Offensive-Defensive Interactions Between Herbivores and Plants: Their Relevance in Herbivore Population Dynamics and Ecological Theory Author(S): David F

Offensive-Defensive Interactions between Herbivores and Plants: Their Relevance in Herbivore Population Dynamics and Ecological Theory Author(s): David F. Rhoades Reviewed work(s): Source: The American Naturalist, Vol. 125, No. 2 (Feb., 1985), pp. 205-238 Published by: The University of Chicago Press for The American Society of Naturalists Stable URL: http://www.jstor.org/stable/2461633 . Accessed: 12/03/2012 11:49

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http://www.jstor.org Vol. 125, No. 2 The AmericanNaturalist February 1985

OFFENSIVE-DEFENSIVE INTERACTIONS BETWEEN HERBIVORES AND PLANTS: THEIR RELEVANCE IN HERBIVORE POPULATION DYNAMICS AND ECOLOGICAL THEORY

DAVID F. RHOADES

Departmentof Zoology, Universityof Washington,Seattle, WA 98195

SubmittedNovember 9, 1983; Accepted June 26, 1984

Manyspecies of smallherbivorous animals such as insects,voles, rabbits, and leaf-eatingbirds exhibitwide variationin populationnumbers through time. Populationsof somespecies remain at low levelsfor a numberof years, erupting to highlevels at irregularintervals (Berryman and Baltensweiler1981). Spruce budworm(Morris 1963), the Africanarmyworm (Khasimuddin 1981a; Odiyo 1981),many species of bark beetles (Berryman 1979), and locusts (Kennedy 1956; Tsyplenkov1978) typify these species. Populationsof otherspecies exhibit re- markablyregular cycles (Berryman and Baltensweiler1981) with periodicities of about4 yrin microtinerodents (voles and lemmings;Keith 1974; Finerty 1980), andabout 10 yrin muskrats,hares (Keith 1974; Finerty 1980), grouse and ptarmigan (Keith 1963),larch budmoth (Baltensweiler et al. 1977),Douglas-fir tussock moth(Brookes et al. 1978),and foresttent caterpillars (Hodson 1941). These populationvariations have been of great interest to theoreticalecologists and pest and game managersfor many years. Traditionally, population variations have been attributedto a combinationof directweather-induced changes in mortality and natalityof herbivores,together with effects of competitionfor food and varyinglevels of predation,parasitism, and disease (see Cold SpringHarbor Symposiaon QuantitativeBiology 1957). This is becausepopulation eruptions are sometimescorrelated with unusual weather, and populationcollapses are some- timesassociated with food depletion and increased levels of parasitism, predation, and disease. However,mathematical population models based on theseclassical factorshave so farproved relatively unsuccessful in predictingpopulation trends (Baltensweiler1968; Fye 1974;Stehr 1974; Waters and Stark1980). The correla- tionbetween eruptions and unusualweather is notclear-cut. Usually the correlation is only a partialone. It is also becomingclear thatweather often acts indirectlyrather than directly affecting herbivore mortality. Similarly, populations oftencollapse in thepresence of an abundanceof food, and in a waythat cannot be accountedfor by weather,predation, parasitism, or disease (see Rhoades 1983a).

Am. Nat. 1985. Vol. 125, pp. 205-238. ? 1985 by The Universityof Chicago. 0003-0147/85/2502-0007$02.00.All rightsreserved. 206 THE AMERICAN NATURALIST

DEFENSIVE OFFENSIVE ADAPTATIONS ADAPTATIONS

|PRODUCERS ONS MER

FIG. 1.-Offensive-defensivecoevolution between consumers and producers. Solid arrows = "lead to theevolution of"; dashedarrows = "selectsagainst." Defensive adaptations referto producersand offensiveadaptations refer to consumers.

In thesetraditional models, plants have been viewedas passiveparticipants. Thereis now strongevidence, however, that plants are farfrom passive in their interactionswith herbivores. In thispaper, I brieflyreview the evidencethat plantsare defendedagainst herbivores, that plant nutritional quality to herbivores can vary as a functionof physicalstress of plantsand degreeof herbivory experiencedby plants, and thatdefensive communication between plants exists. I postulatethat acquired immunity to herbivoresmay be an importantcomponent ofplant defense. Finally, I suggestthat there may be twoalternative strategies of herbivoresto counterplant defensive systems. These strategiesmay explain why populationlevels of some species of herbivores are variablewhile those of others are relativelyinvariant, why some speciesof herbivoresexhibit phase polymorphism,and togetherwith other considerations, why it has proveddifficult to demonstratecompetition between herbivores.

DEFENSIVE ADAPTATIONS OF PLANTS AND COMPLEMENTARY OFFENSIVE ADAPTATIONS OF HERBIVORES Offensive-DefensiveCoevolution between Consumersand Producers The existenceof producerorganisms has led to the evolutionof consumer organismsthat prey on them(fig. 1). Individualproducer organisms with properties whichrender them less suitableas preyshould be at a relativeadvantage comparedto individualproducers which lack these properties.Predation by consumerson producersshould therefore lead to the evolutionof defensive adaptationsin producers(fig. 1). Similarly,individual consumers with properties thatenable them to overcomeprey defenses will be at an advantage.This should lead to the evolutionof offensiveadaptations in consumersthat decrease the effectivenessof prey defenses. These offensiveadaptations, in turn,feed back to selectfor amplified prey defenses, and so on. The evolutionarypositive-feedback loop betweenoffense and defenseis probablylargely controlled by the metabolic cost (Leonard1977; McKey 1979;Rhoades 1979;McLaughlin and Shriner1980; Mooneyand Gulman1982) of defensiveand offensiveadaptations (fig. 1). For each knowndefensive adaptation in producerorganisms we can thereforeexpect to findcomplementary offensive adaptations in consumers and vice versa. Known and possibledefensive adaptations of plantsagainst herbivores and theircom- INTERACTIONS BETWEEN HERBIVORES AND PLANTS 207

DEFENSIVEADAPTATIONS OFFENSIVEADAPTATIONS OF HERBIVORES OF PLANTS

STEALTH OPPORTUNISM 10 11 12 COMMUNICATION SUPPRESS, EMIT BETWEEN 'COMMUNICATION'ICOUNTERS IGNALS' --- - PLANTS L ? --

7 8 9 ACQUIRED SUPPRESS L IMMUNITY_ 'RECOGNITION SURPRISE L __EGI______L _EC_PRECOGNITION_ __ I__N 5 ~~~~~6 r 4 | |SUPPRESS [fINDUCE| INDUCIBLE INDUCED DECREASED DEFENSES DEFENSES DEFENSES

I 2 3

CODENSTVES 11IDETOXIFY [AVOID LITTLEOR NO EVIDENCE 5 MUCHEVIDENCE O SOMEEVIDENCE LJ[ FIG. 2.-Defensive adaptationsof plantsand complementaryoffensive adaptations of herbivores.Each knownor postulatedadaptation is referredto bynumber in thetext. plementaryknown and possibleoffensive adaptations in herbivoresare displayed infigure 2. For each defensiveattribute of plants, two alternative offensive tactics in herbivoresare knownor can be postulated(fig. 2), as in thefollowing discussion.

Passive Plant Defense and Counteradaptationsof Herbivores Duringthe last 30 yearsit has becomeclear thatmany of the chemicalcon- stituentsof plants (plant secondary metabolites) protect plants against attack from pathogensand herbivores,and are used by plantsto interferewith the growth or germinationof competing plants (Rice 1974;Wallace and Mansell 1976; Harborne 1978;Rosenthal and Janzen1979). With respect to plant-herbivoreinteractions, attentionhas beenfocused, until quite recently, on preformedconstitutive (Levin 1971)defensive substances of plants(fig. 2.1) thatdeter and toxifyherbivores. Some of thesecompounds, such as alkaloidsand cyanogens,have a directtoxic action.Others, such as tanninsand lignins, may act by reducing the digestibility of planttissues (Feeny 1975,1976; Rhoades and Cates 1976;Rhoades 1979;Swain 1979;but see Bernays1981; Klocke and Chan 1982;Zucker 1983). To circumventthe effectsof plant defensivesubstances, herbivores have evolveddetoxification mechanisms (fig. 2.2). The mostwidely recognized of these mechanismsis metabolicconversion of the defensivesubstance to a less toxic derivative,followed by excretionof the metaboliteor its conjugate(Millburn 1978;Brattsten 1979; Dowd et al. 1983).In addition,dietary toxins are degraded withinthe gut of ruminantand nonruminantvertebrates by microbialactivity 208 THE AMERICANNATURALIST

(Freelandand Janzen1974; Allison and Cook 1981).The highgut pH observedin manyphytophagous insects may be an adaptationto inhibitcomplex formation betweenplant tannins and proteinsor otherdietary constituents, to thuscircum- ventthe digestibility-reducingaction of tanninsin planttissues (Feeny 1970; Rhoades 1977;Berenbaum 1980). Some adaptedherbivores have evolvedrefrac- torymetabolism in which target enzyme systems are relatively insensitive to plant toxins(Rosenthal et al. 1976;Vaughan and Jungreis1977; Jaenike et al. 1983). In additionto detoxifyingplant defensive metabolites, most herbivores, to one degreeor another,use thesesubstances as cuingstimuli to aid in therecognition of theirhost plants (see Rhoades 1983a). Use of plantdefensive chemicals has been carrieda stagefurther by manyherbivores which store them for their own defense(Rothschild 1973) or nutritionallybenefit from their presence in thefood (Rosenthalet al. 1977;Berenbaum 1981; Bernays and Woodhead 1982; McFarlane and Distler1982). Besidesdetoxifying and using plant defensive substances, herbivores also avoid them(fig. 2.3). Food selectionby herbivoresis determinedlargely by a general positiveresponse to sugars,salts, amino acids, and other primary nutrients found in all plants,coupled with positive and negativeresponses to thespecific second- arymetabolites in hostand nonhostplant species (see Rhoades1983a). Withina hostplant species, or withinan individualhost plant, herbivores often preferentiallyattack those plants or tissueswhich contain low levels of secondary metabolites (Jones 1972; Cates 1975; McKey 1979; Rhoades 1979; Schultz 1983a; Whitham1983). The demonstrationofdeterrence of herbivore feeding or oviposi- tionby secondary metabolites (fig. 2.3) has beenone ofthe main methods used to establishthe protective action of secondary metabolites to plants(Rhoades 1979). The discussionto thispoint encompasses what can be termedthe theoryof passive plant defense against herbivores(see Fraenkel 1959; Ehrlichand Raven 1965;Feeny 1975,1976; Rhoades and Cates 1976).Salient features can be sum- marizedas follows.Each speciesof planthas evolveda uniqueset of defensive metaboliteswhich deter attack from most herbivores except those few species whichhave brokenthrough the defenses by counteradaptation.Each speciesof herbivorehas evolvedcounteradaptations against the defenses of a limitednum- berof plant species. Herbivores use theplant defensive systems to whichthey are adaptedas host-findingcues and feedingstimulants, while avoiding plant species containingdefensive systems to whichthey are notadapted and thosetissues of theirhost species whichcontain levels of defensivesubstances sufficient to overloadthe accommodation mechanisms of the herbivores. Apart from containingdefensive chemicals, the plants were regarded as passive,and theirdefenses wereregarded as static.It is nowbecoming clear that plants are much less passive in theirinteractions with herbivores than originally conceived, and their defenses are farfrom static.

