Southwestern Association of Naturalists

Variable Budbreak and Folivory of Gambel Oak (Quercus gambelii: ) Author(s): Stanley H. Faeth and Robert F. Rooney, III Source: The Southwestern Naturalist, Vol. 38, No. 1 (Mar., 1993), pp. 1-8 Published by: Southwestern Association of Naturalists Stable URL: http://www.jstor.org/stable/3671636 Accessed: 07/05/2010 20:37

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http://www.jstor.org THE SOUTHWESTERN NATURALIST 38(1):1-838(1): 1 -8 MARCH 1993

VARIABLE BUDBREAK AND INSECT FOLIVORY OF GAMBEL OAK (QUERCUS GAMBELH: FAGACEAE)

STANLEY H. FAETH AND ROBERT F. ROONEY, III

Department of Zoology, State University, Tempe, Arizona 85287-1501

ABSTRACT-Budbreakof individualramets of clonal Gambeloak (Quercusgambelii: Fagaceae) was advancedexperimentally to test the effects of altered timing of budbreakand hence, age, on patternsof folivory.Early-season folivory by leaf-chewinginsects was significantlygreater on younger of controlramets than older leaves of experimentalramets. However, differences in cumulative folivory between control and experimentalramets disappearedby the end of the growing season. Colonization by three species of late-season leafminers was also unaffected by altered budbreak, indicatingthe impact of altered budbreakon folivoresis concentratedearly in the growing season. Analyses of nutritionaland allelochemicalcontent of experimentaland controlramets correspond to the patternsof folivory;leaves of experimentalramets were significantlyhigher in gallotannincontent than leaves of controlramets, but these differencesalso waned by the middle of the growing season. Our resultssuggest that variablebudbreak can alter degreeof folivoryon Gambeloak, but only early in the growing season.The evolutionaryimplications of, and constraintson, variationin budbreakin woody are discussed.

Many folivorous insect species that feed on trition, and morphology (Haukioja et al., 1985; or semi-evergreen prefer and per- Tuomi et al., 1989). Despite the potential of vari- form better on younger leaves than old ones (e.g., able budbreak in altering folivore abundances on Feeny, 1970; Rockwood, 1974; Schweitzer, 1979; trees, relatively few studies of herbivore- in- Cates, 1980; Rauscher, 1981; Kraft and Denno, teractions have focused on this plant trait. Those 1982; Coley, 1980; Niemela and Haukioja, 1982; studies that have, have produced conflicting re- Niemela et al., 1982; Fowler and Lawton, 1984). sults. Feeny (1976) concluded that early or late As leaves age, they change in surface area, water flushing oaks harbor fewer than the pop- content, toughness, thickness, chemical compo- ulation in general. Defoliated branches of moun- sition and nutritional quality (Feeny, 1970; tain birch (Betula pubescens ssp. tortuosa) break Crawley, 1983; Raupp and Denno, 1983; Coley, bud later in the following year, and Tuomi et al. 1980; Faeth, 1985a). Therefore, the synchrony (1989) hypothesized that these branches should between budbreak of host trees and folivore emer- have less herbivory than branches that flush leaves gence from overwintering stages is critical to foli- earlier. Similarly, late breaking holly oaks (Quer- vore success. Insects that emerge too early may cus ilex) had less herbivory from the folivore Tor- starve (Futuyma and Wasserman, 1980; Hunter, trix viridana than early breaking trees (Du Merle, 1990), while insects that emerge too late may 1988). In contrast, experimentally retarded, encounter a suboptimal food source (Embree, younger foliage of Betula pubescens had more her- 1965; Feeny, 1970, 1976). bivory than older, control foliage (Fowler and Variation in timing of budbreak often occurs Lawton, 1984). Also, tropical plants with late, within populations of trees. For example, pedun- asynchronous leaf flush typically have higher rates culate oak (Quercus robur) trees vary in timing of herbivory (Rockwood, 1974; Lieberman and of budbreak by as much as two weeks within a Lieberman, 1984; Aide, 1988). given locality (Feeny, 1970). Because timing of We tested the influence of variable budbreak budbreak is at least partly determined by genetic on folivory by advancing the timing of budbreak factors (Kramer and Kozlowski, 1979), variation experimentally within clones of Gambel's oak in time of budbreak has been considered a plant (Quercus gambelii Nutt.). Since spring folivores defense against folivores, similar to other variable generally prefer and perform better on younger plant characteristics such as allelochemistry, nu- leaves than older leaves, presumably because of 2 The Southwestern Naturalist vol. 38. no. 1

