Exploratory Survey of Serpentine Leafminers and Its Parasitoids in the Highlands of Cordillera

NICASIO S. BAUCAS
Department of Agriculture-Regional Field Unit-Cordillera Administrative Region
Cordillera Integrated Agricultural Research Center
BPF Cpd., Sto. Tomas Road, Dontogan, 2600 Baguio City
Tel. No. (074) 444-5144
Telefax: (074) 444-8986

RAVINDRA C. JOSHI
Philippine Rice Research Institute
Maligaya, Muñoz Science City, 3119 Nueva Ecija
Tel. No. (044) 4560-285 Local 227
Fax: (044) 4560-112

ELIZABETH A. VERZOLA
Department of Agriculture-Regional Field Unit-Cordillera Administrative Region
BPI Complex, Guisad, 2600 Baguio City
Telefax: (074) 443-4621

ABSTRACT
A survey was conducted from July 2000 to December 2001 to generate information on serpentine leafminer flies belonging to the family Agromyzidae, their host plants, and indigenous parasitoids in selected municipalities of the Cordillera. Leaf samples of vegetable crops, ornamental plants, and weeds infested with serpentine leafminers were collected from the fields, and reared in the laboratory for emergence of leafminer and parasitoids. Specialists identified leafminer species both by conventional and modern molecular taxonomic tools while parasitoids were determined using conventional taxonomic keys. A total of 39 municipalities from the six Cordillera provinces, including Baguio City, were surveyed. We identified 26 vegetable crops and 19 ornamental plants and weeds that were infested by leafminers. Five leafminer species were identified. Four species belonged to genus Liriomyza and one species belonged to genus Chrotomyia. Their taxonomic identification were: Liriomyza huidobrensis (Blanchard), Liriomyza trifolii (Burgess), Liriomyza sativae Blanchard, Liriomyza chinensis (Kato), and Chrotomyia horticola. The indigenous parasitoids identified were: Asecodes delucchii (Boucek), Diglyphus isaea (Walker), Hemiptarsenus varicornis (Girault), Neochrysocharis formosa (Westwood), Neochrysocharis okazakii Kamijo, Pnigalio katonis (Ishii), Quadrastichus liriomyzae Hansson & LaSalle, Opius sp., and Zagrammosoma sp.

Keywords: Survey, Cordillera, Serpentine leafminers, Indigenous parasitoids, Distribution, Cultivated plants, Weeds, Outbreak, Liriomyza spp.

INTRODUCTION

An insect fly unknown to farmers started to devastate potato crop in Loo, Buguias, Benguet in September 1999. In December of the same year, the outbreak of this pest was reported officially to the Department of Agriculture-Cordillera Administrative Region Field Unit (DA-CARFU), and other agricultural institutes based in Baguio including the Office of the Provincial Agriculturist (OPAg), Benguet. The pest was identified as leafminer based on its damage symptoms, but lacked zoological identity. In response, the DA-CARFU in concert with agricultural agencies created the Potato Leafminer Task Force (PLMTF). The PLMTF members were tasked to make field visits and provide quick response services to abate the leafminer problem.

Rationale:
Extensive research has been done on leafminer flies in the United States, Netherlands, West Indies, Japan, and Peru. Its outbreak in the Province of Benguet, Philippines was of recent origin. Therefore, most extension materials and taxonomic identifications were referred only from the International Potato Center (CIP) publications. Absolutely there were no refereed publication on leafminer flies from the Philippine ecosystems, which could guide on species complexity, their indigenous natural enemies, ecology, and management. In the book of Dr. Clare R. Baltazar entitled “An Inventory of Philippine Insects”; no mention has been made on the observance of Liriomyza spp. 
Likewise, recent unpublished work of PLMTF indicated that leafminer flies have infested several localities in Benguet and Mt. Province, but failed to identify various leafminer species on various crops and locations. It basically reported that in close coordination with the municipal local government units (LGUs), the municipal offices reported in few months time that out of the eight municipalities in Benguet that reported infestation, there were already a total of more than 1,000 hectares grown with vegetable crops that were infested. It noted that in September 1999, leafminer invasion in Benguet already amounted to P19M.
Since there is almost no basic information on leafminers and their indigenous natural enemies currently available in the Cordilleras as basis for management options, this research was pursued. The result of this exploratory work would provide information for the development of component technologies and management strategies against leafminers devastating potato, vegetables and ornamental industries in the Cordilleras.

