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Article

Population Dynamics and Parasitism of the Kudzu Bug, Megacopta cribraria, by Egg Parasitoid, Paratelenomus saccharalis, in Southeastern USA

by
Worrel Diedrick
1,
Lambert H. B. Kanga
1,*,
Muhammad Haseeb
1,
Mrittunjai Srivastava
2 and
Jesusa C. Legaspi
3
1
Center for Biological Control, College of Agriculture and Food Sciences, Florida A&M University, 310 Perry Paige Building South, Tallahassee, FL 32307, USA
2
Florida Department of Agriculture and Consumer Services, Division of Plant Industry, 1911 SW 34th St., Gainesville, FL 32608, USA
3
United States Department of Agriculture—Agricultural Research Service—Center for Medical, Agricultural and Veterinary Entomology, 6383 Mahan Drive, Tallahassee, FL 32308, USA
*
Author to whom correspondence should be addressed.
Agriculture 2023, 13(1), 13; https://doi.org/10.3390/agriculture13010013
Submission received: 30 November 2022 / Revised: 12 December 2022 / Accepted: 14 December 2022 / Published: 21 December 2022
(This article belongs to the Special Issue Insect Ecology and Pest Management in Agriculture)
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Abstract

:
Megacopta cribraria (Fabricius) (Hemiptera: Plataspidae), commonly called the kudzu bug, is a pest of concern in many soybean and legume-producing states. It was first detected in the United States in 2009. In the southeastern United States, M. cribraria reduced crop yields by 47% in untreated soybean fields. Paratelenomus saccharalis (Dodd) (Hymenoptera: Platygastridae) is a known parasitoid of the kudzu bug, and a potential biological control agent. This study was comprised of three phases: (1) Preliminary assessment of the presence of the kudzu bug and its parasites in north Florida and south Georgia. (2) Measurements of the levels of parasitism in 12 sites selected from the preliminary evaluation to compare population dynamics in two growing seasons in agricultural, forested, and urban areas. (3) Laboratory studies to measure parasitism after 21 days in controlled environments. The preliminary assessment showed that in both 2016 and 2017, P. saccharalis emerged from eggs of M. cribraria collected in Leon and Gadsden County. Additionally, parasitism was recorded for the recently discovered egg parasitoid in north Florida, Ooencyrtus nezarae (Ishii) (Hymenoptera: Encyrtidae). In the assessment of parasitism in the field, differences were observed in the average level of parasitism within the urban and forest area in both years, and in the agricultural area for 2017. Between-group comparisons indicated significant differences between the average parasitism levels in agricultural, urban, and forested areas in 2016; in 2017, the differences between the areas were not significant. In the laboratory, after 21 days of observation, an average of 77.4% of freshly laid and 61.6% of cooled eggs were parasitized by P. saccharalis, and adult parasitoids emerged. There was a significant difference in the emergence of freshly laid eggs over cooled eggs. This study suggests that both P. saccharalis and O. nezarae exert some levels of natural control of the kudzu bug in the field and may be useful as biological control agents in an integrated pest management program.