TABLE 1-Budbreak phenology of experimental (E) Typical leaf flush of Gambel's oak at Aztec Peak and control (C) ramets. occurs in late April to early May. Most leaves remain on trees until late September to early November. No leaf flush occurred on the dur- Expo- Differ- secondary study genets the course of this Most leaves abscise sure (E) (C) ence ing study. by mid-November, although some senesced leaves remain 1 N 16 April 30 April 14 days on the ramet until budbreak in the following spring. 1 S 16 April 30 April 14 days Gambel oak exists in clones (genets) composed of many 1 E 16 April 30 April 14 days individual shoots (ramets), connected to the same root 30 14 1 W 16 April April days system. By using clones, we could manipulate budbreak of adult trees in the while for 2 N 26 April 5 May 9 days field, controlling genetic treatment and control ramets in 2 S 30 April 5 May 5 days variability between to 2 E 26 April 5 May 9 days resistance folivory. To of Gambel's oak 2 W 26 April 5 May 9 days advance budbreak, four genets were selected on the basis of similar size (approxi- 3 N 30 15 May 15 days April mately 10 m in height and 10 m in diameter) and 3 S 30 15 May 15 days April exposure (level ground in full sunlight). All genets were 3 E 30 15 15 days April May apparently healthy and located within a 300-m radius. 3 W 30 15 15 days April May Clonal Gambel's oak in this area grows as large, dis- 4 N 26 April 12 May 16 days tinct genets composed of 10-50 ramets, which range 4 S 30 April 12 May 12 days from less than 1 m to over 10 m in height. Study genets 4 Eb were divided into four quadrants corresponding to the 4 W 26 April 12 May 16 days four cardinal compass points to account for variation in budbreak within clones due to different sun expo- a Mean difference in budbreak between experiment sure. One experimental and one control ramet were (E) and control (C) ramets = 12.8 ? 3.28 days. selected from the pool of ramets within quad- b Ramet 4EX was snow on 17 randomly destroyed by April, rants of 1.5-3 m in and not more 1988. approximately height than 2 m from the outermost ramets, giving a total of 16 control and 16 experimental ramets. lower amounts of allelochemicals and degree of On 29 March 1988, all experimental ramets were and amounts of nutrients (Feeny, toughness higher enclosed in 1 m x 2 m bags of 2.5 mm thick polyeth- we that older leaves 1970), predicted produced ylene to increase temperatures sufficiently to induce leaf flush should have lower rates of by early early budbreak. All enclosed and control ramets were folivory than control (normal budbreak) leaves. inspected twice weekly for time of budbreak. Bags were We monitored nutrition (protein) and allelo- removed from experimental ramets when the control chemistry (tannins) to determine phytochemical ramet from paired controls broke bud, so that exposure differences between advanced and control leaves time to folivores was equivalent on experimental and control ramets. The ramets broke bud an that might explain any differences in folivory. experimental of 12.8 earlier than the control We also examined the distribution of late-season average (+3.28) days ramets (Table 1). Some frost damage was recorded on leaf-mining insects to determine whether differ the experimental ramets of Trees 1 and 2 on 12 May, ences in the advanced leaves and experimental resulting in the loss of some leaves. A late snowstorm the control leaves for late-season younger persist on 17 April resulted in the loss of ramet 4EX due to folivores. breakage caused by accumulation of snow on the bag. Ramet 4EX was therefore treated as a missing value MATERIALS AND METHODS-Experiments and ob- in all statistical analyses. The frost damage to Trees 1 servations were conducted on clones of Gambel oak and 2 was ignored since loss of leaves was minimal. (Quercus gambelii) at Aztec Peak (2,225 m elevation), Leaves were scored for leaf-chewing insect damage Tonto National Forest, Gila County, Arizona, from on 29 May, 7 July, and 5 August 1988. All damage March 1988 to November 1988. The study site is an estimates were cumulative. For ramets with fewer than open canopy mixed woodland dominated by mixed oak 400 leaves, all leaves were examined for presence or (Quercusgambelii and Quercusarizonica), Arizona wal- absence of damage. Leaves on ramets with >400 leaves nut (Juglans major), ponderosa pine (), were sampled haphazardly until approximately 50- Douglas fir (Pseudotsuga taxifolia), and quaking aspen 75% of the leaves had been examined. Sucking insect (Populus tremuloides). Clearcutting of the study area damage was not included; we recognize that sucking in 1959 and subsequent regrowth of Gambel's oak has insects may be important herbivores, but estimation of resulted in genets with oldest ramets of approximately the impact of sucking insects was beyond the scope of uniform age, although rootstock age is unknown. this study. March 1993 Faeth and Rooney-Budbreakand insect folivory 3

