Northeastern Naturalist Vol. 26, No. 1 T. Heiselmeyer, A. Boulton, and V. Beauchamp 2019 183 2019 NORTHEASTERN NATURALIST 26(1):183–201 The Relationship Between Native Insects and an Invasive Grass (Oplismenus undulatifolius) in the Mid-Atlantic United States Tamara Heiselmeyer1, April Boulton1,*, and Vanessa Beauchamp2 Abstract - Understanding relationships between insects and invasive plant species in their introduced range is important for management of a new invader and prioritization of its control. This study investigates the insect communities associated with Oplismenus undulatifolius (Wavyleaf Basketgrass), an invasive grass in the mid-Atlantic US, and looks at the effect of herbivory on the species’ growth and reproduction. We surveyed aerial and grounddwelling insect communities in areas with and without Wavyleaf Basketgrass and examined leaf samples from caged and uncaged patches of Wavyleaf Basketgrass for type and amount of insect damage. Insect richness, evenness, and diversity were similar between invaded and uninvaded areas. At the plot level, there was no difference in abundance of insects caught in pitfall traps, but there were more insects captured in sticky traps at the uninvaded area. Orthoptera in general and Rhaphidophoridae specifically, were indicators of uninvaded plots, along with Sciaridae in the Diptera and Scarabaeidae in the Coleoptera. Indicators of the invaded plots included Blattidae within the Blattodea and Staphylinidae and Carabidae within the Coleoptera. Leaf damage was minor; the 6 most heavily damaged leaves lost between 15% and 21% of their leaf area. Punctures, stippling, and mining were the most common types of leaf damage observed, and most leaves had fewer than 25 incidences of damage per leaf. There was no significant difference in leaf damage, plant biomass, or inflorescence production between caged and uncaged plots. Differences in insect community composition in invaded and uninvaded areas may be due to Wavyleaf Basketgrass itself or concomitant increases in plant cover and changes in microclimate. At least some insect groups are using Wavyleaf Basketgrass as habitat, which may be important in areas where excessive deer browse has removed most of the herbaceous layer. Introduction An invasive species is a non-native species that proliferates and spreads when introduced to a new range, often causing economic and ecological damage (Mack et al. 2000, Sakai et al. 2001). Invasive species can affect ecosystems in a variety of ways, including displacement of native species, as seen in the US with the impacts of Dreissena polymorpha (Pallas) (Zebra Mussel) in the Great Lakes (Ricciardi et al. 1998) and Linepithema humile Mayr (Argentine Ant) in the west and southeast (Holway 1999). Other invasive species like Cryphonectria parasitica (Murrill) Barr (Chestnut Blight), Lymantria dispar L. (Gypsy Moth), and Agrilus planipennis Fairmaire (Emerald Ash Borer) directly kill host species, causing shifts 1Environmental Biology, Hood College, 401 Rosemont Avenue, Frederick, MD 21701. 2Department of Biological Sciences, Towson University, 8000 York Road, Towson, MD 21252. *Corresponding author - boulton@hood.edu. Manuscript Editor: Ralph Grundel Northeastern Naturalist 184 T. Heiselmeyer, A. Boulton, and V. Beauchamp 2019 Vol. 26, No. 1 in community composition and dramatic declines of once-dominant forest species (Abrams 1998, 2003; Gandhi and Herms 2010; Nowacki and Abrams 1992). Invasive species can also alter ecosystem properties including nutrient and fire cycles. Myrica faya Ait. (Firetree) has changed nitrogen cycles in Hawaii (Vitousek and Walker 1989), and the spread of exotic annual grasses has altered fire cycles in the western US (Brooks et al. 2004, D’Antonio and Vitousek 1992). Invasive species can affect food webs. Predation on birds by Boiga irregularis Merrem (Brown Tree Snake) on Guam has set off a trophic cascade leading to an increase in spider populations on the island (Rogers et al. 2012), while escaped Python molurus bivittatus Kuhl (Burmese Python) in the Everglades have resulted in the decrease of many prey species (Dorcas et al. 2012). In addition to these sometimes dramatic, top-down effects, invasive species can also exert bottom-up effects on consumers (Harvey et al. 2010), leading to decreased richness and abundance of arthropod and avian species (Ballard et al. 2013, Burghardt et al. 2010, Flanders et al. 2006, George et al. 2013). Negative bottomup effects of invasive plant species on consumers are not universal. The impact of invasive plant species on arthropod communities can vary based on the identity or functional group of the invader, the identity or feeding group of arthropod, or the collateral effects of the invader on community diversity or structure (Bezemer et al. 2014, Fork 2010, Marshall and Buckley 2009, Pétillon et al. 2010, Spafford et al. 2013, Sunny et al. 2015, van Hengstum et al. 2014, Weilhoefer et al. 2017, Wolkovich et al. 2009). The effect of consumers on invasive plant