Laboratory feeding and fecundity bioassays, and field defoliation surveys were conducted on 73 Ulmus and eight Zelkova taxa to determine their relative susceptibility, preference, and suitability for the adult Japanese beetle (Popillia japonica Newman). Ulmus alata Michx., U. crassifolia Nutt., U. davidiana Planch., U. elliptica K. Koch, , U. glabra Hudson, U. laevis Pall., U. microcarpa, L.K. Fu, U. multinervis (syn. U. castaneifolia) Hemsl., U. parvifolia Jacq., U. propinqua Koidz., U. prunifolia Cheug and L.K. Fu,, U. rubra Muhlenb., U. suberosa Henry, U. sukaczevii Andr., U. .szechuanica Fang., U. taihangshensis S.Y. Wang, U. thomasii Sarg, U. wilsoniana Schneid., ‘Frontier', ‘Homestead', ‘New Horizon', ‘Pioneer', ‘Patriot', U. ‘Morton' Accolade, and U. ‘Morton' Triumph, and Zelkova serrata (Thunb.) Mak. cultivars ‘Green Valley' and ‘Village Green', and Z. schneideriana Hand.-Mazz were the least susceptible to feeding and/or the least suitable for reproduction. Percent leaf tissue removed was highly correlated with field defoliation ratings, but was not a good predictor of fecundity. Asian and European elm leaves were thicker compared with North American elms, and Asian elm leaves were tougher compared with European and North American elm leaves. Host susceptibility and suitability were not related to leaf thickness or toughness. Adult female beetles laid significantly more eggs when feeding on Asian elm taxa compared with European, Eurasian, and North American elm taxa. Hybridization appears to affect host susceptibility. Results reported here provide new insight for the use of Ulmaceae taxa for future reforestation and tree breeding programs.

Species used in this study:Ulmus alata Michx., U. americana L., U. bergmaniana var. lasiophylla Schneid., U. canascens Melville, U. carpinifolia Gled.., U. castaneifolia Hemsl., U. changii Hangchow, U. chenmoui Cheng, U. crassifolia Nutt., U. davidiana Planch., U. elliptica K.Koch., U. foliaceae Gilbert, U. gaussenii Cheng,, U. glabra Hudson, U. glaucescens Franch., U. glaucescens Franch. var. lasiocarpa Rehd., U. japonica Sarg., U. laevis Pall., U. lanceaefolia Roxb., U. lamellosa C. Wang et S.L. Chang et L.K. Fu, U. macrocarpa Hance, U. microcarpa L.K. Fu, U. multinervis (syn.U. castaneifolia) Cheng, U. parvifolia Jacq., U. procera Salisb, U. propinqua Koidz., U. propinqua var. suberosa Henry , U. prunifolia Cheng et L.K. Fu , U. pseudopropinqua Wang et Li, U. pumila L., U. rubra Muehl., U. serotina Sarg., U. suberosa Henry, U. sukaczevii Andr., U. szechuanica Fang, U. taihangshanensis S.Y. Wang , U. thomasii, U. wallichiana Planch., U. wilsoniana Schneid., Zelkova serrata (Thunb.) Mak., Z. carpinifolia (Pall.) K. Koch., Z. schneideriana Hand.-Mazz,. Z. sinica C.K. Schneid, Sassafras albidum (Nutt.) Nees.

Seventy-three Ulmus and eight Zelkova taxa were evaluated in a series of no-choice and multiple-choice laboratory feeding bioassays and field defoliation studies for susceptibility, preference, and suitability for the adult Japanese beetle (Popillae japonica). North American elms Ulmus alata Michx., U. crassifolia Nutt, U. rubra Muhlenb, U. thomasii Sarg.; European elms U. elliptica K. Koch,, U. glabra Hudson, U. laevis Pall., U. suberosa Henry, U. sukaczevii Andr., Asian elms U. davidiana Planch., U. microcarpa, L.K. Fu, U. multinervis (syn. U. castaneifolia) Hemsl., U. parvifolia Jacq., U. propinqua Koidz., U. prunifolia Cheug and L.K. Fu., U. szechuanica Fang., U. taihangshensis S.Y. Wang, U. wilsoniana Schneid., cultivars New Harmony', ‘Valley Forge', ‘Frontier', ‘Homestead', ‘New Horizon', ‘Pioneer', ‘Patriot', U. ‘Morton' Accolade, and U. ‘Morton' Triumph, and Zelkova serrata (Thunb.) Mak. cultivars ‘Green Valley' and ‘Village Green', and Z. schneideriana Hand.-Mazz. were the least susceptible to feeding and/or the least suitable for reproduction. Laboratory no-choice feeding studies were correlated with field defoliation ratings, but were not a good predictor of adult female fecundity. Physical leaf characteristics (i.e. leaf thickness and toughness) differed by geographic origin. Asian and European elm leaves were thicker than North American elms, and Asian elm leaves were tougher than European and North American elm leaves, but leaf thickness and toughness was not related to host susceptibility or adult female fecundity. Hybridization significantly affected host susceptibility and appears to contribute to an “U. pumila and U. carpinifolia factor” for host preference, susceptibility, and suitability. Results from this study suggests there is a rich pool of Ulmus and Zelkova taxa for future breeding programs and for reforestation efforts due to loss of landscape trees and urban forest cover by lethal insect pests (i.e. Asian longhorn beetle [Anoplophora glabripennis (Motschulsky, 1853)], emerald ash borer (Agrilus planipennis Fairmaire, 1888) and diseases (i.e. Dutch elm disease [Ophiostoma ulmi (Buisman) Nannf. and Ophiostoma novo-ulmi Brasier]), and for their broad hardiness range, ability to tolerate variety of soil conditions, and minimal maintenance in harsh urban environments.

Since its introduction into the United States around 1916, the Japanese beetle, Popillia japonica Newman has become one of the most destructive and hard to control pests of nursery crops and landscape plants. Adult beetles feed on over 300 species of wild and cultivated plants including but not limited to members of Rosaceae, Malvaceae, Vitaceae, Polygonoceae, Aceraceae, Ulmaceae, and Salicaceae (Fleming 1972, Ladd 1986, 1987, 1989, Miller and Ware, 1999, Miller et al. 1999, Miller 2000, Miller et al. 2001a, Potter and Held 2002, Held 2004). Highly preferred hosts include lindens (Tilia spp. L.), sassafras [Sassafras albidum (Nuttall) Nees], and purple plum (Prunus cerostifera Erhart), all of which may be completely defoliated by adult beetles (Fleming 1972, Ladd 1986, 1987, 1989, Potter and Held 2002, Held 2004).

Common to most woody landscape plants, host plant resistance to P. japonica is poorly documented (Raupp et al. 1992), with susceptible or resistant plant lists being compiled from anecdotal descriptions and field observations (Hawley and Metzger 1940, Fleming 1972). No-choice laboratory bioassays conducted by Ladd (1987, 1989) have revealed considerable variations in feeding preference by P. japonica among plant species listed by Fleming (1972) as being either favored hosts, minor hosts, or non-host species.

Little or very limited information is available on P. japonica feeding preference among cultivars or varieties of common hosts with the exception of a few flowering woody ornamental plants and shade trees. Variation in host susceptibility, preference, and suitability can be quite distinct even within genera (Ranney and Walgenbach 1992, Spicer et al. 1995, Loughrin et al. 1996, 1997, Potter et al. 1998, Miller and Ware 1999a, Miller et al. 1999, 2001b, Rowe and Potter 2000, Potter and Held 2002, Held 2004, Potter and Redmond 2013). Feeding damage ratings for P. japonica was conducted by Ranney and Walgenbach (1992) on selected cultivars of birch (Betula spp. L.), cherry (Prunus spp. L.), and crabapple (Malus spp. Mill.) during one growing season. In addition, Spicer et al. (1995) found consistent differences in defoliation to 42 different cultivars of flowering crabapples and Potter et al. (1998) observed significant relative differences in susceptibility of flowering crabapples, lindens, and roses (Rosa spp. L.).

The Ulmaceae are considered a preferred host of the Japanese beetle (Fleming 1972). With the recent renewed interest and success in development of new American elm taxa and cultivars for Dutch elm disease (DED) and elm yellows resistance (Carter and Carter 1974, Rauscher et al. 1974, Townsend and Schreiber 1975, Townsend 1979, Smalley and Guries, 1993, Townsend et al. 1995a,b, 2005, Sinclair et al. 2000, Townsend 2000, Townsend and Douglass, 2001, Sinclair and Lyon, 2005, Townsend et al. 2005) and reduced feeding susceptibility and preference by herbivorous insects (Cunningham and Dix 1983, Hall 1986, Hall and Young 1986, Hall and Townsend 1987, Hall et al. 1987, Miller 2000, Miller et al. 2001b, Miller and Ware 2014) elms have the potential once again to be included in landscape and shade tree plantings (Warren 2000, Dirr 2009). More recently, the accessibility and procurement of Asian elm seed sources has greatly added to the number of potential elm genotypes available for breeding and hybridization (Fu 1980, Ware 1992, 1995, Warren 2000). Simple and complex Eurasian and Asian elm taxa have shown to have varied resistance to DED, elm yellows, elm leaf beetle, spring and fall cankerworm, Japanese beetle, and elm leaf miner (Ware 1992, Gurries and Smalley 1994, Miller and Ware 1994, Ware 1995, Miller and Ware 1997, 1999b, Miller and Ware 2001a,b,c,d, Miller 2000, Miller and Ware 2002, 2003, Sinclair and Lyon 2005, Miller and Ware 2014, Griffin et al. 2017). Previous laboratory and field studies by Miller et al. (1999, 2001a), Condra et al (2010), and Potter and Redmond (2013) have provided valuable information on the relative susceptibility and preference of recently acquired and developed Ulmus taxa of North American, European, and Asian elm parentage for feeding by P. japonica.

Plants protect themselves from herbivores by using either physical plant traits, chemical defenses, or a combination of both. In all likelihood, that is the case here with Ulmus taxa and Japanese beetles (Hoxie et al. 1975, Meredith and Schuster 1979, Johnson et al. 1980a,b, Ryan et al. 1982, Southwood 1986, Tingey and Laubengayer 1986, Matsuda and Senbo 1986, Doss et al. 1987, Potter and Kimmerer 1988, Ranney and Walgenbach 1992, Patton et al. 1997, Fulcher et al. 1998, Rowe and Potter 2000, Dalin and Bjorkman 2003, War et al. 2012 ). However, information is lacking on the suitability of many of these elm taxa for Japanese beetle reproduction, and possible physical leaf factors responsible for feeding susceptibility and preference.

In this study, our objectives were to evaluate the relative susceptibility, preference, and suitability of North American, European, and Asian elm, and Zelkova taxa and related cultivars and varieties, simple elm hybrids (a plant resulting from the crossing of two taxa), including U. pumila x U. japonica, and Asian elm hybrids, complex Asian elm hybrids (a plant in which three or more taxa are parents), and complex Eurasian elm hybrids for adult Japanese feeding and reproduction. Ulmus americana is genetically heterogeneous and most U. americana are reported to be tetraploid (2n = 4x = 56, where x=14). However, the diploid form of U. americana (2n = 2x = 28) was included in this study because both diploids and tetraploids may grow in proximity to each other and because further studies are needed to determine the potential for defoliation of diploid forms by herbivorous insect pests (Santamour 1993, Whittemore and Olsen 2011, Whittemore and Xia 2017). Additionally, we examined physical elm leaf characteristics, namely leaf thickness, toughness, and pubescence, and their possible role in adult feeding susceptibility, preference, and suitability. Results from this study will contribute to the potential use of additional Ulmus and Zelkova taxa for comprehensive tree breeding programs for disease and insect pest host plant resistance.

No-Choice (NC) laboratory feeding bioassays (Susceptibility)

Laboratory no-choice bioassay feeding studies were conducted on adult Japanese beetles as previously described by Miller and Ware, 1999a, Miller et al. (1999, 2001a), and Miller and Wiegrefe (2021). Seventy-three elm taxa and eight Zelkova taxa were evaluated. Refer to Table 1 for a list of Ulmus and Zelkova taxa evaluated. Sassafras [Sassafras albidum (Nutt.) Nees], a highly favored host of the Japanese beetle (Fleming 1972, Miller et al. 2001a, Miller and Wiegrefe 2021), served as the standard. Candidate Ulmus and Zelkova taxa growing in the Ulmaceae and geographic collections at The Morton Arboretum, Lisle, IL, ranged in height from 3 to 10 m (10-33 ft.), with diameters at breast height of 8-40 cm (3-16 in).

Table 1

Ulmaceae and Zelkova taxa evaluated in no-choice, multiple-choice, fecundity, and field defoliation studies for susceptibility, preference and suitability for the adult Japanese beetle.