Active Plant Defense and Counteradaptationsof Herbivores A varietyof influencesstressful to plantspromotes attack by phytophagous insects.These stressfulinfluences include water deficit or surplus,unusual or INTERACTIONS BETWEEN HERBIVORES AND PLANTS 209 rapidlychanging climatic conditions, nutrient-poor soils, competition from other plants,pollution, and damageduring cultural operations (see Mattsonand Addy 1975; Rhoades 1983a). White(1969, 1974, 1976) suggestedthat insects often preferentiallyattack physically stressed plants, and exhibithigh fecundity and survivalwhen feeding on them,because stressleads to increasedconcentrations of freeamino acids and othersoluble nitrogenous constituents in planttissues. Compromiseddefensive systems in stressedplants are probablyof greater importance,however (Rhoades 1979, 1983a; Wrightet al. 1979;Waring and Pitman 1983).Thus, by attacking stressed plants, herbivores can minimizetheir exposure to plantdefenses (fig. 2.3). Forexample, the oleoresin exudation pressure of pines experiencinga water deficit is reduced,resulting in increasedbark beetle survival (Vite 1961). Similarly,defoliation causes decreasedmonoterpene production in the stemsof grandfirs, which promotes successful attack by the firengraver beetle(Wright et al. 1979).In othercases, theeffects of stresson plantdefensive chemistryare less clear-cut.While some compounds decrease in concentrationin tissuesof stressed plants, other compounds increase. This may be due to realloca- tion,by stressedplants, of resources from costly but effective defensive systems to less costlybut less effectivedefensive systems (Rhoades 1979, 1983a). While most experimentalwork and theoryconcerning the effectsof plant defenseson plant-herbivoreinteractions has, until recently, focused on preformed constitutivedefenses, the dual importanceof constitutiveand inducibleplant defenseshas longbeen recognized by plant pathologists (Muller and Borger 1941; Muller1956; Levin 1971; Horsfalland Cowling1980). Inoculationwith fungi (Suzuki1980), bacteria (Goodman 1980), viruses (Hamilton 1980), and nematodes (McIntyre1980) can increaseresistance of plantsto furtherchallenges by the pathogens(see also Kuc 1982).In thecase ofattack by fungi, the mechanisms of inducedresistance are fairlywell understood.They involve the accumulation of low molecularweight antibiotic compounds (phytoalexins) and polymericlignins, tannins,enzyme inhibitors, and agglutinins(Kuc and Caruso 1977;Suzuki 1980). Duringthe last 10 yearswe have recognizedthat plants also possess inducible defensesagainst herbivores (fig. 2.4). Plantscan changetheir chemical properties to rendertheir tissues less suitablefor herbivore growth and development in direct responseto herbivoredamage or simulatedherbivore damage. Much of the evidencefor these plant responses has been reviewedby Rhoades(1979, 1983a; see also Berryman1972; Raffa and Berryman1982; Schultz and Baldwin1982; Karban 1983; McNaughtonand Tarrants1983). Rapid responses,which affect currentherbivores, and delayedresponses, which protect plants against subsequentgenerations of herbivores, are known(Haukioja and Hakala 1975;Haukioja 1980;Rhoades 1983a). Responsesdo notappear to be restrictedto plantsof any particulartaxonomic affinity or growthform. Systemic accumulation of leaf phenoliccompounds following leaf damage has beenobserved in manyspecies of trees.Local productionof terpenes at thesite of damage is a commonresponse of conifersto attackby bark beetles.A varietyof chemicalresponses has been observedin herbaceous plants. Whether damage-induced responses are caused by increasedcontent of constitutivedefensive chemicals or the accumulationof differentsubstances is unknownin manycases, butboth types of response have 210 THE AMERICANNATURALIST beenobserved. For example,fiber (lignocellulose) in larch(Benz 1974,1977) and wheatgrass(Higgins et al. 1977)or tanninlikesubstances in birch(Niemela et al. 1979),alder (Rhoades 1983b), sedge (Rhoades 1983a), oak (Schultzand Baldwin 1982), maple and poplar (Baldwin and Schultz 1983), or silica in grasses (McNaughtonand Tarrants1983) are all presentat relativelyhigh concentrations inthe unattacked plants, with moderate increases stimulated by insect or mechanical damage.On the otherhand, proteinase inhibitors in tomato(Nelson et al. 1983), coumestrol(an estrogeniccompound) in alfalfa(Loper 1968), and juvabione-relatedcompounds (potential insect juvenile hormone analogues) in firs (Puritchand Nijholt1974), produced by the plantsin responseto insectsor mechanicaldamage, are not presentor are scarcelydetectable in unattacked plants.I suggestthat the conceptsof "qualitative"and "quantitative"plant defensivesystems proposed by Feeny(1975, 1976; see also Rhoadesand Cates 1976;Rhoades 1979)may be usefulin explainingthis dichotomy. Quantitative defensivesubstances such as lignin,tannins, and silicaare postulatedto act in a dose-dependentmanner, even againstadapted herbivores. An attackedplant can thereforegain protection against subsequent attack from the same herbivoreby increasingthe concentration of these substances in itstissues. On theother hand, qualitativedefensive substances such as specificenzyme inhibitors and animal hormoneanalogues, although providing protection from nonadapted herbivores at low concentration,are postulatedto providelittle protection against adapted herbivoreseven at veryhigh concentrations. An attackedplant would therefore gainlittle protection against subsequent attack from the same consumerby increasingthe concentrationof qualitativedefensive substances already present duringthe initialattack. In this case, the synthesisof novel substances,not presentin the unattackedplant, would be a moreeffective defense. We can thereforeexpect that responses involving quantitative defensive substances usually should resultfrom increases in concentrationof substancespresent in significantquantities in unattackedplants, whereas responses involving qualitativedefensive substances should usually be caused by substancesnot found in significantconcentrations in unattackedplants. In otherwords, quantitative defenses should participate mainly in quantitative responses and qualitative defenses should participatemainly in qualitative responses. The existenceof inducibledefensive responses in plantsshould select for adaptationsin herbivoresto suppressthe responses (fig. 2.5). In addition,given thatplant defensive systems are plastic,adaptations in herbivoresthat actively decreaselevels of defense in plants(fig. 2.6) are likely.There is evidencefor both ofthese tactics in herbivores.Many species of bark beetles mass-attack their host treesusing aggregation pheromones (Coster and Johnson1979; Wood 1982).In some conifers,exudation pressure of preformedresin (the constitutive defense) and local synthesisof resinat the site of attack(the induceddefense) are so reducedby the weightof numbersof attackingbeetles that the treesuccumbs (Berryman1969, 1972; Cates and Alexander1982; Raffa and Berryman1983). Thus,through concerted attack, bark beetles can reducethe effectiveness of host defensesfar below thatexperienced by a singleattacking beetle (fig. 2.6). Some insects,particularly bark beetles and otherboring insects, are dependenton INTERACTIONS BETWEEN HERBIVORES AND PLANTS 211 ectosymbioticrelationships with viruses, mycoplasms, bacteria, fungi, protozoa, or nematodesto achievesuccessful attack. The symbiontsinfest and propagate in theplant, increase the nutritional quality of plant tissues to theinsect, and in some cases, themselvesbecome the mainfood source(Norris 1979; Whitney 1982). Leaf compostingby leaf-cutting ants (Cherrett 1972) can be viewedas an extreme formof this tactic. Gall-formingand plant-suckingarthropods in generalare known,or stronglysuspected, to injectsubstances into plants that increase their nutritionalquality (Miles 1968a, 1968b,1978; Dieleman 1969; Carter 1973; Os- borne1973; Markkula et al. 1976;Hori 1976;Hori and Endo 1977;Dropkin 1979; Norris1979; Cornell 1983a, 1983b).For instance,the saliva of Hemipteraoften containspolyphenoloxidase enzymes which appear to oxidativelyneutralize plant defensivephenolic compounds and/or be involvedin theproduction of auxin-like compoundsin situ(fig. 2.6; Miles 1968a,1968b, 1978). Sirex wood wasps inject a toxinand spores of a symbioticfungus during oviposition in stemsof Pinus radiata.The toxinblocks translocation of photosynthate from the leaves, curtail- ingsynthesis by theplant of polyphenols and resinsin theattack lesions. Exuda- tionof preformedresin into the lesions is also reduced.The fungusthen rapidly invadesthe conductivetissue of the plantto inducetranspirational stress and providea suitablesubstrate for the developing Sirex larvae (fig. 2.6; Coutts1968, 1969a,1969b; Madden 1977). Some lepidopteran leaf-miners retard senescence of leavesin whichthey are feedingto produce"green islands" in theleaves. Mined areasof leaves and thecaterpillars contain high levels of cytokinins (Engelbrecht et al. 1969;Engelbrecht 1971). Green islands have also beenobserved to develop aroundthe feedingsites of otherinsects (see Osborne1973; Kahn and Cornell 1983). The squashbeetle Epilachna tredecimnota cuts a circulartrench around an area of squash leaf,so thatonly a fewveins and pieces of lowerepidermis hold the encircledleaf sectionin place. The beetlethen feeds on theexcised area. This behaviorprevents the plant from mobilizing defensive substances into the feeding site(fig. 2.5; Carrolland Hoffman1980). Alder sawflies (Eriocampa ovata) cutall themain veins of a leafof red alder before feeding on it (Mackayand Wellington 1977).Many insect species girdle a stembefore feeding on thedistal part or attack a petiolebefore feeding on theleaf (see Rhoades1983a). These behaviorsproba- blyprevent the mobilization of defensivechemicals into the feeding region (fig. 2.5), or cause theaccumulation of nutrients in it,or both.There may also be less obviousways in whichherbivores suppress plant defensive responses (fig. 2.5), forinstance by producing salivary components that interfere with the mechanisms whichplants must possess in orderto recognizedamage. For instance,Miles (1968a) suggestedthat one of the functionsof the salivarysheath secreted by phytophagousHemiptera may be to reducethe chance of defensive responses by theplants. It wouldbe adaptivefor plants to recognizethe difference between mechanical damageand herbivoredamage and also betweendamage by differentherbivore species(fig. 2.7). Acquiredimmunity of plants against particular herbivore species is a furtherpossibility (fig. 2.7). Effectsof this kindare well establishedin interactionsbetween plants and pathogens.In manycases, plantpathogens suc- 212 THE AMERICANNATURALIST cessfullyinvade susceptiblehosts not so muchbecause theycan detoxifyor toleratethe defensive response of their host plant, but rather because they are not recognizedas foreignby the plant and defensiveresponses are not induced (Sequeira 1980).To myknowledge, there is no directevidence for differential defensiveresponse of plantsto mechanicalversus herbivore damage, to damage by differentherbivore species, or foracquired immunity in plantsto particular herbivorespecies. There is, however,considerable evidence showing that regrowthrates of plants following grazing by grasshoppers and ungulates, or follow- ingmechanical clipping plus application of saliva or salivacomponents, can differ significantlyfrom regrowth rates following clipping alone (Reardonet al. 1972, 1974;Dyer and Bokhari1976; Dyer 1980;Capinera and Roltsch1980; Detling and Dyer 1981;Detling et al. 1981).In somecases regrowthwas reducedcompared to clippedcontrols, in othersit was stimulated,and in stillothers no differencewas observed.These variouseffects on regrowthrates are possiblymanifestations of underlyingoffensive-defensive interactions between plants and herbivoresin whichenhanced regrowth rates are associatedwith an inducedincrease in food qualitycaused by herbivoresalivary secretions, whereas decreased regrowth ratesare associatedwith an induceddecrease in foodquality controlled by the plant.In otherwords, herbivore saliva may contain factors which cause plantsto allocatemore resources to growthand less to defense(fig. 2.6). If theplant has evolvedmechanisms to recognizethe salivary factors of the particular herbivore, withor withoutprior conditioning from attack by thatherbivore, the plant allo- cates less to growthand moreto defensefollowing an attack(fig. 2.7). Compari- sonsof defensive commitment and regrowthrates of plants following mechanical damagewith those following attack by a seriesof herbivoreswhich vary in their degreeof naturalassociation with the plants, and followingattack by herbivores on naive plantsversus plantsconditioned by previousattack, may prove re- vealing. My interpretationof the effectsof salivaryconstituents on plantregrowth followingdamage differs from that of Dyer et al. (1982).These investigators(see also Owen and Wiegert1976, 1982) inferred,from cases in whichgrazing or treatmentwith salivary extracts stimulated plant growth, that plant-grazer interac- tionshave a mutualisticcomponent, at leastat low levelsof damage. As notedby McNaughton(1979) and Stenseth(1983), however, increased growth caused by grazingdoes notnecessarily lead to increasedplant reproductive fitness. To my knowledge,there is no evidencefor enhancedreproductive fitness of grazed plantsrelative to ungrazedcompetitors. In addition,it is difficultto reconcile cases of decreasedgrowth of plantscaused by salivaryand crop secretions (Detlingand Dyer 1981),or decreasedgrowth of plantsgrazed by herbivores comparedto clippedcontrols (Capinera and Roltsch1980), with plant-grazer mutualism.On theother hand, both stimulation and inhibitionof plant growth by herbivoresand theirsecretions can be readilyunderstood if herbivoreshave evolvedadaptations to manipulateplant nutritional quality to theadvantage of the herbivores,and plants,in turn,have evolvedmechanisms to recognizethese adaptationsand use themas defensivecues. Ifrecognition and acquired immunity are componentsof plant defensive adapta- INTERACTIONS BETWEEN HERBIVORES AND PLANTS 213 tion(fig. 2.7), we can expectadaptations, such as salivarysecretions, to suppress recognitionin some herbivores(fig. 2.8). Surprisewould be an alternativetactic (fig.2.9). All mobileherbivores which feed on manydifferent individual plants duringtheir lifetime possibly employ surprise to one degreeor another,since thereis littletime for induction of defensiveresponses before departure of the herbivore.Herbivore species in whichmigration or dispersalare importantfea- turesof theirpopulation dynamics, such as locusts(Uvarov 1977;Taylor 1979), sprucebudworm (Clark et al. 1978),larch budmoth (Baltensweiler and Fischlin 1979),tent caterpillars (Wellington 1980), armyworms (Odiyo 1981),and voles (Thompson1955; Finerty1980), may also use thistactic by immigratinginto populationsof naiveplants and thenemigrating before, or as soon as, defensive responsesare induced. Advancedwarning of attack (fig. 2.10) wouldbe highlyadvantageous to plants. There is limitedevidence that unattacked plants can detectand defensively respondto airbornesubstances emitted by nearbyattacked plants. Rhoades (1983b)found that leaf quality, as measuredin bioassays, of Salix sitchensis trees attacked by tentcaterpillars and nearbyunattacked control trees declined within 14.5 days of the initiationof attack. No evidence was foundfor root connections between the trees. Given thatplants in general (Hanover 1972; Rasmussen 1972; Abeles 1973; Freeland 1980; Smith 1981), and willows in particular(Rasmussen 1970),emit volatile organic compounds into the atmosphere,and thatin some cases the amountsand type of emissionscan be changedby plantdamage (Rhoades,in prep.),Rhoades (1983a) proposedthat plants could receive phero- monalsignals emitted by nearbyattacked trees. To testthis idea, Baldwinand Schultz(1983) confined individually potted sugar maple seedlings in twogrowth chambers.They thentore leaves on some of the plantsin one chamberand comparedthe phenolic chemistry of the damaged plants, undamaged plants in the same chamber(communication controls) and undamagedplants in the separate chamber(true controls), for several days following damage. They found increased levelsof leaf total phenolics and tannins in leaves of the damaged plants and in the communicationcontrols compared to the true controls.Similar results were obtainedwith poplar. Their results support the hypothesis of pheromonalcom- municationbetween plants in responseto damage.Perry and Pitman(in press) foundchanges in foliagetoxicity of Douglas-firto westernspruce budworm that occurredcoincidentally with the appearance of a rapidlybuilding natural population of budwormin the vicinityof theirstudy trees. They suggestintertree communicationas a possibleexplanation for this result. If damage-inducedpheromonal communication between plants is commonwe can expect some herbivoresto have evolvedadaptations that suppress it (fig. 2.11).This could occur as an indirectresult of suppression of recognition of attack (fig.2.8) or throughherbivore secretions that block the release of communication substancesfrom the wound. Alternatively, some herbivores may themselves emit pheromonalcountersignals to confuse,mimic, or otherwiseinterfere with the signalsgenerated by plants(fig. 2.12). For example,herbivores may produce a signalwhich causes plantsto reallocatedefensive substances from the attacked tissueto othertissues, leading to an increasein nutritionalquality of thefood. 214 THE AMERICANNATURALIST

Indeed,if plant pheromonal communication is common, it wouldbe surprisingif someherbivores did not exploit the system, especially considering that herbivores heavilyutilize airborne chemical signals such as sex, alarm,and aggregation pheromones,many of whichare closelyrelated to or even derivedfrom plant volatiles(Prokopy 1981; Roelofs 1981; Borden 1982; Wood 1982;Weldon 1983). An exampleof the reversephenomenon, in whicha plantinterferes with a pheromonalcommunication system of an herbivore,is knownin wild potato whichrepels aphids by releasingthe alarm pheromone of theaphid (Gibson and Pickett1983). It is thereforepossible that offensive-defensive interactions be- tweenherbivores and plants are conducted,in part, at thepheromonal level. If so, interactionsat the level of gustation,plant tissue chemistry,and catabolic detoxification,stressed in muchrecent research, may in manycases assumea secondaryrole. I suggestthat the combinations of herbivore offensive tactics 2, 5, 8, 11,or 3, 6, 9, 12 (fig.2) constitutealternative attack strategies, which I termstealth and opportunism,respectively.

