TY - JOUR
AU - C, Quick, James
AB - Abstract Lagerstroemia is a genus of plants comprised of deciduous shrubs or small trees native to China southward into Southeast Asia. There is a wide range among cultivars of tolerance to key pests and diseases, such as powdery mildew, Erysiphe australiana (McAlpine), flea beetle, Altica spp., crape myrtle aphid, Tinocallis kahawaluokalani Kirkaldy (Hemiptera: Aphididae), and Japanese beetle, Popillia japonica Newman (Coleoptera: Scarabaeidae). We found variation in bee visitation to 40 cultivars evaluated in a 2-yr study in north Georgia. The cultivars ‘Seminole’ and ‘Victor’ were the two most often visited by all bees, including honey bees, carpenter bees, and several small bee species. ‘Apalachee’, however, was the cultivar most frequently visited by bumblebees. Plant height and flower color also influenced frequency of bee visitation. Dark pink, dark purple, and white were the flower colors most frequently visited among the nine color categories evaluated. Pollinator visitation should be a consideration in cultivar choice along with pest susceptibility and horticultural attributes. pollinator, crape myrtle, Apidae, Halictidae, Megachillidae Crape myrtle, Lagerstroemia, is a genus that includes numerous popular landscape shrubs and small trees that vary in horticultural attributes and pest management requirements (Chappell et al. 2012). These popular ornamentals are native to China, Japan, and Korea southward to Oceania and many have been cultivated in the United States for more than 175 years (Quxiang 1991, Chappell et al 2012). Host plant resistance attributes have been reported for key insect pests including crape myrtle aphid, Tinocallis kahawaluokalani Kirkaldy (Alverson and Allen 1992, Mizell and Knox 1993, Herbert et al. 2009); the Japanese beetle, Popillia japonica Newman and flea beetles, mainly Altica spp (Pettis et al. 2004, Braman et al. 2012). Disease susceptibility to powdery mildew, caused by Erysiphe australiana (McAlpine) U. Braun & S. Takamatsu, and Cercospora leaf spot, caused by Pseudocercospora lythracearum (Heald & Wolf) Liu & Guo have also been assessed (Hagan et al. 1998, 2002; Holcomb 2002, 2005; Holcomb and Owings 2002; Holcomb et al. 2003, 2005, 2006, 2007; Knox 2003). Hybrids between L. indica × L. fauriei comprise many new introductions with >130 commercially available cultivars (Chappell et al. 2012). Evaluation of products that control key pests with minimal negative effects on natural enemies and pollinators was identified as a priority in the pest management strategic plan for container and field-produced nursery crops in the southeast, revised in 2015 (Braman et al. 2015). Although prone to these few key pest problems, for which systemic insecticides are sometimes applied, this non-native plant supports predaceous insects and is attractive to pollinators. Riddle and Mizell (2016) determined that crape myrtle provides pollen for native bee species and honey bees, and that bees varied in their cultivar preference among 14 cultivars in Florida, USA. Their data suggested that use of crape myrtle cultivars blooming at different times could provide additional support for pollinators. They further emphasized the need for additional research to fully understand the ecological roles and value of Lagerstroemia species. We sought to both extend the range of this information and to further identify predictors of pollinator preference by examining bee visitation to 40 crape myrtle cultivars in north Georgia in a 2-yr study. Materials and Methods Study Area and Experimental Design Four, one-gallon replicates of forty crape myrtle cultivars representing a range of flower color and plant heights were planted in a randomized complete block design on 4.6 m centers at the University of Georgia Mountain Research and Education Center in Blairsville in May 2004. Plants were mulched with pine bark mulch and irrigated as necessary to establishment, then maintained with pine bark mulch and mowed, tall fescue, Festuca arundinacea Schreb., between rows. Previously, Pettis et al. (2004) and Braman et al. (2012) reported the range in P. japonica and Altica