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Technical Report

Feeding by Adult Spotted Lanternfly Affects Carbon Allocation Postinfestation in Young Grapevines

View ORCID ProfileAndrew D. Harner, Taran K. Rowles, View ORCID ProfileSuraj Kar, Lauren Briggs, View ORCID ProfileMichela Centinari
Am J Enol Vitic.  2025  76: 0760014  ; DOI: 10.5344/ajev.2025.25002
Andrew D. Harner
1The Pennsylvania State University, Department of Plant Science, University Park, PA 16802;
2The Virginia Polytechnic Institute and State University, Alson H. Smith, Jr., Agricultural Research and Extension Center, Winchester, VA 22602;
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  • For correspondence: dharner@vt.edu mzc22@psu.edu
Taran K. Rowles
1The Pennsylvania State University, Department of Plant Science, University Park, PA 16802;
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Suraj Kar
1The Pennsylvania State University, Department of Plant Science, University Park, PA 16802;
3California Polytechnic State University, Wine and Viticulture Department, San Luis Obispo, CA 93407.
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Lauren Briggs
1The Pennsylvania State University, Department of Plant Science, University Park, PA 16802;
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Michela Centinari
1The Pennsylvania State University, Department of Plant Science, University Park, PA 16802;
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Abstract

Background and goals The spotted lanternfly (SLF), Lycorma delicatula White, is an invasive sap-feeding planthopper that can negatively affect grapevine carbon assimilation and allocation, but it is unclear if such negative effects persist postinfestation. This study examined whether adult SLF feeding affects carbon allocation after SLF removal, with the aim to determine if starch storage in young vines was negatively affected by prolonged adult SLF feeding.

Methods and key findings 13C pulse labeling was used to measure 13C content of vegetative tissues in young, container-grown Cabernet franc grapevines. We measured total nonstructural carbohydrates in stems and roots. Feeding by SLF affected carbon allocation: SLF-infested vines had about two times greater 13C content in stems and over four times less 13C in roots than control vines, 12 days after SLF removal. We confirmed that SLF feeding can inhibit carbon allocation to roots, as demonstrated via reductions in root 13C.

Conclusions and significance This study demonstrates that the effects of adult SLF feeding on carbon allocation may persist following SLF removal, suggesting that carbon reserve refilling may be limited following substantial late season feeding. These results highlight the importance of controlling the exposure time of vines to high populations of adult SLF to avoid negative effects on carbon allocation and storage.

  • invasive pest
  • Lycorma delicatula
  • pulse labeling
  • source-sink relationships
  • starch

Introduction

Seasonal assimilation and allocation of carbon can influence the long-term health of woody perennial plants like grapevines. In each season, the demands of carbon for growth, reproduction, and maintenance must be balanced with allocation to carbon reserves. Starch, a major component of carbon reserves in grapevines, is an important source of metabolic energy that supports early-season growth following dormancy (Noronha et al. 2018), as well as plant metabolic responses to biotic and abiotic stressors (Ribeiro et al. 2022), and its storage in plant tissues can shift in response to such stressors. For example, previous work on grapevines indicated that sustained drought conditions can significantly deplete starch reserves (Prats et al. 2023). Similarly, sap feeding by belowground and aboveground insects such as phylloxera (Daktulosphaira vitifoliae Fitch; Griesser et al. 2015, Savi et al. 2019) and spotted lanternfly (SLF) (Lycorma delicatula White; Harner et al. 2022) can significantly alter starch reserves in woody tissues, sometimes with negative consequences for long-term plant health and functioning.

Evaluating how chewing- or sap-feeding insect pests affect assimilation and allocation of carbon is critical to understanding the impacts that insect outbreaks may have on plant health and crop production. Broadly, sap-feeding insects tend to reduce the rate of carbon assimilation in woody plants in natural systems (reviewed in Zvereva et al. 2010). In some cases, these negative effects persist following insect removal, such as in goldenrod (Solidago altissima L.) exposed to feeding by spittlebugs (Philaenus spumarius L.) (Meyer and Whitlow 1992). Patterns of plant starch allocation can also be altered by sap-feeding insects, an effect documented in both woody perennial ornamental species (Soltis et al. 2015) and cultivated species, including grapevines (Griesser et al. 2015, Harner et al. 2022). However, the impact of insect feeding on plant carbon dynamics depends on the timing, duration, and severity of infestation, and long-lasting effects are less studied in sap-feeding than in chewing-feeding insects.

