Next Article in Journal
Negative Contrast: A Simple and Efficient Image Augmentation Method in Crop Disease Classification
Next Article in Special Issue
Seasonal Dynamics of the Brown Marmorated Stink Bug, Halyomorpha halys (Hemiptera: Pentatomidae), in Apple Orchards of Western Slovenia Using Two Trap Types
Previous Article in Journal
National Agricultural Science and Technology Parks in China: Distribution Characteristics, Innovation Efficiency, and Influencing Factors
Previous Article in Special Issue
Down-Regulation of Strigolactone Biosynthesis Gene D17 Alters the VOC Content and Increases Sogatella furcifera Infectivity in Rice
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Agriculture
Volume 13
Issue 7
10.3390/agriculture13071460
agriculture-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Seasonal Abundance of Various Hymenopteran Parasitoids of Leafminers in Beans and Comparative Abundance in Bean, Tomato, and Squash

by
Dakshina R. Seal
1,*,
Oscar Liburd
2 and
Jian Li
3
1
Tropical Research and Education Center, University of Florida-IFAS, Homestead, FL 33033, USA
2
Entomology and Nematology Department, University of Florida-IFAS, Gainesville, FL 32603, USA
3
Independent Researcher, 1828 SW 63RD AVE, Gainesville, FL 32608, USA
*
Author to whom correspondence should be addressed.
Agriculture 2023, 13(7), 1460; https://doi.org/10.3390/agriculture13071460
Submission received: 26 May 2023 / Revised: 15 July 2023 / Accepted: 18 July 2023 / Published: 24 July 2023
(This article belongs to the Special Issue Advances in Integrated Pest Management Strategies)
Browse Figures
Review Reports Versions Notes

Abstract

:

Simple Summary

Vegetable leafminer, Liriomyza trifolii (Burgess) is a common pest of almost all vegetable crops grown in Florida, USA. Leafminer infestation begins as soon as vegetable seedlings are above the ground. Growers start using insecticides of various chemical classes to control leafminer. They continue insecticide sprays until 2–3 weeks before harvesting crops. This practice of using insecticides deleteriously affects our biotic and abiotic environments. In our four-years research study, we recorded thirteen species of hymenopteran parasitoids of L. trifolii belonging to three families: Braconidae, Eulophidae, and Pteromalidae. Among all parasitoids, Opius, Euopius, Diglyphus, and Diaulinopsis were the predominant ones on beans and other vegetables. Their peak abundance occurred in November–January while most vegetable crops are in their peak growing stage. This study also investigated the preference of parasitoids for the three major vegetable crops: bean, squash, and tomato planted in randomized complete block design in field plots. This information could be of great benefit in developing an IPM of vegetable leafminers balancing biocontrol agents and insecticide application.

Abstract

The composition and seasonal abundance of hymenopteran parasitoids of Liriomyza trifolii (Burgess) was investigated on snap bean (Phaseolus vulgaris L.), tomato (Solanum lycopersicum L.), and squash (Cucurbita pepo L. ‘Enterprise’) from 2010 to 2016 in South Florida in two studies. In the first study (2010–2016), 13 species of parasitoids were collected from the snap bean crop. Opius dissitus Muesebeck (Braconidae) was the most abundant parasitoid throughout the study period from September 2010 to February 2016. Diaulinopsis callichroma Crawford (Eulophidae) was the second most abundant parasitoid on bean in 2010, 2012, 2014, and 2016. Other parasitoids included Euopius sp. (Braconidae)., Diglyphus begini (Ashmead), D. intermedius (Girault), D. isaea (Walker), Neochrysocharis sp., Closterocerus sp., Chrysocharis sp., Zagrammosoma lineaticeps (Girault), Z. muitilineatum (Ashmead), Pnigalio sp. (all Eulophidae), and Halticoptera sp. (Pteromalidae). In the second study on the comparative abundance of parasitoids in three crops conducted in 2014 and 2016 using bean (Phaseolus vulgaris L., tomato (Solanum lycopersicum L.) and squash (Cucurbita pepo L.) arranged in a randomized complete block design, bean attracted more parasitoids than tomato and squash irrespective of parasitoid species and years. This information will help in devising a biocontrol-based integrated program for managing leafminers in beans and other vegetable crops.

1. Introduction

South Florida is a major vegetable production area in the USA, ranking first in the value of fresh market snap bean and cucumber production and second in squash and tomato production [1]. Various insect pests including sweet potato whitefly (Bemisia tabaci Biotype B or MEAM1) (Hemiptera: Aleyrodidae), thrips of various species (Thysanoptera: Thripidae), aphids (Homoptera: Aphididae), cucumber beetle (Diabrotica spp., Coleoptera: Chrysomelidae), armyworms (Spodoptera frugiperda (J.E. Smith, Lepidoptera: Noctuidae), and leafminers (Diptera: Agromyzidae) infest these vegetable crops and cause economic damage. Among the insect pests, the leafminers (Liriomyza spp.), comprising of more than 300 spp., have a significant economic impact on vegetable production worldwide [2,3]. Yield losses may account for >70% in snap bean and potato [4]. Leafminers, Liriomyza trifolii (Burgess), L. sativae (Riley), and L. huidobrensis (Blanchard) are important in threatening US agriculture [5,6,7,8]. Among leafminers, L. trifolii has a broad host range consisting of about 400 species of plants [6,9] and poses a serious threat to global agriculture [10]. Commercial growers use broad spectrum insecticides as a primary means for controlling Liriomyza leafminers [11,12]. As the development of leafminers takes place inside leaf-mines, most of these insecticides only target the adult fly and fail to provide effective control against other life stages. The ultimate result of widespread and intensive use of insecticides has a high potential for developing leafminer resistance against these insecticides [13,14]. Most importantly, the use of insecticides decimates potential natural enemies of leafminers and causes an outbreak of leafminer abundance [13,15].
Hymenopteran parasitoids possess potentials in suppressing initial populations of leafminers [6]. Noyes [16] reported about 300 species of parasitoids that attack agromyzid leafminers, and about 80 of them were listed to parasitize larvae of Liriomyza species. Stegmaier [17] recorded 31 species of hymenopteran parasitoids in 19 genera and five families that parasitize agromyzid leafminers in South Florida. Many of these species in Braconidae and Eulophidae are potential parasitoids of agromyzid leafminers [3]. Several regional reviews on leafminer parasitoids in Asia include Petcharat et al. [18], Xu et al. [19], Zhu et al. [20]. Neochrysocharis formosa (Westwooe) (Hymenoptera: Eulophidae) is a larval endoparasitoid and has been used to control leafminers in tomato, bean, and eggplant in Japan [21,22]. Over 40 species of parasitoids have been reported from Liriomyza leafminer worldwide [23,24]. Johnson et al. [15] reared 40 parasitoid species in four families from the major leafminer L. sativae Blanchard in Hawaii. Oatman and Johnson [25] recorded as many as 20 parasitoid spp. from Liriomyza sativae. Among all parasitoids, Diglyphus begini, Halticoptera circulus (Walder), and Chrysomotomyia punctiventris (Crawford) were the most abundant.
Insecticide-based management for leafminers can also negatively impact natural enemies and enhance the resurgence of leafminer populations. Johnson et al. [15] found two leafminer parasitoids, Diglyphus begini (Ashmead) and C. punctiventris (Crawford), that were negatively impacted by treatments of methomyl and chlordimeform. Leafminer population density increased and hymenopterous parasitoids decreased after application of broad-spectrum insecticides [5,26]. Saito [27] observed a high level of resistance in leafminer with reduction in parasitism after application of insecticides in commercial garden pea fields.
Several studies have been conducted to identify leafminer parasitoids in various regions and on different plant hosts in North America [8,17,28,29]. Schuster and Wharton [8] reported four families and 15 species of leafminer parasitoids on tomato in Florida. The leafminers’ hymenopteran parasitoids were found in the bean crop during various growing seasons. Understanding parasitoids composition and status are primary steps for investigating new potential biological agents for leafminer control. In addition, leafminers’ parasitoid interactions and community structure are important factors to develop an IPM program for Liriomyza species.
Snap bean is an important agricultural product in Florida, valued at $131,280 million [1]. The leafminer L. trifolii is the most significant pest on bean crops.
The objective of this study was to investigate the composition and seasonal abundance of L. trifolii parasitoids on snap beans in South Florida. We also studied the comparative abundance of four parasitoid species in three commonly grown major vegetable crops.

