Journal of Entomology and Zoology Studies 2017; 5(4): 277-283

E-ISSN: 2320-7078 P-ISSN: 2349-6800 JEZS 2017; 5(4): 277-283 New host record of three hymenopteran © 2017 JEZS parasitoids associated with Melanagromyza obtusa Received: 04-05-2017 Accepted: 05-06-2017 (Malloch) and their level of natural parasitism B Chiranjeevi Department of Agricultural

Entomology, Sri B Chiranjeevi and NR Patange Krishnadevaraya College of Agricultural Sciences, Abstract Anantapur-515002 (ANGRAU), Andhra Pradesh, India The present study was conducted on the incidence of parasitoids of Melanagromyza obtusa (Malloch) at Research Farm and Laboratory, Agricultural Entomology Unit, Agriculture Research Station, Badnapur NR Patange (Vasantrao Naik Marthwada Krishi Vidyapeeth [VNMKV], Parbhani), Maharashtra, India during Kharif National Agricultural Research season of 2014-15. Six hymenopteran parasitoids recorded were; Eduderus sp. Ashmead, Systasis Project, Aurangabad-431005 dasyneurae Mani, Torymus sp. Dalman, Epitranus sp. Walker, Eurytoma sp. Illiger and Ormyrus sp. (VNMKV, Parbhani), Walker. As per the literature available and reviewed; Systasis dasyneurae Mani, Torymus sp. Dalman and Maharashtra, India Epitranus sp. Walker are the first ever record for new host association reported from M. obtusa maggots and pupae as ecto and endo-parasitoids. The incidence of natural parasitism of Systasis dasyneurae Mani, Torymus sp. Dalman and Epitranus sp. Walker ranged from 1.69 to 7.32, 5.08 to 29.27 and 2.13 to 4.88 per cent, with a mean parasitism of 0.98, 9.70 and 0.64 per cent, respectively. The new record of natural parasitism of M. obtusa larvae and pupae by Torymus sp., Systasis dasyneurae and Epitranus sp. would add knowledge on biological control of the pest.

Keywords: Melanagromyza obtusa, Natural parasitism, New host record, Epitranus sp., Systasis dasyneurae and Torymus sp.

1. Introduction Melanagromyza obtusa (Malloch) (Diptera: Agromyzidae), commonly known as pigeonpea pod fly or red-gram pod fly or tur pod fly is a major pest; attacking pigeonpea and act as a key [1, 2] pest causing heavy crop losses in India . In recent years, the pigeonpea growing areas of Maharashtra as well as remaining states of India have been threatened by the occurrence of notorious pest; pigeonpea pod fly, M. obtusa. M. obtusa caused considerable loss in both quality and quantity of seed or grain of pigeonpea crop. It was reported to infest 12 to 100 per cent pods causing losses of 2.4 to 95.0 per cent on seed and 2,50,000 tonnes by weight [3, 4, 5].

The total loss in terms of production and monetary value is estimated to be around 250 to 300 [6] [7] thousand tones and 3750 to 4500 million rupees per year, respectively . While, have estimated losses due to pod fly damage at Rs. 16,384 million or US $ 256 million annually [8]. The maggot as damaging stage of pod fly surpasses inside the pods and do not show any symptoms from outside until exit of the adult, which makes complicacy for their management [9, 10] . Though concealed behavior of pod fly renders ineffective control by insecticides; till date, chemicals are the only available efficient strategy against M. obtusa yet it involves several limitations like no promising management of the pest even after two or three applications of insecticides, the crop still undergo considerable losses and also the insecticides are mostly unsafe to natural enemies and also cause hazards to environment and mankind [11]. Biological control is emphasized as an important remediation strategy to combat pest [12-15] outbreaks by many workers . The natural bio-control agents play an important role in the management of pests. Till date, several chalcidoid parasitoids are known to attack this notorious pest. The occurance of parasitism level has been recorded by various researchers [14, Correspondence 16-24] and more than twenty hymenopteran parasitoids have been reported on pod fly immature B Chiranjeevi [25-39] Department of Agricultural stages . Among them Euderus lividus (Eulophidae) as larval ecto-parasitoid and Ormyrus Entomology, Sri orientalis (Ormyridae) as larval-pupal endo-parasitoid reported as major bio-control agents of Krishnadevaraya College of M. obtusa and caused 80.00 and 46.66 per cent parasitism [23]. The use of natural enemies of Agricultural Sciences, the pod fly, as bio-control agents for its management is a promising and viable strategy [13]. Anantapur-515002 (ANGRAU), Therefore, the present study was carried out to know the potential parasitoids of pigeonpea pod Andhra Pradesh, India fly, M. obtusa to promote the eco-friendly management of this notorious pest. ~ 277 ~ Journal of Entomology and Zoology Studies