The SLF, a phloem-feeding planthopper native to east Asia, was discovered in the eastern United States in 2014. Resident populations are now present in 18 states and wild and cultivated grapevine (Vitis spp.) are some of its preferred hosts in the quarantine area, among other woody tree species. Recent studies evaluated how woody plant species respond to different infestation scenarios, with a particular focus on plant carbon dynamics. For example, prolonged feeding by adult SLFs negatively affected root starch storage and plant water use in mature grapevines (Vitis vinifera Riesling and Vitis hybrid Marquette; Harner et al. 2022, 2025), and prolonged exposure to feeding by nymph and adult SLFs decreased root starch in several tree species, including silver maple (Acer saccharinum L.) and tree of heaven (Ailanthus altissima (Mill.) Swingle) (Hoover et al. 2023). Exposure to feeding by a high number of adult SLFs (e.g., ≥8 SLFs/shoot) also decreased fruit sugar accumulation in Riesling (Harner et al. 2022) and other V. vinifera cultivars at harvest after one season (M. Centinari and F. Acevedo, unpublished data), and in some instances increased starch concentrations in stems at the end of one infestation season (Harner et al. 2022).

In general, previous work indicated that above- and belowground carbon allocation may be affected in trees and vines exposed to extended late-season adult SLF sap feeding. However, further exploration of the effects on carbon source-sink dynamics in preferred hosts like grapevines is needed. Currently, it is unclear if the effects of prolonged feeding by SLFs on carbon allocation in young, non-bearing vines mimic those reported for mature vines, or whether these effects persist when SLF populations are no longer feeding. Given that adult SLFs infest grapevines late in the growing season, any effects that persist postinfestation could have negative implications for reserve refilling in the fall and vine recovery from potential damage.

The goal of this study was to elucidate how late-season feeding by adult SLFs affects carbon allocation to vegetative tissue sinks in young Cabernet franc (V. vinifera) grapevines after prolonged exposure (37 days). We hypothesized that SLF feeding would alter the pattern of carbon allocation within the plant after infestation ends, leading to accumulation of carbon in aboveground vegetative sinks (e.g., stems) where SLFs were previously feeding, while depriving allocation of carbon to belowground sinks (e.g., roots). This would suggest that vine recovery and belowground carbon reserve refilling postinfestation may be reduced by previous exposure to feeding. Dry biomass and total nonstructural carbohydrates (TNC) in above- and belowground tissues were also measured to confirm the cumulative effects of prolonged SLF feeding on growth and carbon storage in young vines at the whole plant organ level. Overall, this study aimed to contextualize how SLFs affect carbon allocation after periods of heavy feeding by adult SLF.

Materials and Methods

Plant material and experimental design

The experiment was conducted in 2022 at The Pennsylvania State University, in University Park, PA (40°31′N; 77°51′W). Twenty 3-yr-old Cabernet franc (V. vinifera L.) grapevines grafted to 101-14 Mgt (Vitis riparia × Vitis rupestris) rootstock were potted in 2021 in 20-L pots with a custom substrate (1:1:1 field topsoil, perlite, and compost) and grown outdoors at the Russell E. Larson Agricultural Research Center in Pennsylvania Furnace, PA (17 km from the main campus) until the beginning of the experiment. All vines were irrigated using drip irrigation at a rate of 3.8 L/hr for 2 hr every other day, or less frequently, based on rainfall, and fertilized once shortly after budbreak using slow-release fertilizer tablets at a rate of two tablets per vine (Agriform 20-10-5 tablets, ICL Americas). Vines were thinned to an average of three shoots per vine and clusters were removed. Shoots were vertically trained to a trellis. All vines were managed using standard disease management practices common to the eastern U.S., but insecticides were not applied, to avoid potential effects on SLF performance (Wolf 2008).

