DOI: 10.1111/eea.12449 Effects of drought stress on oviposition preference and offspring performance of the lace bug Corythucha marmorata on its goldenrod host, Solidago altissima

Maxwell S. Helmberger*, Timothy P.Craig & Joanne K. Itami Department of Biology, University of Minnesota Duluth, 1035 Kirby Drive, Duluth, MN 55812, USA Accepted: 24 April 2016

Key words: plant stress hypothesis, nitrogen, development time, plant-insect interaction, phytophagy, Hemiptera, Tingidae, Asteraceae

Abstract Stress and vigor are endpoints on a continuum of the suitability of plants for insect herbivores. Senes- cence-feeding insects, such as the chrysanthemum lace bug, Corythucha marmorata (Uhler) (Hemi- ptera: Tingidae, Tingitini), are hypothesized to benefit from any stressor hastening the senescence of plant tissues, such as drought. They are also hypothesized to prefer feeding and ovipositing on stressed plants, due to increased performance of themselves and their offspring. We conducted choice and no-choice field-cage experiments to test the effects of drought stress on the oviposition prefer- ence and nymph survival of C. marmorata on its goldenrod host, Solidago altissima L. (Asteraceae). We placed lace bugs on high- and low-water treatment plants, surveyed egg and nymph densities twice weekly, and at the end of the experiment, collected newly developed adults, weighed them, and determined their nitrogen concentration. Low-water treatment plants experienced decreased growth and increased leaf senescence. Lace bug nymphs had significantly greater survival, faster maturation, and higher adult mass on low-water treatment plants than on high-water treatment plants. We observed a non-significant, though consistent trend toward increased oviposition preference for low- water treatment plants. Nitrogen concentrations of lace bugs did not differ by treatment, but lace bugs from low-water treatment plants contained more nitrogen in total due to their higher mass. These results suggest that lace bugs perform better on drought-stressed plants due to mobilization of structural nitrogen increasing the nutritional quality of stressed tissues.

1999). Senescence-feeders, i.e., consumers of mature, Introduction senescing tissues, benefit from plant stress as this hastens Both stressed and vigorous plants can be favorable senescence. Inversely, flush-feeders consume young, grow- resources for various trophic groups of phytophagous ing tissues and thus benefit from plant vigor as this pro- insects (Price, 1991; De Bruyn, 1995; Schowalter et al., motes growth (White, 2009, 2015). Both hypotheses stress 1999). White’s (1976, 1978, 1984) plant stress hypothesis the importance of soluble nitrogen flows out of senescing and Price’s (1991) plant vigor hypothesis have both been tissues and into growing tissues, as those flows grant easy supported by many plant-insect pairs (Pickford, 1966; access to a crucial and limiting nutrient. During plant Craig et al., 1989; De Bruyn, 1995; Fritz et al., 2000; Inbar stress, this nitrogen comes from the breakdown of struc- et al., 2003; White, 2014), with the plant vigor hypothesis tural proteins in tissues slated for senescence (Kemble & accounting for the majority of observations (Cornelissen MacPherson, 1954), while fresh growth receives pulses of et al., 2008). The two hypotheses are valid for plant-insect nitrogen from elsewhere in the plant (Price, 2003). pairs with different insect feeding strategies (Larsson, Phytophagous insects feeding on tissues high in soluble 1989; Price, 1991; Koricheva et al., 1998; Schowalter et al., nitrogen have a distinct fitness advantage (Strong et al., 1984), and so preference for those tissues in feeding and oviposition behavior is expected to evolve. Such prefer- *Correspondence and present address: Maxwell S. Helmberger, ence-performance linkages have been found for numerous Department of Entomology, Cornell University, 2130 Comstock Hall, insect herbivores, including ones benefitting from plant Ithaca, NY 14583, USA. E-mail: [email protected] vigor (Craig et al., 1989; Price, 2003; Scheirs & De Bruyn,

© 2016 The Netherlands Entomological Society Entomologia Experimentalis et Applicata 160: 1–10, 2016 1 2 Helmberger et al.

