Abstract
Crapemyrtle bark scale (CMBS; Acanthococcus lagerstroemiae Kuwana), a fast-spreading invasive insect, has been causing damage to popular landscape plants in at least 17 states in the United States since 2004. This invasive insect has a list of documented plant hosts in ∼23 genera, which includes its primary hosts, crapemyrtles (Lagerstroemia spp.), as well as other important plant species, such as pomegranates, apple, and the native plant American beautyberry. Previous studies have shown CMBS causes different levels of feeding damage among its plant hosts, while the underlining plant defense mechanisms toward CMBS attacks remain elusive. A better understanding of plant–CMBS interactions and how CMBS performs under different plants (e.g., a susceptible vs. a resistant host) can provide valuable guidance for integrated pest management. Therefore, in this study, we conducted the age-stage, two-sex table study analysis to evaluate the biological parameters of CMBS on different species or cultivars of crapemyrtle under laboratory conditions (25 °C and 250 μmol·m−2·s−1 light with a photoperiod of 12 hours:12 hours (light:dark). Crapemyrtle bark scale development was found to be greatly influenced by the hosts. This study aims to provide important biological and ecological data on CMBS using a comprehensive life table study to gain a thorough understanding of its development, survival, and fecundity on different crapemyrtle species or cultivars.
Crapemyrtle bark scale (CMBS; Acanthococcus lagerstroemiae), native to East Asia, was originally categorized under the genus Eriococcus, and it was first described from specimens of adult females collected by Kuwana in Japan in 1907 (Kuwana 1907). The binomial name A. lagerstroemiae was first used by Borchsenius in 1960, where he also provided descriptions and keys based on the morphology of adult female samples collected in China (Borchsenius 1960). Crapemyrtles (Lagerstroemia spp.), the primary host of CMBS, are one of the best-selling flowering landscape plants of the southern United States, with market value increasing to $70 million over the past 2 decades [Supplemental Fig. 1; US Department of Agriculture National Agriculture Service (USDA NASS), 2001, 2009, 2014, 2019].
Crapemyrtle, through years of adaptation in the landscape, has been a significant component of the local ecosystem in the southeast United States (Riddle and Mizell 2016). Although crapemyrtle flowers do not produce nectar, they offer a significant amount of pollen to reward visiting pollinators such as bees (Harris 1914; Kim et al. 1994). Studies have shown that crapemyrtle pollen is a major protein source with a nutritional makeup suitable for bee ingestion (Nepi et al. 2003). Crapemyrtle blooms heavily and extensively during summer months (Pounders et al. 2006; Pounders et al. 2010), which makes it a critical food source for pollinators, especially when many other flowering plants are not in bloom (Lau et al. 2019).
Infestation by CMBS has been reported to cause the reduction of flowering in crapemyrtle (Harp 2022; Wu et al. 2022b; Xie et al. 2020). Furthermore, the continuous spread of CMBS not only lowers the value of crapemyrtle as perceived by consumers and producers (Marwah et al. 2021) but also threatens other plant species (native or nonnative) in the United States (Wu et al. 2021, 2022b; Xie et al. 2021). The infestation of CMBS has been confirmed on several native plants in the United States, including American beautyberry and St. Johnswort (Schultz and Szalanski 2019; Wu et al. 2022b) and plants in the rose family, such as apple and spirea (Xie et al. 2020, 2021). Successful strategies for managing CMBS on its primary hosts could slow down its spread to more economically important crops and could be applicable in case the infestation on more economically important crops becomes a significant issue. Therefore, the study of the interaction between CMBS and the plant species within crapemyrtle genus (Lagerstroemia) can provide a better understanding and identification of host plant susceptibility and resistance to this insect, potentially leading to the breeding of insect-resistant cultivars and reduce pesticide use in the future.
Historically, interspecific breeding effects have resulted in numerous disease and pest tolerance traits in the current crapemyrtle genetic reservoir. For example, the interspecific hybridization between L. indica and L. fauriei has resulted in powdery mildew–resistant cultivars such as ‘Tuscarora’, ‘Tuskegee’, and ‘Tonto’ (Egolf 1981, 1986, 1990; Hagan et al. 1998). The interspecific cultivars such as ‘Natchez’, ‘Tonto’, and ‘Muskogee’ have shown increased resistance toward major pests, including flea beetle (Altica spp.) and Japanese beetle (Popillia japonica Newman) (Pettis et al. 2004).
The most popular crapemyrtle cultivars (with the greatest sales) are interspecific hybrids ‘Natchez’, ‘Muskogee’, and ‘Tuscarora’ (Marwah et al. 2021), which are all susceptible to CMBS attacks according to greenhouse feeding trials (Wang et al. 2019) and our observations. In previous studies, six crapemyrtle species (L. caudata, L. fauriei ‘Kiowa’, L. indica ‘Dynamite’, L. limii, L. speciosa, and L. subcostata) and the hybrid cultivars (L. indica × fauriei ‘Spiced Plum’ and L. ‘Natchez’) were evaluated as for their suitability as CMBS hosts under greenhouse conditions (Wu et al. 2021; Xie et al. 2020). The CMBS infestations were found on all tested plant species, with L. speciosa showing relatively low infestation levels. For example, among the species with the most severe infestations, L. limii had ∼1000 male pupae and 600 female ovisacs per plant at the peak of the CMBS population. In contrast, L. speciosa had the lowest infestation, with ∼45 male pupae and 57 female ovisacs, respectively (Wu et al. 2021).