species is still uncertain (Colautti et al. 2004, Hawkes 2007). The enemy-release hypothesis assumes that invasive plants benefit from being exposed to fewer herbivores and pathogens in their introduced ranges (Keane and Crawley 2002) or that they possess traits that allow for resistance or tolerance of herbivores (Puliafico et al. 2008, Strauss and Agrawal 1999, Wang and Feng 2016). Some invasive plant species do support fewer insect herbivore species and experience less damage in their novel ranges than neighboring native plant species (Agrawal et al. 2005, Cappuccino and Carpenter 2005, Carpenter and Cappuccino 2005, Liu and Stiling 2006). However, other community-level studies comparing enemy diversity and herbivore damage have found that the diversity of herbivores and extent of damage they inflict on leaves of non-native plants is often equal to or greater than that experienced by native species in the invaded range (Agrawal and Kotanen 2003, Avanesyan and Culley 2015, Fielding and Conn 2011, Hawkes 2007, Wein et al. 2016). A review by Maron and Vilà (2001) found that native herbivores decreased exotic plant performance by one-third to one-half depending on life stage and caused over 60% of exotic plant mortality. Conversely, some invasive plant species may be able to tolerate herbivory through compensatory growth, with little impact to fitness (Muller-Scharer et al. 2004, Schierenbeck et al. 1994, Strauss and Agrawal 1999, Wang and Feng 2016, Zou et al. 2008). Understanding the relationships between invasive plant species and insects in introduced ranges is important for management in order to predict the ecosystem effects of a new invader and support prioritization for its control (Fork 2010). One Northeastern Naturalist Vol. 26, No. 1 T. Heiselmeyer, A. Boulton, and V. Beauchamp 2019 185 relatively recent plant introduction to the mid-Atlantic US is Oplismenus undulatifolius (Ard.) P. Beav. (Wavyleaf Basketgrass; Barkworth 2010, Beauchamp et al. 2013). This grass species was first discovered in small patches in Patapsco Valley State Park, near Baltimore, MD, in 1996 (Peterson et al. 1999) and it has since spread to thousands of acres across Maryland, Virginia, and most recently, Pennsylvania (Beauchamp et al. 2013, EDDMapS 2018) (Fig. 1). Wavyleaf Basketgrass is a perennial C3 grass, native to tropical and subtropical regions of Asia, Australia, and southern Africa. Reproduction occurs vegetatively via stolons that root at each node, and sexually through the production of unusually sticky seeds that allow for long-distance dispersal on fur, skin, and clothing (Beauchamp et al. 2013, Peterson et al. 1999). In Maryland, Wavyleaf Basketgrass germinates in May, develops inflorescences in July through August, seeds from September through November, and senesces in the winter. Vegetation can stay green under the leaf litter through the winter (V. Beauchamp, pers. observ.). Although an analysis of risk posed by weeds identified Wavyleaf Basketgrass as a “high risk” species (USDA 2012), little research exists on its ecological impact in invaded habitats (Beauchamp et al. 2013). Specifically, no studies have examined whether insects feed on Wavyleaf Basketgrass or if there is a difference in the insect community between invaded and uninvaded areas. In its native range, Wavyleaf Figure 1. Reports of O. undulatifolius (Wavyleaf Basketgrass) sightings in Maryland, Virginia, and Pennsylvania. (a) Data and map from the Early Detection and Distribution Mapping System (EDDMapS 2018). The star indicates the location of initial invasion report and project study site. (b and c) Detail of grass showing characteristic hairs on stem and wavy leaves. (d) Forest understory with high Wavyleaf Basketgrass cover. Panels b–d © V. Beauchamp. Northeastern Naturalist 186 T. Heiselmeyer, A. Boulton, and V. Beauchamp 2019 Vol. 26, No. 1 Basketgrass is a food source for many species of Lepidoptera (e.g., Sugisima 2005), so there is potential for it to attract insect herbivores in its invaded range. A leafhopper, a gall midge, and damage from an unknown leaf miner have been documented on blades of Wavyleaf Basketgrass in Maryland (Fig. 2; Richard Orr, Mid-Atlantic Invertebrate Field Studies, Columbia, MD, pers. comm.). Despite these observations, most Wavyleaf Basketgrass leaves in the field show no visible evidence of insect herbivory or other damage (V. Beauchamp, pers. observ.), although T. Heiselmeyer observed microscopic punctures and small spots of discoloration on leaves during preliminary investigations for this project. The primary objectives of this study were to (1) compare ground-dwelling and aerial insect abundance, richness, and community composition between a stand of Wavyleaf Basketgrass and a nearby uninvaded area, (2) determine if insects feed on Wavyleaf Basketgrass, and (3) measure the impact of insect herbivory on the reproduction and growth of Wavyleaf Basketgrass. Due to the lack of evidence for herbivory in the field, we predicted that the abundance, richness, and