2005), though results are less consistent for insects feeding and performance exists in C. marmorata, and therefore on drought-stressed plants. Though preference for that females will preferentially oviposit onto whichever drought-stressed plants is often observed (Haglund, 1980; type of plant (stressed or unstressed) their offspring per- Showler & Moran, 2003; Showler & Castro, 2010; Gut- form best on. brodt et al., 2011), the expected increase in performance is not always seen (Showler & Moran, 2003; Gutbrodt et al., Materials and methods 2011; Weldegergis et al., 2014). In general, the occurrence of preference-performance linkages depends on the Experimental setup insect’s life history (Price, 2003) and on characteristics of To measure lace bug preference and performance, we the host plant (Craig & Itami, 2008). transplanted 100 S. altissima rhizomes into 3.8-l pots con- Solidago altissima L. (Asteraceae) is a native, perennial taining Pro-Mix mycorrhizal growth medium (Premier herb common to meadows, abandoned fields, and similar Tech Home & Garden, Mississauga, ON, Canada). Rhi- habitats throughout eastern North America (Semple & zomes were chosen randomly from among eight genotypes Cook, 2006). The senescence-feeding chrysanthemum lace collected as rhizomes from asexual clones near Duluth, bug, Corythucha marmorata (Uhler) (Hemiptera: Tingi- MN, USA and grown at the University of Minnesota dae, Tingitini), is also native to the USA. Overwintering Duluth Research and Field Studies Center. We paired the C. marmorata adults emerge in spring and oviposit on the pots and randomly assigned each pair as a replicate in one underside of S. altissima leaves, after which developing of four categories: (1) no-choice (n = 20), (2) choice nymphs move from leaf to leaf on the same plant, piercing (n = 15), (3) nitrogen-analysis (n = 10), and (4) lace bug- the epidermis and sucking the contents of mesophyll cells free (n = 5). We then randomly designated one plant in (Maddox & Root, 1990). Lace bug feeding causes chlorosis each replicate as high-water treatment and the other as and decreases rates of gas exchange and photosynthesis low-water treatment, though from establishment in the due to parenchyma damage (Buntin et al., 1996). Our pots on 18 June until 7 July 2014, we watered all plants field observations show that the lace bug is multivoltine, equally. We caged the no-choice, nitrogen-analysis, and though likely with fewer generations per year than are lace bug-free pots individually with chicken wire support observed in warmer climates (Kato & Ohbayashi, 2009). and Agribon fabric covering (Polymer Group, San Luis Among sap-feeding insects, most research on how Potosı City, San Luis Potosı, Mexico), whereas the choice drought stress affects insect performance has been done on cages were covered such that a single cage contained both aphids (McVean & Dixon, 2001), and leafhoppers (Hoff- plants of a replicate. All cages were 1 m high with sides man & Hogg, 1992). These studies typically show decreases parallel to the sides of the contained pot(s). Starting 7 July, in insect populations on drought-stressed plants, some- we watered the plants as follows: 39 a week, we measured times despite increases in phloem amino acid content soil moisture content in each pot with a handheld digital (Hale et al., 2003). These and other experimental results, soil moisture meter (OMEGA Engineering, Stamford, CT, contrasted with observational studies linking drought USA), and gave low-water treatment plants 130 ml of stress to outbreaks of sap-feeding insects (White, 1969), water if the soil moisture in their pot was <2%, and 55 ml led Huberty & Denno (2004) to suggest a modification of if it was between 2.0 and 4.9%. We gave high-water treat- the plant stress hypothesis, termed ‘pulsed plant stress ment plants 260 ml if the soil moisture in their pot was hypothesis’. The pulsed plant stress hypothesis states that <10% and 130 ml if not. The goal in our watering was to intermittent drought stress increases insect performance, maintain soil moisture in the low-water treatment pots at particularly that of sap-feeding insects, because increased 5% and at 15% in the high-water treatment pots. We turgor pressure following a return to normal moisture excluded natural rainfall with a manually deployable rain- content allows insects to better exploit the increase in sol- out shelter; on two occasions during the course of the uble nitrogen brought on by periods of stress. Few explicit experiment was the shelter deployed too late to prevent tests of the pulsed plant stress hypothesis exist, and like the some uncontrolled watering. plant stress hypothesis, results are mixed, with some tests on sap-feeding insects failing to support it (Mody et al., Lace bug choice and no-choice experiments 2009; Tariq et al., 2012). We collected wild C. marmorata adults and late-instar We conducted a no-choice experiment to test the nymphs (which developed into adults between collection hypothesis that lace bug performance is increased on and use in the experiment) and stored them in an outdoor drought-stressed plants, and a choice experiment to assess cage containing 12 potted S. altissima plants to ensure ovipositing lace bugs’ preference for stressed or unstressed adequate numbers for the experiment. On 16 July, we plants. We hypothesize that a linkage between preference inserted two males and two females into each choice and Preference-performance on drought-stressed plants 3 no-choice cage. In the choice cages, we placed the lace bugs plant. We used a FlashEA 1112 NC Analyzer (Thermo Sci- on a cardboard platform between the high- and low-water entific, Waltham, MA, USA) to determine the nitrogen treatment plants, allowing them to choose a plant to feed concentration of all leaf and lace bug samples. and oviposit on. In the no-choice cages, we placed the lace bugs directly