Beginning on 26 September 1988, leaves about ready mond, California) to determine whether there were to abscise were collected from each ramet. Any leaf significant differences between treatments and among exhibiting a change in color was pulled lightly and trees. Condensed tannins were determined by using a collected only if it broke at the abscission zone. If the modified acidified vanillin method (Broadhurst and leaf could not be detached by light pressure then the Jones, 1978). Hydrolyzable tannin concentrations were leaf was left on the tree until the next biweekly sample. determined using a modified iodate technique (Bate- This process was repeated until all leaves were col- Smith, 1977) and are expressed as percent dry mass lected from each ramet. After each collection, leaves tannic acid equivalents (TAE) as compared to a tannic were taken to the lab, pressed and air dried. Leaves acid standard curve prepared for each run. See Faeth were then examined to determine total amounts of leaf- (1986, 1990) for a more detailed description of all chewing insect damage. We estimated the percent leaf phytochemical analyses. area removed (LAR) by leaf chewers, with leaves as- We used a repeated measures ANOVA (SAS GLM signed to the following damage level categories: <10% facility, SAS Institute, Cary, North Carolina) with LAR, 10-25% LAR, 25-50% LAR and 50+% LAR. treatments nested within trees and ramets nested within A length measurement taken from leaf base to distal treatments to analyze cumulative damage (arcsine end was used to estimate total leaf area. Simple re- squareroot transformed) by leaf-chewing and leaf min- gression of leaf length on leaf area (n = 200) accounted ing insects. Quadrant was not used as a factor in the for 96.5% of the variability in leaf area (regression statistical analyses because budbreak within clones was equation; AreaI'2= 0.05(length) + 0.23 where area is almost invariant with respect to sun exposure (Table measured in square centimeters and length is measured 1). A missing value generated by the loss of ramet 4EX in millimeters). resulted in an unbalanced experimental design. The leaf-chewing insects that we observed feeding A similar repeated measures nested ANOVA (Wi- on Gambel's oak were primarily (Arcti- ner, 1971) was used to test for differences among trees idae, Noctuiidae, Geometridae, Stenomidae and Tor- and between treatments in concentrations of hydrolyz- tricidae), and Coleoptera (Chrysomelidae and Cur- able tannins and protein (arcsine squareroot trans- culionidae). Leaf damage by these folivores occurs formed) in leaves collected on three dates during the mainly early in the growing season although lesser season. Analyses of condensed tannins showed concen- amounts of leaf-chewing insect damage occur through- trations near zero for the three sample dates and these out the growing season. data were therefore not statistically analyzed. Leaves collected from experimental and control ra- mets were also examined for the presence of four leaf- RESULTS-Experimental (older) leaves had less mining species that occur on Gambel's oak, Coptodisca in the season than did control sp. (Lepidoptera: ), Stigmella sp. (Lepi- damage early leaves treatment ef- doptera: Nepticulidae), Cameraria sp. (Lepidoptera: (younger) (Fig. 1, significant = = Gracillariidae), and Phyllonorycter sp. (Lepidoptera: fect, F 47.13, d.f. 1,24, P < 0.0001). Leaf- Gracillariidae). All of these miners are primarily late chewing damage also varied significantly among season feeders (Rooney, 1989), appearing in July, al- trees (F= 115.13, d.f. = 3,24, P < 0.0001). Most though a few individuals of Stigmella were observed leaves of both experimental and control ramets earlier in the season. Individuals of Coptodisca sp. ap- were damaged early in the season (significant on one of 16 ramets and therefore were peared only effect of time, F= 301.93, df. = 3,72, P < 0.0001), excluded from analyses. with the rate of damage to leaves previously un- Leaves for phytochemical analyses were collected damaged decreasing as the season progressed (Fig. from control and experimental ramets when the control as the season cumula- ramets broke bud. Leaves from experimental and con- 1). However, progressed, tive differences in insect lev- trol ramets were then sampled at mid-season and late leaf-chewing damage season. At each interval, a haphazard sample of un- els between experimental and control leaves di- damaged leaves was removed from each ramet and minished. The cumulative amount of LAR at the placed immediately on dry ice for transportation back end of the growing season was not significantly Wet to the lab. weights were taken, and leaves were different between experimental and control ra- then and to obtain lyophilized re-weighed dry weights. mets (X2 for means = 0.55, df. = 3, P > 0.90). Leaves were then ground in a mill in Wiley preparation In both treatments, approximately 90% of leaves for phytochemical analyses. Ground leaf samples were damaged by leaf-chewing insects had less than stored in tightly capped bottles in a 5?C cold room until 10% of their leaf area removed 2). phytochemical analyses could be performed. All anal- (Fig. of leaves mined yses were performed in triplicate and the readings av- Proportions by Stigmella sp., Cameraria leafminers did eraged to minimize experimental error. sp., Phyllonorycter sp. Total protein content of ground lyophilized leaf sam- not vary significantly between treatments (Stig- ples was analyzed using the BioRad Method (Rich- mella sp., F= 2.02, d.f. = 1,7, P= 0.17, Cameraria 4 The Southwestern Naturalist vol. 38, no. 1