spp. response to these cultivars. Here, the same plants were observed for pollinator visitation on 23 dates during July and August 2015–2016. Crape myrtles bloom later in the season. Start dates for observations were based on preliminary sampling to capture the beginning bloom and pollinator activity in the north Georgia location and continued until bloom senesced and little to no pollinator activity was apparent. Visual observations between 1000 and 1400 h were supplemented with capture samples to evaluate effect of cultivar, plant height and flower color on bee visitation. Three branches per plant with blooms were randomly selected and were observed on each date for 2 min per observation. Blooms were not standardized but were not widely disparate in size. Visual observations of bees did not allow fine taxonomic differentiation. Categories were honey bees, bumble bees, carpenter bees, and all other bees combined into a small bee category. A bee visit was considered an event when the bee landed on a flower. Additional blooms were also sampled by quickly covering them with 3.8-liter plastic bags and occupants dislodged into the bags, sealed and returned to the laboratory for additional microscopic identification to determine what particular species were present (Mitchell 1960, Michener et al. 1994, Droege et al. 2008, Gibbs 2011, Williams et al. 2014). Vouchers have been placed in the University of Georgia insect collection. Sample dates were July 16, 17, 26, 27, 29, 30, 31, August 1, 5, 6, 9, 10, 12, 13, and 17, 18 in 2015 and July 1, 7, 16, 29, August 5, 11, and 20 in 2016. Plants were assigned to one of four height categories: small shrub (4 cultivars)—mature shrub under 6 ft, medium shrub (8 cultivars)—mature shrub 6–12 ft, large shrub (13 cultivars)—mature shrub 12–20 ft and small tree (15 cultivars)—mature tree over 20 ft. Nine flower color categories were recognized for analysis: white, lavender, pink, red, purple, magenta, dark purple, dark pink, and bicolor pink and white. Statistical comparisons were conducted using the general linear mixed model (GLIMMIX) procedure in SAS/STAT Software version 14.1 (SAS Institute Inc. 2017, Cary, NC). Cultivar or plant height or flower color and replication were modeled by year of collection with replication designated as the random variable. All response variables were modeled with a negative binomial distribution. When differences among treatments were detected (α = 0.05), treatment means were separated following the LSMEANS procedure. When using the negative binomial distribution, reported means were back-transformed using the ILINK function; nontransformed means and standard errors are presented in the text, table and figures. For multivariate analysis, non-metric multidimensional scaling (NMDS) in the Vegan package for R (Dixon 2003, Oksanen 2015) was used with a Bray–Curtis rank similarity matrix. Principal component analysis identified significant environmental factors. Environmental vectors were then fit on the ordination using the envfit function from the Vegan package with permutation testing using 999 iterations. These analyses permitted significance testing and graphics to describe differences in bee visitation behavior affected by flower color and plant height on the NMDS ordinations. Results Number of total bees observed varied by cultivar, plant height, and bloom color (Table 1). All 40 cultivars were visited by some bees (Table 2). Bees observed included Apidae: honey bees, Apis mellifera L., bumble bees, Bombus impatiens Cresson, Eastern Carpenter bees Xylocopa virginica (L.), the hibiscus bee, Ptilothrix bombiformis L. and Tepanec long-horned bee, Melissodes tepaneca (Cresson); Halictidae: sweat bees Lasioglossum imitatum (Smith), Lasioglossum illinoensis (Robertson), Augochlorella aurata Smith and Augochlora pura pura Say; Megachilidae: leaf cutter and resin bees, Megachile frigida Smith, Megachile rotunda (Fab.), and Megachile sculpturalis Smith. Table 1. Analysis of variance results for various effects on number of bees observed per crape myrtle branch/bloom among 40 cultivars on 23 dates during 2015 and 2016 Effect (df) Total Bees