lab report

THE ROLE OF NODDING STEMS IN THE GOLDENROD–GALL–FLY INTERACTION: A test of the "ducking" hypothesis Author(s): Michael J. Wise, Warren G. Abrahamson and Julia A. Cole Source: American Journal of Botany, Vol. 97, No. 3 (March 2010), pp. 525-529 Published by: Botanical Society of America, Inc. Stable URL: http://www.jstor.org/stable/27793166 Accessed: 02-11-2017 17:34 UTC

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) American Journal of

botany American Journal of Botany 97(3): 525-529. 2010.

BRIEF COMMUNICATION

the role of nodding stems in the goldenrod-gall-fly interaction: A test of the "ducking" hypothesis1

Michael J. Wise2 5, Warren G. Abrahamson3, and Julia A. Cole4

2Blandy Experimental Farm, 400 Blandy Farm Lane, Boyce, Virginia 22620 USA; department of Biology, Bucknell University, Lewisburg, Pennsylvania 17837 USA; and department of Biology, Skidmore College, 815 North Broadway, Saratoga Springs,

New York 12866 USA

Herbivores are among the most pervasive selective forces acting on plants, and the number of plant chemicals that presumably evolved for defense against herbivory is immense. In contrast, biologists are only beginning to appreciate the important roles that architectural traits can play in antiherbivore defense. One putative architectural-resistance trait is the nodding stem apex of some goldenrods (Solidago; Asteraceae). Individuals of S. altissima genets that undergo temporary nodding in the late spring (i.e., "candy-cane" ramets) have been shown to be more resistant than individuals of erect-stemmed genets to certain apex-attacking herbivores. We tested the hypothesis that the greater resistance of candy-cane ramets is accomplished by the ramets' "ducking" from the herbivores. In a greenhouse experiment, nodding candy-cane ramets were significantly more resistant to oviposition by the gall-inducing fly Eurosta solidaginis than were ramets of the same genets that had been experimentally straightened. The straightened candy-cane stems were just as susceptible to ovipositions as were ramets of erect-stemmed genets. Thus, ducking indeed appears to confer a resistance advantage to candy-cane genets of S. altissima.

Key words: architectural defense; Asteraceae; candy-cane stems; Eurosta solidaginis; goldenrod; oviposition; resistance by ducking; Solidago altissima.

Virtually all plants are subject to the depredations of herbi vores, and they have responded by evolving a diversity of de fensive traits. While toxic chemicals and mechanical structures

(e.g., spines, thorns, and trichomes) have long been recognized as important elements in the defensive arsenal of plants, re searchers have only recently begun to appreciate the importance of architectural traits (Espirito-Santo et al, 2007; Grubb and Jackson, 2007). Potential architectural defenses include the number of branches, size of internodes, spacing of leaves, growth habit, and architectural complexity in general (Oghiakhe et al., 1993; Larson and Whitham, 1997; Marquis et al., 2002; Ara?jo et al., 2006; Rudgers and Whitney, 2006). Because ar chitectural traits may serve basic functions for plant growth or may even be a passive result of developmental constraints, their

1 Manuscript received 4 August 2009; revision accepted 4 December 2009. The authors thank J. Vu and members of the Abrahamson laboratory?

C. Blair, A. Dincer, A. Peterson, B. Rhodes, and M .Takahashi?for technical assistance in the project. They also thank R. Helbig and A. Helbig for permission to collect goldenrod rhizomes from their property, and C. Blair and N. Dorchin for constructive comments on the manuscript. J.A.C, participated in Blandy Experimental Farm's undergraduate research program, which was funded by a National Science Foundation grant (DBI 0755198) to T. Roulston and M. McKenna. M.J.W. was supported by National Science Foundation grants DEB-0515483 to W.G.A. and M.J.W. and DEB-0614395/0745562 to D. Carr and M. Eubanks. Funding for the experiment and greenhouse facilities was provided by Bucknell University ' s David Burpee Plant Genetics Chair endowment. Any opinions, findings, and conclusions expressed in this material are those of the authors and do not necessarily reflect the views of the National Science Foundation.

