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Quinney Natural Resources Research Library, The Bark Beetles, Fuels, and Fire Bibliography S.J. and Jessie E.

1987

Role of Drought in Outbreaks of Plant-Eating Insects

William J. Mattson

Robert A. Haack

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Recommended Citation Mattson, W. and Haack, R. (1987). Role of drought in outbreaks of plant-eating insects. Bioscience, 37(2): 110-118.

This Article is brought to you for free and open access by the Quinney Natural Resources Research Library, S.J. and Jessie E. at DigitalCommons@USU. It has been accepted for inclusion in The Bark Beetles, Fuels, and Fire Bibliography by an authorized administrator of DigitalCommons@USU. For more information, please contact [email protected]. The Role of Drought in Outbreaksof Plant-eatingInsects Drought'sphysiological effects on plants can predict its influenceon insect populations

WilliamJ. Mattsonand RobertA. Haack

r ubstantial evidence indicates increasesto an optimum,and thereaf- that drought stress promotes We present here a more ter decreases.Thus, severe and pro- outbreaks of plant-eating (phy- longed droughtcan become debilitat- tophagous) fungi and insects. Obser- holistic conceptual model ing to phytophagousinsects, just as it 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 Droughtstress affects stem cankers, and sometimes wilts traits and foliar diseases are much higher insect outbreaks plant on water-stressed plants than on nor- I Gene expressionand genomicchange. mal plants (Schoeneweiss 1986). The Drought affects virtually every plant evidence associating insects and here a more holisticconceptual model process; the magnitude of the effect drought is more circumstantial, con- to better explain how drought may dependson the drought'sseverity and sisting largely of observations that provoke insect outbreaks.Unlike ar- durationas well as the plant's devel- outbreaks around the world of such gumentsby Schoeneweiss(1986) that opmental stage (Kramer 1983). insects as bark beetles and leaf feeders plant susceptibility and suitability Droughtstress includes aspects of wa- (see Table 1) are typically preceded by to pathogens increase continuously ter, temperature, and nutrient stress. unusually warm, dry weather. There with 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 and abilityof conditionsfor insect coloni- (McClintock 1984, Walbot and Cullis Haack 1987). zation and reproduction first 1985). For example, water stress To explain these phenomena, the have been following hypotheses pro- Table 1. Selected of forest and insects that have reached both and in combi- genera range historically posed separately outbreakproportions 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 Generaof woody hosts White 1984); lowered plant defenses (Rhoades 1983, 1985); and a more Coleoptera Buprestidae Agrilus Betula, Populus, Quercus Abies suitable physical environment (Begon Cerambycidae Tetropium Scolytidae Corthylus Acer 1983, Rhoades 1983). We present Dendroctonus Picea, Pinus Ips Picea, Pinus Scolytus Abies, Carya WilliamJ. Mattson is an insect ecologist Homoptera Aphididae Aphis Crataegus and Robert A. Haack is a researchento- Psyllidae Cardiaspina Eucalyptus mologist with the United States Depart- Hymenoptera Diprionidae Neodiprion Pinus ment of Agriculture, Forest Service, Lepidoptera Geometridae Bupalus Pinus located at the North Central Forest Lambdina Abies, Picea Station at the Pesticide Selidosema Pinus Experiment Lymantriidae Lymantria Picea,several hardwoods Research Center, Department of Ento- Tortricidae Choristoneura Abies, Picea, Pinus mology, Michigan State University,East Orthoptera Acrididae Severalgenera Many grassesand rangeplants Lansing, MI 48824.