Review of Literature. 
Several species of Liriomyza have been reported worldwide, except from the Philippines. According to Parrella (1987), the genus Liriomyza, erected in 1894, contains more than 300 species. They have wide distribution, abundant in temperate areas; though few species inhabit in the tropics. Within this genus 23 species are economically important, known to cause damage to agricultural and ornamental plants by their leaf-mining activity. Many of these damaging species are polyphagous, though this characteristic is uncommon among the family Agromyzidae. Of 2,450 described species in this family only 11 are considered to be polyphagous, and five of these are in genus Liriomyza. 
In 1984, Langefeld mentioned four major species of leafminers, namely: Liriomyza huidobrensis, Liriomyza sativae, Liriomyza trifolii, and Chrotomyia syngenesiae. In the same year, Parrella cited that the pea leafminer, Liriomyza huidobrensis (Blanchard) has a history of causing serious economic damage to ornamental plants and vegetable crops in California and South America. L. huidobrensis originated in the neotropics, and had distribution confined to Central and South America until the 1980’s. Thereafter, it rapidly spread to other areas in Africa, Europe, and Asia (Cisneros, et al., 1998), and most recent outbreak in Israel in 1992 (Weintraub, et al. 1997). Likewise, Macdonald (1991) cited that Liriomyza trifolii was first identified in UK in 1977 on Chrysanthemum cuttings imported from Malta and Kenya. Earlier in 1978, Poe et al. reported that Liriomyza sativae is a recurring pest of potato and tomato crops in Florida, USA. Few reported host plants infested by complex of Liriomyza spp. included watermelons in Hawaii (Lynch et.al, 1987), cantaloupes and peppers (Getzin, 1960); and Aster, Dahlia, Galinsoga, beans, garden pea, eggplant, potato, celery, and carrot (Stegmaier, 1968). On the other hand, Cisneros et al. (1998) observed in Peru’s central coast, a rich complex of parasitoids species regulated leafminers. They reported the most abundant ectoparasitoid as Digliphus spp. and two endoparasitoids, Halticoptera arduine, and Chrysocharis spp. As early as 1966 in Florida, Stegmaier identified five kinds of parasitoids from three Hymenoptera families parasitic on Liriomyza munda. They were: Braconidae - Opius spp., Eulophidae - Chrysocharis spp., closterocerus cinctipennis, Derostenus spp., and Pteromalidae - Haltecopetra patellana.

OBJECTIVES 

A. General: To generate exact information on the leafminers, their natural enemies, and leafminer hosts in the locality for better management of leafminers.
B. Specific:
1. To map out the areas affected by one or several species of leafminers on vegetable crops and ornamentals plants; and
2. To determine the natural enemies of leafminers in the Cordillera and their potential for management of leaf miners.

METHODOLOGY

The survey period was from July 2000 until December 2001. It covered 39 selected municipalities in the 6 provinces of the Cordillera namely Abra, Apayao, Benguet, Ifugao, Kalinga, and Mountain Province, including Baguio City. These municipalities were identified for large areas planted to vegetable crops and ornamental plants. Leaf samples of vegetable crops, ornamental plants, and weeds showing stipples and mines caused by serpentine leafminers were collected in the field. Samples may contain all or either the following development stages (eggs, larvae, pupae) of leafminers. Adults were not collected in the field for identification purposes to avoid error on their exact host plants as they may be transient. Samples were collected in the field and were placed individually in plastic containers labeled with the name of crop, location, date, and collector name(s). These were brought to the laboratory and then transferred to plastic jars, covered with cloth, and then retained till adults of leafminers and or parasitoids emerged. The emerging adults (leafminers and parasitoids), were collected and sent for identification to specialists. Leafminers were identified through DNA sequence analysis by Dr. S. Scheffer, United States Department of Agriculture (USDA) (Figure 1), and through morphological structures by Dr. M. Sasakawa, Dr. A. Iwasaki (from Japan), Dr. D. Henshaw (UK), and Dr. M. Martinez (France). Parasitoids were identified by Dr. J. LaSalle (Australia), Dr. K. Kamijo, Dr. K. Konishi (from Japan). Host plants particularly the weed species were identified using the book published by the Weed Science Society of the Philippines, UPLB, College, Laguna (1984) entitled “Major Weed in the Philippines ”authored by Moody, K., Monroe, C.E., Lubigan R.T., and Paller, A.C. Jr. Likewise, additional samples were collected for determination of the presence of parasitoids in the different areas but not necessarily for species identification. 

