Ecology, 89(12), 2008, pp. 3275–3281� 2008 by the Ecological Society of America

DUCKING AS A MEANS OF RESISTANCE TO HERBIVORYIN TALL GOLDENROD, SOLIDAGO ALTISSIMA

MICHAEL J. WISE1

AND WARREN G. ABRAHAMSON

Department of Biology, Bucknell University, Lewisburg, Pennsylvania 17837 USA

Abstract. Many populations of goldenrod show a peculiar, genetically controlled stemdimorphism. In Solidago altissima, for instance, while most stems are erect, a sizable minority(the ‘‘candy-cane’’ stems) nod at the apex during growth. We used data from three studies totest the hypothesis that this candy-cane growth form confers resistance to herbivory. In acontrolled growth trial, we showed that nodding is a temporary phenomenon that coincideswith the oviposition period of at least two common apex-attacking herbivores: the tephritidgaller Eurosta solidaginis and the gall midge Rhopalomyia solidaginis. In a large field survey,stems of candy-cane genets were only half as likely to be ovipunctured by E. solidaginis. In acommon-garden study, candy-cane stems were less likely to be ovipunctured by E. solidaginis,and they were galled only half as often by R. solidaginis as erect stems. These results suggestthat the candy-cane stems of goldenrod possess a resistance strategy that allows them toessentially duck and hide from certain herbivores.

Key words: candy-cane stems; ducking; Eurosta solidaginis; galls; goldenrod; resistance to herbivory;Rhopalomyia solidaginis; Solidago altissima; stem morphology.

INTRODUCTION

While chemical toxins and mechanical deterrents

dominate the arsenal of known or suspected herbivore

defenses in plants, architectural features of plants may

also serve important roles in plant resistance (Lawton

1983, Kareiva and Sahakian 1990, Alonso and Herrera

1996, Espırito-Santo et al. 2007). Investigators have

identified a variety of architectural characteristics that

can affect resistance to herbivory, including number of

buds, branches, or flowers (Oghiakhe et al. 1993, Araujo

et al. 2006), size of internodes (Larson and Whitham

1997), spacing of leaves (Marquis et al. 2002), rolling of

young leaves (Grubb and Jackson 2007), pod angle

(Oghiakhe et al. 1992), growth habit (e.g., erect,

prostrate, or spreading [Oghiakhe et al. 1993, Rudgers

and Whitney 2006]), and architectural complexity in

general (Kaitaniemi et al. 2004). Perhaps the most basic

feature of plant architecture, however, is size. Plant

height, in particular, can have a major influence on a

plant’s susceptibility to herbivory.

Although being tall may provide trees and shrubs

protection against browsing (Palo et al. 1993), some

vertebrate (Merton et al. 1976) and many invertebrate

herbivores, particularly flying insects, tend to prefer

taller plants (Bach 1981, Karban and Courtney 1987,

Marquis 1992, Haysom and Coulson 1998). Plant height

may be an indication of host vigor, or taller plants may

just be more apparent and thus more likely to be found

by herbivores (Lawton 1983). As such, short stature can

reduce a plant’s susceptibility to herbivory, and, to the

extent that height is genetically controlled, shortness

might be favored by natural selection to reduce

herbivore damage. However, the evolution of shortness

as a resistance strategy is likely to be strongly

constrained by the disadvantages short plants face in

competing with taller neighbors for access to light or

pollinators. In this paper, we report on a trait that can

potentially enable plants to take advantage of short

stature to increase resistance while minimizing the

associated costs.

The stems of the common herbaceous perennial

Solidago altissima L. (‘‘tall goldenrod,’’ Asteraceae)

display a genetically controlled dimorphism. The stems

emerge from rhizomes in spring, and after a couple of

weeks each stem develops an apical-leaf bud that lasts

until the apical meristem begins to produce flower buds

in mid-summer. In most stems (the ‘‘erect’’ morpholo-

gy), the apical-leaf bud points straight up throughout

the growing season until the plants flower. In a

substantial minority of plant genets (i.e., genetic

individuals), however, the stem begins to bend near the

apex as the apical-leaf bud forms until the apex points

straight down. Although the stem appears wilted, the

apex is turgid. The stem remains recurved for weeks, and

the resemblance of the stem shape to a familiar candy

earned this nodding morphology the nickname ‘‘candy-

cane’’ stem (Fig. 1). The candy-cane stems straighten

back up just prior to flowering.