100 60 * CONTROL * CONTROL - C1 90so - * EXPERIMENTAL * EXPERIMENTAL QwLJ z 50- 80- z I z 70 - 40- LI- 60- U,CtD -Jm 50 - 30- s N 40 - 0 20 - z 30- I 0 20 - m 10 - 0I 10 -

0 0 i i i i i JUN JUL AUG SEP OCT JUNE JULY AUGUST SAMPLEDATE SAMPLEDATE FIG. 1-Percentage of experimental and control leaves FIG. 3-Foliar gallotannin concentrations (ex- damaged as a function of time. Each point is the mean pressed as mean tannic acid equivalents + SE) of ex- for all ramets in each treatment, weighted by the num- perimental and control ramets as a function of time. ber of leaves on each ramet, ?SE.

(F = 304.11, d.f. = 2,48, P < 0.0001) but did not = sp., F = 0.32, d.f. = 1,7, P = 0.58; Phyllonorycter vary between treatments (Fig. 4, F = 0.10, d.f. sp., F = 3.34, d.f. = 1,7; P = 0.08). Proportion 1,24, P > 0.75) or among clones (F = 0.66, d.f. of leaves mined by Cameraria sp. varied signifi- = 3,24, P > 0.50). Protein content was highest cantly among trees (F = 9.80, d.f. = 3,7, P < early in the season, and then declined (Fig. 4). 0.001) but proportion of leaves mined by Stig- mella sp. and Phyllonorycter sp. did not (Stigmella DISCUSSION-Early in the season, younger sp., F = 2.45, d.f. = 3,7, P = 0.08; Phyllonorycter control leaves of Gambel oak suffered more fo- sp., F = 1.40, d.f. = 3,7, P = 0.26). livory by leaf-chewing insects than older exper- Gallotannin concentrations varied significantly imental leaves did. Past studies also show that with time (F = 219.76, d.f. = 2,48, P < 0.0001), many (e.g., Feeny, 1970; Ayres and MacLean, between treatments (Fig. 3, F = 16.05, d.f. = 1,24, 1987) but not all (e.g., Fowler and Lawton, 1984) P < 0.001), and among clones (F = 6.04, d.f. insect species prefer and perform better on youn- 3,24, P < 0.01). Most of the differences occurred ger foliage. Early-season Macrolepidoptera, the on the first sampling date (Fig. 3). dominant early-season chewing folivores in this Protein content varied significantly with time study, typically prefer young foliage (Niemela