RESULTS AND DISCUSSION

Areas surveyed in CAR with serpentine leafminer cases

All of the 39 municipalities within the 6 provinces of Cordillera, and Baguio City surveyed showed the presence of serpentine leafminer infestation (Table 1 & Figure 2). The province of Benguet where outbreak status was observed had all its 13 municipalities, including Baguio City, affected with LM. It was followed by Mountain Province, Ifugao, Abra, Apayao, and Kalinga with 8, 6, 5, 4, and 3 municipalities, respectively. 

Since most of the areas visited and sampled harbored 100% the leaf-mining flies, the survey results suggested that they are probably widely distributed in the Cordillera. 

Identified leafminer species and their distribution in the different provinces of Cordillera 

There were 5 different leafminer species infesting vegetables, ornamental crops and weeds in the Cordillera (Table 2). These were identified as Liriomyza huidobrensis (Blanchard); Liriomyza trifolii (Burgess); Liriomyza sativae (Blanchard), Liriomyza chinensis (Kato); and Chrotomyia horticola. The result showed that these species were found in the following provinces: L. huidobrensis and L. trifolii in Benguet, Ifugao, Mt. Province and Baguio City; L. sativae and L. chinensis in Benguet, Ifugao, and Mt. Province; and C. horticola in Benguet and Baguio City. In terms of location, Benguet had all the five species. Ifugao and Mountain Province had L. huidobrensis, L. trifolii, L. sativa, and L. chinensis; while Baguio City had L. huidobrensis, L. trifolii, and C. horticiloa. Species identification in Abra, Apayao, and Kalinga is still under review. A distribution map of leafminer species in the Cordillera is presented in Figure 3. The leafminer species L. huidobrensis, L. sativae, and L. trifolii that were identified through DNA sequence analysis, were found to be identical with the specimens identified from other countries.

Host plants of leafminer species identified in the Cordillera 

There were 26 vegetable crops, 19 ornamental plants, and weeds infested by serpentine leafminers (Table 3). Benguet registered the highest number of host plants with a total number of 45, followed by Mountain Province (31), Ifugao (15), Kalinga (13), Baguio City (12), Apayao (8), and Abra (5). 

Among those crops considered by farmers as having been economically damaged are celery, chinese cabbage, chrysanthemum, onion leek, potato and tomato. Likewise other important crops infested are bell pepper, bitter gourd, broccoli, carrot, chayote, cucumber, eggplant, garden pea, gobo, Japanese melon, lettuce, mustard, onion leek, okra, patani, peanut, pechay, radish, sitao, snap beans, sponge gourd, squash, sweet potato, water cress, and Zucchini. It also includes ornamentals and weeds such as Amaranthus spinesus L., “amti” (Physalis angulata L.), “ar-aritos” (Heliotropium indicum L.), aster, “bangbanget”, “bunot”, dahlia, “gagattang” (Emilia sonchifolia L.), “gandey”, (Rorippa indica), impatience, mugwort (Artemisia vulgaris), “pagpagey”, “palpalsik”, “pullet” (Bidens pilosa L.), “sapsapon” (Crassocephalum crepidioides Benth S. Moore), Galinsoga parviflora Cav., shasta daisy, sweet william, wild legume and wild tomato. 

The wide range of host plants identified in this survey confirmed their polyphagous behavior. Similar observations in other countries by Stegmaier (1968) listed aster, dahlia, galinsoga, beans, garden pea, eggplant, potato, celery, and carrot, among others as host plants of leafminers. The wide range of host plants could contribute for this pest to stay longer in an area. Weeds may serve as alternate host during the off-season. 

Natural enemies (parasitic wasps) identified in the Cordillera

There were 9 parasitic wasps (parasitoids) that emerged from leafminer samples collected from the field and reared in the laboratory. Parasitoids that emerged were: Asecodes delucchi (Boucek), Diglyphus isaea (Walker); Hemiptarsenus varicornis (Girault); Neochrysocharis Formosa (Westwood); Neochrysocharis okazakii Kamijo; Pnigalio katonis (Ishii); Quadrastichus liriomyzae Hansson & LaSalle; Zagrammosoma sp., and Opius sp. (Table 4).