On 22 Aug 2022, all vines were transported to a greenhouse on campus to enable SLF infestation under controlled conditions and avoid insect escape and infestation of other grapevines at the Agricultural Research Center. Half of the vines were randomly assigned to a zero SLFs (control) treatment (n = 10), while the other half were assigned to a high number of SLFs (15 to 20 SLFs/shoot, equal to 45 to 60 SLFs/vine) treatment (n = 10), in a completely randomized design. The infestation density was chosen to reflect uncontrolled feeding by high SLF populations experienced in commercial vineyards (Leach and Leach 2020). The greenhouse was not equipped with grow lights so all vines were grown under ambient solar radiation conditions. A cooling system was programmed to turn on when the greenhouse temperature reached 28°C during the day and a heating system was programmed to provide heating if nighttime temperatures reached 13°C. While we did not collect air temperature data inside the greenhouse, the outdoor mean daily air temperature measured by a nearby weather station at the Agricultural Research Center was 16.2°C from 22 Aug through 13 Oct. Therefore, air temperature conditions inside the greenhouse were likely within the optimal range of temperatures for adult SLF activity (Nixon et al. 2022).

On the day before SLF infestation (24 Aug), all main shoots were trimmed to 2.0 m and enclosed within 76.2-cm wide × 152.4-cm long insect exclusion netting with zippers (AgFabric, WellCo Industries, Inc.). The netting was tied near the bottom of the vine, leaving 20% (on average) of the shoot’s base and trunk outside of the netting (Supplemental Figure 1). Control vines were also netted to account for any effects of netting on vine microclimate.

Wild populations of adult SLFs of mixed sex were manually collected from untreated woodlots within the quarantine area. Treatment vines were infested with SLFs from 25 Aug to 30 Sept (total of 37 days) to correspond with the seasonal occurrence of peak adult SLF populations in Pennsylvania vineyards (Leach and Leach 2020). Each vine was monitored for SLF mortality three times per week and dead insects were counted and replaced (an average of five SLFs per vine per week) to maintain infestation levels. At the end of the infestation, all SLFs and nets were removed from all vines. Vines were kept in the greenhouse until 13 Oct then placed back at the Agricultural Research Center to cold-acclimate under natural conditions. On 18 Nov, vines were moved to an onsite walk-in cooler to avoid winter cold injury and stored at 4.4°C until the following spring. Vines were removed from the walk-in cooler and destructively sampled to measure root system biomass in June 2023, when labor was available for washing and sampling roots.

Application of 13CO2 and determination of 13C content

Application of 13CO2 occurred in the greenhouse on 30 Sept, immediately after SLFs were manually removed from infested vines. Grapevines were fed with 13CO2 using a method adapted from earlier studies (Morinaga et al. 2003, Frioni et al. 2018). Details of the adapted method can be found in Appendix 1. Six vines per treatment were randomly selected for pulse labeling and the remaining four vines were used as unlabeled controls. Vines from each treatment were randomly paired, so that one control and one SLF vine were pulsed concurrently. A main shoot on each vine was randomly selected and enclosed in a 30-L (88.2 × 76.5 cm) inert plastic bag, covering ~55 to 60% of the total shoot from the shoot apex to the lower portion, including lateral shoots. Five mL of 85% lactic acid (Sigma-Aldrich) was added to a sealed 50-mL centrifuge vial containing 342.8 mg of Na13H-CO3 (99 atomic %13C; Sigma-Aldrich), releasing 13CO2 into the vial headspace. 13CO2 was pumped into the labeling bag and circulated for 30 min using a hand-held suction pump attached via tubing to the vial and the labeling bag. After labeling, the bags were removed and the shoots were exposed to ambient air.