diversity of ground-dwelling and aerial insects would be lower in a location invaded by Wavyleaf Basketgrass than in an uninvaded location. We further anticipated differences in the composition of the insect community between invaded and uninvaded areas. Finally, we hypothesized that, due to low levels of insect herbivory, similar amounts of damage would occur to Wavyleaf Basketgrass plants either exposed to or protected from insect herbivory, and that this damage would have minimal impacts on reproduction and growth of Wavyleaf Basketgrass. Methods Field-site description We conducted this study at a site in a deciduous hardwood forest in Patapsco Valley State Park (Fig. 3), near the location of the reputed initial introduction site of Figure 2. Insects and insect damage on Wavyleaf Basketgrass including (a) the leafhopper Tylozygus geometricus (Signoret) (Cicadellidae), (b) wood midges in the Cecidomyiidae (species of Lestremiinae), and (c,d) leaf-miner damage. Panels a–c © R. Orr, Mid-Atlantic Invertebrate Field Studies. Panel d © J. Snitzer. Northeastern Naturalist Vol. 26, No. 1 T. Heiselmeyer, A. Boulton, and V. Beauchamp 2019 187 Wavyleaf Basketgrass in the US (star in Fig. 1; Peterson et al. 1999). The invaded and uninvaded portions of the site used in this study were separated by 3.65 km, and both had an overstory dominated by Liriodendron tulipifera L. (Tulip Poplar) and Fagus grandifolia Ehrh. (American Beech). Odocoileus virginianus Zimmermann (White Tailed Deer) density in the region is very high, varying from 13 to 34 deer/km2 (30 to 95 deer/mi2; MBHWG 2014), resulting in elimination of most native groundcover. The groundcover at the invaded area consisted of a near-monoculture of Wavyleaf Basketgrass (75–100% cover), while the ground in the uninvaded area was largely devoid of vegetation (less than 10% plant cover). Due to the high density of White-tailed Deer, no areas with high abundance of native groundcover exist for comparison with areas of high Wavyleaf Basketgrass cover in this region. Assessment of the insect community We sampled insects in eighteen 1.5 m x 1.5 m plots in the invaded and uninvaded areas of the site (n = 18 at each area for a total of 36 samples). Due to the almost total absence of herbaceous vegetation at the uninvaded area, we did not employ plant vacuum-sampling but focused on ground-dwelling and aerial insect species. This situation of an understory either denuded of vegetation or Figure 3. (a) Location of study site relative to Baltimore, MD and (b) location of invaded and univaded areas studied (stars) within Patapsco Valley State Park. (c) Low (less than 10%) herbaceous cover at uninvaded area due to White-tailed Deer browsing and (d) 70–100% Wavyleaf Basketgrass cover at invaded area. Panel c © V. Beauchamp, and panel d © T. Heiselmeyer. Northeastern Naturalist 188 T. Heiselmeyer, A. Boulton, and V. Beauchamp 2019 Vol. 26, No. 1 dominated by invasive species is typical of areas in Maryland and Virginia invaded by Wavyleaf Basketgrass. Plots at each location consisted of 1 pitfall trap and 1 sticky trap (Leather 2005), and we situated plots at least 30 m apart and at least 30 m from trails and the forest edge. While this distance is sufficient for statistical independence, at least for Carabidae (Digweed et al. 1995), the small scale of this project warrants that our conclusions regarding insect community composition be interpreted conservatively. We constructed pitfall traps with a 240-ml (8-oz) plastic cup buried so its top was set flush with the soil surface and filled with 80 ml (1/3 cup) of propylene glycol plus 1 drop of unscented liquid detergent to break the surface tension. We covered traps with metal flashing designed to leave a small space for insects to enter but prevent debris from falling into the trap. Each sticky trap consisted of a 7.6-cm x 12.7-cm yellow card, sticky on both sides (Stiky Strip Traps 3” x 5”; Bioquip®, Rancho Dominguez, CA), supported by a metal rod standing 25 cm above the ground. We deployed pitfall and sticky traps on 8 June, 13 July, and 14 August 2014 and left them in place for 48 h. We transported all sticky traps and pitfall samples to the lab, where pitfall contents were transferred to vials containing 70% ethanol. We identified adult insects caught in the pitfall and sticky traps using Triplehorn et al. (2005); insects from pitfall traps were identified to family. The gummy substance on the sticky traps distorted many of the captured individuals, making precise identification impossible in many cases, so we identified insects on sticky traps only to order. Due to the recent changes in the taxonomic nomenclature of Hemiptera and Homoptera, we listed all individuals that fell into 1 of these 2 orders as Hemiptera (Triplehorn et al. 2005). We grouped larvae, non-insect invertebrates, and macro-arthropods such as collembolans in the category “unidentifiable”. These taxa comprised less than 10% of all individuals sampled. We scored empty pitfall traps as zero for analysis. We