TY - JOUR
AU - Koch, Robert L
AB - Abstract The Japanese beetle, Popillia japonica Newman, is an invasive insect to the United States that feeds on turfgrass roots as a larva and the foliage, flowers, and fruit of many major ornamental and agricultural crops, such as apple, as an adult. Despite its generalist feeding behavior, P. japonica shows preferences for certain plant species and cultivars. Classical biological control for P. japonica, including release of Istocheta aldrichi (Mensil), has been pursued in Minnesota. This study was conducted to assess the effects of apple cultivar on season-long abundance of adult P. japonica and their defoliation; and to assess effects of apple cultivar and P. japonica abundance and sex on parasitism of P. japonica by I. aldrichi. Sampling occurred during the summers of 2017 and 2018 on Zestar! and Honeycrisp cultivars in four different apple orchards. Abundance and defoliation of P. japonica was higher on Honeycrisp than Zestar!. Parasitism of P. japonica by I. aldrichi was higher for females than for males. In 2018, the relationship between parasitism of P. japonica and host density varied by cultivar. These findings may help growers determine which apple cultivars should be prioritized for scouting and management efforts and may provide an estimate of potential biological control by I. aldrichi in agricultural areas in the Midwest. Popillia japonica, integrated pest management, cultivar selection, variety selection, invasive species The Japanese beetle, Popillia japonica Newman, which is native to northern Japan (Fleming 1976), was introduced to the United States in 1916 in Riverton, New Jersey (Dickerson and Weiss 1918), and has since spread to most U.S. states east of the Rocky Mountains and five Canadian provinces (CFIA 2020, USDA-APHIS 2018, Shanovich et al. 2019). As larvae, P. japonica is a destructive and costly turfgrass pest, feeding on roots of lawns and athletic fields (Vittum et al. 1999, USDA-NASS 2016). As adults, this insect is a polyphagous pest with records of it feeding on over 300 plant species (Potter and Held 2002). It mainly feeds on flowers and foliage, between leaf veins leaving a characteristic skeletonized appearance (Potter and Held 2002). The significance of this invasive insect in the midwestern U.S. is increasing due to its continued spread and population increase. Popillia japonica is a pest of many agricultural (Shanovich et al. 2019), horticultural, and ornamental plants, including wild and cultivated plants in the Rosaceae family, such as apple (Malus domestica Borkh.) (Rosales: Rosaceae), which are especially favored host plants (Fleming 1972, Potter and Held 2002). Popillia japonica feeds on the foliage of apple trees but has been found to be unable to directly injure intact fruits (Pires and Koch 2020). Despite its generalist feeding behavior, P. japonica shows distinct preferences for certain plant species and cultivars (Hammond et al. 2001, Potter and Held 2002, Gu and Pomper 2008, Hammons et al. 2010, Chandrasena et al. 2012, Shanovich et al. 2019) with nonpreferred plants generally thought to contain feeding deterrents (Potter and Held 2002, Adesanya et al. 2016). Leaves of preferred cultivars generally contain higher levels of nitrogen and sugars, and lower amounts of tannins than less preferred cultivars (Loughrin et al. 1996). Cultivars of ornamental crabapple (Malus spp.) (Rosales: Rosaceae) and commercial apple cultivars have also been reported to differ in attractiveness to P. japonica defoliation (Spicer et al. 1995, Hogmire and Miller 2005). However, besides measurements of defoliation, we are unaware of studies documenting differential populations of P. japonica on crop cultivars in the field. Currently in the U.S., the predominant control method for adult P. japonica is broad-spectrum insecticides, such as carbamates and pyrethroids, because of their efficacy and relatively low cost (Potter and Held 2002, Shanovich et al. 2019). However, classical biological control, including release of Istocheta aldrichi (Mensil) (Diptera: Tachinidae) (synonymous with Centeter cinerea Aldrich and Hyperecteina aldrichi Mensil), has been