We hypothesized that the candy-cane morphology

acts as a resistance mechanism to reduce attack by

herbivores that oviposit or feed on the apical-leaf bud.

Specifically, we asked whether candy-cane stems in-

Manuscript received 8 February 2008; revised 16 June 2008;accepted 27 June 2008; final version received 23 July 2008.Corresponding Editor: R. J. Marquis.

1 E-mail: mjw6j@virginia.edu

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curred less damage than erect stems from two common

stem-gall-inducing dipterans: the fruit fly Eurosta solid-

aginis (Fitch) (Tephritidae) and the gall midge Rhopa-

lomyia solidaginis Lw. (Cecidomyiidae). This study

involved three components: (1) in greenhouse trials, we

compared the growth phenology of stems of erect and

candy-cane genets; (2) in a large field survey, we

measured ovipositions by E. solidaginis and subsequent

gall formation on stems of 110 erect and 11 candy-cane

genets; and (3) in a common garden study, we measured

ovipositions by E. solidaginis and galling rates of both E.

solidaginis and R. solidaginis on stems of 21 erect and

five candy-cane genets.

METHODS

Study species

Solidago altissima is a perennial herbaceous weed

abundant in roadsides, old fields, and waste places

throughout much of the eastern United States and

southern Canada. The herbivore fauna of S. altissima is

one of the best studied for any plant species (Maddox

and Root 1987, Root 1996, Abrahamson and Weis

1997), and 138 species of insects have been identified as

feeding on S. altissima in the Finger Lakes region of

New York state alone (Root and Cappuccino 1992).

Many of these insects attack the apices of goldenrod in

spring and early summer, during the window in which

the candy-cane stem morphology is expressed. Two of

the most common of these species are the gall-inducing

flies Eurosta solidaginis and Rhopalomyia solidaginis.

Previous studies have shown that both of these species

can negatively affect the growth and reproduction of S.

altissima (Hartnett and Abrahamson 1979, Stinner and

Abrahamson 1979, Abrahamson and Weis 1997, Wise et

al. 2006a).

Eurosta solidaginis is a univoltine specialist on S.

altissima in the study area (central Pennsylvania). Adults

emerge from galls in mid-to-late May and mate on

goldenrod ramets (Horner and Abrahamson 1992).

Females oviposit on apical-leaf buds, often after walking

up and down the stem several times and making test

punctures with their ovipositors in the bud (Uhler 1951,

Walton et al. 1990). These ovipunctures are visible as

one or more linear series of holes in the apical-leaf bud,

and later as an identical pattern of holes repeated on

successive leaves that were formerly overlapping in the

apical bud. Eggs hatch in about a week and spherical

stem galls become visible within three weeks (Uhler

1951, Craig et al. 2000). Each gall contains one larva,

but a single ramet occasionally forms up to three galls

(Hess et al. 1996, Wise et al. 2008). Full-grown larvae

diapause over winter inside galls and pupate the

following spring.

Overwintering first-instar larvae of the gall midge

Rhopalomyia solidaginis form relatively inconspicuous,

generally single-chambered galls on the apical meristems

of newly emerged goldenrod shoots in early spring: late

April in this study area (McEvoy 1988; N. Dorchin,

personal communication). Adults emerge in late May,

and gravid females lay eggs on S. altissima leaf buds.

The larvae initiate large, generally multi-chambered,

leafy ‘‘rosette’’ galls that can have major effects on

goldenrod morphology (Hartnett and Abrahamson

1979, Raman and Abrahamson 1995, Wise et al.