aggregated samples from each plot over all 3 trapping sessions. Insect herbivory We located paired caged and uncaged subplots within the insect-trapping plots at the invaded portion of the study site. We situated the caged and uncaged subplots such that Wavyleaf Basketgrass percent cover was consistent within each pair. Cages measured ~33 cm2 by 1.2 m tall and were covered with mosquito netting. We wrapped metal flashing pushed into the ground around the base of each cage to keep Wavyleaf Basketgrass inside the cage from branching out underneath the netting (Costamagna et al. 2008, Pelletier et al. 2001). Each uncaged subplot consisted of a frame matching the dimensions of the closed cages, but with only netting over the top to mimic the shade cover created in the closed treatment. We erected cages on 31 May 2014 and left them in place until 16 August 2014. We checked cages periodically for structural damage and repaired them as necessary. To determine if insects were feeding on Wavyleaf Basketgrass, we conducted a visual assessment for damage to leaves collected in August from paired caged and uncaged subplots. To collect leaves,we used a 16-cell grid cut from pre-made Northeastern Naturalist Vol. 26, No. 1 T. Heiselmeyer, A. Boulton, and V. Beauchamp 2019 189 plastic trellis that matched the base dimensions of the cages. We placed the grid inside the cage edges, and picked 1 leaf from each cell, which we then pressed, placed in a labeled glassine envelope, and stored in the refrigerator for later analysis. We eliminated leaves from analysis if their tips or bases were broken during collection or processing; a total of 9–12 leaves per caged or uncaged plot were analyzed. We inspected each leaf under a dissecting scope (180x) for evidence of damage from insect herbivory in the form of punctures (P), stippling (S), mines (M), edge chewing (EC), and unknown insect damage (ID). We defined punctures as dark or light, small circular spots with a pin-hole center and a defined border that did not cross veins. Stippling spots were white or had a yellowish hue and were irregularly shaped with no defined border. Mines were distinct trails between the layers of leaf material that crossed veins and were typically irregularly shaped with a yellowish border that sometimes contained frass or larvae. We identified edge-chewing damage as distinct chewing along the leaf edge. We classified all other damage patterns as unknown insect damage. Plant responses We compared inflorescence production and plant biomass between caged and uncaged subplots to determine if insect herbivory had an effect on reproductive effort and growth. We counted the numbers of inflorescences developed within each of the open and closed cages, then used scissors to harvest all stems at ground level within each closed and open cage, dried the cut stems to a constant weight at 70 °C, and weighed them. Data analysis We calculated the Shannon diversity index and evenness for each plot and used Mann–Whitney U tests to compare total insect abundance and order-level richness, diversity, and evenness in sticky traps, and family-level richness, diversity, and evenness in pitfall traps between the invaded and uninvaded area. We conducted Mann–Whitney U tests in SPSS version 23 (IBM Corp. 2015). For each trap type, we adjusted our level of α to account for multiple comparisons. We compared the insect community composition of the invaded and uninvaded areas of the site at the family and order level for the pitfall-trap contents and at the order level for the sticky-trap contents using PERMANOVA with a Sørensen distance measure. We also identified indicator taxa of each group using an indicator- species analysis. Indicator-species analysis compares the relative abundance and relative frequency of the taxa found in each area to identify taxa that are characteristic of invaded and uninvaded areas (McCune and Grace 2002, McCune and Mefford 2006). We conducted both the PERMANOVA and the indicator species analysis in PC-ORD version 5. We compared incidences of insect damage and inflorescence number and vegetation biomass between caged and uncaged subplots. Variables, expect for total damage, did not meet assumptions for parametric statistics and were compared between treatments with Wilcoxon signed-rank tests. We compared total damage between treatments with paired t-test in SPSS version 23 (IBM Corp. 2015). Northeastern Naturalist 190 T. Heiselmeyer, A. Boulton, and V. Beauchamp 2019 Vol. 26, No. 1 Results Insect abundance and community composition We caught more insects in pitfall traps at the invaded area (859) than at the uninvaded area (637) over the study period, but the difference in mean number of insects per plot between areas was not significant (Table 1). We identified 6 orders at each area, which included 21 families at the uninvaded area and 26 families at the invaded area, but this difference was also not significant at the plot level. Hymenoptera (mainly Formicidae), Orthoptera, and Coleoptera were the