2. Materials and Methods presented below. An experiment was conducted at Research Farm and Laboratory, Agricultural Entomology Unit, Agricultural 1) Genus Systasis Mani Research Station, Badnapur (Vasantrao Naik Marathwada : Chalcidoidea: Pteromalidae: Ormocerinae Krishi Vidyapeeth [VNMKV], Parbhani), Maharashtra, India to study the incidence of parasitoids of Melanagromyza (a) Synonyms obtusa (Malloch) with their extent of natural parasitism = Guieralia Risbec, 1951 during Kharif season of 2014-15. The pigeonpea genotype, = Paruriella Girault, 1913 ICP-8863 (Maruthi) was raised in a plot size of 9.0 m × 9.0 m = Systasis Walker, 1834 with a spacing of 60 cm and 30 cm between rows and plants, = Systasis (Systasina) Boucek, 1956 respectively; along with standard agronomical practices to raise a good crop. No insecticide was applied to protect the (b) Diagnostic characters crop from the infestation of M. obtusa. The larvae and pupae Fore wing venation reduced, with fewer than 2 closed cells. of pod fly, M. obtusa were collected from randomly selected Tarsi 5 segmented, protibial spur curved apically and bifid. 100 pigeonpea pods covering all the plants of net plot area Funicle with 5 or more segments. Mesopleuron not swollen, (7.8 m × 8.4 m) at weekly intervals on basis of standard concave, variously sculptured, shorter than high. Hind femur meteorological weeks (SMW) till harvest of crop by using not enlarged, >3X as long as broad, smootgh ventrally. destructive sampling method [15, 24]. The collected larvae and Axillar and parascutal carinae converging on dorsum mesad pupae were maintained in plastic vials (30 ml capacity) at the of wing base in V-like fashion. Pronotum transverse in dorsal rate of one per vial and reared on pigeonpea seeds at ambient view. Head and dorsum lacking umbilicate sculpture, usually laboratory conditions (25±2 °C temperature and 80±2% reticulate. Body usually metallic. Pronotum in dorsal view not relative humidity) for observing the emergence of different narrowed medially. Notauli at least visible anteriorly on parasitoids. Emerged parasitoids were identified based on mesoscutum, often complete. Protibia lacking dorsoapical taxonomic keys with the help of taxonomists. Thus the data spicules. Head without occipital carina or if with carina then obtained on parasitoids emergence from the host stages metacoxa usually subcircular in cross section and narrowly (larvae and pupae of M. obtusa) was processed properly to attached to mesosoma. Fore wing venation was different than calculate the per cent parasitism and to interpretation of all chalcidoids. Thorax moderately convex, funicle segments results. The per cent parasitism was calculated by using the and pedicel different. Fore wing with disc moderately setose, following formulae. area between post marginal and stigmal usually bare, in male antennal scape never flattened. Mandibles heterodont, left 3 Number of infected larvae / pupae and right 4 - dentate. Antenna with second anellus thick. Fore Per cent larval / pupal parasitism = ------× 100 wing with stigma round. Total number of larvae / pupae (c) Distribution Number of infected larvae + pupae India: Karnataka, Bihar, Haryana, Maharashtra, Uttar Pradesh Per cent total parasitism = ------× 100 and Madhya Pradesh; Spain: Balearics. Total number of larvae + pupae (d) Biology 3. Results and Discussion Primary parasites of the larvae of Cecidomyiidae [41, 42] and The present investigations revealed presence of six Pyralidae [43]; which were quite important pests of hymenopteran parasitoids namely, Euderus sp. Ashmead economically important plants. (Hymenoptera: Chalcidoidea: Eulophidae), Systasis dasyneurae Mani (Hymenoptera: Chalcidoidea: Syastasis dasyneurae Mani (Fig. 1) Pteromalidae), Torymus sp. Dalman (Hymenoptera: = Semiotellus dasyneurae (Mani, 1939) Chalcidoidea: Torymidae), Epitranus sp. Walker It was recorded on Cv. ICP-8863 of Cajanus cajan from (Hymenoptera: Chalcidoidea: ), Eurytoma sp. Agricultural Research Station, Badnapur, Maharashtra during Illiger (Hymenoptera: Chalcidoidea: Eurytomidae) and the year 2014-2015. Syastasis dasyneurae Mani is an ecto- Ormyrus sp. Walker (Hymenoptera: Chalcidoidea: larval parasitoid of M. obtusa. The incidence of infestation Ormyridae) on immature stages i.e. larvae and pupae of and parasitism is given in Table 1. Melanagromyza obtusa (Malloch). Among these parasitoids, The activity of Systasis dasyneurae Mani on pod fly maggot Euderus sp. Ashmead, Systasis dasyneurae Mani and was observed on 3rd SMW i.e. one and three parasitized larvae Torymus sp. Dalman recorded as ecto-parasitoids of M. per 100 pods, which increased gradually and attained its peak obtusa maggots; and Epitranus sp. Walker, Eurytoma sp. on 4th SMW (three parasitized larvae per 100 pods). Later it Illiger and Ormyrus sp. Walker recorded as endo-parasitoids was declined and minimum parasitized larvae was observed of M. obtusa pupae. No reports of Systasis dasyneurae Mani, on 5th SMW (one parasitized larvae per 100 pods) with a Torymus sp. Dalman and Epitranus sp. Walker as parasitoids mean of 0.45 parasitized maggots per 100 pods over a period of M. obtusa was documented earlier. In the present study, the of 11 meteorological weeks (52nd to 10th SMW). parasitoids; Systasis dasyneurae Mani, Torymus sp. Dalman The natural parasitism of pod fly maggots due to Systasis and Epitranus sp. Walker emerged from maggots and pupae dasyneurae Mani was ranged from 1.69 to 7.32 per cent, and, of M. obtusa is a new record associated with pod fly, M. it’s maximum level was observed on 4th SMW (7.32 per cent) obtusa. The emergence of Systasis dasyneurae Mani, and the minimum was observed on 3rd SMW (1.69 per cent), Torymus sp. Dalman and Epitranus sp. Walker are the first respectively with a mean of 0.98 per cent over a period of 11 ever record on pigeonpea pod fly, M. obtusa maggots and meteorological weeks (52nd to 10th SMW). Later the pupae as per the literature available and reviewed. parasitism gets declined and no parasitism was observed from Brief description of the new parasitoids of pod fly recorded 6th SMW onwards. based on the morphological characters and taxonomic keys is ~ 278 ~ Journal of Entomology and Zoology Studies