1. Introduction

Megacopta cribraria (Fabricius) (Hemiptera: Plataspidae), commonly called the kudzu bug, is a pest of concern in many soybean (Glycine max [L.] Merr.; Fabales: Fabaceae) and legumes producing states [1]. This pest is a native of Asia and was first detected in the United States in 2009 [2]. It has a high reproductive potential and is capable of completing three generations per year [3,4]. Megacopta cribraria is known for its capability to reduce the biomass of kudzu [Pueraria montana var. lobata (Willd.)], its main host, by up to 33% [5]. However, in the southeastern United States, M. criberia, a phloem feeder, has been observed primarily on kudzu and soybean [6]. Heavy feeding by nymphs and adults on soybean leaves, petioles, and stems tends to weaken and stress plants, and could result to fewer pods, fewer seeds, and smaller seed size [7]. In addition, intensity of feeding of M. cribraria can reduce the assimilation of photoassimilates in legumes by defoliation and excess sooty mold growth on leaves [5]. In the southeastern United States, M. cribraria reduced crop yields in untreated fields from 0 to 47%, although the average yield loss was 18% [8,9]. In controlled experimental plots, yield losses reached 59.6% [7].
Three important families of egg parasitoids have been reported on M. cribraria in its native range: Platygastridae, Aphelinidae, and Encyrtidae [8]. The Aphelinidae are represented by older records from Malaysia, India, and Zaire [10] under the name Dirphys boswelli (Girault) (now Encarsia) [11]. Females of Ooencyrtus nezarae (Ishii) (Hymenoptera: Encyrtidae) and Paratelenomus saccharalis (Hymenoptera: Platygastridae) are commonly observed parasitizing eggs of M. cribraria [12]. Records of egg parasitism on M. cribraria were also reported from soybeans in other provinces of China (e.g., Jiangsu and Fujian) by both P. saccharalis and encyrtid species of Ooencyrtus (mainly O. nezarae Ishii). In those locations, parasitism was observed from May to October at levels ranging from 22.4% to 76.9% [8,13]. Ooencyrtus sp. is widely distributed in Korea, Japan, China, Brazil, and Thailand [14,15], and is also reported in North America [16].
Unlike P. saccharalis, O. nezarae parasitizes eggs of 13 hemipteran species [15], including Pentatomidae, Coreidae, and Alydidae [16]. Parasitism of M. cirbraria on kudzu and catnip (Nepeta cataria) by O. nezarae was first reported in Florida by Diedrick et al. [17] (Figure 1). In the United States, few studies have evaluated the level of parasitism of egg masses of the kudzu bug by this egg parasitoid [3,17,18]. Generally, egg parasitoids are good candidates for biological control of various stink bugs and have been used successfully in augmentation (the release of additional numbers of a natural enemy) and importation (the deliberate introduction of an exotic natural enemy) approaches [19,20].
This paper reports the population dynamics of the kudzu bug and its parasites in relation to precipitation in north Florida and South Georgia. Precipitation patterns, and how they are affected by climate change, will have profound effects on the population dynamics of both herbivorous insects and their natural enemies [21,22]. Parasitism of the recently discovered parasitoid in north Florida, O. nezarae, was compared to that of P. saccharalis, a known specialist of the Plataspidae. Additionally, we assessed the level of egg parasitism of P. saccharalis on M. cribraria in laboratory and field experiments, and compared parasitism of P. saccharalis against Ooencyrtus nezarae, which was found in a forested site at the end of the second year of these studies.

2. Materials and Methods

2.1. Preliminary Evaluation of the Distribution on P. saccharalis in North Florida and South Georgia

Eggs of M. cribraria were collected biweekly in the field from 23 March to 25 September 2016, and from 27 March to 13 August 2017, in four counties: Leon, Gadsden, and Jefferson counties in north Florida, and Grady County in south Georgia. The egg masses were attached predominantly to shoot tips or leaves of host plants. Eggs masses on foliage were gathered from urban, forested, and agricultural areas at different sites in each county. The collected egg masses were placed in plastic containers (15.24 cm × 15.24 cm) with ventilated covers, then put in a cooler with ice packs and transported to the laboratory of the Center for Biological Control (CBC), Florida Agricultural and Mechanical University (FAMU). The plastic containers were placed in rearing cages (60 cm × 60 cm × 60 cm, Bug Dorm II, BioQuip Products) and kept at ambient temperature (27 ± 1 °C) until the emergence of kudzu bugs or their parasitoids. The M. cribraria eggs were observed for emergent adults of P. saccharalis for up to 21 days, a period based on data of [23]. Prevalence was expressed as a binary variable in a yes/no format based on whether or not the eggs were parasitized by P. saccharalis. Precipitation and temperature data were obtained from US Climate Data 2022 (version 3.0) by US Climate Data.

2.2. Assessment of Parasitism in the Field

From the areas surveyed for the presence of P. saccharalis in the preliminary evaluation, 12 sites were selected to assess the parasitism level of P. saccharalis on M. cribraria (Figure 1). Twenty-five plants were marked at each site in the urban, forested, and agricultural areas. This resulted in five replications per site. All replications were marked with flags so that the same plants could be followed during the season. The host plants were kudzu and soybean in the agricultural area, and kudzu in the forested and urban area. For soybean, five adjacent host plants were chosen for monitoring; for kudzu, five plant areas of 929 cm2 (1 sq ft) each were delimited using a quadrant assembled with 4 sections of 30.48 cm polyvinyl chloride (PVC) pipes.
Egg masses of M. cribraria from all marked plants were collected and counted. All adults and nymphs of M. cribraria observed were also counted. The egg masses were transported to the CBC laboratory as previously described. In the laboratory, the number of eggs were counted using an Olympus stereoscope. Individual egg masses were then placed in separate glass vials (1.7 cm × 6 cm), capped with absorbent cotton, and placed in observation cages (30 cm × 30 cm × 30 cm, BugDorm I, BioQuip Products) at a temperature of 27–28 °C with 70–80% relative humidity on a 12:12 h L:D photoperiod. The M. cribraria egg masses were examined daily for 21 days for evidence of parasitism. Mainali et al. [24] in their study held Riptortus pedestris (F.) (Hemiptera: Alydidae) eggs parasitized by Ooencyrtus at 26.6 °C, 75% relative humidity, and a 16:8 h L:D photoperiod for 16 days before emergence and servers as a reference point for the duration of time M. cribraria parasitized eggs were observed for in this study. Adult P. saccharalis that emerged or failed to emerge were counted and the parasitism level was expressed as the percentage of eggs parasitized relative to the total number of eggs.
For the comparison of Paratelenomus and Ooencyrtus, a plot was selected where unusual levels of egg masses were present, but this plot was separate from all marked plots. In July and August 2017, fresh egg masses without visible evidence of parasitism were collected from this kudzu plot. Eggs were cultured as described previously.