On 12 Oct, when the vines were at Eichhorn-Lorenz (E-L) stage 41 (“after harvest; cane maturation complete”; Coombe 1995), the tissues within each labeling bag (e.g., lateral shoot apices less than 5 cm long, stems and petioles combined, and leaves) were sampled separately from tissues of the same shoot that were outside of the bag, to account for the presence/absence of 13CO2-enriched atmosphere between the two tissue groups. Only the 13CO2-pulsed shoot was sampled for analysis. On the same day, a sample of woody roots between 1.0 and 3.0 mm diameter, representing 0.4 to 1.9% of the total root biomass, was also collected throughout the rooting zone using a trowel, soil knife, and pruners. The roots were washed with deionized water before drying. All tissue samples were dried at 60°C until constant mass was reached. Dry biomass was measured using a benchtop scale (Ranger 3000, Ohaus Corp.). Tissues were milled (<1 mm mesh; UDY Cyclone Mill, UDY Corporation) and mailed to the Cornell University Stable Isotope Laboratory in Ithaca, NY, where 2-mg subsamples were analyzed for 13C. For each tissue, 13C atomic excess (%) and excess 13C content (mg) were determined using calculations outlined in previous work (Morinaga et al. 2003).

Analysis of TNC in stem and root tissues

Concentrations of TNC were measured in stem and root tissues according to a protocol based on Comas et al. (2005) and Marais et al. (1966), with modifications outlined in Appendix 2. Samples of lignified roots (1 to 5 mm) and three stem internode sections from the top, middle, and bottom of the stem were collected on 12 Oct, the same day samples were collected for 13C analysis. Root samples were washed to remove soil, snap-frozen in liquid N2, and stored at −80°C. Samples were lyophilized for 1 wk at −50°C and 10 Pa (FreeZone 12 Liter Freeze Dryer, LabConco) and milled (<1-mm mesh). Two 5-mg subsamples for each tissue type were weighed per vine: one subsample was enzymatically digested using a modified version of the method described by Comas et al. (2005), and the second was used to estimate the reducing sugars present in the undigested tissue matrix. All samples were run in triplicate and averaged. Content of starch, soluble sugars, and TNC were determined for stems and the whole root system by multiplying the respective concentrations by the dry biomass for each tissue.

Single-leaf gas exchange

Gas exchange measurements were conducted once during 1000 and 1400 hr on 29 Sept, one day before application of 13CO2, to ensure that vines were actively assimilating carbon. Three leaves were randomly selected per vine from the upper canopy, representing the most functionally active leaves at that time of the season. The measurements were conducted using a CIRAS-III portable gas exchange system (PP Systems), equipped with a PLC3 universal leaf cuvette with an 18 × 25 mm cuvette window. The CO2 reference was set to 410 ppm, the H2O reference at 11 mb, and the leaf temperature controlled to 25°C. Ambient light conditions (PPFD > 1200 μmol/m2/sec) were used for all measurements.

Statistical analysis

All data were analyzed using SAS 9.4 (SAS Institute, Inc.), with a one-way analysis of variance via PROC GLM. Model assumptions were confirmed with the UNIVARIATE procedure. Data were log-transformed if not normally distributed and the analysis was performed on the transformed data after confirming model assumptions again. For analyses of 13C composition, minimal (0.1 to 2.5 mg) excess 13C was quantified in stem and leaf tissues of the lower, non-pulsed section of the shoot outside the pulse labeling bag; no statistical differences in 13C concentration and content were measured for these tissues (i.e., non-pulsed stems and leaves) between infested and control vines. Stem and leaf tissue biomass and 13C content were thus combined from the upper, pulsed and lower, non-pulsed portions of the same shoot into single samples per vine, respectively, and analyzed and presented together. Graphs were constructed using OriginPro ver. 2024 (OriginLab Corporation).

Results

Effects of SLF feeding on 13C allocation to vegetative tissues following infestation

Single-leaf gas exchange data indicated that both control and SLF vines were actively photosynthesizing the day before application of 13CO2 and there were no differences in any measured parameter between treatments (Supplemental Figure 2). For example, carbon assimilation of control and SLF-infested vines averaged to 9.40 and 8.58 μmol/m2/sec, respectively.