Ulmaceae and Zelkova taxa evaluated in no-choice, multiple-choice, fecundity, and field defoliation studies for susceptibility, preference and suitability for the adult Japanese beetle.
Ulmaceae and Zelkova taxa evaluated in no-choice, multiple-choice, fecundity, and field defoliation studies for susceptibility, preference and suitability for the adult Japanese beetle.

Ulmus and Zelkova taxa leaves for the no-choice (NC) and multiple-choice (MC) laboratory feeding bioassays were randomly collected from ground level from all four cardinal directions and held in cold storage in plastic bags at 5 C (41 F) for a maximum of 2 d. Leaves collected from each test tree were combined for the NC and MC laboratory feeding bioassays. Depending on availability, one to three individual trees of each Ulmus and Zelkova taxon were evaluated.

Adult beetles used in the NC and MC studies were field-collected from plants at The Morton Arboretum, Lisle, IL and The Chicago Botanic Garden, Glencoe, IL. Upon collection, the adult beetles were held in clear plexiglass cages under a photoperiod of 16:8 (L:D) h at 25 C (77 F). While being held in the cages (no longer than 12 hours), the beetles were allowed to feed on fresh crabapple (Malus spp.) foliage to ensure predisposition to feeding. Prior to the beginning of the feeding trials, the Japanese beetles were sexed, and one adult male/female Japanese beetle pair was placed into each of 10 clear plastic petri dishes (10.0 cm diam by 0.6 cm depth) along with one leaf of the specific Ulmus or Zelkova taxon to be tested. Each beetle pair was used only once. There were 10 dishes (sub-replicates) for each tree for each taxon evaluated for a total of 10 to 30 male/female beetle pairs per taxon. Petri dishes were examined daily for beetle mortality and evidence of feeding. Foliage was replaced every 2 d. At the time of leaf removal, the leaves were visually rated (nearest 5%) for the percent of leaf tissue removed, by two independent estimators using a defoliation template. Petri dishes were placed in clear plastic bags to prevent drying of the foliage and were held in a growth chamber under a 16:8 (L:D) h photoperiod at ∼ 25 C (77 F). Condensation of water on the lid of the petri dish indicated a high relative humidity. At the end of seven days, the remaining foliage and fecal pellets were removed from each petri dish and the fecal pellets were oven dried and weighed (nearest mg). The NC feeding bioassays were terminated after 7 days. The measure of the susceptibility for each taxon was defined by mean percent leaf tissue removed and mean dried fecal pellet weights.

Multiple-Choice (MC) laboratory feeding bioassays (Preference)

Laboratory multiple-choice bioassay feeding studies were conducted on adult Japanese beetles as previously described by Miller and Ware, 1999a, Miller et al. (1999, 2001a) and Miller and Wiegrefe (2021). One adult female Japanese beetle was placed into each of 10 plastic petri dishes (15.0 by 0.6 cm) with each petri dish serving as a replicate. Depending on the number of elm selections tested in each study, (including the reference taxon), four to seven Ulmus and/or Zelkova leaf discs, representing four to seven different elm selections, were placed around the perimeter of each petri dish. The leaf discs were taken from the center of each leaf for each taxon and were 2.54 cm in diameter. Beetles had access to all leaf discs. The petri dishes were examined daily for seven days. Each day, the foliage discs were removed from the dishes, replaced, and visually evaluated (nearest 5%) by two independent estimators using a defoliation template for the amount of leaf tissue removed. New foliage discs were arranged randomly in the dish each day to eliminate possible bias. The measure of preference for each Ulmus and Zelkova taxon was defined by the mean percent of leaf tissue removed.

Field defoliation survey

In late August, after all adult beetle feeding had ceased, a field defoliation survey was conducted by visually examining the tree canopy from all four cardinal directions of all available Ulmus and Zelkova taxa. Trees were rated by two independent estimators for evidence of feeding using a scale of 0-4 as follows: 0=no feeding, 1=very light feeding, 2=light feeding, 3=moderate feeding, and 4=heavy feeding. Depending on the availability of Ulmus and Zelkova taxa, three to five single tree replicates were evaluated per taxon. Host susceptibility and preference was defined by using the feeding damage scale.

No-Choice (NC) laboratory fecundity bioassays (Suitability)

A male/female pair of field-collected adult Japanese beetles was placed into a 5.7 L (6 qt) capacity Clear-View™ plastic container (SteriliteR, Townend, MA) with approximately 5.0 cm. of finely sifted moist silt-loam soil, and foliage of the candidate Ulmus or Zelkova taxon to be tested. Sassafras (Sassafras albidum), a highly favored hosts of the Japanese beetle (Fleming 1972, Miller et al. 2001a, Miller and Wiegrefe 2021), served as the standard. Foliage was kept turgid and fresh using floral water piks. The boxes containing the beetles and foliage were kept at room temperature in the laboratory under natural daylength. The boxes were examined every third day and elm foliage was replaced if wilted or defoliated. At 7, 14, and 21 days from the initiation of the study, the soil in each container was visually examined for eggs, and the total number of eggs per container and adult beetle mortality was recorded. After each egg counting, the original male/female beetle pair was returned to the container. Ten single containers (replicates) containing one male/female pair were used for each of three single trees per Ulmus or Zelkova taxon for a total of 30 beetle pairs per taxon. The study was terminated after 21 days.

Trichome density and morphology

Ten mature leaves, for each of the 11 pubescent Ulmus taxon, were used to determine trichome density on the upper and lower leaf surfaces. The leaves were positioned under a light microscope and a 1cm2 template was placed halfway between the leaf blade and midrib on both the adaxial and abaxial leaf surfaces. The total number of trichomes within the 1 cm2 sampling area was counted and recorded. Scanning electron microscopy (SEM) was performed at The Morton Arboretum (TMA) electron microscopy laboratory, to observe trichome morphology, as previously described by St.-Laurent et al. (2000) and Bosu and Wagner (2007). The trichomes were examined in scanning electron microscopy (LEO 1430 VP) at an acceleration voltage of 10.6 kV. Trichomes were characterized as either simple (non-glandular) trichomes, and further divided into short (50-100 microns) and long (1-3 mm), or as bulbous (glandular) trichomes as previously detected and described on soybean [Glycine max (L.) Merrill] leaves (Peter et al. 1995), on 20 elm taxa (Bosu and Wagner 2007), and on birch leaves (Ventralla and Marinho 2008).

Effect of trichomes on host preference and suitability

In order to determine the effect of trichomes or lack of trichomes on beetle feeding preference, a MC laboratory feeding bioassays were conducted for 11 pubescent Ulmus taxa. The MC studies were conducted as described previously except that only one Ulmus taxon was tested in paired choices. The trichomes were removed from leaves of each respective taxon using a microscope slide and gently scraping the upper and lower leaf surfaces exerting enough pressure to remove the trichomes but not enough to tear or rupture the leaf epidermis.

To determine the effect of trichomes or lack of trichomes on adult female fecundity, a NC fecundity study was initiated for the same 11 pubescent elm taxa mentioned previously. Methods and materials for this study were the same as mentioned above for trichome removal, and the NC laboratory fecundity bioassays.

Measuring elm leaf thickness and toughness

Prior to using the leaves for the NC laboratory feeding bioassays, 10 leaves for each taxon were measured for leaf thickness, and inner and outer leaf toughness. Leaves were collected in the field as previously described. Leaf thickness was determined by using a Vernier caliper to measure the thickness of each leaf (nearest mm) approximately one-half the distance from the leaf margin to the mid-rib. Inner and outer leaf toughness was determined to the nearest gram using a Chatillon™ digital force meter (pentrometer) (Greensboro, N.C.) applied to within 0.5 cm from the edge of the leaf for measuring outer toughness, and in the center of the leaf adjoining the mid-rib for inner toughness, respectively.

Measures of susceptibility, preference, and suitability

Measures of susceptibility for adult Japanese beetles feeding on Ulmus and Zelkova taxa was defined as the percent leaf tissue removed, and the dry fecal pellet weight in the NC feeding bioassays, and the field defoliation ratings. Preference was determined by the amount of leaf tissue removed in the MC feeding bioassays. Host suitability was determined by the total number of eggs (fecundity) laid by females for each taxon, percent of females ovipositing, and male and female longevity.

Statistical analysis

Measures of susceptibility, preference, and suitability were subjected to analysis of variance (ANOVA) using taxon as the main effect. Means of significant effect (5%) were compared with the Dunn's test. Coefficients of correlation were determined by regression analysis for the rankings for comparing measures of susceptibility, preference, and suitability, and for leaf thickness, toughness, and pubescence. Percent leaf tissue removed for each taxon was arcsine transformed before analysis to correct for non-normality. All data are presented as original means + standard error of the mean (SE). Data were analyzed using the SigmaStat for Windows (Jandel Scientific 1992).

No-Choice (NC) laboratory feeding bioassays (Susceptibility)

Adult Japanese beetles removed significantly more leaf tissue (>80%) from the North American taxa of U. americana-diploid form and U. americana as compared with U. americana cultivars ‘Jefferson', ‘Valley Forge', and ‘New Harmony (F=56.5, P<0.0001). Adult beetles produced significantly less dry fecal weight (F=92.4, P<0.0001) when feeding on ‘Valley Forge', and ‘New Harmony', and the greatest amount when feeding on the diploid form of U. americana and U. americana. Adult beetles produced an intermediate amount of dry fecal weight when feeding on ‘Jefferson' (Table 2). American elm is very unusual in the Ulmus genus cytologically with the majority being tetraploids, but also diploids in some cases. Ulmus americana ‘Jefferson' [National Park Service (NPS)-3-487] is considered to be triploid and is considered a hybrid between diploid and tetraploid elms (Sherald et al. 1994, Whittemore and Olsen 2011). ‘Jefferson' has shown to be less susceptible to DED along with ‘Valley Forge' and ‘New Harmony'. It is possible that some of the same genetic traits have been extended to reflect reduced feeding by adult Japanese beetles. Conversely, the U. americana-diploid form was equally susceptible to adult Japanese beetle feeding as U. americana, and both have been shown to be highly susceptible to DED. It appears that ploidy may confer some level of resistance to both DED and feeding by the Japanese beetle. Further research is needed to understand the origin and relations of the different ploidy levels, and the potential for pest and disease resistance (Santamour 1993, Whittemore and Olsen 2011, Whittemore and Xia 2017).

Table 2

Percent leaf tissue removed and dry fecal pellet weight for adult female Japanese beetles feeding on Ulmaceae in no-choice (NC) feeding studies.

Percent leaf tissue removed and dry fecal pellet weight for adult female Japanese beetles feeding on Ulmaceae in no-choice (NC) feeding studies.
Percent leaf tissue removed and dry fecal pellet weight for adult female Japanese beetles feeding on Ulmaceae in no-choice (NC) feeding studies.

Adult Japanese beetles feeding on simple and complex Eurasian elm hybrids removed significantly more leaf tissue (>80%) when feeding on ‘Pioneer', ‘Regal', and ‘Patriot' and removed the least amount of leaf tissue (50%) when feeding on ‘Homestead' (F=68.0, P<0.0001). Adult beetles removed an intermediate amount of leaf tissue when feeding on ‘Frontier' and ‘Urban' elm. Dry fecal pellet weights followed the same ranking order as mean percent leaf tissue removed (F=19.2, P<0.0001) (Table 2).

For simple U. pumila and U. japonica hybrids, beetles removed significantly more leaf tissue (>77%) from ‘Sapporo Autumn Gold' and ‘New Horizon' compared with beetles feeding on ‘Cathedral' (F=23.0, P<0.0001). Mean dry fecal pellet weights followed the same ranking as the mean percent leaf tissue removed (F=15.8, P=0.006) (Table 2).

Significantly more leaf tissue (>37%) was removed by adult beetles when feeding on U. parvifolia cultivars of ‘Athena' and ‘Dynasty' as compared to U. parvifolia (F=17.1, P<0.0002). Japanese beetles feeding on ‘Athena' and ‘Dynasty' produced 2X more dry fecal pellet weights compared with U. parvifolia. Dry fecal pellet weights were not significantly different among the three U. parvifolia taxa. It is possible that the two U. parvifolia cultivars were more nutritious contributing to greater dry fecal pellet production. Dirr (2009) states that ‘Athena' leaves are a darker green, almost black, compared with the U. parvifolia phenotype which would suggest higher chlorophyll levels and better overall nutrition which was reflected in the higher dry fecal pellet weights.

Adult Japanese beetles removed significantly more leaf tissue (>40%) when feeding on simple Asian hybrids of U. japonica x U. pumila ‘Columnar', U. japonica x U. wilsoniana ‘Single Stem', U. japonica x U. wilsoniana ‘Arnold', U. pumila x U. americana, and ‘Vanguard x the diploid form of U. americana compared with beetles feeding on U. japonica-wilsoniana-rubra (F=19.7, P<0.012). Adult beetles produced significantly more frass (F=18.1, P<0.001) when feeding on U. japonica x U. wilsoniana ‘Arnold' compared with U. japonica x U. wilsoniana ‘Single Stem', U. japonica-wilsoniana-rubra, U. pumila x U. americana, and ‘Vanguard' x diploid form of U. americana. Intermediate amounts of dry fecal pellets were produced when feeding on U. japonica x U. pumila ‘Columnar' (Table 2).