pursued for this pest (Shanovich et al. 2019). Istocheta aldrichi, which attacks adult P. japonica, was first released in the U.S. during the 1920s. This tachinid is currently known to be established throughout New England (Sabrosky and Arnaud 1965) and parts of Canada (O’Hara 2014, Gagnon and Giroux 2019), but surveys have failed to document it in Arkansas (Petty et al. 2012) and Michigan (Cappaert and Smitley 2002). In Minnesota, I. aldrichi was released in 1998 in the Twin Cities area and has been recovered since 2004 with parasitism of adult P. japonica in urban areas estimated at ~10% (Shanovich et al. 2019). However, to our knowledge, parasitism of I. aldrichi in agricultural areas, such as apple orchards, has not been quantified in the United States. Istocheta aldrichi oviposit on the pronotum of adult P. japonica and are thought to parasitize higher proportions of female P. japonica than males (Clausen et al. 1927). Istocheta aldrichi larvae burrow directly from their eggs into the hosts where they feed on the tissues of the hosts (Clausen et al. 1927). Parasitized P. japonica then burrow into the soil and die soon afterward. Istocheta aldrichi larvae pupate and remain within the dead hosts for about 10 mo before emerging as adults in the next growing season (Clausen et al. 1927). Based on life-history studies, nearly all beetles bearing I. aldrichi eggs die within 6 d of egg deposition by I. aldrichi (Clausen et al. 1927). Since P. japonica is a pest of increasing concern in the Midwest (Shanovich et al. 2019), there is a need for further work to study its ecology and impacts in crops, such as apples, in the region. In this study, we quantified the season-long abundance of adult P. japonica and their defoliation in two popular apple cultivars grown in the Midwest over 2 yrs. To accomplish this, we documented P. japonica season-long abundance using vacuum sampling and visual estimation of defoliation in four conventional apple orchards in Minnesota. We also examined parasitism of I. aldrichi on adult P. japonica in the apple orchards by recording the number of I. aldrichi eggs on the collected P. japonica. Results of this research will provide valuable information on the seasonal dynamics of this pest on important apple cultivars in the Midwest. These findings will help growers to determine which apple cultivars should be prioritized for scouting and management efforts. Additionally, these results will provide an estimate of potential biological control of adult P. japonica by I. aldrichi in agricultural areas for the Midwest. Materials and Methods Research Sites and Experimental Design Popillia japonica reported on here were collected as bycatch in a study focused on natural enemies in conventional apple orchards in southeast Minnesota in 2017 and 2018 (Shanovich et al. 2020). The apple cultivars Honeycrisp and Zestar! were selected for sampling as they represent two popular cultivars grown in the Midwest. Four orchards were sampled, two located in Washington County and two in Dakota County, Minnesota, which will be referred to as WA-1, WA-2, DK-1, and DK-2, respectively. The DK-1 orchard was dropped from the study in 2018 due to removal of their Zestar! trees. All trees sampled were a minimum of 10-yr old (y/o) and grafted on dwarfing Malling and Budagovsky rootstock (standardly abbreviated M and B, respectively). Honeycrisp trees were 14 y/o on M7 rootstock at DK-1, 12 y/o on M26 rootstock at DK-2, 15 y/o on B9 rootstock at WA-1, and 18 y/o on M7 at WA-2. Zestar! trees were 16 y/o on B9 rootstock at DK-1, 12 y/o on M26 rootstock at DK-2, 10 y/o on B9 rootstock at WA-1, and 18 y/o on M7 rootstock at WA-2. All trees were spaced 6 m between rows and 2.5 m within rows, and managed under conventional recommendations for the area (Bordelon et al. 2019). At each orchard, cultivars sampled occurred in blocks of three to six rows, with none of the rows bordering a field edge. Twelve representative trees of each cultivar were sampled every other week, from July through mid-September 2017 and from June through mid-September 2018. Representative trees were chosen at random in each orchard by walking through each cultivar