110 BioScience Vol. 37 No. 2 ?e w --i ! .....lr .j i

The pine sawfly, Diprion similis (above), introducedfrom Europe,occurs throughout eastern North America. Young larvae feed gregariously,attacking primarily eastern white pine but also jack, Scotch, and red pines. Severeand repeateddefoliations can resultin tree death. The forest tent caterpillar(right), Malacosoma disstria, is found in most of the US and Canada. Larvaeoften feed gregariouslyon hardwoods such as quakingaspen, oaks, and watertupelo. Outbreaksoccur sporadically over vast forested areas,causing reduced growth and some tree mortality.Outbreaks in Canadaare often precededby consecutiveyears of unusuallycold winters and warm springs. alone has been found to induce quan- chemical changes that occur in matur- titative changes in patterns of protein ing cells and the ensuing morphologi- synthesis in barley (Jacobsen et al. cal changes) is not as sensitive to lowing (Kramer 1983). 1986) and both quantitative and drought as are the growth processes. Even more importantly, drought- qualitative changes in maize seedlings Differentiation may actually be en- stressed plants are consistently warm- (Heikkila et al. 1984). High tempera- hanced during moderate stress, be- er than well-watered plants. This ef- ture or heat shock is known to upset cause with the decline in growth there fect is due to stomatal closure normal patterns of protein synthesis are abundant photosynthates to fuel reducing the transpirational cooling. in favor of novel heat shock proteins the maturation processes (Lorio Although temperature differences are (Walbot and Cullis 1985). The full 1986). The net result is thicker cell usually 2?-4? C, differences as great impact of these changes on a plant is walls, more abundant fiber and con- as 15? C have been recorded (Matt- largely unknown. Nevertheless, the ducting elements, and higher concen- son and Haack 1987). In fact, the wide distribution of these responses trations of such secondary products measurement of plant temperature in prokaryotic and eukaryotic orga- as terpenes, alkaloids, and waxes has become an important and simple nisms suggests that they are an impor- (Lorio 1986, Sharpe et al. 1985). index of the degree of stress a plant is tant and ancient developmental However, severe stress eventually cur- experiencing (Reicosky et al. 1985). mechanism (Kurtz et al. 1986). tails the differentiation process when During the gradual dehydration of levels of photosynthates and other plants caused by prolonged water Plant growth and differentiation. One raw materials become limiting stress, there is a 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 the stress 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 result is smaller plants and plant parts acoustic emissions. The spectral and coming from single cells. The fre- (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- tosynthesis itself is not as sensitive, stress. Leaf reflectance increases in 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 (Drake 1976). For example, severe smaller cells such as fibers and tra- (Kramer 1983, Sharpe et al. 1985). drought stress inhibits chlorophyll cheids (Sandford and Grace 1985). The process of differentiation (the production and thus induces leaf yel- Cavitation apparently occurs first in

February 1987 111 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) tend have 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, glucosinolates temperatures 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 et al. (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 ground tissues of drought-stressed ly packed on smaller than normal whole insect typically increase in a plants (Mattson and Haack 1987). leaves (Gershenzon 1984). Likewise, sigmoidal fashion in relation to tem- Viets (1972) reported that a plant's in moderately stressed conifers, levels perature (Wagner et al. 1984). Surviv- depth of rooting influences its mineral of low molecular weight terpenoids al and fecundity usually exhibit an S- content. During drought, for exam- increase (Sharpe et al. 1985). Xero- or a dome-shaped relation to tem- ple, deep-rooted plants draw water phytes allocate extremely large perature (Morris and Fulton 1970). mainly from deep soil where nutrients amounts of energy and carbon to Many studies have shown that merely are scarce. As a result, the diluted allelochemical production (Hoffmann providing insects with optimal tem- tissue nutrients limit plant function et al. 1984). perature regimes, without changes in before water does. On the other hand, Plant allelochemical concentrations 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. Severe mortality, and lay more eggs per unit tissue, and water becomes limiting drought stress in conifers, for exam- of ingested food (Mattson and Haack long before nutrients do. ple, lowers oleoresin production (and 1987). During drought, concentrations of also exudation pressure, flow rate, such nitrogenous compounds as ami- viscosity, and rate of crystallization) Drought-stressed plants are behavior- no acids (especially proline), nitrate, and induces compositional changes in ally 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, Mattson and tions (Hodges and Lorio 1975, Matt- temperatures, and greater infrared re- Haack 1987). Although soluble nitro- son et al. 1987). Similarly, severe flectance of drought-stressed plants gen generally increases during drought in rubber (Hevea) trees re- may make them more attractive or drought, the effects on total nitrogen duces the production and flow rate of acceptable to insects. The insects may are tissue and stress dependent. Dur- latex (Buttery and Boatman 1976). detect thermal, acoustic, biochemical, ing mild to moderate water stress, for Many environmental stresses com- and electromagnetic properties. Elec- 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 in ethanol, 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, con- are often considered to be stress 1983), and several others have heat centrations of sugars and sugar alco- metabolites, but their effects at the and infrared receptors (Altner and hols (e.g., inositol) typically increase, level of the whole plant are poorly Loftus 1985). For example, the bu- while complex carbohydrates (e.g., understood (Ayers 1984). prestid beetle Melanophila acuminata starch) decrease (Kramer 1983). Total has infrared receptors that apparently carbohydrate concentrations are of- for insects assist it in finding fire-scorched coni- ten high in foliage of drought-stressed Implications fers, in which it oviposits (Evans and plants (Kramer 1983, Mattson and We will consider six major mecha- Kuster 1980). Although evidence ex- Haack 1987). nisms by which drought may affect ists that some insects use color and aspects of insect behavior and physi- infrared perception in host finding, Plant allelochemicals and volatile ology (Figure 1). much research is still needed.