Adult Japanese beetles feeding on North American elms of U. alata and U. americana, removed significantly more leaf tissue (>80%) as compared with beetles feeding on U. rubra. Ulmus crassifolia, U. serotina, and U. thomasii were moderately fed upon (F=90.8, P<0.0001). Rankings for dry fecal pellet weights were consistent with the percent of leaf tissue removed (F=71.7, P<0.0001) (Table 2).

Japanese beetles removed significantly more leaf tissue (>70%) when feeding on the European elms of U. canascens, U. carpinifolia, U. foliacea, and U. laevis as compared with U. elliptica, U. glabra, U. suberosa, and U. sukaczevii with < 60% of leaf tissue removed (F=63.5, P<0.0001). Rankings for dried fecal pellet weight were consistent with the percent of leaf tissue removed (F=44.8, P<0.0001) (Table 2).

Adult beetles removed significantly more leaf tissue (F=81.9, P<0.0001, and produced significantly more dry fecal pellets (F=29.5, P<0.0001) when feeding on the Asian elms of U. changii and U. wallichiana compared with U. prunifolia, U. wilsoniana ‘Prospector', and U. wilsoniana-98. Ulmus lanceaefolia, U. pseudopropinqua, and U. taihangshanensis were immediate in susceptibility and production of dry fecal pellets by Japanese beetles.

Evaluating eight different Zelkova taxa, adult Japanese beetles removed significantly more leaf tissue (>40%) (F=26.7, P<0.0001) when feeding on Z. serrata, Z. sinica, and Z. carpinifolia (D-Russia) compared with Z. serrata cultivars ‘Green Vase' and ‘Village Green', Z. carpinifolia (T-Russia), and Z. schneideriana (T-Russia and N-China). Mean dry fecal pellet weight rankings were consistent with the percent of leaf tissue removed (F=32.0, P<0.0001) (Table 3).

Table 3

Percent leaf tissue removed, dry fecal pellet weight, and percent field defoliation for adult female Japanese beetle feeding on Zelkova taxa and cultivars in no-choice laboratory feeding bioassays, and field defoliation study.

Percent leaf tissue removed, dry fecal pellet weight, and percent field defoliation for adult female Japanese beetle feeding on Zelkova taxa and cultivars in no-choice laboratory feeding bioassays, and field defoliation study.
Percent leaf tissue removed, dry fecal pellet weight, and percent field defoliation for adult female Japanese beetle feeding on Zelkova taxa and cultivars in no-choice laboratory feeding bioassays, and field defoliation study.

Dry fecal pellet weights (Susceptibility)

Dry fecal pellet weights were strongly correlated with the percent of leaf tissue removed (R=0.84, P<0.001) for all Ulmus and Zelkova taxa evaluated in this study,

Field defoliation survey (Susceptibility)

Overall, highly significant differences in feeding damage were observed among the 30 Ulmus and six Zelkova taxa evaluated on the grounds of The Morton Arboretum (F=118.3, P<0.0001) Table 4). Ulmus americana-diploid, U. carpinifolia, ‘Urban' elm, U. pumila, the hybrids U. japonica x U. wilsoniana ‘Single Stem', U. pumila x U. americana, ‘Commendation', U. elliptica, U. foliacea, and U. americana (reference) had >30% feeding damage compared with the remaining taxa with < 25% feeding damage (Table 4). Overall, the field feeding damage ratings were moderately correlated with the percent leaf tissue removed in the no-choice (NC) laboratory feeding studies (R=0.38, P=0.02). This could be due to a number of variables found in natural environments including leaf phenology, adult feeding habits, and environmental conditions compared with the controlled laboratory feeding studies.

Table 4

Percent field defoliation of selected elm (Ulmus) taxa for adult Japanese beetles feeding .

Percent field defoliation of selected elm (Ulmus) taxa for adult Japanese beetles feeding .
Percent field defoliation of selected elm (Ulmus) taxa for adult Japanese beetles feeding .

Multiple-Choice (MC) laboratory feeding bioassays (Preference)

Overall, there was no correlation between the percent leaf tissue removed in the no-choice (NC) and multiple-choice (MC) laboratory feeding studies. A significant difference (F=6.36, P=0.009) in feeding preference was observed in MC study #1 where adult beetles were presented U. americana ‘Jefferson', U. americana ‘Valley Forge' and the reference species U. americana (Table 5). The least amount of leaf tissue removed (12%) occurred on the diploid form of U. americana. Results from MC-1 were not consistent with the field defoliation survey. These differences could be due to the greater preference for U. americana by adult Japanese beetles in a controlled MC experiment with limited choices compared to field conditions where beetles would have to search for a more preferred species. These finding are consistent with other studies involving herbivorous insects where a highly preferred host tends to dominate preference in controlled multiple-choice (MC) studies (Miller, and Ware, 1994, 1997, Miller and Ware, 1999a, b, Miller et al., 1999, 2000b).

Table 5

Percentage of leaf tissue removed by adult Japanese beetles in multiple-choice (MC) laboratory feeding preference studies on Ulmaceae.

Percentage of leaf tissue removed by adult Japanese beetles in multiple-choice (MC) laboratory feeding preference studies on Ulmaceae.
Percentage of leaf tissue removed by adult Japanese beetles in multiple-choice (MC) laboratory feeding preference studies on Ulmaceae.

In multiple-choice (MC) study #2, a significant difference (F=41.9, P=0.0001) in feeding preference was observed. ‘Pioneer' and U. carpinifolia were the most preferred with U. glabra being least preferred. The cultivar, ‘Frontier' was intermediate in preference (Table 5). Like MC-1 study, the amount of leaf tissue removed and the field defoliation ratings were not related to feeding preference for the same taxa (Tables 2 and 5). Ulmus carpinifolia was found to be highly susceptible to feeding both in the NC and field defoliation studies which might have contributed to the greater preference for ‘Frontier' and ‘Pioneer' in this MC study. Like U. americana in MC-1, and for the same reasons mentioned previously, U. carpinifolia may have dominated preference in this controlled MC study compared with feeding preference in a more natural setting. Conversely, U. glabra was found to be much less susceptible and/or preferred for feeding in both the NC and MC studies, and the field defoliation studies, but in the case of ‘Pioneer', may have had only minimal genetic contribution to feeding susceptibility and preference.

In MC study #3, Japanese beetles fed significantly less on ‘Homestead', ‘Regal', and ‘Urban' elm (F=39.8, P<0.0001). Ulmus x hollandica ‘Vegeta', and U. carpinifolia were more preferred and Ulmus pumila was intermediate in preference (Table 5). In this study, the percent leaf tissue removed was very strongly correlated with leaf thickness (R=0.93, P<0.0001) but not for inner or outer leaf toughness for these same taxa.

MC study #4 revealed highly significant differences (F=44.7, P<0.0001) in feeding by adult beetles when they were allowed to choose between ‘Sapporo Autumn Gold', ‘Cathedral', ‘New Horizon', U. japonica, U. pumila, and the reference species, U. americana. Beetles removed significantly more leaf tissue on U. americana compared with ‘Cathedral', ‘New Horizon', and U. japonica where <12% of leaf tissue was removed. ‘Sapporo Autumn Gold' and U. pumila were intermediate in preference (Table 5). In this study, the mean percent leaf tissue removed was very strongly correlated with mean percent field defoliation (R = 0.93, F=13.9, P=0.06).When the highly preferred reference species of U. americana was not included in MC study #5, preference shifted to U. pumila with 56% of leaf tissue consumed compared to <22% of leaf tissue consumed for beetles presented with ‘Sapporo Autumn Gold', ‘Cathedral', ‘New Horizon', and U. japonica (F=44.7, P<0.0001) (Table 5).

In MC study #6, U. americana was highly preferred over the six Asian taxa (F=47.2, P,0.00010 (Table 5). In MC study #7, adult female beetles removed significantly more leaf tissue when presented with Z. serata, Z. carpinifolia (T-Russia) and the reference, U. americana (F=35.2, P<0.0001). Less than 3% of leaf tissue was removed on the remaining four Zelkova taxa (Table 5). Results from this multiple-choice study were very strongly correlated with the field defoliation survey (R=0.98, P=0.005)

No-Choice (NC) laboratory fecundity bioassays (Suitability)

Overall, adult female Japanese beetles laid significantly more eggs (> 300 eggs) on Asian elm taxa compared with European (95 eggs), Eurasian (88 eggs), and North American (22 eggs) elm taxa (F=123.0, P<0.0001) (Table 6).

Table 6

Fecundity of adult female Japanese beetles by geographic origin of Ulmaceae.

Fecundity of adult female Japanese beetles by geographic origin of Ulmaceae.
Fecundity of adult female Japanese beetles by geographic origin of Ulmaceae.

North American taxa

Ulmus americana and U. serotina was significantly more suitable for egg laying (>18 eggs) compared with U. alata, U. crassifolia, U. thomasii, and U. americana ‘Jefferson' with <4 total eggs laid (F=86.1, P=0.02) (Table 7).

Table 7

Fecundity of adult female Japanese beetles ovipositing when feeding on Ulmaceae leaves.

Fecundity of adult female Japanese beetles ovipositing when feeding on Ulmaceae leaves.
Fecundity of adult female Japanese beetles ovipositing when feeding on Ulmaceae leaves.

Simple and complex Eurasian hybrids

Adult females feeding on simple and complex Eurasian hybrids laid significantly more eggs on ‘Regal' (12 eggs), ‘Urban' elm (10 eggs), and ‘Frontier' (9 eggs) compared with ‘Homestead', ‘Pioneer', ‘Patriot', and ‘Prospector' with <4 eggs per taxon (F=129.0, P<0.001) (Table 7).

Complex Asian hybrids

‘Morton Plainsman' Vanguard was significantly more suitable (total eggs = 54) (F=43.8, P<0.0001) compared with ‘Morton' Accolade, and ‘Morton Glossy' Triumph (<23 eggs produced). ‘Morton Stalwart' Commendation and ‘Morton Red Tip' Danada Charm were intermediate in suitability with a total of 38 and 42 eggs laid, respectively (Table 7).

Ulmus pumila x U. japonica hybrids

‘Sapporo Autumn Gold' was found to be more suitable for egg laying by adult female beetles (total of 21 eggs) compared with ‘New Horizon' with a total of only five eggs laid (t=143, P<0.01) (Table 7).

European elm taxa

Adult female beetles laid significantly more eggs on U. carpinifolia (48 eggs) compared with the other five European elm taxa (< 20 eggs laid) (F=117.2, P<0.0001) (Table 7).

Asian taxa and simple hybrids

Adult female beetles laid significantly more eggs (>40 eggs) (F=53.8, P<0.0001) when feeding on U. bergmaniana var. lasiophylla, U. chenmoui , U. lamellosa, U. macrocarpa, U. parvifolia, U. szechuanica x U. japonica, and ‘Vanguard' x U. japonica-wilsoniana-pumila). Adult female beetles laid an intermediate number of eggs (mean=30 total eggs) when feeding on U. davidiana, U. davidiana x. U. japonica-wilsoniana-pumila, U. gaussenii, U. glaucescens, U. japonica, U. multinervis (syn. U. castaneifolia), and U. propinqua var. suberosa. Adult female Japanese beetles laid significantly fewer eggs (<20 total eggs) on the remaining Asian elm taxa (Table 7).

Zelkova taxa

For the Zelkova taxa (Ulmaceae), Z. sinica was the most suitable for egg laying with a total of 38 eggs compared with Z. schneideriana (N-China), Z. serrata, and the cultivars of Z. serrata ‘Green Vase', and ‘Village Green' with <2 total eggs laid (F=75.1, P<0.001) (Table 7). Not surprisingly, the highly preferred sassafras (Sassafras albidum) was by far the most suitable with females producing a total of 200 eggs. These results are consistent with previous studies by Keathley and Potter (2008) and Miller and Wiegrefe (2021). One adult female beetle laid one egg in the blank reference container without foliage.

For all of the elms tested in this study, percent leaf tissue removed and dry fecal pellet weight were not good predictors of fecundity (percent leaf tissue removed, R=0.36, P=0.10 and dry fecal pellet weight, R=0.05, P=0.82, respectively). However, fecundity was strongly correlated with percent females ovipositing (R=0.72, P<0.001). Our findings are consistent with a study by Miller and Wiegrefe (2021) evaluating the suitability of Carpinus taxa for Japanese beetle reproduction.