block in a zig-zag fashion between rows and selecting trees of median size; any two trees sampled were a minimum of 9.6 m apart. Sampling Trees for P. japonica Within each orchard, the two cultivars were sampled via vacuum sampling the tree foliage, which is an effective method for sampling arthropods in tree canopies (Bassett et al. 1997). Vacuum sampling was conducted using a modified 400-cfm gas-handheld blower vacuum (Homelite Consumer Products Inc., Anderson, SC) with the upper blower tube and sweeper nozzles attached. The vacuum was modified similarly to that described by Zou et al. (2016), by drilling a hole approximately 8 cm down from the mouth of the sweeper nozzle and inserting a large hexagonal screw into it. A 19-liter mesh paint strainer was inserted inside the sweeper nozzle and affixed to the rim with an adjustable Velcro-elastic band fastened around the nozzle and opening of the paint strainer beneath the screw to prevent the paint strainer from sliding up the nozzle and getting sucked into the vacuum while in use. Vacuum sampling of the trees was conducted every other week from early-July through mid-September in 2017 and from mid-June through mid-September in 2018. The foliage of each tree was vacuumed between 1 and 3 m from the ground for 2 min; 1 min on each side of the row, spending equal time on the inner and outer canopy. After sampling each tree, the contents of the paint strainer were emptied into labeled resealable plastic bag and immediately put on ice upon collection. Samples were then stored in a −18°C freezer until they could be processed. Abundance and Parasitism of P. japonica For each tree and sample date, the number of P. japonica was recorded and each individual was sexed. Because I. aldrichi eggs are readily visible (i.e. distinctive white coloration, relatively large size and reported to be laid on the pronota of adult P. japonica) (Clausen et al. 1927; Fig. 1), we assessed parasitism by the presence of these eggs on the cuticle of P. japonica adults rather than rearing adult tachinids from parasitized hosts. The cuticle of the entire body of each P. japonica adult was visually inspected under a dissecting scope and the number of I. aldrichi eggs on each P. japonica was recorded. To confirm the identity of the eggs, a subsample of 20 eggs from randomly selected parasitized beetles across all samples were sent to LifeScanner (Biolytica Inc., Guelph, Ontario, Canada) for DNA-based species identification (i.e., DNA-barcoding). LifeScanner is a DNA-barcoding service that generates taxonomic identifications through the Barcode of Life Data (BOLD) Systems ID Engine following DNA extraction (Ratnastingham and Herbert 2007). Vacuum sampling has been previously used to estimate parasitism by tachinids (Young 2009). Though I. aldrichi eggs are strongly adhered to the cuticle of P. japonica (HNS, personal observation), this sampling method may have dislodged some small proportion of the eggs resulting in slight underestimates of actual parasitism, but the magnitude of such an effect would likely not differ between sexes of P. japonica or cultivars of apples from which they were collected and therefore would not confound our results. Fig. 1. Open in new tabDownload slide Adult Popillia japonica feeding on Honeycrisp apple leaf exhibiting zonal chlorosis. This P. japonica has an Istocheta aldrichi egg on its pronotum as indicated by the arrow. Photo by HNS. Fig. 1. Open in new tabDownload slide Adult Popillia japonica feeding on Honeycrisp apple leaf exhibiting zonal chlorosis. This P. japonica has an Istocheta aldrichi egg on its pronotum as indicated by the arrow. Photo by HNS. Defoliation From P. japonica Estimates of P. japonica defoliation were made once in mid-September at each orchard in 2018. Defoliation by P. japonica can be distinguished from other insect defoliation due to its distinct skeletonized appearance (Potter and Held 2002). Furthermore, the abundance of other defoliating insects (e.g., Bordelon et al. 2019) was extremely low in the vacuum samples (data not shown); therefore, we are confident that P. japonica was the cause of this defoliation. At each orchard, 10 trees