2006a). Second generation adults emerge from these

galls in late summer, and females lay eggs in soil or

seemingly haphazardly on plants (McEvoy 1988). Upon

hatching, larvae crawl underground to diapause over

winter, probably within goldenrod rhizomes (N. Dorch-

in, personal communication).

Stem-growth phenology

To compare stem-growth phenologies, we randomly

chose four candy-cane and four erect genets from a set

of 26 S. altissima genets originally collected as rhizomes

from a field in 2003 and grown in controlled conditions

each year (see methods in Common garden-experiment).

Rhizomes of these genets were removed from refriger-

ation on 26 June 2006 and cut into 2-mL segments,

which were measured using water displacement in a

graduated cylinder. The segments were planted into flats

in ProMix BX (Premier Horticulture Ltd., Dorval,

Quebec, Canada) in a greenhouse at Bucknell Univer-

sity. Shoots emerged in about one week, and eight

healthy ramets of each genet were transplanted into

16.5-cm plastic azalea pots on 24 July. Measurements

FIG. 1. Nodding, candy-cane stem of Solidago altissima.

MICHAEL J. WISE AND WARREN G. ABRAHAMSON3276 Ecology, Vol. 89, No. 12R

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were taken weekly until flowering (through 16 Septem-

ber) on (1) height from ground to highest point, (2)

height from ground to apex tip, and (3) total stem

length. For an erect stem, these three measurements are

equivalent.

Field survey

As part of a study to examine the stability of E.

solidaginis galling patterns in genets over time (McCrea

and Abrahamson 1987), we marked all the ramets of 121

spatially distinct genets (110 erect-stem and 11 candy-

cane-stem genets) in a roadside population along an 8.2-

km section of Route 147 in Northumberland County,

Pennsylvania, USA and measured galling rates from

1982 to 1984. In early June of 1984, immediately after

the period of E. solidaginis oviposition activity, we

counted all ramets from the 121 genets and loosely tied

small wire bands around ramets with E. solidaginis

ovipunctures. At the end of the growing season, we

revisited the plants to observe whether galls were formed

on each ramet.

Data analysis involved one-tailed t tests of the hypoth-

esis that candy-cane genets were more resistant than erect

genets. The response variables were the proportion of

rametsper genet (1)withE. solidaginisovipunctures and (2)

with mature E. solidaginis galls. Both proportions were

square-root transformed prior to analysis. A third, two-

tailed t-test was performed to test whether the proportion

of punctured ramets that ended up with mature galls

differed between stem types. These proportions were

arcsine-square-root transformed prior to analysis.

Common-garden experiment

In early April of 2003, rhizomes were collected from

26 S. altissima genets, which were separated by at least

30 m, from a 3-ha field population in Union County,

Pennsylvania (4085705400 N, 7685701800 W). (Rhizomes of

21 of these genets produced erect stems, and five

produced candy-cane stems.) The rhizomes were

cleaned, cut into 5-cm segments and planted into flats

in ProMix BX. After shoot emergence, the plants were

transplanted into 16.5-cm diameter plastic azalea pots.

In mid-June, 15 ramets of each genet (390 pots total)

were transplanted into a 300-m2 garden plot that had

been treated with herbicide, cleared, and plowed. The

garden plot was divided into a grid with planting

positions 90 cm apart within a row and 90 cm between

rows. Each sequence of 26 positions in the plot was

considered one statistical block, and one ramet from

each genet was placed in a randomized position in each

of the 15 blocks.

In mid-March of 2004, we collected over 1200 E.

solidaginis galls from the goldenrod field from which the

rhizomes were collected the previous spring. To inocu-

late the garden plot with E. solidaginis, we placed three

galls at each of the 390 planting positions. Rhopalomyia

solidaginis colonized the garden plot on its own. In mid-

to-late May, we tagged up to five of the nearest newly

emerged ramets to each planting position that had

clearly arisen from the original individual. Usually more

than five ramets were available, but there were always at

least two ramets per position (mean number tagged ¼4.83, SD¼0.53 ramets). Between 25 May and 3 June, we

examined each tagged ramet for E. solidaginis ovipunc-

tures). In late July and again in December, we revisited

each ramet and recorded the presence of E. solidaginis

and R. solidaginis galls.

