). Wahl and Ulm the effects of nutrition and stress
escape the on
control of their natural
(1983) reported that honeybees were immunocompetence hasenemies.
been For
doneexample, Wilson (1974)
more sensitive to various pesticides with vertebrates. The vertebrate reportedstud-
that optimal temperatures
when their diet contained pollen that ies indicate that nutrient for deficiencies
the microsporidian parasite No-
was unusually low in protein and and imbalances can reduce sema general
fumiferanae of the spruce bud-
vitamins. Although poorly under- immunocompetence. For worm were below 23? C, but optimal
example,
stood, nutrition may also influence Porter et al. (1984) temperatures
demonstrated thatfor the budworm are
pesticide penetration and target site undernourished mice were more sen- near 27? C (Haack et al. unpublished
sensitivity (Campbell and Hayes sitive to virus; this is also generally data, Regniere 1982). A similar diver-
1974). true for insects (Biever and Wilkinson gence in optimal temperatures exists
We hypothesize that both elevated 1978, Mattson and Haack 1987). between the Banks grass mite Oligon-
temperatures and improved nutrition- Chandra (1985) reported that protein ychus pratensis and its predators
al properties of drought-stressed and energy malnutrition and vitamin (Toole et al. 1984). Glare et al. (1986)
plants can enhance the insect's de- and mineral deficiencies can affect and Strong et al. (1984) give more
toxication system, at least with re- many components of the immune sys- examples.
spect to some toxicants. The nutri- tem. Furthermore, because compe- In addition, the low humidity and
tional aspect of this scenario may be tence of the vertebrate immune sys- high sunlight levels associated with
similar to the mechanism that permits tem depends on its anatomical and drought may lower amounts and vir-
the fungus Armillaria mellea to colo- biochemical links to the nervous sys- ulence of pathogens. For example,
nize roots of stressed trees. According tem (Garfield 1986, Mattson and drought may restrict fungal diseases
to Wargo (1981), A. mellea succeeds Haack 1987), it is possible that cer- because spores require high humidity
in stressed trees because the increased tain plant traits may favor or disfavor for germination and penetration of
concentrations of sugars and amino insect immunocompetence via the the insect's integument (Ferron
acids increase its ability to oxidize the central nervous system. 1985). Similarly, bacterial and viral
normally inhibitory phenols and even diseases may be reduced during
Drought favors mutualistic microor-
to utilize the phenolics as a carbon drought because many are inactivated
source. ganisms but not natural enemies of by the higher ultraviolet radiation lev-
phytophagous
The chemical changes induced ininsects. Drought may els (Ali and Sikorowski 1986, Brock
influence
drought-stressed plants may phytophagous insects indi-
influence et al. 1984, Mattson and Haack
rectly by optimizing conditions for
interactions between phytophages 1987). Hence, the normal guild of
and organisms pathogenictheir exo- and endo-symbionts. Be-
to them. natural enemies could be rendered
cause many
The changes may either directly microbes have thermal less effective during drought, and
affect
the pathogens or may enhance 25?-30? C (Brock et al. thereby fail to regulate an incipient
optima of the
insect's immune system. High1984),
gut high temperatures associ- outbreak.
thelev-
ated with drought could stimulate
els of allelochemicals that accumulate
microbial
in stressed plants can inhibit growth. Likewise, some of Drought may induce genetic changes
growth
the chemical
of ingested pathogens (Barbosa andchanges in drought- in insects. The elevated temperatures
Saunders 1985, Mattson stressed plants could enhance micro- and solar radiation associated with
and Haack
1987). In addition, improvedbial growth;
nutri-for example, levels of drought may not only affect the rate
and fructose often increase in and efficiency of enzymatic reactions
glucose capaci-
tion could increase the insect's
ty to suppress pathogenic the inner bark and sapwood of within an insect, but they along with
microorga-
nisms (e.g., protozoans, fungi,
drought-stressed trees (Hodges and various plant biochemical changes
Lorio 1969, Mattson and Haack may induce random as well as pro-
bacteria, and viruses), nematodes,
and parasitoids. Moreover,1987).