Honey Bees Bumble Bees Carpenter Bees Small Bees F P F P F P F P F P Cultivar (39) 35.79 0.0001 46.7 0.0001 31.2 0.0001 5.4 0.0001 13.9 0.0001 Color (8) 40.8 0.0001 45.0 0.0001 57.8 0.0001 7.2 0.0001 19.8 0.0001 Height (3) 237.8 0.0001 197.4 0.0001 161.3 0.0001 17.1 0.0001 97.7 0.0001 Effect (df) Total Bees Honey Bees Bumble Bees Carpenter Bees Small Bees F P F P F P F P F P Cultivar (39) 35.79 0.0001 46.7 0.0001 31.2 0.0001 5.4 0.0001 13.9 0.0001 Color (8) 40.8 0.0001 45.0 0.0001 57.8 0.0001 7.2 0.0001 19.8 0.0001 Height (3) 237.8 0.0001 197.4 0.0001 161.3 0.0001 17.1 0.0001 97.7 0.0001 View Large Table 1. Analysis of variance results for various effects on number of bees observed per crape myrtle branch/bloom among 40 cultivars on 23 dates during 2015 and 2016 Effect (df) Total Bees Honey Bees Bumble Bees Carpenter Bees Small Bees F P F P F P F P F P Cultivar (39) 35.79 0.0001 46.7 0.0001 31.2 0.0001 5.4 0.0001 13.9 0.0001 Color (8) 40.8 0.0001 45.0 0.0001 57.8 0.0001 7.2 0.0001 19.8 0.0001 Height (3) 237.8 0.0001 197.4 0.0001 161.3 0.0001 17.1 0.0001 97.7 0.0001 Effect (df) Total Bees Honey Bees Bumble Bees Carpenter Bees Small Bees F P F P F P F P F P Cultivar (39) 35.79 0.0001 46.7 0.0001 31.2 0.0001 5.4 0.0001 13.9 0.0001 Color (8) 40.8 0.0001 45.0 0.0001 57.8 0.0001 7.2 0.0001 19.8 0.0001 Height (3) 237.8 0.0001 197.4 0.0001 161.3 0.0001 17.1 0.0001 97.7 0.0001 View Large Table 2. Mean (±SE) bees observed per crape myrtle branch among 40 cultivars on 23 dates during 2015 and 2016 with 10,764 individual observations and a total of 21,411 bees observed Cultivar Total Bees Honey Bees Bumble Bees Carpenter Bees Small Bees Seminole 4.27 (0.21)a 1.85 (0.12)b 0.51 (0.05)ef 0.27 (0.04)a 1.64 (0.07)a Victor 4.23 (0.22)a 2.55 (0.16)a 0.19 (0.03)j-o 0.04 (0.01)d-h 1.45 (0.08)ab Apalachee 3.30 (0.17)b 0.81 (0.07)e-g 1.26 (0.08)a 0.13 (0.02)b-e 1.10 (0.06)e-h Hope 3.30 (0.16)b 1.42 (0.10)c 0.28 (0.03)h-m 0.16 (0.03)bc 1.44 (0.07)a-c Hopi 3.29 (0.15)b 1.09 (0.07)de 0.74 (0.06)b-d 0.13 (0.03)b-e 1.34 (0.06)b-e Pink Velour 3.27 (0.15)b 1.37 (0.09)cd 0.29 (0.03)g-m 0.11 (0.02)b-f 1.50 (0.07)ab Miami 3.07 (0.14)bc 1.44 (0.09)c 0.23 (0.03)j-n 0.02 (0.01)f-h 1.38 (0.07)a-d Pecos 2.99 (0.18)b-d 1.07 (0.08)de 0.77 (0.06)bc 0.11 (0.03)b-f 1.04 (0.07)f-h Yuma 2.88 (0.14)b-e 0.46 (0.04)h-n 0.84 (0.06)b 0.13 (0.03)b-d 1.45 (0.07)ab Tuscarora 2.72 (0.14)c-f 0.98 (0.07) ef 0.44 (0.05)e-i 0.13 (0.03)b-d 1.16 (0.06)d-g Acoma 2.52 (0.15)def 0.64 (0.07)g-j 0.86 (0.07)b 0.06 (0.02)c-h 0.96 (0.06)f-i Sioux 2.43 (0.12)e-g 0.97 (0.06) ef 0.39 (0.04)e-j 0.02 (0.01)e-h 1.04 (0.06)f-h Catawba 2.38 (0.11)e-h 0.63 (0.05)g-j 0.59 (0.05)c-e 0.10 (0.02)b-g 1.05 (0.06)f-h Zuni 2.33 (0.12)f-i 0.58 (0.04)g-k 0.56 (0.04)de 0.13 (0.02)b-e 1.06 (0.06)f-h Ozark Spring 2.21 (0.13)f-j 0.49 (0.05)h-n 0.48 (0.05)e-h 0.18 (0.03)ab 1.05 (0.06)f-h Natchez 1.97 (0.17)g-k 0.42 (0.05)h-n 0.58 (0.07)c-e 0.11 (0.02)b-f 0.87 (0.07)h-k Lipan 1.88 (0.11)h-k 0.41 (0.04)h-n 0.57 (0.05)c-e 0.04 (0.01)d-h 0.85 (.05)h-m Dynamite 1.86 (0.10)h-k 0.63 (0.06)g-j 0.04 (0.01)no 0 (0)h 1.18 (0.06)c-f Byer’s Red 1.83 (0.11)h-k 0.52 (.05)g-m 0.20 (0.03)j-o 0.10 (0.02)b-g 1.00 (0.06)f-h Powhatan 1.79 (0.11)i-k 0.33 (0.04)j-o 0.49 (0.04)e-h 0.10 (0.02)b-g 0.86 (0.06) h-l Regal Red 1.71 (0.11)j-m 0.57 (0.05)g-l 0.14 (0.03)j-o 0.07 (0.02)c-g 0.93 (0.06)f-j Velma’s R.D. 1.69 (0.10)j-m 0.37 (0.04)i-o 0.31 (0.04)g-k 0.13 (0.03)b-d 0.88 (0.06)h-k Osage 1.66 (0.12)j-m 0.52 (.06)g-m 0.52 (0.05)e 0.02 (0.01)e-h 0.59 (0.05)m-p Byer’s White 1.66 (0.09)j-m 0.54 (.05)g-m 0.14 (0.02)k-o 0.02 (0.01)e-h 0.96 (0.05)f-i Centennial 1.59 (0.11)k-o 0.31 (0.07)k-o 0.31 (0.04)f-k 0.07 (0.02)c-g 0.91 (0.06)g-j Wm. Toovey 1.59 (0.14)k-o 0.55 (0.06)g-l 0.24 (0.04)j-n 0.09 (0.02)b-h 0.70 (0.06)i-n Wichita 1.58 (0.12)k-o 0.60 (0.06)g-l 0.23 (0.04)j-n 0.06 (0.02)c-g 0.69 (0.05)i-n Choctaw 1.58 (0.11)k-o 0.71 (0.06)f-h 0.14 (0.02)k-o 0.10 (0.03)b-g 0.63 (0.05)k-o Pokomoke 1.51 (0.11)k-p 0.64 (0.06)g-j 0.15 (0.03)k-o 0.03 (0.01)d-h 0.69 (0.05)j-n Commanche 1.49 (0.11)k-p 0.66 (0.06)f-h 0.09 (0.02)l-o 0.04 (0.01)d-h 0.70 (0.05)i-n Tonto 1.29 (0.09)m-s 0.46 (0.04)g-m 0.20 (0.03)j-n 0.03 (0.01)d-h 0.60 (0.05)l-p Cent. Spirit 1.25 (0.08)n-t 0.23 (0.03)m-o 0.10 (0.02)l-o 0.04 (0.01)d-h 0.87 (0.06)h-k Tuskeegee 1.16 (0.10)n-t 0.38 (0.04)k-o 0.18 (0.03)k-o 0.03 (0.01)e-h 0.57 (0.05)n-q Potomac 1.08 (0.10)o-t 0.38 (0.05)k-o 0.09 (0.02)l-o 0.01 (0.01)gh 0.60 (0.05)l-p Muskogee 1.06 (0.09)o-t 0.23 (0.03)m-o 0.29 (0.04)g-l 0.02 (0.01)f-h 0.52 (0.05)m-p Ca. Beauty 1.02 (0.09)q-t 0.28 (0.04)l-o 0.01 (0.01)o 0.02 (0.01)f-h 0.72 (0.06)i-n Hardy Lav. 0.97 (0.10)q-t 0.27 (0.04)l-o 0.14 (0.02)k-o 0.06 (0.01)c-g 0.51 (0.05)n-q Biloxi 0.80 (0.09)s-u 0.17 (0.03)no 0.25 (0.03)i-m 0.04 (0.01)d-h 0.34 (0.04)pq Red Rocket 0.68 (0.09)tu 0.27 (0.04)l-o 0.01 (0.01)o 0.01 (0.01)gh 0.39 (0.05)o-q Rasp. Sundae 0.42 (0.05)u 0.07 (0.02)o 0.01 (0.01)o 0.01 (0.01)gh 0.32 (0.04)q Cultivar Total Bees Honey Bees Bumble Bees Carpenter Bees Small Bees Seminole 4.27 (0.21)a 1.85 (0.12)b 0.51 (0.05)ef 0.27 (0.04)a 1.64 (0.07)a Victor 4.23 (0.22)a 2.55 (0.16)a 0.19 (0.03)j-o 0.04 (0.01)d-h 1.45 (0.08)ab Apalachee 3.30 (0.17)b 0.81 (0.07)e-g 1.26 (0.08)a 0.13 (0.02)b-e 1.10 (0.06)e-h Hope 3.30 (0.16)b 1.42 (0.10)c 0.28 (0.03)h-m 0.16 (0.03)bc 1.44 (0.07)a-c Hopi 3.29 (0.15)b 1.09 (0.07)de 0.74 (0.06)b-d 0.13 (0.03)b-e 1.34 (0.06)b-e Pink Velour 3.27 (0.15)b 1.37 (0.09)cd 0.29 (0.03)g-m 0.11 (0.02)b-f 1.50 (0.07)ab Miami 3.07 (0.14)bc 1.44 (0.09)c 0.23 (0.03)j-n 0.02 (0.01)f-h 1.38 (0.07)a-d Pecos 2.99 (0.18)b-d 1.07 (0.08)de 0.77 (0.06)bc 0.11 (0.03)b-f 1.04 (0.07)f-h Yuma 2.88 (0.14)b-e 0.46 (0.04)h-n 0.84 (0.06)b 0.13 (0.03)b-d 1.45 (0.07)ab Tuscarora 2.72 (0.14)c-f 0.98 (0.07) ef 0.44 (0.05)e-i 0.13 (0.03)b-d 1.16 (0.06)d-g Acoma 2.52 (0.15)def 0.64 (0.07)g-j 0.86 (0.07)b 0.06 (0.02)c-h 0.96 (0.06)f-i Sioux 2.43 (0.12)e-g 0.97 (0.06) ef 0.39 (0.04)e-j 0.02 (0.01)e-h 1.04 (0.06)f-h Catawba 2.38 (0.11)e-h 0.63 (0.05)g-j 0.59 (0.05)c-e 0.10 (0.02)b-g 1.05 (0.06)f-h Zuni 2.33 (0.12)f-i 0.58 (0.04)g-k 0.56 (0.04)de 0.13 (0.02)b-e 1.06 (0.06)f-h Ozark Spring 2.21 (0.13)f-j 0.49 (0.05)h-n 0.48 (0.05)e-h 0.18 (0.03)ab 1.05 (0.06)f-h Natchez 1.97 (0.17)g-k 0.42 (0.05)h-n 0.58 (0.07)c-e 0.11 (0.02)b-f 0.87 (0.07)h-k Lipan 1.88 (0.11)h-k 0.41 (0.04)h-n 0.57 (0.05)c-e 0.04 (0.01)d-h 0.85 (.05)h-m Dynamite 1.86 (0.10)h-k 0.63 (0.06)g-j 0.04 (0.01)no 0 (0)h 1.18 (0.06)c-f Byer’s Red 1.83 (0.11)h-k 0.52 (.05)g-m 0.20 (0.03)j-o 0.10 (0.02)b-g 1.00 (0.06)f-h Powhatan 1.79 (0.11)i-k 0.33 (0.04)j-o 0.49 (0.04)e-h 0.10 (0.02)b-g 0.86 (0.06) h-l Regal Red 1.71 (0.11)j-m 0.57 (0.05)g-l 0.14 (0.03)j-o 0.07 (0.02)c-g 0.93 (0.06)f-j Velma’s R.D. 1.69 (0.10)j-m 0.37 (0.04)i-o 0.31 (0.04)g-k 0.13 (0.03)b-d 0.88 (0.06)h-k Osage 1.66 (0.12)j-m 0.52 (.06)g-m 0.52 (0.05)e 0.02 (0.01)e-h 0.59 (0.05)m-p Byer’s White 1.66 (0.09)j-m 0.54 (.05)g-m 0.14 (0.02)k-o 0.02 (0.01)e-h 0.96 (0.05)f-i Centennial 1.59 (0.11)k-o 0.31 (0.07)k-o 0.31 (0.04)f-k 0.07 (0.02)c-g 0.91 (0.06)g-j Wm. Toovey 1.59 (0.14)k-o 0.55 (0.06)g-l 0.24 (0.04)j-n 0.09 (0.02)b-h 0.70 (0.06)i-n Wichita 1.58 (0.12)k-o 0.60 (0.06)g-l 0.23 (0.04)j-n 0.06 (0.02)c-g 0.69 (0.05)i-n Choctaw 1.58 (0.11)k-o 0.71 (0.06)f-h 0.14 (0.02)k-o 0.10 (0.03)b-g 0.63 (0.05)k-o Pokomoke 1.51 (0.11)k-p 0.64 (0.06)g-j 0.15 (0.03)k-o 0.03 (0.01)d-h 0.69 (0.05)j-n Commanche 1.49 (0.11)k-p 0.66 (0.06)f-h 0.09 (0.02)l-o 0.04 (0.01)d-h 0.70 (0.05)i-n Tonto 1.29 (0.09)m-s 0.46 (0.04)g-m 0.20 (0.03)j-n 0.03 (0.01)d-h 0.60 (0.05)l-p Cent. Spirit 1.25 (0.08)n-t 0.23 (0.03)m-o 0.10 (0.02)l-o 0.04 (0.01)d-h 0.87 (0.06)h-k Tuskeegee 1.16 (0.10)n-t 0.38 (0.04)k-o 0.18 (0.03)k-o 0.03 (0.01)e-h 0.57 (0.05)n-q Potomac 1.08 (0.10)o-t 0.38 (0.05)k-o 0.09 (0.02)l-o 0.01 (0.01)gh 0.60 (0.05)l-p Muskogee 1.06 (0.09)o-t 0.23 (0.03)m-o 0.29 (0.04)g-l 0.02 (0.01)f-h 0.52 (0.05)m-p Ca. Beauty 1.02 (0.09)q-t 0.28 (0.04)l-o 0.01 (0.01)o 0.02 (0.01)f-h 0.72 (0.06)i-n Hardy Lav. 0.97 (0.10)q-t 0.27 (0.04)l-o 0.14 (0.02)k-o 0.06 (0.01)c-g 0.51 (0.05)n-q Biloxi 0.80 (0.09)s-u 0.17 (0.03)no 0.25 (0.03)i-m 0.04 (0.01)d-h 0.34 (0.04)pq Red Rocket 0.68 (0.09)tu 0.27 (0.04)l-o 0.01 (0.01)o 0.01 (0.01)gh 0.39 (0.05)o-q Rasp. Sundae 0.42 (0.05)u 0.07 (0.02)o 0.01 (0.01)o 0.01 (0.01)gh 0.32 (0.04)q Means within a column followed by different letters are significantly