STEALTH, OPPORTUNISM, AND HERBIVORE POPULATION DYNAMICS Althoughall herbivorepopulations fluctuate to somedegree, population levels of some species are muchmore variable and rise to muchhigher levels than others.Differences in generationtimes and intrinsicrates of populationincrease amongherbivore species are obviouslyinvolved to somedegree. Invertebrate and smallvertebrate herbivores often have shortergeneration times and higher repro- ductionrates than large vertebrate herbivores. This probablycontributes to the highervariability of populationnumbers in the formergroup by allowingtheir populationsto respondrapidly to favorablechanges in food qualityand other influences.There are, however,great differences in populationvariability even amonginvertebrate and smallvertebrate species. In naturalsystems, most species ofsmall herbivores have low, relatively stable populations but a fewspecies show wide populationswings (Berryman and Baltensweiler1981; Schultz 1983b). Schultz(1983b) estimated that fewer than 10% of thespecies listed in theCana- dian Forest Surveyof Lepidoptera(Prentice 1962, 1963) exhibitperiodic or occasionaloutbreaks. Despite their small number, these pest species often consti- tutethe mostabundant and destructiveherbivores in naturalenvironments. I suggestthat species withlow, relativelyconstant populations may be stealthy, whereasthose with variable populations may be opportunistic(fig. 2, table1), or at leastmay employ the latter strategy part of thetime.

Population Dynamics of StealthyHerbivores Inhibitionof plantdefensive response is an importantcomponent of thepro- posed stealthystrategy. Since defensiveresponses are morelikely to be induced as amountof damageincreases, we can expectstealthy herbivores to display adaptationsthat minimize their impact on plantfitness. Thus, stealthy herbivores shouldattack tissues that are of relativelylow valueto theirhost plants, such as INTERACTIONS BETWEEN HERBIVORES AND PLANTS 215

TABLE 1 PROPOSEDCHARACTERISTICS OF STEALTHY AND OPPORTUNISTIC HERBIVORE SPECIESOR PHASES IN ADDITIONTO THOSEOF FIGURE2

Stealthy Opportunistic

Invariantpopulation levels Variable populationlevels Conservativeuse of the host plant Profligateuse of the host plant Attack tissues of low value to the host Attack tissues of highvalue to the host High efficiencyof conversionof ingested Low ECI material(ECI)t Low rate of conversionof ingestedmaterial (RCI) Variable* RCI High digestibilityof food (AD)t Low AD Low feedingrate (consumptionindex, CI)t Variable* CI Low body temperature High body temperature Low metabolicrate High metabolicrate Constantlevels of parasitismand predation Variable** levels of parasitismand predation Constantgrowth, survival, and reproductiverates Variable* growth,survival, and reproductive rates Low maximumintrinsic rate of populationincrease High I'max

(rmax) Low maximumfecundity (bmax) High bmax Nonmigratory Migratoryand nonmigratory Sexual reproduction Sexual and parthenogeneticreproduction Mutual interference Mutual facilitation Single eggs Clusteredeggs Solitary Gregarious Territorial Colonial Regular spatial dispersionof damage Contagious spatial dispersionof damage

* High duringpopulation increase, low duringpopulation decrease. ** Low duringpopulation increase, highduring population decrease. t Nomenclaturefollows Waldbauer (1968). matureleaves as opposed to youngleaves and growingtips, and theyshould efficientlyconvert plant biomass into herbivore biomass. They should also avoid theirfellows when foraging or ovipositingsince a plantexperiencing attack from a singleherbivore is less likelyto responddefensively than one attackedby many. In otherwords, mutual interference should occur betweenstealthy herbivores thatattack the same type of tissue. This should result in a solitaryhabit; the wide dispersalof singleeggs by invertebrates(see Stamp 1980); a regular(even) dispersion(Southwood 1978) of damage among individual host plants; and territorial defenseof the resourcein some cases (table 1). Territorialityis common amonginvertebrate and vertebratefolivores, particularly in butterflies,grasshoppers,and primates(Hladik 1978;Montgomery 1978; Baker 1983).The stealthy strategywould lead to low and relativelyconstant populations because as herbivorepopulations rose above a certainlevel, rapid plant responses, acting on the attackinggeneration of herbivores, should lower their fecundity and increase their mortality.Besides directlyaffecting herbivores, the plant responses should also increasetheir susceptibility to parasitismand predation(see Priceet al. 1980; Schultz1983a; Rhoades 1983a). Populationlevels of stealthy herbivores are thus viewedas beingunder the influence of rapidnegative feedback from changes in plantnutritional quality and consumersat highertrophic levels. 216 THE AMERICAN NATURALIST

Population Dynamics of OpportunisticHerbivores

For opportunisticherbivore species, two substrategiesare suggested.First, theypreferentially attack plants whose defensesare compromisedby physical stress(fig. 2.3). Afterthe periodof stresshas passed, the plantsregain their defensivecapabilities, responses are induced,and the herbivorepopulations collapseunder the influence of direct nutritional effects and increased susceptibil- ityto parasitesand predatorscaused by poorfood (Rhoades 1983a). This results in eruptivepopulation dynamics, with the timingof outbreakscorrelated with climaticor otherevents stressful to plants.Outbreaks of locusts(see below), sprucebudworm (Morris et al. 1958;see also Rhoades1983a), and barkbeetles (Berryman1978) are inthis category. If the period of plant stress is sustained,this resultsin continuedhigh populations of herbivoresand totaldestruction of the plantresource in somecases, leadingto herbivorepopulation collapse from lack of food. Strongmigratory or dispersalability should be characteristicof the herbivoresto enable themto locate stressedhosts. Alternatively, opportunists invadea portionof their geographical range occupied by naive plants which have notbeen immunized by recentattack (fig. 2.9). High-qualityfood leads to a rapid and largeincrease in herbivorepopulation. The plantsultimately increase their chemicaldefenses and the herbivoresemigrate. In timethe plantslose their immunityand the herbivoresreturn. This resultsin cyclicpopulation dynamics withthe periodicity dependent on theinduction and relaxationtimes of acquired immunityand associated changesin plantdefensive commitment. Cycles of grouse,ptarmigan (Keith 1963), voles, lemmings, snowshoe hares (Finerty 1980; Bryant1981), larch budmoth (Baltensweiler and Fischlin 1979), and Urania moths (Smith,in press)may result from this mechanism. Possibly,opportunists emit countersignals (fig. 2.12) thatcause increasedplant nutritionalquality (fig. 2.6) untilrecognition (fig. 2.7) occurs.Alternatively, these signalsmay delay recognition and theonset of defensive responses. In contrastto stealthyherbivores, opportunists can be expectedto displayadaptations which stresstheir host plants (e.g., barkbeetles and Sirex), and to attacktissues of high valueto theplant. Mass attack,to overloadplant defense mechanisms, may be an importantcomponent of theopportunistic strategy. Aggregation would also lead to numericalamplification of countersignals.In otherwords, mutual facilitation betweenopportunists is probable.We can thereforeexpect opportunists to displayadaptations which promote aggregation, such as eggclustering (e.g., spruce budworm,Douglas-fir tussock moth, gypsy moth, tent caterpillars, fall webworm, fallcankerworm, armyworms, Urania moths,and locusts),aggregation pheromones(Prokopy 1981), and coloniality.A contagious(clumped) spatial dispersion (Southwood1978) of damage and a migratoryhabit are also to be expected(table 1). Migratorybehavior, however, is nota necessaryrequirement in specieswith variablepopulations if they undergo transition between stealthy and opportunistic phases(see Douglas-firtussock and gypsymoths discussed below). Rapidpopulation build-up of opportunistswould enable them to takethe most advantageof transitory circumstances that impair plant defensive capability, thus selectingfor high maximum fecundity and high maximum intrinsic rates of popula- INTERACTIONS BETWEEN HERBIVORES AND PLANTS 217 tionincrease in opportunistsas opposed to stealthyherbivores. Growth rates, survival,and reproductiverates of opportunistsshould therefore be highduring populationeruption resulting from high-quality food and low duringpopulation collapse, whereasthese propertiesshould be relativelyconstant for stealthy herbivores.Similarly, mortality of opportunistsfrom parasitism and predation shouldbe low duringpopulation increase as the resultof satiationand low susceptibilitycaused by high-quality food of the herbivores, whereas it shouldbe highduring collapse. On theother hand, stealthy herbivores should exhibit relativelyconstant rates of parasitismand predation(table 1). Populationsof oppor- tunistsare thusviewed as beingunder the influence of positive feedback resulting frommutual facilitation and predatorsatiation during population increase, and delayed negativefeedback from plant defensive responses and consumersat highertrophic levels during population decrease. Watt (1965) analyzeddata for Macrolepidopteragathered by the Canadian ForestInsect Surveyand foundthat although there were far fewer gregarious species (n = 32) thansolitary species (n = 520), gregariousspecies had much higheraverage abundances and farmore variable population levels than solitary species.This findingsupports the present analysis, but whether the same trend willbe foundfor solitary and gregariousherbivore species other than Canadian forest Macrolepidoptera remains to be seen. Insects that feed colonially are generallymore successful when raised en masse than when raised singlyor in smallgroups on theirfood plant, whereas the converse is truefor solitary species (Wellington1957; Iwao 1968; Way and Cammell1970; Shiga 1976;Peters and Barbosa 1977). These observationsare consistentwith the hypothesisof mutual facilitationbetween opportunists and mutualinterference between stealthy herbivores.

Host-Plant Specificityof Stealthyand OpportunisticHerbivores Manyspecies of herbivorousinsects with variable populations such as gypsy moth,fall cankerworm, spruce budworm, fall webworm, locusts, and sometent caterpillarspecies appear to be dietarygeneralists in that they have been recorded attackingmany different plant species (see Prentice1962, 1963; Uvarov 1977; Gerardiand Grimm1979). Watt (1964), however, found that in Canadianforest Macrolepidopterathere is no clear-cutcorrelation between the degree of dietary generalismand variabilityof populationnumbers. If anything,he foundthat, on average,generalist species have slightlymore variable populations than special- ists. Argumentscan be advanced in favorof both dietaryspecialization and generalismin stealthyand opportunisticherbivores. On one hand, fromthe "Jack-of-all-trades-master-of-none"hypothesis we mightexpect specialization to be evolutionarilyfavored in bothgroups since close associationwith few host speciesis likelyto lead to theevolution of more-effectiveoffensive adaptations thanassociation with many hosts. On theother hand, opportunists should also be underselection for broad host range because this would provide them with more opportunitiesto exploit.The advantageto evenlydispersing their damage among plantsshould also selectfor broad host range in stealthyherbivores. Therefore, 218 THE AMERICANNATURALIST althoughthe relationship between dietary specialization and population variability remainsan open question,I suggestthat little correlation will be found.

PHASE CHANGES IN HERBIVORES AND THEIR RELATIONSHIP TO POPULATION STABILITY Strikingchanges in herbivore"quality" are oftenobserved during population fluctuations.In extremecases of thisphenomenon discrete phases or ecotypes characteristicof endemicor epidemicpopulations have been recognized. I suggest thatphase changes in herbivoresmay be due to facultativetransition between the strategiesof stealthand opportunism.

Locusts and Armyworms:A Population Model The mostwidely recognized and distinctexamples of phase polymorphism are found in locusts (Schistocerca gregaria, Locusta migratoria,Nomadacris sep- temfasciata,Locustana pardalina, Chortoicetesterminifera, and other species; Uvarov 1966). At low populationdensities, the solitariaphase occurs. In this phase,each locustlives well separated from other individuals. Nymphs hatching fromegg pods laidby solitaryfemales are crypticallycolored (light gray, fawn, or green;Uvarov 1966). Hatchingis asynchronousand the nymphsscatter upon emergence(Kennedy 1956). The gregariaphase occursat highpopulation density.Adults of thisphase are moreactive than solitaria adults. They aggregate duringfeeding and egg layingto producevast fieldsof egg pods whichhatch synchronously,and theytake flightin cohesivemigratory swarms (Nolte 1974; Uvarov 1966,1977). Adults of thetwo phases differmorphometrically (Uvarov 1966).Gregaria nymphs are muchdarker than solitaria nymphs, because of the presenceof melanin in their cuticle. Together with yellow or orange markings, this darkcoloration makes them more conspicuous than solitaria nymphs. Gregaria nymphsare moreactive thansolitaria nymphs, they grow faster, and have a markedtendency to aggregatewhen feeding and resting(Kennedy 1956; Nolte 1974; Uvarov 1966, 1977). Most investigatorshave reportedhigher metabolic ratesin gregariathan in solitaria(Butler and Innes 1936;Uvarov 1966). Intermediateforms occur both in the field and in the laboratory (Kennedy 1956). In thelaboratory, phase change can be inducedby raising nymphs under crowded or solitaryconditions. The transitionbegins within the first generation, but con- tinuousexposure to the appropriateconditions for two or moregenerations is moreeffective (Kennedy 1956; Uvarov 1966).These changesresult from pheno- typicplasticity, since they occur without the intervention of selection.Transition to the gregariaform and aggregationof locustsare stimulatedby an airborne "gregarizationpheromone" produced in the feces of crowdednymphs (Nolte 1963,1977; Ellis and Gillett1968; Gillett 1968; Gillett and Phillips1977). Nolte (1974, 1977) claimed that he had identifiedthis pheromoneas 2-methoxy-5- ethylphenolin a numberof locust species and that this compound caused changes in chromosomemorphology (increased chiasma frequencies) in thedividing cells of testesof exposed nymphs,but his findingshave been vigorouslychallenged (Dearn 1974a,1974b; Gillett 1983). Gillett and Phillips (1977) found evidence for a solitarizingpheromone produced in thefeces of adults. INTERACTIONSBETWEEN HERBIVORES AND PLANTS 219

