~

PLANT MECHANICAL DEFENSES AGAINST INSECT HERBIVORY

o. Wilson Fernandesl

ABSTRACT. Plants offer an enormous variety of new habitats and niches for insects.Herbivory added many dimensions to plant's existence thus influencing theirdistribution over space and tirne and ultirnately their evolution and diversity.Hence, plants defend themselves against herbivores that lessen their lifetirnefitness. Some cases are presented in which plant mechanical defenses (pubescence,waxes, latex, crystals, resins, and texture) are relevant against insect herbivory.Whenever possible, examples from tropical systerns, which are generally rare inthe current literature on plant defense mechanisrns, are also provided. The interplayof the mechanisms in the plant defense against herbivory , plant physiology, andadaptation to the environment is also discussed.

KEYWORDS. HERBIVORY; INSECf HERBIVORY; MECHANICAL DEFENSES; PLANT DEFENSES;

PLANT HAIRS.

INTRODUCTION

The impact of insect herbivores on their host plants has been known sinceancient times. An enormous bulk of the literature on insect-plant relationships iscentered on the impact that herbivores have on their host plants' survival and fitness(for general reviews see ROSENTHAL & JANZEN, 1979; PRICE, 1984; STRONG et al., 1984;HERMS & MA1TSON, 1992). An even greater alllount of research has been done on theimpact of herbivorous insects on plants of agricultural, forest, and ornamentalimportance (e.g., JOHNSON & LyON, 1976~ PIMENTEL, 1981; COULSON & WI1TER, 1984;

FERNANDES, 1987).To survive and succeed plants must be able to circumvent herbivore pressure.

Thus, plants must defend themselves against unbidden herbivores. Plant defensesinclude, first, those that decrease the chance of discovery and second, those that lessenor repel feeding after discovery (Fox, 1981). In the former category, we can includeplant distribution, association with other plants, phenological, and developmentaldefense types, whereas in the second category we'[md chemical defenses (see PRICE,1984). Other ways of defending against herbivores include acquiring mutualistrelationships with other organisms to help in the defense, for exalllple the cases knownas the ant/acacia mutualism and microorganism-plant associations, or throughgenetically-induce changes such as in somatic mutations. However, categories ofdefense mechanisms are arbitrary because of the intrincate associations that existalllong plants and insects both in time and space.

Many hypotheses have been erected on the evolution of plant defenses againstherbivores (e.g., Fox, 1981; MA1TSON et al., 1988), but they can be grouped into threegeneral hypotheses. Firstly, the hypothesis that plant defense evolved primarily inresponse to herbivore pressure. Second, the hypothesis that plant defense evolvedprimarily in response to environmentally induced damage (which in some waysmimics herbivore pruning or damage) or situations, such as nutrient-poor soils.Finally, the hypothesis that defense mechanisms are by-products of plant normal

1. Departamento de Biologia Geral, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais,Caixa Postal 486, 30161-970 Belo Horizonte Mo, Brasil.

..

422 FERNANDES

metabolism or an integral part of plant development (the nul1 hypothesis). Empiricalstudies in this area have increased exponential1y, and a modern American unifyingtheory on insect-plant relaiionship has been proposed recently by HERMS & MATTSON(1992).

This review is an attempt to bring together examples of plant mechanicaldefenses used against herbivores, and whenever possible to bring to light examplesfrom tropical studies. Advances in this area have been achieved primarily in thetemperature region where plant resistance mechanisms have been scrutinized in a moreexperimental approach. I shall describe each mechanism or strategy of defense as aseparate module, although we should bear in mind that the relationships existingbetween plant physiology and the several defense types discussed interplay in complexways as yetnot fully understood (seeSEIGLER & PRICE 1976, HERMS & MA1TSON, 1992).The length of each topic may be seen as an indicator of the amount of research in thefield. For instance, more will be said on plant trichomes than on plant crystals asadaptive strategies against herbivores. It is not an exhaustive revision on the subjectas the field has expanded enormously. Forthcoming papers will cover other mechanismsof plant defense against insect herbivores.

MECHANICAL DEFENSES

Perhaps all plant parts offer some sort of resistance against herbivory .Theyrange from tissue hardness to higWy complex glandular trichomes and spines (LEVIN,1973; SOUTHWOOD, 1986). All structural plant are obviously composed and mantainedby the plant ' s physiological and chemical machinery so that a distinction made in here

is didactical. I will present some cases where pubescence, tissue hardness, crystals,latex, waxes and resins has been influential in defending plánts against insectherbivores.

PubescenceThe plant epidermis is often covered by outgrowths called trichomes. They are

found in all major groups of terrestrial plants (ESAu, 1965; JOHNSON, 1975). Theyoriginate from epidermal tissue and then develop and differentiate to produce hair-likestructures (UPHOLF, 1962). Trichomes can be divided into two distinct categories,glandu1ar and non-glandular. The trichome cover of individual plants can vary gr~atlyin quantity and quality, from organ to organ, and from tissue to tissue (DE CANDOLE,1841). They vary from soft pubescence to glandular stinging hairs to large spines(SOLEREDER, 1908). Trichomes vary enormously among plant tissue and are higWyvariable among plant populations. Younger leaves of several herbaceous species areknown to be more pubescent than older leaves (Y APP, 1912; STOBER, 1917). The samepattem is also observed on many trees. For instance, the unfolded and younger leavesof the tropical Tabebuia ochracea (Bignoniaceae) tree are covered by a thick layer ofhigWy complex trichomes (RIBEIRO et al., 1994). WARMING (1909) observed thatpubescence is positively associated with harsh moisture regimes (but see LEVIN, 1973;JOHNSON, 1975); andCLAusEN etal. (1940) showedthatPote!liilla (Rosaceae) individualsplanted in sunny sites were more pubescent than individuaIs planted in shady sites.Common garden experiments have shown that the degree of pubescence is underrelatively simple genetic control of one or two genes (NIELSEN et al., 1982).

..

RevIa bras Enl 3812).