112 BioScience Vol. 37 No. 2 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, emis- usually ultrasonic, Soil temperature sions. Many branch- and trunk-in- bark beetles and festing buprestids Decreased: Rainfall have well-developed acoustical senses (Barr 1969, Carlson and Knight Humidity 1969). Several insect species are capa- . , ble of detecting ultrasonic sound, at least up to 100 kHz (Prosser 1973). Therefore, we can speculate that HOSTPLANT 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 to to pathogens) appear respond Acoustic emissions blends of plant compounds (Miller Stress metabolites and Strickler 1984). Because Decreased: drought Osmolytes stress alters the biochemical composi- Numbers Soluble N tion of plants, qualitative and quanti- Virulence 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 spectra 1986). The amino acid and salt recep- Electromagnetic Plant tors are necessary to phytophages be- morphology cause their foods often contain only small amounts of these nutrients \ (Haack and Slansky 1987, Mattson - and Scriber 1987). However, it is not PHYTOPHAGOUSINSECT clear why proline and inositol, which are not essential nutrients for insects, Improved: are feeding stimulants for so many Nutrition and Haack species (Mattson 1987, Thermal environment Stadler 1984). We hypothesize that Immunocompetence because proline and inositol are com- Detoxication mon plant osmolytes that accumulate rates during drought, they may aid insects Developmental in detecting stressed plants. Host finding Phytophagous insects appear to Host accepting have the necessary sensory apparatus- Hostutilization es to detect common plant osmolytes Escapefrom natural enemies and moreover they exhibit positive Growthof symbionts feeding responses to most of these compounds (Mattson and Haack Altered: Stadler As 1987, 1984). osmolytes Genomic expression increase during drought, they may Natural selection

Figure 1. Hypothetical representation of how drought influences host plants, phy- tophagous insects, and their natural ene- INSECTOUTBREAK mies to provoke insect outbreaks.