Solitariaand gregariadiffer in so manymorphological, physiological, and behavioralways that they were regarded as differentspecies until Uvarov (1921, 1928)proposed his phase theory.The phase theoryexplained the taxonomic puzzle of thesudden appearance and disappearanceof destructivepests, which could notbe foundexcept during periods of highabundance. It did notexplain whypopulations of locustssometimes rise to a densitysufficient to triggerthe appearanceof thedestructive form (Key 1950). Populationexplosions of locustsare of theirregular, eruptive type (Key 1950; Kennedy1956; Uvarov 1977). Outbreaks are initiatedfrom restricted areas within thegeographic range of the solitaria form which itself exhibits a narrowerrange of occurrencethan that invaded by thegregaria form (Tsyplenkov 1978; Kennedy 1956;Uvarov 1977).Typically these outbreak foci are riverdeltas, floodplains, lake margins,and otherareas likelyto experiencewide seasonal and annual variationin soil moisture,and inwhich the effects of local or distantdeviations in rainfallare likelyto be magnified(Symmons 1978; Tsyplenkov 1978). At intervals, whichmay vary between 3 and20 or moreyr, the populations of locusts undergo a dramaticincrease associated with the appearance of thegregaria phase. Migra- torymarching and flightby gregarizednymphs and adultsfrom the outbreak foci lead to progressiveinvasion, by subsequentgenerations, of areas farremoved fromthe point of origin of the outbreak. After a numberof years, which may vary between2 or 3 and 15 or more,the outbreaksubsides, the locustsbecome solitarized,and disperseback to theirrestricted habitat. It is generallyaccepted thatvariations in degreeof parasitismand predationare not responsiblefor populationsurges and collapses(Tsyplenkov 1978; Uvarov 1977). An associationbetween the timingof the initiationof locustoutbreaks and drought,or in somecases excessiveprecipitation, has beenknown for many years (see Tsyplenkov1978; White 1976). Many workers have assumed that this association is caused by directeffects on locust mortalityand natality,but it now appearsthat the influence of weatheron locustpopulations is mainlyindirect by somehowaltering the habitat of the solitary form (Tsyplenkov 1978; White 1976). White(1976), as partof his general hypothesis to explainthe association between insectoutbreaks and unusualweather, has suggestedthat stress of locustfood plants(mainly graminoids and forbs),as a resultof deviantrainfall, leads to increasedfood quality of the plants resulting in an outbreak.In White'sscheme, outbreaksare thusmost likely to be initiatedfrom restricted areas with unpredict- able soil moisturecontents, which most of themare. White(1976) does not addressphase transformation, however, and hishypothesis does notexplain why locustoutbreaks continue long after weather stress has passed,why swarms can invadeand increasein areas of unstressedplants, and whyoutbreaks ultimately collapse. I suggestthe following scheme which combines White's stress hypothesis with conceptsof alternative attack strategies of herbivores and attack-induced changes indefensive posture of plants, developed earlier in this paper. The combinationof morphological,physiological, and behavioralattributes which constitute the solitariaphase are adaptationswhich enable these insects to attacktheir food plants usingthe stealth strategy. This strategy is employedat lowpopulation densities by 220 THE AMERICANNATURALIST locusts,and it is the mode characteristicof nonpestgrasshopper species. Low metabolicrates and a sedentaryhabit permit efficient conversion of plant to insect biomass and minimaldamage to food plantsper unitconverted. Behavioral dispersionminimizes damage to individualfood plants. This maybe combined withadaptations, such as salivarysecretions, to suppressrecognition of attack by thefood plants.Territoriality, exhibited by some grasshopperspecies, is to be expectedin solitaria. Populationsare held in check by rapidplant defensive responsesinduced when the total populations of locusts and otherstealthy herbi- voresrise above a criticallevel. Plant defensive responses exert direct effects on mortalityand natality of solitaria andalso increasetheir susceptibility to parasites and pathogens. Followingany event which leads to a highpopulation density of solitaria they can changeinto the opportunistic gregaria form,and an outbreakwill result, if the localfood plants have not been recently attacked by gregaria. The mostimportant triggeringevent is waterstress to the host plantsin the outbreakfoci which compromisesplant defenses, leading to rapidpopulation build-up and gregarizationof the locusts.Concentration of scatteredsolitaria by convergentairflows maybe anothermechanism whereby outbreaks are initiated(Waloff 1966, 1972). Followingfood depletion in thefoci, the gregarious locusts migrate en masseinto surroundingareas of unstressedfood plants.Given that these unstressed food plantshave notbeen recently attacked by gregaria, thegregarious locusts, acting in concert,can inducefavorable food quality in theplants. This maybe accomplishedby mass attack which overloads rapid response capability in the plants (cf. barkbeetles) and maintains food quality near the constitutive level (alternative A). Alternatively,gregaria mayproduce offensive pheromones in theirsaliva or emit theminto the air whichcause an increasein foodquality above theconstitutive level (alternativeB). This maybe accomplishedby causingthe plants to reduce theconcentration of defensive metabolites in theiraerial parts, or to increasethe levelsof nutrientsin them,or both.The airborneoffensive pheromone and the gregarizationpheromone (discussed above) may be one and the same. High metabolicrate and high levels of locomotory activity lead to inefficientconversion ofplant to insectbiomass and highdamage to thefood plants per unit converted. The opportunisticstrategy is successfulonly on naiveplants. After a shortperiod, perhapsafter a singlemass attack,the plantsbecome resistant.This would accountfor the marchingbehavior of gregariousnymphs (Uvarov 1977)which constantlyexposes themto unattackedplants. With respect to alternativeA (above), acquiredresistance may be manifestas powerfuldelayed defensive responsesin theremaining portions of attackedplants. In alternativeB, whichI favor,resistance may be due to a recognitionprocess involving alteration of the receptivityof the plantsto the offensivepheromones of the locustsfollowing previousattack, such that increased nutritional quality is no longerstimulated by thepheromones. Indeed, following immunization, the offensive pheromone may stimulatedecreased nutritional quality. As plantpopulations become immunized, the swarm migrates into naive plant populations.The swarmincreases in size as a resultof highfecundity, non- INTERACTIONSBETWEEN HERBIVORES AND PLANTS 221

diapausingeggs, and gregarizationof resident solitaria in invadedareas (see Key 1950).This leads to progressiveinvasion of areas remotefrom the original outbreakfoci (see Uvarov1977). The outbreaksubsides when the swarm is unableto locatenaive food-plant populations. At this time solitarization and dispersal to the solitariahabitat occur. After a numberof years (I suggest3 to 4 yr)the plants lose theiracquired resistance and againbecome vulnerable to invasionby gregaria. Thus,there is potentialfor cyclicity in thepopulation dynamics of locusts,with the cycle perioddependent on the timespan of inductionplus relaxationof acquiredresistance. I furthersuggest that the periodicity is rarelymanifest because theaverage time span betweentriggering events is longcompared to the induction-relaxationtime. This scheme has similaritiesto thatproposed by Berry- manand othersfor the initiation and propagationof barkbeetle epidemics (see Berryman1978). At low populationdensities, the beetlespersist in individual trees weakenedby lightningstrike, disease, ice and wind storms,and other factors,but are unableto successfullyattack healthy trees. At highpopulation density,however, the beetles can overcomehealthy trees. So, anyevent which leads to the formationof a largelocal population,such as temporaryweather stressof the trees or damage fromcultural operations, can resultin a self- sustainingoutbreak of beetles that progressively invades areas of healthy trees far removedfrom the site of initiation. The populationecology and phase transformationof armyworms(ground- feedingnoctuid moths) share many striking similarities with those of locusts. The Africanarmyworm Spodoptera exempta is a well-studiedexample. Outbreaks are ofthe eruptive type (Khasimuddin 1981a; Odiyo 1981). African armyworms feed mainlyon grassesand sedges(Odiyo 1981). At low densities the larvae are mainly greenin color, solitary,sluggish, inconspicuous, and have low feedingrates. Duringpopulation outbreaks, the larvae are predominantlyblack in color, gregarious, active,conspicuous, developmentally synchronized, highly voracious, and exhibitmarching behavior (Faure 1943b; Rose 1975;Khasimuddin 1981 a, 1981b; Odiyo 1981).The gregariousphase growsfaster than the solitaryphase (Rose 1975).Transition between forms can occurin one generation.When raised under crowdedconditions gregarious-phase larvae are produced,whereas when raised singly,solitary-phase larvae result (Khasimuddin 1981 a). Dark-colored,active, fast-growingforms of otherspecies of noctuidmoth larvae can be inducedby crowding(Faure 1943a;Matthee 1947; Iwao 1962).Eggs of armyworms are laidin masses(Rose 1975).Adults from gregarious larvae tend to migratereadily, while mothsfrom solitary larvae usually oviposit in the same general area that they were raisedin, to produceendemic populations (Odiyo 1981).During outbreak years, migrationof adultsleads to progressiveshifts in theposition of outbreakepicen- tersat monthlyintervals (the generation time; Odiyo 1981).Rose (1975) found restrictedoutbreaks in two areas 150 kmapart, in bothof whichheavy out-of- season hailstormshad occurred2 to 3 wk beforethe outbreaks were reported. Thissuggests that food-plant stress may be importantin initiating outbreaks of the Africanarmyworm. I suggestthe same generalscheme to explainpopulation outbreaksand phase polymorphismin armywormsas thatsuggested for locusts. 222 THE AMERICANNATURALIST

IncipientPhase Polymorphism

The appearanceof dark-colored forms at highpopulation density in the field or whenraised under crowded conditions in thelaboratory is notunique to locusts (Orthoptera:Acrididae)and armyworms(Lepidoptera:Noctuidae). It has been observedin manyother herbivorous insects in theorders Lepidoptera and Or- thoptera,namely, larch budmoth (Tortricidae; Day and Baltensweiler1972; Bal- tensweileret al. 1977);species of Plusiidae (Long 1953);Saturniidae (Long 1953; Iwao 1968);Notodontidae, Geometridae, Sphingidae (Iwao 1968;Futuyma et al. 1981;Mitter and Futuyma1983); species of Noctuidaenot normally classified as armyworms(Long 1953; Iwao 1968); katydids(Tettigoniidae; Chopard 1949); walkingstickinsects (Phasmidae; Key 1957);and a cricket(Gryllidae; Fuzeau- Braesch 1960, 1968). The dark crowdedlarvae usuallygrow faster, are more active,and havelower mortality than the pale solitaryforms when raised on their food plants.Interestingly, the species displayingthis incipient phase polymor- phismare, whereknown, those whose populationsare proneto eruptto high levels. Usuallythey lay theireggs in clustersand thelarvae have a colonialor semicolonialhabit at leastpart of thetime. The low-densityforms are pale-coloredand relativelyinactive whereas the high-densityforms are dark-coloredand activepossibly because they are stealthy and opportunistic,respectively. The stealthystrategy is to minimizedamage sufferedby theplant per unitof plantbiomass converted to insectbiomass, to avoidinducing defensive responses in the plant. In otherwords, stealthy forms or speciesare ECI (table1) maximizers.This strategy requires low levels of physical activityand low metabolicrate. Low metabolicrate is promotedby low body temperatureso thelow-density forms are pale-coloredpossibly to reduceincident radiationload andenable them to readily maintain a low body temperature. On the otherhand, the strategy of opportunistsis "hitand run." This strategyrequires highlevels of physicalactivity and a highmetabolic rate. Opportunistsmay attemptto maximizethe rate of conversionof plantmaterial to insectbiomass (RCI) ratherthan the efficiency of conversion(see Smith1976). Higher rates of conversionare promotedby higherbody temperatures so thehigh-density forms are dark-coloredpossibly to increaseabsorption of solar radiationand help maintainhigh body temperature (table 1). To date, the nutritionalecology of herbivoresand theirvarious nutritional indicessuch as growthrates, efficiencies of conversion,and food digestibility have beenexamined largely in termsof the degree of food-plant specialization of theherbivores (monophagous, oligophagous, polyphagous) and thegrowth form (herb,shrub, tree) of theirfood plants(Scriber and Feeny 1979; Scriberand Slansky1981; Scriber 1983). The presentanalysis suggests that the attack strategies of herbivoresmay also be important,perhaps of overridingimportance, in determiningthese parameters. In general,we shouldexpect innocuous species, withlow, relativelyinvariant population levels, to exhibithigh ECI, fooddigest- ibility(AD), and low feedingrates (CL), and RCI. On theother hand, species with variablepopulations (pest species)should exhibit low ECI, AD, and variableCI and RCI (see table 1). INTERACTIONSBETWEEN HERBIVORES AND PLANTS 223

Otherstriking changes in herbivore"quality" besides color changes have been observedbetween high- and low-densitypopulations, and duringpopulation increases and declines,for insects, voles, and grouse(see Haukiojaand Hakala 1975;Rhoades 1983a). Usually,the forms predominant in increasingpopulations are morefecund, more active, and havelower mortality than those characteristic ofdeclining populations. These changescan be interpretedas merelythe result of changingfood quality during increase and declinebut a componentof incipient phase polymorphismis probable. In cases oflocusts, armyworms, and otherinsects previously discussed, where transitionbetween light and darkmorphs can be inducedin one or a fewgenera- tionsby crowding,it is clear thatthe changes are theresult of plasticityrather thandifferential survival of light or darkgenotypes. The sameis probablygener- allytrue of phase change and other changes in herbivore quality during population fluctuations. Douglas-Fir Tussock Moth, GypsyMoth, and Other NonmigratoryPest Species: A Population Model The associationbetween herbivore population variability and migratoryability has been emphasizedin thispaper. However, the females of some tree-feeding speciesof insectswith variable population levels have reducedwings or, even if theypossess developedwings, they rarely fly. This is trueof Douglas-fir tussock moth(Brookes et al. 1978);gypsy moth (Gerardi and Grimm1979); many other speciesof Lymantriidae (Browne 1968); and fallcankerworm (Geometridae; Mit- terand Futuyma1983). Similar to mostinsects with variable populations, these insectsdeposit their eggs in masses.The flightlesshabit possibly arose as partof an alternatingstealthy-opportunistic attack strategy as in thefollowing scheme. At low density,the insects are stealthy.Upon hatchingfrom the egg mass, the larvaeimmediately disperse by crawlingor silkballooning to lead a solitarylife utilizingadaptations to suppressrecognition and minimizeplant damage as previouslydiscussed. There comes a pointwhen the plantshave lost theiracquired immunityto theopportunistic form, upon which the insects switch to thatstrat- egy. Insteadof dispersing,the opportunistic larvae maintain loose aggregations and utilizeadaptations to increasethe nutritional quality of thefood plants. An outbreakerupts, the plants become resistant, and theoutbreak subsides. Surviv- ing insectsrevert to the stealthyform, reestablishing an endemicpopulation. Inductionof the opportunistic form and rapid population build-up may be aidedby physicalstress of the food plants(see V. I. Benkevitch[1961-1964], M. G. Khanislamovet al. [1962]as summarizedin Campbellet al. [1978],Bess [1947], Spurret al. [1947],Campbell and Sloan [1977]for evidence of association between outbreaksof gypsymoth with weather and otherstresses of host trees; see Brookeset al. [1978]for similar effects on Douglas-firtussock moth). This scheme predictsa fundamentalcyclicity in thepopulation dynamics of the insects, which is determinedby the inductionand relaxationtimes of acquiredimmunity, but whichis modulatedin amplitudeand exacttiming by physicalstress of thehost plants.The populationdynamics of Douglas-firtussock moth match this pattern remarkablywell. In thewestern United States, outbreaks of tussockmoth have 224 THE AMERICANNATURALIST occurredon averageevery 8 to 9 yr(Mason and Luck 1978).Stage (1978) found thatthe timingof outbreakscan be predictedif it is assumedthat there is a minimumwaiting time of 7 yrfrom the date of the previous outbreak, to whichis addeda shortrandom time period in whicha criticalevent occurs, with an annual probabilityof 0.3. The waitingtime is probablyinduction plus relaxationof acquiredhost resistance and thecritical event is probablyphysical stress of the trees. A tendencyfor femaleSightlessness to evolve in insectswith sessile stealthyand opportunisticphases would be expectedsince this allows increased allocationof resourcesto eggproduction. This tendencywould be reinforcedin species whichattack trees, since largefood-plant size would allow effective within-plantdispersion of stealthy-phase larvae, and long food-plant life span may allowadaptation over many generations of the insects to theproperties of individual treesif females oviposit on the same treeson whichthey fed as larvae(see Alstadand Edmunds1983). Thereare twomain differences between the proposed tussock moth scheme and thatpreviously outlined for locusts and armyworms.First, in thetussock moth case, epidemicserupt from and collapse to endemicpopulations, rather than proceedingunder the influence of migration.Second, in thetussock moth case, theaverage time span betweenevents stressful to thefood plants is shortcom- paredto plantdefensive induction-relaxation time, whereas in thecase oflocusts and armywormsthe opposite was proposed.Thus, for tussock moth the funda- mentalperiodicity of the cycle is revealed,whereas for locusts and armywormsit is normallymasked. The interactionbetween the timing of events stressful to food plantsand the timespan of inductionplus relaxationof acquiredresistance to herbivoreattack may explain other cases oferuptive and cyclic herbivore popula- tionbehavior (see Rhoades 1983a,fig. 3, and discussion).It is interestingto note thatmajor outbreaks of tussock moth have been recorded mainly at interiorsites withextreme continental climates in thewestern United States (Beckwith 1978), wherehost stress would be expectedto be moreintense and more frequent than in coastal regionswith mesic maritimeclimates. Major outbreakshave not been reportedin coastal areas, althoughlow-density endemic populations of tussock mothare present.An alternativeexplanation for the geographical distribution of Douglas-firtussock moth outbreaks is thatthere are geneticdifferences in defensive responsesbetween plants in thetwo regions.Based partlyon thework of Haukioja and coworkers(Haukioja 1980),I suggestedthat the propensityof herbivoreoutbreaks to occur in regionsof harshclimate (high latitude and al- titude)was due to recentclimatic warming which enabled herbivores to invadethe coolerregions of theirrange. Because theyhad been partlyprotected from the herbivoresby theirphysical location, the plants in thecooler regions were sug- gestedto have evolvedweak rapid-defensiveresponses but strongdelayed responses,and thispromoted herbivore population instability (see Rhoades1983a, pp. 191-193).