(a) Larva of Systasis dasyneurae (b) Adult of Systasis dasyneurae

Fig 1: Immature (a) and adult (b) stages of Systasis dasyneurae Mani obtained from pod fly maggots.

Table 1: Level of parasitism of three new hymenopteran parasitoids of M. obtusa.

Parasitized larvae Parasitism (%) Epitranus sp. SMW Larva Pupa Systasis dasyneurae Torymus sp. Systasis dasyneurae Torymus sp. Parasitized pupae Parasitism (%) 52 47.00 0.00 0.00 0.00 0.00 20.00 0.00 0.00 1 59.00 0.00 3.00 0.00 5.08 41.00 0.00 0.00 2 60.00 0.00 5.00 0.00 8.33 37.00 0.00 0.00 3 59.00 1.00 14.00 1.69 23.73 41.00 2.00 4.88 4 41.00 3.00 12.00 7.32 29.27 47.00 1.00 2.13 5 57.00 1.00 9.00 1.75 15.79 41.00 0.00 0.00 6 54.00 0.00 4.00 0.00 7.41 38.00 0.00 0.00 7 30.00 0.00 3.00 0.00 10.00 22.00 0.00 0.00 8 14.00 0.00 1.00 0.00 7.14 9.00 0.00 0.00 9 13.00 0.00 0.00 0.00 0.00 4.00 0.00 0.00 10 2.00 0.00 0.00 0.00 0.00 9.00 0.00 0.00 Avg. 39.64 0.45 4.64 0.98 9.70 28.09 0.27 0.64 Total parasitism (%) 7.92