February 1987 113 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 living tems 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 that ferring 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 a Mayetiola destructor appear to be neura fumiferana, for example, the repellent to an attractant level for very temperature sensitive; resistance larva's peak feeding response occurs many bark beetles. Such trees may usually declines with increases in tem- between 0.01 and 0.05 M sucrose not only be more attractive to bark perature, but for some traits the op- (Albert et al. 1982), whereas sucrose beetles, but they may be less toxic as posite may occur (Gousseau et al. levels range between 0.004 and 0.011 well. For example, alpha-pinene, 1985, Sosa 1979). Likewise, the rate 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 (Puritchand Mullick 1975). would likely increase the level of this nene, which decrease in amount, are stimulant and thus promote greater among the most toxic monoterpenes Drought enhances insect detoxication feeding. The same is true for some to bark beetles (Cates and Alexander systems and immunocompetence. Be- other insects, such as the grasshopper 1982, Mattson and Haack 1987). cause levels of many insect-resistance Locusta migratoria and several lepi- allelochemicals increase during dopterans, that have peak responses Drought-stressed plants are physio- drought, it would seem that stress to relatively high sucrose levels (Matt- logically more suitable for insects. may actually fortify rather than son and Haack 1987). In addition, Drought-stressed plants may be more weaken plant defenses against some the varying levels of osmolytes proba- suitable for insect growth, survival, classes of consuming insects. How bly interact synergistically to further and reproduction because plant nutri- then can outbreaks of these consum- promote host acceptance and feeding ents 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- ticular importance to insects that feed bivore's detoxication systems more chemicals in moderately stressed on woody plants because amounts of than the plant's defenses. One possi- plants would seemingly be detrimen- nitrogen, sugar, and minerals are of- bility is that the increased tempera- tal to insects. However, these in- ten 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 1987, White 1984). Logically, in- detoxicate some plant allelochemi- detoxication capacities of specialized creasing and/or improving the bal- cals. For example, Hinks (1985) re- insects. Moreover, such increases may ance of these nutrients should favor ported that increasing temperatures actually benefit the specialists that insect performance (Haack and reduce susceptibility of the grasshop- utilize allelochemicals as host finding Slansky 1987, House 1974). per Melanoplus sanquinipes to pyre- and accepting cues (Mattson and Several investigators have shown throid insecticides. Similar relation- 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- vival, or reproduction of various Ho- and some carbamates (Hinks 1985, lowing stress (Kimmerer and Koz- moptera, 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 and enhance an insect's ability to detoxi- many bark- and wood-inhabiting sco- mites declined on severely stressed cate compounds. Many studies indi- lytid and cerambycid beetles (Dunn et plants, probably reflecting supraopti- cate that pesticide efficacy varies with al. 1986, Haack and Slansky 1987), mal temperatures, lowered turgor the plant cultivar or species consumed 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 arthropods of 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 during some nontoxic allelochemicals, that Chararas 1979). Not all terpenes are severe drought owing strictly to a stimulate production of the insect's equally reduced, and the concentra- decline in ongoing defenses. For ex- detoxicating enzymes (Terriere1984); 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

114 BioScience Vol. 37 No. 2 concentrationsmay 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 sensitivityof detoxi- The immune system of insects is vironments on insect-symbiont cation mechanisms, such as the less complex than that of vertebrates interactions. 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 on escape the control of their natural (1983) reportedthat honeybeeswere immunocompetence has been done enemies. For example, Wilson (1974) more sensitive to various pesticides with vertebrates. The vertebrate stud- reported that optimal temperatures when their diet containedpollen that ies indicate that nutrient deficiencies for the microsporidian parasite No- was unusually low in protein and and imbalances can reduce general sema fumiferanae of the spruce bud- vitamins. Although poorly under- immunocompetence. For example, worm were below 23? C, but optimal stood, nutrition may also influence Porter et al. (1984) demonstrated that temperatures for 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 hypothesizethat both elevated 1978, Mattson and Haack 1987). between the Banks grass mite Oligon- temperaturesand improvednutrition- 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 similarto the mechanismthat permits tem depends on its anatomical and drought may lower amounts and vir- the fungus Armillariamellea to colo- biochemical links to the nervous sys- ulence of pathogens. For example, nize roots of stressedtrees. 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 stressedtrees becausethe increased tain plant traits may favor or disfavor for germination and penetration of concentrationsof sugars and amino insect immunocompetence via the the insect's integument (Ferron acids increaseits abilityto oxidize the central nervous system. 1985). Similarly, bacterial and viral normallyinhibitory phenols and even diseases may be reduced during to utilize the phenolics as a carbon Drought favors mutualistic microor- drought because many are inactivated source. ganisms but not natural enemies of by the higher ultraviolet radiation lev- The chemical changes induced in phytophagous insects. Drought may els (Ali and Sikorowski 1986, Brock drought-stressedplants may influence influence phytophagous insects indi- et al. 1984, Mattson and Haack interactions between phytophages rectly by optimizing conditions for 1987). Hence, the normal guild of and organisms pathogenic to them. their exo- and endo-symbionts. Be- natural enemies could be rendered The changesmay eitherdirectly affect cause many microbes have thermal less effective during drought, and the pathogens or may enhance the optima of 25?-30? C (Brock et al. thereby fail to regulate an incipient insect'simmune system. High gut lev- 1984), the high temperatures associ- outbreak. els of allelochemicalsthat accumulate ated with drought could stimulate in stressedplants can inhibit growth microbial growth. Likewise, some of Drought may induce genetic changes of ingested pathogens (Barbosa and the chemical changes in drought- in insects. The elevated temperatures Saunders1985, Mattson and Haack stressed plants could enhance micro- and solar radiation associated with 1987). In addition, improved nutri- bial growth; for example, levels of drought may not only affect the rate tion could increasethe insect'scapaci- glucose and fructose often increase in and efficiency of enzymatic reactions ty to suppresspathogenic microorga- the inner bark and sapwood of within an insect, but they along with nisms (e.g., protozoans, fungi, drought-stressed trees (Hodges and various plant biochemical changes bacteria, and viruses), nematodes, Lorio 1969, Mattson and Haack may induce random as well as pro- and parasitoids. Moreover, there may 1987). Because these sugars are the grammed genetic changes in insect be significant synergistic interactions most readily used sources of carbon populations. For example, at the pop- 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