dominant orders in pitfall traps at both areas. The abundance of insects caught in sticky traps was significantly greater in the uninvaded area when compared to the invaded area of the site, with 3107 insects caught in the 18 uninvaded plots over the 3 sampling periods and 1738 insects caught in the invaded plots (Table 1). Although 5% of the trapped insects could not be identified to order due to distortion of features on the sticky trap, those that could be identified comprised 8 orders at the uninvaded area and 7 at the invaded area. Diptera, Hymenoptera, and Coleoptera were dominant at both areas. There was no difference in insect richness, evenness, or diversity between the invaded and uninvaded plots for either trap type. Comparison of insect communities from the invaded and uninvaded areas indicated that community composition differed significantly between treatments at both the Order and Family levels in the pitfall traps and at the Order level in the sticky traps (Table 2). Indicator analysis of pitfall trap contents at the Order and Family levels identified Orthoptera in general and Rhaphidophoridae specifically, as indicators of uninvaded plots, along with the Sciaridae in the Diptera and the Scarabaeidae in the Coleoptera. Indicators of the invaded plots comprised the Blattidae in the Blattodea as well as Coleoptera in general and the Staphylinidae and Table 1. Area- and plot-level insect abundance and diversity in pitfall and sticky traps in an uninvaded area and an area dominated by O. undulatifolius (Wavyleaf Basketgrass; n = 18 in each area). Comparisons between areas were conducted with Mann-Whitney U tests. Asterisks (*) indicate (mean ± 1 SE) significant differences between invaded and uninvaded areas at the plot level. We adjusted significance levels for multiple comparisons; the critical value of α for pitfall traps = 0.01 and α for sticky traps = 0.0125. Trap type/ Uninvaded Invaded Uninvaded Invaded Variable abundance abundance plot mean plot mean Test Pitfall Total insects 637 859 35.22 ± 4.83 47.67 ± 6.19 U = 125.0, P > 0.05 Orders 6 6 4.50 ± 0.25 4.67 ± 0.20 U = 148.5, P > 0.05 Families 21 26 8.56 ± 0.68 9.39 ± 0.55 U = 132.5, P > 0.05 Diversity (Family) 2.08 2.04 1.71 ± 0.7 1.76 ± 0.08 U = 151.0, P > 0.05 Evenness (Family) 0.69 0.63 0.83 ± 0.02 0.80 ± 0.03 U = 143.0, P > 0.05 Sticky Total Insects 3107 1738 172.61 ± 8.16 96.56 ± 5.35 U = 10.0, P < 0.001* Orders 8 7 4.50 ± 0.17 4.89 ± 0.23 U = 131.0, P > 0.05 Diversity (Order) 0.81 0.81 0.79 ± 0.04 0.78 ± 0.04 U = 153.0, P > 0.05 Evenness (Order) 0.39 0.42 0.53 ± 0.02 0.50 ± 0.02 U = 127.0, P > 0.05 Northeastern Naturalist Vol. 26, No. 1 T. Heiselmeyer, A. Boulton, and V. Beauchamp 2019 191 Carabidae specifically (Table 3). Indicator-species analyses of sticky-trap contents identified Diptera, Hymenoptera, and Coleoptera as significant indicators of the uninvaded area. There were no significant indicators of the invaded area identified in the sticky traps (Table 3). Table 3. Taxonomic composition in pitfall and sticky traps in an uninvaded area and an area dominated by O. undulatifolius (Wavyleaf Basketgrass; n = 18 in each area). Values in parentheses are the percentage of total insects captured at the area level. Plot values are means ± 1 SE. Taxa identified by indicator-species analysis as significant indicators of uninvaded or invaded areas are noted in the indicator column. Only families with >5% of the total insects for either treatment are included, except for Sciaridae which was identified as an indicator of uninvaded plots. Trap type/ Uninvaded Invaded Uninvaded Invaded Taxon abundance abundance plot mean plot mean Indicator Pitfall Blattodea (Blattidae) 24 (4) 84 (10) 1.33 ± 0.24 4.67 ± 0.82 Invaded Coleoptera 148 (23) 226 (26) 8.22 ± 1.14 12.56 ± 1.31 Invaded Curculionidae 57 (9) 34 (4) 3.17 ± 0.72 1.89 ± 0.46 Carabidae 9 (1) 45 (5) 0.50 ± 0.17 2.50 ± 0.57 Invaded Scarabaeidae 9 (1) 0 (0) 0.50 ± 0.15 0.00 ± 0.00 Uninvaded Staphylinidae 20 (3) 69 (8) 1.11 ± 0.38 3.83 ± 0.65 Invaded Nitidulidae 47 (7) 68 (8) 2.61 ± 0.54 3.78 ± 0.52 Diptera 59 (9) 80 (9) 3.28 ± 0.75 4.44 ± 0.92 Drosophilidae 27 (4) 49 (6) 1.50 ± 0.54 2.72 ± 0.61 Sciaridae 20 (3) 4 (less than 1) 1.11 ± 0.36 0.22 ± 0.10 Uninvaded Hemiptera 3 (less than 1) 1 (less than 1) 0.17 ± 0.38 0.06 ± 0.24 Hymenoptera 236 (37) 370 (43) 13.11 ± 2.61 20.56 ± 4.76 Formicidae 229 (35) 361 (42) 12.72 ± 2.55 20.06 ± 4.82 Orthoptera 167 (26) 98 (11) 9.28 ± 1.51 5.44 ± 0.95 Uninvaded Gryllidae 130 (20) 89 (10) 7.22 ± 1.29 4.94 ± 0.83 Rhaphidophoridae 37 (6) 9 (1) 2.06 ± 0.50 0.50 ± 0.17 Uninvaded Sticky Coleoptera 153 (5) 60 (3) 8.50 ± 1.36 3.33 ± 0.68 Uninvaded Diptera 2136 (69) 1234 (71) 118.67 ± 1.22 68.56 ± 4.83 Uninvaded Hymenoptera 564 (18) 256 (15) 31.33 ± 2.20 14.22 ± 1.10 Uninvaded Hemiptera 64 (2) 61 (3) 3.56 ± 0.41 3.39 ± 0.49 Table 2. PERMANOVA comparison of insect species composition from pitfall and sticky traps in an uninvaded area and an area dominated by O. undulatifolius (Wavyleaf Basketgrass). Trap and taxon level