Parthenogenesisand Population Stability J. C. Schultz(personal communication) has suggestedthat parthenogenesis maybe particularlycommon in herbivorousinsect species with variable popula- INTERACTIONS BETWEEN HERBIVORES AND PLANTS 225 tionlevels. Among such species, parthenogenesis occurs frequently infall cankerworm(Mitter et al. 1979; Mitterand Futuyma1983), pest species of sawflies (Koehler1956; Wagner and Benjamin1981), and aphids(Way 1973),and occa- sionally in gypsy moth (Gerardi and Grimm 1979) and locusts (Kennedy 1956; Uvarov1966). Facultative or obligateparthenogenesis also occursin manyother herbivorousspecies of Orthoptera,Homoptera, Coeloptera, Lepidoptera, and Diptera(Cockayne 1938; White 1973; Went 1982). It is conceivablethat thelytok- ous (female-producing)parthenogenesis may be morecommon among opportunistic species or phases thanamong stealthy herbivores since by dispensingwith males,opportunists could achievea morerapid population build-up than with a sexuallyreproducing population (table 1). Facultativethelytokous parthenogenesis, combinedwith facultative winglessness, would be an ideal combinationof adaptationsfor opportunists. These are preciselythe characteristics,together withaggregation during population build-up, shown by manypest aphid species (Bonnemaison1968; Dixon 1973;Way 1973).

CONCLUDING REMARKS The conceptof alternative herbivore attack strategies, developed here, explains variabilityand invariancein herbivorepopulation levels. It also explainsphase polymorphismin herbivoresand suggeststhat qualitative changes observed in manyherbivore species during population fluctuations are incipientphase transi- tions.Developed to accountfor the properties of smallherbivore species, these ideas may also be applicableto largeherbivores. For instance,sloths may be slothful,howler monkeys may howl, and koalas may be sedentary(see Montgom- ery 1978),because theyare stealthy. It can be shownby simplearithmetic that for two species of organisms with the samemean reproductive rate, when arithmetically averaged over several generations,but with different variances in reproductive rate from one generationto the next,the species withlower variance will leave moreprogeny in thelong term (Gillespie1974; Root and Kareiva 1983).In an invariantenvironment we would thereforeexpect the evolution of invariantreproductive rates across generations forall species.The continuingexistence of herbivore species with highly variable populationlevels and reproductiverates occurs in spiteof thisleveling process, and is probablymaintained by variations in theenvironment which create oppor- tunitiesfor opportunists to exploit. Herbivorepopulation dynamics are probablybetter understood in termsof varyingquality and quantityof bothplants and herbivores(see Haukioja and Hakala 1975;Denno and McClure 1983) than in terms of only quantitative changes in amountof vegetationand numbersof herbivores.In naturalsystems, herbi- voresrarely reach outbreak levels. They usually consume only a smallfraction of thenet primary production (Hairston et al. 1960;Mattson and Addy 1975; Fox and Morrow1983). Even in grasslands,which tend to be heavilyutilized compared to mostplant communities, consumption usually ranges only from 25% to 50% (Dyer et al. 1982).Thus, in termsof foodquantity, herbivores must seldom compete witheach other.In addition,aggregation with conspecifics during feeding clearly benefitsmany herbivores. (Besides cases previouslydiscussed see Teale 1949; 226 THE AMERICANNATURALIST

Long 1955; Kalkowski1958; Ghent 1960; Iwao 1968;Way and Cammell1970; Shiga1976; Hikada 1977;Kalin and Knerer1977; Peters and Barbosa 1977; Weyh and Maschwitz1978; Fitzgeraldand Edgerley1979; Capinera1980; Haukioja 1980;Tsubaki 1981; and references therein.) Positive interactions in termsof food choice and reproductivesuccess are also commonbetween herbivore species. They occur betweenbark beetle species (Wood and Bedard 1977;Birch et al. 1980;Borden 1982); between boring beetles and defoliators(Staley 1965; Nichols 1968;Dunbar and Stephens1976; Schultz and Allen1977; Berryman and Wright 1978); betweeninsects inhabiting Heliconia bracts(Seifert and Seifert1976); betweena folivorousgrasshopper and a stem-girdlingbeetle (Lewis 1979);be- tweenstem-girdling beetles and otherinsects (Mares et al. 1977);among ungulate species(Bell 1971;McNaughton 1976); between prairie dogs and bison(Coppock et al. 1983);and possiblybetween snail species (Hershey 1983). Therefore, that simplecompetition theory based largelyon changesin amountof resourceshas provedof little value in explaining co-occurrence and other patterns of herbivores (Hairstonet al. 1960;Lawton and Strong1981; Strong 1983) is notsurprising. On the otherhand, the evidencethat herbivore attack can lead to decreased plantnutritional quality, caused by plantdefensive response, is substantialand growingrapidly. These changes in quality can be inducedby low levels of damage (see Rhoades1983b). There is also evidencethat individual herbivores and aggregationsof herbivores can activelyinduce favorable changes in food-plant quality. These changesin food quality can be expectedto affectboth the inducing species and otherherbivore species. Therefore,although negative interactions between herbivoresmediated through decreased food quantityare probablyrare, both negativeand positiveinteractions mediated through changes in foodquality are probablycommon. I thereforesuggest that the conceptof competitionamong herbivoresis oflimited value because, by definition, itencompasses only negative interactions.Interactions among herbivores are morecomprehensively described in termsof the dual, complementaryconcepts of interferenceand facilitation. Withinspecies of stealthyherbivores and amongstealthy species that feed on the sametissue, interactions are mediatedthrough interference, whereas the interac- tionswithin and amongspecies of opportunistic herbivores are mediatedthrough facilitationduring population increase, and delayed interference during population decrease.Stealthy herbivores should have little effect on thepopulation dynamics of opportunists.On theother hand, opportunists can be expectedto facilitateor interferewith population growth of stealthyherbivores that feed on the same tissue,during population increase or decreaseof theopportunists, respectively. Interactionsamong opportunists that feed on differenttissues and effectsof opportunistson stealthyherbivores that feed on differenttissues should depend on the degreeto whichreallocation of defensivemetabolites occurs between attackedand nonattackedtissues. Thereis a clearanalogy between the opportunism-stealth dichotomy of attack strategiesand ther-K continuum of lifehistory strategies developed by MacAr- thurand Wilson (1967). In manyways, opportunism and stealth can be considered to be specialcases ofr- and K-selected life histories, respectively (cf. table 1 with Pianka1970, table 1; see also Southwood1976). The maindifference is thatin the INTERACTIONS BETWEEN HERBIVORES AND PLANTS 227 presentscheme individual stealthy and opportunisticherbivores both strongly interactwith other herbivores, in thefirst case byinterference, and in thesecond case by facilitationand interference.In r-Ktheory, individual K-strategists compete (interfere)strongly with other organisms at the same trophiclevel, but r- strategistsinteract with them minimally. In the same way thatchanges in plantquality are provingto be importantin herbivore-plantinteractions, changes in prey behavior(quality) may also be importantin predator-prey interactions in general. Symmetrical and asymmetrical facilitationare commonamong predators, for example, wolf packs, mixed-species foragingflocks of birds,and armyant-bird associations. According to Potts (1981),primary outbreaks of crown-of-thorns starfish preying on coralpolyps are probablycaused by aggregationsof adultsfrom normal low-density populations, or enhancedlarval recruitment,following abnormal storms and otherdistur- bances.Antonelli and Kazarinoff(1983) have found that the population dynamics of thestarfish can be successfullymodeled if they include a quadratic"coopera- tive"term in the predator equation. This underlines the importance of aggregation and suggestsmutual facilitation within aggregations of the starfish.By analogy withplant-herbivore systems, I suggestthat the population dynamics of crown-of- thornsstarfish can be understoodin termsof transitionby thestarfish between stealthyand opportunisticattack strategies, in responseto stressof coralpolyps whichlowers their defensive capacity. I furthersuggest that induced defensive responsesof coral will prove important in the population dynamics of the starfish. Facilitationbetween producer species may also be common(e.g., see Connell andSlatyer 1977). In myview, the present controversy concerning the importance ofcompetition in structuringcommunities (see Lewin1983a, 1983b; Salt 1984)is a directresult of the narrowfocus of competitiontheory on negativeinfluences amongorganisms resulting from mutually induced decrease in resourcequantity. If communitystructure is determinedby a combinationof interference,facilitation,changes in resource quantity and quality,and alternative strategies of organ- ismsat each trophiclevel, the observation that communities do notconform to the patternspredicted by competitiontheory is to be expected.This viewpoint is far differentfrom that expressed by some participantsin the currentcompetition controversy(see Lewin 1983a,1983b), who would have us believethat ecological generalizationsare oflittle value, and thatcommunities are structuredlargely by randomfactors.

SUMMARY A considerationof known defensive attributes of plants, and othersthat can be reasonablypostulated, leads to thedescription of two alternative offensive strategies of herbivores,termed stealth and opportunism,to counterplant defenses. Stealthyherbivores display adaptations to minimizedamage and defensivere- sponsesof theirfood plants. On theother hand, opportunists take advantage of circumstances,such as physicalstress and loss of acquiredresistance of food plants,that impair plant defensive capability. In addition,opportunists them- selvesdisplay adaptations, such as mass-attackbehavior, that stress food plants. 228 THE AMERICANNATURALIST

Herbivorespecies withlow, relativelyinvariant population levels may be stealthy,whereas those with variable population levels may be opportunistic.Phase changesin herbivores may be theresult of transition between the two strategies. It is suggestedthat interactions within and amongspecies of herbivoresare better understoodin termsof interference and facilitationthan in termsof competition.

ACKNOWLEDGMENTS I thankNancy E. Beckage,Alan A. Berryman,Mel I. Dyer,Peter W. Miles, andunidentified reviewers for many valuable suggestions and LynnErckmann for theillustrations. This work was supportedby National Science Foundation grant BSR-8307581to G. H. Oriansand D. F. Rhoadesand by WhitehallFoundation grant83548 to D. F. Rhoades.