of each cultivar were randomly selected from the representative 12 that were vacuum sampled for visual estimation of P. japonica defoliation. Methods for estimation of defoliation were modified from Spicer et al. (1995) and Kozlov and Zvereva (2018), in which one observer (HNS) rated P. japonica defoliation of the entire canopy for each tree on the following injury rating scale: 1 = 0–0.9% defoliation, 2 = 1–4% defoliation, and 3 = 5–10% defoliation. These ratings were performed by walking around the entire tree, looking at both external and internal canopy leaves, spending ~5 min per tree. Visual estimation of defoliation has been shown to provide accuracy similar to that of image processing and measurements with a grid (Kozlov and Zvereva 2018). Statistical Analysis Since the cultivar Zestar! is harvested about 2 wk earlier than Honeycrisp in Minnesota, comparison of P. japonica abundance and parasitism between cultivars was restricted to the initial sampling date through the harvest of Zestar! (30 August 2017 and 28 August 2018). All analyses were conducted with R, version 3.4.4 (R Core Team 2018) and R Studio, version 1.2.1335 (RStudio Team 2019). Based on the underlying distributions of the counts of P. japonica, years were analyzed separately. A random intercept generalized linear mixed effect model with a negative binomial response (packages, code: lme4, MASS, glmer.nb; Bates et al. 2015, Ripley et al. 2019) and a random intercept generalized linear mixed effect model with a Poisson response (package, code: lme4, glmer; Bates et al. 2015) were used in 2017 and 2018, respectively, to compare P. japonica abundance between cultivars. In each model, cultivar was included as a fixed effect to compare numbers of adult P. japonica per tree per sample date. To accommodate potential spatial or temporal autocorrelation, a random effect for tree nested within orchard (i.e., orchard and the interaction of tree and orchard) was included in the model (Bolker et al. 2009). Furthermore, the fact that we collected (i.e., did not release) the captured P. japonica eliminated the risk of recounting individuals. Likelihood-ratio χ 2-tests were used to assess the significance of the fixed effects on the response (package, code: car, Anova; Fox et al. 2019). In 2018, to see if there was an effect of P. japonica abundance (i.e., density dependence) on the proportion of P. japonica parasitized (i.e., number of P. japonica with at least one I. aldrichi egg/total number of P. japonica), we used a random intercept generalized linear mixed effect model (package, code: lme4, glmer; Bates et al. 2015) with a binomial response and fixed effects for cultivar, sex of P. japonica, the total number of P. japonica, and their interactions. Data points where the number of P. japonica were equal to zero (i.e., no occurrence of P. japonica) were omitted from the analysis to avoid overdispersion and overestimation of no parasitism. In addition, a random effect for tree nested within orchard was included for the same reason described above (Bolker et al. 2009). Correlation coefficients between model variables were checked to make sure no variables were highly correlated (i.e., correlation coefficients were all <0.7); therefore, all variables were included in the model (Dormann et al. 2013). A likelihood-ratio χ 2-test (package, code: car, Anova; Fox et al. 2019) was used to assess the significance of the main effects in the model. Density dependent relationships were confirmed by testing the slopes against zero (package, code: emmeans, emtrends; Lenth et al. 2020). Analyses for 2017 were not performed because parasitism was extremely low. Based on the underlying distribution of the defoliation damage class rankings, a generalized linear model with Poisson response was used to compare P. japonica defoliation between cultivars (package, code: stats, glm; R Core 2018). Cultivar was included as a fixed effect to compare P. japonica defoliation per tree and a random effect was not included. Likelihood-ratio χ 2-tests were used to assess the significance of the fixed effect on the response (package, code: car, Anova; Fox et al. 2019). Results Abundance of