different (P < 0.05). View Large Table 2. Mean (±SE) bees observed per crape myrtle branch among 40 cultivars on 23 dates during 2015 and 2016 with 10,764 individual observations and a total of 21,411 bees observed Cultivar Total Bees Honey Bees Bumble Bees Carpenter Bees Small Bees Seminole 4.27 (0.21)a 1.85 (0.12)b 0.51 (0.05)ef 0.27 (0.04)a 1.64 (0.07)a Victor 4.23 (0.22)a 2.55 (0.16)a 0.19 (0.03)j-o 0.04 (0.01)d-h 1.45 (0.08)ab Apalachee 3.30 (0.17)b 0.81 (0.07)e-g 1.26 (0.08)a 0.13 (0.02)b-e 1.10 (0.06)e-h Hope 3.30 (0.16)b 1.42 (0.10)c 0.28 (0.03)h-m 0.16 (0.03)bc 1.44 (0.07)a-c Hopi 3.29 (0.15)b 1.09 (0.07)de 0.74 (0.06)b-d 0.13 (0.03)b-e 1.34 (0.06)b-e Pink Velour 3.27 (0.15)b 1.37 (0.09)cd 0.29 (0.03)g-m 0.11 (0.02)b-f 1.50 (0.07)ab Miami 3.07 (0.14)bc 1.44 (0.09)c 0.23 (0.03)j-n 0.02 (0.01)f-h 1.38 (0.07)a-d Pecos 2.99 (0.18)b-d 1.07 (0.08)de 0.77 (0.06)bc 0.11 (0.03)b-f 1.04 (0.07)f-h Yuma 2.88 (0.14)b-e 0.46 (0.04)h-n 0.84 (0.06)b 0.13 (0.03)b-d 1.45 (0.07)ab Tuscarora 2.72 (0.14)c-f 0.98 (0.07) ef 0.44 (0.05)e-i 0.13 (0.03)b-d 1.16 (0.06)d-g Acoma 2.52 (0.15)def 0.64 (0.07)g-j 0.86 (0.07)b 0.06 (0.02)c-h 0.96 (0.06)f-i Sioux 2.43 (0.12)e-g 0.97 (0.06) ef 0.39 (0.04)e-j 0.02 (0.01)e-h 1.04 (0.06)f-h Catawba 2.38 (0.11)e-h 0.63 (0.05)g-j 0.59 (0.05)c-e 0.10 (0.02)b-g 1.05 (0.06)f-h Zuni 2.33 (0.12)f-i 0.58 (0.04)g-k 0.56 (0.04)de 0.13 (0.02)b-e 1.06 (0.06)f-h Ozark Spring 2.21 (0.13)f-j 0.49 (0.05)h-n 0.48 (0.05)e-h 0.18 (0.03)ab 1.05 (0.06)f-h Natchez 1.97 (0.17)g-k 0.42 (0.05)h-n 0.58 (0.07)c-e 0.11 (0.02)b-f 0.87 (0.07)h-k Lipan 1.88 (0.11)h-k 0.41 (0.04)h-n 0.57 (0.05)c-e 0.04 (0.01)d-h 0.85 (.05)h-m Dynamite 1.86 (0.10)h-k 0.63 (0.06)g-j 0.04 (0.01)no 0 (0)h 1.18 (0.06)c-f Byer’s Red 1.83 (0.11)h-k 0.52 (.05)g-m 0.20 (0.03)j-o 0.10 (0.02)b-g 1.00 (0.06)f-h Powhatan 1.79 (0.11)i-k 0.33 (0.04)j-o 0.49 (0.04)e-h 0.10 (0.02)b-g 0.86 (0.06) h-l Regal Red 1.71 (0.11)j-m 0.57 (0.05)g-l 0.14 (0.03)j-o 0.07 (0.02)c-g 0.93 (0.06)f-j Velma’s R.D. 1.69 (0.10)j-m 0.37 (0.04)i-o 0.31 (0.04)g-k 0.13 (0.03)b-d 0.88 (0.06)h-k Osage 1.66 (0.12)j-m 0.52 (.06)g-m 0.52 (0.05)e 0.02 (0.01)e-h 0.59 (0.05)m-p Byer’s White 1.66 (0.09)j-m 0.54 (.05)g-m 0.14 (0.02)k-o 0.02 (0.01)e-h 0.96 (0.05)f-i Centennial 1.59 (0.11)k-o 0.31 (0.07)k-o 0.31 (0.04)f-k 0.07 (0.02)c-g 0.91 (0.06)g-j Wm. Toovey 1.59 (0.14)k-o 0.55 (0.06)g-l 0.24 (0.04)j-n 0.09 (0.02)b-h 0.70 (0.06)i-n Wichita 1.58 (0.12)k-o 0.60 (0.06)g-l 0.23 (0.04)j-n 0.06 (0.02)c-g 0.69 (0.05)i-n Choctaw 1.58 (0.11)k-o 0.71 (0.06)f-h 0.14 (0.02)k-o 0.10 (0.03)b-g 0.63 (0.05)k-o Pokomoke 1.51 (0.11)k-p 0.64 (0.06)g-j 0.15 (0.03)k-o 0.03 (0.01)d-h 0.69 (0.05)j-n Commanche 1.49 (0.11)k-p 0.66 (0.06)f-h 0.09 (0.02)l-o 0.04 (0.01)d-h 0.70 (0.05)i-n Tonto 1.29 (0.09)m-s 0.46 (0.04)g-m 0.20 (0.03)j-n 0.03 (0.01)d-h 0.60 (0.05)l-p Cent. Spirit 1.25 (0.08)n-t 0.23 (0.03)m-o 0.10 (0.02)l-o 0.04 (0.01)d-h 0.87 (0.06)h-k Tuskeegee 1.16 (0.10)n-t 0.38 (0.04)k-o 0.18 (0.03)k-o 0.03 (0.01)e-h 0.57 (0.05)n-q Potomac 1.08 (0.10)o-t 0.38 (0.05)k-o 0.09 (0.02)l-o 0.01 (0.01)gh 0.60 (0.05)l-p Muskogee 1.06 (0.09)o-t 0.23 (0.03)m-o 0.29 (0.04)g-l 0.02 (0.01)f-h 0.52 (0.05)m-p Ca. Beauty 1.02 (0.09)q-t 0.28 (0.04)l-o 0.01 (0.01)o 0.02 (0.01)f-h 0.72 (0.06)i-n Hardy Lav. 0.97 (0.10)q-t 0.27 (0.04)l-o 0.14 (0.02)k-o 0.06 (0.01)c-g 0.51 (0.05)n-q Biloxi 0.80 (0.09)s-u 0.17 (0.03)no 0.25 (0.03)i-m 0.04 (0.01)d-h 0.34 (0.04)pq Red Rocket 0.68 (0.09)tu 0.27 (0.04)l-o 0.01 (0.01)o 0.01 (0.01)gh 0.39 (0.05)o-q Rasp. Sundae 0.42 (0.05)u 0.07 (0.02)o 0.01 (0.01)o 0.01 (0.01)gh 0.32 (0.04)q Cultivar Total Bees Honey Bees Bumble Bees Carpenter Bees Small Bees Seminole 4.27 (0.21)a 1.85 (0.12)b 0.51 (0.05)ef 0.27 (0.04)a 1.64 (0.07)a Victor 4.23 (0.22)a 2.55 (0.16)a 0.19 (0.03)j-o 0.04 (0.01)d-h 1.45 (0.08)ab Apalachee 3.30 (0.17)b 0.81 (0.07)e-g 1.26 (0.08)a 0.13 (0.02)b-e 1.10 (0.06)e-h Hope 3.30 (0.16)b 1.42 (0.10)c 0.28 (0.03)h-m 0.16 (0.03)bc 1.44 (0.07)a-c Hopi 3.29 (0.15)b 1.09 (0.07)de 0.74 (0.06)b-d 0.13 (0.03)b-e 1.34 (0.06)b-e Pink Velour 3.27 (0.15)b 1.37 (0.09)cd 0.29 (0.03)g-m 0.11 (0.02)b-f 1.50 (0.07)ab Miami 3.07 (0.14)bc 1.44 (0.09)c 0.23 (0.03)j-n 0.02 (0.01)f-h 1.38 (0.07)a-d