Thus, previous greenhouse feeding trials suggested that potential species-specific CMBS resistance exists among the tested plants, providing valuable guidance for future pest management. For instance, species with low CMBS infestations, such as L. caudata and L. speciosa, may be used in future breeding programs to develop CMBS-resistant crapemyrtle cultivars. However, the mechanisms and factors underneath the differentiated CMBS infestations found on different crapemyrtle species or cultivars are still unknown.
Plant–CMBS interactions throughout the entire life cycle of insects should be further understood to characterize potential phenotypic traits contributing to insect resistance for better plant selections. Host plant resistance to insect herbivores is generally categorized into complete or partial resistance, which consists of antixenosis (nonpreference), antibiosis, and tolerance to insect damage (Thomas and Waage 1996). The successful development of scale insect colonies can be affected and evaluated by various biological (or life table) parameters, including survival rate, developmental durations, sex ratio, and reproduction (Birch 1948; Carey 2001; Chi and Liu 1985; Manly 1974), which interact with the effects of host plant conditions (Brodbeck and Strong 1987; Mopper 1996; Wallner 1987) and genetic backgrounds (Maxwell 1985; Sharma and Ortiz 2002).
The study of insect biological parameters and life tables is a system of analytical and mathematical approaches to collect, quantify, and interpret insect population data (Harcourt 1969). The acquisition of biological parameters for an insect generally involves well-established insect-rearing and record-keeping systems, followed by data analysis to generate age-stage specific survival rate, age-stage specific fecundity, age-stage specific life expectancy, and population growth parameters (Chi et al. 2020). Life table study is a fundamental ecological and biological tool that provides insight into the population dynamics of the arthropods of interest (Chi 1988; Muhamad et al. 2011; Naranjo and Ellsworth 2017). Thus, studying insects’ biological parameters in terms of developmental responses and population dynamics under experimental conditions can be a useful approach for gaining in-depth knowledge about host plant resistance toward invasive insects such as CMBS.
The effect of different plant hosts on the biological parameters of insect development has been studied for different species of scale insects or mealybugs, including Hemiberlesia sp. (Hill et al. 2009), Aspidiotus sp. (Cortaga et al. 2019; Erol et al. 2019; Salahuddin et al. 2015), Pseudaulacaspis Pentagona (Hanks and Denno 1994), Kerria lacca (Rout et al. 2018), Phenacoccus solenopsis (El Aalaoui and Sbaghi 2022), and Planococcus citri (Polat et al. 2008). However, such information for CMBS, especially the effect of different crapemyrtle hosts on insect development and population dynamics, is currently lacking.
To obtain basic information on CMBS biology, the biological parameters of CMBS should be investigated through the construction of life tables on different crapemyrtle hosts. This study focuses on acquiring critical biological information in terms of the fertility life table for CMBS to expand the current knowledge related to the interaction between CMBS and different species or cultivars of crapemyrtle to help the development of effective integrated pest management and plant breeding program in controlling this pest insect.
Material and Methods
Insect source and handling.
Branches/twigs infested with CMBS were collected from crapemyrtle trees on campus (lat. 30°36′30.4″ N, long. 96°21′01.9″ W; Texas A&M University, College Station, TX, USA) and stored in zip-lock bags under constant temperature (25 °C). Colonies of CMBS were established and maintained in the greenhouse and growth chamber (Controlled Environments Inc., Pembina, ND, USA) by inoculating healthy crapemyrtle plants with CMBS-infested branches. White coverings (ovisacs) of the female scales were carefully lifted using a fine pin/needle to obtain eggs. After removing all existing eggs inside the ovisacs, the gravid females were transferred, using a fine brush, onto a moist filter paper and placed in a petri dish (Falcon Disposable petri dishes, 60 mm × 15 mm; Corning, Glendale, AZ, USA). All newly laid eggs were collected the next day (within 24 h) and kept under 25 °C for incubation until hatched.
Plant materials.
Crapemyrtle species and cultivars, including Lagerstroemia fauriei Kiowa, L. limii, and L. indica × fauriei Tuscarora, were maintained in the greenhouse, and cuttings were collected from these stock plants and used as host/food source for the CMBS rearing experiment in petri dishes. Life history data generated from CMBS populations reared on these species and cultivars were compared with those reared on the seedlings of L. fauriei Fantasy (Xie et al. 2022) using the same rearing method. Small plants (liners) of L. indica ‘Dynamite’, L. fauriei ‘Kiowa’, and L. indica × fauriei ‘Natchez’ were also used to conduct CMBS insect-rearing experiments with a group-rearing method.
Insect rearing experiment using feeding chambers.