PLANT MECHANICAL DEFENSES 423

Plant trichomes can act as structural defenses against insect herbivores.RICHARDSON (1943) observed that bean leaf hooked hairs immobilized and starvedbedbugs to death. The hook1ike trichomes of Passiflora adenopoda (Passifloraceae)provide a specific and effective defense against its major class of herbivore, theheliconiine butterfly larvae (GILBERT, 1971). The host hairs entrap and killlarva by acombination of starvation and loss of hemolymph caused by numerous puncturewounds in the larval integument. RATHCKE & POOLE (1975) showed, however, that atleast one species of ithomiid butterfly, Mechanitis isthmia, has evolved a uniqueadaptation for avoiding the trichomes on its spiny Solanum hosts (Solanaceae) (seea1so HULLEY, 1988). PILLEMER & TINGEY (1976, 1978) provided direct evidence ofadaptation showing differential survivorship of Empoasca fabae (Homoptera,Aphididae) feeding on two plant genotypes that differed in density of hookedtrichomes (see also Poos & SMITH, 1931; TAYLOR, 1956). The frequency ofherbivorecapture and mortality were highly correlated with trichome density, but trichomeeffectivenesswas dependent on its angle of insertion in the epidermis. WOODMAN &FERNANDES ( 1991) showed that Verbascum thapsus (Scrophulariaceae) leaves varied inthe density of hairs and demonstrated that generalist herbivores selected the leastpubescent leaves as opposed to those with high pubescence. In a hairy gall formed bya Cecidomyiidae (Diptera) on the tropical treeMachaerium aculeatum (Leguminosae)trichomes confered some protection to the gall-former by trapping and killingparasitoids of the larva and small sucking herbivores that feed on the gall tissue(FERNANDES et al., 1987).

In addition to feeding and movement impedance, trichomes can influence theattachment of insects to the leaf surface. For example, V AN DUyN et al. ( 1972) observedthat the Mexican bean beetle, Epilachna varivestis (Coleoptera, Çhrysomelidae) fallsoff leaves without trichomes. Other studies have shown that several insects prefer hairyleaves for attachment (e.g., CALLAHAN, 1957; LUKEFAHR et al., 1970).

An enhanced leveI of defense is achieved by those plant species or biotypes thatpresent glandular trichomes. A broad spectrum of chemical substances have beendescribed from glandular trichomes such as alkaloids (RODRIGUEZ et al., 1984),flavonoides (KELSEY et al., 1984; WOLLENWEBER; 1984), diterpenes (BAKKER et al.,1972), triterpenes (DAWSON et al., 1966; DELL & McCoMB 1975), mixed-terpenes(WILLINSKY, 1973; TuRNERetal., 1977, 1978),andsesquiterpenes(KELsEY&SHAFIZADEH,1980; CROTEAU & JOHNSON, 1984). GIBSON & TURNER (1977) showed that Solanunpolyadenium and S. berthaultii have four-Iobed head hairs which release a stickysubstance when ruptured. On S. polyadenium, these hairs trapped aphids, coloradopotato beetle larvae, and leafhoppers (see also GIBSON, 1971,1974, 1976abc). The twowiJd potato species defend against infestation by Empoasca fabae (Homoptera,Aphididae) by encasing the mouth parts and tarsi with a viscous exudate that rapidlydarkens and hardens (TINGEY & GIBSON, 1978). Feeding and mobility are impaired,leading to early death and reduced herbivore field populations (see also BROERSMA etal., 1972). In addition to trapping and/or poisoning insects, nonvolatile trichomeexudates may act as gustatory repellents (e.g. BURH et al., 1958; EISNER, 1964; HARLEY& THORSTEINSON, 1967; LEVIN, 1973, see also REYNOLÚS & RODRIGUEZ, 1986). Forinstance, ISHIKA w A& HIRAO ( 1966) found that menthol released from trichomes ofseveral Labiatae plants were strong repellents to silkworms.LEvIN (1973) advanced thehypothesis that volatile components of trichome exudates act as another line of defense

..RevIa bras. Ent. 38(2), 1994

FERNANDES424

by advertising the presence of substances that insects would find repellent should theysample their host. An enonnous variation in the protection of the fruit coat is found insympatric Species of Chamaecrista (Leguminosae) (G.W. FERNANDES, pers. observ.).A spectruni of fruit coating exists: in one direction it varies from bare to longtrichomes; in another it varies from simple trichomes to highly complex trichomes; ina third category it may be bare or glandular; and yet in another direction it varies indensity. Attack rates by seed beetles ( Coleoptera, Bruchidae) varies among theChamaecrista species and are probably related to the differential protection of thefruits (BICALHO & FERNANDES, 1994; M; TAVARES & Y. ITABAIANA, pers. comrn.). Thissort of variation in a system offers an excellent opportunity to mechanistically test theefficiency and effects of plant escalation in defenses against herbivores (see EHRLICH& RAVEN, 1964; Fox, 1981). The glandu1ar hairs of the Mexican plant Arbutusxalapensis (Ericaceae) confer resistance against herbivory (BECERRA & EZCURRA,1986), and have u1timately influenced its herbivore fauna (EZCURRA et al., 1987).Correlational studies on subtropical islands support the contention that hairy morphsof Conocarpus erectus (Combretaceae) suffer leaf removal by insect herbivores andthat pubescence is an effective deterrent against herbivory (SCHOENER, 1988). Thus,variation in trichome cover may have important influence on an insect herbivore

comrnunity.Variation in herbivory rates are influenced by the behaviors of the ovipositing

female herbivores. Female insect herbivores have been shown to have evolvedbehaviors to avoid host plants that diminish larval perfonnance (THOMPSON, 1988).STEPHENS ( 1959) andSTEpHENs & LEE (1961) found thatAnthonomus grandis (Coleoptera,Curcu1ionidae) oviposition and feeding preference decreased with increasing hostplant bud pubescence. In many case studies, females prefer to lay eggs on low densitytrichome cu1tivars ofwheat (ROBERTS et al., 1979; LAMPERT et al., 1983), and on beans(CHIANG&NORRIS, 1983). Inonestudy (GROSS & PRICE, 1988), leaftrichomemorphologyhas favored the evolution of obligate endophytism in a leaf miner, Tildenia inconspicuella(Lepidoptera, Gelechiidae) on its host Solanum carolinense by selecting against minearchitectures that wou1d allow miners easy access to the leaf surface. Parasitoid speciesrichness was much greater on 7: inconspicuella than on a relative, 7: georgiei, thatmines Physalis heterophylla var. antigua (Solanaceae). Parasitoids are excludedfromthe 7: georgiei miner because it can drop off from its host plant leaves which bearflexible, thin, and relatively simple hairs. However, T. inconspicuella cannotleave S.carolinense leaves which present sessile stellate trichomes. The authors argued thatobligate endophitism, which is uncomrnon among related gelechiids, is a specificadaptation to S. carolinense leaf morphology, that has made the 7: inconspicuellaminer available to more parasitoid species that its vagile relative.

Some insects are known, however, to walk and feed freely on hairy plant parts.This is the case for stilt bugs (Hemiptera, Berytidae). They are generally associatedwith glandu1ar hairs of several plant families (WHEELER & SCHAEFER, 1982). Theseinsects have long legs and the tips of their femora are swollen giving an enlarged tibio-femoral articu1ation, thus increasirtg the leverage to swing the apex of the leg(SOUTHWOOD, 1986). FERNANDES et al., (1987) reported on the association of threespecies of berytids with the sticky glandu1ar hairs of the cecidomyiid leaf gall on M.aculeatum in Brazil. The berytids are able to feed on the gall in spite of the glandu1arhairs. In addition, the gall inquiline Tanaostigmodes fernandesi (Hymenoptera,

.