Pecos 2.99 (0.18)b-d 1.07 (0.08)de 0.77 (0.06)bc 0.11 (0.03)b-f 1.04 (0.07)f-h Yuma 2.88 (0.14)b-e 0.46 (0.04)h-n 0.84 (0.06)b 0.13 (0.03)b-d 1.45 (0.07)ab Tuscarora 2.72 (0.14)c-f 0.98 (0.07) ef 0.44 (0.05)e-i 0.13 (0.03)b-d 1.16 (0.06)d-g Acoma 2.52 (0.15)def 0.64 (0.07)g-j 0.86 (0.07)b 0.06 (0.02)c-h 0.96 (0.06)f-i Sioux 2.43 (0.12)e-g 0.97 (0.06) ef 0.39 (0.04)e-j 0.02 (0.01)e-h 1.04 (0.06)f-h Catawba 2.38 (0.11)e-h 0.63 (0.05)g-j 0.59 (0.05)c-e 0.10 (0.02)b-g 1.05 (0.06)f-h Zuni 2.33 (0.12)f-i 0.58 (0.04)g-k 0.56 (0.04)de 0.13 (0.02)b-e 1.06 (0.06)f-h Ozark Spring 2.21 (0.13)f-j 0.49 (0.05)h-n 0.48 (0.05)e-h 0.18 (0.03)ab 1.05 (0.06)f-h Natchez 1.97 (0.17)g-k 0.42 (0.05)h-n 0.58 (0.07)c-e 0.11 (0.02)b-f 0.87 (0.07)h-k Lipan 1.88 (0.11)h-k 0.41 (0.04)h-n 0.57 (0.05)c-e 0.04 (0.01)d-h 0.85 (.05)h-m Dynamite 1.86 (0.10)h-k 0.63 (0.06)g-j 0.04 (0.01)no 0 (0)h 1.18 (0.06)c-f Byer’s Red 1.83 (0.11)h-k 0.52 (.05)g-m 0.20 (0.03)j-o 0.10 (0.02)b-g 1.00 (0.06)f-h Powhatan 1.79 (0.11)i-k 0.33 (0.04)j-o 0.49 (0.04)e-h 0.10 (0.02)b-g 0.86 (0.06) h-l Regal Red 1.71 (0.11)j-m 0.57 (0.05)g-l 0.14 (0.03)j-o 0.07 (0.02)c-g 0.93 (0.06)f-j Velma’s R.D. 1.69 (0.10)j-m 0.37 (0.04)i-o 0.31 (0.04)g-k 0.13 (0.03)b-d 0.88 (0.06)h-k Osage 1.66 (0.12)j-m 0.52 (.06)g-m 0.52 (0.05)e 0.02 (0.01)e-h 0.59 (0.05)m-p Byer’s White 1.66 (0.09)j-m 0.54 (.05)g-m 0.14 (0.02)k-o 0.02 (0.01)e-h 0.96 (0.05)f-i Centennial 1.59 (0.11)k-o 0.31 (0.07)k-o 0.31 (0.04)f-k 0.07 (0.02)c-g 0.91 (0.06)g-j Wm. Toovey 1.59 (0.14)k-o 0.55 (0.06)g-l 0.24 (0.04)j-n 0.09 (0.02)b-h 0.70 (0.06)i-n Wichita 1.58 (0.12)k-o 0.60 (0.06)g-l 0.23 (0.04)j-n 0.06 (0.02)c-g 0.69 (0.05)i-n Choctaw 1.58 (0.11)k-o 0.71 (0.06)f-h 0.14 (0.02)k-o 0.10 (0.03)b-g 0.63 (0.05)k-o Pokomoke 1.51 (0.11)k-p 0.64 (0.06)g-j 0.15 (0.03)k-o 0.03 (0.01)d-h 0.69 (0.05)j-n Commanche 1.49 (0.11)k-p 0.66 (0.06)f-h 0.09 (0.02)l-o 0.04 (0.01)d-h 0.70 (0.05)i-n Tonto 1.29 (0.09)m-s 0.46 (0.04)g-m 0.20 (0.03)j-n 0.03 (0.01)d-h 0.60 (0.05)l-p Cent. Spirit 1.25 (0.08)n-t 0.23 (0.03)m-o 0.10 (0.02)l-o 0.04 (0.01)d-h 0.87 (0.06)h-k Tuskeegee 1.16 (0.10)n-t 0.38 (0.04)k-o 0.18 (0.03)k-o 0.03 (0.01)e-h 0.57 (0.05)n-q Potomac 1.08 (0.10)o-t 0.38 (0.05)k-o 0.09 (0.02)l-o 0.01 (0.01)gh 0.60 (0.05)l-p Muskogee 1.06 (0.09)o-t 0.23 (0.03)m-o 0.29 (0.04)g-l 0.02 (0.01)f-h 0.52 (0.05)m-p Ca. Beauty 1.02 (0.09)q-t 0.28 (0.04)l-o 0.01 (0.01)o 0.02 (0.01)f-h 0.72 (0.06)i-n Hardy Lav. 0.97 (0.10)q-t 0.27 (0.04)l-o 0.14 (0.02)k-o 0.06 (0.01)c-g 0.51 (0.05)n-q Biloxi 0.80 (0.09)s-u 0.17 (0.03)no 0.25 (0.03)i-m 0.04 (0.01)d-h 0.34 (0.04)pq Red Rocket 0.68 (0.09)tu 0.27 (0.04)l-o 0.01 (0.01)o 0.01 (0.01)gh 0.39 (0.05)o-q Rasp. Sundae 0.42 (0.05)u 0.07 (0.02)o 0.01 (0.01)o 0.01 (0.01)gh 0.32 (0.04)q Means within a column followed by different letters are significantly different (P < 0.05). View Large Bee species varied in plant preference. The two most visited cultivars among all bees were ‘Seminole’, a large shrub with pink flowers and ‘Victor’, a small shrub with red flowers during the 2 yr of study. Bumble bees, however were most commonly observed visiting ‘Apalachee’, a large shrub with lavender flowers. ‘Biloxi”, ‘Red Rocket’ and ‘Raspberry Sundae’ were visited least often by all bees. Plant height category significantly influenced bee visitation (Table 1). Among all cultivars, combined bees and the small bee category were most often observed on the small shrub category, followed by medium and large shrubs, with fewest observations on the small tree category (Fig. 1). Bumble bees, however were more frequently observed on the combined medium shrub cultivars, followed by large shrubs, then small shrubs and finally small trees. Honey bees were most frequently observed in the small shrub category, followed by large shrubs, then medium shrubs and small trees. Carpenter bees were observed in similar numbers among small, medium and tall shrubs, and less frequently on the small tree cultivars. Fig. 1. View largeDownload slide Mean ± SE number of bees observed on Lagerstroemia cultivars of varying heights during a 2-min observation period of three branches per plant on 23 dates during 2015 and 2016; Means (bars) within