2. Materials and Methods

2.1. Snap Bean Sites

The leafminer parasitoids’ composition and abundance in snap beans were investigated in 2010, 2012, 2014, and 2016. Each year, we had three plantings of snap beans: 1st planting in the second week of September 2nd planting in the second week of October, and 3rd planting in the second week of December. Bean growing season in South Florida starts in September and continues through March. As bean is a short time crop (58–65 days), we planted bean three times to cover the growing season. Each year, all three plantings were performed on the same site spacing 61 m between the plantings, where each planting site was 2 acres. In 2010 and 2012, study sites were established in the Tropical Research and Education Center (TREC), University of Florida-IFAS, Homestead, FL, USA (25°30′33.7″ N 80°30′17.1″ W). In 2014 and 2016, the sites were in growers’ fields. Raised, open soil beds (91 cm wide, 20 cm height) were prepared with a Kennco superbedder (Kenco Manufacturing Company Inc., Atoka, OK, USA) to plant beans in each site. Beds were 60 cm wide with one row of bean plants in the center of each bed. Plants within the row were spaced 5 cm. Snap beans were seeded directly on the raised beds of Rockdale soil in all sites by placing Caprice snap bean seeds individually into a 2.5-cm-deep hole performed by a seed planter (3-Point Crop-Seeder, Zoro #: G204039667, China). Planting space within the bed was 7.6 cm and in between the bed 91.4 cm. Snap bean seeds were supplied by Harris Moran Seed Company, Modesta, CA, USA. Pre-plant herbicide, halosulfuron methyl (Sandea®, Gowan Company LLC., Yuma, Arizona), was applied at 51.9 g/ha to control emergence of nutsedge (Cyperus esculentus) and broad-leaf weeds. At the time of preparing beds, granular fertilizer 6:12:12 (N:P:K) was applied in the furrow on both sides of the seed row on each bed at 1345 kg/ha. Two drip tubes were placed parallel with 30.5 cm spacing on the center of the bed for irrigating plants. Plants were irrigated once a day, delivering approximately 2.5 cm to maintain soil moisture. Liquid fertilizer (4:0:8) was applied through the drip irrigation system at the rate of 0.56 kg N/ha/day 3, 4, and 5 weeks after planting. The fungicide Chlorothalonil (Bravo®, Syngenta Crop Protection, Inc., Greensboro, NC, USA) was used at 2.81 L/ha 4 weeks after planting to prevent fungal diseases. No insecticide was used at these study sites.
In the second study, we recorded abundance and composition of various parasitoids in three commonly grown major vegetable crops including tomato, bean, and squash planted in TREC research plots (25°30′33.7″ N 80°30′17.1″ W) in 2014 and 2016. Florida ranks first or second in growing these crops. The experimental field for this study consisted of 16 beds, each 67 m long, 1.8 m wide, and 15.2 cm high. Four such adjacent beds constituted one block. Each block was divided into 4 equal plots of 15.2 m long, 7.32 m wide which constituted a plot. The abovementioned three crops were planted using a randomized complete block design, each replicated four times. All crops were planted on raised beds of Rockdale soil covered with white on black plastic mulch. In 2014, bean and squash were seeded on 12 September, and tomato was transplanted two weeks after bean and squash. In 2016, the same planting dates as 2014 were used. Plant spacing for tomato was 45.7 cm within the bed and 183 cm in between the beds. The spacing for squash and bean was 30.5 cm and 15.2 cm within the bed, respectively. All other methods for maintaining crops were as discussed above or otherwise following standard cultural practices mentioned in the Vegetable Production Handbook of Florida [30]. Chlorothalonil (Bravo Weather Stik, Syngenta Crop Protection LLC, St. Louis, MO, USA. 1.7 L/ha), mancozeb (Manzate® Pro-Stick, United Phosphorus Inc., Cary, NC 27513, USA. 1.7 L/ha), pyrimethanil (Scala®, Bayer CropScience, St. Louis, MO, USA. 0.5 L/ha), and penthiopyrad (Fontelis®, 1.0 L/ha) were used in weekly rotation to prevent fungal and bacterial diseases (target spot, Rhizoctonia root rot, leaf spot, late blight). No other pesticides were used to control foliage pests except Bacillus thuringiensis subsp. Aizawai strain ABTS 1857, (Valent BioSciences Corporation, Libertyville, IL, USA, 1.7 kg/ha) two times to control beet armyworm on tomato.

2.2. Leaf Sampling and Insect Rearing

In the first study, parasitoids were collected from foliage of bean. Sampling began when bean plants had two primary leaves fully unfolded. To address all variability in sampling, four sections (=plots), each consisting of four rows × 15.2 m long, were randomly selected from each experimental field. Ten full grown and widely open leaves, one leaf per plant, were randomly collected from each plot-row weekly (40 leaves per week). When the bean plants became mature and their primary leaves dropped off, the older bottom leaves were always collected from the plants because of L. trifolii feeding preference for the older and mature leaves [31,32]. The sampled leaves from each plot-row were placed into 15 cm diameter Petri dishes (10 leaves per Petri dish) and marked with the date and plot number. The samples were then transported to the vegetable IPM laboratory at the Tropical Research and Education Center and placed into a growth chamber at 25 °C, 70% RH, 14:10 (L:D) h for the development of leafminer and its parasitoids. The bean leaves were checked daily for collecting leafminer pupae. The emerging pupae in each Petri dish were separated and transferred to a new Petri dish and labeled with the same sampling date. The separated pupae were also checked daily for recording the larval endoparasitoids’ emergence. Bean leaves were checked daily for collecting the larval ectoparasitoids from mines on the leaves.
In the second study, from each plot of four rows each 15.2 m long, the sample consisted of randomly selected 10 full grown infested leaves/row, 10 × 4 = 40 leaves/plot. For the convenience of parasitoid collection, leaves from each row (10 leaves) were placed separately in a Petri dish (10 cm diam). All other procedures were accomplished following the above study.