LITERATURE CITED Abeles,F. B. 1973.Ethylene in plantbiology. Academic Press, New York. Allison,M. J., and H. M. Cook. 1981. Oxalate degradationby microbesof the largebowel of herbivores:the effect of dietary oxalate. Science 212:675-676. Alstad,D. N., and G. F. Edmunds,Jr. 1983. Adaptation, host specificity, and gene flow in theblack pineleafscale. Pages413-426 in R. F. Dennoand M. S. McClure,eds. Variableplants and herbivoresin naturaland managedsystems. Academic Press, New York. Antonelli,P. L., andN. D. Kazarinoff.1983. Starfish predation of a growingcoral reef community. J. Theor.Biol. 107:667-684. Baker,R. R. 1983.Insect territoriality. Annu. Rev. Entomol.28:65-89. Baldwin,I. T., and J. C. Schultz.1983. Rapid changes in treeleaf chemistry induced by damage: evidencefor communication between plants. Science 221:277-279. Baltensweiler,W. 1968.The cyclicpopulation dynamics of the grey larch tortrix, Zeraphera griseana Huber(=Semasia dinianaGuenee) (Lepidoptera:Tartricidae). Pages 88-97 in T. R. E. Southwood,ed. Insectabundance. Blackwell, Oxford. Baltensweiler,W., G. Benz, P. Bovey,and V. Delucchi.1977. Dynamics of larch bud moth populations.Annu. Rev. Entomol.22:79-100. Baltensweiler,W., and A. Fischlin.1979. The roleof migrationfor the population dynamics of the larchbud moth,Zeiraphera diniana GN. (Lep. Tortricidae).Mitt. Schweiz. Entomol. Ges. 52:259-271. Beckwith,R. C. 1978.Geographic range. Page 25 inM. H. Brookes,R. W. Stark,and R. W. Campbell, eds. The Douglas-firtussock moth: a synthesis.US Dep. Agric.For. Serv. Sci. Education AgencyTech. Bull. 1585. Bell, R. H. V. 1971.A grazingsystem in theSerengeti. Sci. Am. 225(1):86-93. Benz, G. 1974.Negative Ruckkoppelung durch Raum- und Nahrungs-Konkurrenzsowie zyklische Veranderungder Nahrungsgrundlage als Regelprinzip in derPopulationsdynamik des gruen Larchenwicklers,Zeiraphera diniana (Guenee) (Lep. Tortricidae).Z. Angew.Entomol. 76:196-228. 1977.Eucarpia/IOBC working group breeding for resistance to insectsand mites. Bull. SROP, 1977/3.(Report 1st meeting held at Wageningen,The Netherlands,7 to 9 Dec. 1976,pages 155-159). Berenbaum,M. 1980.Adaptive significance of midgutpH in larvalLepidoptera. Am. Nat. 115:138- 146. 1981.Effects of linearfuranocoumarins on an adaptedspecialist insect (Papilio polyxenes). Ecol. Entomol.6:345-351. Bernays,E. A. 1981.Plant tannins and insectherbivores: an appraisal.Ecol. Entomol.6:353-360. INTERACTIONS BETWEEN HERBIVORES AND PLANTS 229

Bernays,E. A., andS. Woodhead.1982. Plant phenols utilized as nutrientsby a phytophagousinsect. Science216:201-202. Berryman,A. A. 1969. Responsesof Abies grandisto attackby Scolytusventralis (Coleoptera: Scolytidae).Can. Entomol.101:1033-1041. 1972. Resistanceof conifersto invasionby barkbeetle-fungus associations. BioScience 22:598-602. 1978.A synopticmodel of the lodgepole pine/mountain pine beetle interaction and its potential applicationin forestmanagement. Pages 98-105in D. L. Kibbee,A. A. Berryman,G. D. Amman,and R. W. Stark,eds. Theoryand practice of mountain pine beetle management in lodgepolepine forests. Forest, Wildlife and Range Experiment Station, University of Idaho, Moscow,Idaho. 1979.Dynamics of bark beetle populations: analysis of dispersal and redistribution. Bull. Soc. Entomol.Suisse 52:227-234. Berryman,A. A., and W. Baltensweiler.1981. Population dynamics of forest insects and the manage- mentof future forests. Proc. IUFRD WorldCongr. 17:423-430. Berryman,A. A., andL. C. Wright.1978. Defoliation, tree condition and bark beetles. Pages 81-87 in M. H. Brookes,R. W. Stark,and R. W. Campbell,eds. The Douglas-firtussock moth: a synthesis.US Dep. Agric.For. Serv. Sci. EducationAgency Tech. Bull. 1585. Bess, H. A. 1947.Relation of forest and siteto gypsymoth abundance. Harv. For. Bull. 22:7-26. Birch,M. C., P. Svihra,T. D. Paine,and J. C. Miller.1980. Influence of chemically mediated behavior on host treecolonization by fourcohabiting species of barkbeetles. J. Chem. Ecol. 6:395-414. Bonnemaison,L. 1968. L'effetde groupechez les aphides.Colloq. Int. Cent. Natl. Rech. Sci. 173:213-236. Borden,J. H. 1982.Aggregation pheromones. Pages 74-139 in J.B. Mittonand K. B. Sturgeon,eds. Barkbeetles of NorthAmerican conifers. University of Texas Press,Austin. Brattsten,L. B. 1979.Biochemical defense mechanisms in herbivoresagainst plant allelochemicals. Pages200-270 in G. A. Rosenthaland D. H. Janzen,eds. Herbivores:their interaction with secondaryplant metabolites. Academic Press, New York. Brookes,M. H., R. W. Stark,and R. W. Campbell.1978. The Douglas-firtussock moth: a synthesis. US Dep. Agric.For. Serv. Sci. EducationAgency Tech. Bull. 1585. Browne,F. G. 1968.Pests and diseasesof forest plantation trees. Clarendon, Oxford. Bryant,J. P. 1981.Phytochemical deterrence of snowshoehare browsing by adventitiousshoots of fourAlaskan trees. Science 213:889-890. Butler,C. G., andJ. M. Innes.1936. A comparisonof the rate of metabolic activity in the solitary and migratoryphases of Locusta migratoria. Proc. R. Soc. Lond. B. 119:296-304. Campbell,R. W., L. C. Levitan,E. Sobecki,and M. F. Tardiff.1978. Population dynamics of the gypsymoth: an annotatedbibliography. US Dep. Agric.For. Serv. Gen. Tech. Rep. NE- 48:1-124. Campbell,R. W., and R. J. Sloan. 1977.Release of gypsy moth populations from innocuous levels. Environ.Entomol. 6:323-330. Capinera,J. L. 1980.A trailpheromone from the silkproduced by larvaeof therange caterpillar Hemileucaolivae (Lepidoptera: Saturniidae) and observationson aggregationbehavior. J. Chem. Ecol. 6:655-664. Capinera,J. L., and W. J. Roltsch.1980. Responseof wheatseedlings to actualand simulated migratorygrasshopper defoliation. J. Econ. Entomol.73:258-261. Carroll,C. R., and C. A. Hoffman.1980. Chemical feeding deterrent mobilized in responseto insect herbivoryand counteradaptation by Epilachna tredecimnota. Science 209:414-416. Carter,W. 1973.Insects in relationto plantdisease. Wiley, New York. Cates,R. G. 1975.The interfacebetween slugs and wildginger: some evolutionary aspects. Ecology 56:391-400. Cates, R. G., and H. Alexander.1982. Host resistanceand susceptibility.Pages 212-263in J. B. Mittonand K. B. Sturgeon,eds. Bark beetlesin NorthAmerican conifers. University of Texas Press,Austin. 230 THE AMERICAN NATURALIST

Cherrett,J. M. 1972.Chemical aspects of plantattack by leaf-cuttingants. Pages 13-24 in J. B. Harborne,ed. Phytochemicalecology. Academic Press, New York. Chopard,L. 1949.L'6tat actuel de la questiondes phaseschez les insects.Annee Biol. 25:105-109. Clark,W. C., D. P. Jones,and C. S. Holling.1978. Patches, movements, and population dynamics in ecologicalsystems. Pages 385-432in J. H. Steele,ed. Spatialpatterns in planktoncom- munities.Plenum, New York. Cockayne,E. A. 1938.The geneticsof sex in Lepidoptera.Biol. Rev. 13:107-132. Cold SpringHarbor Symposia on QuantitativeBiology. 1957. Population studies: animal ecology and demography.Long Island Biological Association. Cold Spring Harbor Symp. Quant. Biol. 22. Connell,J. H., and R. D. Slatyer.1977. Mechanisms of successionin naturalcommunities and their rolein communitystability and organization.Am. Nat. 111:1119-1144. Coppock,D. L., J. E. Ellis,J. K. Detling,and M. I. Dyer. 1983.Plant-herbivore interactions in a NorthAmerican mixed-grass prairie. II. Responsesof bison to modificationofvegetation by prairie-dogs.Oecologia 56:10-15. Cornell,H. V. 1983a. The secondarychemistry and complexmorphology of galls formedby the Cynipinae(Hymenoptera): why and how.Am. Midl.Nat. 110:225-234. 1983b.Why and howgall wasps form galls: cynipids as geneticengineers? Bull. R. Entomol. Soc. Lond. 9:53-58. Coster,J. E., andP. C. Johnson.1979. Dispersion patterns of Dendroctonusfrontalis and itspredator Thanasimusdubius: influenceof behavioralchemicals. Mitt. Schweiz. Entomol.Ges. 52:309-322. Coutts,M. P. 1968.Rapid physiological change in Pinus radiata following attack by Sirex noctilio and itsassociated fungus, Amylostrereum sp. Aust.J. Sci. 30:275-277. 1969a.The mechanismof pathogenicityof Sirexnoctilio on Pinusradiata I. Effectsof the symbioticfungus Amylostrereum sp. (Thelephoraceae).Aust. J. Biol. Sci. 22:915-924. 1969b.The mechanismof pathogenicityof Sirexnoctilio on Pinusradiata II. Effectsof S. noctiliomucus. Aust. J. Biol. Sci. 22:1153-1161. Day, K. R., and W. Baltensweiler.1972. Change in proportionof larval colourtypes of the larchform Zeirapheradiniana when reared on twomedia. Entomol. Exp. Appl. 15:287-298. Dearn,J. M. 1974a.Phase transformation and chiasma frequency variation in locustsI. Schistocerca gregaria.Chromosoma 45:321-338. 1974b.Phase transformationand chiasmafrequency variation in locustsII. Locustamigra- toria.Chromosoma 45:339-352. Denno,R. F., and M. S. McClure,eds. 1983.Variable plants and herbivores in naturaland managed systems.Academic Press, New York. Detling,J. K., and M. I. Dyer. 1981.Evidence for potential growth regulators in grasshoppers. Ecology62:485-488. Detling,J. K., C. W. Ross, M. H. Walmsley,D. W. Hilbert,C. A. Bonilla,and M. I. Dyer. 1981. Examinationof North American bison saliva for potential plant growth regulations. J. Chem. Ecol. 7:239-246. Dieleman,F. L. 1969. Effectsof gall midgeinfestation on plantgrowth and growthregulating substances.Entomol. Exp. Appl. 12:745-749. Dixon,A. F. G. 1973.Biology of aphids. Edward Arnold, London. Dowd, P. F., C. M. Smith,and T. C. Sparks.1983. Detoxification of planttoxins by insects.Insect Biochem.13:453-468. Dropkin,V. H. 1979.How nematodesinduce disease. Pages 219-238in J. G. Horsfalland E. B. Cowling,eds. Plantdisease. Vol. 4. AcademicPress, New York. Dunbar,D. M., andG. R. Stephens.1976. The bionomics of the twolined chestnut borer. Pages 73-83 inJ. F. Andersonand H. K. Kaya,eds. Perspectivesin forest entomology. Academic Press, New York. Dyer,M. I. 1980.Mammalian epidermal growth factor promotes plant growth. Proc. Natl. Acad. Sci. USA 77(8):4836-4837. Dyer,M. I., and V. G. Bokhari.1976. Plant-animal interactions: studies of the effects of grasshopper grazingon bluegrama grass. Ecology 57:762-772. Dyer,M. I., J. K. Detling,D. C. Coleman,and D. W. Hilbert.1982. The role of herbivoresin INTERACTIONS BETWEEN HERBIVORES AND PLANTS 231

grasslands.Pages 255-295in J. R. Estes,R. J. Tyrl,and J. N. Brunken,eds. Grassesand grasslands.University of OklahomaPress, Norman. Ehrlich,P. R., and P. H. Raven. 1965.Butterflies and plants:a studyin coevolution.Evolution 18:586-608. Ellis, P. E., and S. Gillett.1968. Social aggregationand an airbornegregarising factor in locusts. Colloq. Int.Cent. Natl. Rech. Sci. 173:173-183. Engelbrecht,L. 1971.Cytokinin activity in larval infected leaves. Biochem. Physiol. Pflanz. 162:8-27. Engelbrecht,L., V. Orban,and W. Heese. 1969.Leaf-miner caterpillars and cytokininsin thegreen islandsof autumn leaves. Nature223:319-321. Faure,J. C. 1943a.The phasechanges of the lesser armyworm (Laphygma exigua (Hubn.)). Farming S. Afr.18:69-78. 1943b.Phase variation in the armyworm Laphygma exempta (Walk.). Sci. Bull.Dep. Agric.S. Afr.234. Feeny,P. P. 1970.Seasonal changes in oak leaftannins and nutrientsas a cause ofspring feeding by wintermoth caterpillars. Ecology 51:565-581. 1975.Biochemical coevolution between plants and their insect herbivores. Pages 3-19 inL. E. Gilbertand P. H. Raven,eds. Coevolutionof animals and plants. University of Texas Press, Austin. 1976.Plant apparency and chemicaldefense. Rec. Adv. Phytochem.10: 1-40. Finerty,J. P. 1980.The populationecology of cycles in smallmammals. Yale UniversityPress, New Haven,Conn. Fitzgerald,T. D., and J. S. Edgerly.1979. Specificity of trailmarkers of forestand easterntent caterpillars.J. Chem.Ecol. 5:564-574. Fox, L. R., andP. A. Morrow.1983. Estimates of damage by herbivorous insects on eucalyptustrees. Aust.J. Ecol. 8:139-147. Fraenkel,G. S. 1959.The raisond'ftre of secondaryplant substances. Science 129:1466-1470. Freeland,W. J. 1980.Insect flight times and atmospherichydrocarbons. Am. Nat. 116:736-742. Freeland,W. J., and D. H. Janzen.1974. Strategies in herbivoryby mammals:the role of plant secondarycompounds. Am. Nat. 108:269-289. Futuyma,D. J.,S. L. Leipertz,and C. Mitter.1981. Selective factors affecting clonal variation in fall cankerworm,Alsophila pometaria (Lepidoptera:Geometridae). Heredity 47:161-172. Fuzeau-Braesch,S. 1960.Etude biologiqueet biochimiquede la pigmentationchez un insecte= Gryllusbimaculatus de Geer(Orthopteres, Gryllidae). Bull. Biol. Fr. Belg.94:527-629. 1968.L'effet de groupechez le grillon:niveaux et relativity de ses manifestations.Colloq. Int. Cent.Natl. Rech. Sci. 173:115-125. Fye,R. E. 1974.Populations defined and approaches to measuringpopulations, density, dispersal and dispersion.Pages 46-61 in F. G. Maxwelland F. A. Harris,eds. Proc.of the summer institute on biologicalcontrol of plant insects and diseases. University of Mississippi Press, Jackson. Gerardi,M. H., andJ. K. Grimm.1979. The history,biology, damage and controlof the gypsy moth Porthetriadispar (L.). AssociatedUniversity Presses, London. Ghent,A. W. 1960. A studyof the group-feedingbehaviour of larvaeof thejack pine sawfly, Neodiprionpratti banksianae Roh. Behaviour 16:110-148. Gibson,R. W., and J. A. Pickett.1983. Wild potatorepels aphids by release of aphid alarm pheromone.Nature 302:608-609. Gillespie,J. H. 1974.Natural selection for within-generation variance in offspringnumber. Genetics 76:601-608. Gillett,S. D. 1968.Airborne factors affecting the grouping behaviour of locusts. Nature 218:782-783. . 1983.Primer pheromones in thedesert locust. Anim. Behav. 31:221-230. Gillett,S. D., andM. L. Phillips.1977. Faeces as a sourceof a locustgregarisation stimulus. Effects on social aggregationand on cuticularcolour of nymphsof the desertlocust, Schistocerca gregaria(Forsk.). Acrida 6:279-286. Goodman,R. N. 1980.Defenses triggered by previousinvaders: bacteria. Pages 305-317in J. G. Horsfalland E. B. Cowling,eds. Plantdisease. Vol. 5. AcademicPress, New York. Hairston,N. G., F. E. Smith,and L. B. Slobodkin.1960. Community structure, population control and competition.Am. Nat. 94:421-425. 232 THE AMERICAN NATURALIST