P. japonica Across cultivars and years, a total of 2,276 adult P. japonica were collected from 762 samples. In 2017, 1,079 P. japonica (43% females and 57% males) were collected from 311 samples from the two cultivars from early July through the harvest of Zestar! (30 August). Then, after the harvest of Zestar! to mid-September, 19 P. japonica were collected from an additional 60 samples from Honeycrisp. In 2018, 1,197 P. japonica (50% females and 50% males) were collected from 451 samples from the two cultivars from early June through the harvest of Zestar! (28 August). Then, after the harvest of Zestar! to mid-September, 50 P. japonica were collected from an additional 36 samples from Honeycrisp. In each year, the mean seasonal abundance of P. japonica per tree per sample date across orchards was about 9.5× greater in Honeycrisp than Zestar! in 2017 and 6.8× greater in 2018 (Table1). We do not report peak abundances for 2017 as sampling did not begin until July and therefore cannot definitively say when peak abundance occurred (Fig. 2A and B). However, in 2017, at the DK-1 orchard across cultivars, mean abundance of P. japonica was consistently low, never exceeding 1 individual per tree; while all other orchards exhibited a wider range in at least one cultivar (Fig. 2A and B). In 2018, peak abundance of P. japonica in Honeycrisp at each orchard was on 11 July, 17 July and 27 July at DK-2, WA-2, and WA-1 orchards, respectively (Fig. 2C). In Zestar!, peak abundance of P. japonica at each orchard was slightly later, occurring on 24 July, 27 July, and 31 July at DK-2, WA-1, and WA-2, respectively (Fig. 2). Table 1. Results from likelihood-ratio χ 2-tests for main effects on the season-long abundance of adult Popillia japonica, on mean parasitism rate of Istocheta aldrichi on adult P. japonica, and on defoliation by P. japonica in apple orchards in 2017 and 2018 Year . Modela . Main effect . LR χ 2 . df . P-value . 2017 Abundance Cultivar 37.559 1 <0.001 481.400 1 <0.001 2018 Parasitismb Popillia japonica abundance 2.409 1 0.121 Popillia japonica sex 38.145 1 <0.001 Cultivar 0.104 1 0.964 Popillia japonica abundance × Cultivar 8.364 1 0.004 Popillia japonica abundance × P. japonica sex 0.991 1 0.319 Cultivar × P. japonica sex 3.677 1 0.055 Popillia japonica abundance × Cultivar × P. japonica sex 0.972 1 0.324 2018 Defoliationc Cultivar 6.321 1 0.012 Year . Modela . Main effect . LR χ 2 . df . P-value . 2017 Abundance Cultivar 37.559 1 <0.001 481.400 1 <0.001 2018 Parasitismb Popillia japonica abundance 2.409 1 0.121 Popillia japonica sex 38.145 1 <0.001 Cultivar 0.104 1 0.964 Popillia japonica abundance × Cultivar 8.364 1 0.004 Popillia japonica abundance × P. japonica sex 0.991 1 0.319 Cultivar × P. japonica sex 3.677 1 0.055 Popillia japonica abundance × Cultivar × P. japonica sex 0.972 1 0.324 2018 Defoliationc Cultivar 6.321 1 0.012 Parasitism levels were too low to perform analyses in 2017. aTree nested within orchard was included as a random effect in all models, except for defoliation. bCalculated as number P. japonica with at least one I. aldrichi egg/total number of P. japonica. cData on defoliation was not recorded in 2017. Open in new tab Table 1. Results from likelihood-ratio χ 2-tests for main effects on the season-long abundance of adult Popillia japonica, on mean parasitism rate of Istocheta aldrichi on adult P. japonica, and on defoliation by P. japonica in apple orchards in 2017 and 2018 Year . Modela . Main effect . LR χ 2 . df . P-value . 2017 Abundance Cultivar 37.559 1 <0.001 481.400 1 <0.001 2018 Parasitismb Popillia japonica abundance 2.409 1 0.121 Popillia japonica sex 38.145 1 <0.001 Cultivar 0.104 1 0.964 Popillia japonica abundance × Cultivar 8.364 1 0.004 Popillia japonica abundance × P. japonica sex 0.991 1 0.319 Cultivar × P. japonica sex 3.677 1 0.055 Popillia japonica abundance × Cultivar × P. japonica sex 0.972 1 0.324 2018 Defoliationc Cultivar 6.321 1 0.012 Year . Modela . Main effect . LR χ 2 . df . P-value . 