Insects were reared in individual feeding chambers (Supplemental Fig. 2) using the same methods (Xie et al. 2022). Briefly, insect feeding chambers were constructed using small petri dishes (Falcon disposable petri dishes, 60 mm × 15 mm; Corning) with the bottom half filled with agar medium (1%) with 0 to 0.01 Murashige and Skoog (MS) salt supplementations (0 to 0.043 g MS salt per 1 L media). Rooted stem cuttings with shoots or bud nodes were transferred from rooting containers to the insect-rearing chambers before the experiments. 0.01 MS salt solution or deionized water was added as needed to prevent the media from drying out. Depending on the condition of the medium, rooted cuttings were carefully removed from the old medium and transferred to fresh medium regularly throughout the rearing experiment. The rearing chambers were placed in Conviron growth chambers (Controlled Environments Inc.) set at 25 °C and 250 μmol·m−2·s−1 light with a photoperiod of 12 h:12 h (light:dark).
Ten to 20 newly hatched crawlers (per plant) were transferred onto rooted stem cuttings using a fine brush or pin. Daily observations were made to record the settling status of nymphs. Once CMBS crawlers settled on one location and started feeding, an ID was assigned to each individual to track the insect development. Rearing chambers with nymphs that failed to settle and initiate feeding (i.e., no CMBS found on the plants) were discarded.
Insect-rearing experiments on different crapemyrtle species or cultivars were conducted and repeated from 2019 to 2021. Daily observations were made as nymphs started feeding, and the duration of each developmental stage (including nymphal stages, pupa, and adult stages) was recorded. When a male reached the adult stage, it was transferred to pair with a female for mating to complete the life cycle. Fecundity data (the number of eggs an adult female produces) and longevity (the number of days a female lives) were recorded as the gravid females completed their life cycle.
Insect group-rearing experiment.
Insect-rearing experiments on different crapemyrtle species were conducted on small crapemyrtle liners (Supplemental Fig. 3) from May 2021 to February 2022. Small crapemyrtle plants in 2-inch trays were used as host plants for CMBS (Supplemental Fig. 3). Crapemyrtle species and hybrid cultivars, including L. indica ‘Dynamite’, L. fauriei ‘Kiowa’, and L. indica × fauriei ‘Natchez’, were selected as host plants for the CMBS group-rearing experiments. One hundred newly hatched crawlers per plant (three replications) were transferred using a fine brush or pin. Each plant was examined two to three times per week, and the number of CMBS at different developmental stages was recorded (Supplemental Fig. 4).
Data analysis and statistics.
The developmental stages of both male and female CMBS were determined by morphological changes and daily monitoring of the insect exuviates (the number of molts) (Xie et al. 2022). According to the age-stage, two-sex life table theory (Chi 1988; Chi and Liu 1985), the fecundity data (number of eggs each adult female produced) and longevity data (the number of days each CMBS nymph lives) can be obtained to calculate the biological parameters of CMBS.
The life history data of CMBS were analyzed using the same method as previously described (Xie et al. 2022). The population (life table) parameters of CMBS reared on different crapemyrtle species or cultivars were generated by TWOSEX-MS Chart (Chi 2020). According to the age-stage, two-sex life table theory (Chi et al. 2020), age-stage specific survival rate (sxj, where x = age in days and j = stage), age-stage specific fecundity [f (x, female), where x = age in days], age-stage specific life expectancy (exj, where x = age in days and j = stage), and population parameters including mean generation time (T), net reproduction rate (Ro), the intrinsic rate of increase (r), and the finite rate of natural increase (λ) were obtained to construct the age-stage, two-sex life table. Data calculated for the biological parameters of CMBS were subjected to bootstrap resampling with 100,000 replications to estimate the standard errors. Differences in the duration of each developmental stage and the population parameters of CMBS reared at different nutrient conditions were compared using the paired bootstrap test.
Results and Discussion
The effect of hosts on developmental stages.
CMBS showed various developmental times and population dynamics on different crapemyrtle species and cultivars. The life cycle of CMBS has been previously characterized and documented in detail (Xie et al. 2022). Briefly, the development of CMBS involves stages of egg, two nymph stages [N1 (first instar) and N2 (second instar)], three pupa stages for males [P1 (second instar male that developed the male sac), P2 (prepupa), and P3 (pupa)], and adults [male (alate) and female (third instar nymph)] (Xie et al. 2022). The mean development durations of the male first instar were similar among Lagerstroemia fauriei ‘Kiowa’, L. limii, and the L. fauriei ‘Fantasy’ seedling (∼17 d) but longer compared with the CMBS reared on L. indica × fauriei ‘Tuscarora’ (∼14 d) (Table 1). For the females, the mean development durations of first instar ranged from 15 to 18 d on L. fauriei ‘Kiowa’, L. limii, L. indica × fauriei ‘Tuscarora’, and the L. fauriei ‘Fantasy’ seedling (Table 2).
Means ± SEs and sample size (N) of development duration (days) of male Acanthococcus lagerstroemiae under laboratory conditions of 25 °C and 250 μmol·m−2·s−1 light with a photoperiod of 12:12 (light:dark). Data within a row followed by different letters are significantly different at P < 0.05 by using paired bootstrap test.