2) Genus Torymus Dalman concave, variously sculptured, shoter than high. Hind femur Hymenoptera: Chalcidoidea: Torymidae: Toryminae: not enlarged, >3X as long as broad, smootgh ventrally. Torymini Axillar and parascutal carinae converging on dorsum mesad of wing base in V-like fashion. Pronotum transverse in dorsal (a) Synonyms view. Head and dorsum lacking umbilicate sculpture, usually = Callimome Spinola, 1811 reticulate. Body usually metallic. Pronotum in dorsal view not = Callimomus Thomson, 1876 narrowed medially. Notauli at least visible anteriorly on = Diamorus Walker mesoscutum, often complete. Protibia lacking dorsoapical = Dihomerus Schulz, 1906 spicules. Head with occipital carina (may be fine). Metacoxa = Diomorus Walker, 1834 usually subtriangular in cross section and broadly attached to = Diomorus (Diomorus) Walker, 1834 mesosoma. Fore wing usually with marginal vein long and = Diomorus (Paradiomorus) Zerova & Seryogina, 2001 stigma vein short. Metapleuron separated by a sinuous line = Hemitorymus Ashmead, 1904 from mesopleuron, projecting anteriorly. Metafemur not = Lioterphus Thomson, 1876 convex ventrally, sometimes serrate. Marginal vein at most 5 = Misocampe Latreille, 1818 times as long as stigma vein and more than 3 times as long as = Misocampus Stephens, 1829 postmarginal vein. = Nannocerus Mayr, 1885 = Parasympiesis Brèthes, 1927 (c) Distribution = Syntomaspis Förster, 1856 Australia, Austria, Bulgaria, Canada, Costa Rica, Czech = Torymus Dalman, 1820 Republic, Czechoslovakia, Finland, France, Germany, = Torymus (Arctorymus) Zavada, 2003 Hungary, India, Italy, Japan, Korea, Korea, South Nearctic, = Torymus (Aretorymus) Zavada, 2003 Netherlands, New Zealand, Pakistan, Peoples' Republic of = Torymus (Callimome) Spinola, 1811 China, Spain, Switzerland, Trinidad & Tobago, Turkey, = Torymus (Callimomus) Thomson, 1876 United Kingdom, United States of America, USSR and West = Torymus (Lioterphus) Thomson, 1876 Africa. = Torymus (Paratorymus) Zerova & Seryogina, 2003 = Torymus (Syntomaspis) Förster, 1856 (d) Biology = Torymus (Torymus) Dalman, 1820 These were the primary parasites of the larvae of Bruchidae [44]; Curculionidae, Rhynchitidae, Scolytidae, Cecidomyiidae (b) Diagnostic characters [45], Tephritidae [46], Psyllidae [47], Tenthredinidae [48], Fore wing venation reduced, with fewer than 2 closed cells. Coleophoridae [45], Gelechiidae [49], Lasiocampidae [45] and Tarsi 5 segmented, protibial spur curved apically and bifid. Tortricidae [45]; which are quite important pests of Funicle with 5 or more segments. Mesopleuron not swollen, economically important plants. ~ 279 ~ Journal of Entomology and Zoology Studies

Torymus sp. Dalman (Fig. 2) parasitized larvae per 100 pods), respectively. Later it was This parasitoid was recorded on Cv. ICP-8863 of Cajanus declined and minimum infected larvae was observed on 8th cajan from Agricultural Research Station, Badnapur, SMW (one parasitized larvae per 100 pods) with a mean of Maharashtra during the year 2014-2015. It is recorded as ecto- 4.64 parasitized maggots per 100 pods over a period of 11 larval parasitoid of M. obtusa. The parasitoid larvae pupate in meteorological weeks (52nd to 10th SMW). pod itself. The number of parasitoids per pod varies with the Torymus sp. Dalman was found in the 1st SMW of January pest status. The incidence of pod infestation and parasitism is with 5.08 per cent parasitism. The incidence of parasitism given in Table 1. increased up to 29.27 per cent on 4th SMW by the end of The activity of Torymus sp. Dalman on pod fly maggot was January. Later it was declines and no parasitism was observed observed on 1st standard meteorological week (SMW) i.e. on 10th SMW of March, respectively, with a mean parasitism three parasitized larvae per 100 pods, which increased of 9.70 per cent. gradually and attained its peak on 3rd SMW (fourteen

(a) Larva of Torymus sp. (b) Adult of Torymus sp.