Data analysis involved ANOVA and one-tailed t tests

of the hypothesis that candy-cane stems were more

resistant than erect stems. The original planting position

was considered the independent statistical unit, and the

response variables were the proportion of ramets at each

planting position with (1) E. solidaginis ovipunctures, (2)

mature E. solidaginis galls, and (3) R. solidaginis galls.

Four observers searched plants for ovipunctures in

different sections of the plot. To account for potential

spatial differences in ovipuncture frequencies in the field,

or differences in observers’ ability to spot ovipunctures,

observer identity was included in the ANOVA for

ovipunctures.

RESULTS

Stem-growth phenology

About three weeks after stems emerged, the candy-

cane ramets began to nod (Fig. 2). The apices pointed

downward for at least a month, after which time stems

began turning upward. At the peak of the difference, the

apices of erect ramets were an average of nearly 10 cm

(or 36%) higher than the apices of candy-cane ramets.

For the stems of one candy-cane genet, the heights of the

apices at the peak of nodding were an average of 44%

lower than they would have been had the stems been

FIG. 2. Phenology of shoot ducking; 64 ramets wereincluded: eight ramets from each of four candy-cane genetsand four erect genets. Day zero is the day the ramets weretransplanted into pots, which was ;3–4 weeks after stememergence from rhizomes (ramets emerged on different days).All ramets had flower buds by day 55. Circles represent meanheights for 32 candy-cane ramets and 32 erect ramets atmeasuring day, and error bars represent 6 SE.

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straight (based on total main-stem length). By the time

the plants were flowering (around 12 weeks post

emergence), the candy-cane stems had straightened

completely, and the heights of the stems of the two

types no longer differed.

Field survey

In the 1984 survey of a roadside population of 121 S.

altissima genets, the stems of the 11 candy-cane genets

were only about half as likely to have ovipunctures as

the stems of the 110 erect genets (one-tailed t¼ 2.43, P¼0.008; Fig. 3A). By the end of the season, 9% of the

candy-cane stems and 13% of the erect stems had mature

E. solidaginis galls (one-tailed t ¼ 1.08, P ¼ 0.14; Fig.

3B). This disparity in galling rates between stem types

was not as large as the disparity in ovipuncture rates

because candy-cane stems were slightly (but not

statistically significantly) more likely to form galls once

ovipunctured than were erect stems (43% vs. 33%; two-

tailed t¼�1.24, P ¼ 0.22; Fig. 3C).

Common-garden experiment

The stems of the five candy-cane genets in the

common-garden experiment were only 82% as likely to

be ovipunctured by E. solidaginis as erect stems (one-

tailed P¼ 0.0006, Fig. 4, Table 1). As in the field survey

of 1984, this significant difference in resistance to

ovipuncturing did not translate into a significant

difference in the presence of mature E. solidaginis ball

galls on the two stem types. Ball galls were found on an

average of 19.0% 6 3.3% of the stems of the candy-cane

genets and 21.4% 6 1.6% of the stems of erect genets

(one-tailed P ¼ 0.32). Again, there was no significant

difference in the probability of the two stem types

forming galls once oviposited: 39.1% 6 7.5% for candy-

cane stems vs. 32.8% 6 3.8% for erect stems (two-tailed

P ¼ 0.65).

There was a larger discrepancy between the stem types

in resistance to the gall midge R. solidaginis. By the end

of the summer, stems of candy-cane genets were only

half as likely to have R. solidaginis rosette galls as stems

of erect genets (P , 0.0001; Fig. 5, Table 1).