Tanaostigmatidae) and the parasiteEurytoma minasensis (Hymenoptera, Eurytomidae )were never observed to be trapped by the hairs (DE SANTIS & FERNANDES, 1989) becauseof their large size relative to the secretory trichomes. The differences between insectspecies preferences and hair impact on herbivores is a matter of sca1Íng and form,which is influenced by the kinds of trichomes present (see SOUTHWOOD, 1986).

The ultimate leveI of trichome protection and specialization may have beenachieved by insectivorous plants. During the early evolutionary stages, their stickyhairs and secretions were used to defend themselves against herbivores. Defensesshould be very effective in nutrient-poor sites Ín which these exist ~ESLOP-HARRISON,1976). Once the herbivores were trapped, selection may have favored plants that usedthem as an altemative food source (WILLIAMS, 1976; THOMPSON, 1981; JOEL, 1986;JUNIPER 1986; JUNIPER et al., 1989).

Nevertheless, plant trichomes may also function Ín a variety of physiologicalprocesses such as altering leaf ref1ectance and leaf surface microclimate for example(e.g., UPHOLF, 1962; ESAU, 1965; WUENSCHER, 1970; RODRIGUEZ et al., 1984). We needto test the hypotheses that trichomes are adaptations to water economies or barriers tolessen impact by Ínsect herbivores or a combination ofboth. Leafhairs have a dual role:protection against herbivore pressure and barriers against evapotranspiration (W OODMAN& FERNANDES, 1991). For reviews on the role of trichomes on defense against insectherbivores SeeLEVIN (1973), JOHNSON (1975), WEBSTER (1975), RODRIGUEZ etal. (1984),and JUNIPER & SOUTHWOOD (1986).

Tissue HardnessPlant tissues vary enormously in texture, i.e., from very soft to very hard. Plant

tissue hardness is determined by the properties of the epidermis and any thick walledcells immediately beneath it (GRUBB, 1986; JUNIPER & SOUTHWOOD, 1986). GRUBB( 1986) provides data on the distribution of hard leaf surfaces Ín the plant kingdom.Tissue texture may prevent herbivore feeding. Successful stylet penetration ofParabemisia myricae (Homoptera, Aleyrodidae) Ín its host plant leaves is decreasedwith increasÍng host tissue hardness and age (WALKER, 1985, 1988). In addition,females prefer young leaves and survive better on -them as opposed to old, hard leaves(WALKER & AITKEN, 1985; WALKER, 1987). The hardening of gall wal1s preventspenetration of the ovipositor of parasitoid wasps that would reach the larva (CRAIG etal., 1990), and inhibitsfeeding on the gal1 tissue by herbivores. However, other studieshave shown that leafhardness is not an effective deterrent against piercÍng insects (e.g.,SOGAWA, 1982; see also FERNANDES & PRICE, 1988, 1991). In a classic tropical study,COLEY (1983) concluded that, Ín addition to water content, leaftoughness was the mostimportant predictor of leaf palatability of several persistent and pioneer trees oftropical rain forest Ín Panama. The amount of leaf area lost to herbivores was moststrongly correlated with leaf area toughness. Leaf hardness Íncreases sharply with agein the tropical shrub Coccoloba cereifera (Polygonaceae). Nevertheless, a generalistdiaspidid, Chrysomphalus dyctiospermi (Homoptera, Diaspididae) is found primarilyon the most hard, older, and least nutritious leaves of the plant. This apparent paradoxis partial1y solved because younger and softer leaves have an astonishing amount oftoxins and tannins which would diminish herbivore performance and survivorship.

Tissue hardness is, however, Ínfluenced by several other environmental factorssuch as water availability (WARMING. 1909; GRUBB. 1986). water potentia1 (OKALI.

levtA bras. Ent. 38(2). 1994

.

"426 FERN AND BS

1977),andnutrientdeficientsoils (LOVELESS, 1961,1962; MEDINA, 1983; MEDINAetal.,1978). Hypotheses testing.is necessary to sort out direct and indirect effects of tissuehardness on insect herbivory and adaptation to the environment.

Crystals and Other InclusionsA poorly investigated defense trait is that of crystalline structuresin plant parts.

The best known crystalline fonnations in plants are calcium oxalate crystals. Theyoccur in many plant species and in most organs and tissues (FRANCESCHI & HORNER,1980). Calcium oxalate crystals are known to cause irritation and buming sensationsin vertebrate herbivores (KINGSBURY, 1964) and thus may discourage feeding. Contactdennatitis, vomiting, healing prevention, perirenal edema, and even death have beenreported as consequences of Ca oxalate ingestion (BLACK, 1918; KINGSBURY, 1964;BUCK et al., 1966; FRANCESCHI & HORNER, 1980). Despite evidence of their value asfeeding deterrents against vertebrate herbivores, few studies addressed the influenceof crystals on insect herbivore feeding, and nutritional ecology .Cicadellids (Homoptera,Cicadellidae) and tingids (Hemiptera, Tingidae) choose to feed on larger leaves thatalso have low levels of calcium oxalate crystals of the tropical tree Tabebuia ochracea(Bignoniaceae) (RIBEIRO et al., 1994). Interestingly, new findings in a study of plantgalls produced by insects indicate that crystals may be very commom on the modifiedtissues of the galls (FERNANDES et al. , 1990) .N evertheless, the function of these crystalsremain to be investigated.

Silica bodies have also influenced herbivore feeding.McNAUGHTON & T ARRANTS(1983) argued that silicification in grass leaves is an effective barrier against herbivoryand that ultimately sialification of grass leaves contributed to the adaptive radiation ofthe grazing marnmal fauna.

A consensus on the adaptive value of plant crystalline structures against insectherbivory cannot be stated at present. Relevant work should be perfonned on thegrowth and dynamics of these crystals and their effectiveness against the several insectherbivore taxa known to feed on crystal producing plants. Other important questionsshould be addressed such as: do plants secreting calcium oxalate support an impoverishedherbivore fauna compared to non-calcium oxalate.secreting plants ? How do calciumoxalate levels correlate with herbivore density and plant damage ? Are plant calciumoxalate feeding herbivores more specialized than herbivores not feeding on calciumoxalate ?

Nevertheless, we are again faced with multi-functional values of a plant trait.Various functions have been attributed to plant Ca oxalate crystals. Most studies relatethem to ionic balance, storage (under calcium stress), or structural support (seeFRANCESCHI & HORNER, 1980 for a review). Studies on their differential efficacy againstvertebrate and invertebrate herbivores would also be very valuable, especially in casewhere both herbivore types feed on the same plant species.