Sample collections from the different provinces showing emergence of parasites species are: Benguet (7) with Diglyphus isaea (Walker), Hemiptarsenus varicornis (Girault), Pnigalio katonis (Ishii), Neochrysocharis okazakii (Kamijo), Neochrysocharis Formosa (Westwood), Quadrastichus liriomyzae Hansson & LaSalle, and Zagrammosoma sp.; Baguio City (5) with Diglyphus isaea (Walker), Hemiptarsenus varicornis (Girault), Neochrysocharis okazakii (Kamijo), Neochrysocharis Formosa (Westwood), and Opius sp.; and Ifugao (3) with Asecodes delucchi (Boucek), Quadrastichus liriomyzae Hansson & LaSalle, and Opius sp. A distribution map of natural enemies in the Cordillera is presented (Figure 4).

The presence of Diglyphus spp in the country is very interesting to uncover if it is indigenous in the Philippines or was introduced. Dr. LaSalle (per com) admitted that this is his first time to run across large numbers of this species of parasitoid in South East Asia (which includes Philippines), though present in farther north (China and Japan). 

Parasitoids emergence on different serpentine leafminer species infesting various host plants

The presence of leafminer species on its host plants, and emergence of parasitoid species on its leafminer host are presented in Table 5. The dominant species of leafminer infesting plants is Liriomyza huidobrensis (Blanchard), followed by Liriomyza sativae (Blanchard), Liriomyza trifolii (Burgess), Liriomyza chinensis (Kato) and Chrotomaya horticola.

a. Leafminer species vs. host plants
Leafminer infestation on crops varied. L. huidobrensis infested 27 plants such as bitter gourd, broccoli, cabbage, carrot, celery, chinese cabbage, cucumber, eggplant, garden pea, burdock (gobo), lettuce, mustard, onion leek, pechay, potato, radish, sitao, snap beans, sponge gourd, tomato, water cress, zucchini, aster, chrysanthemum, and wild cherry tomato. L. sativae infested 9 plants such as Physalis angulata L., cucumber, pechay, potato, snap beans, Squash, tomato, wild cherry tomato, and zucchini. L. trifolii infested 7 plants such as cucumber, pechay, snap beans, squash, tomato, zucchini, and mugwort. C. horticola were found in 4 plants such as garden pea, lettuce, radish, and Galinsoga parviflora, while L. chinensis infested 3 plants such as pechay, radish, and lettuce. 

b. Parasitoid species vs. leafminer (vs. host plants)
Based on host plants of emerging leafminers, Digliphus isea (Walker) parasitized different leafminer species in 19 plants. Asecodes delucchi emerged from 12 host plants, Diglyphus isaea from 18 host plants, Hemiptarsenus varicornis from 7 host plants, Pnigalio katonis from 5 host plants, Neochrysocharis okazakii from 7 host plants, Neochrysocharis formosa from 8 host plants, Quadrastichus liriomyzae from 5 host plants, and Opius sp. from 2 host plants.

The different leafminer species were definitely parasitized by the following parasitoids: Liriomyza huidobrensis --- Asecodes delucchi (Boucek), Diglyphus isaea (Walker), Hemiptarsenus varicornis (Girault), Neochrysocharis formosa (Westwood), Quadrastichus liriomyzae Hansson and LaSalle, Opius sp., Zagrammosoma sp.; Liriomyza trifolii --- Diglyphus isaea (Walker), Pnigalio katonis (Ishii), Quadrastichus liriomyzae Hansson and LaSalle; and Liriomyza sativa --- Diglyphus isaea (Walker) (Table 6). On the other hand, the following leafminer species are possibly parasitized by the following parasitoids: Liriomyza chinensis --- Diglyphus isaea (Walker), Hemiptarsenus varicornis (Girault), Neochrysocharis okazakii (Kamijo), Neochrysocharis formosa (Westwood), Opius sp.; and Chrotomyia horticola --- Diglyphus isaea (Walker), Hemiptarsenus varicornis (Girault), Quadrastichus liriomyzae Hansson and LaSalle, Opius sp.