DISCUSSION

Stems of candy-cane genets of Solidago altissima were

less likely to be ovipunctured by the ball-galling fly

Eurosta solidaginis, and they were less likely to be form

rosette galls induced by the midge Rhopalomyia solid-

FIG. 3. Herbivory by Eurosta solidaginis on S. altissima in the field survey. Columns represent mean percentages (6 SE) oframets for 110 erect genets and 11 candy-cane genets: (A) ovipuncture rate (P¼ 0.008); (B) mature gall presence (P¼ 0.14); (C)gall-formation rate of ovipunctured ramets (P¼ 0.22).

FIG. 4. Herbivory by Eurosta solidaginis on S. altissima in the common-garden experiment. The experiment included fivecandy-cane and 21 erect genets, replicated in 15 spatial blocks. Columns represent least-squares means proportions (6 SE) oframets for each stem type from an ANOVA on stem type, block, and data collector: (A) ovipuncture rate (P¼ 0.0006); (B) maturegall presence (P¼ 0.32); (C) gall-formation rate of ovipunctured ramets (P¼ 0.65).

MICHAEL J. WISE AND WARREN G. ABRAHAMSON3278 Ecology, Vol. 89, No. 12R

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aginis, than were stems of erect genets. Because both of

these gallers can severely impact the growth and

reproduction of S. altissima (Hartnett and Abrahamson

1979, Stinner and Abrahamson 1979, Abrahamson and

Weis 1997, Wise et al. 2006a), candy-cane stems should

enjoy a clear fitness advantage due to their greater

resistance.

With such an important resistance benefit, a big

question is why the candy-cane stems are always in the

minority, at least in the geographic area of this study.

One possibility is simply that the ducking trait has

evolved only recently, and selection will drive it to be

more common in the future. Alternatively, balancing

selection may act on stem morphology, and ducking

may entail costs to the plants.

The simplest evidence for a cost to the candy-cane

strategy would be lower seed production than erect

stems in the absence of gall flies. The results of a

separate study on the plants involved in the common-

garden study show no evidence for such a cost (M. J.

Wise and W. G. Abrahamson, unpublished data).

Specifically, 18 ramets of each of the five candy-cane

and 21 erect-stemmed genets were exposed to a range of

levels of spittlebug herbivory (but no galling) (Wise et al.

2006b). The genets differed in seed production (F25, 434¼24.49, P , 0.0001), but the difference had nothing to do

with stem morphology. The mean for the candy-cane

genets was 22,068 6 3503 seeds per ramet, while the

mean for the erect genets was 19 450 6 1709 seed per

ramet (t ¼ 0.67, P ¼ 0.51).

Though differences in seed production between stem

morphs were not observed in the spittlebug study, the

candy-cane morphology may still entail costs that would

not have been evident in that study. For instance, it is

possible that there are tradeoffs among different

components of defense against the gall inducing flies.

In the field and garden studies, there was a slight

indication that ovipunctured candy-cane ramets might

be more likely to form galls than ovipunctured erect

ramets. Such a pattern would indicate that the

antixenosis (i.e., avoidance) resistance advantage of

candy-cane stems could cost the plants in terms of

lower antibiosis resistance. In addition, because resis-

tance and tolerance are sometimes negatively correlated

(Leimu and Koricheva 2006), it is possible that candy-

cane stems have lower tolerance of galling than erect

stems. It is also possible that candy-cane stems are less

resistant than erect stems to species of herbivores otherthan these gall inducing flies. While we have no data

indicating that such tradeoffs exist, we plan to look

more closely into these possibilities in the future.

Another potential cost of the candy-cane morphologymay be apparent in more light-limiting environments.

FIG. 5. Rhopalomyia galling rates on S. altissima in thecommon-garden experiment. The experiment included fivecandy-cane and 21 erect genets, replicated in 15 spatial blocks.Columns represent least-squares means (6 SE) of the percent-age of ramets ovipunctured for each stem type from anANOVA on stem type and block (P , 0.0001.)

TABLE 1. ANOVA results for resistance of candy-cane- and erect-stem morphs of Solidago to gallflies (Eurosta solidaginis) and gall midges (Rhopalomyia solidaginis).