Fig 2: Immature (a) and adult (b) stages of Torymus sp. Dalman obtained from pod fly maggots.

3) Genus Epitranus Walker Hymenoptera: Chalcidoidea: Chalcididae: Epitraninae (C) Distribution (a) Synonyms Australia, Brazil, Guyana, Hawaii, India, Africa, Japan, = Anacryptus Kirby, 1883 Indonesia, Malaysia, Democratic Republic of Congo (Zaire), = Arretocera Kirby, 1883 Papua New Guinea, Sri Lanka, South Asia, Taiwan, United = Chalcitella Westwood, 1835 States of America and Thailand. = Chalcitelloides Girault, 1914 = Epitranus Walker, 1834 (D) Biology = Lamoundella Shafee & Dutt, 1986 Host data were rare but small moths of family Pyralidae and = Neoanacryptus Girault, 1913 Tineidae and some associated with stored grains were the = Paranacryptus Girault, 1915 hosts of members of this genus. Adults are usually found on = Pararretoceroides Mani, 1938 foliage of trees and shrubs but not found on grass usually [50]. Epitranus Sp. (Fig. 3) (b) Diagnostic characters It is recorded on Cv. ICP-8863 of Cajanus cajan from Fore wing venation reduced, with fewer than 2 closed cells. Agricultural Research Station, Badnapur, Maharashtra during Tarsi 5 segmented, protibial spur curved apically and bifid. the year 2014-2015. Epitranus sp. Walker is an endo- Funicle with 5 or more segments. Mesopleuron not swollen, parasitoid of M. obtusa pupae. The incidence of infestation concave, variously sculptured, shorter than high. Hind femur and parasitism is given in Table 1. enlarged, <3X as long as broad, dentate ventrally. Axillar and The parasitoid appeared for the first time during 3rd SMW of parascutal carinae converging directly above wing base in January with two parasitized pupae per 100 pods and in the arch like fashion. Abdomen not sessile, distinctly petiolate. next subsequent week i.e. 4th SMW with one parasitized Head without horns, post marginal vein of fore wings present. pupae per 100 pods, respectively, with a mean of 0.27 Antennal sockets present below the level of ventral margin of parasitized pupae 100 pods. The incidence of parasitism compound eyes. Petiole carinate and anterior margin decreased from 4.88 (3rd SMW) to 2.13 (4th SMW) per cent laminate. Gaster with slender striate petiole, gaster bulging during January and no parasitism was observed from 5th ventrally; antennal toruli located very low on a shield SMW onwards with a mean parasitism of 0.64 per cent. The protruding over mouth; scrobe virtually absent; marginal vein total parasitism of these three new parasitoids of M. obtusa very long, stigmal rudimentary, postmarginal absent. was 7.92 per cent.

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(a) Parasitized M. obtusa pupa (b) Adult of Epitranus sp.

Fig 3: Adult Epitranus sp. Walker along with its parasitized pupae (a, b) of pod fly.