CONCLUSION AND RECOMMENDATIONS

Conclusion

The leaf plant samples collected in areas surveyed from the six provinces and one city in the Cordillera had been infested with serpentine leafminer. The 39 municipalities surveyed in the provinces that harbored leafminers were: Abra (Boliney, Bucay, Bucloc, Pidigan, and Sallapadan); Apayao (Sta Marcela, Flora, Puydtol, and Luna); Benguet (Atok, Bakun, Bokod, Buguias, Itogon, Kabayan, Kapangan, Kibungan, La Trinidad, Mankayan, Sablan, Tuba, and Tublay); Ifugao (Asipulo, Banaue, Kiangan, Lagawe, Lamut, and Tinoc); Kalinga (Pinukpuk, Rizal, and Tabuk); Mountain Province (Barlig, Bauko, Besao, Bontoc, Sabangan, Sadanga, Sagada and Tadian); and Banguo City.

There were five serpentine leafminer species identified in the Cordillera region. These are Liriomyza huidobrensis (Blanchard), Liriomyza trifolii (Burgess), Liriomyza sativae (Blanchard), Liriomyza chinensis (Kato), and Chrotomyia horticola. The identified species were observed in Benguet, Ifugao, Mountain Province and Baguio City. 

The host plants infested by serpentine leafminers were categorized into three groups: vegetable crops (Bell pepper, Broccoli, Cabbage, Carrot, Celery, Chinese Cabbage, Cucumber, Eggplant, Garden Pea, Gobo, Lettuce, Mustard, Mongo, Onion Leek, Patani, Pechay, Potato, Radish, Red Cabbage, Sitao, Snap Beans, Sponge Gourd, Squash, Tomato, Water Cress, Zucchini); ornamental plants (Chrysanthemum, Dalhia, Impatiens, Sweet Williams, Shasta Daisy); and weeds (Amaranthus spinesus. L., Amti (Physalis angulata L.), Aster, “Ar-aritos” (Heliotropium indicum L.); “Bangbanget”, “Bunot”, Cotton Weed, “Gagattang”, (Emilia sonchifolia L.),“Gandey” (Rorippa indica), Galinsoga parviflora Cav., Mugwort (Artemisia vulgaris),“Palpalsik”, “Pulet” (Bidens pilosa L.), “Sapsapon” (Crassocephalum crepidioides), Wild Sunflower, “Tabtabako”, Wild Cherry Tomato).

The serpentine leafminers were parasitized by nine indigenous parasitoids such as: Asecodes delucchi (Boucek), Quadrastichus liriomyza Hansson and LaSalle, Diglyphus isaea (Walker), Opius spp., Hemiptarsenus varicornis (Girault), Neochrysocharis okazakii (Kamijo), Pnigalio katonis (Ishii), Zagrammosoma sp., and Neochrysocharis fomosa (Westwood). Their distribution in the region covers Benguet, Ifugao and Baguio City. In Abra, Apayao, Kalinga, and Mountain Province, species are still to be determined.
The numbers of leafminer parasitoids on leafminer species and on different host plants were complex. One crop was attacked by more than one leafminer species. A leafminer species could also infest more than one host plant. Similarly, most parasitoids attacked more than one leafminer species. 

Recommendations

It is recommended that the indigenous natural enemies should be conserved in the farmers’ fields and in certain cases augmentative releases could be considered. The degree of parasitism in the field and mass rearing of parasitoids should be undertaken for future biological control program. This research should be coupled by the determination of the specific (dominant) parasitoid for a leafminer species and the host plant. 

ACKNOWLEDGMENTS

We are grateful to serpentine leafminer taxonomists and parasitoid specialists around the globe for their kind assistance and cooperation: Dr. S. Scheffer, United States Department of Agriculture (USDA) for identifying leafminer species through DNA sequence analysis, and Drs. M. Sasakawa, A. Iwasaki (from Japan), D. Henshaw (UK), and M. Martinez (France) through morphological structures; and Drs. J. LaSalle (Australia), K. Kamijo and K. Konishi (from Japan) for identifying parasitoids. The contact with the Japanese leafminer taxonomists, parasitoid specialists, and leafminer experts (Dr. T. Saito and Dr. Y. Abe) were made through the kind introduction by Dr. T. Hidaka, Former Research Director, JIRCAS, Japan to Dr. R. C. Joshi. 
The authors would like to thank Geraldine L. Sacla and Joseph A. Panas for their untiring efforts and assistance in the field collection and rearing of leaf samples in the laboratory. Special thanks also goes to the following for their contribution in collecting plant samples: E. Pitas, D. Dimas, M. Baucas, N. Wales, and G. Binmaliw. 
Special thanks is also extended to Charles A. Picpican of GIS Unit, DA-CHARM Project for providing the digitized Cordillera map, and Dennis Glenn L. Flores for the lay-out and inputting of data and vital information in the figures. 
The authors finally express their gratitude to Hon. Edgardo J. Angara for providing financial assistance to this project during his term as Secretary of the Department of Agriculture.