2.3. Insects Collection and Identification

All the emerged parasitoids were collected and preserved in 75% alcohol for identification. The leafminers were identified following morphological characters described by Capinera [7] (2001), and further verified by the Division of Plant Industry (DPI), Gainesville, FL, USA. The parasitoids were identified based on the external characters used in previous studies [3,28,33]. The leafminers parasitoids were sent for verification to the Division of Plant Industry (DPI), Gainesville, FL, USA, and further confirmed by Systematic Entomology Laboratory, USDA, MD. Voucher specimens were stored in the Entomology, Tropical Research and Education Center, Homestead, FL, USA.

2.4. Statistical Analysis

All data in the first study (abundance and composition of parasitoids in beans) and second study (comparative abundance in three crops) were square root transformed before analyses. Non-transformed means are reported in the tables. Transformed data of both studies were analyzed using a mixed model ANOVA. In the first study, fixed effect consisted of parasitoid species, year of study, and months, and random effect consisted of replications, whereas in the second study (comparative abundance of parasitoid species in three crops), fixed effect consisted of parasitoid species, crops, years, and months, and random effects consisted of plots. Both fixed and random effects in both studies were used to account for experimental design (PROC GLIMMIX model, SAS Version 9.3, SAS Institute Inc., Cary, NC, USA [34]). In the PROC GLIMMIX model, the Kenward–Roger method was used to estimate the degree of freedom. Means were separated using Tukey’s Honestly Significant Difference (HSD) test in SAS. All data were analyzed at a 5% level of significance.