February 1987 115 stress may change gene expressionto (Mattson et al. 1987). Drought pro- of insects whose populations were induce alternate isozymes (Ho- vokes outbreaks of leaf feeders by greatly enlarged during the stress pe- chachka and Somero 1984, Schott providing thermal and nutritional riod (Mulock and Christiansen and Brusven1980). conditions that favor their growth, 1986). Moreover,the thermaland dietary detoxication, and immunocompe- (biochemical)effects of drought can tence. Moreover, these changes also and other stresses trigger genomic modifications, such favor the insects' escape from regula- Drought 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 in is rather limited. Therefore, we hy- Ploeg et al. 1985), amplification of the 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 and decline. 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 et nitrogen in plant foliage, inner bark, temperatures and toxins are generally al. 1984). Such reductions, coupled and 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 of sulfur 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 to Fliickiger 1984), nutrient deficiencies response to stress deserves attention, more innocuous levels (Mattson and (Goring and Thien 1979, Huber especially considering that certain Haack 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 to universal responses to stress, then during outbreaks and latent phases of be primarily regulated by powerful many phytophagous insects appear to their population gradients (Baltens- host defenses, such as preformed be 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 et this 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 If one insect becomes es- feeding guilds dangerous. 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 defense Miller 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 ner-bark feeders. The relative impor- Recovery even under ideal conditions tance of the individual mechanisms is Albert, P. J., C. Cearley, F Hanson, and S. Pari- nearly impossible. sella. 1982. of eastern the of host Feeding responses may depend upon types Compromised plant defenses, spruce budworm larvae to sucrose and other defenses normally encountered; the droughts, and such other factors as carbohydrates.J. Chem. Ecol. 8: 233-239. nutritional quality of host tissues or fire, lightening strikes, and natural Ali, S., and P. P. Sikorowski. 1986. 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Entomol. 8: 439-490. natural enemies, and low nutrient lev- malize, populations of these insects Ayres, P. G. 1984. The interaction between stress and biotic dis- els. It is sufficient for plants to control decline primarily, we believe, because environmental injury ease physiology. Annu. Rev. Phytopathol. these insects imprecisely, because of the plant's restored defenses. How- 22: 57-75. most plants can compensate for and ever, even these "recovered" plants Baltensweiler, W. 1984. The role of environ- recover from the feeding damage may be overwhelmed by mass attacks ment and reproduction in the population

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