2.3. Assessment of Parasitism in the Laboratory

Kudzu vines with roots attached, but without kudzu bugs or their eggs, were collected from the field and grown in the laboratory in quart mason jars using a solution of 30 mL of liquid fertilizer (Alaska Pure Kelp Plant Food, 0.13-0-0.06 concentrate) and 3.8 L of water. Two mason jars were placed in each of four rearing cages. Adult M. cribraria were collected from the field and transported to the CBC laboratory. In the laboratory, the adults were transferred into larger rearing cages (BugDorm II) containing the live kudzu vines. The vines were examined daily for the presence of kudzu bug egg masses. Newly laid M. cribraria egg masses were collected, starting one day after establishment. After counting the freshly laid M. cribraria eggs in each egg mass, the eggs were placed in glass vials (1.7 cm × 6 cm) with P. saccharalis adults at a ratio of two females to one male. The glass vials were then plugged with absorbent cotton moist with honey solution (1-part honey to 2-parts of tap water) to provide nourishment for the wasps. The glass vials were observed for parasitism up to 21 days. The parasitism level was expressed as the percentage of adult P. saccharalis that emerged relative to the number of eggs. Parasitized eggs that did not hatch were also counted.
In order to continue to culture P. saccharalis in winter where no eggs were available, we experimented with storing eggs of M. cribraria at low temperatures [24]. Some freshly laid M. cribraria egg masses collected from the field in spring 2016 were taken to the CBC laboratory and stored in a fridge (temperature of 2 ℃) for five months [24]. Those eggs were thawed and exposed to adult P. saccharalis in the laboratory following the same method used for the newly laid M. cribraria egg masses. Parasitism level was assessed up to 21 days.

2.4. Statistical Analysis

The percentage of M. cribraria eggs parasitized by P. saccharalis was subjected to an ANOVA PROC Mixed statistical test [25]. Treatments were modelled as fixed effects; site-by-parasitoid interactions were modeled as random effects. A Tukey’s studentized range test [25] was used to compare the means of parasitism between treatment groups. The data were arcsine transformed to satisfy the assumption of normality before analysis. The means of the percentage of M. cribraria eggs parasitized in each treatment were used to compare successful emergence of parasites and unhatched eggs using Tukey’s studentized range test [25]. A significance level of 0.05 was used for all statistical tests.

3. Results

3.1. Preliminary Evaluation of Distribution on P. saccharalis in North Florida and South Georgia

In both 2016 and 2017, P. saccharalis emerged from eggs of M. cribraria collected in Leon and Gadsden County (Table 1). In Leon County for the year 2016, the parasitoid was reared from eggs in the urban area, whereas in 2017 it was seen from eggs gathered from both agricultural and urban areas. In Gadsden County, the agricultural and forested areas were monitored in 2017 and both P. saccharalis and Ooencyrtus sp. Were reared from M. cribraria eggs; in the forested area, P. saccharalis was present in both years. Host plants in agricultural sites were soybeans or kudzu growing near soybeans. All hosts in urban and forest sites were kudzu, except for the occasional presence of catnip (Nepeta cataria L. (Lamiales: Lamiaceae), which also hosted kudzu bugs and their egg masses, and some of these were parasitized by P. saccharalis.