3. Results and Discussion

3.1. Seasonal Abundance in Beans

We recorded 13 species of hymenopteran parasitoids of L. trifolium (Figure 1) on beans in south Florida during the four years (2010, 2012, 2014, and 2016) of the present study. They belonged to three families including Braconidae (Opius dissitus (Muesebeck) and Euopius sp.), Eulophidae (Diaulinopsis callichroma (Crawford), Diglyphus begini Ashmead), D. intermedius (Girault), D. isaea (Walker), Neochrysocharis sp. Kurdjumov, Closterocercus sp. Westwood, Zagrammosoma lineaticeps (Girault), Z. multilineatum (Ashmead), Pnigalio sp. Schrank, Chrysocharis sp. Hahn), and Pteromalidae (Halticoptera sp.). Among these, Opius dissitus and Diaulinopsis callichroma were the most abundant species in all four years of study followed by Euopius sp., Diglypohus begini, and Neochrysocharis sp. (Table 1). Other species were present in a low density, 0.23–0.56 in 2010 and 0.17–0.51 in 2012, 0.45–0.97 in 2014 and 0.17–0.64 in 2016. The highest number of parasitoids, irrespective of species, was recorded in 2014 ( x ¯ = 13.29) followed by 2010 ( x ¯ = 11.93), 2012 ( x ¯ = 9.51) and 2016 ( x ¯ = 8.69). Total parasitoid abundance, irrespective of species, showed a strong positive relationship (r = 0.94, p < 0.0001) with leafminers’ abundance. Rauf et al. [35] also recorded 10 Eulophid parasitoids out of 11 spp. from infested vegetable leaves in Indonesia. Variation in the density among parasitoid species in different years could be due to the variation in abundance of the host Liriomyza, quality of crop, and temperature. During the present study over four years, mean monthly temperature (°C) varied from 19 °C in December to 24.4 °C in October. Johnson and Hara [36] emphasized the matching of parasitoid species, with favorable Liriomyza species and crop for the development of effective biological control.
Two different Braconid parasitoids, O. dissitus (Figure 2) and Euopius sp. (Figure 3), were observed on beans. Opius dissitus is a solitary larval endo parasitoid of L. trifolii [37,38,39]. The adults are black in color with long antennae and are 1.5 mm in length. The parasitoid females deposit their eggs inside the leafminer larvae. The parasitized host larvae continue to develop throughout the larval stage and emerge from the puparium. This observation is supported by Bordat et al. [38], who reported that parasitoid females lay their eggs directly inside their host larvae. At the end of the development, the parasitoid adults emerged from the host puparium. One O. dissitus adult was found to emerge from a single leafminer pupa in our study.
Opius dissitus was the most abundant leafminer parasitoid on snap beans in all four years of this study in the Miami-Dade County (Table 1). A significantly higher number of O. dissitus was recorded in each of this study than the other parasitoid species. Opius sp. occurred on bean during all months of the study (Figure 4a). Opius dissitus abundance was high in November, December, and January during four years of the study. Population density decreased after January. The density of O. dissitus was positively correlated (r = 0.80, p < 0.0001) with leafminer density within the whole growth season. The density of O. dissitus was high when the temperature was cool (15~19 °C) in December 2010 and January 2011. The optimum temperature for both O. dissitus male and female was 20 °C, and the female had a higher reproduction at 25 °C [39]. Opius dissitus was reported as the most abundant larval parasitoid from leafminer infested tomato foliage in Florida [8].
Euopius sp. (Figure 3) is a larval endoparasitoid. One Euopius sp. adult was found to emerge from a single host puparium. Euopius sp. has almost the same body size and antennae as O. dissitus. However, Euopius sp.’s body has a yellow color, which differentiates it from O. dissitus (being black in color). The abundance of Euopius sp. (Table 1) was low in 2010 ( x ¯ ) = 0.83) and 2012 ( x ¯ ) = 0.78) and did not differ statistically from 2016 ( x ¯ = 1.12). The highest density of Euopius was recorded in 2014 ( x ¯ ) = 1.33). Peak density of Euopius was recorded in September of 2010, December of 2012 and 2016, and January of 2014, which differed significantly from the rest of the years (Figure 4b). The Euopius sp. was reared from Liriomyza-infested weeds on Bidens alba (L.) (Asterales: Asteraceae) [40].
There were ten different species of parasitoids found in the family of Eulophidae. Diaulinopsis callichroma (Figure 5) was found to be the second largest group of L. trifolii parasitoids in this study (Table 1). The highest population density was recorded in 2010, followed by 2012 and 2014. The lowest density was recorded in 2016, which did not differ statistically from 2014. D. callichroma occurred across the season during the four years of this study. However, population abundance peaked in November followed by December. The population abundance of D. callichroma a showed positive correlation (r = 0.65, p < 0.0001) with leafminers abundance when its populations across the four years are considered. The hind femora of adult D. callichroma is dusky basally, while the fore and middle femora are pale [33]. The male adult’s basal antennal segments are black and enlarged. The body size of adults is about 1.1–1.3 mm in length. This parasitoid is a larval ectoparasitoid of leafminer. D. callichroma larvae feed directly on the host larva and eventually kill the larva. The parasitoid larvae pupate inside the mine, eventually emerging from the mine. The abundance of D. callichroma might be affected by both host density and temperature condition.
D. callichroma population density was the highest in 2010 ( x ¯ ) = 2.35), which did not differ statistically from 2012 ( x ¯ ) = 2.09). The lowest population density of D. callichroma was observed in 2016 ( x ¯ ) = 1.690). Its abundance was high in November and December of each year (Figure 4c). Population density decreased before and after this duration (November–December). The abundance of D. callichroma might be affected by both host density and temperature.
Three different species of Diglyphus parasitoids (Figure 6, Figure 7 and Figure 8: D. begini, D. intermedius and D. isaea) were reared from bean foliage. The abundance of D. begini was significantly higher than that of D. intermedius and D. isaea in 2010 and did not differ in other years. The D. begini population density was low until December during this study (Figure 4d). The population abundance peaked in January.
Diglyphus spp. parasitoids were the third largest group in the study. These are larval ectoparasitoids, and adult females generally lay more than one egg by the side of the host larva [41]. Diglyphus spp. are characterized by their antennae with two funicular segments. The forewings of these three species of Diglyphus have dense setose, whereas the basal cell has uniformly dense setose. These three abovementioned species of Diglyphus can be distinguished from each other based on the dark area on their hind tibia. D. begini basal hind tibia has a short and less than 25% metallic dark area (Figure 6).
D. intermedius basal tibia has a relatively larger area of 25–35% dark color and with extended dusky color (Figure 7).
Alternatively, D. isaea basal hind tibia has over 75% metallic dark color proportion (Figure 8) [28,33].
Schuster and Wharton [8] reported that Diglyphus parasitoids were the most abundant larval ectoparasitoids on the tomato crop in Florida and that both species (D. intermedius and D. begini) were recorded in the current study. In our study, the most abundant larval ectoparasitoid on bean crop was D. callichroma. It should be noted that D. isaea has been used as an effective biological control agent in greenhouse for controlling Liriomyza spp. leafminer in the Netherlands [41,42].
Neochrysocharis sp. (Figure 9) was recorded as the fifth largest group of leafminer parasitoids during our four years of study. The population abundance was higher in 2010 ( x ¯ = 0.89) and 2014 ( x ¯ = 0.97) than that of 2012 ( x ¯ = 0.61) and 2016 ( x ¯ = 0.47). Adults emerge from mines on the leaves. The adult body is metallic green, and eyes are red. The fore, middle, and hind tibia are pale. Neochrysocharis sp. is reported as an endoparasitoid of the leafminer larva [8]. Tran [43] reported a high abundance of Neochrysocharis in the north central coast region of Vietnam. This species was also reported from Indonesia and is considered as a potential biocontrol agent for invasive agromyzid pests [44].
The population of Closterocerus sp. (Figure 10) was low on bean foliage during this study. Based on our four years of study, it is the eighth largest group of leafminer parasitods in bean. Density of Closterocerus ranged from 3.58% in 2012 to 5.79% in 2014. Closterocerus is an endoparasitoid of the leafminer’s young instars [3].
The adult body length is 1.0–1.3 mm with characteristic dark bands on the forewings. Stegmaier [29] reported that C. cinctipennis is a parasitoid of the leafminer L. trifolii in Florida. Rauf et al. [35] reported Closterocerus sp. from snow peas (Pisum sp.) infested with this Asian leafminer species Chromatomyia horticola (Goureau). C. mirabilis has been reported as a potential parasitod of agromyzid leafminers in Australia [45].
We recorded two species of Zagrammosoma (Figure 11 and Figure 12), Z. lineaticeps (Girault) and Z. multilineatum (Ashmead). The density of Z. lineaticeps ranged from 2.63% in 2012 to 3.54% in 2014 and that of Z. multilineatum ranged from 0.17% in 2012 to 0.80% in 2014. Both species are larval ectoparasitoids of Liriomyza leafminer. Both Z. lineaticeps and Z. multilineatum were found in Florida [8,17]. Zagrammosoma spp. were also collected from leafminer infested vegetable leaves in Indonesia [38]. Zagrammosoma lineaticeps is black or dark-colored and the forewing has a dark line along the apical margin (Figure 10), while Z. mulitilineatum is predominately yellow and mesoscutum has dark stripes (Figure 11). The abundance of both species was high in October and November 2010. In the study, Z. multilineatum was relatively more abundant (20 adults) than Z. lineaticeps (10 adults) (Table 1). Zagrammosoma spp. were also collected from Liriomyza-infested faba bean (Vicia faba) in Egypt [46].
Pnigalio sp. (Figure 13) is the 10th largest group of parasitoids. It occurred in a low density on bean ranging from 2.43% in 2010 to 4.29% in 2016. Pnigalio sp. is a larval ectoparasitoid of the leafminer Liriomyza. The genus was also reported to parasitize Lepidoptera, Hymenoptera, and Coleoptera [3]. The body length of adult females is 1.7~1.9 mm and male is 1.5~1.7 mm. The antennae have four funicular segments, and for the male, it is a laterally branched structure antenna [3]. Lasalle and Parrella [28] indicated that only one Nearctic species, P. flavipes (Ashmead), attacks Liriomyza. However, Schuster and Wharton [8] reported species of P. maculipes (Crawford) reared from tomato foliage in Florida. Pnigalio spp. abundance was 12.3% among the hymenopteran parasitoid complex of citrus leafminer in Texas [47].
Chrysocharis sp. (Figure 14) is a larval-pupal endoparasitoid of leafminer and was the second most abundant larval-pupal endoparasitoid (Table 1). Chrysocharis sp. showed a consistent population density during the four years of this study. In our study, Chrysocharis density ranged from 1.79% in 2012 to 4.29% in 2014. Chrysocharis sp. Post-marginal vein is always longer than the stigma vein, and the petiole is present and distinct. Chrysocharis sp. Is a primary parasitoid of leaf-mining larvae of Diptera, Lepidoptera, and Hymenoptera [48]. The authors [48] found a low percentage of Chrysocharis sp (0.04–0.17) and highest percentage of Halticoptera sp. (32–52%) on vegetable crops in winter and autumn in the Middle Volga Basin in Russia. Chrysocharis sp. was reported from Liriomyza huidobrensis (Blanchard) (Diptera: Agromyzidae)-infested vegetable leaves in Indonesia [35].
Halticoptera sp. (Figure 15) belongs to the family of Pteromalidae. This species is another larval-pupal endoparasitoid of leafminers in beans. The abundance of this species was the lowest in 2010 (1.93%) and highest in 2014 (3.39%). The antenna has six funicular segments. Schuster and Wharton [8] reported a high population of Halticoptera sp. on tomato. Shahein and El-Maghraby [49] recorded a very low percentage of Halticoptera sp. on broad beans (Vicia faba L.) in Egypt. They found Diglyphus sp. and Opius as the most abundant species on bean. In addition, H. circulus was reported to be the only one Nearctic species of Halticoptera known to parasitize Liriomyza leafminer [28]. Halticoptera arduine (Walker) successfully parasitized L. trifolii, L. sativae, and L. huidobrensis leafminers and developed in them as endoparasitoids [50].