Feeding by adult SLFs affected how 13C was allocated to vegetative tissues of young grapevines late in the growing season, following prolonged (37 days) infestation (Figure 1). Grapevines previously exposed to SLF feeding had more 13C content in stem tissues and less 13C content in root tissues than the control vines 12 days postinfestation (Figure 1). In aboveground tissues, SLF feeding only affected 13C content in the stem (p = 0.010), which was on average 98.4% greater in SLF vines than in control vines (Figure 1A). Comparatively, the average 13C content in root systems of SLF vines was over four times less (p = 0.006) than that of control vines (Figure 1B).

Figure 1
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Figure 1

Excess 13C content in a single 13CO2-pulsed shoot (stem apices, stem, and leaf tissues) and belowground tissues (whole root system) of 3-yr-old Cabernet franc grapevines exposed to zero spotted lanternflies (SLFs) (Control; 0 SLFs/vine; n = 6) or high numbers of adult SLFs (SLF; 15 to 20 SLFs/shoot, or 45 to 60 SLFs/vine; n = 6). Tissues were sampled 12 Oct 2022, 12 days following application of 13CO2 and SLF removal. In both panels, an asterisk indicates a significant treatment difference due to SLF infestation within each tissue (p < 0.001), determined using one-way analysis of variance. Bars show means ± standard errors.

Cumulative effects of SLF feeding on tissue biomass and TNC

Among all the plant tissues analyzed, prolonged exposure to SLF feeding (37 days) only negatively affected dry biomass of the whole root system, which was 32.2% lower than that of control vines (p = 0.001; Figure 2). Exposure to SLF feeding did not affect the biomass of aboveground tissues in the pulsed shoots, such as main and lateral shoot apices (p = 0.865), stems (p = 0.147), or leaves (p = 0.164), even though the average dry biomass of stems and leaves was 20.6% and 20.3% less than in control vines, respectively (Figure 2A).

Figure 2
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Figure 2

Dry biomass of a single 13CO2-pulsed shoot (stem apices, stem, and leaf tissues) and belowground tissues (whole root system) of 3-yr-old Cabernet franc grapevines exposed to zero spotted lanternflies (SLFs) (Control; 0 SLFs/vine; n = 10) or high numbers of adult SLFs (SLF; 15 to 20 SLFs/shoot, or 45 to 60 SLFs/vine; n = 10). The asterisk indicates a significant treatment difference due to SLF infestation (p = 0.001), determined using one-way analysis of variance. Bars show means ± standard errors.

While SLF feeding did not consistently affect above- and belowground tissue biomass, prolonged SLF feeding appeared to more consistently affect concentrations of soluble sugars and starch in these tissues (Figure 3). In stem tissues, grapevines exposed to SLF feeding had 44.5% less starch (p < 0.001) and 21.8% more soluble sugars (p = 0.003) than control vines, resulting in a 33.5% lower concentration of TNC (p < 0.001) overall (Figure 3A). Although still significant, these effects were less pronounced for woody roots, with vines exposed to SLF feeding having 11.1% less starch (p = 0.031) and 15.7% more soluble sugars (p = 0.016) than roots of control vines (Figure 3B). Considered together, this amounted to 9.0% lower concentration of TNC (p = 0.060) in roots of vines previously exposed to SLF feeding, relative to the control vines (Figure 3B).

Figure 3
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Figure 3

Total nonstructural carbohydrate (TNC) concentrations and content in stem tissue of a single 13CO2-pulsed shoot and the whole root system of 3-yr-old Cabernet franc grapevines exposed to zero spotted lanternflies (SLFs) (Control; 0 SLFs/vine; n = 10) or high numbers of adult SLFs (SLF; 15 to 20 SLFs/shoot, or 45 to 60 SLFs/vine; n = 10). Stacked bars represent TNC, comprised of starch and soluble sugars. Asterisks indicate significant treatment effects (p < 0.05) of SLFs feeding on TNC concentrations and content. In stem tissue, Control and SLF had different starch (p < 0.001) and soluble sugar (p = 0.003) concentrations; in roots, there were significant treatment effects for starch (p = 0.031) and soluble sugars (p = 0.016). In stem tissue, Control and SLF had different starch (p < 0.001) and soluble sugar (p = 0.071) content; in roots, there were significant treatment effects only for starch (p < 0.001), and not for soluble sugars. Treatment effects were determined using one-way analysis of variance. Bars show means ± standard errors.