3.2. Assessment of Parasitism in the Field

For all 12 sites studied, a total of 3804 parasitized eggs were recovered from 21,056 eggs collected (15.2% in 2016 and 16.9% in 2017). Paratelenomus saccharalis was found at only six sites in two counties. No parasitoids were found in Jefferson County, Florida, or Grady County, Georgia (Table 1). For sites with P. saccharalis, the average parasitism in 2016 varied from approximately 7% to 37% with the lowest level (7.4%) seen in the forested site in Gadsden County and the highest level (37.4%) in an urban site in Leon County (Table 2). The forested site was south of Quincy in Gadsden County; population dynamics there recorded two peaks of M. cribraria egg deposition (Figure 2: 204 eggs in May and 281 eggs in July). Similarly, the most active urban site in Leon County also had two peaks of egg deposition (Figure 3: 504 eggs in May and 428 eggs in August). In contrast, the most active agricultural site located at the USDA-ARS soybean research field (Leon County) recorded a single peak of M. cribraria egg deposition (Figure 4: 130 eggs in August). For 2016 and 2017 study period, it was observed on the graphs (Figure 2, Figure 3, Figure 4, Figure 5, Figure 6 and Figure 7) that there were two peaks in parasitism in urban and forested areas where kudzu vine was the host crop and a single peak in agricultural area where soybean was the host crop. The first peak of parasitism in the nonagricultural areas coincide with the vigorous growth of kudzu vines right after the winter.
Differences were observed in the average level of parasitism within the urban and forest area in both years, and in the agricultural area for 2017 (Table 2). In 2017, the lowest level of parasitism (8.8%) was recorded at another urban site in Leon County, whereas the highest level (61.4%) was found at the USDA-ARS agricultural research site in Leon County (Table 2). As in 2016, population dynamics in 2017 for the most active urban and forested sites (Figure 5 and Figure 7) showed two peaks of M. cribraria egg deposition: 338 eggs in April and 446 eggs in June, and 164 eggs in May and 123 eggs in August, respectively. Population dynamics for the USDA-ARS agricultural site in Leon County showed a unimodal pattern similar to that of 2016 (Figure 6: one peak of 138 eggs in July).
Between-group comparisons indicated significant differences (F = 13.77; df = 2, 52; p < 0.0001) between the average parasitism levels in agricultural, urban, and forested areas in 2016; in 2017, the differences between areas were not significant (F = 1.96; df = 2, 52; p = 0.1566). The total level of parasitism for all sites increased from 8.02% in 2016 to 14.56% in 2017 (Figure 8), and the between-year difference was significant (F = 3.80; df = 1108; p = 0.0537).
Results summarized above (Table 3, Figure 8) compare the four-county study region. Levels of parasitism may also be expressed for only the sites where P. saccharalis was present. Parasitism at these sites over two years averaged 29.1%. Considering only parasitized egg masses, the rate of parasitism varied from 27.8–100% with an average of 70% for both years (71% in 2016, 69% in 2017). Data from the preliminary study of dual parasitism by P. saccharalis and O. nezarae are summarized in Table 4. These results are from a plot adjacent to the field plots. All egg masses were parasitized, and many eggs were parasitized by both species.
In 2016, precipitation was broadly bimodal throughout all habitats, with a first peak in March and April followed by a decline in May and a second prolonged increase from July to November. In 2017, a single peak occurred in May to July in all habitats. Precipitation was focused on more than temperature in this population dynamics study since the result of increased precipitation over time can influence vigorous growth in host plants. New growth in host plants encourages kudzu bug egg deposition. Conversely, the impact of precipitation on the kudzu bug population can be negative. Precipitation can wash away nymphs, and increased moisture in the field encourages the growth of entomopathogens which will result in population reduction. Average minimum temperature did not differ much throughout the season (Figure 2, Figure 3, Figure 4, Figure 5, Figure 6 and Figure 7).

3.3. Assessment of Parasitism in the Laboratory

In laboratory experiments, 911 freshly laid eggs were compared with 349 M. cribraria eggs, which had been cooled for five months (Table 5). They were isolated and offered to predators to determine the level of parasitism in the absence of environmental factors and competing predators. After 21 days of observation, an average of 77.4% of freshly laid and 61.6% of cooled eggs were parasitized by P. saccharalis and an adult wasp emerged. There was a significant difference (F = 5.16; df = 1, 60; p >0.0268) in emergence of freshly laid eggs over cooled eggs (Table 5).