3.2. Comparative Abundance of Parasitoids in Three Crops

Opius sp. occurred in all three vegetable crops with the highest number in bean, followed by tomato and squash in both years’ studies (F = 218.34, df = 2, 53.4, p = 0.001) (Figure 16A,B). The population abundance of Opius sp. was negatively correlated with the temperature increase (r = −0.80) in all crops during this study. In the instance of Euopius sp., the highest abundance was recorded in bean, followed by squash and tomato (F = 6.32; df = 2, 32.1; p = 0.004). Month did not influence population abundance of Euopius, irrespective of crops (F = 0.16; df = 5, 44.48; p = 0.16). Year (F = 4.59, df = 1, 53.24; p = 0.036), crop x year (F = 4.78; df = 2, 32.1; p = 0.015), and crop x month (F = 3.43; df = 10, 16.95; p = 0.012) significantly impacted the Euopius population in tomato in 2014 (Figure 16C,D). However, in 2016, the highest abundance was recorded in bean, followed by tomato and squash. On all crops, Euopius population abundance was negatively correlated with temperature increase in both years’ studies (r = −0.25 to −0.52). The abundance of Diaulinopsis was significantly higher in bean followed by tomato and squash in both years (F = 54.92; df = 2, 43.19; p = 0.001) (Figure 16E,F). Year of study did not impact the population abundance of Diaulinopsis sp. Month of study alone (F = 10.14; df = 5, 29.11; p = 0.0001) and crop x month (F = 8.44; df = 10, 41.35; p = 0.001) significantly increased population abundance of Diaulinopsis. The population increase in Diaulinopsis was positively correlated with temperature in squash (r = 0.36 in 2014); otherwise, it followed the same trend of population increase like the above species. The population of Diglyphus sp. was higher in bean followed by squash and tomato in both years (F = 7.99; df = 2, 25.06; p = 0.0025) (Figure 16G,H). The year of study positively impacted the population of Diglyphus sp. (F = 24.49; df = 11, 081; p = 0.0005). The month of study did not cause a statistical difference in the population increase in Diglyphus. Crop × year and crop–month interactions had a positive effect on the increase in the Diglyphus population. The Diglyphus population abundance was positively correlated with temperature in squash (r = 0.51) and tomato (r = 0.14), and negatively correlated in bean in both years’ studies (2014: r = −0.47; 2016: r = −0.2015). Overall, population abundance of parasitoids were high when density of leafminer was high and temperature was relatively low (Figure 17).
Very little information is available on the comparative abundance of parasitoids using replicated vegetable crop plots. Tran et al. [51] surveyed various vegetable crop fields for the abundance of parasitoids associated with agromyzid leafminer and reported Neochrysocharis formosa as the most abundant parasitoid on French bean, tomato, and casava in Vietnam.

4. Conclusions

Vegetable crops are mostly infested by leafminers. The present study provided information about thirteen species of hymenopteran parasitoids that attack leafminers. Among all parasitoids, four species were recorded to be more abundant on beans, squash, and tomato than the rest of the parasitoid species recorded in this study. Leafminer abundance was high between 7.2° and 23.8 °F. Parasitoid species presence followed the pattern of leafminers abundance. Insecticide applications severely impact the population abundance of parasitoids, although this was not studied in the current study. Biocontrol of leafminers will be effective if insecticides are applied selectively.

Author Contributions

D.R.S. conceptualized the project, collected resources to set up the field experiment, analyzed data, and prepared final version of the manuscript. O.L. helped in writing the manuscript. J.L. collected data and prepared images of parasitoids. All authors have read and agreed to the published version of the manuscript.

Funding

The research was funded by obtaining in kind support from vegetable growers.

Institutional Review Board Statement

The manuscript was checked by TREC faculty, and their comments were addressed to finalize the manuscript.

Data Availability Statement

Dakshina Seal maintains excel file of all data used in this study.

Acknowledgments

Cathie Sabines assisted in collecting samples. Tomato, bean, and squash growers supported this study by providing land and growing crops. USDA and DPI helped in confirming parasitoid species.

Conflicts of Interest

There is no conflict of interest with any coauthors, or any researchers in conducting and publishing this work.