Means ± SEs and sample size (N) of development duration of female Acanthococcus lagerstroemiae under laboratory conditions of 25 °C and 250 μmol·m−2·s−1 light with a photoperiod of 12:12 (light:dark). Data within a row followed by different letters are significantly different at P < 0.05 by using paired bootstrap test.
The development durations of second instars of both males and females demonstrated the largest difference among crapemyrtle hosts, with the longest time found from the male populations on the L. fauriei ‘Fantasy’ seedling, which doubled the durations on L. fauriei ‘Kiowa’ (Table 1). The development of male second instars is shorter than the female second instars on L. fauriei ‘Kiowa’. However, a longer developmental time of male second instars was found on L. indica × fauriei ‘Tuscarora’, L. limii, and the L. fauriei ‘Fantasy’ seedling compared with females (Tables 1 and 2).
According to the life table analysis of CMBS on different crapemyrtles, the insect population developed fastest on the L. fauriei ‘Kiowa’, with the shortest mean generation time (T) of 78.65 ± 6.12 (days ± SE), compared with the most prolonged T (113.749 ± 5.252 d) found on the L. fauriei ‘Fantasy’ seedling (Table 3), which suggests that the development rate of CMBS infestation is greatly influenced by different crapemyrtle hosts.
Intrinsic rate of increase (r) ± SEs, finite rate of increase (λ) ± SEs, net reproduction rate (Ro) ± SEs, mean generation time (T) ± SEs, and gross reproductive rate (GRR) ± SEs of Acanthococcus lagerstroemiae in individual feeding chambers under laboratory conditions of 25 °C and 250 μmol·m−2·s−1 light with a photoperiod of 12:12 (light: dark). N represents number of individuals in the monitored populations from the beginning of experiment. Data within a column followed by different letters are significantly different at P < 0.05 by using paired bootstrap test.
There were significant differences in male pupa duration between CMBS reared on the different crapemyrtle species and cultivars according to paired bootstrap test at a 0.05 confidence level (Table 1). A male individual can be easily identified after the second instar (P1) forms the typical male pupa sac, and hence the duration of the P1 stage can be determined by daily monitoring of exuviae. Once the P1 nymph molts, it will push out the exuviae from the rear opening of the male sac, which signifies the end of the P1 stage. Moreover, according to our observations, male second instars would retract their mouth part from the plant tissue and start locating a suitable spot before pupation (the forming of the male sac). Thus, a P1 nymph is no longer actively feeding and attached to the plants as a typical second instar (N2) and can be taken out from the male sac and transferred into an empty petri dish, where the P1 can continue to develop into P2 and P3, with the respective durations determined in this manner (Xie et al. 2022). For the duration of pupa developments, the most extended P1 was observed in the male individuals reared on L. limii. The duration of the prepupa stage (P2) was similar on L. limii, L. indica × fauriei ‘Tuscarora’, and the L. fauriei ‘Fantasy’ seedling, while the shortest P2 was found on L. fauriei ‘Kiowa’ (Table 1). For the pupa stage (P3), the longest duration was found in the populations reared on the L. fauriei ‘Fantasy’ seedling compared with the rest of the crapemyrtle hosts (Table 1).
Studies suggest that insect performance strongly relates to the nutritional requirements of insects at different stages (Panizzi 1987; Scriber and Slansky 1981), and the accessibility of essential nutrients to insect herbivores could be influenced by different plant characteristics such as physical structures and allelochemicals in the plant sap (Slansky 1990). For example, seed-sucking hemipterans such as green stink bug (Acrosternum hilare Say) requires higher nutrient content at the fifth instar stages than the earlier nymphal and adult stages, and the plant structures such as trichomes and seedcoat play a significant role in early nymphal mortality (Panizzi 1987). Thus, future studies should be conducted to comprehensively analyze the relationship between different plant features and nutritional constituents and how they affect the CMBS developmental stages and population dynamics.
The effect of hosts on population dynamics.
The survival rate, population growth, and life expectancy of CMBS were also greatly influenced when reared on different species or cultivars of crapemyrtles (Figs. 1–3), which suggests that the population dynamics of CMBS could vary drastically based on host suitability. Typically, less than 20% of the initial CMBS population reached the adult stages (adult female or adult male stage) on all tested species and cultivars (Fig. 1). The CMBS male pupae were observed as early as around 17 d on L. fauriei ‘Kiowa’, whereas no male pupae and adult males were observed until day 50 on L. limii, L. indica × fauriei ‘Tuscarora’ and the L. fauriei ‘Fantasy’ seedling (Fig. 1).
Age-stage specific survival rate (sxj) of Acanthococcus lagerstroemiae reared on (A) Lagerstroemia fauriei ‘Kiowa’, (B) L. indica × fauriei ‘Tuscarora’, (C) L. limii, and (D) L. fauriei ‘Fantasy’ seedling under laboratory conditions of 25 °C and 250 μmol·m−2·s−1 light with a photoperiod of 12:12 (light:dark).