5 Author for correspondence (e-mail: [email protected])

doi:10.3732/ajb.0900227

roles in natural-enemy defense are easily overlooked. Here, we investigate the potential defensive role of one architectural trait: the peculiar nodding morphology displayed by the stems of some goldenrod (Solidago altissima) individuals in late spring and early summer. Most genets of S. altissima produce stems that are erect (with

the apical bud facing upward) from emergence in spring through flowering and senescence in fall. A substantial minority of gen ets, however, produce stems that emerge erect, but after 3-4 wk begin to nod so that the apex is pointing straight downward. These "candy-cane" stems remain nodding for several weeks but straighten again in time to flower. We recently proposed that the candy-cane stems help plants to resist herbivores that oviposit in stem apices in late spring and early summer (Wise and Abrahamson, 2008). In essence, we hypothesized that a ramet of a candy-cane genet "ducks" its apical bud to hide from would-be herbivores, then straightens back up when the herbi vores are gone to regain full height by flowering.

In a series of studies, we found that candy-cane genets are indeed more resistant than erect genets to at least three common apex-attacking herbivores: the tephritid fly Eurosta solidaginis and the cecidomyiid gall midges Rhopalomyia solidaginis and Asphondylia solidaginis (Wise and Abrahamson, 2008; Wise, 2009; Wise et al., 2009). The coincidence of the phenology of plant nodding and the flight period of the herbivores lends cre dence to the ducking hypothesis. However, it is possible that there is something about the candy-cane genets, other than the nodding morphology, that confers resistance. A direct test of the ducking hypothesis is challenging because it would require testing either candy-cane genets possessing erect stems or erect genets possessing nodding stems. We have previously observed that candy-cane stems tend to

straighten when the plants experience strong shade. We took

American Journal of Botany 97(3): 525-529, 2010; http://www.amjbot.org/ ? 2010 Botanical Society of America

525

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526 American Journal of Botany [Vol. 97

advantage of this phenomenon to create a set of candy-cane ramets with erect stems. In a greenhouse trial, we exposed a set of nodding and straightened candy-cane stems (and appropriate erect-genet controls) to oviposition by Eurosta solidaginis. If ducking is indeed the mechanism of resistance of candy-cane genets, then we would expect: (1) nodding candy-cane stems to be more resistant to oviposition than straightened candy-cane stems and stems of erect genets and (2) straightened candy-cane stems to be equally susceptible to E. solidaginis oviposition as stems of erect genets. If we do not see these patterns, then we would conclude that there is something besides the nodding that confers candy-cane genets with increased resistance to apex attacking herbivores, and we would reject the ducking hypothesis.

MATERIALS AND METHODS

Study system?Solidago altissima L. (Asteraceae), or tall goldenrod, is a rhizomatous perennial herb abundant in roadsides, old fields, and disturbed ar eas. It is native to eastern North America but has spread to most of the United States and is invasive in parts of Europe and Asia (Weber, 1997, 2000, 2001). The stem-nodding habit has been reported in the Great Plains of the United States (Croat, 1972) and in central Europe (Weber, 1997). We have encoun tered candy-cane ramets in S. altissima populations in our studies in the north central and northeastern United States (from Michigan to Maine and south to Virginia). Though nearly always present, candy-cane ramets have consistently been less common than erect-stemmed ramets in our observations of S. al

tissima populations. Tall goldenrod hosts a diversity of insect herbivores, including several that

either consume the apical meristem or lay eggs in the apical-leaf bud (Root and Cappuccino, 1992; Root, 1996). Among apex attackers, the tephritid gall-in ducer Eurosta solidaginis has received the most study. This species is found throughout the North American range of its goldenrod hosts?across southern Canada and in the United States from Florida up to Maine and west to Wash ington (Uhler, 1951 ; Abrahamson and Weis, 1997). The nonfeeding adults of E. solidaginis eclose from overwintering galls in spring (mid to late May in central Pennsylvania, the site of this study). Male flies display on the apical-leaf buds of S. altissima to attract females (Uhler, 1951). After mating, a female begins to search for appropriate oviposition sites. She exhibits a series of behaviors that

may include walking up and down a goldenrod stem several times, rubbing the apical-leaf bud with her forelegs, and pulling the bud tip to her mouthparts (Uhler, 1951; Abrahamson et al., 1989; Walton et al., 1990). Upon accepting a leaf bud, she may puncture the bud in several locations with her ovipositor be fore laying an egg (Fig. 1), but once she begins puncturing, she will generally lay at least one egg prior to leaving the bud (Uhler, 1951; Abrahamson and

Weis, 1997). This puncturing behavior leaves a visible series of holes (i.e., ovipunctures) in the leaf bud, such that oviposition may be easily inferred even several days after the fly has departed.