Resistance measure Source of variation df MS F P

Percentage of ramets with stem morph 1 1.5582 10.6802 0.0012E. solidaginis ovipunctures� block 14 0.2896 1.9849 0.018

observer 3 1.9459 13.3371 ,0.0001error 371 0.1459

Mature E. solidaginis galls� stem morph 1 0.1625 0.2317 0.63block 14 1.0132 1.4443 0.13error 372 0.7015

E. solidaginis galls per stem morph 1 0.2071 0.1947 0.66ovipunctured ramet� block 14 1.7590 1.6989 0.054

observer 3 3.8285 3.6958 0.012error 331 1.0359

R. solidaginis galls� stem morph 1 3.364 21.9222 ,0.0001block 14 0.2583 1.6823 0.057error 372 0.1536

Note: Analyses were performed on transformed data to better meet assumptions of ANOVA.� Data were arcsine-square-root transformed.� Data were natural-log transformed.

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During the period in which they are nodding, it is likely

that candy-cane stems are less able to compete for light

with the erect stems. In fact, we have observed that

candy-cane stems will generally straighten out (become

erect) within a few days of being placed in heavy shade.

This phenomenon would seem to indicate that light

limitation can be a factor in candy-cane stems. Finally,

the resistance advantage of candy-cane stems may be

frequency dependent. Ducking may provide a large

advantage when the majority of stems do not duck, but

the advantage may attenuate as the frequency of

ducking plants rises. If candy-cane stems were to

approach a majority in a population, then the costs

(whatever they may be) may overshadow the shrinking

resistance benefits.

Several architectural resistance mechanisms have been

identified in other plant species (Marquis et al. 2002,

Kaitaniemi et al. 2004, Araujo et al. 2006). However, the

candy-cane strategy of goldenrod is different in that it is

a more active, almost behavioral trait. A candy-cane

stem starts out straight, then bends at just the time that

susceptibility to galling insects (and probably other

species) is the greatest. After the danger has passed, the

stems straighten back out, and the candy-cane stems are

just as tall as the erect stems by the time of flowering.

This growth pattern is tantamount to slow-motion

ducking, and to our knowledge, it is the first document-

ed instance of resistance by means of ducking.

The ducking strategy does not appear to be unique to

S. altissima, but we do not know how widespread it may

be. We have observed candy-cane stems in Pennsylvania

in two other old-field goldenrods: S. gigantea and S.

juncea. Both of these species host a community of apex-

attacking herbivores and would presumably also benefit

from a ducking strategy. However, we have never

observed candy-cane stems of S. rugosa, another old-

field goldenrod with apex-attacking herbivores. It seems

likely that the ducking strategy may be found in other

fast-growing, herbaceous plants in open habitats, where

individual stems are relatively conspicuous to flying

herbivores.

ACKNOWLEDGMENTS

We thank C. Blair and N. Dorchin for discussions andcomments on the manuscript. S. Anderson, K. McCrea, and A.Weis assisted with data collection in the 1984 field survey. B.Davis and A. Turbett assisted with planting the gardenexperiment in 2003; R. Fox, P. March, J. Partelow, and A.Snyder collected ovipuncture data in 2004; and P. Marchcollected rosette-gall data in 2004. Rolf and Annick Helbigkindly granted permission to collect goldenrod rhizomes ontheir property for the garden experiment. We acknowledge theDavid Burpee Chair of Plant Genetics endowment of BucknellUniversity for supporting this research. The National ScienceFoundation also provided financial support for parts of thestudy under the following grants: DEB-8205856 to W. G.Abrahamson, DEB-0343633 to W. G. Abrahamson and J. T.Irwin, and DEB-0515483 to W. G. Abrahamson and M. J.Wise. Any opinions, findings, and conclusions expressed in thispaper are those of the authors and do not necessarily reflect theviews of the National Science Foundation.