Adult longevity

Overall, adult male and female beetles lived an average of 20 days on all Ulmus taxa evaluated in this study. Results presented here are consistent with other studies (Potter et al. 1998, Miller et al. 1999, 2001a, Miller and Ware 1999a, 2001, Potter and Held 2002, Miller and Wiegrefe 2021). However, adult male Japanese beetles feeding on Zelkova taxa lived significantly longer (21 days) on ‘Green Vase' and ‘Village Green' compared to the other Zelkova taxa (males: 17-18 days, F=13.6, P<0.009 and females: 16-18 days, F=12.2, P<0.016) (Data not shown).

Elm leaf thickness and toughness

A summary of elm leaf thickness and toughness by geographic origin and taxa is presented in Tables 8 and 9. Asian and European elms had significantly thicker leaves (1.5X) than North American elms (F=70.0, P<0.001), and Asian elm leaves were significantly tougher than European and North American elms by a factor of 1.3X and 1.4X for inner and outer leaf toughness, respectively (inner toughness, F=31.1, P<0.001 and outer toughness, F=39.1, P<0.001, respectively) (Table 8). There was no significant difference between inner and outer leaf toughness for all of the Ulmus taxa evaluated in this study, Leaf thickness was moderately and strongly correlated with inner and outer leaf toughness (inner toughness, R=0.43, P<0.006, outer toughness, R=0.52, P<0.001), respectively, and inner leaf toughness was very strongly correlated with outer leaf toughness (R=0.93, P<0.001).

Table 8

Summary of leaf thickness, and inner and outer leaf toughness by geographic origin for Asian, European, and North American Ulmus taxa.

Summary of leaf thickness, and inner and outer leaf toughness by geographic origin for Asian, European, and North American Ulmus taxa.
Summary of leaf thickness, and inner and outer leaf toughness by geographic origin for Asian, European, and North American Ulmus taxa.
Table 9

Summary of elm (Ulmus) leaf thickness, and inner and outer leaf toughness.

Summary of elm (Ulmus) leaf thickness, and inner and outer leaf toughness.
Summary of elm (Ulmus) leaf thickness, and inner and outer leaf toughness.

For the 20 Asian and complex hybrids, evaluated, U. castaneifolia had significantly thicker leaves and U. gausenni, U. glaucescens, U. japonica, U. pumila, and the complex hybrids of ‘Accolade', ‘Commendation', and ‘Vanguard' had significantly thinner leaves. Leaves of the remaining Asian elm taxa and hybrids were intermediate in thickness (F=353.3, P<0.001). Leaves of U. gausenni, U. japonica, and U. pumila were the most tender (least tough) compared to the toughest leaves of U. lamellosa, U. macrocarpa, U. parvifolia, U. taihangshanensis, U. wilsoniana, “Accolade', ‘Commendation', ‘Danada Charm', and ‘Triumph'. Leaves of the remaining Asian elm taxa were intermediate in inner and outer leaf toughness (inner toughness, F=254.4, P<0.001, outer toughness, F=303.0, P<0.001).

For the simple and complex Eurasian hybrids, ‘Frontier', ‘Homestead' and ‘Regal' had significantly thinner and more tender leaves than ‘Patriot' and ‘Pioneer' (thickness, F = 47.4, P<0.001, inner leaf toughness, F=17.2, P<0.001, outer leaf toughness, F=17.8, P <0.001).

Among European elms, U. foliaceae had the thinnest leaves and U. procera and U. sukaczevii had significantly thicker leaves (F=44.2, P<0.001). Ulmus elliptica and U. procera had significantly tougher leaves compared with U. sukaczevii (inner leaf toughness, F=30.6, P<0.001, outer leaf toughness, F=4.9, P<0.001).

The North American elm, U. thomasii had significantly thinner leaves compared with U. alata and U. crassifolia (F=40.4, P<0.001). There was no significant difference in inner leaf toughness for all of the North American elms tested in this study, but outer leaf toughness for U. alata was significantly greater compared with U. americana and U. thomasii (F=4.8, P<0.005).

Elm leaf thickness, toughness, and susceptibility

Overall, the percent leaf tissue removed in the no-choice (NC) laboratory feeding studies was not correlated with leaf thickness (R=0.06, P=0.70), inner leaf toughness (R=0.25, P=0.13), or outer leaf toughness (R=0.22, P=0.18). Likewise, leaf thickness and inner and outer leaf toughness were not good predictors of the amount of dry frass pellet weight produced (thickness R=0.0, P=0.95, inner R=0.18, P=0.27, outer R=0.18, P=0.37).

Elm leaf thickness, toughness, and suitability

Leaf thickness for Asian elms and complex hybrids was not correlated with adult female fecundity (R=0.09, P=0.68), but fecundity was moderately related with both inner and outer leaf toughness for Asian elms (inner toughness, R=0.44, P=0.04, outer toughness, R=0.48, P=0.02) (i.e. the more tender the leaf, the more eggs that were laid). Conversely, fecundity was not related to leaf thickness or inner or outer leaf toughness for simple and complex Eurasian hybrids (leaf thickness, R=0.69, P=0.13. inner toughness, R=0.69, P=0.13, outer toughness, R=0.71, P=0.11), European taxa (thickness, R=0.53, P=0.29, inner toughness, R=0.27, P=0.61, outer toughness, R=0.21, P=0.69), or North American taxa (thickness, R=0.06, P=0.93, inner toughness, R=0.68, P=0.21, outer toughness, R=0.18, P=0.78).

Elm leaf trichome density

A summary of trichome density per mm2 of leaf surface, by taxon, is presented in Table 10. Ulmus glaucescens, U. lamellosa, and U. propinqua var. suberosa had significantly greater trichome density per mm2 (581, 512, 486, respectively) compared with U. gausennii, U. glaucescens var. lasiocarpa, U. propinqua, and U. prunifolia with 184, 147, 171, 187 leaf trichomes per mm2, respectively. The remaining taxa had intermediate leaf trichome density (F=91.9, P<0.0001) (Table 9).

Table 10

Leaf trichome density per mm2 of leaf surface for Asian elm taxa.

Leaf trichome density per mm2 of leaf surface for Asian elm taxa.
Leaf trichome density per mm2 of leaf surface for Asian elm taxa.

Elm leaf trichome density and host susceptibility

Collectively, for the 11 pubescent Asian elms evaluated here, there was no significant difference in percent leaf tissue removed when adult beetles were feeding on leaves with leaf trichomes present or when trichomes were removed, and percent leaf tissue removed was not correlated with leaf trichome density (R=0.16, P=0.64). However, in single taxon, paired no-choice (NC) feeding studies, adult female beetles removed significantly more leaf tissue when trichomes were removed from leaves of U. chenmoui (t=215.3, P=0.03), U. gausennii (t=423.4, P<0.001), U. glaucescens var. lasiocarpa (t=230.0, P=0.02), U. lamellosa (t=199.2, P=0.048), and U. macrocarpa (t=575.0, P<0.0001 (Table 11). There was no significant difference in percent leaf tissue removed for beetles feeding on U. davidiana, U. propinqua, U. propinqua var. suberosa, U. prunifolia, U. pseudopropinqua leaves with or without trichomes present (Table 11). Additionally, there was no significant difference in dry fecal pellet weights for all 11 taxa evaluated for beetles feeding on leaves with trichomes present or removed.

Table 11

Paired single taxon no-choice (NC) feeding (% leaf tissue removed) studies for adult female Japanese beetles feeding on pubescent Asian elms with leaf trichomes present and with trichomes removed.

Paired single taxon no-choice (NC) feeding (% leaf tissue removed) studies for adult female Japanese beetles feeding on pubescent Asian elms with leaf trichomes present and with trichomes removed.
Paired single taxon no-choice (NC) feeding (% leaf tissue removed) studies for adult female Japanese beetles feeding on pubescent Asian elms with leaf trichomes present and with trichomes removed.

Effect of trichomes on host suitability

For all Asian elms evaluated in this study, with either glabrous or pubescent leaves, there was no significant difference in total eggs produced, (t=0.23, P=0.82), eggs produced per female; (t=0.51, P=0.62), or eggs produced per ovipositing female (t=1.32, P=0.20) (Data not shown).

For these same 11 highly pubescent Asian elm taxa mentioned above, pubescence or lack there-of, did not have a significant effect on the total number of eggs laid for females feeding on leaves with trichomes present (440 eggs) or where trichomes had been removed (407 eggs) (t=0.227, P=0.82) or number of eggs per ovipositing female (t=1.32, P=0.20). However, there was a significant difference in the percentage of females ovipositing when feeding on leaves with trichomes present (46%) versus leaves with trichomes removed (74%) (t=3.31, P=0.003). There was no relationship between total eggs produced with leaf trichomes present (R=0.27, P=0.42) or without trichomes, (R=0.21, P=0.54), eggs per female with trichomes present (R=0.00, P=0.99) or without trichomes (R=0.05, P=0.89), percent females ovipositing with trichomes present (R=0.11, P=0.74), or eggs per ovipositing female with trichomes present (R=0.19, P=0.58) and without trichomes (R=0.02, P=0.95).

However, in the single paired taxon, no-choice (NC) feeding studies, adult female beetles laid significantly more eggs when feeding on U. gausennii, (t=12.1, P=0.0001), U. propinqua var. suberosa (t=24.3, P=0.0001), and U. prunifolia (t=16.4, P=0.0001) leaves where trichomes had been removed compared with leaves with trichomes present (Table 12). Conversely, adult beetles feeding on U. davidiana (t=10.7, P=0.001), U. glaucescens, (t=9.8, P=0.001), U. lamellosa, (t=6.6, P=0.008), U. macrocarpa, (t=7.2, P=0.004) and U. propinqua (t=7.6, P=0.005) laid significantly more eggs on leaves with trichomes present compared with leaves where trichomes were removed (Table 12). There was no significant difference in total eggs laid, for adult beetles feeding with or without trichomes present, on U. chenmoui, U. glaucescens var. lasiocarpa, and U. pseudopropinqua. Results from this study provide new insight into the relative susceptibility, preference, and suitability of Ulmus and Zelkova taxa for feeding and reproduction by adult Japanese beetles, and for their potential use in tree breeding programs. Leaf tissue chemical analysis, and its influence on host susceptibility, preference, and suitability, was beyond the scope of this study, and was not examined; however, we did attempt to examine, and will discuss possible physical plant traits (i.e. leaf thickness, toughness, and pubescence) of Ulmus and Zelkova leaves that affect relative host plant resistance to adult Japanese beetles.

Table 12

Paired single taxon fecundity studies for adult female Japanese beetles feeding on pubescent Asian elms with leaf trichomes present and with trichomes removed.

Paired single taxon fecundity studies for adult female Japanese beetles feeding on pubescent Asian elms with leaf trichomes present and with trichomes removed.
Paired single taxon fecundity studies for adult female Japanese beetles feeding on pubescent Asian elms with leaf trichomes present and with trichomes removed.

Leaf thickness and toughness, and host susceptibility and preference

Physical plant traits, such as leaf toughness and thickness, can greatly influence invertebrate feeding and usually correlate with leaf fiber and lignin content (Graca and Zimmer 2005). Agrawal and Fishbein (2006) found leaf toughness could be used to predict herbivory of many plants including milkweeds (Asclepias spp.), and Raupp (1985) found that the toughness of willow (Salix spp.) leaves reduced leaf beetle feeding due to mandibular wear. In field defoliation trials, Bosu et al. (2007) observed that the thicker and tougher leaves of Asian elm taxa and taxa experienced much less defoliation by the elm leaf beetle (Pyrrhalta luteola Muller). Potter and Kimmerer (1988) found that the thick glabrous cuticle and tough leaf margins of the American holly (Ilex opaca Ait.) leaves were more important than leaf margin spines in deterring edge feeding caterpillars. Miller and Ware (2014), determined that the thicker and tougher leaves of most Asian elm taxa and hybrids were less susceptible to feeding by the elm leafminer (Fenusa ulmi Sundevall).

In earlier field defoliation studies and no-choice (NC), and multiple-choice (MC) laboratory bioassay feeding studies, evaluating Ulmaceae for feeding host susceptibility and preference for the Japanese beetle, Miller et al. (1999, 2001a), Condra et al. (2010), Potter and Redmond (2013), and Griffin et al. (2017) found that the thicker and tougher leaves of certain Asian elm species such as U. parvifolia and cultivars, U. propinqua, U. lamellosa, U. macrocarpa, U. pseudopropinqua, U. prunifolia, and U. taihangshanensis were much less susceptible to feeding by Japanese beetles. The complex Asian hybrids of ‘Accolade', ‘Commendation', ‘Danada Charm', ‘Triumph', and ‘Vanguard' were more susceptible to feeding even though they had variable leaf thickness and toughness (Miller et al. 1999, Condra et al. 2010, Potter and Redmond 2013, Griffin et al. 2017). Miller, et al. (1999) found that the thicker leaves of U. castaneifolia were equally appealing as the thinner leaves of U. gausenii, U. japonica, and U. szechuanica.