onto the single plant. Twice each week there- Statistical analysis after, we counted the lace bug eggs, nymphs, and adults We used a repeated-measures MANOVA in JMP v.12 present on each plant. The counts continued until 12 (SAS Institute, Cary, NC, USA) to analyze variation in September, when a threat of frost forced us to collect the eggs, nymphs, and adults among treatments in the choice lace bugs for further analyses and terminate the field and no-choice experiments. MANOVA is recommended experiments. We calculated lace bug survival percentage instead of ANOVA when the assumption of compound on each no-choice plant as its maximum number of symmetry is violated (Zar, 1996), and preliminary analysis recorded adults divided by its maximum number of using the Mauchly criterion indicated that this assumption recorded eggs. We did not calculate lace bug survival on was not met. Moisture treatment was the between-subject choice plants because adults can move between the two variable, and sample period and the interaction of sample plants in a cage, and determining an adult’s plant of origin period and moisture treatment were within-subject vari- is not possible. ables. To test for differences in the proportion of lace bugs that Plant morphology and physiology surveys survived from egg to nymph, from nymph to adult, and On 7 and 13 July, we measured the stem height of all no- from egg to adult in each treatment, we divided the sum of choice, choice, and lace bug-free plants and counted the all individuals counted in one stage on all sampling dates green, yellow, and dead leaves on each. We defined green by the sum of all individuals in the earlier stage. This over- leaves as those with >50% green tissue, dead leaves as those estimated the absolute number of individuals in each stage, with >50% brown and dry tissue, and yellow leaves with because some individuals were counted in multiple sur- >50% yellow tissue or >50% yellow and brown tissue but veys, but was assumed to provide an accurate estimate of <50% brown tissue. We conducted final surveys in the the proportion that survived from one stage to another. same manner at the end of the experiment. We then arcsine-square root transformed the proportion At the end of the experiment, we harvested and dried a data to normalize the variance, and tested for the differ- subsample of choice, no-choice, and nitrogen-analysis ence in means of the treatments with a one-way ANOVA. plants and determined the ratio of aboveground mass to Using R v.3.1.2 (R Development Core Team, 2014), we belowground mass by weighing. We also separately used a two-way ANOVA to test for effects of water treat- weighed each plant’s current-year rhizome growth and ment and lace bug sex on average individual dry mass and determined the percentage of new rhizomatous mass (new average individual nitrogen content between the lace bug rhizome mass divided by total mass). composites, after checking the assumptions with the Sha- piro-Wilk test for normality and Bartlett’s tests of homo- Nitrogen analysis of plants and adult lace bugs geneity of variance. We then used a Tukey’s Honest We took two green, undamaged leaves from each nitro- Significant Difference test to determine which of the four gen-analysis plant prior to imposing the various water composite types (high-water treatment female, high-water treatments, and again at the end of the experiment. Fol- treatment male, low-water treatment female, and low- lowing collection, we dried the leaves for 48 h at 65 °C water treatment male) differed significantly from the before cutting them into small slivers. On 12 September, others in average mass and nitrogen content. To determine we removed all adult lace bugs from the no-choice plants the effects of treatment and sex on nitrogen concentration, and dried them at 60 °C following separation of males and we used a Kruskal–Wallis rank sum test, as the assump- females. Individual lace bugs lack sufficient mass for nitro- tions for an ANOVA were not met. We then used the gen analysis, so we pooled multiple lace bugs into a total of ‘PMCMR’ package in R (Pohlert, 2014), to conduct a nine composites, two of high-water treatment males, two Kruskal–Wallis post-hoc test after Nemenyi in the same of high-water treatment females, two of low-water treat- fashion as the Tukey’s test above. ment males, and three of low-water treatment females. We conducted unpaired t-tests to determine the signifi- Composites comprised 20–58 individuals and 2.6–5.3 mg cance of differences in plant growth and aboveground:be- in mass. Average individual dry masses for the lace bugs in lowground mass ratio, and percent change in leaf nitrogen each composite were obtained by dividing the total mass concentration between treatments, after confirming nor- of the composite by its number of lace bugs. No two com- mality with Shapiro–Wilks tests. We assessed homogeneity posites contained lace bugs of the same sex from the same of variance with F-tests and adjusted the t-tests 4 Helmberger et al. accordingly. One of the 10 low-water treatment nitrogen- analysis plants died between initial and final leaf sampling, and so it was not included in the analysis, leaving 10 high- water and nine low-water plants to analyze. The new rhi- zome mass percentage data and final dead leaf percentage data were not normally distributed, and so for those data we used Wilcoxon rank sum tests to assess differences between treatments. We also conducted linear regression analysis to relate the mean soil moisture (as an estimate of water availability and subsequent drought stress) of each no-choice plant’s pot and each plant’s final dead leaf percentage (a second proxy for drought stress) to the plant’s lace bug survival percentage. We arcsine-square root transformed all per- centage data before analysis, and confirmed normality of the linear model residuals via the Shapiro–Wilk test.