2017 Abundance Cultivar 37.559 1 <0.001 481.400 1 <0.001 2018 Parasitismb Popillia japonica abundance 2.409 1 0.121 Popillia japonica sex 38.145 1 <0.001 Cultivar 0.104 1 0.964 Popillia japonica abundance × Cultivar 8.364 1 0.004 Popillia japonica abundance × P. japonica sex 0.991 1 0.319 Cultivar × P. japonica sex 3.677 1 0.055 Popillia japonica abundance × Cultivar × P. japonica sex 0.972 1 0.324 2018 Defoliationc Cultivar 6.321 1 0.012 Parasitism levels were too low to perform analyses in 2017. aTree nested within orchard was included as a random effect in all models, except for defoliation. bCalculated as number P. japonica with at least one I. aldrichi egg/total number of P. japonica. cData on defoliation was not recorded in 2017. Open in new tab Fig. 2. Open in new tabDownload slide Mean abundance of adult Popillia japonica per tree per sample date (collected via vacuum samples) on Honeycrisp (A and C) and Zestar! (B and D) apple trees at Minnesota orchards in 2017 (A and B) and 2018 (C and D). The range of values on the y-axis differ among the panels in this figure. Fig. 2. Open in new tabDownload slide Mean abundance of adult Popillia japonica per tree per sample date (collected via vacuum samples) on Honeycrisp (A and C) and Zestar! (B and D) apple trees at Minnesota orchards in 2017 (A and B) and 2018 (C and D). The range of values on the y-axis differ among the panels in this figure. Parasitism of P. japonica The DNA-barcoding results, generated through BOLD, identified the eggs on the cuticles of P. japonica as Istocheta aldrichi (code number BOLD-3ZMS508K7). Across cultivars and years, a total of 120 P. japonica (5.3%) had at least one I. aldrichi egg on their cuticles and all I. aldrichi eggs were found on the pronota of P. japonica (e.g., Fig. 1). In 2017, only eight P. japonica (~0.01%) were found with I. aldrichi eggs, with each individual having one egg. These parasitized P. japonica were all females, and came from only two of the four orchards (WA-1 and WA-2) and only in Honeycrisp, collected 31 July 2017 and 7 August 2017. In 2018, P. japonica were found with I. aldrichi eggs at all three of the orchards for a total of 112 P. japonica (10.3%) parasitized that year. All the parasitized P. japonica from 2018 had one egg each on their pronota, except for two individuals having two eggs each and one individual having three eggs. The first and last parasitized P. japonica were collected on 25 June 2018 and 21 August 2018 (Fig. 3), respectively. In 2018 in Honeycrisp, peak parasitism of P. japonica by I. aldrichi occurred on 25 June, 3 July, and 12 July at DK-2, WA-2, and WA-1, respectively (Fig. 3A). In Zestar!, peak parasitism of P. japonica by I. aldrichi occurred on 3 July, 11 July, and 27 July in WA-2, DK-1, and WA-1, respectively (Fig. 3B). Fig. 3. Open in new tabDownload slide Proportion of Popillia japonica parasitized by Istocheta aldrichi per tree per sample date on (A) Honeycrisp and (B) Zestar! apple trees at three Minnesota orchards in 2018. Fig. 3. Open in new tabDownload slide Proportion of Popillia japonica parasitized by Istocheta aldrichi per tree per sample date on (A) Honeycrisp and (B) Zestar! apple trees at three Minnesota orchards in 2018. In 2018, season-long mean parasitism was about 4× higher for female P. japonica than males across both cultivars (Table 1). The abundance of P. japonica did not have an effect on the mean proportion parasitism of P. japonica, but the interaction between P. japonica abundance and apple cultivar did have a significant effect on parasitism of P. japonica (Table 1). For male P. japonica, the proportion of parasitized P. japonica remained constant as the abundance of P. japonica increased on both Honeycrisp (Slope: −0.007, Z-ratio: −0.329, P-value: 0.742) and Zestar! (Slope: −0.645, Z-ratio: −0.719, P-value: 0.472), indicating a density independent relationship between male P. japonica and I. aldrichi. For female P. japonica, the proportion of parasitized P. japonica slightly decreased as the abundance of P. japonica increased on Honeycrisp (Slope: −0.031, Z-ratio: −2.324, P-value: 0.020), indicating an inverse density-dependent relationship. However, on Zestar!, the proportion of parasitized female P. japonica increased as the abundance of P. japonica increased (Slope: 0.219, Z-ratio: 2.648, P-value: 0.008) indicating a