Results from the ten-year national elm field trial revealed that ‘Homestead' and ‘Pioneer' had the highest Japanese feeding damage while U. parvifolia, U. propinqua, ‘Valley Forge', ‘New Harmony', ‘Prospector', ‘New Horizon', and ‘Frontier' were the most resistant to Japanese feeding damage (Griffin et al. 2017). In this study, ‘Homestead' and ‘Frontier' had significantly thinner and more tender leaves compared to ‘Pioneer', but all three taxa were much less preferred in the field study. However, in our multiple-choice (MC) studies, ‘Pioneer' was more preferred, but ‘Homestead' was one of the least preferred. Our results are also consistent with studies by Rowe and Potter (2000) who found that Japanese beetles fed the same on sun and shade leaves of rose (Rosa variety floribunda ‘Class Act') of equal toughness as well as the thicker sun and thinner shade rose leaves. Similar conflicting results with regard to leaf thickness and toughness were reported by Keathley and Potter (2008) for both preferred and non-preferred hosts of Japanese beetle, and for Carpinus taxa by Miller and Wiegrefe (2021). It appears that in this study, leaf thickness and inner and outer leaf toughness are not good indicators of host susceptibility for Japanese beetle feeding.

Hybridization, susceptibility, preference, and suitability

Hybridization may have both a positive and/or negative influence on susceptibility, preference, and suitability for adult Japanese beetles and may be polygenic, and not the result of a single gene expression (Paige and Capman 1993, Fritz et al. 1999, Cheng et al. 2011). It is well known that secondary metabolites are a common chemical defense employed by plants against herbivorous insects and hybridization may increase the variation of secondary metabolites affecting herbivore resistance (Patton et al, 1997, Fulcher et al. 1998, Orians 2000, Cheng et al. 2011). Most secondary metabolites (SMs) may be present in the parents, but hybrids may miss some parental SMs or have novel ones (Paige and Capman 1993, Cheng et al. 2011, Lopez-Caamal and Tovar-Sanchez 2014). In this study, U. carpinifolia, U. pumila, and members of the David (U. davidiana) complex (i.e. U. japonica, U. wilsonsiana, U. propinqua) appear to either increase, decrease, and/or have no effect on feeding preference. For example, in the multiple-choice (MC) laboratory feeding bioassays and field defoliation studies, when a susceptible or preferred species such as U. carpinifolia or U. pumila is crossed with a much less susceptible or preferred species (i.e. U. parvifolia or U. glabra), the resulting hybrids of ‘Frontier' and ‘Pioneer' are more preferred. Further, when highly preferred U. pumila is crossed with U. japonica, preference increased for the ‘Sapporo Autumn Gold' hybrid (U. pumila x U. japonica), but the opposite is also true for the U. pumila x U. japonica hybrids of ‘Cathedral' and ‘New Horizon' where preference decreased. However, in the case of ‘Homestead' and ‘Urban elm', both complex hybrids including U. pumila, U. carpinifolia, and U. x hollandica ‘Vegeta' parentage, there was a reduction in preference. When U. wilsoniana is crossed with the less preferred U. japonica (i.e. ‘Accolade', ‘Danada Charm'), there is no appreciable change in preference, but preference decreases when combined with U. carpinifolia and U. pumila parentage for ‘Commendation'. It appears that U. carpinifolia and U. pumila tend to increase preference in simple and complex elm hybrids, but members of the David elm (U. davidiana) complex (i.e. U. wilsoniana and U. japonica) tend to decrease preference.

The reason for this hybrid effect is not clear but is probably related to leaf chemistry and to a lesser extent, leaf pubescence. A similar phenomenon, the “U. pumila and U. carpinifolia factor” has been observed in elms (Ulmus spp.), where when Siberian elm (U. pumila) is incorporated into hybrids with other taxa it appears to affect the susceptibility, preference, and suitability of elms to an extensive defoliating insect guild including Japanese beetle, elm leaf beetle (Pyrrhalta luteola), spring cankerworm (Paleacrita vernata Peck), fall cankerworm (Alsophila pometaria Harris), and elm leafminer (Fenusa ulmi) (Miller and Ware 1994, 1997, 1999a, 2014, Miller et al. 1999, 2001a,b,c, 2014, Bosu et al. 2007, Bosu and Wagner 2007, Condra et al. 2010, Griffin et al. 2017).

Leaf thickness and toughness, and host suitability

There does not appear to be a clear relationship between leaf thickness and host suitability (i.e. fecundity). However, inner and outer leaf toughness was related to suitability. For example, adult female beetles feeding on the thicker leaves of U. lamellosa, U. macrocarpa, and U. propinqua laid significantly more eggs compared to female beetles feeding on the thinner leaves of U. gausenii, U. japonica, and U. szechuanica. Keathley and Potter (2008) found that the fecundity of Japanese beetles feeding on the tougher leaves of susceptible Virginia creeper [Parthenocissus quinquefolia (L.) Planch] was comparable to S. albidum, a highly preferred host. Similarly, Miller and Wiegrefe (2021) determined that adult Japanese beetles feeding on the thicker leaves of Carpinus caroliniana, and the hybrids of C. betulus x C. tschonoskii and C. caroliniana x C. betulus laid a similar number of eggs as S. albidum. Keathley and Potter (2008) also reported that Japanese beetles feeding on the resistant, and thin leaves of Cornus florida L. laid far fewer eggs. In contrast, Miller and Wiegrefe (2021) found that beetles feeding on the thinner and more-tender C. laxiflora leaves were significantly more fecund, but in the same study, Japanese beetles feeding on the thinner and more-tender leaves of C. japonica and C. cordata laid fewer eggs. Conversely, in the same study by Miller and Wiegrefe (2021), adult beetles feeding on thicker and tougher leaves of C. coreana, C. fargesii, C. turczaninari, and the hybrids of C. caroliniana x C. cordata, C. caroliniana x C. coreana, and C. caroliniana x C. orientalis laid significantly fewer eggs. It appears that leaf characteristics (i.e. leaf chemistry) other than thickness and toughness are more important for determining suitability for adult Japanese beetles (Ladd 1986, Barbosa and Krischik 1987, Ladd 1988, Stamp and Harmon 1991, Fulcher et al. 1996, 1998, Keathley et al. 1999, Potter and Held 1999, Paluch et al. 2006).

Leaf trichomes and host susceptibility

While leaf trichomes may provide a general defense, the effect of pubescence may be positive, negative, or non-existent depending on the herbivore species, and can be influenced by genotype, the environment, leaf development stage, and previous feeding (Levin 1973, Roberts et al. 1979, Southwood 1986, Peter et al. 1995, Hare and Elle 2002, Bosu and Wagner 2007, Handley et al. 2005, Dalin et al. 2008, Kariyat et al. 2018). Trichomes may also help protect plants from insect herbivores specifically as it relates to feeding, growth, survival, and oviposition. Feeding may be negatively correlated with trichome density, but is generally considered a “soft weapon” in plant defense compared to other plant traits (Levin 1973, Potter et al. 1998, Miller and Ware 1999a, Miller 2000, Miller et al. 2001a,b,c, Dalin et al. 2008).

In this study, leaf trichome density does not appear to be a good indicator of feeding susceptibility. For example, of the 11 pubescent elm taxa evaluated in paired single taxon NC feeding studies, adult Japanese beetles removed significantly less leaf tissue on five taxa including U. chenmoui, U. gausennii, U. glaucescens var. lasiophylla, U. lamellosa, and U. macrocarpa where trichomes were present, but trichome densities ranged from 184 to 512 per mm2 on U. gausennii and U. lamellosa leaves, respectively. Conversely, adult Japanese beetles feeding on U. glaucescens leaves removed significantly more leaf tissue on leaves with trichomes present compared with leaves where the trichomes had been removed (t=4.2, P<0.0002). Why this occurred is not clear. Ulmus glaucesens leaves have the highest density of trichomes (581 per mm2) compared with the other pubescent elm taxa, but adult Japanese beetles removed significantly more leaf tissue from U. glaucescens leaves with trichomes present compared with leaves where the trichomes had been removed (t=4.2, P<0.0002). The leaves of U. glaucescens are significantly thinner and much less tough than the other pubescent elm taxa studied here which may allow for greater adult beetle feeding. Additionally, U. glaucescens leaves contain a combination of non-glandular and glandular trichomes, and it is possible that the glandular trichomes may act as a feeding attractant (Dalin and Bjorkman, 2003, Valkama et al. 2003, Ventrella and Marinho 2008) and/or the non-glandular trichomes found on U. glaucescens leaves do not serve as a significant feeding deterrent. Dalin et al. (2008) found that the leaf beetle (Phratora vulgatissima) was capable of removing non-glandular trichomes when feeding on willow (Salix viminalis) leaves. However, our findings here contradict a study by Miller et al. (1999), where they found U. glaucescens to have low susceptibility in NC laboratory feeding studies, and a low field defoliation rating. However, for the remaining six pubescent elm taxa, there was no significant difference in leaf tissue removed with respect to trichome density.

In a recent study, Miller and Wiegrefe (2021) found that the pubescent leaves of Carpinus japonica and C. tschonoskii differed in their suitability for adult Japanese beetles. Pubescent C. tschonoskii leaves, with trichomes present, were less susceptible, preferred, and suitable for feeding by adult Japanese beetles, pubescent C. japonica leaves were found to be highly susceptible and preferred for feeding but were less suitable for Japanese beetle reproduction. Additionally, ‘Patriot' elm has pubescence on the underside of the leaf, and in NC feeding studies had significantly less leaf tissue removed by elm leaf beetles compared to ‘Homestead' and ‘American Liberty' (Townsend et al. 1995). However, in our study, feeding by adult Japanese beetles on ‘Patriot', which has similar adult feeding habits to elm leaf beetle, was significantly higher in our NC studies. This suggests that leaf pubescence is not universal in preventing feeding by herbivorous insects. Our findings are consistent with a field study conducted by Condra et al. (2010), where they found that there was no overall relationship between Japanese beetle injury and elm leaf pubescence ratings, and their mean pubescence rating did not differ between their six most and least resistant elm taxa. Further study is required to determine these inconsistencies in feeding susceptibility preference, and suitability, and the role of leaf trichomes in host plant resistance.

Leaf trichome morphology and susceptibility

Plants have the ability to produce glandular (chemical-producing) and non-glandular trichomes. These trichomes may vary in the morphology and diversity among plant species, and even genetically within individual plant species (Southwood 1986, Agarwal 1999, 2000, Werker 2000, Dalin and Bjorkman 2003, Valkama et al. 2003, Ventrella and Marinho 2008). Non-glandular trichomes function in structural defense and have low nutritional value compared with glandular trichomes which may provide both structural and chemical defense and may contain terpenes and alkaloids that act as feeding deterrents or toxins (Levin 1973, Shade et al. 1979, Robinson et al. 1980, Rautio et al. 2002, Valkama et al. 2003, Ventrella and Rarinho 2008, War et al. 2012). Many studies have demonstrated that the presence of simple and glandular trichomes may deter or impede feeding susceptibility, preference, and/or oviposition by leaf-feeding beetles such as the alfalfa weevil (Danielson 1987), alfalfa blotch leafminer (MacLean and Byers 1983), blackvine weevil (Doss et al. 1987), Colorado potato beetle (Casagrande 1982), cereal leaf beetle (Hoxie et al. 1975) and Japanese beetle (Potter et al. 1998, Miller and Ware 1999a, Miller 2000,Miller et al. 2001b, Held 2004, Condra et al. 2010, Miller and Wiegrefe 2021). In the aforementioned Japanese beetle studies, leaves of Tilia, Ulmus, and Carpinus taxa with thick trichome mats, long upright hairs, and moderate to dense leaf pubescence had less leaf area consumed compared to more glabrous leaves or leaves with very sparse trichome density.

While not thoroughly examined in this study, trichome morphological traits (i.e. simple or glandular, and length) may also be a factor in attracting the herbivore to the host plant and for oviposition (Lill et al. 2006). For example, certain wheat varieties with long, erect trichomes deter leaf-beetle oviposition much more than varieties with a sparse growth of short trichomes (Hoxie et al. 1975, Roberts et al. 1979). Some glandular trichomes emit adhesives, resins, and/or mixtures of aldehydes, alkanes, and esters entrapping and/or killing the herbivorous insect (Webb et al. 1971, Schalk and Stoner 1976, Kennedy and Yamamoto 1979, Johnson et al. 1980a,b, Ryan et al. 1982, Tingey and Laubengayer 1986, Yencho and Tingey 1994). Simple trichome morphology may demonstrate antibiotic effects contributing to host plant resistance. Hooked trichomes can impale young leafhopper nymphs, puncture eggs of leaf feeding beetles, and impair movement of young leaf feeding caterpillars (Pillemer and Tingey 1976, Wellso,1979, Ramalho et al. 1984,). Conversely, trichomes may also play a role in attracting herbivores to the host plant (Southwood 1986).