Negative effects of SLF feeding on TNC were more pronounced when examining the TNC content (i.e., the TNC concentration scaled up to the total tissue biomass) of the pulsed stem and the whole root system (Figure 3). Grapevine stems exposed to SLF feeding had 33.8% lower TNC content than control stems (p = 0.006), which was mostly due to these vines also having a 45.1% lower starch content than control vines (p < 0.001; Figure 3C). Root TNC content was 37.4% less in SLF vines than in control vines (p < 0.001; Figure 3D). Again, this effect was driven by changes in starch content, with SLF feeding causing vines to have 38.9% lower starch content than control vines (p < 0.001; Figure 3D).

Discussion

The overall goal of this study was to assess how carbon allocation to vegetative tissues is affected by adult SLF sap feeding in young, non-bearing vines, and whether exposure to adult SLFs has lasting impacts on carbon allocation following insect removal. We demonstrated that SLF feeding can disrupt storage and partitioning of carbon in grapevines during and after infestation.

Prolonged exposure to adult SLF feeding strongly affects root tissues

In this study, both carbon storage and biomass of root systems of young, container-grown grapevines were affected by prolonged SLF feeding. We reported previously that vines exposed to high numbers of adult SLFs for 31 to 42 days had up to 64.7% lower root starch concentration in field-grown 5-yr-old Riesling vines and up to 77% less starch in container-grown 6-yr-old Marquette vines (Harner et al. 2022). Similarly, various young tree species grown in a common garden had up to 51% less root starch when exposed to nymphal and adult SLF feeding for a single growing season than did trees not infested by SLFs (Hoover et al. 2023). Here, we report a relatively smaller impact on root starch concentration in young Cabernet franc vines (11.1% less starch in SLF-infested vines relative to the control). However, we documented stronger negative effects of extensive SLF feeding on starch in stems relative to roots, while our previous work indicated a slight increase in stem starch in mature Riesling vines exposed to adult SLF feeding for 31 days (Harner et al. 2022). It is important to note that Riesling canes were sampled at a different phenological stage (E-L 47), since samples were collected in November after leaf fall and about a month after the removal of SLFs, while Cabernet franc shoots were sampled in October, 12 days postinfestation and before leaf fall (E-L 41). It is possible that the increased starch in Riesling stems may have been due to remobilization of root reserves to canes that had been heavily infested and had their reserves depleted or negatively affected by SLFs. If this is the case, the accumulation of 13C in stems of Cabernet franc exposed to SLF may have also reflected a similar response, but further remobilization was interrupted by the sampling time. We also cannot exclude that shifts in carbon allocation induced by SLF may vary in fruit-bearing versus non-bearing shoots, as a reduction in fruit soluble sugars (e.g., total soluble solids) might alter potential effects on vegetative tissues. Finally, we recognize that trunk tissues are also an important source of reserve carbon that may contribute to overall effects of SLF feeding on TNC reserves, but these tissues were not included within this analysis. Further work to determine the degree of reserve remobilization following SLF infestation is necessary to better understand potential recovery mechanisms.

We report for the first time two additional effects of SLF feeding on root tissues. First, young vines exposed to feeding had a substantially smaller root system biomass (32.2%) than control vines by the end of the season. Second, young vines allocated limited amounts of carbon to the roots following prolonged SLF feeding, as illustrated using a 13C pulse labeling approach. This confirms our hypothesis that heavy SLF feeding can exert a lasting influence on carbon allocation in the time following infestation, and also indicates that a possible recovery and refilling of carbon storage may be limited during this time, at least under the conditions of this study.