Source df SS MS F P Pitfall Area 1 0.2961 0.2961 2.679 0.0364 Order Residual 34 3.7584 0.1105 Total 35 4.0545 Pitfall Area 1 0.5308 0.5308 3.436 0.0048 Family Residual 34 5.2526 0.1545 Total 35 5.7834 Sticky Area 1 0.6676 0.6676 32.662 0.0002 Order Residual 34 0.6949 0.0204 Total 35 1.3625 Northeastern Naturalist 192 T. Heiselmeyer, A. Boulton, and V. Beauchamp 2019 Vol. 26, No. 1 Insect herbivory on Wavyleaf Basketgrass We compared insect damage on leaves between uncaged and caged plots of Wavyleaf Basketgrass at the invaded portion of the site. The number of punctures, mines, and all damage incidences per leaf were about 1.5 times greater in the uncaged plots than in the caged plots, but there was no significant difference in any category of leaf damage between treatments (Table 4). Insect damage on leaves in closed cages may be due to larvae already present in the soil or on the plants when cages were erected in May. One of the caged subplots had an exceptional amount of stippling damage (480 times the average level of damage in the other caged plots). Punctures were the predominant type of damage, comprising 55.1% ± 4.9 SE of all damage incidences in caged plots and 62.3% ± 4.3 SE of all damage incidences in uncaged plots. Leaf damage overall was minor; the 6 most heavily damaged leaves collected for the entire experiment lost between 15% and 21% of their leaf area. Of the 397 leaves used for the damage analyses, 15 showed no damage of any kind, and most leaves had fewer than 25 incidences of damage per leaf. Impact of innsect herbivory on the growth and reproduction of Wavyleaf Basketgrass No measures of plant fitness were significantly different between the uncaged and caged plots. Mean plant biomass and inflorescence production were higher in the closed plots, but these differences were not statistically significant (Table 5). Discussion Insect abundance and community composition To look at differences in insect abundance, diversity, richness, and community composition, we examined an area invaded with >70% cover of Wavyleaf Basketgrass and an uninvaded area with no Wavyleaf Basketgrass and less than 10% total Table 5. Aboveground biomass and inflorescence production of protected (caged) and unprotected (uncaged) O. undulatifolius (Wavyleaf Basketgrass; n = 18 in each area). Variable Caged Uncaged Test Mass (g) 7.62 ± 0.72 6.88 ± 0.78 t(17) = 1.185, P > 0.05 Inflorescences (count per 0.10 m2) 20.22 ± 3.86 18.67 ± 3.93 t(17) = 0.557, P > 0.05 Table 4. Incidences of insect damage on leaves from protected (caged) and unprotected (uncaged) O. undulatifolius (Wavyleaf Basketgrass) patches (n = 18). We adjusted significance levels for multiple comparisons; critical value of α = 0.008. Damage type Caged Uncaged Test Puncture 13.17 ± 1.78 22.36 ± 2.76 Z = -2.286, P = 0.02 Stippling 6.84 ± 6.60 0.58 ± 0.21 Z = -0.471, P > 0.05 Mining 0.11 ± 0.08 0.20 ± 0.08 Z = -1.491, P > 0.05 Edge 0.01 ± 0.01 0.01 ± 0.07 Z = -0.743, P > 0.05 Unknown 8.83 ± 1.05 11.10 ± 1.55 Z = -1.590, P > 0.05 Total 28.97 ± 5.98 34.24 ± 3.45 t(17) = -1.526, P > 0.05 Northeastern Naturalist Vol. 26, No. 1 T. Heiselmeyer, A. Boulton, and V. Beauchamp 2019 193 plant cover. Counter to our hypothesis, there was no difference in plot-level insect richness, evenness, or diversity between the invaded and uninvaded areas for insects caught in pitfall or sticky traps. At the plot level, there was no difference in the abundance of insects caught in pitfall traps. There was a higher number of insects captured per plot in sticky traps at the uninvaded area providing only partial support for our prediction that insect abundance would be higher at the uninvaded area. The number of aerial insects in the uninvaded plots was more than twice the number in invaded plots. There was a paucity of native plant species in the uninvaded portion of the site; thus, the greater abundance of aerial insects was likely driven by the difference in plant biomass between the 2 areas. Sticky-trap yield is greatly impacted by plant density of the area as traps in plant-sparse areas can capture more insects due to increased accessibility (Muirhead-Thompson 2012). We were careful to place sticky traps above the average vegetation line at both the uninvaded and invaded areas to reduce this influence on our capture rates. In contrast, the pitfalltrap data suggest that, overall, the invaded area had greater ground-dwelling insect abundance than the uninvaded plots. We captured nearly 50% more insects at the invaded area compared to the uninvaded area. This difference was not significant at the plot level, due to the high variation in Formicidae among plots in both areas and the high variation in total insects collected per plot at the invaded area; however, the landscape-level (area) pattern suggests that, counter to our hypothesis, insect abundance may be increased by Wavyleaf Basketgrass invasion. Rather than interpreting the area-level increase in ground-dwelling insects at the invaded area as providing evidence of ground-dwelling