4. Discussion

The presence of the wasp P. saccharalis was confirmed in north Florida and, unexpectedly, Ooencyrtus sp. was also discovered. This is the first record from Florida, but Ooencyrtus sp. Has been found in Virginia in 2015 [26]. From March to September of 2016 and March to August of 2017, P. saccharalis was reared from eggs of M. cribraria in two of four counties studied and in three environmental areas: urban, forest, and agricultural. The habitat diversity of this wasp parasitizing kudzu bug eggs has been documented in many parts of the world, including the United States [26,27,28].
Hoshino et al. [27] investigated seasonal occurrence of the wasp in Japan in urban areas of Fukuoka and Tokyo where P. saccharalis coexists on kudzu bug eggs with the generalist parasitoid Ooencyrtus nezarae. Based on research in Japan [27], the two parasitoids can occur on the same host together, however, some seasonal separation was observed, as P. saccharalis was found earlier in the season. When both species occurred together, the only measurable effect of this coexistence was an increase in the relative number of male O. nezarae, but more studies on their interactions are needed [27]. Nothing is known concerning the importance or interactions of the two parasitoids in Florida.
This appears to be the first record of the adult kudzu bug on catnip; however, this study did not follow growth on catnip to determine if the kudzu bug could complete its life cycle on this host, and only eggs and first instar nymphs were observed. Paratelenomus saccharalis did parasitize those available kudzu bug eggs deposited on catnip. Catnip may be an incidental record, as we observed that the kudzu bug seems to deposit its eggs on any available surface. Egg masses were observed on dry twigs and catnip in the field and on the sides of rearing cages in the laboratory.
In the field evaluation of M. cribraria egg masses, significant differences were found in M. cribraria egg parasitism by P. saccharalis within sites of collection for both years (Table 2). Parasitism was highest within urban sites in 2016 and this could be a result of favorable weather conditions for the kudzu plants in early spring. This contributes to robust growth for the host plant, and healthy plants attract M. cribraria. In 2017, one of the urban sites was destroyed, and the other sites had a reduced level of parasitism in that year. Agricultural sites for 2017 recorded levels of parasitism up to 61.40% from no parasitism in 2016.
Variability in the level of parasitism was also seen in many studies in different environments where the kudzu vine is prevalent. High levels of parasitism were seen on kudzu in Japan where the average parasitism for M. cribraria eggs by P. saccharalis varied from 57–81% [29]. In Georgia, Gardner et al. [17] reported 47.5% parasitism on kudzu bug egg masses collected in DeKalb County. On another leguminous host, Bin and Colazza [30] recorded an average range of parasitism by P. saccharalis of 4.5–34.2%.
There was also a significant difference in the average level of parasitism between the agricultural, urban, and forested areas in 2016, although there was no difference in the mean rate of parasitism between these areas in 2017 (Table 3). Parasitism increased in the agricultural areas from 0% in 2016 to 21.7% (±6.0%) in 2017. Forest areas also experienced an increase from 2.5% (±1.5%) to 11.7% (±4.6%) in 2016 and 2017, respectively. Zhang et al. [5] reported that the number of M. cribraria egg masses in different seasons may also affect the rate of parasitism. The single peak in soybean parasitism may have been related to its late May planting season. Kudzu vines would be available in mid-April while soybeans would not be available for invasion until June, which would coincide with the second peak of egg population on kudzu. The fungus Beauveria bassiana was also observed at the agricultural site (USDA-ARS) infecting and killing all stages of kudzu bugs in 2016 (Diedrick, unpublished data).