Citation: HortScience 58, 5; 10.21273/HORTSCI17009-22
Age-stage specific survival rate (sxj) of Acanthococcus lagerstroemiae reared on (A) Lagerstroemia fauriei ‘Kiowa’, (B) L. indica × fauriei ‘Tuscarora’, (C) L. limii, and (D) L. fauriei ‘Fantasy’ seedling under laboratory conditions of 25 °C and 250 μmol·m−2·s−1 light with a photoperiod of 12:12 (light:dark).
Citation: HortScience 58, 5; 10.21273/HORTSCI17009-22
Age-stage specific survival rate (sxj) of Acanthococcus lagerstroemiae reared on (A) Lagerstroemia fauriei ‘Kiowa’, (B) L. indica × fauriei ‘Tuscarora’, (C) L. limii, and (D) L. fauriei ‘Fantasy’ seedling under laboratory conditions of 25 °C and 250 μmol·m−2·s−1 light with a photoperiod of 12:12 (light:dark).
Citation: HortScience 58, 5; 10.21273/HORTSCI17009-22
Age-stage specific fecundity f (x, female), age-specific fecundity (mx), and age-specific maternity (lxmx), and cumulative net reproduction rate {Cumul[(lx)*(mx)]} of Acanthococcus lagerstroemiae reared on (A) Lagerstroemia fauriei ‘Kiowa’, (B) L. indica × fauriei ‘Tuscarora’, (C) L. limii, and (D) L. fauriei ‘Fantasy’ seedling under laboratory conditions of 25 °C and 250 μmol·m−2·s−1 light with a photoperiod of 12:12 (light:dark).
Citation: HortScience 58, 5; 10.21273/HORTSCI17009-22
Age-stage specific fecundity f (x, female), age-specific fecundity (mx), and age-specific maternity (lxmx), and cumulative net reproduction rate {Cumul[(lx)*(mx)]} of Acanthococcus lagerstroemiae reared on (A) Lagerstroemia fauriei ‘Kiowa’, (B) L. indica × fauriei ‘Tuscarora’, (C) L. limii, and (D) L. fauriei ‘Fantasy’ seedling under laboratory conditions of 25 °C and 250 μmol·m−2·s−1 light with a photoperiod of 12:12 (light:dark).
Citation: HortScience 58, 5; 10.21273/HORTSCI17009-22
Age-stage specific fecundity f (x, female), age-specific fecundity (mx), and age-specific maternity (lxmx), and cumulative net reproduction rate {Cumul[(lx)*(mx)]} of Acanthococcus lagerstroemiae reared on (A) Lagerstroemia fauriei ‘Kiowa’, (B) L. indica × fauriei ‘Tuscarora’, (C) L. limii, and (D) L. fauriei ‘Fantasy’ seedling under laboratory conditions of 25 °C and 250 μmol·m−2·s−1 light with a photoperiod of 12:12 (light:dark).
Citation: HortScience 58, 5; 10.21273/HORTSCI17009-22
Age-stage specific life expectancy (exj) of Acanthococcus lagerstroemiae reared on (A) Lagerstroemia fauriei ‘Kiowa’, (B) L. indica × fauriei ‘Tuscarora’, (C) L. limii, and (D) L. fauriei ‘Fantasy’ seedling under laboratory conditions of 25 °C and 250 μmol·m−2·s−1 light with a photoperiod of 12:12 (light:dark).
Citation: HortScience 58, 5; 10.21273/HORTSCI17009-22
Age-stage specific life expectancy (exj) of Acanthococcus lagerstroemiae reared on (A) Lagerstroemia fauriei ‘Kiowa’, (B) L. indica × fauriei ‘Tuscarora’, (C) L. limii, and (D) L. fauriei ‘Fantasy’ seedling under laboratory conditions of 25 °C and 250 μmol·m−2·s−1 light with a photoperiod of 12:12 (light:dark).
Citation: HortScience 58, 5; 10.21273/HORTSCI17009-22
Age-stage specific life expectancy (exj) of Acanthococcus lagerstroemiae reared on (A) Lagerstroemia fauriei ‘Kiowa’, (B) L. indica × fauriei ‘Tuscarora’, (C) L. limii, and (D) L. fauriei ‘Fantasy’ seedling under laboratory conditions of 25 °C and 250 μmol·m−2·s−1 light with a photoperiod of 12:12 (light:dark).
Citation: HortScience 58, 5; 10.21273/HORTSCI17009-22
Net reproduction rate (Ro), the intrinsic rate of increase (r), and the finite rate of natural increase (λ) are population parameters used for projecting the reproductive potential of insects. Ro represents the number of offspring that an individual (including male and female) within the population could produce over its lifetime, whereas r and λ describe the population growth rate as the time approaches infinity and the population reaches stable status. Crapemyrtle bark scale with the highest population growth rate (r and λ) was found on L. fauriei ‘Kiowa’, compared with the lowest found on the L. fauriei ‘Fantasy’ seedlings (Table 3). In terms of the reproductive parameters, the lowest gross reproductive rate (GRR) of CMBS was observed on L. indica × fauriei ‘Tuscarora’ (with 62.6 ± 22.7 offspring per individual), while the highest mean GRR was found on the L. limii (94.3 ± 4.6 offspring per individual) (Table 3). However, with the high fecundity of individual females, the CMBS reared on L. limii has the lowest value for the Ro (Table 3) due to the high mortality of immature nymphs in the experimental populations. Overall, the fecundity values were not significantly different among all tested crapemyrtle species and cultivars (Table 3).