insects’ preference for invasive Wavyleaf Basketgrass, it is more likely that such species require dense ground-level plant biomass, native or invasive, directly for shelter and nesting and indirectly for food or associated herbivore prey. Heavy White-tailed Deer browsing can cause shifts in leaf-litter invertebrate communities due to changes in forest structure or microclimate (Putman et al. 1989). White-tailed Deer density in the eastern US in general (Horsley et al. 2003) and in our study region specifically (Duguay and Farfaras 2011, Gilgenast et al. 2009) has been elevated above sustainable levels for decades (deCalesta and Stout 1997, Rooney and Waller 2003). In some areas, this situation has led to destruction of the herbaceous understory, except for a few species unpalatable to deer (Putman et al. 1989, Rooney and Waller 2003, Vavra et al. 2007, Waller and Alverson 1997). In areas denuded by high White-tailed Deer populations, a dense carpet of Wavyleaf Basketgrass may be beneficial for ground-dwelling invertebrates and the higher trophic levels that feed on them (Metcalf and Emery 2015, Tang et al. 2012). Extensive field observations indicate that White-tailed Deer do not consume Wavyleaf Basketgrass (V. Beauchamp, pers. observ.). There were some compositional differences in the ground-dwelling insect communities between the invaded and uninvaded areas. As with the abundance data, these differences may be driven by the differences in groundcover between the 2 areas, rather than the presence or absence of Wavyleaf Basketgrass. Other Northeastern Naturalist 194 T. Heiselmeyer, A. Boulton, and V. Beauchamp 2019 Vol. 26, No. 1 studies looking at invasive plant species have also found differences in insect community composition that could be attributed to environmental changes rather than the presence of a specific invader (Metcalf and Emery 2015, Simao et al. 2010, Tang et al. 2012, Weilhoefer et al. 2017). Marshall and Buckley (2009) found similar insect richness and abundance, but different insect community composition, in patches with and without Microstegium vimineum (Trin.) A. Camus (Japanese Stiltgrass), another invasive grass species common in the eastern US. They attributed increases in Acrididae and Gryllidae to overall increases in plant cover and litter nitrogen in invaded patches and decreases in Blattellidae and Chrysomelidae to changes in litter decomposition and decreased abundance of other plant species in invaded patches (Marshall and Buckley 2009). Similar to Marshall and Buckley’s sites (2009), our invaded area had considerably higher groundcover, so it is not surprising to see higher numbers of some ground-dwelling species in the invaded portion of our site. Blattidae, Carabidae, and Staphylinidae were all indicator taxa of the invaded area. Many members of these groups are sensitive to changes in plant biomass, soil moisture, temperature, and humidity (Byers et al. 2000, Stewart 2001) and likely benefited from the increased ground cover provided by Wavyleaf Basketgrass. Our analysis identified Rhaphidophoridae, Scarabaeidae, and Sciaridae as indicators of uninvaded plots. Camel crickets (Rhaphidophoridae) often prefer large patches of bare ground for digging burrows (Clayton 2002); bare ground characterized the uninvaded area of our site. Scarab beetles (Scarabaeidae) are a large, diverse family that occur worldwide in a variety of habitats (McGavin 2002, Triplehorn et al. 2005). Scarabs can be found in soil, mammal dung, rotting wood, or decaying matter, and their presence and distribution can be affected by many factors including dominant flora and fauna, temperature, soil type, soil pH, precipitation, and the supply of excrement (Price 2004). Dark-winged fungus gnats (Sciaridae) are associated with fungus-rich detritus, organic compost, and mushrooms (Merritt et al. 2009). In our system, Wavyleaf Basketgrass may change the quality of the leaf litter and detritus such that it is not preferred or is actively avoided by these species or by the fungi that inhabits it, resulting in low abundances of these groups in invaded areas (Bassett 2014, Motard et al. 2015, Wolkovich et al. 2009). Compositional differences in the aerial insect community between invaded and uninvaded areas at this study site are driven by the higher abundance of Diptera, Hymenoptera, and Coleoptera at the uninvaded area. We recorded nearly double the number of Diptera and more than twice as many Hymenoptera and Coleoptera per plot at the uninvaded area when compared to the invaded area. All other orders had similar abundance or very low abundance at both areas. Insect herbivory and its impact on Wavyleaf Basketgrass Results from our cage study indicate that insects do feed on Wavyleaf Basketgrass, but this activity does not result in a detectable effect on plant biomass or inflorescence production. The presence of trichomes on Wavyleaf Basketgrass stems and leaves may deter herbivory (Speight et al. 2008), but nothing is known Northeastern Naturalist Vol. 26, No. 