?) loo 7 80 z 6 w H 0CL < 60 0 5

4 I 40 z z 3 LJ CLi OU w Y 20 0, 2 I.

<10% 10-25% 26-50X 51-100X % LEAF AREA REMOVED JUNE JULY AUGUST SAMPLEDATE FIG. 2-Amount of leaf area removed from exper- imental and control leaves. Bars are the mean for all FIG. 4-Foliar protein concentration (mean + SE) ramets in each treatment, weighted by the number of of experimental and control ramets as a function of leaves on each ramet, +SE. time. March 1993 Faeth and Rooney-Budbreakand insect folivory and Haukioja, 1982; Fowler and Lawton, 1984). but slightly, damaged control leaf (e.g., 4% of Variation in folivory between treatments corre- area removed) with the same amount of late- sponds to foliar quality in terms of tannin content. season damage (4% + 5% = 9%). To determine Gallotannin content of older, advanced experi- whether previously damaged leaves truly escape mental leaves was higher than that of younger additional folivory late in the season, future stud- control leaves, at least early in the season. ies will need to refine damage categories, partic- Folivory by leaf chewers increased on experi- ularly the <10% category of leaf area consumed. mental ramets late in the season, so that folivory Colonization by three species of leaf miners in differences between treatments eventually dis- this study was unaffected by leaves of different appeared (Fig. 1). Older leaves with less early- ages. Leaf miners on Gambel oak are predomi- season damage thus appear more susceptible to nantly late-season feeders, and most adults ovi- late-season damage than the more heavily-dam- posit after differences in chemistry and leaf-chew- aged control leaves. Late-season, leaf-chewing in- ing insect damage between treatments had sects apparently prefer to feed on previously un- disappeared (adult females determine feeding sites damaged leaves. There are several possibilities of sedentary larval offspring). Thus, any leaf se- for this preference. First, wound-induced changes lection differences between treatments based on in palatability or attractiveness caused by pre- chemistry or previous damage (Faeth, 1985b, vious insect damage (Edwards and Wratten, 1983, 1986) would not be apparent. These results, cou- 1985; Gibberd et al., 1988) may explain the pref- pled with those above involving the leaf chewers, erence for previously undamaged leaves. Damage suggest that any impacts of variable budbreak on of individual leaves (Fig. 2) also corroborates this folivory are most likely concentrated very early hypothesis since the amount of leaf area removed in the growing season and are not maintained late from most damaged leaves was less than 10%, into the growing season. suggesting that leaf-chewing folivores remove only Feeny (1976) proposed that deciduous trees, small fractions of individual leaves. We did not such as oaks, in temperate climates may escape examine chemical or physical changes associated herbivory in time by flushing leaves either earlier with folivory (only undamaged leaves were an- or later than average budbreak of the population. alyzed phytochemically), but other studies with For example, Du Merle (1988) found that late- oaks have shown induction of purported allelo- breaking trees of two species of oak (Quercuspu- chemicals with folivory (Schultz and Baldwin, bescens and Q. ilex) were more resistant to de- 1982; Faeth, 1986). Second, folivores may avoid foliation by the green oak leafroller, Tortrix virid- or suffer greater mortality on damaged leaves due ana, than early-breaking trees. Tuomi et al. (1989) to increased attack by natural enemies that use suggested that leaves produced asynchronously visual or chemical cues associated with leaf dam- within individual trees also are protected from age (Heinrich and Collins, 1983; Faeth, 1986; early season folivores. Faeth and Bultman, 1986). Third, late-season We examined experimentally the relationship insects may be specialists on mature, older foliage between this latter type of variation in budbreak (Rhoades and Cates, 1976; Cates 1980) and (i.e., variation of ramet budbreak within genets) therefore prefer older, experimental leaves. This and folivory. Ramets with advanced leaf flush explanation seems doubtful since, by mid-season, had reduced leaf-chewing insect damage early in experimental leaves did not differ from control the growing season, but cumulative levels of fo- leaves phytochemically (Fig. 3) and new foliage livory did not differ among treatments. However, on Gambel's "hardens" within two weeks, long reduction of early-season folivory could still in- before late-season folivores begin to feed. Finally, crease plant fitness despite similarities in cu- the apparent preference for undamaged leaves mulative folivory between experimental and con- may simply be an artifact of categorizing leaves trol ramets because younger foliage is generally by amount of damage. More than 70% of all considered to be of greater photosynthetic value leaves suffer some damage (Fig. 1), and -90% to plants than mature foliage (Feeny, 1970; Lev- of these leaves have <10% of area removed (Fig. in, 1971). 2). A previously undamaged leaf slightly chewed Variability in timing of budbreak also occurs by folivores late in the growing season (e.g., 5% among clones of Gambel oak (Table 1, budbreak of leaf area removed) was placed in the same of controls). If early budbreak can reduce folivory category (<10% of area removed) as a previously, by insects, then why don't trees of Gambel oak 6 The Southwestern Naturalist vol. 38, no. 1