LatexWhen injured, many plants, such as Euphorbiaceae, Apocynaceae,

Asclepiadaceae, and some Asteraceae, exude latex. In general, latex can be describedas an aqueous suspension of serveral types of particles originated from living cells,which include different kinds of rubbers, essential oils, and resins (LEWINSOHN, 1991).Latex production is widespread among plant families (40 families) (METCALF, 1967;LEWINSOHN, 1991) and recognized for their effectiveness in defense against herbivores

.Revt" h"", Fnt ~R(2\ 1QQ4

427PLANT MECHANICAL DEFENSES

(e.g., JANZEN, 1985). More latex-producing plants are found in the tropics than in thetemperate region, and LEWINSOHN ( 1991) argued that this difference is due to the higherherbivory rates found in tropical plants.

Latex is very effective against most generalist mining, boring, and chewinginsectherbivores (e.g., JANZEN, 1985). Evenifthe herbivorecansurvive themechanicaleffect of latex, it may be killed by insecticidal chemicals present in the latex (JANZEN,1985). However, some insects evolved ways to circumvent this defense type (e.g.JAMES, 1887; COMPTON, 1987; DUSSOURD & EISNER, 1987; DussouRD, 1990). The plantCnidoscolus urens (Euphorbiaceae) is protected frominsectherbivores by a combinationof urticating hairs and sticky latex. However, Erinnyis ello larvae (a generalistsphingid moth, Lepidoptera) completely avoid plant defenses by grazing the hairsfrom the leaf petiole, and then constricting the petiole (DILLON et al., 1983). Thiseffectively stops latex flow into the leaf. Despite the antiherbivore properties of latexin several tropical plant families, many gal1ing insect species accumulated on them(see FERNANDES, 1992). For instance, no latex is observed in the nutritive tissue of gal1son leaves of the Euphorbiaceae (Manihot esculenta, Sapium biglandulosum), andApocynaceae (Aspidosperma australis) (see FERNANDES et al., 1988). Nevertheless,plant latex may have other adaptive values other than to entrap and kil1 plant enemies.Studies are needed of within species distribution of latex, seasonal variation, and latexquality and quantity, and effectiveness against generalist and specialist insect herbivoresas wel1 as on adaptations to the physical environment.

Waxes and ResinsMany plants exude waxes, resinous, muscilaginous, and other sticky materials

that may contribute to defense against insect herbivores (RHOADES, 1977). Severalplants of arid regions have waxy and/or resinous surfaces which .are believed to beadaptations to harsh environments. For instance, leaf wax and resin productionincreases the reflection of solar radiation (DELL, 1977). Larrea tridentata(Zygophylaceae) resin serves as an antidessicant, solar radiation filter, and also as aherbivore deterrent (RHOADES 1977). Several species of Baccharis (Asteraceae) thatinhabit harsh environments have sticky leaf resinS (G.W. FERNANDES, pers. observ.).Nonetheless, the richness and abundance of gal1-forming insects is similar on B.concinna (high resin production) and B. dracunculifolia (low resin production) inBrazil. Befaria racemosa (Ericaceae) buds, abaxial surface of petals, and developingfruits are coated with a viscous adhesive material that trap several insect species(SMALL, 1930; EISNER & ANESHANSLEY, 1983). KERNER (1878) reported onseveral stickysubstances on flowers and their effects on insect herbivores. Aciurina trixa (Diptera,Tephritidae) gal1s on Chrysothamnus nauseosus hololeucus (Asteraceae) have stickysecretions on the walls which trap and kil1 host plant aphids and some predatory antsthat attack the gal1-forming larva (FERNANDES & PRICE 1994).

Resin is known to play an important role in defense against insect herbivory .Ecological literature contains numerous references to the "pitching out" of barkbeetles by a copious flow of resin (VITÉ & WOOD, 1961; WOOD, 1962; STARK, 1965;RAFFA & BERRYMAN, 1982). Success of western pine beetle on ponderosa pinedecreased as resin flow increased (SMITH 1966, 1969, 1972). Resin production ispositively associated with plant water availability in pine trees (MERKER, 1967; SMITH,1972). Resin pr6duction by Chrysothamnus nauseosus (Asteraceae) inhibits feeding

RevIa bras. Ent. 38(2), 1994

.

~

428 FERNANDES

by the third instar Colorado potato beetle larvae (ROSE, 1980). The xylem resin in thisplant invades the gal1s formed by Aciurina trixa kil1ing its larva (FERNANDES & PRICE,1992), and is the most relevant mortality factor in some populations. Resin productionwas also found to be a feeding deterrent against aphids (ROSE et al., 1981). The larvaldevelopmental time ofNeodiprion sertifer(Hymenoptera, Diprionidae) is significantlylonger for larvae that were fed on Pinus silvestris (Pinaceae) needles high in resin acids(LARSSON et al., 1986). In addition, larvae fed needles high in resin acids sufferedsignificantly high mortality during the f1fSt larval instars. Nevertheless, late larvalinstars preferred and searched for high resin acid plant tissues. This apparent paradoxis explained by the fact that resin acids are used by the larvae for defense againstpredators (EISNER et al., 1974). Although resins are wel1 known among members thePinaceae, they are uncommon in flowering plants. The relatively few species knownto produce resins are predominantly xerophitic (McLAUGHLIN & HOFFMANN, 1982;HOFFMANN et al., 1983).

An altemative hypothesis to the anti-herbivore properties of waxes and resinsis that they represent a phytochemical adaptation to harsh environments. More work,is however, necessary on insect deterrence and trapping by plant waxes and resins, theirdistribution and physiological value to establish their effectiveness against insectherbivores. Studies of wax and resin production in tropical plants are rare and thoserelated to its effectiveness against herbivory poorly developed.

SUMMARY AND CONCLUSIONS

Mechanical defenses lessen the impact herbivores have on plant's fitness. Plantmechanical defenses act negatively on herbivores, diminishing their larval and adultperformance. Nevertheless, clear cut examples on the evolution of plant mechanicaltraits in response to herbivores are rare (but see GILBERT, 1975; BENSON et al., 1976).Generally, a plant character may present two or more roles at least in some phase ofa plant's life history .I discussed a few cases where pubescence, tissue texture, crystals,latex, waxes and resins are effective against insect herbivores. A review on the plantphysiology associated with these plant traits would convince the audience equally oftheir role in the plant's physiology and survival in different environments andcircumstances. From this brief list of studies, we can observe that there is a lack ofhypotheses testing on the primary role of plant mechanical traits. Few experimentshave performed tests on the role of plant traits for protection against herbivoresandplant physiology simultaneously (e.g., WOODMAN & FERNANDES, 1991). While manystudies have been performed on the evolution of plant chemistry against herbivores(e.g., EHRLICH & RAVEN, 1964; GILBERT, 1975; SPENCER, 1988), very few studies havefocused on the evolution of plant mechanical traits in response to herbivore pressure(see JUNIPER & SOUTHWOOD, 1986). These are challenging and open areas for studies.