Hamilton,R. I. 1980.Defenses triggered by previous invaders: viruses. Pages 279-303 in J. G. Horsfall and E. B. Cowling,eds. Plantdisease. Vol. 5. AcademicPress, New York. Hanover,J. W. 1972.Factors affecting the release of volatile chemicals by forest trees. Mitt. Forstl. Bundes-Versuchsanst.Wien 97:625-645. Harborne,J. B. 1978.Biochemical aspects of plantand animalcoevolution. Academic Press, New York. Haukioja,E. 1980.On therole of plantdefenses in thefluctuation of herbivorepopulations. Oikos 35:202-213. Haukioja,E., andT. Hakala. 1975.Herbivore cycles and periodic outbreaks. Formulation of a general hypothesis.Rep. Kevo SubarcticRes. Stat. 12:1-9. Hershey,A. E. 1983.Competition among two co-existing snails: a laboratoryexperimental analysis. Bull. Ecol. Soc. Am. 64:89. Higgins,K. M., J.E. Browns,and B. A. Haws. 1977.The black grass bug (Lapbops hesperius Uhler): itseffect on severalnative and introducedgrasses. J. RangeManage. 30:380-384. Hikada,T., ed. 1977.Adaptation and speciationin thefall webworm. Kodansha, Tokyo. Hladik,C. M. 1978.Adaptive strategies of primates in relationto leaf-eating.Pages 373-395 in G. G. Montgomery,ed. The ecologyof arborealfolivores. Smithsonian Institution, Washington, D.C. Hodson,A. C. 1941.An ecologicalstudy of the forest tent caterpillar, Malacosoma disstria Hbn. in northernMinnesota. Univ. Minn. Agric. Exp. Stn.Minn. Tech. Bull. 148:1-55. Hori,K. 1976.Plant growth-regulating factor in thesalivary glands of severalheteropterous insects. Comp.Biochem. Physiol. 53B:435-438. Hori,K., andM. Endo. 1977.Metabolism of ingested auxins in the bug Lygus disponsi: conversion of indole-3-aceticacid and gibberellin.J. InsectPhysiol. 23:1075-1080. Horsfall,J. G., and E. B. Cowling.1980. Plant disease. Vol. 5. AcademicPress, New York. Iwao, S. 1962.Studies on thephase variation and relatedphenomena in somelepidopterous insects. Mem.Coll. Agric.Kyoto Univ. 84. 1968.Some effectsof grouping in lepidopterousinsects. Colloq. Int.Cent. Natl. Rech. Sci. 173:185-212. Jaenike,J., D. A. Grimaldi,A. E. Sluder,and A. L. Greenleaf.1983. cx-amanitintolerance in mycophagousDrosophila. Science 221:165-166. Jones,D. A. 1972.Cyanogenic glycosides and theirfunction. Pages 103-124in J. B. Harborne,ed. Phytochemicalecology. Academic Press, New York. Kahn,D. M., and H. V. Cornell.1983. Early leaf abscission and folivores: comments and considerations.Am. Nat. 122:428-432. Kalin,M., and G. Knerer.1977. Group and masseffects in diprionidsawflies. Nature 267:427-429. Kalkowski,W. 1958. Investigationson territorialorientation during ontogenetic development in Hyponomeutaevonymellus L., Lepidoptera,Yponmeutidae, Part II. Folia Biol. Krakow 6:245-263. Karban,R. 1983. Inducedresponses of cherrytrees to periodicalcicada oviposition.Oecologia 59:226-231. Keith,L. B. 1963.Wildlife's ten-year cycle. University of Wisconsin Press, Madison. 1974.Some features of population dynamics in mammals. Proc. Int. Congr. Game Biol., 11th. 1973:17-58. Kennedy,J. S. 1956.Phase transformation in locust biology. Biol. Rev. 31:349-370. Key, K. H. L. 1950.A critiqueon thephase theory of locusts.Q. Rev. Biol. 25:363-407. . 1957.Kentromorphic phases in threespecies of phasmatodea. Aust. J. Zool. 5:247-284. Khasimuddin,S. 1981a. Behavioralecology of the African armyworm, Spodoptera exempta (Walker): observationson populationprocesses during a high-densityoutbreak. Insect Sci. Appl. 1:143-146. 1981b. Phase variationand "offseason" survivalof the Africanarmyworm, Spodoptera exempta(Walker) (Lepidoptera:Noctuidae). Insect Sci. Appl. 1:357-360. Klocke,J. A., and B. G. Chan. 1982.Effects of cotton condensed tannin on feedingand digestionin thecotton pest Heliothis zea. J. InsectPhysiol. 28:911-915. INTERACTIONS BETWEEN HERBIVORES AND PLANTS 233

Koehler,W. 1956.Acantholyda nemoralis Thoms. in the Silesian forests. Rocz. NaukLesnych. 15:3- 194. Kuc, J. 1982.Induced immunity to plantdisease. BioScience 32:854-860. Kuc, J.,and F. L. Caruso. 1977.Activated coordinated chemical defense against disease in plants. Am. Chem.Soc. Symp.Ser. 62:78-89. Lawton,J. H., andD. R. Strong,Jr. 1981. Community patterns and competition infolivorous insects. Am. Nat. 118:317-338. Leonard,K. J. 1977.Selection pressures and plantpathogens. Ann. N.Y. Acad. Sci. 287:207-222. Levin,D. A. 1971.Plant phenolics: an ecologicalperspective. Am. Nat. 105:157-181. Lewin,R. 1983a.Santa Rosalia was a goat.Science 221:636-639. . 1983b.Predators and hurricaneschange ecology. Science 221:737-740. Lewis, A. C. 1979. Feedingpreference for diseased and wiltedsunflower in the grasshopper Melanopus differentialis.Entomol. Exp. Appl. 26:202-207. Long,D. B. 1953.Effects of populationdensity on larvaeof Lepidoptera.Trans. R. Entomol.Soc. Lond. 104:543-585. 1955.Observations on sub-socialbehavior in two speciesof lepidopterouslarvae, Pieris brassicaeL. and Plusia gammaL. Trans.R. Entomol.Soc. Lond. 11:421-437. Loper,G. M. 1968.Effect of aphid infestation on thecoumestrol content of alfalfa varieties differing in aphidresistance. Crop Sci. 8: 104-106. MacArthur,R. H., and E. 0. Wilson.1967. The theoryof island biogeography. Princeton University Press,Princeton, N.J. McFarlane,J. E., and M. H. W. Distler.1982. The effectof rutinon growth,fecundity and food utilizationin Achetadomesticus (L.). J. InsectPhysiol. 28:85-88. McIntyre,J. L. 1980.Defenses triggered by previous invaders: nematodes and insects. Pages 333-343 inJ. G. Horsfalland E. B. Cowling,eds. Plantdisease. Vol. 5. AcademicPress, New York. Mackay,P. A., and W. G. Wellington.1977. Notes on thelife history and habitsof thered-backed sawflyEriocampa ovata (Hymenoptera:Tenthredinidae). Can. Entomol.109:53-58. McKey, D. 1979.The distributionof secondarycompounds within plants. Pages 56-133 in G. A. Rosenthaland D. H. Janzen,eds. Herbivores:their interaction with secondary plant metabolites.Academic Press, New York. McLaughlin,S. B., and D. S. Shriner.1980. Allocation of resources to defenseand repair. Pages 407- 431 in J. G. Horsfalland E. B. Cowling,eds. Plantdisease. Vol. 5. AcademicPress, New York. McNaughton,S. J. 1976. Serengetimigratory wildebeest: facilitation of energyflow by grazing. Science 191:92-94. 1979.Grazing as an optimizationprocess: grass-ungulate relationships in theSerengeti. Am. Nat. 113:691-703. McNaughton,S. J.,and J. L. Tarrants.1983. Grass leaf silicification: natural selection for an inducible defenseagainst herbivores. Proc. Natl. Acad. Sci. USA 80:790-791. Madden,J. L. 1977.Physiological reactions of Pinus radiata to attack by woodwasp, Sirex noctilio F. (Hymenoptera:Siricidae).Bull. Entomol.Res. 67:405-426. Mares,M. A., F. A. Enders,J. M. Kingsolver,J. L. Neff,and B. B. Simpson.1977. Prosopis as a nichecomponent. Pages 123-149in B. B. Simpson,ed. Mesquite.Dowden, Hutchinson & Ross, Stroudsburg,Pa. Markkula,M., S. Laurema,and K. Tiittanen.1976. Systemic damage caused by Triozaapicaulis on carrot.Pages 153-155in T. Jermy,ed. The hostplant in relationto insectbehavior and reproduction.Plenum, New York. Mason,R. R., andR. F. Luck. 1978.Population growth and regulation. Pages 41-47 in M. H. Brookes, R. W. Stark,and R. W. Campbell,eds. The Douglas-firtussock moth: a synthesis.US Dep. Agric.For. Serv. Sci. EducationAgency. Tech. Bull. 1585. Matthee,J. J. 1947.Phase variation in the lawn caterpillar (Spodoptera abyssinia Guen.). J. Entomol. Soc. S. Afr.10:16-23. Mattson,W. J.,and N. D. Addy.1975. Phytophagous insects as regulatorsof forest primary production.Science 190:515-522. 234 THE AMERICAN NATURALIST

Miles,P. W. 1968a.Insect secretions in plants.Ann. Rev. Phytopathol.6:137-164. 1968b.Studies on thesalivary physiology of plant-bugs.Experimental induction of galls. J. InsectPhysiol. 14:97-106. 1978.Redox reactions ot hemipterous saliva in plant tissues. Entomol. Exp. Appl.24:534-539. Millburn,P. 1978.Biotransformation of xenobiotics by animals.Pages 35-73 in J. B. Harborne,ed. Biochemicalaspects of plantand animalcoevolution. Academic Press, New York. Mitter,C., andD. J.Futuyma. 1983. An evolutionary-geneticview of host-plant utilization by insects. Pages 427-459in R. F. Dennoand M. S. McClure,eds. Variableplants and herbivoresin naturaland managedsystems. Academic Press, New York. Mitter,C., D. J. Futuyma,J. C. Schneider,and J. D. Hare. 1979.Genetic variation and hostplant relationsin a parthenogeneticmoth. Evolution 33:777-790. Montgomery,G. G., ed. 1978.The ecologyof arboreal folivores. Smithsonian Institution, Washing- ton,D.C. Mooney,H. A., and S. L. Gulman.1982. Constraints on leafstructure and functionin referenceto herbivores.BioScience 32:198-206. Morris,R. F., ed. 1963.The dynamics of epidemic spruce budworm populations. Mem. Entomol. Soc. Can. 31:1-332. Morris,R. F., C. A. Miller,D. 0. Greenbank,and D. G. Mott.1958. The populationdynamics of the sprucebudworm in easternCanada. Proc. 10thInt. Congr. Entomol. 4:137-149. Muller,K. 0. 1956.Einige einfache versuche zum nachweisvon phytoalexinen.Phytopathol. Z. 27:237-254. Muller,K. O., and H. Borger.1941. Experimentelle untersuchungen uber die phytophora-resistenz derkartoffel. Arb. Biol. Reichsanst.Land-Forstwirtsch., Berlin-Dahlem 23:189-231. Nelson,C. E., M. Walker-Simmons,D. Makus,G. Zuroske,J. Graham,and C. A. Ryan. 1983. Regulationof synthesisand accumulationof proteinaseinhibitors in leaves of wounded tomatoplants. Am. Chem.Soc. Symp.Ser. 208:103-122. Nichols,J. 0. 1968.Oak mortalityin Pennsylvania.A ten-yearstudy. J. For. 66:681-694. Niemela,P., A. M. Aro,and E. Haukioja.1979. Birch leaves as a resourcefor herbivores. Damage- inducedincrease in leafphenols with trypsin-inhibiting effects. Rep. Kevo SubarcticRes. Stn. 15:37-40. Nolte,D. J. 1963.A pheromonefor melanization of locusts.Nature 200:660-661. 1974.The gregarizationof locusts.Biol. Rev. 49:1-14. 1977.The actionof locustol.J. InsectPhysiol. 23:899-903. Norris,D. M. 1979.How insectsinduce disease. Pages 239-255 in J. G. Horsfalland E. B. Cowling, eds. Plantdisease. Vol. 4. AcademicPress, New York. Odiyo,P. 0. 1981.Development of the first outbreaks of the African armyworm, Spodoptera exempta (Walk.),between Kenya and Tanzania during the "off-season" months of July to December. InsectSci. Appl. 1:305-318. Osborne,D. J. 1973.Mutual regulation of growth and development in plants and insects. Pages 33-42 in H. F. van Emden,ed. Insect/plantrelationships. Blackwell, London. Owen,D. F., and R. C. Wiegert.1976. Do consumersmaximize plant fitness? Oikos 27:488-492. . 1982.Grasses and grazers:is therea mutualism?Oikos 38:258-260. Perry,D. A., andG. B. Pitman.Genetic and environmental influences in host resistance to'herbivory: Douglasfir and thewestern spruce budworm. J. Appl.Entomol. (in press). Peters,T. M., and P. Barbosa. 1977.Influence of population density on size,fecundity and develop- mentrate of insectsin culture.Annu. Rev. Entomol.22:431-450. Pianka,E. R. 1970.On r-and K-selection.Am. Nat. 104:592-597. Potts,D. C. 1981.Crown-of-thorns starfish: man-induced pest or naturalphenomena. Pages 55-86 in R. L. Kitchingand R. E. Jones,eds. The ecologyof pests (some Australian case histories). CSIRO, Melbourne. Prentice,R. M. 1962.Forest Lepidoptera of Canada. Vol. 2. Bull. 128.Canada Dep. Forestry,Ottawa. 1963.Forest Lepidoptera of Canada. Vol. 3. Publ. 1013.Canada Dep. Forestry,Ottawa. Price,P. W., C. E. Bouton,P. Gross,B. A. McPheron,J. N. Thompson,and A. E. Weis. 1980. Interactionsamong three trophic levels: influence of plantson interactionsbetween insect herbivoresand naturalenemies. Ann. Rev. Ecol. Syst. 11:41-65. INTERACTIONS BETWEEN HERBIVORES AND PLANTS 235