References

  1. USDA-NASS. National Agricultural Statistics Service; United States Department of Agriculture: Washington, DC, USA, 2015.
  2. Spencer, K.A. Agromyzidae (Diptera) of Economic Importance; Series Entomologica; Springer Science & Business Media: Berlin/Heidelberg, Germany, 1973; Volume 9, pp. 1–418. [Google Scholar]
  3. Asadi, R.; Talebi, A.A.; Fathipour, Y.; Moharramipour, S.; Rakhshani, E. Identification of parasitoids and seasonal parasitism of the Agromyzid leafminers genus Liriomyza (Dip: Agromyzidae) in Varamin. Iran. J. Agric. Sci. Technol. 2006, 8, 293–303. [Google Scholar]
  4. Shepard, B.; Samsudin, M.; Braun, A.R. Seasonal incidence of Liriomyza huidobrensis (Diptera: Agromyzidae) and its parasitoids on vegetables in Indonesia. Int. J. Pest Manag. 1998, 44, 43–47. [Google Scholar] [CrossRef]
  5. Trumble, J.T.; Nakahara, H. Occurrence, parasitization, and sampling of Liriomyza species (Diptera: Agromyzidae) infesting celery in California. Environ. Entomol. 1983, 12, 810–814. [Google Scholar] [CrossRef]
  6. Parrella, M.P. Biology of Liriomyza. Annu. Rev. Entomol. 1987, 32, 201–224. [Google Scholar] [CrossRef]
  7. Capinera, J.L. American Serpentine Leafminer, Liriomyza trifolii (Burgess) (Insecta: Diptera: Agromyzidae); Entomology and Nematology Department, Florida Cooperative Extension Service, Institute of Food and Agricultural Sciences, University of Florida: Gainesville, FL, USA, 2001; Available online: http://edis.ifas.ufl.edu/in506.a (accessed on 25 May 2023).
  8. Schuster, D.J.; Wharton, R.A. Hymenopterous parasitoids of leaf-mining Liriomyza spp. (Diptera: Agromyzidae) on tomato in Florida. Environ. Entomol. 1993, 22, 1188–1191. [Google Scholar] [CrossRef]
  9. Mruphy, S.T.; LaSalle, J. Balancing biological control strategies in the IPM of New Worl invasive Liriomza leafminers in field vegetable crops. Biocontrol News Inf. 1999, 20, 91–104. [Google Scholar]
  10. Poe, S.L.; Montz, J.K. Preliminary results of a leafminer species survey. In Proceedings of the IFAS-Industry Conference on Biology and Control of Liriomyza Leafminers, Lake Buena Vista, FL, USA, 3–4 November 1981; pp. 24–34. [Google Scholar]
  11. Cox, D.L.; Remick, M.D.; Lasota, J.A.; Dybas, R.A. Toxicity of avermectins to Liriomyza trifolii (Diptera: Agromyzidae) larvae and adults. J. Econ. Entomol. 1995, 88, 1415–1419. [Google Scholar] [CrossRef] [Green Version]
  12. Kaski, R.; Parrella, M.P. Improving the biological control of leafminers (Diptera: Agromyzidae) using the sterile insect technique. J. Econ. Entomol. 2006, 99, 1168–1175. [Google Scholar]
  13. Keil, C.B.; Parrella, M.P.; Morse, J.G. Methods for monitoring and establishing baseline data for resistance to Permethrin by Liriomyza trifolii (Burgess). J. Econ. Entomol. 1985, 78, 419–422. [Google Scholar] [CrossRef]
  14. Leibee, G.L.; Capinera, J.L. Pesticide resistance in Florida insects limits management options. Fla. Entomol. 1995, 78, 386–399. [Google Scholar] [CrossRef]
  15. Johnson, M.W.; Oatman, E.R.; Wyman, J.A. Effects of insecticides on populations of the vegetable leafminer and associated parasites on summer pole tomatoes. J. Econ. Entomol. 1980, 73, 61–66. [Google Scholar] [CrossRef]
  16. Noyes, J. Universal Chalcidoidea Database. The Natural History Museum [Online]. 2004. Available online: http://www.nhm.ac.uk/entomology/chalcidoids/ (accessed on 25 May 2023).
  17. Stegmaier, C.E. Parasitic Hymenoptera bred from the family Agromyzidae (Diptera) with special reference to south Florida. Fla. Entomol. 1972, 55, 273–282. [Google Scholar] [CrossRef]
  18. Petcharat, J.; Ling, Z.; Weiqiu, Z.; Zaifu, X.; Quisong, W. Larval Parasitoids of Agromyzid leafminer genus Liriomyza in Southern Thailand: Species and their Host Plants. Songklanakarin. J. Sci. Technol. 2002, 24, 467–472. [Google Scholar]
  19. Xu, P.; Wan, Z.-W.; Chen, X.-X.; Liu, S.; Feng, M.-G. Immature morphology and development of Opius caricivorae (Hymenoptera: Braconidae), an endoparasitoid of the leafminer Liriomyza sativae (Diptera: Agromyzidae). Ann. Entomol. Soc. 2007, 100, 425–432. [Google Scholar] [CrossRef]
  20. Zhu, C.-D.; LaSalle, J.; Huang, D.-W. A review of the Chinese Diglyphus Walker (Hymenoptera: Eulophidae). Orient. Insects 2000, 34, 263–288. [Google Scholar] [CrossRef]
  21. Saito, T.; Ikeda, F.; Ozawa, A. Effect of pesticides on parasitoid complex of serpentine leafminer Liriomyza trifolii (Burgess) in Shizuoka Prefecture. J. Appl. Enomol. Zool. 1996, 40, 127–133. [Google Scholar] [CrossRef] [Green Version]
  22. Arakaki, N.; Kinjo, K. Notes on the parasitoid fauna of the serpentine leafminer Liriomyza trifolii (Burgess) (Diptera: Agromyzidae) in Okinawa, Southern Japan. Appl. Entomol. Zool. 1998, 33, 577–581. [Google Scholar] [CrossRef] [Green Version]
  23. Waterhouse, D.F.; Norris, K.R. Liriomyza species (Diptera: Agromyzidae) leafminers. In Biological Control: Pacific Prospects; Waterhouse, D.F., Norris, K.R., Eds.; Inkata Press: Melbourne, Australia, 1987; pp. 159–176. [Google Scholar]
  24. Konishi, K. An illustrated key to the Hymenopterous parasitoids of Liriomyza trifolii in Japan. Misc. Publ. Natl. Inst. Agro-Environ. Sci. 1998, 22, 27–76. (In Japanese) [Google Scholar]
  25. Oatman, E.R.; Johnson, M.W. Leafminer parasite interactions. In Proceedings of the Institute Food and Agricultgural Science-Industry Conference Biology and Control of Liriomyza leafminers, Lake Buena Vista, FL, USA, 3–4 November 1981; pp. 99–105. [Google Scholar]
  26. Oatman, E.R.; Kennedy, G.G. Methomyl induced outbreak of Liriomyza sativae on tomatoes. J. Econ. Entomol. 1976, 69, 667–668. [Google Scholar] [CrossRef]
  27. Saito, T. Outbreak of the pea leafminer, Chromatomyia horticola, caused by insecticide applications. Plant Prot. 2004, 58, 295–299. [Google Scholar]