Results Soil moisture readings The mean of soil moisture values for all plants across all measuring dates for low-water treatment plants was 4.8%, with a 95% confidence interval of 4.5–5.1%. For high- water treatment plants, this was 13.5% (95% CI = 13.0– 14.1%).

Plant morphology and physiology surveys High- and low-water treatment plants did not differ until the end of the experiment. Low-water treatment plants Figure 1 Effect of high- and low-water treatment on goldenrod grew less than high-water treatment plants Æ = Æ Æ (A) plant growth (% stem height increase) and (B) leaf (mean SE 34.4 1.8 vs. 49.3 2.6% height senescence (% dead leaves at end of experiment). Box lower = = increase; two-sample t-test: t 4.57, d.f. 77) and had margin, inside line, and upper margin represent 1st quartile, Æ higher percentages of dead leaves (31.1 1.1 vs. median, and 3rd quartile respectively. Whiskers represent upper 23.1 Æ 1.4%; Wilcoxon rank sum test: W = 297.5, both and lower bounds of the data, and circles represent outliers. P<0.0001; n = 79) (Figure 1). In addition, low-water treatment plants allocated a smaller proportion of their higher as well on low-water treatment plants on most sam- biomass to new rhizomatous growth during the 2-month ple dates (Table 1, Figure 2B), but this difference was not period than high-water treatment plants (0.7 Æ 0.2 vs. significant either (repeated measures multiple ANOVA: Æ = 12.9 1.1%; Wilcoxon rank sum test: W 271, F1,28 = 0.035, P = 0.85). P = 0.0018) and had higher aboveground:belowground mass ratios (1.3 Æ 0.1 vs. 0.9 Æ 0.1%; two-sample t-test: t = 3.22, d.f. = 35, P = 0.0028; both n = 37). Table 1 Repeated measures multiple ANOVA of the effects of treatment (high- or low-water), sampling date, and their interac- Lace bug choice experiment tion on the number of chrysanthemum lace bug eggs and nymphs Sample date had a significant impact on the number of on each goldenrod plant in the choice experiment eggs and nymphs, and neither water treatment nor the interaction of treatment and sample date had a significant No. eggs No. nymphs effect (Table 1). On all sample dates, 5–105% more eggs Source d.f. F P d.f. F P were laid on low-water treatment plants than on high- water treatment plants (Figure 2A), yet this difference was Moisture 1,28 0.923 0.34 1,28 0.0350 0.85 not significant (repeated measures multiple ANOVA: Date 7,22 4.04 0.005 8,21 12.32 0.002 Moisture*date 7,22 0.746 0.64 8,21 0.8813 0.55 F1,28 = 0.923, P = 0.34). Nymph numbers were slightly Preference-performance on drought-stressed plants 5

Figure 2 Mean (Æ SE) numbers of chrysanthemum lace bug (A) eggs and (B) nymphs on low-water treatment (open circles) and high-water treatment (closed circles) goldenrod plants in the choice experiment. Neither egg nor nymph numbers differed significantly between treatments.

Lace bug no-choice experiment Adult numbers were higher on low- than on high-water treatment plants (Table 2, Figure 3C), but the water treat- ments had no significant effect on egg or nymph numbers Figure 3 Mean (Æ SE) numbers of chrysanthemum lace bug (A) (Figure 3A,B). Egg, nymph, and adult numbers were all eggs, (B) nymphs, and (C) adults on low-water treatment (open influenced by sample date. Egg numbers were slightly circles) and high-water treatment (closed circles) goldenrod higher on the low-water treatment on all but one date, and plants in the no-choice experiment. Neither egg nor nymph there was no significant interaction between water treat- numbers differed significantly between treatments, though when ment and sample date. We first observed nymphs on 1 new adults began developing, low-water treatment plants held August, and nymph maturation continued throughout the more adults during all sampling periods except the last.

Table 2 Repeated measures multiple ANOVA of the effects of treatment (high- or low-water), sampling date, and their interaction on the number of chrysanthemum lace bug eggs, nymphs, and adults on each goldenrod plant in the no-choice experiment

No. eggs No. nymphs No. adults Source d.f. F P d.f. F P d.f. F P Moisture 1,38 0.219 0.64 1,38 0.005 0.94 1,38 4.42 0.042 Date 7,32 9.547 <0.001 9,30 8.99 <0.001 5,34 9.50 <0.001 Moisture*date 7,32 0.6923 1.0 9,30 2.166 0.054 5,34 1.8 0.14 6 Helmberger et al.

Figure 4 Scatterplot relating mean soil moisture (%) in each no- choice experiment goldenrod plant’s pot to the survival (%) of chrysanthemum lace bugs upon that plant. y = À0.5818x + 0.7191, r2 = 0.10, P = 0.031.

Table 3 ANOVA of the effects of goldenrod water treatment (high- or low-water), chrysanthemum lace bug sex, and their interaction on adult lace bug mean mass (lg) and individual nitrogen content (lg)

Adult mass Nitrogen content Source d.f. F P F P Treatment 1 48.01 0.001 86.35 <0.001 Sex 1 28.33 0.003 15.53 0.011 Treatment*sex 1 1.04 0.35 0.39 0.56 Error 5 Total 8 remainder of the experiment. Nymph numbers were higher on low-water treatment plants during the early sample dates and then shifted to being higher on high- water treatment plants during the last three sample dates, and the interaction of water treatment and sample date was marginally non-significant for nymphs (Table 2). We first observed newly developed adults on 22 August and saw more new adults on each subsequent sample date. New adult numbers were higher on low-water treatment plants on all dates except the last. Figure 5 Mean (+ SE) individual (A) mass (lg), (B) nitrogen The probability that lace bugs would survive from eggs content (lg), and (C) nitrogen concentration (%) for to adults was significantly higher in the low-water treat- chrysanthemum lace bug composites segregated by water ment than in the high-water treatment treatment of the goldenrod host plants (low, high) and sex (mean Æ SE = 49.1 Æ 3.1 vs. 38.5 + 2.2%; one-way (female, male). Means within a panel capped with different letters < ANOVA: F1,36 = 8.20, P = 0.007). The difference was due are significantly different [mass, N content: Tukey test: P 0.05; N to greater survival of nymphs to the adult stage on low concentration: Tukey and Kramer (Nemenyi) test: P<0.05]. water treatment plants (43.4 Æ 1.9 vs. 36.1 Æ 1.5%; one- way ANOVA: F1,36 = 5.31, P = 0.03). Survival of eggs to Lace bug survival decreased with increasing soil mois- the nymph stage did not differ significantly between treat- ture (y = À0.5818x + 0.7191, r2 = 0.10, P = 0.031; Fig- ments. ure 4) and increased with the proportion of dead leaves Preference-performance on drought-stressed plants 7 on their plant (y = 0.5549x + 0.2488, r2 = 0.16, where performance was higher, but this preference was not P = 0.0069; both n = 38). statistically significant. In the no-choice experiment, lace bug survival Nitrogen analysis of plants and adult lace bugs decreased as soil moisture increased. We found no differ- Despite the low sample sizes (n = 3 for low-water treat- ence in survival between the egg and nymph stages; ment females and n = 2 for all other treatment*sex com- however, survival from nymphs to adults was higher on binations), both water treatment and lace bug sex, but not low-water treatment plants, and there was a significant dif- their interaction significantly affected lace bug dry mass ference in adult numbers between treatments. Given that and total nitrogen content (Table 3, Figure 5). Lace bugs the plant stress hypothesis cites food quality as the reason from low-water treatment plants were heavier than those for increased performance on stressed plants, it is not sur- from high-water treatment plants, and females weighed prising that survival differences only became apparent more than males (Figure 5A). Low-water treatment lace once the lace bugs began to feed. The difference in adult bugs had higher individual nitrogen contents than high- emergence curves on high- and low-water treatment plants water treatment lace bugs, and females had higher nitrogen indicated somewhat faster development on stressed plants. contents than males, due to their higher mass (Figure 5B). This may be due to increased nutritional quality of stressed Nitrogen concentration was significantly affected by sex tissues, though increased nutrient concentrations do not (Kruskal–Wallis rank sum test: v2 = 6, d.f. = 1, always increase development rates (Stamp, 1990). The P = 0.014), but not by treatment (v2 = 2.16, d.f. = 1, number of adults on low-water treatment plants increased P = 0.14), with males having overall higher nitrogen con- more rapidly and peaked earlier than on the high-water centrations than females. Of the four sex*treatment com- treatment plants. Earlier development can itself increase posite types, only the difference in nitrogen concentration fitness as faster achievement of the adult stage leads to a between low-water females and high-water males was sig- shorter generation time, increasing population growth nificant [Nemenyi (Tukey-type) multiple comparisons potential and increasing the chance that a lace bug popula- procedure: P = 0.046; Figure 5C]. tion can produce diapausing adults before the onset of Nitrogen concentration decreased in plants of both winter. The greater body mass of lace bugs raised on low- treatments over the course of the experiment, from an ini- water treatment plants also implies a fitness advantage to tial (mean Æ SE =)1.35Æ 0.07% N to a final feeding on stressed tissues, as a larger body size can 0.97 Æ 0.06% N for low-water treatment plants and from increase insect fecundity (Denno & McCloud, 1985; 1.51 Æ 0.11 to 1.10 Æ 0.11% N for high-water treatment Honek, 1993) and overwintering survival (Ohgushi, plants. The magnitude of the decrease did not differ signif- 1996). However, further research would be required to icantly between treatments (low-water: 26.9 Æ 19.0%, confirm these associations for C. marmorata, as the for- high-water: 25.6 Æ 26.9%; two-sample t-test: t = 0.73, mer does not always hold true (Leather, 1988), and few d.f. = 17, P = 0.48; n = 19). data exist on the latter. The lack of significant differences in leaf sample nitro- Discussion gen concentrations between treatments was likely due to our analysis of green leaves only, whereas nitrogen mobi- Plant drought stress significantly altered plant growth and lization happens mostly during leaf senescence (Feller & lace bug performance, while producing a non-significant Fischer, 1994). As such, the greater senescence on low- but consistent increase in lace bug preference. The low- water treatment plants is reflective of increased mobiliza- water treatment decreased plant growth and final plant tion of soluble nitrogen, thus leading to increased perfor- height, increased leaf senescence, and decreased under- mance of the senescence-feeding lace bugs raised on those ground biomass allocation compared to the high-water plants. The higher mass and nitrogen content of low-water treatment, indicating that drought stress significantly treatment lace bugs is consistent with the capture of more altered plant physiology. In the no-choice experiment, off- nitrogen from plant tissues. Nitrogen concentrations were spring performed better on low-water treatment plants, lower in females than in males, and we hypothesize that consistent with the plant stress hypothesis. Continuous this is due to females allocating nitrogen to eggs that they water deprivation positively impacted lace bug perfor- had oviposited onto the plant (Barry & Wilder, 2013). mance, which is not consistent with the pulsed plant stress However, without specific data on leaf soluble nitrogen or hypothesis (Huberty & Denno, 2004), although we did not amino acid content, we cannot definitively state that explicitly test this hypothesis by including a pulsed stress increased available nitrogen is the only factor influencing treatment in our experiment. In the choice experiment, lace bug success on our stressed plants. Other factors, such there were consistently more eggs on low-water plants, as changes in plant secondary metabolites (Gershenzon, 8 Helmberger et al.

1984), may have affected lace bug preference and perfor- experience. Lace bug development from egg to adult takes mance on drought stressed plants. However, although a mean of 22 days in Duluth (Y Sakata, TP Craig, JK Itami, drought stress can reduce plant defenses (Gutbrodt et al., M Yamasaki, & T Ohgushi, unpubl.). Plant stress during 2011), increases in defensive compounds can also occur oviposition may have not been sufficient to significantly (Gershenzon, 1984; English-Loeb et al., 1997). influence oviposition preference, but later it was severe We did not find statistically significant support for the enough to influence survival to the adult stage. It is possi- prediction that natural selection should result in oviposi- ble that the impact of drought stress is so unpredictable tion preferences positively correlated with offspring per- that lace bugs cannot evolve a positive preference-perfor- formance. Performance was higher on drought-stressed mance relationship, or simply that this experiment failed plants, and in the choice experiment more eggs were con- to produce a noticeable effect of drought stress during the sistently deposited on drought-stressed plants, but these period of oviposition. Further experiments that vary the differences were not significant. Several factors other than severity and timing of drought stress are necessary to fully drought stress may have influenced host preference in our understand the preference-performance relationship in experiment, thus obscuring the relationship between plant C. marmorata. drought stress and oviposition preference. First, the Understanding preference, performance, and their rela- impact of plant genotype on lace bug preference and per- tionship is key to understanding herbivorous insect popu- formance was not measured, and this has been demon- lation dynamics (Price, 2003), and understanding these strated to influence goldenrod’s resistance to other population dynamics on drought-stressed plants of partic- herbivores (Maddox & Root, 1987; Craig et al., 2011). Sec- ular interest. We have shown that lace bug performance ond, the impact of lace bug feeding on subsequent oviposi- improves on drought-stressed plants, and ours and other tion preference was not assessed. In Japan, where lace bugs results (Cappuccino & Root, 1992; Smith-Fiola, 2004) can reach very high densities (Sakata et al., 2014), high provide some indication that lace bugs prefer to oviposit levels of lace bug damage can reduce subsequent oviposi- on drought-stressed plants. Past tests of the preference- tion preference (TP Craig, JK Itami, & T Ohgushi, performance hypothesis have produced highly variable unpubl.), whereas moderate levels can stimulate more results (Thompson, 1988; Craig et al., 1989; Craig & Itami, feeding and oviposition (Craig, 2010). Third, we did not 2008; Gripenberg et al., 2010), and negative results for measure the influence of solar insolation or temperature, some other S. altissima herbivores (Craig et al., 1999; which can affect insect development rates (Begon, 1983; Craig & Itami, 2008). On drought-stressed plants specifi- Stamp, 1990; Cappuccino & Root, 1992). Our high- and cally, positive linkages have been shown for some chewing low-water treatment plants received equal sunlight and insects, such as grasshoppers (Lewis, 1984) and caterpillars ambient temperatures; we induced drought stress solely by (Mody et al., 2009), but many other studies find correla- withholding water. In contrast, drought-stressed plants in tions between preference for and performance on natural environments may be found in brighter, hotter drought-stressed plants to be absent or even negative locations than unstressed plants in the same local area. (Showler & Moran, 2003; Gutbrodt et al., 2011; Weldeger- However, despite identical light and temperature condi- gis et al., 2014). Because of extensive previous research tions, we observed faster development on low-water treat- and the relative ease of manipulating drought stress and ment plants, indicating an effect of drought stress measuring its impact on the plant and insect, the lace bug- independent of temperature. goldenrod system is ideal for gaining further insight into The timing and severity of drought stress may have also the importance of plant drought stress on oviposition influenced the relationship between oviposition preference preference and offspring performance. Further research on and offspring performance. In particular, oviposition this interaction should examine wider ranges of timing choices were made at the start of the experiment when and severity of drought stress, as well as the impact of other drought stress had just been initiated, but performance factors, such as plant genotype, on lace bug preference and was affected all throughout the experiment, as the differ- performance. ences between plants grew starker. When females made their oviposition decisions, some of the low-water treat- Acknowledgements ment plants may not have been stressed to the point at which females could have detected differences between This project was made possible through a University treatments. Craig & Itami (2008) hypothesized that posi- of Minnesota Duluth Biology Undergraduate Research tive preference-performance linkages cannot evolve when in Science and Technology fellowship to MS Helm- resource quality at the time of oviposition is not an accu- berger and a grant from the National Science Founda- rate predictor of the resource quality that offspring tion DEB 0949280 to TP Craig and JK Itami. The Preference-performance on drought-stressed plants 9 authors would like to thank J Welch, P Miller, and D Feller U & Fischer A (1994) Nitrogen-metabolism in senescing Johnston for assistance in the design, construction, leaves. Critical Reviews in Plant Sciences 13: 241–273. and conduction of field experiments. W Licht’s previ- Fritz RS, Crabb BA & Hochwender CG (2000) Preference and ous unpublished efforts in lace bug research served as performance of a gall-inducing sawfly: a test of the plant vigor – a guide for the present study. B Dewey and J Pastor’s hypothesis. 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