advance budbreak to that of experimental ra- Feeny, 1976; Hunter, 1990) starve if buds and mets? In addition to escaping early season folivo- young leaves are not available. Trees breaking ry, early budbreak also lengthens the growing bud early relative to the population escape in time season. Advancing budbreak in temperate decid- as early-season folivores are confronted with old- uous forests is, however, constrained by environ- er, and hence, supposedly poorer quality, leaf mental factors such as photoperiod, temperature resources (Feeny, 1976; Fowler and Lawton, and moisture availability (Feeny, 1976; Kramer 1984; Haukioja et al., 1985). The latter seems to and Kozlowski, 1979; Fitter and Hay, 1987). apply to our study; advanced leaves of experi- Buds that break too early are susceptible to late mental ramets were higher in gallotannin content frosts and snows. For example, the loss of the than younger control leaves at the beginning of enclosed ramet 4EX was due to late snow at Aztec the growing season. Peak and some experimental leaves were lost to In tropical plant-herbivore systems, suscepti- frost damage on enclosed, experimental ramets of bility of young, expanding leaves also appears to clones 1 and 2. Young leaves exposed to frost or influence patterns of budbreak. Production of snow are usually damaged severely or abscised leaves after the peak of budbreak of trees results (Kramer and Kozlowski, 1979). Thus, early bud- in increased herbivory (Rockwood, 1974; Lie- break would increase plant fitness only if the berman and Lieberman, 1984; Aide, 1988) unlike increased risk of frost damage is outweighed by most temperate trees, perhaps because the sea- benefits of reduced folivory and longer growing sonal nature of insect species in the tropics is less season. Stochastic abiotic factors such as late frosts pronounced than in temperate zones (Aide, 1988). may select for later budbreak while escape from However, woody tropical plants can escape fo- early-season folivores and increasing length of the livory by advancing budbreak into the dry season growing season may select for early budbreak when insect abundances are lower (Aide, 1988), (Feeny, 1976). The mean time of budbreak in similar to reduction of folivory of experimentally populations of Gambel's oak may be therefore a advanced ramets of Gambel oak in this study. result of stabilizing selection from these opposing Our results and those from other studies sug- selective forces. gests that protection of vulnerable, young foliage Our results suggest that young, expanding may influence patterns of variable budbreak ob- leaves are most susceptible to folivory, probably served among many woody plants. Other factors, due to their allelochemical, nutritional, and phys- however, such as frost damage and length of ical differences from mature leaves. Fowler and growing season probably constrain the influences Lawton (1984) also showed that young, and pre- of folivores on variation in budbreak. sumably high quality, leaves of birch, Betula pen- dula, are usually preferred by folivorous species We thank B. Axelrod, C. Febus and M. Tabbarah regardless of when they appear in the growing for assistancein the field and the laboratory.W. Boeck- season. Faeth (1987) found that late-season leaf len, W. D. Clark, S. W. Rissing, R. Spellenberg,and an reviewer constructivecom- miners prefer and perform better on newly-flushed anonymous provided mentson the manuscript.This researchwas leaves that were produced atypically by defolia- supported by NSF grants BSR 8717543 and 9107296 to SHF. tion late in the growing season. These results suggest most insect species prefer new foliage, if available. The of this ex- susceptibility young, LITERATURECITED panding foliage appears to be a common theme among woody plants, and may be a common un- AIDE, T. M. 1988. Herbivoryas a selectiveagent on derlying cause of various patterns of budbreak the timing of leaf productionin a tropical under- found among woody plants, at least within con- story community.Nature (London), 336:574-575. M. AND S. F. 1987. De- straints imposed by other factors. In temperate AYRES, P., MACLEAN,JR. of birchleaves and the climates, trees with budbreak relative to velopment growthenergetics delayed of autumnata 68: the suffer less leaves Epirrita (Geometridae).Ecology, population folivory because 558-568. are out of with insect Insect synchrony emergence. BATE-SMITH,E. C. 1977. tannins of Acer to feed on new buds Astringent species specialized only (Du species. Phytochemistry,16:1421-1426. or those that Merle, 1988; Hunter, 1990) species BROADHURST, R. B., AND W. T. JONES. 1978. Anal- emerge from overwintering stages within narrow ysis of condensedtannins using acidifiedvanillin. windows of time (Varley and Gradwell, 1968; J. Sci. Food & Agric., 29:788-794. March 1993 Faeth and Rooney-Budbreakand insectfolivory 7

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