Prokopy,R. J. 1981.Epideictic pheromones that influence spacing patterns of phytophagous insects. Pages 181-213in D. A. Nordlund,R. L. Jones,and W. J.Lewis, eds. Semiochemicals:their rolein pestcontrol. Wiley, New York. Puritch,G. S., andW. W. Nijholt.1974. Occurrence of juvabione-related compounds in grand fir and Pacificsilver fir infested by balsamwooly aphid. Can. J. Bot. 52:585-587. Raffa,K. F., and A. A. Berryman.1982. Accumulation of monoterpenesand associatedvolatiles followinginoculation of grandfir with a fungustransmitted by thefir engraver, Scolytus ventralis(Coleoptera: Scolytidae). Can. Entomol.114:797-810. . 1983.The role of host plant resistance in the colonization behavior and ecology of bark beetles (Coleoptera:Scolytidae). Ecol. Monogr.53:27-49. Rasmussen,R. A. 1970.Isoprene: identified as a forest-typeemission to the atmosphere. Environ. Sci. Technol.8:667-671. . 1972.What do hydrocarbonsfrom trees contribute to air pollution?J. Air Pollut.Contr. Assoc. 22:537-543. Reardon,P. O., C. L. Leinweber,and L. B. Merrill.1972. The effectof bovine saliva on grasses.J. Anim.Sci. 34:897-898. 1974.Responses of sideoatesgrama to animalsaliva and thiamine.J. RangeManage. 27: 400-401. Rhoades,D. F. 1977.The antiherbivorechemistry of Larrea. Pages 135-175in T. J. Mabry,J. H. Hunziker,and D. R. Difeo,Jr., eds. Creosotebush. Dowden, Hutchinson & Ross, Strouds- burg,Pa. 1979.Evolution of plant chemical defense against herbivores. Pages 3-54 in G. A. Rosenthal and D. H. Janzen,eds. Herbivores:their interaction with secondary plant metabolites. AcademicPress, New York. 1983a.Herbivore population dynamics and plantchemistry. Pages 155-220in R. F. Denno and M. S. McClure,eds. Variableplants and herbivoresin naturaland managedsystems. AcademicPress, New York. 1983b.Responses of alder and willowto attackby tent caterpillars and webworms: evidence forpheromonal sensitivity of willows.Am. Chem.Soc. Symp.Ser. 208:55-68. Rhoades,D. F., andR. G. Cates. 1976.Toward a generaltheory of plant antiherbivore chemistry. Rec. Adv. Phytochem.10:168-213. Rice,E. L. 1974.Allelopathy. Academic Press, New York. Roelofs,W. L. 1981.Attractive and aggregating pheromones. Pages 215-235 in P. A. Nordlund,R. L. Jones,and W. J. Lewis,eds. Semiochemicals:their role in pestcontrol. Wiley, New York. Root,R. B., andP. M. Kareiva.1983. The searchfor resources by cabbage butterflies (Pieris rapae): ecologicalconsequences and adaptivesignificance of Markovianmovements in a patchy environment.Ecology 65:147-165. Rose,D. J.W. 1975.Field development and quality changes in successivegenerations of Spodoptera exempta(Wlk.), the African armyworm. J. Appl.Ecol. 21:727-739. Rosenthal,G. A., D. L. Dahlman,and D. H. Janzen.1976. A novel meansof dealingwith L- canavanine,a toxicmetabolite. Science 192:256-258. Rosenthal,G. A., and D. H. Janzen,eds. 1979.Herbivores: their interaction with plant secondary metabolites.Academic Press, New York. Rosenthal,G. A., D. H. Janzen,and D. L. Dahlman.1977. Degradationand detoxificationof canavanineby a specializedseed predator.Science 196:658-660. Rothschild,M. 1973.Secondary plant substances and warningcolouration in insects.Pages 59-83 in H. F. van Emden,ed. Insect/plantrelationships. Blackwell, London. Salt, G. W., ed. 1984.A roundtable on researchin ecologyand evolutionarybiology. Am. Nat. 122:583-705. Schultz,D. E., and D. C. Allen.1977. Characteristics ofsites with high black cherry mortality due to barkbeetles following defoliation by Hydria prunivorata. Environ. Entomol. 6:77-81. Schultz,J. C. 1983a. Habitatselection and foragingtactics of caterpillarsin heterogeneoustrees. Pages 61-90 in R. F. Denno and M. S. McClure,eds. Variableplants and herbivoresin naturaland managedsystems. Academic Press, New York. 1983b.Impact of variableplant defensive chemistry on susceptibilityof insectsto natural enemies.Am. Chem.Soc. Symp.Ser. 208:37-54. 236 THE AMERICAN NATURALIST

Schultz,J. C., and I. T. Baldwin.1982. Oak leafquality declines in responseto defoliationby gypsy mothlarvae. Science 217:149-151. Scriber,J. M. 1983.Evolution of feedingspecialization, physiological efficiency, and hostraces in selectedPapilionidae and Saturniidae.Pages 373-412in R. F. Dennoand M. S. McClure, eds. Variableplants and herbivoresin naturaland managedsystems. Academic Press, New York. Scriber,J. M., and P. P. Feeny.1979. The growthof herbivorous caterpillars in relationto degreeof feedingspecialization and to growthform of their foodplants (Lepidoptera:Papilionidae and Bombycoidea).Ecology 60:829-850. Scriber,J. M., and F. Slansky,Jr. 1981. The nutritionalecology of immatureinsects. Annu. Rev. Entomol.26: 183-211. Seifert,R. P., and F. H. Seifert.1976. A communitymatrix analysis of Heliconia insectcommunities. Am. Nat. 110:461-483. Sequeira,L. 1980.Defenses triggered by the invader: recognition and compatibility phenomena. Pages 179-200in J.G. Horsfalland E. B. Cowling,eds. Plantdisease. Vol. 5. AcademicPress, New York. Shiga,M. 1976.Effect of group size on thesurvival and development of young larvae of Malacosoma neustria testacea Motschulsky(Lepidoptera, Lasiocampidae) and its role in the natural population.Kontyu (Tokyo) 44(4):537-553. Smith,C. C. 1976.When and howmuch to reproduce:the trade-off between power and efficiency. Am. Zool. 16:763-774. Smith,N. G. Periodicmigrations and populationfluctuations by the neotropicalday-flying moth Urania fulgens throughthe isthmus of Panama.Pages 135-147in E. G. Leigh,Jr., A. S. Rand,and D. M. Windsor,eds. The ecologyof a tropicalforest. Smithsonian Institution, Washington,D.C. (in press). Smith,W. H. 1981.Air pollution and forests.Springer-Verlag, New York. Southwood,T. R. E. 1976.Bionomic strategies and population parameters. Pages 26-48 in R. M. May, ed. Theoreticalecology. Blackwell, London. 1978.Ecological methods. Chapman & Hall, London. Spurr,S. H., E. W. Littlefield,and H. A. Bess. 1947.Ecology of susceptible and resistant forest types and stands.Harv. For. Bull. 22:27-39. Stage,A. R. 1978.Modeling probability ofoutbreak occurrence and stand involvement. Pages 59-61 in M. H. Brookes,R. W. Stark,and R. W. Campbell,eds. The Douglas-firtussock moth: a synthesis.US Dep. Agric.For. Serv.Sci. EducationAgency Tech. Bull. 1585. Staley,J. M. 1965.Decline and mortalityof red and scarletoaks. For. Sci. 11:2-17. Stamp,N. E. 1980.Egg depositionpatterns in butterflies:why do some speciescluster their eggs ratherthan deposit them singly? Am. Nat. 115:367-380. Stehr,F. W. 1974.Release, establishment and evolution of parasites and predators. Pages 124-136in F. G. Maxwelland F. A. Harris,eds. Proc.of the summer institute of biological control of plantinsects and diseases.University of MississippiPress, Jackson. Stenseth,N. C. 1983.Grasses, grazers, mutualism and coevolution: a commentabout handwaving in ecology.Oikos 41:152-153. Strong,D. R., Jr.1983. Natural variability and themanifold mechanisms of ecological communities. Am. Nat. 122:636-645. Suzuki,H. 1980.Defenses triggered by previous invaders: fungi. Pages 319-332 in J.G. Horsfalland E. B. Cowling,eds. Plantdisease. Vol. 5. AcademicPress, New York. Swain,T. 1979.Tannins and lignins.Pages 657-682in G. A. Rosenthaland D. H. Janzen,eds. Herbivores:their interaction with plant secondary metabolites. Academic Press, New York. Symmons,P. M. 1978.The preventionof plaguesof thered locust. Acrida 7:55-78. Taylor,R. A. J. 1979.Simulation model of locustmigratory behaviour. J. Anim.Ecol. 48:577-602. Teale, E. W. 1949.The insectworld of J. HenriFabre. Dodd, Mead,New York. Thompson,D. Q. 1955.The 1953lemming emigration at PointBarrow, Alaska. Arctic 8:37-45. Tsubaki,Y. 1981.Some beneficialeffects of aggregationin younglarvae of Pryeria sinica Moore (Lepidoptera:Zygaenidae). Res. Popul.Ecol. 23:156-167. INTERACTIONS BETWEEN HERBIVORES AND PLANTS 237

Tsyplenkov,E. P. 1978. HarmfulAcridoidea of the USSR. U.S.D.C. Natl. Tech. Inf. Serv. Springfield,Va. Uvarov,B. P. 1921.A revisionof the genus Locusta L. (=PachytylusFieb.), with a newtheory as to theperiodicity and migrationsof locusts.Bull. Entomol.Res. 12:135-163. 1928.Locusts and grasshoppers.Imperial Bureau of Entomology,London. . 1966.Grasshoppers and locusts.Vol. 1. CambridgeUniversity Press, Cambridge. . 1977.Grasshoppers and locusts.Vol. 2. Centrefor Overseas Pest Research, London. Vaughan,G. L., andA. M. Jungreis.1977. Insensitivity oflepidopteran tissues to ouabain: physiological mechanismsfor protection from cardiac glycosides. J. InsectPhysiol. 23:585-589. Vite,J. P. 1961.The influenceof water supply on oleoresinexudation pressure and resistance to bark beetleattack in Pinusponderosa. Contrib. Boyce ThompsonInst. PlantRes. Prof.Pap. 21:37-66. Wagner,M. R., and D. M. Benjamin.1981. Allelochemics and nutritionalindices for larch sawfly, Pristiphoraerichsonii (Hartig): a specialistfeeding on Larixspp. J. Chem. Ecol. 7:165-174. Waldbauer,G. P. 1968.The consumptionand utilization of food by insects. Pages 229-288 in J. W. L. Beament,J. E. Treherne,and V. B. Wigglesworth,eds. Advancesin insect physiology. Vol. 5. AcademicPress, New York. Wallace,J. W., and R. L. Mansell,eds. 1976.Biochemical interaction between plants and insects. Plenum,New York. Waloff,Z. 1966.The upsurgesand recessionsof the desert locust plague: an historicalsurvey. Anti- LocustMem. 8: 1-111. 1972.The plaguedynamics of the desert locust Schistocerca gregaria (Forsk.). Pages 363-369 in Proceedingsof theinternational study conference on thecurrent and futureproblems of Acridology,London, 1970. Centre for Overseas Pest Research, London. Waring,R. H., and G. B. Pitman.1983. Physiological stress in lodgepolepine as a precursorfor mountainpine beetle attack. Z. Ang.Entomol. 96:265-270. Waters,W. E., and R. W. Stark.1980. Forest pest management: concept and reality.Annu. Rev. Entomol. 25:479-509. Watt,K. E. F. 1964.Comments on fluctuationsof animalpopulations and measuresof community stability.Can. Entomol.96:1434-1442. 1965.Community stability and thestrategy of biological control. Can. Entomol.97:887-895. Way,M. J. 1973.Population structure in aphid colonies. Pages 76-84 in A. D. Lowe,ed. Perspectives in aphidbiology. Entomology Society of New Zealand,Aukland. Way,M. J.,and M. Cammell.1970. Aggregation behaviour in relationto foodutilization by aphids. Pages 229-247in A. Watson,ed. Animalpopulations in relationto theirfood resources. Blackwell,Oxford. Weldon,P. J. 1983.The evolutionof alarmpheromones. Pages 309-312in D. Muller-Schwarzeand R. M. Silverstein,eds. Chemicalsignals in vertebrates.Vol. 3. Plenum,New York. Wellington,W. G. 1957.Individual differences as a factorin population dynamics: the development of a problem.Can. J. Zool. 35:293-323. 1980.Dispersal and population change. Pages 11-24in A. A. Berrymanand L. Safranyik,eds. Dispersalof forestinsects: evaluation, theory and managementimplications. Washington StateUniversity Coop. Ext. Serv.,Pullman. Went,D. F. 1982.Egg activation and parthenogenetic reproduction ininsects. Biol. Rev. 57:319-344. Weyh,R., and V. Maschwitz.1978. Trail substance in larvaeof Eriogasterlanestris L. Naturwis- senschaften65:64. White,M. J. D. 1973.Animal cytology and evolution.Cambridge University Press, Cambridge. White,T. C. R. 1969.An indexto measureweather-induced stress of trees associated with outbreaks of psyllidsin Australia.Ecology 50:905-909. 1974. A hypothesisto explainoutbreaks of loopercaterpillars with special reference to populationsof Selidosema suavis in a plantationof Pinus radiata in NewZealand. Oecologia 16:279-301. 1976.Weather, food and plaguesof locusts.Oecologia 22:119-134. Whitham,T. G. 1983.Host manipulationof parasites:within-plant variation as a defenseagainst 238 THE AMERICAN NATURALIST

rapidlyevolving parasites. Pages 15-41in R. F. Dennoand M. S. McClure,eds. Variable plantsand herbivoresin naturaland managedsystems. Academic Press, New York. Whitney,H. S. 1982.Relationships between bark beetles and symbioticorganisms. Pages 183-211in J.B. Mittonand K. B. Sturgeon,eds. Barkbeetles in North American conifers. University of Texas Press,Austin. Wood, D. L. 1982.The role of pheromones,kairomones and allomonesin thehost selection and colonizationbehavior of barkbeetles. Annu. Rev. Entomol.27:411-446. Wood,D. L., and W. D. Bedard.1977. The roleof pheromonesin thepopulation dynamics of the westernpine beetle. Proc. Int. Congr. Entomol. 15:643-652. Wright,L. C., A. A. Berryman,and S. Gurusiddaiah.1979. Host resistance to thefir engraver beetle. 4. Can. Entomol.111:1255-1262. Zucker,W. F. 1983.Tannins: does structuredetermine function? An ecological perspective. Am. Nat. 121:335-365.