Overlapping developmental stages were observed in all tested CMBS populations but with various levels, caused by different survival rates of nymphs reared on different crapemyrtle species and cultivars (Fig. 1). For example, the highest survival rate of second instars was found on L. limii (∼90% of the initial population reached the N2 stage), compared with only ∼60% on L. indica × fauriei ‘Tuscarora’ (Fig. 1). As the male individual loses the capacity to feed after the P1 stage, the specific and sole role of the adult male is to facilitate the sexual reproduction of CMBS. Therefore, coinciding emergence of both sexes is essential for maintaining and increasing the population size. Overall, the males had shorter life spans and age-specific life expectancy than the females (Fig. 3), especially the populations on L. fauriei ‘Kiowa’ or L. limii, suggesting the effect of different hosts influenced the availability of adult males for mating.
Furthermore, the longevity of certain individuals, such as second instars (sex unknown) and females, is a significant contributor to the stages overlapping, leading to generations overlapping in the population development. For example, female individuals on L. fauriei ‘Kiowa’ started laying eggs as early as day 41 (Fig. 2), when the majority of the individuals within the population were still in the immature stages (N2). The longest lived females observed were 125, 125, 137, and 145 d old on L. fauriei ‘Kiowa’, L. indica × fauriei ‘Tuscarora’, L. limii, and the L. fauriei ‘Fantasy’ seedlings, respectively, which suggests that the coexistence of multiple generations could be expected under natural settings.
Although the effects of hosts could be manifested by varied reproduction in the development of insect population (El Aalaoui and Sbaghi 2022; Polat et al. 2008), our current results suggest that the different levels of CMBS infestation were due to factors other than the fecundity of the female individuals (such as nymphal survival rate and development durations). Studies have shown that the establishment of insect populations on different hosts can be primarily attributed by the mortality rate of individuals before sexual maturity (Hill et al. 2009; Nath and Rai 2010; Rout et al. 2018). For instance, Hill et al. (2009) reported that Hemiberlesia rapax (an armored scale insect) had a lower nymph survival rate on the resistant kiwifruit (Actinidia spp.) cultivars than the susceptible ones, while the fecundity of females did not show a difference.
Crapemyrtle aphid Tinocallis kahawaluokalani (Kirkaldy), another major sap-sucking pest on crapemyrtle, has been studied for the insect performance on different crapemyrtles (Alverson and Allen 1992; Herbert et al. 2009; Mizell and Knox 1993). Crapemyrtle aphid is host-specific to crapemyrtle and primarily feeds on the underside of the leaves compared with the polyphagous CMBS, which mainly feeds on the woody parts of the plant (Mizell and Knox 1993). The mean number of crapemyrtle aphids was found to be varied significantly across crapemyrtle cultivars and influenced by different plant features, including sizes (e.g., dwarf, medium, and tall types) and resistance levels to powdery mildew (Mizell and Knox 1993). Herbert et al. (2009) evaluated the host suitability of seven crapemyrtle cultivars for crapemyrtle aphids and found that while the total aphid fecundity differs among some cultivars with L. indica or L. indica × L. fauriei parentage, the daily fecundity of individuals did not show a difference, and the total fecundity was positively correlated with the adult longevity.
Notably, L. speciosa was reported to be an unsuitable host for crapemyrtle aphids, potentially due to the immature-stage insects’ rejection of tested leaves (Herbert et al. 2009). Lagerstroemia speciosa is also known as queen’s crapemyrtle with its distinct characteristics such as the large, leathery leaves and the overall robust growth that is different from crapemyrtle cultivars with L. indica or L. fauriei parentage (Pounders et al. 2007). Thus, the host suitability for sap-sucking insects could be related to the combination of factors, including host plant resistance traits and the nutritional quality of host plants, leading to the acceptance, rejection, survival, and longevity of immature nymphs as well as reproductive adults.
In our previous greenhouse feeding trials, we confirmed that L. speciosa is a host plant for CMBS, but it showed more resistance than all other tested crapemyrtle species and cultivars (Wu et al. 2021). Yet it was unclear how different plant features affect the performance of sap-sucking insects with their nutritional requirements at different developmental stages. Through an electrical penetration graph (EPG) system, we previously demonstrated the difference in the feeding behavior of CMBS on L. speciosa compared with other more susceptible crapemyrtle species and cultivars (Wu et al. 2022a). It was found that fewer individuals were able to access the phloem of L. speciosa. In general, CMBS spent more time trying to reach (probing) the phloem but less time ingesting the phloem sap on L. speciosa (Wu et al. 2022a). The difficulty for CMBS to access and ingest the phloem sap may be due to the existence of certain antinutritional factors. Studies have found that the levels of triterpenoids (Ashnagar et al. 2013), ellagic acids (Osawa et al. 1974), alkaloids (Kim et al. 2009; Watanabe et al. 2007), coumarins, and lignans (Dou et al. 2005) in the leaves differ among crapemyrtle cultivars. Huang et al. (2013) reported three unique compounds in L. speciosa leaves, including one ellagic acid derivative and two flavellagic acid derivatives, that were not previously found in the Lagerstroemia genus. In the future, crapemyrtle species and cultivars with different nutritional profiles can be evaluated in association with EPG-based technologies to monitor the feeding activities of different stage CMBS. The investigation of the stage-specific nutritional requirements of pest insects can thus help pinpoint successful host plant resistance tactics against CMBS attacks.
The effect of different rearing methods on the population dynamics.
In addition to feeding chamber experiments, CMBS rearing experiments on different crapemyrtle cultivars were conducted on small crapemyrtle liners to demonstrate the response of CMBS populations to different rearing methods in laboratory environments. The effects of different crapemyrtle hosts were noticeable, as CMBS populations responded differently to L. indica × fauriei ‘Natchez’, L. fauriei ‘Kiowa’, and L. indica ‘Dynamite’. Of 300 newly hatched crawlers (100 per plant) inoculated on the test crapemyrtle cultivars, 155, 211, and 47 crawlers were recorded during the first observation on L. indica × fauriei ‘Natchez’, L. fauriei ‘Kiowa’, and L. indica ‘Dynamite’, respectively. Thus, these recorded first instars were considered individual nymphs that successfully settled and started feeding (Table 4). The loss of crawlers might be due to the dispersion or mortality of insects during the early stages of colony establishment, which suggested the varied levels of antixenosis and antibiosis traits exhibited by tested hosts.
Intrinsic rate of increase (r), finite rate of increase (λ), net reproduction rate (Ro), and mean generation time (T) of Acanthococcus lagerstroemiae using group rearing method on Lagerstroemia indica × fauriei ‘Natchez’, L. fauriei ‘Kiowa’, L. indica ‘Dynamite’ crapemyrtle under laboratory conditions of 25 °C and 250 μmol·m−2·s−1 light with a photoperiod of 12:12 (light: dark).
According to the stage-specific survival curve, the first instar stage was the shortest on L. indica ‘Dynamite’, for ∼17 d. On the contrary, the first instar (N1) stage was much longer on L. fauriei ‘Kiowa’ and L. indica × fauriei ‘Natchez’, lasting up to 30 and 65 d, respectively (Fig. 4). With a lower number of crawlers established on L. indica ‘Dynamite’, a higher proportion (80%) of first instars reached the second instar (N2) stage, compared with L. fauriei ‘Kiowa’ and L. indica × fauriei ‘Natchez’. However, the number of surviving second instars decreased rapidly after the first month of the rearing experiment, and none of the second instars developed into the following stages, eventually causing the population to die out (Fig. 4). The poor insect performance suggested that L. indica ‘Dynamite’ exhibits potential resistance. However, it could not be concluded that L. indica ‘Dynamite’ has complete resistance, given the inoculation level (100 crawlers per plant) was relatively low compared with a natural setting, where it was reported that one CMBS female could produce up to 320 eggs under natural settings (Jiang and Xu 1998). Furthermore, our previous greenhouse feeding experiment showed that the inoculation of CMBS (using infected branches) could develop a relatively modest level of infestation (less than 100 gravid females per plant developed during a study period of 25 weeks) on L. indica ‘Dynamite’ (Wu et al. 2021). Further research would be required to investigate whether there is a ‘threshold’ number of CMBS that can successfully lead to the establishment of infestation on different plant hosts.
Age-stage specific survival rate (sxj) of Acanthococcus lagerstroemiae reared on (A) Lagerstroemia indica × fauriei ‘Natchez’, (B) L. fauriei ‘Kiowa’, and (C) L. indica ‘Dynamite’ under group-rearing conditions.
Citation: HortScience 58, 5; 10.21273/HORTSCI17009-22
Age-stage specific survival rate (sxj) of Acanthococcus lagerstroemiae reared on (A) Lagerstroemia indica × fauriei ‘Natchez’, (B) L. fauriei ‘Kiowa’, and (C) L. indica ‘Dynamite’ under group-rearing conditions.
Citation: HortScience 58, 5; 10.21273/HORTSCI17009-22
Age-stage specific survival rate (sxj) of Acanthococcus lagerstroemiae reared on (A) Lagerstroemia indica × fauriei ‘Natchez’, (B) L. fauriei ‘Kiowa’, and (C) L. indica ‘Dynamite’ under group-rearing conditions.