Electron microscopy and observations by the authors of leaf trichomes on the abaxial (lower) and adaxial (upper) leaf surfaces of the elm taxa of U. chenmoui, U. glaucescens, U. lamellosa, U. macrocarpa, and U. propinqua revealed some interesting contrasts (Figures 1a,b,c,d and 2 a,b,c,d). For example, adult Japanese beetles removed the greatest amount of leaf tissue from U. chenmoui leaves when trichomes were present. In a study by Miller et al. (1999), U. chenmoui was found to be highly susceptible and preferred by Japanese beetles. Trichomes on the lower leaf surface of U. chenmoui are of medium density, uneven length, and not all are upright. On the upper leaf surface, trichomes are scattered with bulbous bases, some curving and of uneven lengths. Trichomes on the lower leaf surface of U. glaucescens (Figures 1d, 2d) and upper leaf surface of U. propinqua (Figure 1c) are very dense and thick, fine, straight, and of even length, with some curvature on the upper leaf surface. In this study, U. glaucescens and U. propinqua had moderate amounts of leaf tissue removed which is consistent with a study by Miller et al. (1999) where both taxa were moderately susceptible and more preferred. In contrast, the leaf trichomes on the lower and upper surfaces (Figures 2 a, c) of U. macrocarpa are of medium density, but have a bulbous base which may suggest they are glandular, and possess feeding deterrent chemicals making the leaf less palatable. This is evidenced in our study by minimal leaf feeding by adult Japanese beetles on U. macrocarpa leaves when trichomes are present, and is consistent with a study by Miller et al. (1999) where they found U. macrocarpa was not susceptible to feeding or preferred by Japanese beetles. The trichomes on U. lamellosa leaves are scattered and many tend to be broken off during the growing season, giving the leaves a very rough or sandpapery feel (author's personal observations) (Figures 1a, 2b). This sandpapery feel may account for the lower level of feeding in this study, and in a study by Miller et al. (1999), for adult feeding susceptibility and preference. Additionally, Miller and McMahan (in press) found that the “sandpapery” upper leaf surface of Fraxinus chinensis was less susceptible to feeding the adult emerald ash borer (Agrilus planipennis).

Fig. 1a, b, c, d

Elm leaf trichomes. a. (upper left) U. lamellosa, upper surface (840X), b. (upper right) U. glaucescens, upper surface (60X), c. (lower left) U. propinqua, upper suface (620X), d. (lower right) U. glaucescens, lower surface (1,510X).

Fig. 1a, b, c, d

Elm leaf trichomes. a. (upper left) U. lamellosa, upper surface (840X), b. (upper right) U. glaucescens, upper surface (60X), c. (lower left) U. propinqua, upper suface (620X), d. (lower right) U. glaucescens, lower surface (1,510X).

Close modal
Fig. 2a,b,c,d

Elm leaf trichomes. a. (upper left) U. macrocarpa, lower surface (430X), b. (upper right) U. lamellosa, upper surface (65X), c. (lower left) U. macrocarpa, upper surface (63X), d. (lower right) U. glaucescens, lower surface (60X).

Fig. 2a,b,c,d

Elm leaf trichomes. a. (upper left) U. macrocarpa, lower surface (430X), b. (upper right) U. lamellosa, upper surface (65X), c. (lower left) U. macrocarpa, upper surface (63X), d. (lower right) U. glaucescens, lower surface (60X).

Close modal

Leaf trichome morphology and suitability

The relationship between trichome density and morphology, and host suitability is unclear. Collectively, of the 11 pubescent Asian elms evaluated in this study, there was no significant difference in total eggs laid, eggs produced per female, or eggs produced per ovipositing female (Data not shown). However, a significantly higher percentage of females oviposited when feeding on leaves with the trichomes removed compared with leaves with trichomes present (Data not shown). It is possible that trichome morphology (simple vs. glandular) may be a factor in host suitability (Peter et al. 1995). Adult female Japanese beetles feeding on the long, thin, and fine trichomes of U. chenmoui, laid a similar number of eggs compared with leaves where the trichomes had been removed. Further, adult females laid significantly more eggs when feeding on U. glaucescens and U. propinqua leaves, both with similar trichome structure and lacking glandular trichomes, than on leaves where the trichomes had been removed. Conversely, trichome morphology differed considerably between U. lamellosa and U. macrocarpa leaves, but adult female beetles laid significantly more eggs when feeding on U. macrocarpa leaves with bulbous (i.e. glandular) trichomes present, and on U. lamellosa with short, but simple trichomes. While glandular trichomes are generally considered to possess feeding deterrent chemicals, it possible that they may exude chemicals that enhance their suitability for certain herbivorous insects such as the Japanese beetle (Southwood 1986). Further studies are needed to better understand the relationship between trichome morphology, and chemistry, and their role(s) in host susceptibility, preference, and suitability for the Japanese beetle, and other herbivorous insect pests.

In conclusion, the complex Asian hybrids of ‘Accolade', ‘Commendation', ‘Danada Charm', ‘Triumph', ‘Vanguard', the simple and complex Eurasian hybrids of ‘Homestead', ‘Prospector', and ‘Cathedral', and recently developed American elm cultivars (i.e. ‘Valley Forge', ‘Jefferson', ‘New Harmony') are already in the trade, and are performing well as parkway and landscape trees due to their resistance to DED, and/or elm yellows, and most sap-feeding and leaf-feeding insect pests (Santamour and Bentz 1985, Smalley and Guries 1993, Sinclair et al. 2000, Jacobs et al. 2003, Costello et al. 2004, Bosu et al. 2007, Herath et al. 2010, Griffin et al. 2017). However, there may be some use limitations for some of the above taxa in settings with chronic and/or heavy elm leaf beetle, elm leafminer, and elm flea weevil (Orchestes ulmi) populations (Guries and Smalley, 1994, Miller, 2000, Miller and Ware 2001a,b,c,d,2014, Miller et al. 2003, Condra et al. 2010, Potter and Redmond 2013, Griffins et al. 2017). Elm selection should be based on hardiness zones, growth characteristics, and tempered with regard to resistance and/or tolerance to local insect and disease pressure when planning for future urban tree plantings

Ulmaceae taxa evaluated in this study, including U. parvifolia and cultivars, members of the David elm complex (i.e. U. japonica, U. wilsoniana, U. propinqua), North American taxa of U. rubra and U. serotina, European taxa including U. suberosa and U. sukaczevii, and certain Zelkova taxa and cultivars, should be considered in future tree breeding efforts because of their desirable horticultural attributes, their ability to tolerate harsh urban growing conditions, their resistance to DED, and feeding damage by herbivorous insect pests, particularly where chronic Japanese beetle populations are sporadic or absent (Ware 1992, 1995, Miller et al. 1999, 2001, Warren 2000, Hartman et al. 2007, Brady et al. 2008, McPherson et al. 2008, Dirr 2009, Condra et al. 2010, Giblin and Gilman 2010, Potter and Redmond 2013, Griffin et al. 2017). More research is needed to better identify the physical and chemical factors involved with Ulmaceae host plant resistance, and how these factors might be incorporated into a more comprehensive tree breeding program.