In July and August of 2017, Ooencyrtus nezarae were reared with P. saccharalis from M. cribraria egg masses. The parasitism of kudzu bug egg masses by these two egg parasitoid species has been reported in many studies where the two were found competing with each other [8,26]. Although 100% of egg masses contained parasites, only 61% of eggs were actually parasitized (Table 4). The ratio of Ooencyrtus was higher in July than in August which differs from results in Japan [27]. The work by Ademokoya et al. [16] did not compare populations, but it seems clear that the Alabama and Florida populations are not as established as those in Asia, and it will be interesting to follow the coexistence of the two parasitoids. While Ooencyrtus parasitizing kudzu bugs represents one more possible biological control agent, it is a generalist predator, and more research is needed to evaluate its importance in Florida.
In order to maintain a population of P. saccharalis over winter, we tried to see if cultures of M. cribraria eggs could be kept long term by freezing eggs in the summer and thawing them later. A second evaluation of parasitism of kudzu bug eggs under controlled conditions, using both fresh and cooled eggs, revealed a significantly poorer emergence rate of P. saccharalis on cooled eggs compared to fresh eggs (Table 5). However, numbers were sufficient to maintain the culture during periods when freshly laid M. cribraria eggs were not available.
The egg parasitoid Paratelenomus saccharalis is established in the state of Florida. This parasitoid of Megacopta cribraria was confirmed in Leon and Gadsden counties after previously being found in Alachua County, where it is no longer present; however, it was not found in adjacent areas in Jefferson County. In 2016, P. saccharalis was found in three urban sites in Leon County (Mahan Dr., Eugenia St., and Tom Brown Park) and one forested site in Gadsden County (south of Quincy); in 2017, its distribution also included two sites in agricultural areas (USDA-ARS in Leon County and UF-NFREC in Gadsden County).
The kudzu bug was first found in Georgia in 2009 and reached Florida three years later. Paratelenomus saccharalis was first recorded in Georgia, Alabama, and Mississippi in 2013 [31], and in 2014 in Florida [28]. Paratelenomus saccharalis has not been found in Georgia since 2015, and it was not found at sites in Grady County, Georgia, in this survey. However, the kudzu bug population significantly declined in Georgia [31] between the years 2013 and 2016. The decline was initially attributed to P. saccharalis and later to the fungus Beauveria bassiana [31]. Populations of P. saccharalis also declined, presumably because of unusually cold winters [31].
In this study, the levels of parasitism of egg masses of the kudzu bug by the parasitoids varied across sites, areas, and counties, and over the study period. Paratelenomus saccharalis is specific to the family Plataspidae and thus host-specific to M. cribraria. In 2017, we also found a second egg parasitoid of the kudzu bug, Ooencyrtus nezarae. The survival of this recently discovered generalist parasitoid may be affected by high and low temperatures [32], but the ability of Ooencyrtus to find alternate hosts may make it easier to maintain a population of natural biocontrol agents against kudzu bugs in the future. In addition to Georgia, seven other states have closely followed the population of the kudzu bug on soybean since 2011 [33,34]. The population has declined in states where it was initially found (North Carolina, then Alabama) but populations are increasing in Mississippi, Tennessee, and now in two of three other states (Arkansas and Louisiana). Although reported in Virginia, it has not yet affected the soybean crop [34,35] where it is being closely monitored.
Agricultural regions carefully monitor invasive species and apply insecticides when needed following extension recommendations, so it appears that the integrated pest management approach is slowly reducing kudzu bug populations in soybean fields. This decline is also due at least in part to natural enemies (parasitoids and fungi). Control of kudzu bugs in urban areas is dependent on the management of kudzu by individual property managers; the heaviest kudzu bug infestations in this study were not on well-kept property. Both the total number of kudzu bug eggs and the parasitoid population density declined over the two years of the study, but not at all sites. Geographically, the population may be in decline in parallel with Florida’s close neighbors Georgia and Alabama. However, our study was limited to only four counties, mainly in northern Florida and southern Georgia. Therefore, more research is needed to confirm any decline; to continue exploring the characteristics and behavior of the parasitoid in other counties, and eventually in other states where the parasitoid is prevalent.