a bee category bearing different letters are significantly different (P < 0.05). Fig. 1. View largeDownload slide Mean ± SE number of bees observed on Lagerstroemia cultivars of varying heights during a 2-min observation period of three branches per plant on 23 dates during 2015 and 2016; Means (bars) within a bee category bearing different letters are significantly different (P < 0.05). Bees were most numerous on crape myrtles in early August during both years of study (Fig. 2). The small bee category was the most numerous and included P. bombiformis, M. tepaneca L. imitatum, L. illinoensis, A. aurata, A. pura pura, M. frigida, M. rotunda and M. sculpturalis. Honey bees were also frequently observed visiting crape myrtle flowers. Fig. 2. View largeDownload slide Mean ± SE number of bees observed on Lagerstroemia cultivars during a 2-min observation period of three branches per plant per date on 23 dates during 2015 and 2016. Fig. 2. View largeDownload slide Mean ± SE number of bees observed on Lagerstroemia cultivars during a 2-min observation period of three branches per plant per date on 23 dates during 2015 and 2016. Total bees, honey bees, bumble bees, small bees, and carpenter bees varied significantly in number observed among the different flower color categories (Table 1, Fig. 3). Dark pink, dark purple, and white were the flower colors most frequently visited among the nine color categories evaluated. Honey bees, however, were most frequently observed on pink-flowered cultivars while bumble bees were most numerous on lavender-flowered and dark purple cultivars. Fig. 3. View largeDownload slide Mean ± SE number of bees observed on Lagerstroemia cultivars with varying flower colors during a 2-min observation period of three branches per plant per date on 23 dates during 2015 and 2016; colors in the figure are 1 = white, 2 = lavender, 3 = pink, 4 = red, 5 = purple, 6 = magenta, 7 = dark purple, 8 = bicolor pink and white, and 9 = dark pink. Fig. 3. View largeDownload slide Mean ± SE number of bees observed on Lagerstroemia cultivars with varying flower colors during a 2-min observation period of three branches per plant per date on 23 dates during 2015 and 2016; colors in the figure are 1 = white, 2 = lavender, 3 = pink, 4 = red, 5 = purple, 6 = magenta, 7 = dark purple, 8 = bicolor pink and white, and 9 = dark pink. We also examined bee visitation with NMDS ordination (Fig. 4). Principal component analysis further confirmed that flower color (P < 0.003) and plant height (P < 0.001) influenced bee visitation. Cluster analysis ellipses for plant height categories show overlapping but distinct groupings based on height. Environmental vector fitting in the same direction of some of the ellipses in Fig. 4 show that bee visitation behavior is affected by both plant height and bloom color. Direction of the gradient of the vectors indicate the direction of the most rapid change in the variables while the similar lengths (strengths) of the gradient demonstrate similar contribution of height and flower color as the length of the arrow is proportional to the correlation between ordination and the variables tested. Fig. 4. View largeDownload slide Bee visitation to crape myrtle cultivars represented by NMDS ordination in two dimensions (stress = 0.13). Points represent incidences of bee visitation to four replications of each cultivar (n = 40) that are grouped by plant height category. Fig. 4. View largeDownload slide Bee visitation to crape myrtle cultivars represented by NMDS ordination in two dimensions (stress = 0.13). Points represent incidences of bee visitation to four replications of each cultivar (n = 40) that are grouped by plant height category. Discussion Previous work has suggested that suburban landscapes in eastern North America have the potential to host relatively diverse and intact bee communities (Fetridge et al. 2008). An increasing understanding of pollinator attraction to urban plantings is providing consumer options. Baker and Potter (2018), for example, determined that among eight milkweed species Asclepias tuberosa and A. fascicularis attracted the greatest number of bees, whereas bee genus diversity was greatest on A. verticillata, A. fascicularis, and A. tuberosa. A simple bee frequency (visitation) count (Frankie et al. 2005) revealed that 76 species of bees, mostly natives, from five families, visited 129 ornamental plants in northern California. Many factors contribute to plant attractiveness for pollinators and other beneficial insects in urban and rural settings (e.g., Harris et al. 2016, Wilson et al. 2016). Our current findings demonstrated the influence of cultivar, flower color and plant height on bee visitation among crape myrtles. Cultivars were not equally attractive to all bee categories and could potentially be more narrowly selected based on the target of conservation efforts. Crape myrtles which have become a dominant feature of southeastern landscapes offer the opportunity to provide a forage resource for native and honey bees, especially during later summer time periods when fewer floral resources are available. Bee visitation in our study was highest from mid-July through mid-August. Crape myrtles are widely used ornamental plants in the southern United States and can bloom as early as May in the deep south and can continue into the fall in more northern limits of the range that may also expand with changing climate. Riddle and Mizell (2016) discussed the opportunity to extend bloom periods and manage bloom accessibility to pollinators through pruning. Crape myrtles bloom on new growth and specific crape myrtle flowering phenologies could be adjusted by pruning to be accessible to bee species at the most opportune times. Synchrony of bee phenologies and crape myrtle flowers could be optimized. Hamblin et al. (2018), however do conclude that simply adding flowers to hot, impervious sites often characteristic of urban settings is unlikely to restore the balanced urban pollinator community. They demonstrated that addition of floral resources benefits large bees more than small bees and suggested that addition of floral resources be combined with impervious surface reduction, or other heat-island–reduction strategies for optimal results. The growing body of knowledge detailing pest management needs of various cultivars, horticultural attributes (Chappell et al. 2012), and comparative attractiveness to pollinators offers the consumer choices in plant preference that minimize the need for intervention for insect or disease suppression and increase likelihood of bee and other beneficial insect conservation. ‘Victor’, ‘Seminole’, and ‘Apalachee’, the most frequently visited cultivars among the 40 in our study have demonstrated fair to good disease resistance but are moderately susceptible to Japanese beetle and other insect pests that frequently require management (Chappell et al. 2012). Strategies that reduce these target pests while conserving pollinators should be a focal area for future research. Acknowledgments Comments by anonymous reviewers on an earlier draft improved the manuscript. We are grateful to the Georgia Mountain Research and Education Center for management of the crape myrtle collection. Ben Gochnour is appreciated for identification of bee spp. J. Davis and C. A. Braman provided valuable statistical consultation. Literature Cited Alverson , D. R. and R. K. Allen . 1992 . Bionomics of the crape myrtle aphid (Homoptera: Aphididae) . J. Entomol. Sci . 27 : 445 – 457 . Google Scholar Crossref Search ADS Baker , A. M. and D. A. Potter . 2018 . Colonization and usage of eight milkweed (Asclepias) species by monarch butterflies and bees in urban garden settings . J. Insect Conservation . 22 : 1 – 14 . doi: https://doi.org/10.1007/s10841-018-0069-5 Google Scholar Crossref Search ADS Braman , S. K. , J. Quick , M. Mead , and S. Nair . 2012 . 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TI - Differential Bee Attraction Among Crape Myrtle Cultivars (Lagerstroemia spp.: Myrtales: Lythraceae)
JF - Environmental Entomology
DO - 10.1093/ee/nvy117
DA - 2018-10-03
UR - https://www.deepdyve.com/lp/oxford-university-press/differential-bee-attraction-among-crape-myrtle-cultivars-lagerstroemia-rNEf3l1hgX
SP - 1203
VL - 47
IS - 5
DP - DeepDyve
ER -