Agrawal,
A.A.,
1999
.
Induced responses to herbivory in wild radish: effects on several herbivores and plant fitness
.
Ecology
80
:
1713
1723
.
Agrawal,
AA.
2000
.
Specificity of induced resistance in wild radish: causes and consequences for two specialist and two generalist caterpillars
.
Oikos
89
:
493
500
.
Agrawal,
A.A.
and
Fishbein
M.
2006
.
Plant defense syndromes
.
Ecology
87
:
S132
S149
.
Barbosa,
P.
and
Krischik
V.A.
1987
.
Influence of alkaloids on feeding preference of eastern deciduous forests by the gypsy moth (Lymantria dispar)
.
American Naturalist
130
:
53
69
.
Bosu,
P.P.
and
Wagner
M.R.
2007
.
Effects of induced water stress on leaf trichome density and foliar nutrients of three elm (Ulmus) species: Implications for resistance to elm leaf beetle
.
Environmental Entomology
36
(3)
:
595
601
.
Bosu,
P.P.,
Miller
F.,
and
Wagner
M. R.
2007
.
Susceptibility of 32 elm species and hybrids (Ulmus spp.) to the elm leaf beetle (Coleoptera: Chrysomelidae) under field conditions in Arizona
.
Journal of Economic Entomology
100
(6)
:
1808
1814
.
Brady,
C.,
Condra
J.,
and
Potter
D.
2008
.
Resistance of landscape suitable elm (Ulmus spp.) cultivars to Japanese beetles, leaf miners, and gall-makers . University of Kentucky: 2008 research report, Nursery and Landscape program.
p.
15
16
.
Carter,
J. C.
and
Carter
L. R.
1974
.
An urban epiphytotic of phloem necrosis and Dutch elm disease, 1944-1972
.
Illinois Natural History Survey Bulletin
31
:
113
143
.
Casagrande,
R.A.
1982
.
Colorado potato beetle resistance in wild potato, Solanum berthaultii
.
Journal of Economic Entomology
75
:
368
372
.
Cheng,
D.,
Vrieling
K.,
and
Klinkhamer
P.G.L.
2011
.
The effect of hybridization on secondary metabolites and herbivore resistance: implications for the evolution of chemical diversity in plants
.
Phytochemistry Review
10
:
107
117
Condra,
J.M.,
Brady
C.M.,
and
Potter.
D.A.
2010
.
Resistance of landscape-suitable elms to Japanese beetle, gall aphids, and leaf miners, with notes on life history of Orchestes alni and Agromyza aristata in Kentucky
.
Arboriculture and Urban Forestry
36
:
101
109
.
Costello,
L.R.,
Scott
S.R.,
and
Drake
C.M.
2004
.
A 10-year evaluation of the performance of four elm cultivars in California, U.S
.
Journal of Arboriculture
30
(2)
:
114
122
.
Cunningham,
P.A.
and
Dix
M.E.
1983
.
Variation among Siberian elms in their susceptibility to defoliation by the spring cankerworm
.
Proc. North Central Tree Improvement Conf. Wooster
,
OH
.
p.
55
60
.
Dalin,
P.
and
Bjorkman
C.
2003
.
Adult beetle grazing induces willow trichome defense against subsequent larval feeding
.
Oecologia
134
:
112
118
.
Dalin,
P.,
Agren
J.,
Bjorkman
C.,
Huttumen
P.,
and
Karkkainen
K.
2008
.
Leaf trichome formation and plant resistance to herbivory. Chapter 4
p.
89
105
In: Induced plant resistance to herbivory. Springer Publishers, New York, New York.
Danielson,
S.D.,
Manglitz
G.R.,
and
Sorensen
E.L.
1987
.
Resistance of perennial glandular-haired Medicago species to oviposition by alfalfa weevils (Coleoptera: Curculionidae). Environmental
.
Entomology
16
:
195
197
.
Dirr,
M.A.,
2009
.
Manual of woody landscape plants: Their identification, ornamental characteristics, culture, propagation, and uses
.
Stipes Publishing Company
,
Champaign, Illinois
.
826
p.
Doss,
R.P.,
Shanks,
C.H.
Jr.,
Chamberlain
J. D.,
and
Garth
J.K.L.
1987
.
Role of leaf hairs in resistance of a clone of strawberry, Fragaria chiloensis, to feeding by adult black vine weevil, Otiorhynchus sulcatus (Coleoptera: Curculionidae)
.
Environmental Entomology
16
:
764
766
.
Fleming,
W.E.
1972
.
Biology of the Japanese beetle. U.S. Department of Agriculture Technical Bulletin #1449.
129
p.
Fritz
R.S.,
Moulia
C.,
and
Newcombe
C. G.
1999
.
Resistance of hybrid plants and animals to herbivores, pathogens, and parasites
.
Annual Review of Ecological Systems
30
:
565
591
.
Fu,
Li-Guo.
1980
.
Studies in the genus Ulmus in China. Northeastern Forest Institute.
40
p.
Fulcher,
A.F.,
Ranney
T. J.,
Burton
J.D.,
Walgenbach
J.F.,
and
Maness
E.P.
1996
.
Natural resistance to Japanese beetles among Malus taxa: Role of endogenous foliar phenolics
.
Proceedings of the Southern Nursery Research Conference
41
:
57
60
.
Fulcher,
A.F.,
Ranney
T.G.,
and
Burton
J.D.
1998
.
Role of foliar phenolics in host plant resistance of Malus taxa to adult Japanese beetles
.
HortScience
233
:
862
865
.
Giblin,
C.P.
and
Gilman
J.H.
2010
.
DED resistant elms for the urban forest. N.E.W. Horticulture Newsletter
.
Volume
33
(2)
:
1
2
,
10-14.
Graca,
M.A.S.
and
Zimmer
M.
2005
.
Leaf toughness. Ch 18 In: Methods to study litter decomposition: A practical guide.
Graca,
M.A.S.,
Barlocher
F.,
and
Gessner
M.O.
eds.
Springer Publishers,
New York, New York.
p.
121
125
.
Griffin,
J.J.,
Jacobi
W.R.,
McPherson
E.G.,
Sadof
C.S.,
McKenna
J.R.,
Gleason
M.L.,
Gauthier
N.W.,
Potter
D.A.,
Smitley
D.R.,
Adams
G.C.,
Gould
A. B.,
Cash
C.R.,
Walla
J. A.,
Starrett
M.C.,
Chastagner
G.,
Sibley
J.L.,
Krischik
V.A.,
and
Newby
A.F.
2017
.
Ten-year performance of the United States national elm trial
.
Arboriculture and Urban Forestry
43
(3)
:
107
120
.
Guries,
R.P.
and
Smalley
E.B.
1994
.
Variations in elm leafminer injury on elms in Wisconsin. Proceedings of the Eighth METRIA conference and the International Ornamental Crabapple Society
.
U.S. National Arboretum
,
Washington, D.C., USA
.
p.
214
218
.
Hall,
R.W.
1986
.
Preference and suitability of elms for adult elm leaf beetle, Xanthogaleruca luteola (Coleoptera: Chrysomelidae)
.
Environmental Entomology
15
:
143
146
.
Hall,
R.W.
and
Townsend
A.M.
1987
.
Suitability of Ulmus wilsoniana, the ‘Urban' Elm, and their hybrids for the elm leaf beetle, Xanthogaleruca luteola (Müller) (Coleoptera: Chrysomelidae)
.
Environmental Entomology
16
:
1042
1044
.
Hall,
R.W.,
Townsend
A.M.,
and
Barger
J.H.
1987
.
Suitability of thirteen different host species for elm leaf beetle, Xanthogaleruca luteola(Coleoptera: Chrysomelidae)
.
Journal of Environmental Horticulture
5
:
143
145
.
Hall,
R.W.
and
Young
C.E.
1986
.
Host suitability of three Asiatic elms to the elm leaf beetle (Xanthogaleruca luteola) (Coleoptera: Chrysomelidae)
.
Journal of Environmental Horticulture
4
:
44
46
.
Handley,
R.,
Ekbom
B.,
Agren
J.
2005
.
Variation in trichome density and resistance against a specialist insect herbivore in natural populations of Arabidopsis thaliana
.
Ecological Entomology
30
:
284
292
.
Hare,
J.D.
and
Elle
E.
2002
.
Variable impact of diverse herbivores on dimorphic Datura wrightii
.
Ecology
83
:
2711
2720
.
Hartman,
J.,
Dixon
E.,
Potter
D.,
Brady
C.,
Edelen
J.,
Hart
J.,
and
Fountain
W.
2007
.
National Elm Trial-Kentucky Data. University of Kentucky Nursery and Landscape Program Overview.
p.
35
36
.
Hawley,
I.M.
and
Metzger
F.W.
1940
.
Feeding habits of the adult Japanese beetle. U.S. Dep. Agric. Circ. 547.
31
p.
Held,
D.W.
2004
.
Relative susceptibility of woody landscape plants to Japanese beetle (Coleoptera: Scarabaeidae)
.
Journal of Arboriculture
30
(6)
:
328
335
.
Herath,
P.,
Hoover
G.A.,
Angelini
E.,
and
Moorman
G.W.
2010
.
Detection of elm yellows in elms and insects using real-time-PCR
.
Plant Disease
94
:
1355
1360
.
Hoxie,
R.P.,
Wellso
S.G.,
and
Webster
J.A.
1975
.
Cereal leaf beetle response to wheat trichome length and density
.
Environmental Entomology
4
:
365
370
.
Jacobs,
K.A.,
Lee
L.M.,
Griffiths
H.M.,
Miller
F.D.,
and
Bottner
K.D.
2003
.
A new member of the clover proliferation phytoplasma group (16SrVI) associated with elm yellows in Illinois
.
Plant Disease
87
:
241
246
.
Jandel Scientific.
1992
.
SigmaStat for Windows
.
San Rafael
,
CA
.
652
p.
Johnson,
K.J.R.,
Sorenson
E.L.,
and
Horber
E.K.
1980
a.
Resistance in glandular haired annual Medicago species to feeding by adult alfalfa weevils
.
Environmental Entomology
9
:
133
136
.
Johnson,
K.J.R.,
Sorenson
E.L.,
and
Horber
E.K.
1980
b.
Resistance of glandular haired annual Medicago species to oviposition by adult alfalfa weevils
.
Environ. Entomology
.
9
:
241
245
.
Kariyat,
R.R.,
Hardison
S.B.,
Ryan
A.B.,
Stephenson
A.G.,
DeMoraes
C.M.,
and
Mescher
M.C.
2018
.
Leaf trichomes affect caterpillar feeding on an instar-specific manner
.
Communicative and Integrative Biology
11
(3)
:
1
6
.
Keathley,
C.P.
and
Potter
D.A.
2008
.
Quantitative resistance traits and suitability of wood plant species for a polyphagous Scarab, Popillia japonica Newman
.
Environmental Entomology
37
(6)
:
1548
1557
.
Keathley,
C.P.,
Potter
D.A.,
and
Houtz
R.L.
1999
.
Freezing-altered palatability of Bradford pear to Japanese beetle: Evidence for compartmentalization and enzymatic degradation of feeding deterrents
.
Entomological Experimental Application
90
:
49
59
.
Kennedy,
G.G.
and
Yamamato
R.T.
1979
.
A toxic factor causing resistance in wild tomato to the tobacco hornworm and some other insects
.
Entomologia Experimentalis et Application
26
:
121
126
.
Ladd,
T.L.,
Jr.
1986
.
Influence of sugars on the feeding response of Japanese beetles (Coleoptera: Scarabaeidae). Journal of Economic Entomology79:668-671.
Ladd,
T.L.,
Jr.
1987
.
Japanese beetle (Coleoptera: Scarabaeidae): influence of favored food plants on feeding response
.
Journal of Economic Entomology
80
:
1014
1017
.
Ladd,
T.L.
1988
.
Japanese beetle (Coleoptera: Scarabaeidae): Influence of sugars on feeding response in larvae
.
Journal of Economic Entomology
81
:
1390
1393
.
Ladd,
T.L.,
Jr.
1989
.
Japanese beetle (Coleoptera: Scarabaeidae): feeding by adults on minor host and nonhost plants
.
Journal of Economic Entomology
82
:
1616
1619
.
Levin.
D.A.
1973
.
The role of trichomes in plant defense
.
Quarterly Review of Biology
.
48
:
3
15
.
Lill,
J.T.,
Marquis
R.J.,
Forkner
R.E.,
LeCorff
J.,
Holmberg
N.,
and
Barber
N.A.
2006
.
Leaf pubescence affects distribution and abundance of generalist slug caterpillars (Lepidoptera: Limacodidae)
.
Environmental Entomology
35
(3)
:
797
806
.
Lopez-Caamal,
A.,
and
Tovar-Sanchez
E.
2014
.
Genetic, morphological, and chemical patterns of plant hybridization
.
Revista, Chilena de Historia Natural
87
:
1
16
.
Loughrin,
J.H.,
Potter
D.A.,
Hamilton-Kemp
T.R.,
and
Byers
M.E.
1996
.
Volatile compounds from crabapple cultivars (Malus spp.) differing in susceptibility to the Japanese beetle (Popillia japonica Newman)
.
Journal of Chemical Ecology
22
:
1295
1305
.
Loughrin,
J.H.,
Potter
D.A.,
Hamilton-Kemp
T.R.,
and
Byers
M.E.
1997
.
Response of Japanese beetles (Coleoptera: Scarabaeidae) to leaf volatiles of susceptible and resistant maple species
.
Environmental Entomology
26
:
334
342
.
MacLean,
P.S.,
and
Byers
R.A.
1983
.
Ovipositional preferences of the alfalfa blotch leafminer (Diptera: Agromyzidae) among some simple and glandular-haired Medicago species
.
Environmental Entomology
12
:
1083
1086
.
Matsuda,
K.
and
Senbo
S.
1986
.
Chlorogenic acid as a feeding deterrent for the salicaceae-feeding leaf beetle, Lochmateae capreae cribrata (Coleoptera: Chrysomelidae) and other species of leaf beetles
.
Applied Entomology and Zoology
21
:
411
416
.
McPherson,
G.,
Costello
L.,
Harding
J.,
Dreistadt
S.,
Flint
M.L.,
and
Mezger
S.
2008
.
National elm trial: Initial report from northern California. Western Arborist, Fall, 2009.
p.
32
36
.
Meredith,
W.R.,
Jr.
and
Schuster
M.F.
1979
.
Tolerance of glabrous and pubescent cottons to tarnished plant bug
.
Crop Science
19
:
484
488
.
Miller,
F.
2000
.
Insect resistance of elm genotypes. Proceedings of the First International Elm Conference. The Elms: Breeding; Conservation, and Disease Management. ed.
Dunn
C.
p. 137-154.
Miller,
F.
and
Ware
G.
1994
.
Preference for and suitability of selected elms, Ulmus spp., and their hybrids for the elm leaf beetle (Pyrrhalta luteola Coleoptera: Chrysomelidae)
.
Journal of Environmental Horticulture
12
:
231
235
.
Miller,
F.
and
Ware
G.
1997
.
Preference for and suitability of Asian elm species and hybrids for the adult elm leaf beetle (Coleoptera: Chrysomelidae)
.
Journal of Economic Entomology
90
(6)
:
1641
1645
.
Miller,
F.
and
Ware
G.
1999
a.
Feeding preference for selected Tilia spp. and cultivars by the adult Japanese beetle (Coleoptera: Scarabaeidae)
.
Journal of Arboriculture
25
(3)
:
168
173
.
Miller,
F.
and
Ware
G.
1999
b.
Resistance of elms of the Ulmus davidiana complex to defoliation by the adult elm leaf beetle (Coleoptera: Chrysomelidae)
.