Plant mechanical defe'nses against herbivores should be more studied in thetropical regions. The chances to unravel and highlight new mechanisms and patternsin plant defense against herbivores are enormous. Therecare few solid and well studiedtropical systems. Just to cite a few interesting open avenues, it may be seen that in harshenvironments many plant traits are adaptive against herbivores, such as resins, waxes,and sclerophyllous leaves.lfharsh environment plants are indeed well defended, whathas this rendered to them in ecological and evolutionary time ? On what is the surplus

RevIa bras. Ent. 38(2). 1994

.

429PLANT MECHANICAL DEFENSES

of energy expended on ? Do they have different sorts of herbivore communities ?Tropical savanna plants may well fit the descriptions but are seldom studied. Thediversity of tropical systems and their evolutionary history make them interestingsystems to be studied. The primary goal of this mini-review will have been met if morestudents persue and bring to light more studies in tropical plant defense mechanismsagainst herbivores.

Acknowledgments. Ithank P.W. Price, J.A. Waquil, and two anonymous reviewers for theircomrnents on the manuscript. I also have benefited with discussions with my pastand present students. Thiswork was supported by CNPq grants (30.0728/91-3,52.0970/93-4, 401.771191-1), FAPEMIG (078/91), and

PRPqfVFMG.

REFERENCES

BAKKER, H.J.; E.L.GHISALBERn & P.R. JEFFEREIES. 1972. Biosynthesis of diterpenes in Beyeria leschenaltii.Phytochem.11: 2221-2231.

BECERRA, J. & E. EZCURRA. 1986. Glandular hairs in theArbutus xalapensis complex in relation to herbivory .Amer. J. Bot. 73: 1427-1430.

BENSON, W.W.; K.S. BROWN & L.W. GILBERT. 1976. Coevolution ofplants and herbivores: passion flowerbutterflies. Evolution 29: 659-680.

BICALHO,J.A. & G. W. FERNANDES. 1994. Herbivoria porinsetosemChamaechristaorbiculata (Leguminosae):o papel de tricomas glandulares na defesa. Revta bras. Ent. (submetido).

BLACK, O.F. 1918. Calcium oxalate in the Dasheen. Amer. J. Bot. 5: 447-451.BROERSMA, D.B.; R.L. Bemard & W.H. Luckmann. 1972. Some effects ofsoybean pubescenceon populations

of the potato leafllopper. J. Econ. Ent. 65: 78-82.Buck, W.B.; K.S. Preston, M. Abel & V.L. Marshall. 1966. Perirenal edema in swine: a disease caused by

comrnon weeds. J. Amer. Vet. Ass.148: 1525-1531.BUHR, H.; R. TOBALL & K. SCHREIBER. 1958. Die wirkung von einigen pflanzenlichen sonderstoffen,

inbesondere von alkaloiden, auf der entwick1ungen der larven des kartoffelkafers (Leptinotarsadecemlineata Say). Entomol. Exper. Appl. 1: 209-224.

CALLAHAN, P.S. 1957. Oviposition response ofthe com earworm to differences in surface texture. J. Kan.Entomol. Soc. 30: 59-63.

CmANG, H.S. & D.M. NORRIS. 1983. Morpho1ogical and physiological pararneters of soybean resistance toagromyzid bean flies. Environ. Entomol. 12: 260-265.

CLAUSEN, J.D.; D. KECK & W.M. HEISEY. 1940. Experimental studies on the nature ofspecies. 1. Effects ofvaried environments on western north American plants. Washington, D.C., Camegie Institute ofWashington # 520.

Coley, P.D. 1983. Herbivory and defensive characteristics oftree species in a 1owland tropical forest. Ecol.Monogr. 53: 209-233.

COMPrON, S.G. 1987 .Aganais speciosa andDanaus ch/}'sippus (Lepidoptera) sabotage the 1atex defenses oftheir host plants. Ecol. Entomol. 12: 115-118.

COULSON, R.N. & J.A. WITrER. 1984. Forest entomology. NewYork, Wiley.CRAIG, T.P.; J.K ITAMI & P.W. PRICE. 1990. The window ofvu1nerability of a shoot-galling sawfly to attack

by a parasitoid. Ecology 71: 1471-1482.CROTEAU, R. & M.A. JOHNSON. 1984. Biosynthesis of terpenoids in glandular trichomes, p. 133-185. 1n: E.

Rodriguez, P.L. Healy & I. Mehta (eds) Biology and chemist/}' ofplant trichomes. New York, Plenum.DAWSON, R.M.; M. W. JARSUS; P .R. JEFFERIES; T .G. PAYNE& R.S. ROSICH. 1966. Acidic constituentsofDodonea

lobulata. Aust. J. Chem. 19: 21-22.DE CANDOLE, A.P. 1841. Vegetable organography: or, an analytical description of the organs of plants

(translated by Boughton Kingdom). v. I., London, Houlston & Stoneman.DELL, B. 1977. Distribution and function of resins and glandular hairs in westem Australian plants. J.R. Soc.

WestAust.59: 199-123.DELL, B. &A.J. MCCOMB. 1975. Glandular hairs, resin production, andhabitatofNewscatelia viscida E. Pritzel

(Dicrastylidaceae). Aust. J. Bot. 23: 373-390.DILLON, P.M.; S. LoWRIE&D. McKEY. 1983. Disanningthe ..Evil Woman": petioleconstriction by asphingid

larva circumventsmechanical defenses of itshostplants, Cnidoscolus urens (Euphorbiaceae ).Biotropica15: 112-116.

.

hra." Ent 3812).1994

DussouRD, D.E. 1990. The vein drain; or, how insects outsmart plants. Nat. Hist. 90: 44-49.DussouRD, D.E. & T. EISNER, 1987. Vein-cutting behavior: insect counterploy to the latex defenses ofplants.

Science 237: 898-901. .

EHRUCH, P.R. & P.H. RAVEN. 1964. Butterflies and plants: a study of co-evolution. Evolution 18: 586-608.EISNER, T. 1964. Catnip: its raison d'etré. Science 146: 1318-1320.EISNER, T. & D.J. ANEsHANSLEY. 1983. Adhesive strength ofthe insect-trapping glue of a plant (Befaria

racemosa). Ann. Entomol. Soc. Amer. 76: 295-298.EISNER, T.; J.S. JOHNESSEE & J. CARREL. 1974. Defensive use by an insect ofa plant resin. Science 184: 996-

999.ESAU, K. 1965. Plantanatomy. NewYork, Wiley.EzcURRA, E.; J.C. GOMEZ & J. BECERRA. 1987. Diverging patterns of host use by phytophagous insects in

relation to leafpubescence inArbutus xalapensis (Ericaceae). Oecologia 72: 479-480.FERNANDES, G .W .1987. Gall forming insects: their economic importance and control.Revta bras. Ent. 31: 379-

.'no

.1992. Plant historical and biogeographical effects oninsular gall-fonning species richness.Lets.Gbl. Ecol. Biogeogr. 2: 71-74.