5. Conclusions

This study suggests that both P. saccharalis and O. nezarae exert some levels of natural control of the kudzu bug in the field and may be useful as biological control agents in an integrated pest management program. This new knowledge on the parasitism level and population dynamics of the kudzu bug in north Florida can enhance management programs to better manage this invasive pest while protecting natural enemies.

Author Contributions

Conceptualization, W.D., L.H.B.K., M.H., M.S. and J.C.L.; methodology, W.D.; formal analysis, W.D. and L.H.B.K.; writing—original draft preparation, W.D. and L.H.B.K.; writing—review and editing, W.D., L.H.B.K., M.H., M.S. and J.C.L.; supervision, L.H.B.K.; funding acquisition, L.H.B.K. All authors have read and agreed to the published version of the manuscript.

Funding

We thank the United States Department of Agriculture (USDA)-Animal Plant Health Inspection Service (APHIS) for financial support.

Institutional Review Board Statement

N/A.

Informed Consent Statement

N/A.

Data Availability Statement

Data available with senior and corresponding authors.

Acknowledgments

We are grateful for the overall support of the Center for Biological Control-College of Agriculture and Food Science (CAFS), Florida A&M University (FAMU), Tallahassee, Florida. We thank Division of Plant Industry (DPI)-Florida Department of Agriculture and Consumer Services (FDACS)], Gainesville, Florida, for assistance in parasitoid identification. Special thanks to Janice Peters (FAMU-CAFS) for her assistance throughout the project. Neil Miller (UDA-ARS-Center for Medical, Agricultural and Veterinary Entomology), Danielle Wolaver (DPI-FDACS), Rodrigue Pierre (FAMU-CAFS), and Andrew Merwin (Florida State University) provided technical assistance. We are grateful to Manuel Pescador (FAMU-CAFS) for his helpful review of the manuscript. This article presents the results of research only. The use of trade, firm, or corporation names in this publication is for the information and convenience of the reader. Such use does not constitute an official endorsement or approval by the United States Department of Agriculture or the Agricultural Research Service of any product or service to the exclusion of others that may be suitable.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Map showing monitoring sites for Paratelenomus saccharalis in north Florida and south Georgia, 2016 and 2017.
Figure 1. Map showing monitoring sites for Paratelenomus saccharalis in north Florida and south Georgia, 2016 and 2017.
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Figure 2. Population dynamics of M. cribraria and P. saccharalis for most active forested site in 2016. Host plant: kudzu.
Figure 2. Population dynamics of M. cribraria and P. saccharalis for most active forested site in 2016. Host plant: kudzu.
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Figure 3. Population dynamics of M. cribraria and P. saccharalis for most active urban site in 2016. Host plant: kudzu.
Figure 3. Population dynamics of M. cribraria and P. saccharalis for most active urban site in 2016. Host plant: kudzu.
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Figure 4. Population dynamics of M. cribraria and P. saccharalis for most active agricultural site in 2016. Host plant: soybean.
Figure 4. Population dynamics of M. cribraria and P. saccharalis for most active agricultural site in 2016. Host plant: soybean.
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Figure 5. Population dynamics of M. cribraria and P. saccharalis for most active forested site in 2017. Host plants: Pueraria montana (kudzu).
Figure 5. Population dynamics of M. cribraria and P. saccharalis for most active forested site in 2017. Host plants: Pueraria montana (kudzu).
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Figure 6. Population dynamics of M. cribraria and P. saccharalis for most active urban site in 2017. Host plant: Pueraria montana (kudzu).
Figure 6. Population dynamics of M. cribraria and P. saccharalis for most active urban site in 2017. Host plant: Pueraria montana (kudzu).
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Figure 7. Population dynamics of M. cribraria and P. saccharalis for most active agricultural site 2017. Host plant: soybean.
Figure 7. Population dynamics of M. cribraria and P. saccharalis for most active agricultural site 2017. Host plant: soybean.
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Figure 8. Total egg parasitism by P. saccharalis on M. cribraria in the three areas (urban, forest, and agricultural) compared by year. Different letters above the bar indicates significant difference between the years, Tukey’s Studentized Range, p < 0.05).