  28. Lasalle, J.; Parrella, M.P. The chalcidoid parasites (Hymenoptera, Chalcidoidae) of economically important Liriomyza species (Diptera, Agromyzidae) in North America. Proc. Entomol. Soc. Wash. 1991, 93, 571–597. [Google Scholar]
  29. Stegmaier, C.E., Jr. Host plants and parasites of Liriomyza trifolii in Florida (Diptera: Agromyzidae). Fla. Entomol. 1966, 49, 75–80. [Google Scholar] [CrossRef]
  30. Olson, S.M.; Santos, B. Vegetable: Production Handbook for Florida 2010–2011; University of Florida-IFAS: Gainesville, FL, USA, 2011. [Google Scholar]
  31. Facknath, S. Leaf age and life history variables of a leafminer: The case of Liriomyza trifolii on potato leaves. Neth. Entomol. Soc. 2005, 115, 79–87. [Google Scholar] [CrossRef]
  32. William, R.S.; Lincoln, D.R.; Norby, R.J. Leaf age effects of elevated CO2-grown white oak leaves on spring-feeding lepidopterans. Global. Chang. Biol. 1998, 4, 235–246. [Google Scholar] [CrossRef]
  33. Gordh, G.; Hendrickson, R.M., Jr. New species of Diglyphus, a world list of the species, taxonomic notes and a key to new world species of Diglyphus and Diaulinopsis (Hymenoptera: Eulophidae). Proc. Entomol. Soc. Wash. 1979, 81, 666–684. [Google Scholar]
  34. SAS Institute. SAS/STAT 9.3 User’s Guide; SAS Institute: Cary, NC, USA, 2013. [Google Scholar]
  35. Rauf, A.; Shepard, B.M.; Johnson, M.W. Leafminers in vegetables, ornamental plants and weeds in Indonesia: Surveys of host crops, species composition and parasitoids. Int. J. Pest Manag. 2000, 46, 257–266. [Google Scholar] [CrossRef]
  36. Johnson, M.W.; Hara, A.H. Influence of host crop on parasitoids (Hymenoptera) of Liriomyza spp. (Diptera: Agromyzidae). Environ. Entomol. 1987, 16, 339–344. [Google Scholar] [CrossRef]
  37. Nelson, J.M.; Roitberg, B.D. Flexible patch time allocation by the leafminer parasitoid, Opius dimidiatus. Ecol. Entomol. 1995, 20, 245–252. [Google Scholar] [CrossRef]
  38. Bordat, D.; Coly, E.V.; Letourmy, P. Influence of temperature on Opius dissitus (Hym., Braconidae), a parasitoid of Liriomyza trifolii (Dipt: Agromyzidae). Entomophaga 1995, 40, 119–124. [Google Scholar] [CrossRef]
  39. Bordat, D.; Coly, E.V.; Roux-Olivera, C. Morphometric, biological and behavioural differences between Hemiptarsenus varicornis (Hym., Eulophidae) and Opius dissitus (Hym., Braconidae) parasitoids of Liriomyza trifolii (Dipt., Agromyzidae). J. Appl. Entomol. 1995, 119, 423–427. [Google Scholar] [CrossRef]
  40. Schuster, D.J.; Gilreath, J.P. Agromyzidae (Diptera) Leafminers and their parasitoids in weeds associated with tomato in Florida. Environ. Entomol. 1991, 20, 720–723. [Google Scholar] [CrossRef]
  41. Minkenberg, O.P.J.M.; van Lanteren, J.C. The Leafminers Liriomyza bryoniae and L. trifolii (Diptera: Agromyzidae), Their Parasites and Host Plants: A Review; Agricultural University Wageningen: Wageningen, The Netherlands, 1986. [Google Scholar]
  42. Boot, W.J.; Minkenberg, O.P.J.M.; Rabbinge, R.; de Moed, G.H. Biological control of the leafminer Liriomyza bryoniae by seasonal inoculative releases of Diglyphus isaea: Simulation of a parasitoid–host system. Neth. J. Plant. Pathol. 1992, 98, 203–212. [Google Scholar] [CrossRef] [Green Version]
  43. Tran, D.H. Agromyzid leafminers and their parasitoids on vegetables in Central Vietnam. J. Issaas 2009, 15, 21–33. [Google Scholar]
  44. Fisher, N.; Salle, J.L. A new species of Neochrysocharis Kurdjumov (Hymenoptera: Eulophidae), a parasitoid of serpentine leafminers (Diptera: Agromyzidae) in Southeast Asia. Zootaxa 2005, 1044, 27–34. [Google Scholar] [CrossRef]
  45. Edwards, C.M.; Salle, J.L. A new species of Closterocerus Westwood (Hymenoptera: Eulophidae), a parasitoid of serpentine leafminers (Diptera: Agromyzidae) from Australia. Aust. J. Entom. 2004, 43, 129–132. [Google Scholar] [CrossRef]
  46. Amer, N.A.; Hegazi, E.M. Parasitoids of the leaf miners Liriomyza spp. (Diptera: Agromyzidae) attacking faba bean in Alexandria, Egypt. Egypt. J. Biol. Pest Control 2014, 24, 301–305. [Google Scholar]
  47. French, J.V.; Legaspi, J.C. Citrus leafminer in Texas: Population dynamics, damage and control. In Proceedings of the Managing the Citrus Leafminer. Proceedings from an International Conference, Orlando, FL, USA, 23–25 April 1996; p. 80. [Google Scholar]
  48. Yefrenova, Z.A.; Mishchenko, A.V. Parasitoid complex (Hymenoptera: Eulophidae) of the Phyllonorycter issikii (Lepidoptera: Gracillariidae) from the Middle Volga Basin. Zool. Zhurn. 2008, 87, 189–196. [Google Scholar]
  49. Shahein, A.; Maghraby, M.M.A. Studies on the hymenopterous parasitoids of Liriomyza trifolii (Burgess) (Dip., Agromyzidae) on broad beans in Egypt. J. Appl. Entomol. 1988, 106, 377–380. [Google Scholar] [CrossRef]
  50. Muchemi, S.K.; Zebitz, C.P.W.; Borgemeister, C.; Akutse, K.S.; Foba, C.N.; Ekesi, S.; Fiaboe, K.K.M. Acceptability and suitability of three Liriomyza species as host for the endoparasitoid Halticoptera arduine (Hymenoptera: Pteromalidae). Environ. Entomol. 2018, 47, 684–691. [Google Scholar] [CrossRef]
  51. Tran, D.H.; Tran, T.T.A.; Konishi, K.; Takagi, M. Abundance of the Parasitoid Conrplex Associated with Liriomyza spp. (Diptera: Agromyzidae) on Vegetable Crops in Central and Southern Vietnam. J. Fac. Agric. Kyushu Univ. 2006, 51, 115–120. [Google Scholar]
Agriculture 13 01460 g001 550
Figure 1. Liriomyza trifolii (Agromyzidae). Photo credit: J. Li.
Figure 1. Liriomyza trifolii (Agromyzidae). Photo credit: J. Li.
Agriculture 13 01460 g001
Agriculture 13 01460 g002 550
Figure 2. Opius dissitus (Braconidae). Photo credit: J. Li.
Figure 2. Opius dissitus (Braconidae). Photo credit: J. Li.
Agriculture 13 01460 g002
Agriculture 13 01460 g003 550