FERNANDES, G.W. & P.W. PRlCE. 1988. Biogeographical gradients in galling species richness: tests ofhypotbeses. ecologia 76: 161-167.

.1991. Comparisonsoftropical and temperate galling species richness: tberoles of environrnentalharshnessand plantnutrientstatus,p. 91-115In: P.W. Price, T.M. Lewinshon, G.W. Femandes& W. W.Benson (eds)Plant-animal interactions: evolutionaryecology in tropical and temperatureregions. NewYork, Wiley.

-.1992. The adaptive significance of insect gall distribution: survivorship of species in xeric andmesic habitats. Oecologia 90: 14-20.

.1994. Life history , courtship, and mating behavior of a gall-forming tephritid, Aciurina trixa,on Chrysothamnus nauseosus hololeucus in nortbem Arizona. Proc. Entomol. Soc. Wash. (in press).

FERNANDES, G. W.; R.P. MAR11NS &E. TAMEIRAoNETO. 1987. Food weJjrelationshipinvolvingAnadiplosissp.galls (Diptera: Cecidomyiidae) on Machaerium aculeatum (Leguminosae). Revta bras Bot. 10: 117-123.

FERNANDES, G.W.; E. TAMEIRAO NETO & R.P. MAR11NS. 1988. Ocorrência e caracterização de ga1hasentomógenas na vegetação do Campus-pampulha, UFMG, Belo Horizonte -MG. Revta bras. Zool. 5:11-29.

FERNANDES, G.W; R.W. PRESZLER & T.N. GRIM. 1990. The occurrence of crystals in a cynipid leaf gall onQuercus turbinella. Beitr. Biol. Pflanz. 65: 377-383.

Fox, L.R. 1981. Defense and dynamics in plant-herbivore systerns. Amer. Zool. 21: 853-864.FRANCESCHI, V.R. & H.T. HORNER. 1980. Calcium oxalate crystals in plants. Bot. Rev. 46: 361-427.GIBSON, R. W .1971. Glandular hairs providing resistance to aphids in certain wild potato species. Ann. Appl.Biol. 68: 113-U9. .

.1974. Aphid-trapping glandular hairs on hybrids of Solanum tuberosum and S. berthaultii.Potato Res. 17: 152-154.

.1976a. Glandular hairs are a possible means of limiting aphid damage to tbe potato crop.Ann.Appl. Biol. 82: 143-146.

.1976b. Glandu1ar hairs onSolanum polyadenium lessen damage by tbe colorado potato beetle.Ann. Appl. Biol. 82: 147-150.

.1976c. Trapping oftbe spidermite, Tetranychus urticae by glandu1arhairs on tbe wild potatoSolanum berthaultii. Potato Res. 19: 179-182.

GIBSON, R.W. & R.H. TuRNER. 1977.Insect-trapping hairs on potato plants. PANS 22: 272-277.GILBERT, L.E. 1971. Butterfly-plant coevolution: has Passiflora adenopoda won tbe selectional race witb

heliconiine butterflies ? Science 172: 585-586..1975. Ecological consequences of a coevolved mutualism between butterflies and plants, p.

108-240 In: Gilbert, L.E. & P .H. Raven ( eds) Coevolution of animals and plants. Austin, University ofTexas.

GROSS, P. & P.W. PRICE. 1988. Plant influences on parasitism oftwo leafminers: a test of enemy-free space.Ecology 69: 1506-1516.

GRUBB, P .J .1986. Sclerophylls, pachyphylls and pycnophylls: tbenature andsignificance ofhard leaf surfaces,p. 137 -150 In: Juniper, B.E. & T .R.E. Soutbwood ( eds.) Insects and the plant surface. London, EdwardAmold.

.

00", ,~.

PLANT MECHANICAL DEFENSES 431

HARLEY, J.L.S. & A.J. THORSTEINSON. 1967. The influence of plant chemicals on the feeding behavior,development and survival of the two-striped grasshopper, Melanopus bivittus (Say), Acrididae:Orthoptera. Can. J. Zool. 45: 305-318.

HERMS, D.A. & W.J. MATrSON. 1992. Thedilemaofplants: to growordefend.Quart. Rev. Biol. 67: 283-335.HESLOP-HARRISON, Y. 1976. Carnivorous plants a century after Darwin. Endeavour 35: 114-122.HOFFMANN,J.F.; B.E. KINGSOLVER; S.P. McLAUGHLIN &B.N. TIMMERMANN. 1983. Productionofresins by aric-

adapted Astereae, p. 251-271 In: B.N. Timmermann, C. Steelink & F.A. Loewus (eds.) Phytochemical

adaptations to stress. New York, Plenum.HULLEY, P.E. 1988. Caterpillar attacks plant chernical defense by mowing trichomes before feeding. Ecol.

Entomol. 13: 239-241.IsHlKAWA, S. & T. HIRAO. 1966. Studieson theolfactorysensationsinthelarvaeofthesilkworm,Bombyx mori.

(III). Attractants and repellents ofhatched larvae. Bull. Sericul. Exper. St. (Japan) 20: 291-321.JAMES, J.F. 1887. The milkweeds.Amer. Natur. 21: 605-615.JANZEN, D.H. 1985. Plant defenses against animaIs in the Amazonianrainforest, p. 207-217 In: G.T. Prance

& T.E. Lovejoy (eds.)Key environments: Amazonia. Oxford, PergaI1lon.JOEL, D.M. 1986. Glandular structures incamivorous plants: their role in mutual and unilateral exploitation

ofinsects,p. 219-234In: Juniper, B. & T.R.E. Southwood (eds.)Insectsandthe plantsurface. London,Edward Amold.

JOHNSON, H.B. 1975. Plant pubescence -an ecological perspective. Bot. Rev. 41: 233-258.JOHNSON, W.T. & H.H. LYON. 1976.1nsects thatfeed on trees and shrubs. New York, Comell University.JUNIPER,B. 1986. Thepathtoplantcamivory,p. 195-218In: Juniper,B& T.R.E. Southwood(eds.)lnsectsand

the plant surface. London, Edward Amold.JUNIPER, B. & T .R.E. Southwood. 1986.1nsects and the plant surface. London, Edward Amold.JUNIPER, R.E.; R.J. Robins & D.M. Joel. 1989. The carnivorous plants. New York, Acadernic.KELSEY, R.G.; G.W. REYNOLDS & E. RODRIGUEZ. 1984. The chemistry of biologically active constituents

secreted and stored in plant glandular trichomes, p. 187-241 /fI: Rodriguez, E., P.L. Healey & I. Mehta(eds.) Biology and chemistry ofplant trichomes. New York, Plenum.

KELSEY, R.G. & F. SHAFIZADEH. 1980. Glandular trichomes and sesquiterpene lactones of Artemisia nova(Asteraceae). Biochem. Syst. Ecol. 8: 371-377.

KERNER, A. 1878. Flowers and their unbidden guests. London, Kegan Paul.KINGSBURY, J .M. 1964. Poisonous plants of the United States and Canada. New Jersey, Prentice-Hall.LAMPERT, E.P.; D.L. HAYNES; A.J. SAWYER; D.P. JOKINEN; G.G. WELLSO, R.L. GALLUM & J.J. ROBERTS. 1983.

Effects of regional releases of resistant wheats on the population dynamics of the cerealleaf beetle(Coleoptera: Chrysomelidae). Ann. Entomol. Soc. Amer. 76: 972-980.

LARSSON, S.; C. BJORKMAN & R. GREF. 1986. Responses of Neodiprion sertifer (Hym., Dirpionidae) larvae tovariation in needle resin acid concentration in Scots pine. Oecologia 70: 77-84.

LEVIN, D.A. 1973. The role oftrichomes in plant defense. Quart. Rev. Biol. 48: 3-15.LEWINSOHN, T.M. 1991. The geographical distribution of plant latex. Chemoecol. 2: 64-68.LoVELESS, A.R. 1961. A nutritional interpretation of sclerophylly based on differences in the chernical

composition of sclerophyllous and mesophytic leaves. Ann. Bot. 25: 168-184.--.1962.FurtherevidencetosupportanutritionalinterpretationofsclerophyllyAnn. Bot. 26: 551-

561.LUKEFAHR, M.J.; C.B. COWAN &J.G. HouGHTALING. 1970. Fieldevaluationsofimprovedcottonstrainsresistant

to the cotton fleahopper. J. Econ. Entomol. 63: 1101-1103.MATrSON, W.J.; J. LEVIEUX & C. BERNARD-DAGAN. 1988. (eds). Mechanisms ofwoody plant defenses against

insects -Searchfor pattern. New York, Springer.McLAUGHLIN, S.P. &J.J. HoFFMANN. 1982. Survey ofbiocrude-producingplantsfrom thesouthwest.Econ. Bot.

36: 323-339.McNAUGHTON, S.J. & J.L. TARRANTS. 1983. Grass leafsilicification: naturalselectionforan inducible defense

against herbivores. Proc. Natl. Acad. Sci. 80: 790-791.MEDINA, E. 1983. Adaptations oftropical trees tomoisturestress, p. 225-2371n: F.B. Golley (ed.)Tropical rain

forest ecosystems; A, Structure andfunction. Arnsterdam, Elsevier.MEDINA, E.; M. SOBRADO & R. HERRERA. 1978. Significance of leaf orientation for leaf temperature in an

Amazoniam sclerophyll vegetation. Rad. Environ. Bioph. 15: 131-140.MERKER, E. 1967. Inducing increased resistance against bark beetle. Algemar. Forst-u. Jagdztg. 138: 13-24.METCALF, C.R. 1967. Distribution of latex in the plant kingdom. Econ. Bot. 21: 115-127.NIELSEN, M.T.; G.A. JONES & G.B. COLLINGS. 1982. Inheritance pattem for secreting and nonsecreting

glandular trichomes in tabacco Nicotiana tabacum. Crop. Sci. 22: 1051-1053.

.

RevIa bras. Ent. 38(2), 1994

"432 FERNANDES

OKALI, D.U.U. 1977. Tissue water relations ofsome woody species at the Accra Plains, Ghana. J. Ecol. 59:89-101.

PILLEMER, E.A. & W.M. TINGEY. 1976. Hooked trichomes: a physical plantbarriertoamajor agricultural pest.Science 193: 482-484.

PiLLEMER, E.A. & W .M. TiNGEY. 1978. Hooked trichomes and resitance of Phaseolus vulgaris to Empoascafabae (Harris). Entomol. Exper. Appl. 24: 83-94.

PiMENTEL, D. 1981. Handbookofpest management in agriculture. (ed.) Boca Raton, CRC.Poos, F.W. & F.F. SMITH. 1931. A comparison ofovipositionandninphal development of Empoascafabae

(Harris) on different host plants. J.. Econ. Entomol. 24: 361-370.PRICE, P.W. 1984.1nsect Ecology. Second edition. New York, Wiley.RAFFA, K.F. & A.A. BERRYMAN. 1982. Physiological differences between lodgepole pines resistant and

susceptible to the mountain pine beetle and associatedrnicroorganisms.Environ. Entomol. 11: 486-492.RATHCKE, B.J. & R.W. POOLE. 1975. Coevolutionary race continues: butterfly larval adaptation to p1ant

trichomes. Science 187: 175-176.REYNOLDS, G.W. & E. RODRIGUEZ. 1986. Dermatotoxic pheno1ics from glandular trichomes of Phacelia

campanulariaandP.pedicellata. Phytochem. 25: 1617-1619.RHOADES, D.F. Integrated antiherbivore, antidesiccant and ultraviolet screening properties of creosotebush

resin. Biochem. Syst. Ecol. 5: 281-290.RIBEIRO, S.P.; H.R. PiMENTA& G. W .FERNANDES. 1994. Herbivory by chewing andsuckinginsectsonTabebuia

ochracea. Biotropica (in press).RlCHARDSON, H.H. 1943. The action of bean leaves against the bedbug. J. Econ. Entomol. 36: 543-545.ROBERTS, J.J.; R.L. GALLUM; F.L. PATTERSON & J.E. FOSTER. 1979. Effects of wheat leaf pubescence on the

Hessian fly.J. Econ. Entomol. 72: 211-214.

RODRIGUEZ, E.; P.L. HEALEY &1. MEHTA. 1984.Biologyandchemistryofplanttrichomes. New York, Plenum.ROSE, A. 1980. Grindelane diterpenoids from Chrysothamnus nauseosus. Phytochem. 19: 2689-2693.ROSE, A.; K. JONES; W. HADDON & D. DREYER. 1981. Grinde1ane diterpenoid acids from Grindelia humilis:

feeding deterrency of diterpen acids toward aphids. Phytochem. 20: 2249-2253.RosENTHAL, G.A. & D.H. JANZEN. 1979. Herbivores: their interaction with secondary plant metabolites. New

York, Academic.DE SANTIS,l. & G.W. FERNANDES. 1989. Brazi1ian parasitoids of gall-forming insects: two new cha1cidoid

species and host records. Entomol. News 100: 29-36.SCHOENER, T. W .1988. Leaf damage inisland buttonwood,Conocarpuserectus: correlations with pubescence,

island area, isolation and the distribution of major camivores. Oikos 53: 253-266.SEIGLER, D. & P. W. PRICE. 1976. Secondary compounds inp1ants: primary functions.Amer. Natur. 110: 101-

105.SMALL, J.K. 1930. Befaria racemosa: tar-flower. Addisonia 15: 21-22.SMiTH, R.H. 1966. Resin qua1ity as a factor in resistance to bark beetle, p. 189-1961n: H.D. Gerhold, R.E.

McDermott, E.J. Shreiner & J.A. Winieski (eds.) Breeding pest-resistant trees. Oxford, Pergamon..1969. Xylem resin as a factor in theresistance ofpines to forced attacks by bark beetles.Second

World Consultation Forest Tree Breeding Proceedings. FO-FTB- 69-5/6, 13p..1972. Xylem resin in the resistance of the pinaceae to bark beetles. USDA Forest Service

General Techinical Report PSW-1, 7p.SOGAWA, K. 1982. The rice brown ricehopper: feeding physiology and host plant interactions. Ann. Rev.

Entomol. 27: 49-73.SOLEREDER, H. 1908. Systematic anatomy of the dicotyledons (translated by Boudle & Fritsch). Oxford,

Claredon.SOUTHWOOD, T.R.E.1986.Plantsurfacesandinsects-anoverview,p.1-221n: Juniper,B.&T.R.E. Southwood

(eds.) 1nsects and the plant surface. London, Edward Arnold.SPENCER, K.C. 1988. Chemical mediation of coevolution. (ed.). New York, Acadernic.STARK, R.W. 1965. Recent trends in forest entomology.Ann. Rev. Entomol. 10: 303-324.STEPHENS, S.G. 1959. Laboratory studies offeeding oviposition preferences of Anthonomus grandisBoh. J.

Econ. Entomol. 52: 390-396.STEPHENS, S.G. &H.S. LEE. 1961. Furtherstudieson thefeedingandovipositionpreferenceofthe boll weevil

(Anthonomus grandis). J. Econ. Entomol. 54: 1085-1090.STOBER, J.P. 1917. A comparative study ofwinter and summer leaves ofvarious herbs. Bot. Gaz. 63: 89-109.STRONG, D.R.; J.H. LAWTON & T.R.E. SOUTHWOOD. 1984. lnsects on plants. Community patterns and

mechanisms. Massachussets, Harvard University.

RevIa bras. Ent. 38(2). 1994

.

PLANT MECHANICAL DEFENSES 433

TAYLOR, N.L. 1956. Pubescence inheritance and 1eafl1opper resistance relationslúps in alfalfa. Agron. Jour.

48: 78-81.THOMPSON, J.N. 1981. Reversed anirnal-plant interactions: the evolution of insetivorous and ant-fed plants.

Biol. J. Linn. Soc. 16: 147-155..1988. Evolutionary ecology of the relationship between oviposition preference of offspring

phytophagous insects. Entomol. Exper. Appl. 47: 3-14.TINGEY, W.M. & R.W. GIBSON. 1978. Feeding and mobility ofthe potato leafl1opper impaired by glandu1ar

trichomes of Solanum berthaultii and S. polyadenium. J. Econ. Entomol. 71: 856-858.TURNER, J.C.; J.K. HEMPHILL & P.G. MAHLBERG. 1977. Gland distribution and cannabinoid content in clones

of Cannabis sativa L. Amer. J. Bot. 64: 687-1978. Quantitative determination of cannabinoids in individual trichomes ofCannabis sativa L.

(Cannabaceae). Amer. J. Bot. 65: 1103-UPHOLF, J.C. 1962. Plant hairs. Berlin, Gebriider Bontrãeger.V AN DUYN, J. W .; S.G. TURNIPSEED & H.D. MAXWELL. 1972. Resistance insoybeans tothe Mexican bean beetle.

II. Reactions ofthe beetle to resistant plants. Crop Sci. 12: 561-562.VITÉ,J.P. & D.L. WooD.1961. Astudyoftheapplicabilityofthemeasurementofoleoresinexudationpressure

in determining susceptibility of second-growth ponderosa pine to bark beetle infestation. Contr. BoyceThomps.1nst. 21: 67-78.

W ALKER, G.P. 1985. Stylet penetration by the bayberry whitefly, as affected by leafageinlemon,Citrus limon.Entomol. Exper. Appl. 39: 115-121.

.1987. Probing andovipositionbehaviorofthe bayberry wlútefly (Homoptera: Aleyrodidae) onyoung and mature lemon leaves. Ann. Entomol. Soc. Amer. 80: 524-529.

.1988. The role of leaf cuticle in leaf age preference by bayberry wlútefly (Homoptera:Aleyrodidae) on lemoIL Ann. Entomol. Soc. Amer. 81: 365-369.

W ALKER, G.P. & D.C.G. AITKEN. 1985. Oviposition and survival ofbayberry wlútefly, Parabemisia myricae(Homoptera: Aleyrodidae) on lemons as a function ofleaf ase. Environ. Entomol. 14: 254-257.

WARMING, E. 1909. Oecology ofplants: an introduction to the study ofplant communities. London, Oxford

University.WEBSTER, J .A. 1975. Association of plant hairs and insect resistance. An annotated bibliography .Miscel. Publ.1297, United St. Dep. Agric., 18 p. .

WHEELER,A.G. &C. W. SCHAEFER. 1982. Reviewofstilt bug (Herniptera: Berytidae) hostplants.Ann. Entomol.Soc. Amer. 75: 498-506.

WILLIAMS, S.E. 1976. Comparative sensory physiology of the Droseraceae: the evolution of a plant sensorysystem. Proc. Amer. Phyl. Soc. 120: 187-204.

WILLINSKY, M.D. 1973. Analytical aspects to Cannabis chernistry, p. 137-165 In: Mechou1am, R. (ed.)Marijuana: Chemistry, pharmacology, metabolism and clinical effects. New York, Academic.

WOLLENWEBER, E. 1984. Thesysternatic irnplicationofflavonoidessecreted byplants,p. 53-69 In: Rodriguez,E., P.L. Healey & I. Mehta (eds.) Biology and chemistry ofplant trichomes. New York, Plenum.

WOOD, D.L. 1962. Experiments on the interrelationslúps between oleoresin exudation pressure in Pinusponderosa and attack by Ips confusus (LeC). Can. Entomol. 94: 473-477.

WOODMAN, R.L. & G.W. FERNANDES. 1991. Differential mechanical defense: herbivory, evapotranspiration,and leafhairs. Oikos 60: 11-19.

WUENSCHER, J.E. 1970. The effect ofleafhairs of Verbascum thapsus on leaf energy exchange. New Phytol.69: 65-73.

Y APP, R.H. 1912. Spircaeaulmaria and its bearing on the problem of xeromorphy in marsh plants. Ann. Bot.26: 815-870.

Received 22.01.1992; accepted 30.03.1994.

RevIa bras. Ent. 38(2), 1994.