Eggs hatch within a few days, and the presence of a larva induces a "ball gall" that becomes visible in the plant stem just below the apex within about three weeks of oviposition (Uhler, 1951; Abrahamson and Weis, 1997; Craig et al., 2000). The larva feeds inside the gall until plant senescence, and the full grown larva overwinters in the gall, pupating soon after breaking diapause the following spring. The presence of a ball gall substantially reduces the reproduc tive capacity of S. altissima (Hartnett and Abrahamson, 1979; Stinner and

Abrahamson, 1979; McCrea and Abrahamson, 1985). Therefore, there is likely a strong benefit for plants that can reduce the likelihood of gall-fly oviposition.

The E. solidaginis individuals used in this study came from galls in an S. altissima population in Lycoming County, Pennsylvania. Approximately 3000 galls were collected on 13 March 2009 and were kept frozen until 6, 7, 9, 11, or 13 May 2009, when they were placed in emergence cages in a growth chamber at 23?C, 85% humidity, and 14:10 L : D. Upon adult emergence, flies were col lected in groups of six into plastic cups and held at 10?C, 85% humidity, and 14:10 L : D until the experiment began.

Experimental design?For this study, we included two erect and two candy cane genets of S. altissima from a set of 26 genets originally collected as rhi zomes from a field in Union County, Pennsylvania in the spring of 2003. The plants have been propagated clonally from new rhizomes each spring since their collection. On 20-21 March 2009, we cut rhizomes (grown in 2008) into

Fig. 1. Female Eurosta solidaginis ovipuncturing the apical-leaf bud of an erect-stemmed Solidago altissima.

multiple segments of equal size. The cutting process involved dipping rhizomes into a 100-mL graduated cylinder (filled with water to the 98-mL mark) down to the point at which the rhizome displaced 2 mL of water (so the water reached the 100-mL mark). We cut the rhizomes at this point, such that each rhizome segment was the same size in terms of volume. We planted the rhizomes in commercial growing medium (ProMix BX, Premier Horticulture Ltd., Dorval, Quebec, Canada) in flats in a greenhouse at Bucknell University. Healthy shoots were transplanted into 16.5-cm plastic azalea pots on 30 April 2009.

Each pot contained a single stem, or ramet. We refer to ramets that arose from the two genets that produce nodding stems as "candy-cane ramets," and we refer to ramets that arose from the two genets that produce erect stems as either "erect-stemmed ramets" or simply "erect ramets." In this study, a candy cane ramet may have either a nodding stem or an experimentally straightened stem. To reduce the chance of confusion, we reserve the phrase "erect stem" for stems from erect genets, though straightened stems of candy-cane genets are also technically erect.

Preparation of the ramets for the experiment involved two light treatments. On 24 May, we placed half of the ramets of each genet on a greenhouse bench under a shade-cloth cage that blocked 80% of ambient light (PAK Unlimited, Cornelia, Georgia, USA). The rest of the ramets received ambient greenhouse light, supplemented with high-pressure sodium-vapor lighting. The shade treat

ment lasted 10 d, by which time the majority of the candy-cane ramets in the shade treatment had straightened.

On the evening of 3 June 2009, we selected 32 candy-cane ramets from the shade treatment that had completely straightened, 32 candy-cane ramets from the full-light treatment that were completely nodding, and 32 erect-stemmed ramets from both the shade and the full-light treatments. We randomized the placement of the 128 ramets (32 nodding and 96 straightened or erect) on one greenhouse bench in eight rows. On the morning of 4 June, we measured the heights of the ramets from the base of the stem to the highest point of the ramet. For the nodding candy-cane ramets, the highest point was one of the younger fully expanded leaves, while for the straightened cahdy-cane and the erect stemmed ramets, the highest point was the tip of the apical-leaf bud.

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March 2010] Wise et al.?The role of nodding in goldenrod stems 527

After measuring the stem heights (at 1030 hours) we released 106 male and 115 female flies amid the bases of the 128 ramets. At first, some flies walked to the ramets from below, but generally they eventually flew up and chose ramets from above. Two hours after releasing the flies, we counted the number of male and female flies on each ramet and checked the apical-leaf buds for ovipunc tures. We repeated the counts every 90 min until 1700 hours. In the evening, we released 41 additional flies (18 males and 23 females). We resumed checking ramets on 5 June at 0900 hours and continued every 90 min until 1500 hours, when only three flies remained on the ramets and we were reasonably certain that ovipositions had ceased. In total, we checked the ramets nine times during the 2 days, during which 13 ramets were ovipunctured.

Data analysis?The main goal of this experiment was to test whether nod ding is responsible for the resistance advantage of candy-cane ramets, and the most relevant measurement for resistance available from this study is the pres ence vs. the absence of ovipuncture scars. We used a nominal-logistic model and likelihood-ratio tests to assess whether nodding candy-cane ramets (from the full-sun treatment) differed in ovipuncture presence from ramets with straight stems (candy-cane ramets from the shade treatment plus erect ramets from both treatments). We used a second nominal-logistic model to test whether straightened candy-cane ramets (from the shade treatment) differed in ovipunc ture presence from erect ramets (from sun or shade treatments).

To gain insight into the mechanism of the resistance difference between nodding and erect or straightened ramets, we tested whether there was a differ ence among ramets in fly presence. We summed the number of male and female flies observed for each ramet over the nine time periods. Two-way analyses of variance (ANOVAs) were run for male flies, female flies, and both sexes com bined, with the explanatory variables stem type (erect vs. candy-cane), light treatment, and their interaction.

Stem height has previously been shown to affect E. solidaginis preferences among individuals of S. altissima (Abrahamson and Weis, 1997). To test whether height affected fly preferences in our experiment, we ran a nominal logistic analysis for ovipuncture presence in the ramets with erect or straight ened stems (N = 96) with height as the explanatory variable. We also ran a linear regression of total fly presence on stem height for all 128 ramets. To as sess differences in heights among plant groups, we ran an ANOVA on stem height with stem type, light treatment, and their interaction as explanatory vari ables. All analyses in this paper were run with the program JMP-IN 4.0.4 (SAS Institute, Cary, North Carolina, USA).

RESULTS

Although oviposition rate was overall relatively low in this experiment (13 of 128 ramets were ovipunctured), resistance patterns were clear (Fig. 2). First, nodding candy-cane stems were significantly less likely to receive ovipunctures than erect stems and straightened candy-cane stems (likelihood-ratio 2 = 7.9577, = 0.0048). Thus, nodding ramets were more resistant than genetically identical straightened ramets, as well as erect ramets. Second, straightened candy-cane stems (from the shade treatment) were equally susceptible to ovipuncturing as the erect plants from both light treatments (likelihood-ratio 2 = 0.1745, = 0.68). Thus, straightened candy-cane stems no lon ger had a resistance advantage over erect stems, and the shade treatment did not have any effect on resistance other than the straightening effect. These results meet both criteria for con cluding that ducking is responsible for the higher resistance of candy-cane genets.

Unlike the ovipuncture results, there was no evidence of a significant difference in fly presence between stem morphs or light treatments (Fig. 3; Table 1). For erect ramets, fly presence

was only half as great on ramets that had experienced the shade treatment as the sun treatment, but this difference was not sta tistically significant. This trend toward preferring light-treat ment ramets was not seen in candy-cane ramets, but such a preference may have been canceled out by an avoidance of nod ding ramets. Such a trade-off is hinted at by the marginally sig

o Erect Candy-cane

Fig. 2. Percentage of Solidago altissima stems ovipunctured in the experiment. Shaded bars represent ramets that underwent a 10-d-shade treatment, and striping represents ramets of candy-cane genets. No ducking candy-cane ramets (i.e., from the full-light treatment) were ovipunctured.

nificant interaction between stem morph and light treatment (Table 1). Importantly, female flies did not spend significantly less time on nodding candy-cane ramets than they did on straightened candy-cane or erect-stemmed ramets.

As expected, nodding candy-cane stems were shorter than any of the other stems (Fig. 4; Table 2). The 10 d of shade treat ment caused both erect and candy-cane ramets to grow about 30% taller than their counterparts in ambient light. Unexpect edly, the differences in height had no effect on resistance. The regression of stem height on fly presence showed no significant effect of height on total fly presence (t = -1.43, df = 1, = 0.70,

Erect Candy-cane Fig. 3. Means and standard errors of the total fly counts (males and

females) per ramet summed over nine observation periods. Shaded bars represent ramets that underwent a 10-d-shade treatment, and striping rep resents ramets of candy-cane genets.

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528 American Journal of Botany fVol. 97

Table 1. Results of ANOVAs of fly presence on stem morph (erect vs. candy-cane) and light treatment (shade vs. ambient light).

Source of variation df MS

Female flies Stem morph Light treatment Stem light Error

Male flies Stem morph Light treatment Stem light Error

All flies combined Stem morph Light treatment Stem light Error

1 1 1

124

1 1 1

124

1 1 1

124

3.1250 1.5313 1.1250 2.1870

0.0313 1.1531 6.1250 2.2404

2.5313 6.1250 12.5000 5.5005

1.4289 0.7002 0.5144

0.0139 0.6835 2.7339

0.4602 1.1135 2.2725

0.23 0.40 0.47

0.91 0.41 0.10

0.50 0.29 0.13

r2 = 0.001). Moreover, for the 96 erect and straightened candy cane ramets, stem height had no effect on the likelihood of be ing ovipunctured (likelihood-ratio 2 = 0.03, = 0.86).

DISCUSSION

As in previous studies (Wise and Abrahamson, 2008; Wise et al., 2009), candy-cane goldenrod plants were less suscepti ble to Eurosta solidaginis oviposition than were the erect stemmed plants. In the previous studies, however, we could not be certain whether it was the nodding itself that made the can dy-cane plants more resistant or whether something else dif fered in the candy-cane plants (e.g., volatile chemicals) that contributed to their greater resistance. In this study, we found that when stems of candy-cane ramets were made to straighten out,

Erect Candy-cane Fig. 4. Means and standard errors of ramet height at the time of fly

release. Shaded bars represent ramets that underwent a 10-d-shade treat ment, and striping represents ramets of candy-cane genets. The height of the ducking candy-cane ramets was measured to the highest leaf, while the height was measured to the tip of the apical-leaf bud for the other three groups.

Table 2. Results of ANOVAs of stem height on stem morph (erect vs. candy-cane) and light treatment (shade vs. ambient light).

Source of variation df MS F

Stem morph 1 552.7813 18.8023 <0.0001 Light treatment 1 7080.5000 240.8358 <0.0001 Stem light 1 0.0313 0.0011 0.97 Error 124 29.3997

they completely lost their resistance advantage and were at least as likely to be ovipunctured as the erect-stemmed ramets. Ramets of the same candy-cane genets that were nodding received no oviposition whatsoever. Thus, this study supports the hypothesis that it is the ducking per se that confers the resistance advantage of candy-cane plants to E. solidaginis. Candy-cane goldenrods have also been shown to be more re

sistant than erect-stemmed plants to two species of gall midges (Wise, 2009). It is likely that it is ducking that confers resistance to these insects as well, but a confirmation will be more difficult than for E. solidaginis because the tiny gall midges are more dif ficult to work with and observe than the much larger E. solidag inis (see Dorchin et al, 2007, 2009). There are at least two ways by which ducking might confer

resistance to S. altissima. Most simply, ducking makes plants shorter, and thus potentially less apparent to flying insects search ing for oviposition sites. As is the case for many herbivorous in sects, E. solidaginis has been shown to prefer taller plants (Walton

Fig. 5. Female Eurosta solidaginis resting on leaf above the nodding apical-leaf bud of a candy-cane Solidago altissima ramet.

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March 2010] Wise et al.?The role of nodding in goldenrod stems 529

et al, 1990; Abrahamson and Weis, 1997; Craig et al, 2000). However, the results of our experiment do not support reduced height as the main mechanism of resistance. In fact, stem height had absolutely no effect on fly presence or oviposition. More over, flies were just as likely to be found on nodding candy-cane ramets as on straightened candy-cane or erect-stemmed ramets: They did not seem to have trouble finding candy-cane plants. It is possible that the plants in the simplified environment of the greenhouse were bound to be found and that a relatively short stature would be more of an asset in the more complex conditions of a field population. Therefore, we are hesitant to rule out the value of the reduced height accomplished by ducking. Neverthe less, our results strongly suggest that decreasing height is not the only way ducking conferred resistance to oviposition.

The more likely mechanism is that the nodding apex of a candy-cane ramet confuses the flies. The mating and oviposition behavior of E. solidaginis is rather ritualized, and the apical-leaf bud is central to both behaviors (Walton et al., 1990; Abraham son and Weis, 1997). The upside-down orientation of the apical leaf bud of a nodding stem, and the fact that the apex is not the highest point of the ramet, may hinder mating and oviposition behavior. In many instances, we observed a female fly sitting on the highest leaf of a ducking ramet rather than going below to the inverted apical-leaf bud, where she could have oviposited (Fig. 5).

Further study will be required to quantify fly behavior to shed more light on how the nodding apex actually hinders oviposition. In this and past studies, we have shown that candy-cane golden rod plants are more resistant than erect-stemmed plants to ovipo sition. Here, we have shown that it is indeed the ducking of the stems that confers the resistance advantage to candy-cane ramets. Ducking is therefore an important resistance mechanism in the arsenal of S. altissima defenses, and it is likely to be important in other goldenrod species in which candy-cane stems have been observed (e.g., S. gigantea and S. juncea). It may well turn out that resistance by ducking is not confined to goldenrods as more plants are observed with an eye toward recognizing novel archi tectural defenses.

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