The negative effect of SLF feeding on the whole root system biomass could be a cumulative effect of plant-insect competition on potential preferential allocation of carbon resources to aboveground organs. It should be noted that our vines were grown in containers, so we cannot extend these findings to field-grown vines, which can explore a larger soil volume with greater variation in resource availability (nutrients and water). Additionally, shoot biomass was measured on only one out of three shoots (i.e., the 13C-labeled shoot) and did not include the trunk, so it is possible that we did not fully capture the potential impacts of SLF on aboveground biomass. Regardless, belowground impacts on root system size in response to sap-feeding insects have been widely reported in various woody horticultural (e.g., apple, Malus domestica (Borkh.)) and ornamental (e.g., Douglas fir, Pseudotsuga menziesii (Mirbel) Franco) species (Zvereva et al. 2010). We suspect that the reduced root biomass in previously infested vines was due to direct removal of photosynthates and nutrients by SLF feeding and the collective sink strength exerted by these insects. However, it is unclear whether reduced root system biomass was a function of decreased root development and growth or increased root senescence due to resource competition. In some cases, aboveground defoliation and increased sink-strength of aboveground tissues can increase fine root mortality (Eissenstat and Yanai 1997), but the impacts of shifts in plant carbon balance on grapevine roots are complex and changes in root biomass do not always imply phenotypical or functional changes at the whole plant level (Anderson et al. 2003, Klodd et al. 2016). Thus, while we documented reduced root system biomass in young vines exposed to SLFs, it is unclear whether root biomass was decreased to an extent that would have biological implications following a single season of infestation.

Stem accumulation of 13C may reflect a reduced capacity for refilling of root reserves

During the postinfestation period, young grapevines previously exposed to SLF feeding for 37 days displayed different carbon allocation patterns to stem tissues than control vines. The greater 13C content in stem tissues of SLF vines could be due to a few factors. First, it may reflect the incorporation of recently assimilated 13C into defense compounds or cell wall components near where SLFs had previously fed (Guérard et al. 2007). Feeding by SLFs can upregulate transcriptional pathways involved in cell wall reformation and the biosynthesis of cell wall components including cellulose, xyloglucan, and pectin (Islam et al. 2022). Further, stems were sampled 12 days after application of 13CO2, at which point any measurable 13C would most likely represent carbon that was incorporated into structural components of tissues like cell walls (Epron et al. 2012). We cannot rule out that the higher 13C content may also reflect an attempt to refill carbon reserves in aboveground tissues postinfestation, since starch reserves were negatively affected by SLF feeding. However, the overall cumulative reduction in stem starch due to SLFs would indicate that this was insufficient to have a relevant effect. Finally, the accumulation of 13C in stems may have occurred in part because photosynthates were traveling through a highly damaged vascular system (Harner et al. 2022). Typically, plants respond to phloem-feeding insects and phloem-inhabiting bacteria by depositing callose and sealing targeted or damaged phloem sieve elements (Twayana et al. 2022, Welker et al. 2022), and it is likely this is occurring in response to SLFs. Further research characterizing anatomical responses to SLF probing and feeding is necessary to explore whether this can contribute to the altered patterns of carbon allocation that we report here.

Conclusion

By coupling measurements of 13C content and TNC postinfestation, we demonstrated that feeding by adult SLFs for an extended period (37 days) modifies source-sink dynamics by decreasing 13C in root tissues and increasing 13C in stem tissues of 3-yr-old potted Cabernet franc vines. Comparatively, we measured a significant reduction in TNC content (mainly starch) in both roots and stem tissues and a lower root system biomass in vines exposed to SLFs, compared to vines never exposed to SLFs. These results suggest that vines previously exposed to extended SLF feeding may have an impaired ability to refill carbon reserves, even after SLF removal or control. Considered together with our previous work on mature vines under field conditions, our findings underscore the necessity of reducing overall exposure time of vines to high SLF populations, as is practiced in commercial settings. Finally, while outside the scope of this study, these results emphasize the importance of quantifying effects of SLF late-season feeding on the following year’s vine growth and fruitfulness, to provide management recommendations to grapegrowers on potential adjustment of pruning or other management practices.

Supplemental Data

The following supplemental materials are available for this article in the Supplemental tab above:

Supplemental Figure 1 Examples of 3-yr-old container-grown Cabernet franc grapevines netted with insect exclusion netting (AgFabric, WellCo Industries, Inc.). The image was taken on 25 Aug 2022. Grapevines were exposed to zero spotted lanternflies (SLFs) (Control; 0 SLFs/vine; n = 10) or high numbers of adult SLFs (SLF; 15 to 20 SLFs/shoot, or 45 to 60 SLFs/vine; n = 10) from 25 Aug to 30 Sept 2022.