Citation: HortScience 58, 5; 10.21273/HORTSCI17009-22
On the basis of the life history and fecundity data, population parameters, including the intrinsic rate of increase (r), finite rate of increase (λ), net reproduction rate (Ro), and mean generation time (T) were obtained to evaluate the population dynamics of CMBS feeding on L. fauriei ‘Kiowa’ and L. indica × fauriei ‘Natchez’ (Table 4). Crapemyrtle bark scale performed better on L. fauriei ‘Kiowa’ and L. indica × fauriei ‘Natchez’, as both populations sustained longer, with adult individuals emerging and producing progenies (Fig. 4). However, only one population on L. indica × fauriei ‘Natchez’ (out of three) produced progenies, while all three populations on L. fauriei ‘Kiowa’ generated fecundity data. The lack of gravid females on L. indica × fauriei ‘Natchez’ suggests that it might be more difficult for CMBS to establish populations on L. indica × fauriei ‘Natchez’ compared with L. fauriei ‘Kiowa’. Moreover, the only L. indica × fauriei ‘Natchez’ population with fecundity data demonstrated a negative r and a λ of less than 1, indicating an overall decline in population size (Table 4). Although insect rearing using small plants/liners provided a more ‘naturalistic’ environment, CMBS populations did not perform better compared with insect rearing in the feeding chamber. Furthermore, the population parameters from L. fauriei ‘Kiowa’ populations indicated that CMBS performed worse on liners, with lower r, λ, and Ro, and longer T, compared with the population reared in feeding chambers (Tables 3 and 4).
Conclusion
In this study, detailed life history data of CMBS on different crapemyrtle hosts were collected and subjected to the age-stage, two-sex life table analysis to provide a comprehensive understanding of CMBS population development under laboratory conditions. Two insect-rearing methods included in this study successfully supported the development of CMBS as the insect was able to complete its life cycle under experimental conditions.
CMBS performance was recorded and evaluated through life table analysis. Of all tested crapemyrtle species or cultivars, the CMBS populations reared on L. indica ‘Dynamite’ showed worse performance as no individual survived to produce progenies. The results indicated the varied insect development, leading to colony establishment, was related to different levels of age-stage specific nymph survival and differentiated developmental durations. No significant difference was recorded for the fecundity among the reproductive adult females reared on different hosts in this study. However, future study is needed to further investigate the reproduction of CMBS females under more plant hosts and other environmental conditions. The ecological data of CMBS obtained in this study could aid field observations to project the insect population dynamics in the field and develop effective control and management strategies for CMBS.
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Total sales of crapemyrtles in 1998, 2009, 2014, and 2019.
Citation: HortScience 58, 5; 10.21273/HORTSCI17009-22
Total sales of crapemyrtles in 1998, 2009, 2014, and 2019.
Citation: HortScience 58, 5; 10.21273/HORTSCI17009-22
Total sales of crapemyrtles in 1998, 2009, 2014, and 2019.
Citation: HortScience 58, 5; 10.21273/HORTSCI17009-22
Example of one rooted crapemyrtle plant maintained in a crapemyrtle bark scale feeding chamber used in the insect rearing experiment.
Citation: HortScience 58, 5; 10.21273/HORTSCI17009-22
Example of one rooted crapemyrtle plant maintained in a crapemyrtle bark scale feeding chamber used in the insect rearing experiment.
Citation: HortScience 58, 5; 10.21273/HORTSCI17009-22
Example of one rooted crapemyrtle plant maintained in a crapemyrtle bark scale feeding chamber used in the insect rearing experiment.
Citation: HortScience 58, 5; 10.21273/HORTSCI17009-22
Example of one crapemyrtle plant (liner) used in crapemyrtle bark scale group-rearing experiment; the red arrows point to the detailed views under a dissecting microscope of specific sections of the same plant used in the insect-rearing experiment.
Citation: HortScience 58, 5; 10.21273/HORTSCI17009-22
Example of one crapemyrtle plant (liner) used in crapemyrtle bark scale group-rearing experiment; the red arrows point to the detailed views under a dissecting microscope of specific sections of the same plant used in the insect-rearing experiment.
Citation: HortScience 58, 5; 10.21273/HORTSCI17009-22
Example of one crapemyrtle plant (liner) used in crapemyrtle bark scale group-rearing experiment; the red arrows point to the detailed views under a dissecting microscope of specific sections of the same plant used in the insect-rearing experiment.
Citation: HortScience 58, 5; 10.21273/HORTSCI17009-22
Example of crapemyrtle bark scale group-rearing monitoring during a 1-month period showing insects at different developmental stages from 2 weeks after inoculation (WAI) to 4 WAI. images represent the views under a dissecting microscope when examining the insect development at the same area on a crapemyrtle plant over time.
Citation: HortScience 58, 5; 10.21273/HORTSCI17009-22
Example of crapemyrtle bark scale group-rearing monitoring during a 1-month period showing insects at different developmental stages from 2 weeks after inoculation (WAI) to 4 WAI. images represent the views under a dissecting microscope when examining the insect development at the same area on a crapemyrtle plant over time.
Citation: HortScience 58, 5; 10.21273/HORTSCI17009-22
Example of crapemyrtle bark scale group-rearing monitoring during a 1-month period showing insects at different developmental stages from 2 weeks after inoculation (WAI) to 4 WAI. images represent the views under a dissecting microscope when examining the insect development at the same area on a crapemyrtle plant over time.
Citation: HortScience 58, 5; 10.21273/HORTSCI17009-22