LITERATURE CITED

Abrahamson, W. G., and A. E. Weis. 1997. Evolutionaryecology across three trophic levels: goldenrods, gallmakers,and natural enemies. Princeton University Press, Princeton,New Jersey, USA.

Alonso, C., and C. M. Herrera. 1996. Variation in herbivorywithin and among plants of Daphne laureola (Thymelaea-ceae): correlation with plant size and architecture. Journal ofEcology 84:495–502.

Araujo, A. P. A., J. D. A. De Paula, M. A. A. Carneiro, andJ. H. Schoereder. 2006. Effects of host plant architecture oncolonization by galling insects. Austral Ecology 31:343–348.

Bach, C. E. 1981. Host plant growth form and diversity: effectson abundance and feeding preference of a specialistherbivore, Acalymma vittata (Coleoptera: Chrysomelidae).Oecologia 50:370–375.

Craig, T. P., J. K. Itami, C. Shantz, W. G. Abrahamson, J. D.Horner, and J. V. Craig. 2000. The influence of host plantvariation and intraspecific competition on ovipositionpreference and offspring performance in the host races ofEurosta solidaginis. Ecological Entomology 25:7–18.

Espırito-Santo, M. M., F. d. S. Neves, F. R. Andrade-Neto,and G. W. Fernandes. 2007. Plant architecture and meristemdynamics as the mechanisms determining the diversity ofgall-inducing insects. Oecologia 153:353–364.

Grubb, P. J., and J. B. C. Jackson. 2007. The adaptive value ofyoung leaves being tightly folded or rolled on monocotyle-dons in tropical lowland rain forest: an hypothesis in twoparts. Plant Ecology 192:317–327.

Hartnett, D. C., and W. G. Abrahamson. 1979. The effects ofstem gall insects on life history patterns in Solidagocanadensis. Ecology 60:910–917.

Haysom, K. A., and C. Coulson. 1998. The Lepidoptera faunaassociated with Calluna vulgaris: effects of plant architectureon abundance and diversity. Ecological Entomology 23:377–385.

Hess, M. D., W. G. Abrahamson, and J. M. Brown. 1996.Intraspecific competition in the goldenrod ball-gallmaker(Eurosta solidaginis): larval mortality, adult fitness, oviposi-tional and host-plant response. American Midland Naturalist136:121–133.

Horner, J. D., and W. G. Abrahamson. 1992. Influence of plantgenotype and environment on oviposition preference andoffspring survival in a gallmaking herbivore. Oecologia 90:323–332.

Kaitaniemi, P., H. Vehvilainen, and K. Ruohomaki. 2004.Movement and disappearance of mountain birch defoliatorsare influenced by the interactive effects of plant architectureand induced resistance. Ecological Entomology 29:437–446.

Karban, R., and S. Courtney. 1987. Intraspecific host plantchoice: lack of consequences for Streptanthus tortuosus(Cruciferae) and Euchloe hyantis (Lepidoptera: Pieridae).Oikos 48:243–248.

Kareiva, P., and R. Sahakian. 1990. Tritrophic effects of asimple architectural mutation in pea plants. Nature 345:433–434.

Larson, K. C., and T. G. Whitham. 1997. Competition betweengall aphids and natural plant sinks: plant architecture affectsresistance to galling. Oecologia 109:575–582.

Lawton, J. H. 1983. Plant architecture and the diversity ofphytophagous insects. Annual Review of Entomology 28:23–39.

Leimu, R., and J. Koricheva. 2006. A meta-analysis of tradeoffsbetween plant tolerance and resistance to herbivores:combining the evidence from ecological and agriculturalstudies. Oikos 112:1–9.

Maddox, G. D., and R. B. Root. 1987. Resistance to 16 diversespecies of herbivorous insects within a population ofgoldenrod, Solidago altissima: genetic variation and herita-bility. Oecologia 72:8–14.