The incidence of parasitism of Systasis dasyneurae Mani, 5. Chauhan R, Dahiya B. Damage due to pod borer and pod Torymus sp. Dalman and Epitranus sp. Walker was found low fly in early maturing genotypes of pigeonpea in Haryana. as compared to major parasitoids viz., Euderus lividus Indian Journal of Plant Protection. 1987; 15(1):5-9. Ashmead and Ormyrus orientalis Walker, respectively. 6. Lal SS, Katti G. Pod fly, Melanagromyza obtusa Malloch Therefore, two to three years continuous studies are required - A key pest of pigeonpea. Published by IIPR, Kanpur, throughout the crop season to evaluate the role of these new 1997, 26. parasitoids in the biological control of pigeonpea pod fly, M. 7. Sarika, Arora V, Iquebal MA, Rai A, Kumar obtusa. D. PIPEMicroDB: microsatellite database and primer generation tool for pigeonpea genome. Database, 2012. 4. Conclusion article ID bas054; doi:10.1093/database/bas054. From the present study, it can be concluded that the new host (http://database.oxfordjoumals.org). 7 February 2013. record of three hemenopteran parasitoids viz., Systasis 8. Sharma OP, Bhosle BB, Kamble KR, Bhede BV, Seeras dasyneurae Mani, Torymus sp. Dalman (ecto-larval NR. Management of pigeonpea pod borers with special parasitoids) and Epitranus sp. Walker (endo-pupal parasitoid) reference to pod fly (Melanagromyza obtusa). Indian associated with M. obtusa infesting Cajanus cajan would add Journal of Agricultural Sciences. 2011; 81(6):539-543. to the existing knowledge on the biological control of the 9. Spencer KA. Agromyzidae (Diptera) of Economic pest. The natural parasitism of these parasitoids ranged from Importance. Series Entomologica. Dr. W. Junk, The 1.69 to 7.32, 5.08 to 29.27 and 2.13 to 4.88 per cent, Hague, Netherlands. 1973; 9:1-419. respectively. However, natural occurrence of these new 10. Lal SS, Yadava CP. Ovipositional response of pod fly hymenopteran parasitoids on pigeonpea pod fly has paved a (Melanagromyza obtusa) on resistant pigeonpea (Cajanus new avenue for its control. cajan) selections. Indian Journal of Agricultural Sciences. 1994; 64(9):658-660. 5. Acknowledgement 11. Sarwar M. The dangers of pesticides associated with The authors are thankful to Dr. S. Manickavasagam, Professor public health and preventing of the risks. International in Entomology, Faculty of Agriculture, Annamalai Journal of Bioinformatics and Biomedical Engineering. University, Annamalai Nagar, Tamil Nadu and Dr. P.M. 2015; 1(2):130-136. Sureshan, Sceintist, Western Ghat Regional Centre, 12. Shanower TG, Lal SS, Bhagwat VR. Biology and Zoological Survey of India, Calicut, Kerala, India for management of Melanagromyza obtusa (Malloch) identification of parasitoids under present investigation (Diptera: Agromyzidae). Crop Protection. 1998; emerged from the maggots and pupae of M. obtusa. 17(3):249-263. 13. Singh SP. Studies on hymenopteran parasites of 6. References Melanagromyza obtusa (Malloch) (Diptera, 1. Revathi K, Sreekanth M, Krishnayya PV, Rao VS. Agromyzidae), a pest of Cajanus cajan Spreng. in India. Incidence of pod fly, Melanagromyza obtusa (Malloch) Anzeiger fur Schadlingskunde, Pflanzenschutz, and its influence on weight loss in different pigeonpea Umweltschutz. 1994; 67:19-21. genotypes. International Journal of Innovative Science, 14. Singh S, Singh SP, Babu SS, Sebastian PC. Bioecology Engineering and Technology. 2015; 2(5):460-464. of Hymenoptera parasites of Agromyzidae (Diptera) 2. Wadaskar RM, Bhalkare SK, Patil AN. Field efficacy of pests species in India. Memories of the School of newer insecticides against pod borer complex of Entomology. (St. John's College, Agra, India.). 1991; pigeonpea. Journal of Food Legumes. 2013; 26(1, 2):62- 11:1-238. 66. 15. Tiwari G, Singh DC, Singh R, Kumar P. Role of abiotic 3. Gangrade GA. Assesment of damage to tur (Cajanus and biotic factors on population dynamics of pigeonpea cajan) in Madhya Pradesh by tur pod fly, Agromyza pod fly (Melanagromyza obtusa Malloch). Journal of obtusa Mall. Indian Journal of Agricultural Sciences. Recent Advances in Applied Sciences. 2006; 21(1, 2):12- 1963; 33(1):17-20. 14. 4. Srivastava AS, Katiyar SSL, Srivastava KM. Damage of 16. Ahmad T. The tur-pod fly, Agromyza obtusa Malloch, a Agromyza obtusa Malloch. (Diptera: Agromyzidae) to pest of Cajanus cajan. Indian Journal of Agricultural Cajanus cajan Linn. Crop. Labdev Journal of Science Sciences. 1938; 8:63-76. and Technology. 1971; 9:71-73. ~ 281 ~ Journal of Entomology and Zoology Studies

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