LITERATURE CITED

B.S.U. Research Digest. 2000. A Quarterly Publication of the Office of the Vice president for Extension. Benguet State University, La Trinidad, Benguet. Vol. II. No.1 January – March 2000. pp. 4,7.

CISNEROS, F and N. MUJICA. 1998. The leafminer fly in potato: plant reaction and natural enemies as natural mortality factors. CIP Program Report 1997-1998. CIP Lima, Peru. pp. 129, 134.

GETZIN L.W. 1960. Selective Insecticides for vegetables for Vegetable Leaf-Miner Control and Parasite Survival. Journal of Economic Entomology. Vol. 53 No. 5, p. 872.

JOSHI, R.C., S.J. SCHEFFER, E.A. VERZOLA and N.S. BAUCAS. 2000. Primer on leafminers of Vegetables in the Cordillera Administrative Region. Philippines. DA-RFU-CAR, Potato Leafminer Task Force. Pp. 4-6, 15-16.

LANGEFELD, J. 1984. Identifying the leafminer. Grower Talks. September 1984. pp.19-
21.

LYNCH A.J. and W. M. JOHNSON 1987. Stratified Sampling of Liriomyza spp. (Diptera: Agromyzidae) and Associated Hymenopterous Parasites on Watermelon. Journal of Economic Entomology. Vol. 80, No. 6, p. 1254. 

MACDONALD, O.C. 1991. responses of the alien leaf miners Liriomyza trifolii and Liriomyza huidobrensis (Diptera: Agromyzidae) to some pesticides scheduled for their control in the UK. Crop Protection. Vol. 10, p. 509.

PARRELLA, M.P. 1987. Biology of Liriomyza. Ann. Rev. Entomol. 32:201-224.

PARRELLA, M.P. and J.A. BETHKE. 1984. Biological studies of Liromyza huidobrensis (Diptera: Agromyzidae) on Chrysanthemum, Aster, and Pea. J. Econ. Entomol. 77:342.

POE, S.L., P. H. EVERET and C. A. MUSGRAVE. 1978. Insecticidal effects on Liromyza sativae larvae and their parasites on tomato. J. Ga. Entomol. Soc. 13: 322.

STEGMAIER, C. E., Jr. 1966. Host plants and parasites of Liriomyza munda in Florida (Diptera: Agromyzidae). Fla. Entomol. 49(2): 83.

_________________ 1968. A Review of recent literature on the host plant range of the 
Genus Liriomyza Mik (Diptera: Agromizidae) in the continental United States and Hawaii, excluding Alaska. The Florida Entomologist 51(3):_____.

WEINTRAUB, P. G. and A. R. HOROWTIZ. 1997. Systemic effects of a neem insecticide 
on Liriomyza huidobrensis larvae. Phytoparasitica 25(4): 283. 

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TABLES

Table 1. Areas surveyed in CAR, Philippines with serpentine leafminer infestation cases.

Table 2. Distribution of serpentine leafminer species identified in CAR, Philippines. 

* Samples are still being identified.

Table 3. Host plants of serpentine leafminer species identified in CAR provinces and Baguio City, Philippines.

Table 4. Distribution of leafminer parasitoids in CAR, Philippines.

Table 5. Parasitoid emergence on different leafminer species infesting various host plants, CAR, Philippines.

Table 6. Definite and possible leafminer host of parasitoids, CAR, Philippines.

DH

PH

DH

PH

DH

PH

DH

PH

DH

PH

DH

PH

DP

PH

DH

PH

DH

DH - Definite Host
PH - Possible Host

Parasitoid Species: 

AD - Asecodes delucchi (Boucek) 
DI - Diglyphus isaea (Walker) 
HV - Hemiptarsenus varicornis (Girault)
PK - Pnigalio katonis (Ishii)
NO - Neochrysocharis okazakii (Kamijo)
NF - Neochrysocharis formosa (Westwood)
QL - Quadrastichus liriomyzae Hansson and LaSalle
OP - Opius sp.
ZA - Zagrammosoma sp.