density dependent relationship. Defoliation From P. japonica Season-long defoliation in 2018 by P. japonica was greater on Honeycrisp than Zestar! (Table 1). The mean damage rating for P. japonica defoliation on Honeycrisp was 2.3 (±0.08 SEM) with damage ratings ranging from 2 to 3 for each tree. The mean damage rating for P. japonica defoliation on Zestar! was 1.4 (±0.09 SEM) with damage classes ranging from 1 to 2 per tree. Discussion Despite the polyphagous nature of P. japonica, variation in attractiveness to P. japonica feeding among closely related plant species and cultivars is known to exist (Potter and Held 2002, Hogmire and Miller 2005, Shanovich et al. 2019). Our results clearly showed differences in attractiveness of apple cultivars to P. japonica, which corroborates previous research findings from Hogmire and Miller (2005). More specifically, to the best of our knowledge, our study provides the first record of P. japonica season-long abundances differing between crop cultivars. Additionally, we found that parasitism of P. japonica by I. aldrichi varies by sex of P. japonica, and with P. japonica abundance depending on cultivar. Mechanisms driving the higher P. japonica season-long abundance and defoliation in Honeycrisp compared with Zestar! apple trees (Fig. 2) remain to be studied but could be due to stimuli at the leaf surface and feeding-induced volatiles. Several studies have found the presence of deterrents to limit host breadth of P. japonica, including cucurbitacins (Tallamy et al. 1997), neriifolin (i.e., a cardenolide) (Reed et al. 1982), phenolic glycosides (Orians et al. 1997), and cyanogenic glycosides (Patton et al. 1997). However, in crabapples (Malus spp.), only one endogenous phenolic compound, phlorizin (i.e., phloridzin), a flavonoid glycoside, was found to be related to P. japonica resistance (Potter et al. 1996). Additionally, many common plant sugars, such as sucrose, fructose, glucose, and maltose have been found to serve as feeding stimulants for P. japonica (Ladd 1986). The cultivar Honeycrisp commonly exhibits a leaf disorder, zonal chlorosis (Fig. 1), in which the leaves accumulate higher levels of nonstructural carbohydrates between predawn and dusk due to lower CO2 assimilation and key enzymes in chlorotic leaves (Chen and Cheng 2004), which could contribute to P. japonica’s preference. Feeding-induced aggregation kairomones on initially colonized and fed upon cultivars may further exacerbate differences in P. japonica abundance and defoliation between cultivars. It is well known that P. japonica exploits volatiles induced by conspecific feeding as aggregation kairomones (Potter and Held 2004). A field study in grapes revealed that grapevines damaged by P. japonica had volatile emissions ~65× greater than from undamaged grapevines and attracted 10–20× more P. japonica than did undamaged grapevines, even when undamaged grapevines were baited with P. japonica (Loughrin et al. 1996). Such effects require further study for P. japonica on apple. Defoliation is a reduction in leaf area (photosynthetic tissue) of a plant, so defoliated trees commonly are assumed to have reduced growth (Pollastrini et al. 2016); with most studies on the topic addressing outbreak levels of plant injury (Kozlov and Zvereva 2018). However, our study found mean whole-canopy defoliation damage ratings were higher for Honeycrisp than for Zestar!. There is accumulating evidence that minor rates of defoliation can affect tree growth and reproduction especially over multiple years (Kozlov and Zvereva 2018, Zvereva et al. 2012). Little is known on the effect of defoliation on fruit and seed production in trees, but several studies have found close relationships between apple yield and total leaf area (Barritt 1989, Palmer 1988). Furthermore, spur (i.e., the shoot complex that normally bears the flower cluster, fruit and lateral bourse shoot) defoliation at bloom and in the month following bloom has been found to decrease flowering and fruit set for that year (Feree and Palmer 1982, Hennerty and Forshey 1971). Additionally, flower bud creation and development for the subsequent year is dependent on light exposure