Figure 3. Euopius sp. (Braconidae). Photo credit: J. Li.
Figure 3. Euopius sp. (Braconidae). Photo credit: J. Li.
Agriculture 13 01460 g003
Agriculture 13 01460 g004 550
Figure 4. Seasonal pattern of abundance of four species of leafminers’ parasitoids in bean in bean in 2010, 2012, 2014 and 2016.
Figure 4. Seasonal pattern of abundance of four species of leafminers’ parasitoids in bean in bean in 2010, 2012, 2014 and 2016.
Agriculture 13 01460 g004
Agriculture 13 01460 g005 550
Figure 5. Diaulinopsis callichroma (Eulophidae). Photo credit: J. Li.
Figure 5. Diaulinopsis callichroma (Eulophidae). Photo credit: J. Li.
Agriculture 13 01460 g005
Agriculture 13 01460 g006 550
Figure 6. Diglyphus begini (Eulophidae). Photo credit: J. Li.
Figure 6. Diglyphus begini (Eulophidae). Photo credit: J. Li.
Agriculture 13 01460 g006
Agriculture 13 01460 g007 550
Figure 7. Diglyphus intermedius (Eulophidae). Photo credit: J. Li.
Figure 7. Diglyphus intermedius (Eulophidae). Photo credit: J. Li.
Agriculture 13 01460 g007
Agriculture 13 01460 g008 550
Figure 8. Diglyphus isaea (Eulophidae). Photo credit: J. Li.
Figure 8. Diglyphus isaea (Eulophidae). Photo credit: J. Li.
Agriculture 13 01460 g008
Agriculture 13 01460 g009 550
Figure 9. Neochrysocharis sp. (Eulophidae). Photo credit: J. Li.
Figure 9. Neochrysocharis sp. (Eulophidae). Photo credit: J. Li.
Agriculture 13 01460 g009
Agriculture 13 01460 g010 550
Figure 10. Closterocerus sp. (Eulophidae). Photo credit: J. Li.
Figure 10. Closterocerus sp. (Eulophidae). Photo credit: J. Li.
Agriculture 13 01460 g010
Agriculture 13 01460 g011 550
Figure 11. Zagrammosoma lineaticeps (Eulophidae). Photo credit: J. Li.
Figure 11. Zagrammosoma lineaticeps (Eulophidae). Photo credit: J. Li.
Agriculture 13 01460 g011
Agriculture 13 01460 g012 550
Figure 12. Zagrammosoma multilineatum (Eulophidae). Photo credit: J. Li.
Figure 12. Zagrammosoma multilineatum (Eulophidae). Photo credit: J. Li.
Agriculture 13 01460 g012
Agriculture 13 01460 g013 550
Figure 13. Pnigalio sp. (Eulophidae). Photo credit: J. Li.
Figure 13. Pnigalio sp. (Eulophidae). Photo credit: J. Li.
Agriculture 13 01460 g013
Agriculture 13 01460 g014 550
Figure 14. Chrysocharis sp. (Eulophidae). Photo credit: J. Li.
Figure 14. Chrysocharis sp. (Eulophidae). Photo credit: J. Li.
Agriculture 13 01460 g014
Agriculture 13 01460 g015 550
Figure 15. Halticoptera sp. (Pteromalidae). Photo credit: J. Li.
Figure 15. Halticoptera sp. (Pteromalidae). Photo credit: J. Li.
Agriculture 13 01460 g015
Agriculture 13 01460 g016 550
Figure 16. Mean number of parasitoids/leaf sample on bean, tomato and squash in different months of 2014 and 2016; Opius sp. (A,B), Euopius sp. (C,D), Diaulinopsis sp. (E,F) and Diglyphus sp. (G,H).
Figure 16. Mean number of parasitoids/leaf sample on bean, tomato and squash in different months of 2014 and 2016; Opius sp. (A,B), Euopius sp. (C,D), Diaulinopsis sp. (E,F) and Diglyphus sp. (G,H).
Agriculture 13 01460 g016
Agriculture 13 01460 g017 550
Figure 17. Mean temperature (mean ± SD) represented by line and mean number of leafminers’ mines/bean leaf (mean ± SD) represented by bars in different months.
Figure 17. Mean temperature (mean ± SD) represented by line and mean number of leafminers’ mines/bean leaf (mean ± SD) represented by bars in different months.
Agriculture 13 01460 g017
Table
Table 1. Mean number of leaf miner parasitoids per bean leaf sample for four years study.
Table 1. Mean number of leaf miner parasitoids per bean leaf sample for four years study.
Family & Species2010201220142016
Braconidae
Opius dissitus12.05 ± 0.90 aA10.08 ± 0.81 aA7.63 ± 0.84 aA6.17 ± 0.93 aA
Euopius sp.1.12 ± 0.14 cdA1.10 ± 0.15 cA2.00 ± 0.20 cA1.50 ± 0.16 cA
Eulophidae
Diaulinopsis callichroma6.83 ± 0.64 bA5.38 ± 0.52 bA4.60 ± 0.73 bA3.23 ± 0.37 bA
Diglyphus begini1.98 ± 0.30 cA0.77 ± 0.12 cdA1.77 ± 0.25 cdA0.70 ± 0.12 dA
D. intermedius0.92 ± 0.14 deA0.63 ± 0.12 ceA0.93 ± 0.18 egA0.47 ± 0.10 deA
D. isaea0.64 dib1.12 ± 0.14 dfB7.63 ± 0.84 cfA7.63 ± 0.84 deB
Neochrysocharis sp.1.40 ± 0.19 cdA0.82 ± 0.14 cdA1.23 ± 0.16 ceA0.47 ± 0.09 deA
Closterocercus0.58 ± 0.10 efA0.370.08 dfaA0.97 ± 0.17 dgA0.40 ± 0.08 deA
Zagrammosoma lineaticedps0.37 ± 0.08 gfA0.25 ± 0.06 efA0.53 ± 0.12 fgA0.27 ± 0.08 deA
Z. multilineatum0.85 ± 0.15 dfA1.03 ± 0.17 fA1.03 ± 0.17 egA0.23 ± 0.08 deA
Pnigalio sp.0.33 ± 0.08 gA0.67 ± 0.14 efA0.67 ± 0.14 egA0.33 ± 0.09 deA
Chrysocharis sp.0.28 ± 0.07 gA0.67 ± 0.14 fA0.67 ± 0.14 egA0.17 ± 0.07 eA
Pteromalidae
Halticoptera sp.0.27 ± 0.07 gA0.47 ± 0.10 efA0.47 ± 0.10 gA0.23 ± 0.08 deA
df = 122,003, F = 191.33
p < 0.0001		df = 122,003, F = 170.39
p < 0.0001		df = 122,003, F = 46.82
p < 0.0001		df = 122,003, F = 49.20
p < 0.0001
According to the Tukey HSD test, means within a column followed by same lowercase letter and within a row followed by same uppercase letter do not differ statistically at p ≥ 0.05.
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Seal, D.R.; Liburd, O.; Li, J. Seasonal Abundance of Various Hymenopteran Parasitoids of Leafminers in Beans and Comparative Abundance in Bean, Tomato, and Squash. Agriculture 2023, 13, 1460. https://doi.org/10.3390/agriculture13071460

AMA Style

Seal DR, Liburd O, Li J. Seasonal Abundance of Various Hymenopteran Parasitoids of Leafminers in Beans and Comparative Abundance in Bean, Tomato, and Squash. Agriculture. 2023; 13(7):1460. https://doi.org/10.3390/agriculture13071460

Chicago/Turabian Style

Seal, Dakshina R., Oscar Liburd, and Jian Li. 2023. "Seasonal Abundance of Various Hymenopteran Parasitoids of Leafminers in Beans and Comparative Abundance in Bean, Tomato, and Squash" Agriculture 13, no. 7: 1460. https://doi.org/10.3390/agriculture13071460

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop