Ecology and management of the crapemyrtle aphid (Hemiptera: Aphididae) on crapemyrtle (Myrtales: Lythraceae) in the southern United States

Abstract

Crapemyrtle aphid [Sarucallis kahawaluokalani (Kirkaldy 1907)] (CMA) is an introduced pest of crapemyrtle (Lagerstroemia spp. L.), which is among the most common ornamental tree genera in the southern United States. Native to Southeast Asia, CMA has become established on 5 other continents. CMAs produce honeydew as they feed which supports sooty mold growth and can result in leaf defoliation on infested trees. CMAs tend to be most abundant in crapemyrtles planted in locations with extensive surrounding impervious surface cover. A large community of generalist natural enemies are found in close association with CMA, which suggests that CMAs may help conserve natural enemy communities in urban areas. Due to the long-lasting blooms produced by crapemyrtle, and the attractiveness of these blooms to pollinators, insecticides should be used as a last resort to manage CMA infestations. While CMA is considered a specialist pest of crapemyrtle, it has been recorded on 3 species outside of the genus Lagerstroemia. The wide distribution of CMA, closely overlapping that of crapemyrtle, suggests that CMA can likely be found wherever crapemyrtles are commonly planted.

Introduction

Since its introduction in the 1790s (Favretti and Dewolf 1971), crapemyrtle (Lagerstroemia spp.) has become a common ornamental tree or shrub in the southern United States (Cothran 2004, Chappell et al. 2012). For example, tree inventories conducted on college campuses in Alabama and North Carolina found that crapemyrtle was the first and third most abundant planted tree species respectively (Martin et al. 2011, Rudder 2011). Crapemyrtles are valued for their summer-long blooms, exfoliating bark, ability to grow in a wide range of soil conditions, and tolerance of heat and drought stress (Chappell et al. 2012). Crapemyrtle aphid, Sarucallis kahawaluokalani (Kirkaldy 1907) (CMA), is a widespread pest of crapemyrtle in the southern United States (Alverson and Allen 1991, Chappell et al. 2012, Frank 2019). This species does not directly cause tree mortality, but the accumulation of black sooty mold as a result of honeydew produced from CMA herbivory can induce extensive defoliation and create sticky surfaces beneath trees (Dozier 1926). CMAs are fed upon by a diverse community of natural enemies, including hover fly larvae (Syrphidae), lady beetles (Coccinellidae), ants (Formicidae), and many other generalist predators (Mizell and Schiffhauer 1987, Bodlah et al. 2013, Parsons and Frank 2019, Parsons et al. 2020). The diverse community of natural enemies that feed on CMA likely prevent aphids from reaching high densities that would otherwise damage trees. Therefore, CMA is likely an important food resource for natural enemy communities wherever crapemyrtles are planted.

Distribution

CMA is native to Southeast Asia—as is crapemyrtle—but was first described in Hawai’i in 1907 (Kirkaldy 1907). The native range of CMA includes all places where crape myrtles grow naturally in Southeast Asia, including China, Japan, Taiwan, Malaysia, the Philippines, and India (Richards 1967, Higuchi 1972, Agarwala et al. 1989, Alverson and Allen 1991, Mizell et al. 2002). Beyond its native range, CMA has been recorded in Europe, Africa, North America, Central America, and South America (Fig. 1). Crapemyrtle is planted as an ornamental tree or shrub in 63 countries across Asia, Europe, Africa, Australia, the Americas, and the Caribbean islands (Secretariat 2019, Rojas-Sandoval and Acevedo-Rodríguez 2020). Since CMA eggs are small and easily hidden within crapemyrtle branches, eggs may have been moved to other countries through the ornamental plant trade, as is the case with many exotic aphid species (Kiritani and Yamamura 2003). Therefore, CMA is likely found in all countries where crapemyrtle is planted as an ornamental tree or shrub. The main factor limiting the distribution of CMA may be the climate preferences of crapemyrtle, which generally does not establish north of USDA Plant Hardiness Zone 6 in the United States where minimum temperatures range from −23.3 to −17.8 °C (Dirr 1990). Therefore, crapemyrtles and CMA are unlikely to be found in other regions of the world where average annual minimum winter temperatures are below −23.3 °C.

CMA’s introduced range in the Americas includes Hawai’i and the southern United States (Kirkaldy 1907, Alverson and Allen 1992), Puerto Rico (Mizell et al. 2002), Cuba (Ravelo 2008), Jamaica (Mizell et al. 2002), Mexico (Mizell et al. 2002, Trejo-Loyo et al. 2004), Honduras (Evans and Halbert 2007), Guadeloupe (Étienne et al. 2018), Guatemala (Ochaeta 2017), Panama (Quiros and Emmen 2006), Brazil (Peronti and Sousa-Silva 2002, Lazzari and Zonta-De-Carvalho 2006), Argentina (Szpeiner 2008), Venezuela (Carrera and Cermeli 2003), and Colombia (Kondo 2014).

In Eurasia, CMA has been found in: Bulgaria (Yovkova and Petrović-Obradović 2011), Montenegro (Petrović-Obradović et al. 2010), Croatia (Pintar et al. 2015), Slovenia (Seljak 2013), Italy (Barbagallo and Massimino Cocuzza 2014), France (Leclant and Renoust 1986), Portugal (Bella 2013), Spain (Durante and Merino 1995), Greece (Tsitsipis et al. 2007), Iran (Gholamzadeh-Chitgar 2017), and Pakistan (Bodlah et al. 2013). Finally, CMA has been recorded in Australia (Hales and Gillespie 2020) and 3 African countries: Cameroon (Mizell et al. 2002), Gabon (Noel et al. 2023), and the Democratic Republic of the Congo (CABI and EPPO 2015).

Biology

Summary of Life Cycle

CMA has a complex life cycle in which 3 distinct forms are produced over the course of 1 yr. Each first-generation female—the fundatrix—emerges from her egg and begins feeding on crapemyrtle leaves when bud break occurs in the spring (Alverson and Allen 1991). The fundatrix produces numerous morphologically identical clones—virginoparae—via live birth. The virginoparae will continue to produce clones via parthenogenesis over the summer (Alverson and Allen 1991). Both fundatrix and virginoparae adults have wings and are capable of dispersing to find new host plants. When day:night light cycles equalize during the fall equinox, females begin producing identical, but physiologically altered, offspring called sexuparae via live birth. The sexuparae then give birth to morphologically distinct, sexually reproducing offspring, sexuales, which are both male and female (Alverson and Allen 1991). Female sexuales are called “oviparae” and are wingless as adults (Alverson and Allen 1992). Male and female sexuales mate, and mated females deposit eggs on branches that will hatch following bud break in spring (Alverson and Allen 1991) although it remains unknown what environmental factors trigger egg eclosion.

Eggs

Mated oviparae oviposit on branches in the fall after leaf senescence begins. Newly laid eggs are oval shaped and yellow but turn black prior to hatching in early spring (Fig. 2) (Lazzari and Zonta-De-Carvalho 2006). Eggs are typically laid in groups of four but are also found singly along the branch (Alverson and Allen 1991). Eggs are laid on buds, under crevices in branches, underneath sloughing bark, on stem surfaces, or under bifurcations of thick branches (Alverson and Allen 1992, Lazzari and Zonta-De-Carvalho 2006). Alverson and Allen, 1992 report that the highest densities of eggs are within 40 cm of the terminal tips of branches, while, Lazzari and Zona-De-Carvalho 2006 and Pierce et al. (1998) report that most eggs are laid between 40 and 60 cm away from the terminal, roughly in the middle of branches. Such differences may be due to the growth form of trees due to different pruning practices (Pierce et al. 1998). Evidently, egg-laying behavior varies considerably between mated females, as eggs can be found over a meter away from the nearest terminal (Alverson and Allen 1992).

Nymphs

Nymphs are pale to bright yellow with black, club-tipped setae on their abdomen, but lack distinct siphunculi (Figs. 3 and 4) (Bodlah et al. 2013). Nymphs proceed through 4 instars before reaching adulthood (Alverson and Allen 1991, 1992). Development time is temperature dependent, ranging from 14 days from birth to adult at 26 °C, to 5 days at 32 °C (Alverson and Allen 1992). Molts from each instar typically occur in 1.6–3.6 days, occurring faster at warmer temperatures; the longest amount of time is spent in the fourth instar, which can take 1.6–4.5 days depending on temperature (Alverson and Allen 1992).

Adults

Adult CMA range from 1.1 – 1.9 mm in length, are yellowish green with pink eyes, and have numerous dark patches on their body with a pair of dorsal tubercles on the base of the abdomen (Figs. 3 and 5) (Alverson and Allen 1991, Chappell et al. 2012, Bodlah et al. 2013, Hales and Gillespie 2020). The dorsal tubercles are a two-pronged hump that separate the wings, which are held horizontally at rest (Alverson and Allen 1991). CMA wings are clear with black pigmentation along most veins and distal wing margins. CMA adults lack distinct siphunculi. All adults have wings except for female sexuales produced toward the end of the summer (Alverson and Allen 1992). Female sexuales have a deeper olive color than virginoparae (Alverson and Allen 1991). Males have a smaller abdomen than their female parents and are darker in coloration (Alverson and Allen 1991).

Damage and Host Range

Nymphs and adults feed on phloem extracted from the leaves of crapemyrtle. The excretion of honeydew from the aphids supports the growth of black sooty mold (Mizell and Knox 1993, Herbert et al. 2009). The accumulation of honeydew and sooty mold on surfaces below trees such as driveways, cars, or outdoor furniture creates sticky surfaces and discoloration that are typically viewed as a nuisance by residents. The sooty mold covers leaves making crapemyrtles appear unsightly and can cause defoliation (Fig. 6). Sooty mold accumulation and resultant leaf loss are typically greatest at the end of summer (Mizell and Knox 1993, Pierce et al. 1998). This effect is most problematic in nurseries, and greenhouse production systems, where extensive sooty mold coverage can render plants unsalable (Chappell et al. 2012). The prevalence of sooty mold on crapemyrtle is associated with the density of aphids within tree canopies, which is also influenced by the Lagerstroemia species and cultivar on which CMA are developing (see the section titled “Host plant resistance”).

Although CMA is commonly recorded feeding on Lagerstroemia indica and L. indica × fauriei, it is unclear which species in the Lagerstroemia genus cannot serve as hosts, or if species from other genera may be susceptible. To date, no feeding trials have been conducted to examine the host range of CMA, but there are records in the literature suggesting that CMA can feed on other hosts. Herbert et al. (2009) used Lagerstroemia speciosa as a negative control in a choice experiment where aphids could choose between various L. indica and L. indica × fauriei cultivars, and the authors found no aphids feeding on L. speciosa. In India, CMA has been recorded infesting Lawsonia alba Lam. (Myrtaceae) (Agarwala et al. 1989) and has been collected off Phyllostachys manii Gamble (Poaceae) (Chakrabarti 1988) although it is unclear if collected aphids from this record were feeding on P. manii. Additionally, Mizell and Knox (1993) mentioned the ability of the aphid to infest pomegranate, Punica granatum L. (Lythraceae) in the Philippines. Whether or not CMA readily uses these alternative hosts and can complete development on them remains unknown.

Urban Ecology

Crapemyrtles are commonly planted in cities and the unique abiotic features of these locations influence CMA proliferation in this host (Parsons and Frank 2019, Parsons et al. 2020). Because crapemyrtles grow in full sun and a variety of soil conditions, they are often planted in parking lots and along roadsides. The impervious surfaces in these areas absorb solar radiation and re-emit it as heat, which warms the local environment; this effect is termed the “urban heat island effect” (Kim 1992). Urban warming can support the proliferation of sap-sucking tree pests, such as scale insects (Coccoidea) on oak and maple trees, in areas with extensive impervious surface coverage (Meineke et al. 2013, Dale and Frank 2014). Similarly, Parsons and Frank (2019) found that CMA abundance in crapemyrtles was positively associated with surrounding impervious surface cover. However, Parsons et al. (2020) found that crapemyrtles with warmer canopies hosted fewer aphids than trees with cooler canopies. Thus, temperature alone may not drive aphid proliferation in urban crapemyrtles. Urban conditions can also exacerbate water stress in planted trees, and water-stressed crapemyrtles tend to host fewer aphids (Parsons et al. 2020). Taken together, these results suggest that CMA is less prevalent on trees in water-stressed conditions that have hot canopy temperatures (Alverson and Allen 1992, Sarah E Parsons et al. 2020). While CMA abundance may decrease in prolonged heat conditions, the prevalence of this pest in summers throughout the southern United States, when temperatures regularly exceed 30 °C, suggests that hot temperatures do not strongly limit CMA. Thus, crapemyrtles surrounded by extensive impervious coverage generally host many aphids, but this effect may not be attributable to heat island effects.

Longevity and fecundity of CMA appear to depend on host parentage and temperature. In urban landscapes, L. indica × fauriei hybrids are commonly planted due to their increased resistance to powdery mildew when compared to L. indica (Herbert et al. 2009). However, CMA is typically more fecund and abundant on hybrids than on L. indica (Mizell and Knox 1993, Herbert et al. 2009). When temperature is kept constant, parentage effects on CMA longevity become clearer. Alverson and Allen (1992) found mean female longevity to be 19.1 ± 1.6 (mean ± standard error) days when reared on L. indica × fauriei “Natchez” cultivars at 26 °C but 12.8 ± 0.8 days when reared on L. indica “Carolina Beauty” at the same temperature. However, parentage differences were less important at higher temperatures. Alverson and Allen (1992) reported that at 32 °C mean CMA adult longevity on “Carolina Beauty” was 7.6 ± 0.5 days and on “Nachez”, 7.5 ± 0.8 days. When kept at a constant temperature, (Parsons et al. 2020) found that CMA fecundity on L. indica × fauriei “Natchez” increased across aphid colonies kept at 26, 29, and 32°C, although the differences between these treatments were not statistically significant. Alverson and Allen (1992) found that female fecundity was greatest at 26 °C compared to 18 and 32 °C when raised on “Carolina Beauty”. These results suggest that under ideal conditions, CMA fecundity maximizes around 26–30 °C, but that longevity at these warmer temperatures might be lower than at cooler temperatures.

A diverse community of natural enemies is associated with crapemyrtle and CMA in urban landscapes. Parasitoid wasps (Hymenoptera), lacewings (Chrysopidae, Hemerobiidae), hover flies (Syrphidae), predatory beetles (Coccinellidae, Staphylinidae), predatory hemipterans (Anthocoridae, Nabidae, and Reduviidae), predatory thrips (Phlaeothripidae), and spiders (Araneae) have all been found in crapemyrtles infested with CMA (Dozier 1926, Mizell and Schiffhauer 1987, Mizell et al. 2002, Bodlah et al. 2013, Parsons and Frank 2019). Coccinellids, hover flies, and minute pirate bugs [primarily Orius insidiosus (Say)] all appear to track CMA densities and are among the most abundant natural enemies in crapemyrtle (Mizell and Schiffhauer 1987, Alverson and Allen 1992, Mizell 2007, Parsons and Frank 2019). Only one record exists of a braconid wasp, Lysiphlebus testaceipes (Cresson), emerging from CMA (Alverson and Allen 1992). However, in a search across two decades in the native and introduced range of crapemyrtles, no additional parasitoid species were recorded emerging from CMA (Mizell et al. 2002). While parasitoids are commonly found in crapemyrtle canopies, they do not appear to manage CMA populations even within their native range (Mizell et al. 2002), therefore all biological control of CMA is exerted by generalist predators.

The presence of parasitoids in crapemyrtle canopies may be due to these species feeding on CMA honeydew, feeding on pollen from the tree, or sheltering from unsuitable environmental conditions. Mizell and Schiffhauer (1987) found that many of the natural enemies of the black margined pecan aphid [Monellia caryella (Fitch)] were also found feeding on CMA. The authors suggested, that crapemyrtles could enhance biological control on pecan trees by providing additional food resources for predators in periods when pecan aphids are less abundant (Mizell and Schiffhauer 1987). However, recent studies have not found a significant relationship between CMA abundance in crapemyrtle canopies and resultant predation by natural enemies, nor a significant effect of natural enemy abundance on aphid densities (Parsons and Frank 2019, Parsons et al. 2020). Whether or not the abundance of CMA supports natural enemy communities and biological control within trees or on adjacent vegetation in urban ecosystems remains unclear and deserves further study.

Management

In residential settings, generalist predators often control CMAs effectively and additional treatment is not needed (Fig. 7). Smaller trees or shrubs planted in locations with extensive impervious surface cover can host high aphid densities and may be less resilient to infestation. In production settings, where crapemyrtles are grown in monoculture, aphid infestations can increase quickly—thus necessitating the need for chemical control (Chappell et al. 2012). No economic thresholds exist for CMA management, and in landscape settings, treatment usually occurs when the aesthetic value of the tree has been affected due to sooty mold accumulation.

Monitoring

Monitoring for CMA should begin in spring coincident with leaf break. Adult aphids will appear as black specks on the underside of leaves and white exuviae from molts are typically found nearby (Fig. 8). The presence of black sooty mold on leaves is a key indicator that a tree is infested and that management tactics should be considered (Fig. 6). Although management interventions for CMA will not remove sooty mold that is already present, effective CMA management will prevent further accumulation of honeydew and thus sooty mold.

Host Plant Resistance

Crapemyrtle cultivars vary in their susceptibility to CMA but also other insect pests such as flea beetles (Altica spp.) and Japanese beetles (Popillia japonica Newman), crapemyrtle bark scale [Acanthococcus lagerstroemiae (Kuwana)] and diseases such as powdery mildew and cercospora leaf spot (Chappell et al. 2012, Wu et al. 2021). Cultivars of L. indica parentage (e.g., “Carolina Beauty”) appear to be more resistant to CMA compared to L. indica × fauriei cultivars, but L. indica cultivars are more susceptible to powdery mildew than cultivars of L. indica × fauriei (Mizell and Knox 1993, Herbert et al. 2009). In a no-choice experiment Herbert et al. 2009 found CMA fecundity to be significantly lower on L. indica “Carolina Beauty” when compared to L. indica “Byers Wonderful White” and 5 other L. indica × fauriei cultivars (“Sioux”, “Natchez”, “Lipan”, “Tuscarora”, and “Apalachee”). Minimal differences in aphid fecundity were found between L. indica × fauriei cultivars. Hybrid cultivars with L. fauriei parentage are also generally more resistant to flea beetles and Japanese beetles than are L. indica cultivars, and include cultivars such as “Natchez”, “Chickasaw”, “Lipan”, “Muskogee”, and “Tonto” (Pettis et al. 2004, Braman et al. 2012). Although L. indica cultivars are generally less resistant to powdery mildew compared to L. indica × fauriei cultivars (Hagan et al. 2002), resistance to both powdery mildew and cercospora leaf spot varies within cultivars of L. indica, L. faurei, and L. indica × fauriei (Hagan et al. 1998). Cultivars that are resistant to both diseases include “Apalachee”, “Basham’s Party Pink”, “Caddo”, “Tonto”, and “Tuscarora” (Chappell et al. 2012). Finally, no cultivars of L. indica, L. fauriei, or L. indica × fauriei have been found to be resistant to crapemyrtle bark scale (Wu et al. 2021). However, Wu et al. 2021 found that crapemyrtle bark scale was not able to grow and develop on L. speciosa, leading the authors to suggest this species could be used to breed resistant cultivars. While CMA will not feed on L. speciosa (Herbert et al. 2009) it is unclear how resistant L. speciosa is to other pests of crapemyrtle.

In summary, L. indica × fauriei cultivars are generally resistant to many insect pests and diseases except for CMA and crapemyrtle bark scale. Chappell et al. (2012) list the following cultivars as being at least moderately resistant to CMA based on the findings of Mizell and Knox (1993) and Herbert et al. (2009): “Acoma”, “Apalache”, “Biloxi”, “Caddo”, “Centennial Spirit”, “Choctaw”, “Comanche”, “Fantasy”, “Hopi”, “Lipan”, “Miami”, “Muskogee”, “Natchez”, “Osage”, “Pecos”, “Sioux”, “Tuscarora”, “Tuskegee”, “Victor”, “Wichita”, “Yuma”, “Tonto”, and “Zuni”. However, “Natchez” cultivars can host high CMA densities in landscape settings (Parsons and Frank 2019), and Parsons et al. (2020) reared CMA in a laboratory setting on “Hopi” cultivars. Addesso and O’Neal (2019) established CMA on “Hopi” cultivars for insecticide experiments and Pettis et al. (2004) documented naturally occurring CMA infestations on “Muskogee” cultivars used in insecticide trials for Japanese beetle. Thus, additional research is needed to better understand which crapemyrtle cultivars act as poorer hosts for CMA and support fewer CMA in landscape settings.

Cultural

Careful consideration of landscape conditions, and pruning practices can help prevent problematic CMA infestations in landscape crapemyrtles. Crapemyrtles surrounded by extensive impervious surface cover tend to host high CMA densities (Parsons and Frank 2019). Therefore, crapemyrtles planted in locations such as parking lots or alongside streets may be more likely to develop CMA infestations. Given that crapemyrtles growing in warmer conditions appear to support fewer CMAs (Parsons et al. 2020), and that crapemyrtles grow best in full sun (Chappell et al. 2012), trees should not be planted in areas with extensive canopy coverage Pruning can reduce populations of CMA, and results in similar population reduction compared to horticultural oil application (Pierce et al. 1998). Heading back 30% of the tree canopy for trees taller than 2 m once per year prior to bud break may help reduce aphid abundance by removing overwintering eggs (Pierce et al. 1998). However, such pruning practices could support infestation by crapemyrtle bark scale, as this species congregates on tree wounds and sites of pruning injury (Chong and Coyle 2020).

Biological

Since many natural enemies feed on CMA, landscaping decisions that maximize local natural enemy populations could provide long-term protection against pest outbreaks. Planting flowers or enhancing vegetation complexity around urban trees and shrubs has been linked with increased generalist predator abundance and greater biological control of pest species (Rebek et al. 2005, Shrewsbury and Raupp 2006). Increased vegetation complexity underneath crapemyrtles can support natural enemy populations in tree canopies, although this effect has not been linked to greater aphid predation in tree canopies (Parsons and Frank 2019, Parsons et al. 2020). Planting shrubs and flowers underneath crapemyrtle trees may provide shelter and nectar resources for natural enemies, which could support their populations, but such interventions may not necessarily result in greater aphid control. The pollen of crapemyrtle flowers may be attractive for foraging natural enemies and serve as a valuable food resource. Whether or not natural enemies feed on and benefit from crapemyrtle pollen remains untested; however, many wild bee species have been recorded collecting crapemyrtle pollen (Riddle and Mizell 2016, Braman and Quick 2018). Effective pruning of crapemyrtles to maximize bloom cover could increase the availability of pollen resources for natural enemies and pollinators, which could support their populations and, ideally, result in consistent regulation of CMA populations. Additional research is needed to identify how biological control of CMA by natural enemies can be enhanced through landscaping practices.

Lagerstroemia species contain alkaloids in their leaves, stems, and seeds, which may be sequestered by CMA that feed on crapemyrtle and could prevent parasitoids that oviposit in CMA from developing within CMA or slow the development rate of predators that consume CMA (Mizell et al. 2002). The cultivar on which CMA grow and develop does not appear to affect the survival of the lacewing predator Chrysoperla rufilabris (Burmeister) but can affect number of adults that emerge from pupae (Herbert 2009). An experiment in which C. rufilabris were fed CMA that developed on L. indica × fauriei “Apalachee”, had a lower rate of emergence in comparison to CMA reared on other cultivars “Natchez”, “Tuscarora”, “Lipan”, “Carolina Beauty”, and “Byers Wonderful White”. The degree to which CMA sequester alkaloids from crapemyrtle, and potential effects on most CMA natural enemies remains unknown.

Chemical

To prevent deleterious effects on pollinators collecting crapemyrtle pollen (Riddle and Mizell 2016, Braman and Quick 2018) and natural enemies feeding on CMA, chemical control should be considered a last resort for reducing aphid populations. Pettis et al. (2005) evaluated the effectiveness of foliar systemic insecticides, horticultural oils, and insecticidal soaps on crapemyrtle aphids on 5 crapemyrtle cultivars in a field and screen house experiment. The authors found that in the field experiment, acephate, imidacloprid, and thiamethoxam resulted in the greatest reduction in aphid abundance. However, insecticidal soaps and horticultural oils were not used for comparison in the field (Pettis et al. 2005). In the screen house experiment, horticultural oils and insecticidal soaps achieved similar levels of control that were not significantly different from neonicotinoid sprays (Pettis et al. 2005). Addesso and O’Neal (2019) tested the efficacy of drench (Flonicamid, Spirotetramat, and Flupyradifurone) and foliar (Flupyradifurone) insecticides on CMA infesting potted crapemyrtles (L. indica. x fauriei “Hopi”). Crapemyrtles treated with Flonicamid and Flupyradifurone had fewer aphid adults and nymphs than the control from 14 to 42 days after treatment (DAT) while the Spirotetramat treatment resulted in fewer adult aphids than the control up to 35 DAT and fewer immatures than the control up to 42 DAT. However, the authors did not compare the efficacy of these products to horticultural oils or insecticidal soaps. Because of the ability of plants to sequester systemic neonicotinoid insecticides into their pollen (Cowles and Eitzer 2017) and the documented toxicity of these compounds to pollinators and natural enemies (Cloyd and Bethke 2011, Godfray et al. 2014, Mach et al. 2018), use of neonicotinoid insecticides on crapemyrtles may adversely affect beneficial insect populations. Thurmond (2019) found that crapemyrtles treated with imidacloprid via soil injection appear to produce greater control of CMA relative to trees treated with soil-injected dinotefuran. However, regardless if trees were treated postbloom/predormancy, prebud break, or postbud break/prebloom, resultant imidacloprid and dinotefuran residues in crapemyrtle pollen were near or exceeded previously published LD50 (lethal dose that kills 50% of individuals) thresholds for honey bee workers. Flonicamid, flupyradifurone, and spirotetramat have low acute toxicity on many natural enemy groups (Azod et al. 2016, Barbosa et al. 2017, Quesada and Sadof 2020), but sublethal effects from these compounds have been observed on natural enemies and bees (Roditakis et al. 2014, Sgolastra et al. 2015, Azod et al. 2016, Tosi et al. 2021). Since horticultural oils and insecticidal soaps have minimal residual toxicity to natural enemies or pollinators, they should be considered first for CMA management before other insecticide classes. If oils and soaps do not produce effective control, selective insecticides (e.g., flonicamid, flupyradifurone, and spirotetramat) should be used instead of broad-spectrum insecticides (e.g., acephate, imidacloprid, dinotefuran, and thiamethoxam).

Conclusion

CMA is a pest of crapemyrtle that reaches its highest densities on landscape crapemyrtles surrounded by extensive impervious surface cover. The wide distribution of CMA across multiple continents suggests CMA may have unrealized invasive potential. Cultural control tactics can be used in conjunction with horticultural oils or insecticidal soaps to lower CMA densities without harming local natural enemy populations. CMA may also be important for supporting natural enemy communities and biological control in urban landscapes.

Acknowledgments

We thank Steve Frank (North Carolina State University), Michael Just (US Army ERDC CERL), and 3 anonymous reviewers for providing feedback on earlier versions of this manuscript. We thank James Baker (North Carolina State University) for providing the photograph used in Fig. 2.

Funding

This publication was supported by start-up funds provided to C.J.W. by the Department of Entomology, University of Kentucky.

Author Contributions

Caleb Wilson (Conceptualization [Lead], Data curation [Lead], Funding acquisition [Lead], Investigation [Lead], Methodology [Lead], Project administration [Lead], Supervision [Lead], Visualization [Supporting], Writing—original draft [Lead], Writing—review & editing [Equal]), and Matt Bertone (Visualization [Lead], Writing—review & editing [Equal])

References