Journal of Economic Entomology
92
(5)
:
1147
1150
.
Miller,
F.,
Jerdan
S.,
and
Ware
G.
1999
.
Feeding preference of adult Japanese beetles (Coleoptera: Scarabaeidae) for Asian elm species and their hybrids
.
Journal of Economic Entomology
92
(2)
:
421
426
.
Miller,
F.
and
Ware
G.
2001
a.
Resistance of temperate Chinese elms (Ulmus spp.) to feeding by the adult elm leaf beetle (Coleoptera: Chrysomelidae)
.
Journal of Economic Entomology
94
(1)
:
162
166
.
Miller,
F.
and
Ware
G.
2001
b.
Host suitability of Asiatic elms species and hybrids for larvae and adults of the elm leaf beetle (Coleoptera: Chrysomelidae)
.
Journal of Arboriculture
27
(3)
:
118
125
.
Miller,
F.
and
Ware
G.
2001
c.
Evaluation of eleven newly acquired Asian elms for their suitability to adult elm leaf beetle (Coleoptera: Chrysomelidae)
.
Journal of Environmental Horticulture Vol
.
19
(2)
:
96
99
.
Miller,
F.
and
Ware
G.
2001
d.
Feeding and ovipositional responses of the adult elm leaf beetle (Coleoptera: Chrysomelidae) to simple and complex Asian elm hybrid selections. Journal of Environmental Horticulture
.
Vol
.
19
:
128
131
.
Miller,
F,
Ware
G.,
and
Jackson
J.
2001
a.
Preference of temperate Chinese elms (Ulmus spp.) for the adult Japanese beetle (Coleoptera: Scarabaeidae)
.
Journal of Economic Entomology
94
(2)
:
445
448
.
Miller,
F.,
Malmquist
K.,
and
Ware
G.
2001
b.
Evaluation of Asian, European, and North American elm (Ulmus spp.) biotypes to feeding by spring and fall cankerworms. Journal of Environmental Horticulture
.
Vol
.
19
:
216
221
.
Miller,
F.
and
Ware
G.
2002
.
Suitability and feeding preference of selected North American, European, and Asian elm (Ulmus spp.) Chrysomelidae)
.
Journal of Arboriculture Vol
.
29
(2)
:
98
103
.
Miller,
F.
and
Ware
G.
2014
.
Seasonal activity, within-tree distribution, and ovipositional and feeding preference of the elm leafminer, Fenusa ulmi (Hymenoptera: Tenthredinidae)
.
Journal of Environmental Horticulture
.
32
(1)
:
29
48
.
Miller,
F.
and
Wiegrefe
S.
2021
.
Relative susceptibility preference, and suitability of Carpinus taxa for the Japanese beetle (Coleoptera: Scarabaeidae)
.
Journal of Environmental Horticulture
39
(1)
:
11
21
.
Orians,
C.M.
2000
.
The effects of hybridization in plants on secondary chemistry: implications for the ecology and evolution of plant-herbivore interactions
.
American J. Botany
87
:
1749
1756
.
Paige,
K.N.
and
Capman
W.C.
1993
.
The effects of host-plant genotype, hybridization, and environment on gall-aphid attack and survival in cottonwood: the importance of genetic studies and their utility in RFLPS
.
Evolution
47
(1)
:
36
45
.
Paluch,
G.,
Miller
F.,
Zhu
J.,
and
Coats
J.
2006
.
Influence of elm foliar chemistry for the host suitability of the Japanese beetle, Popillia japonica, and the gypsy moth Lymantria dispar
.
Journal of Agriculture and Urban Entomology
23
(4)
:
209
223
.
Patton,
C.A.,
Ranney
T.G.,
Burton
J.D.,
and
Walgenbach
J.F.
1997
.
Feeding response of Japanese beetle to naturally occurring metabolites found in rosaceous plants
.
Journal of Environmental Horticulture
.
15
:
222
227
.
Peter,
A.J.,
Shanower
T.G.,
and
Romeis
J.
1995
.
The role of plant trichomes in insect resistance: A selective review
.
Phytophaga
7
:
41
63
.
Pillemer,
E.A.
and
Tingey
W.M.
1976
.
Hooked trichomes: a physical barrier biotypes to elm leaf beetle. Journal of Environmental Horticulture
.
Vol
.
20
(3)
:
148
154
.
Potter,
D.A.
and
Held
D.W.
1999
.
Absence of food-aversion learning by a polyphagous scarab, Popillia japonica, following intoxication by geranium, Pelargonium hortorum
.
Entomological Experiment and Application
91
:
83
88
.
Potter,
D.A.,
and
Held
D.
2002
.
Biology and management of the Japanese beetle
.
Annual Review of Entomology
47
:
175
205
.
Potter,
D.A.
and
Kimmerer
T.W.
1988
.
Inhibition of herbivory on young holly leaves: evidence for the defensive role of saponins
.
Oecologia
78
:
322
329
.
Potter,
D.A.
and
Redmond
C.T.
2013
.
Relative resistance or susceptibility of landscape-suitable elms (Ulmus spp.) to multiple insect pests
.
Arboriculture and Urban Forestry
39
(5)
:
23
243
.
Potter,
D.A.,
Spicer
P.G.,
Held
D.,
and
McNiel
R.E.
1998
.
Relative susceptibility of cultivars of flowering crabapples, lindens, and roses to defoliation by Japanese beetles
.
Journal of Environmental Horticulture
.
16
:
105
110
.
Ramalho,
F.S.,
Parrott
W.L.,
Jenkins
J.N.,
and
McCarty,
J.D.
Jr.
1984
.
Effects of cotton leaf trichomes on the mobility of newly hatched tobacco budworms (Lepidoptera: Noctuidae)
.
Journal of Economic Entomology
77
:
619
621
.
Ranney,
T.G.
and
Walgenbach
J. F.
1992
.
Feeding preference of Japanese beetles for taxa of birch, cherry and crabapple
.
Journal of Environmental Horticulture
10
:
77
80
.
Raupp,
M.J.
1985
.
Effects of leaf toughness on mandibular wear of the leaf beetle, Plagiodera versicolora
.
Ecological Entomology
10
(1)
:
73
80
.
Raupp,
M. J.,
Koehler
C. S.,
and
Davidson
J. A.
1992
.
Advances in implementing integrated pest management for woody landscape plants
.
Annual Review of Entomology
37
:
561
586
.
Rauscher,
K.J.,
Lester
T.,
and
Smalley
E.B.
1974
.
Response of elm species and clones to inoculation with Verticillium albo-atrum
.
Phytopathology
64
:
702
705
.
Rautio,
P.,
Markkola
A.,
Martgel
M.,
Tuomi
J.,
Harma
E.,
Kuikka
K.,
Siitonen
A.,
Riesco
IL,
Roitto
M.
2002
.
Developmental plasticity in birch leaves: defoliation causes a shift from glandular to non-glandular trichomes
.
Oikos
98
:
437
446
.
Roberts,
J.J.,
Gallun
R.L.,
Patterson
F.L.,
and
Foster
J.E.
1979
.
Effects of wheat leaf pubescence on the Hessian fly
.
Journal of Economic Entomology
72
:
211
214
.
Robinson,
S.H.,
Wolfenbarger
D.A.,
and
Dilday
R.H.
1980
.
Antixenosis of smooth leaf cotton to the ovipositional response of tobacco budworm
.
Crop Science
20
:
646
649
.
Rowe,
W.J.
and
Potter
D.A.
2000
.
Shading effects on susceptibility of Rosa spp. to defoliation by Popillia japonica (Coleoptera: Scarabaeidae)
.
Environmental Entomology
.
29
(3)
:
502
508
.
Ryan,
J.D.,
Gregory
P.,
and
Tingey
W.M.
1982
.
Phenolic oxidase activities in glandular trichomes of Solanum berthaultii
.
Phytochemistry
21
:
1885
1887
.
Santamour,
F.S.
Jr.
1993
.
Cytological and biochemical aspects of elm improvement. p 69-74
.
In
Sticken
M. B.
and
Sherald
J. L.
[eds.],
Dutch elm disease research: Cellular and molecular approaches, Springer Verlag, New York, New York, USA.
Santamour,
F.S.
and
Bentz
S.E.
1985
.
Updated checklist of elm (Ulmus) cultivars for use in North America
.
Journal of Arboriculture
21
(3)
:
122
131
.
Schalk,
J.M.
and
Stoner
A.K.
1976
.
A bioassay differentiates resistance to the Colorado potato beetle on tomatoes
.
Journal of American Society for Horticultural Science
101
:
74
76
.
Shade,
R.E.,
Doskocil
M.J.,
and
Maxon
N.P.
1979
.
Potato leafhopper resistance in glandular-haired alfalfa species
.
Crop Sci
.
19
:
287
289
.
Sherald,
J.L.,
Santamour,
F.S.
Jr.,
Hajela
R.K.,
Hajela
N.,
and
Sticklen
M.B.
1994
.
A Dutch elm disease resistant triploid elm
.
Canadian Journal of Forest Research
24
:
647
653
.
Sinclair,
W.A.
and
Lyon
H.H.
2005
.
Diseases of Trees and Shrubs, second edition
.
Cornell University Press
,
Ithaca, New York, United States
.
396
p.
Sinclair,
W.A.,
Townsend
A.M.,
Griffiths
H.M.,
and
Whitlow
T.H.
2000
.
Responses of six Eurasian Ulmus cultivars to a North American elm yellows phytoplasma
.
Plant Disease
84
:
1266
1270
.
Smalley,
E.B.
and
Guries
R.P.
1993
.
Breeding elms for resistance to Dutch elm disease
.
Annual Review of Phytopathology
31
:
325
352
.
Spicer,
P.G.,
Potter
D.A.,
and
McNiel
R.G.
1995
.
Resistance of crabapple (Malus spp.) cultivars to defoliation by the Japanese beetle (Coleoptera: Scarabaeidae)
.
Journal of Economic Entomology
88
:
979
985
.
Southwood,
T.R.E.
1986
.
Plant surfaces and insects – an overview
.
Pp.
1
22
.
In:
Southwood
T.R.E.
and
Juniper
B.
(eds.).
Insects and the plant surface
.
Edward Arnold
,
London, UK
.
Stamp,
N.E.
and
Harmon
G.D.
1991
.
Effect of potassium and sodium on fecundity and survivorship of Japanese beetles
.
Oikos
62
:
299
305
.
St-Laurent,
I.,
Baum
B.R.,
Akpagnana
K.,
and
Arnason
J.T.
2000
.
Leaf trichome
.
Canadian Journal of Botany
78
:
34
39
.
Tingey,
W.M.
and
Laubengayer
J.E.
1986
.
Glandular trichomes of a resistant hybrid potato alter feeding behavior of the potato leafhopper (Homoptera: Cicadellidae)
.
Journal of Economic Entomology
79
:
1230
1234
.
Townsend,
A.M.
1979
.
Influence of specific combining ability and sex of gametes on transmission of Ceratocystis ulmi resistance in Ulmus
.
Phytopathology
69
:
643
645
.
Townsend,
A.M.
2000
.
USDA genetic research on elms
.
p.
271
278
In:
The elms: Breeding, Conservation, and Disease Management
.
Dunn
C.P.
(Ed.).
Kluwer Academic Publishers
,
Norwell, Massachusetts, U.S
.
Townsend,
A.M.
and
Douglass
L.W.
2001
.
Variation among American elm clones in long-term dieback, growth, and survival following Ophiostoma inoculation
.
Journal of Environmental Horticulture
19
(2)
:
100
103
.
Townsend,
A.M.
and
Schreiber
L.R.
1975
.
Recent progress in the breeding and selection of elms
.
Proceedings of the Central States Tree Improvement Conference
9
:
1
6
.
Townsend,
A.M.,
Bentz
S.E,
and
Douglass
L.W.
2005
.
Evaluation of 19 American elm clones for tolerance to Dutch elm disease
.
Journal of Environmental Horticulture
23
(1)
:
21
24
.
Townsend,
A.M.,
Hall
R.W.,
and
Masters
W.O.
1995
.
‘Patriot' elm
.
Journal of Environmental Horticulture
,
113
(2)
:
113
115
.
Townsend,
A.M.,
Bentz
S.E.,
and
Johnson
G.R.
1995
.
Variation in response of selected American elm clones to Ophiostoma ulmi
.
Journal of Environmental Horticulture
13
(3)
:
126
128
.
Valkama,
E.,
Salminen
J.P.,
Koricheva
J.,
and
Pihlaja
K.
2003
.
Comparative analysis of trichome structure and composition of epicuticular flavonoids in Finnish birch species
.
Annals of Botany
91
:
643
655
.
Ventrella,
M.C.
and
Marinho
C.R.
2008
.
Morphology and histochemistry of glandular trichomes of Cordia verbenacea DC. (Boraginaceae) leaves
.
Revista Brasilian Botany
31
(3)
:
457
467
.
War,
A.R.,
Paulrgaj
M.G.,
Ahmad
T.,
Buhroo
A.A.,
Hussain
B.,
Ignacimuthu
S.,
and
Sharma
H.C.
2012
.
Mechanisms of plant defense against insect herbivores. Plant Signaling and Behavior 7:10:1306-1320.
Ware,
G.
1992
.
Elm breeding and improvement at The Morton Arboretum. The Morton Arboretum Quarterly
.
Vol
.
28
:
846
849
.
Ware,
G.
1995
.
Little-known elms from China: Landscape tree possibilities
.
Journal of Arboriculture
21
:
284
288
.
Warren,
K.
2000
.
The return of the elm: The status of elms in the nursery industry in 2000. J.
Schmidt
Frank
and
Co
Son.
Boring, Oregon.
9
p.
Webb,
R.E.,
Stoner
A.K.,
and
Gentile
A.G.
1971
.
Resistance to leafminers in Lycopersicon accessions
.
Journal of the American Society for Horticultural Science
96
:
65
67
.
Wellso,
S.G.
1979
.
Cereal leaf beetle: Interaction with and ovipositional adaptation to a resistant wheat
.
Environmental Entomology
8
:
454
457
.
Werker,
E.
2000
.
Trichome density and development
.
Advanced Botanical Research
31
:
1
35
.
Whittemore,
A.T.
and
Olsen
R.
2011
.
Ulmus americana (Ulmaceae) is a polyploid complex
.
American Journal of Botany
98
:
754
760
.
Whittemore,
A.T.
and
Xia
Z.
2017
.
Genome size variation in elms (Ulmus spp.) and related genera
.
HortScience
52
(4)
:
547
553
.
Yencho,
G.C.
and
Tingey
W.M.
1994
.
Glandular trichomes of Solanum berthaultii alter host preference of the Colorado potato beetle, Leptinotarsa decemlineata
.
Entomologia Experimentalis et Applicata
70
:
217
225
.

Author notes

1

Acknowledgements. The authors wish to extend their sincere appreciation to The Morton Arboretum entomology lab staff for their hard work in assisting with the laboratory feeding studies and field work. Thanks to D. Danielson, The Morton Arboretum, and T. Tiddens, The Chicago Botanic Garden for their assistance in field collection of beetles. A special note of thanks is extended to the J. Frank Schmidt Family Charitable Foundation for providing partial on-going financial support for this project. The authors wish to extend their special thanks to R. Hauer, and D. Potter, for their very helpful reviews of earlier drafts of this manuscript. Thank you to H. Anderson and L. Prazak for their assistance in manuscript formatting and editing.

3

Deceased.