there maythese sugars are the grammed genetic changes in insect
Because
most readily used sources of carbon populations. For example, at the pop-
be significant synergistic interactions
between the insect's immune and de- by the blue stain fungus Ceratocystis ulation level, these environmental
toxication systems. For example, minor (Barras and Hodges 1969), an changes may suddenly favor some
Wahl and Ulm (1983) reported that external symbiont of the bark beetle uncommon allozyme variants and
honeybees infected with Nosema Dendroctonus frontalis, fungal through classical natural selection
were more sensitive to pesticides. growth is likely to be accelerated cause them to rapidly increase in
Similarly, Brattsten (1987) demon- when introduced by the beetle into abundance (Haukioja and Hakala
strated that sublethal virus infections drought-stressed pines (Pinus). Rapid 1975). At the individual level, the
markedly increased sensitivity of to- growth and tissue penetration by blue markedly different physical and/or
bacco budworm Heliothis virescens stain fungi would decrease the likeli- metabolic conditions of drought

115
February 1987

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stress may change gene expression to(Mattson et al. 1987). Drought pro-of insects whose populations were
induce alternate isozymes (Ho- vokes outbreaks of leaf feeders bygreatly enlarged during the stress pe-
chachka and Somero 1984, Schott providing thermal and nutritional riod (Mulock and Christiansen
and Brusven 1980). conditions that favor their growth,1986).
Moreover, the thermal and dietary detoxication, and immunocompe-
(biochemical) effects of drought cantence. Moreover, these changes also
trigger genomic modifications, suchfavor the insects' escape from regula-
Drought and other stresses
as induction of heat-shock genes (Pe- tion by their natural enemies. A plant's repetoire of stress responses
tersen and Mitchell 1985, Van der Drought-induced genetic changes inis rather limited. Therefore, we hy-
Ploeg et al. 1985), amplification ofthe insects may also be involved in pothesize that plant reactions to other
genes (Mouches et al. 1986, Rucker outbreak development. kinds of stress are very similar to their
and Tinker 1986, Walbot and Cullis Outbreaks of leaf feeders often last reactions to drought; one should be
1985), transposition of movable ele- for several years and then rapidly able to detect similar reactions to a
ments (McClintock 1984, Walbot anddecline. Intense, long-term defoliation diverse array of perturbations. For
Cullis 1985), and other rearrange- can lead to severe reductions in quali-example, just as drought stress in-
ments such as polyploidy. (Bidwell et ty and quantity of foliage (Baltens-creases levels of soluble sugars and
al. 1985). While the effects of extreme weiler 1984, Rhoades 1985, Tuomi etnitrogen in plant foliage, inner bark,
temperatures and toxins are generallyal. 1984). Such reductions, coupledand sapwood (Mattson and Haack
well appreciated, the effects of nutri- with decreased phytophage "viru-1987), so do air pollutants such as
ents per se can also significantly affect lence" and the growing numbers ofsulfur dioxide (Kozlowski and Con-
gene expression (Rucker and Tinker the insects' natural enemies, reduce stantinidou 1986), salts (Braun and
1986). The issue of rapid genomic populations of defoliating insects toFliickiger 1984), nutrient deficiencies
response to stress deserves attention, more innocuous levels (Mattson and (Goring and Thien 1979, Huber
especially considering that certainHaack 1987). 1984), and flooding (Kozlowski
grasshoppers and Lepidoptera are In contrast, inner-bark boring in-1984). If plants have more or less
found in different forms (morphs) sects, such as bark beetles, appear touniversal responses to stress, then
during outbreaks and latent phases ofbe primarily regulated by powerfulmany phytophagous insects appear to
their population gradients (Baltens- host defenses, such as preformedbe adapted to detecting and capitaliz-
weiler 1984, Rhoades 1985). We pro- oleoresin or latex systems and imme-ing on these situations. In support of
pose that there could be high-tem- diate inducible defenses (Mattson etthis contention are reports of insect
perature forms of insects that possess al. 1987). Unlike the leaf feeders, in-outbreaks on trees stressed by air
enzymes in higher concentrations ner-bark borers usually encounter nu- pollutants (Baltensweiler 1985, Koz-
and/or with higher catalytic efficien- trient-rich food and receive substan- lowski and Constantinidou 1986),
cies, allowing more efficient detoxica- tial protection from many natural salt (Braun and Fliickiger 1984), and
tion and nutrient utilization. enemies (Haack and Slansky 1987). nutrient deficiencies (Mattson and
The gregarious behavior of many of Haack 1987).
Variation among insect these insects makes them especially
dangerous. If one insect becomes es-
feeding guilds Acknowledgments
tablished, it rapidly attracts others
The importance of the mechanisms by through pheromonal communication. We thank I. Havukkala and J. R.
which drought may promote insect Plants require an iron-clad defenseMiller for their comments on an earli-
outbreaks is likely to vary among against such insects because their er draft of this paper.
insects of different feeding guilds, damage, the girdling of the conduct-
such as external leaf feeders and in- ing phloem and xylem, is devastating. References cited
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