1 T. Heiselmeyer, A. Boulton, and V. Beauchamp 2019 195 about chemical defenses produced by Wavyleaf Basketgrass. In this study, punctures were the most prevalent damage type; punctures per leaf exceeded other types of damage by more than 150%. These punctures are likely evidence of feeding activity by Hemiptera spp. or oviposition attempts by adult agromyzid flies (C. Eiseman, freelance naturalist, western MA, www.charleyeiseman.com, pers. comm.). Stippling was also common on Wavyleaf Basketgrass leaves, which is evidence of feeding activity by leafhoppers (Hemiptera: Cicadellidae) (Eiseman and Charney 2010). If Wavyleaf Basketgrass produces substances to deter insect feeding, piercing- sucking feeders may be able to avoid toxic compounds stored in vacuoles and minimize exposure to these types of plant defenses. High rates of punctures and stipples in Wavyleaf Basketgrass leaves could also indicate the occurrence of compensatory feeding on a lower-quality food source (Burghardt and Tallamy 2013), or that insects were simply “tasting” this novel food source but not actually feeding (Harrison et al. 2012). Leaf miners, which are more intimately associated with their food sources than piercing-sucking feeders, should be much more sensitive to cellular level plant defenses but may be able to selectively feed on more nutritious tissues that contain lower amounts of fiber and secondary compounds (Connor and Taverner 1997). Leaf mines are regularly observed in Wavyleaf Basketgrass leaves in the late fall, but they appear after seed set and just before above-ground tissues die back in the winter. This phenology makes it unlikely that these leaf mines affect growth and fitness, but further research is needed. Identification of insect herbivores that do decrease the spread, growth, or fitness of invasive plants can suggest possible biocontrol species. Most biological control programs for invasive plant species involve “classical” biological control where host-specific agents are imported from a pest’s native range (Van Driesche et al. 2010); however, insects within the introduced range of a plant can also be used as biological control agents (Cofrancesco 2000). Control with native insects is usually less successful due to interaction with natural predators of these insects or other ecological or environmental factors (Cofrancesco 2000). Identification of native insect herbivores on invasive plant species is a first step in developing biological control agents, but the low levels of herbivory we recorded on Wavyleaf Basketgrass argue against development of a successful native insect biocontrol agent from the current invaded range (Pemberton 2000, Wapshere 1990). A native congener, Oplismenus setarius (Lam.) Mez ex Ekman (Basketgrass), grows in the southeastern US (Weakley 2015) and may harbor insect pests with biocontrol potential for Wavyleaf Basketgrass. Conclusions Our findings from this field experiment confirmed that insects fed on Wavyleaf Basketgrass, but not to an extent that it negatively affected the plants’ growth or inflorescence production. Although insect richness and diversity were similar between invaded and uninvaded areas of our study site, aerial insect abundance was higher at the plot level at the uninvaded area, and ground-dwelling insect abundance was higher at the area level at the invaded portion of the site. One Northeastern Naturalist 196 T. Heiselmeyer, A. Boulton, and V. Beauchamp 2019 Vol. 26, No. 1 major shortcoming of this project is that we were unable to separate the effect on insect communities of Wavyleaf Basketgrass itself from the concomitant increases in plant cover and changes in microclimate associated with Wavyleaf Basketgrass invasion. We can conclude that at least some groups of insects are using Wavyleaf Basketgrass as habitat. In fact, this invasive grass may be particularly important habitat for ground-dwelling insects in areas where much of the herbaceous layer has been removed due to excessive White-tailed Deer browsing. This project was also limited in that it looked at plant–insect interactions over 1 season at 1 site. Further investigations over several seasons and locations are needed to confirm these results. It will also be important to determine the extent that these insects are feeding on Wavyleaf Basketgrass and passing this energy up to higher trophic levels (Tang et al. 2012), and to confirm that insects are able to sustain populations in Wavyleaf Basketgrass invaded areas and that these sites are not functioning as ecological sinks or traps (Battin 2004, Schlaepfer et al. 2005). Acknowledgments We thank the following Hood College faculty and staff for their assistance on this project: Hans Wagner, Kathy Falkenstein, and Drew Ferrier. In addition, we thank Kerrie Kyde for assistance in locating field sites with O. undulatifolius and for extensive comments on an earlier draft of this manuscript. Two other anonymous reviewers also provided helpful comments. 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