during the 2 mo following bloom (Jackson 1980, Palmer 1989). In Minnesota, apple trees typically bloom in mid-May (Palmer et al. 2003 or https://apples.extension.org/timing-of-apple-tree-bloom/) and adult P. japonica typically begin emerging in mid-to-late June to early July in the Upper Midwest (Hodgson and Kuntz 2013; Shanovich et al. 2019). Therefore, it is unlikely that P. japonica populations in Minnesota could cause a substantial amount of defoliation before the end of June, which is a critical period known to affect the amount of flower buds, and consequently yield for that year (Hennerty and Forshey 1971, Feree and Palmer 1982). We are unaware of any studies that examined effects of defoliation of apple trees later in the growing season on yield or tree health. Furthermore, the phenology of P. japonica defoliation to apple trees remains unknown. Our study examined defoliation by P. japonica near the end of the growing season, which allowed us to get an estimate of the accumulated season-long defoliation, but not the seasonal phenology of this defoliation. We found parasitism by I. aldrichi on P. japonica to be similar in 2018 (9.3%) to that observed by the Minnesota Department of Agriculture (~10%) in Minnesota in 2004 (Shanovich et al. 2019). We found proportion parasitism by I. aldrichi to be about 4× greater for female P. japonica than males in 2018. Furthermore, the small number of P. japonica parasitized by I. aldrichi in 2017 were all females. This finding of greater parasitism of female P. japonica is consistent with observations from Clausen et al. (1927) in Japan, where 80.4–95.9% of parasitized P. japonica were females across years and locations studied. The small number of parasitized P. japonica captured in 2017 may be due to our sampling missing the main window of I. aldrichi activity. Peak parasitism of P. japonica by I. aldrichi on Honeycrisp occurred between 25 June and 12 July in 2018, whereas sampling did not begin until 23 July in 2017. Clausen et al. (1927) suggested an inverse density dependent relationship between parasitism of P. japonica by I aldrichi and abundance of P. japonica to explain the year-to-year differences in observed parasitism. However, across the observed densities, we found that the effect of abundance of P. japonica on parasitism of P. japonica by I. aldrichi depends on cultivar of the host from which the individuals were collected. Upon further examination of these interactions, we can see the slopes of the regression lines for male P. japonica in both cultivars indicate density independent relationships between P. japonica and I. aldrichi, whereas the slopes of the regression lines for female P. japonica indicate an inverse density-dependent relationship in Honeycrisp and a density-dependent relationship in Zestar! (Price 1997). With P. japonica emerging as a crop pest in the Midwest (Shanovich et al. 2019), understanding P. japonica cultivar preferences could help reduce pesticide use and overall costs for growers. The findings of our study could inform integrated pest management plans for P. japonica in apple production; focusing scouting efforts and chemical applications on more susceptible cultivars like Honeycrisp that may be negatively impacted by defoliation over consecutive years. However, more studies on yield impacts of P. japonica defoliation will be needed to understand the potential for economic impact and if chemical treatments are warranted in orchard or other perennial agricultural systems. Growers may expect the natural biological control (i.e., proportion of parasitized individuals) offered by I. aldrichi in agricultural areas to vary from near zero to ~10% of the P. japonica population depending on the year. 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TI - Seasonal Abundance, Defoliation, and Parasitism of Japanese Beetle (Coleoptera: Scarabaeidae) in Two Apple Cultivars
JO - Journal of Economic Entomology
DO - 10.1093/jee/toaa315
DA - 2021-01-27
UR - https://www.deepdyve.com/lp/oxford-university-press/seasonal-abundance-defoliation-and-parasitism-of-japanese-beetle-bszU8AN9Ff
SP - 1
EP - 1
VL - Advance Article
IS - 
DP - DeepDyve
ER -