MICHAEL J. WISE AND WARREN G. ABRAHAMSON3280 Ecology, Vol. 89, No. 12R

epor

ts

Marquis, R. J. 1992. Selective impact of herbivores. Pages 301–325 in R. S. Fritz and E. L. Simms, editors. Plant resistanceto herbivores and pathogens. University of Chicago Press,Chicago, Illinois, USA.

Marquis, R. J., J. T. Lill, and A. Piccinni. 2002. Effect of plantarchitecture on colonization and damage by leaftyingcaterpillars of Quercus alba. Oikos 99:531–537.

McCrea, K. D., and W. G. Abrahamson. 1987. Variation inherbivore infestation: historical vs. genetic factors. Ecology68:822–827.

McEvoy, M. V. 1988. The gall insects of goldenrod (Compo-sitae: Solidago) with a revision of the species Rhopalomyia(Diptera: Cecidomyiidae). Thesis. Cornell University, Ithaca,New York, USA.

Merton, L. F. H., D. M. Bourn, and R. J. Hnatiuk. 1976. Gianttortoise and vegetation interactions on Aldabra Atoll. Part 1:inland. Biological Conservation 9:293–304.

Oghiakhe, S., L. E. N. Jackai, and W. A. Makanjuola. 1992.Cowpea plant architecture in relation to infestation anddamage by the legume pod borer, Maruca testulalis Geyer(Lepidoptera: Pyralidae). 2. Effect of pod angle. InsectScience and Its Application 13:339–344.

Oghiakhe, S., L. E. N. Jackai, and W. A. Makanjuola. 1993.Cowpea plant architecture in relation to infestation anddamage by the legume pod borer, Maruca testulalis Geyer(Lepidoptera: Pyralidae). 3. Effects of plant growth habit.Insect Science and Its Application 14:199–203.

Palo, R. T., J. Gowda, and P. Hogberg. 1993. Species heightand root symbiosis, two factors influencing antiherbivoredefense of woody plants in East African savanna. Oecologia93:322–326.

Raman, A., and W. G. Abrahamson. 1995. Morphometricrelationships and energy allocation in the apical rosette gallsof Solidago altissima (Asteraceae) induced by Rhopalomyia

solidaginis (Diptera: Cecidomyiidae). Environmental Ento-mology 24:635–639.

Root, R. B. 1996. Herbivore pressure on goldenrods (Solidagoaltissima): its variation and cumulative effects. Ecology 77:1074–1087.

Root, R. B., and N. Cappuccino. 1992. Patterns in populationchange and the organization of the insect communityassociated with goldenrod. Ecological Monographs 62:393–420.

Rudgers, J. A., and K. D. Whitney. 2006. Interactions betweeninsect herbivores and a plant architectural dimorphism.Journal of Ecology 94:1249–1260.

Stinner, B. R., and W. G. Abrahamson. 1979. Energetics of theSolidago canadensis stem gall insect–parasitoid guild interac-tion. Ecology 60:918–926.

Uhler, L. D. 1951. Biology and ecology of the goldenrod gallfly, Eurosta solidaginis (Fitch). Memoir 300. Cornell Univer-sity Agricultural Experiment Station, Ithaca, New York,USA.

Walton, R., A. E. Weis, and J. P. Lichter. 1990. Ovipositionbehavior and response to plant height by Eurosta solidaginisFitch (Diptera: Tephritidae). Annals of the EntomologicalSociety of America 83:509–514.

Wise, M. J., W. G. Abrahamson, and K. Landis. 2006a.Edaphic environment, gall midges, and goldenrod clonalexpansion in a mid-successional old-field. Acta Oecologica30:365–373.

Wise, M. J., D. L. Kieffer, and W. G. Abrahamson. 2006b.Costs and benefits of gregarious feeding in the meadowspittlebug, Philaenus spumarius. Ecological Entomology 31:548–555.

Wise, M. J., J. M. Partelow, K. J. Everson, M. K. Anselmo, andW. G. Abrahamson. 2008. Good mothers, bad mothers, andresistance to herbivory in Solidago altissima. Oecologia 155:257–266.

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