Figure 8. Total egg parasitism by P. saccharalis on M. cribraria in the three areas (urban, forest, and agricultural) compared by year. Different letters above the bar indicates significant difference between the years, Tukey’s Studentized Range, p < 0.05).
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Table
Table 1. Average number of eggs of M. cribraria and presence of P. saccharalis (P. s.) in urban, forested, and agricultural areas in Leon, Gadsden, Jefferson, and Grady Counties.
Table 1. Average number of eggs of M. cribraria and presence of P. saccharalis (P. s.) in urban, forested, and agricultural areas in Leon, Gadsden, Jefferson, and Grady Counties.
. 20162017
CountiesM. cribraria EggsP. s.M. cribraria EggsP. s.
Sitesmean ± SE Sitesmean ± SE
Urban areas
Leon4401.2 ± 57.2Yes3252.6 ± 38.8Yes
Grady1365.0 ± 47.5No1137.4 ± 12.1No
Forest areas
Gadsden1226.2 ± 22.4Yes1126.2 ± 16.8Yes
Grady283.6 ± 24.0No2107.6 ± 9.8No
Agriculture areas
Leon179.4 ± 23.1No178.4 ± 2.2Yes
Gadsden0- 1207.6 ± 21.7Yes
Jefferson136.2 ± 13.7No189.0 ± 33.4No
Grady 138.2 ± 13.5No182.6 ± 19.0No
Table
Table 2. Within-area comparison of M. cribraria eggs parasitized by P saccharalis in 2016 and 2017. Parasitism expressed as a percentage. Within each column, means followed by common letters are not significantly different (Tukey’s Studentized Range; p < 0.05).
Table 2. Within-area comparison of M. cribraria eggs parasitized by P saccharalis in 2016 and 2017. Parasitism expressed as a percentage. Within each column, means followed by common letters are not significantly different (Tukey’s Studentized Range; p < 0.05).
AreasSites% Parasitism (Mean ± SE)
20162017
6a. Urban
 Leon123.40 ± 3.40 a- a
 Leon220.00 ± 7.49 a8.80 ± 2.60 b
 Leon300.00 ± 0.00 c00.00 ± 0.00 c
 Leon437.40 ± 4.16 a29.8 ± 3.72 a
Grady500.00 ± 0.00 c00.00 ± 0.00 c
6b. Forested
 Gadsden67.40 ± 3.94 a35.00 ± 3.94 a
 Grady700.00 ± 0.00 c00.00 ± 0.00 c
Grady800.00 ± 0.00 c 00.00 ± 0.00 c
6c. Agricultural
 Leon900.00 ± 0.00 c61.40 ± 5.01 a
 Gadsden10- b25.20 ± 4.50 b
 Jefferson1100.00 ± 0.00 c00.00 ± 0.00 c
Grady1200.00 ± 0.00 c00.00 ± 0.00 c
a Site 1 kudzu patch was cleared in early 2017. b Site 10 not collected in 2016.
Table
Table 3. Between area comparison of M. cribraria egg parasitized by P saccharalis in 2016 and 2017. Within each column, means followed by common letters are not significantly different (Tukey’s Studentized Range; p < 0.05).
Table 3. Between area comparison of M. cribraria egg parasitized by P saccharalis in 2016 and 2017. Within each column, means followed by common letters are not significantly different (Tukey’s Studentized Range; p < 0.05).
AreasPercentage Parasitism (Mean ± SE)
Sites2016Sites2017
Urban516.16 ± 3.39 a49.65 ± 2.98 b
Forest32.47 ± 1.54 c 311.67 ± 4.59 b
Agriculture30 ± 0 c421.65 ± 5.97 b
No.: represent number of replications per area.
Table
Table 4. Comparison of parasitism of egg masses and eggs from sites with both P. saccharalis (P.s.) and Ooencyrtus nezarae (O.n.) in 2017.
Table 4. Comparison of parasitism of egg masses and eggs from sites with both P. saccharalis (P.s.) and Ooencyrtus nezarae (O.n.) in 2017.
.Egg Masses of M. cribrariaEggs of M. cribrariaRatio
P.s./O.n.
Parasitized by Parasitized by
DateNo.P.s.O.n.BothNo.P.s.O.n.
3 July20023313151:1
18 July3111545261:5
8 August3201472483:1
13 August732316269233:1
Total15637296111728:8
Parasitized40%13%47% 37%24%
Table
Table 5. Comparison of emergence of P. saccharalis (P.s.) from freshly laid eggs and cooled eggs of M. cribraria in laboratory experiments.
Table 5. Comparison of emergence of P. saccharalis (P.s.) from freshly laid eggs and cooled eggs of M. cribraria in laboratory experiments.
Experiment.No. EggNo.Eggs per MassP.s. Emerged
MassesEggsMean + SENo.Mean ± SE
Fresh eggs4591120.2 ± 1.07050.81 ± 0.03 a
Cooled eggs 1734920.5 ± 1.22150.67 ± 0.07 b
a and b means there was a significance difference between the two groups.
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Diedrick, W.; Kanga, L.H.B.; Haseeb, M.; Srivastava, M.; Legaspi, J.C. Population Dynamics and Parasitism of the Kudzu Bug, Megacopta cribraria, by Egg Parasitoid, Paratelenomus saccharalis, in Southeastern USA. Agriculture 2023, 13, 13. https://doi.org/10.3390/agriculture13010013

AMA Style

Diedrick W, Kanga LHB, Haseeb M, Srivastava M, Legaspi JC. Population Dynamics and Parasitism of the Kudzu Bug, Megacopta cribraria, by Egg Parasitoid, Paratelenomus saccharalis, in Southeastern USA. Agriculture. 2023; 13(1):13. https://doi.org/10.3390/agriculture13010013

Chicago/Turabian Style

Diedrick, Worrel, Lambert H. B. Kanga, Muhammad Haseeb, Mrittunjai Srivastava, and Jesusa C. Legaspi. 2023. "Population Dynamics and Parasitism of the Kudzu Bug, Megacopta cribraria, by Egg Parasitoid, Paratelenomus saccharalis, in Southeastern USA" Agriculture 13, no. 1: 13. https://doi.org/10.3390/agriculture13010013

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