Supplemental Figure 2 Single-leaf carbon assimilation, transpiration, and stomatal conductance (measured on 29 Sept 2022) of 3-yr-old, container-grown Cabernet franc grapevines exposed to zero spotted lanternflies (SLFs) (Control; 0 SLFs/vine; n = 10) or high numbers of adult SLFs (SLF; 15 to 20 SLFs/shoot, or 45 to 60 SLFs/vine; n = 10) from 25 Aug to 30 Sept 2022, a day before application of 13CO2.

Appendix 1 Method for analysis of 13C content in grapevine tissues, modified from previously published protocols.

Appendix 2 Method for extraction and analysis of soluble sugars and starch in grapevine tissues, and modifications made to previously published protocols.

Data Availability

All data underlying this study are included in the article and its supplemental information.

Footnotes

  • This work was supported by the United States Department of Agriculture (USDA) National Institute of Food and Agriculture (NIFA) Specialty Crop Research Initiative CAP Award number 2019-51181-30014 and the USDA NIFA Federal Appropriation under Project PEN0 4958 (Accession number 7006644). The authors thank Don Smith and Scott DiLoreto for assistance with management of greenhouse experiments and Meredith Persico for assistance with developing the 13C pulse labeling protocol.

  • Harner AD, Rowles TK, Kar S, Briggs L and Centinari M. 2025. Feeding by adult spotted lanternfly affects carbon allocation postinfestation in young grapevines. Am J Enol Vitic 76:0760014. DOI: 10.5344/ajev.2025.25002

  • By downloading and/or receiving this article, you agree to the Disclaimer of Warranties and Liability. If you do not agree to the Disclaimers, do not download and/or accept this article.

  • Received January 2025.
  • Accepted April 2025.
  • Published online June 2025

This is an open access article distributed under the CC BY 4.0 license.

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Feeding by Adult Spotted Lanternfly Affects Carbon Allocation Postinfestation in Young Grapevines
View ORCID ProfileAndrew D. Harner, Taran K. Rowles, View ORCID ProfileSuraj Kar, Lauren Briggs, View ORCID ProfileMichela Centinari
Am J Enol Vitic.  2025  76: 0760014  ; DOI: 10.5344/ajev.2025.25002
Andrew D. Harner
1The Pennsylvania State University, Department of Plant Science, University Park, PA 16802;
2The Virginia Polytechnic Institute and State University, Alson H. Smith, Jr., Agricultural Research and Extension Center, Winchester, VA 22602;
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Taran K. Rowles
1The Pennsylvania State University, Department of Plant Science, University Park, PA 16802;
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Suraj Kar
1The Pennsylvania State University, Department of Plant Science, University Park, PA 16802;
3California Polytechnic State University, Wine and Viticulture Department, San Luis Obispo, CA 93407.
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Lauren Briggs
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Michela Centinari
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  • For correspondence: dharner@vt.edu mzc22@psu.edu

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Feeding by Adult Spotted Lanternfly Affects Carbon Allocation Postinfestation in Young Grapevines
View ORCID ProfileAndrew D. Harner, Taran K. Rowles, View ORCID ProfileSuraj Kar, Lauren Briggs, View ORCID ProfileMichela Centinari
Am J Enol Vitic.  2025  76: 0760014  ; DOI: 10.5344/ajev.2025.25002
Andrew D. Harner
1The Pennsylvania State University, Department of Plant Science, University Park, PA 16802;
2The Virginia Polytechnic Institute and State University, Alson H. Smith, Jr., Agricultural Research and Extension Center, Winchester, VA 22602;
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Taran K. Rowles
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Suraj Kar
1The Pennsylvania State University, Department of Plant Science, University Park, PA 16802;
3California Polytechnic State University, Wine and Viticulture Department, San Luis Obispo, CA 93407.
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Lauren Briggs
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Michela Centinari
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  • For correspondence: dharner@vt.edu mzc22@psu.edu
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