20042-- J Poorani

Indian Journal of Entomology Review Article (2020) DoI No.:

A REVIEW OF THE PEST STATUS AND NATURAL ENEMY COMPLEX OF BANANA TORUS EVANS IN SOUTH AND ITS MANAGEMENT

J Poorani*, B Padmanaban, Sharanabasappa Deshmukh1, R. Thanigairaj and Gavas Ragesh2

ICAR-National Research Centre for Banana, Thogamalai Road, Thayanur Post, Tiruchirappalli 620102, Tamil Nadu 1Department of Agricultural Entomology, College of Agriculture, University of Agricultural and Horticultural Sciences, Shivamogga 577225, Karnataka 2Banana Research Station, Kerala Agricultural University, Kannara, Thrissur 680652 *Email: [email protected] (corresponding author)

ABSTRACT

Huge outbreaks of the banana skipper, Evans (: Hesperiidae), considered as a minor pest of bananas and plantains in the northeast India, were witnessed in South India during 2012- 16. Its present status as a pest of bananas in South India is briefly reviewed here with information on its natural enemies, seasonal incidence and varietal preference. Natural enemies of E. torus from South India were surveyed during 2015-18 due to the lack of information on its bioagents in Indian conditions and totally 14 parasitoids were observed on various stages of E. torus including five on eggs, seven on larvae and two on pupae. Most of the parasitoids observed in South India are known to parasitize E. torus in other parts of South and South East Asia, except Acropimpla sp. nr. nigroscutis (Hymenoptera: Ichneumonidae), which is reported here as a larval parasitoid of E. torus for the first time in the world. Egg parasitism by Ooencyrtus pallidipes (Ashmead) and early larval parasitism by Elasmus brevicornis Gahan and heavy bird predation on older larvae were identified as major regulatory factors of E. torus in South India. At present, E. torus is mostly confined to parts of Western Ghats with cooler weather than the plains and its population is lower absent in the plains of South India where outbreaks were reported earlier, possibly due to the influence of natural enemies and adverse abiotic factors. Other management options available for the pest are briefly discussed.

Key words: Erionota torus, Hesperiidae, banana, parasitoids, Acropimpla sp., Oencyrtus pallidipes, Elasmus brevicornis, predators, birds, management, Western Ghats

Banana ( spp.) has a special significance in Erionota torus, originally described from Sikkim, South Indian culture as the leaves are widely used as is indigenous to north India (Western Himalaya) and disposable plates for serving food and whole plants found in Nepal, northeast India to southern and with bunches are used as symbols of auspiciousness in Peninsular (Cock, 2015). Erionota torus is religious and cultural functions besides the known use more restricted in its geographic spread than E. thrax, of fruits for dessert and cooking purposes. Two species but now it has been widely introduced in different of skippers of the Erionota Mabille (Lepidoptera: countries including , Japan, Mauritius, and Hesperiidae) are known to feed on the leaves of bananas the Philippines (Cock, 2015; GBIF, 2018) and Sri and plantains in different parts of Southeast and South Lanka (Gunawardana et al., 2015), besides India. In Asia. Cock (2015) critically reviewed the literature India, E. torus is known to be distributed in Arunachal pertaining to the , distribution, food plants, Pradesh (Jayashankar et al., 2018), Assam, Meghalaya, early stages, natural enemiesPreview and biological control of Chhattisgarh, Madhya Pradesh, West Bengal, Manipur, Erionota spp. including E. thrax (L.), E. torus Evans Mizoram, Tripura, Kerala, Karnataka, Maharashtra, and E. acroleuca (Wood-Mason and de Niceville) (=E. Tamil Nadu and Andhra Pradesh (Chitra et al., 2016; hiraca (Moore)), a pest of palms. Of these, E. thrax (L.) Raju et al., 2019; unpublished data). Ghorpade and is more widely distributed in South and South East Asia Kunte (2010) included E. torus in their list of and reported in published literature as banana skipper. In of the Palani Hills of Southern Western Ghats, but it had India, is distributed in the northeastern not been known to be a pest of banana in peninsular region (West Bengal, Meghalaya, Mizoram) (Kunte India until recently. Sporadic outbreaks of E. torus in 2019), where it coexists with its close relative, E. torus. Palghat, Peechi, Nilambur, and some northern districts 2 Indian Journal of Entomology Review Article 2020 of Kerala state, South India, were first reported in 2013, gave characters to separate the adults from E. thrax which spread to the entire state within a year (Soumya et based on appearance and male genitalia. In view of al., 2013; Sivakumar et al., 2014). Soon after, outbreaks their external similarity, E. torus and E. thrax are were witnessed in 2013-14 in the neighbouring states of not easy to identify without examination of the male Tamil Nadu and Karnataka (south and coastal districts), genitalia and females can be reliably identified only by which are major banana growing belts. It was first the genitalia (Cock, 2015). The immature stages and reported from Andhra Pradesh in 2015 (Kamala Jayanthi adults of E. torus (Fig. 1) and E. thrax are externally et al., 2015) and later in 2018 (Reddy and Hemadri, very similar and males of E. torus can usually but not 2018). It is also present in the Western Ghats section always be distinguished from those of E. thrax by the of Maharashtra (Kunte 2019). more rounded distal margin of the forewing in E. torus (Fig. 2b) compared to the straighter margin and apically In South India, outbreaks of E. torus were initially more pointed forewing of E. thrax (Fig. 2a). When wrongly attributed to E. thrax and reported as such by E. torus was introduced in Mauritius, it was initially some workers (Soumya et al., 2013; Padmanaban, 2014; misidentified asE. thrax as the latter was better known Sivakumar et al., 2014), but later the pest was correctly as banana skipper. Unsurprisingly, in South India too, identified as E. torus. The skipper larvae caused direct outbreaks of E. torus were initially attributed to E. thrax damage by feeding on leaf lamina and reduced the total (Soumya et al., 2013; Padmanaban, 2014; Sivakumar et photosynthetic area of leaves and the banana leaf industry al., 2014), but later corrected as that of E. torus. was badly affected due to these outbreaks (Sivakumar et al., 2014).Studies on economic losses due to E. torus The genitalia of E. torus are illustrated by Evans are lacking in India and elsewhere probably because (1949), Inoué and Kawazoé (1970), and Raju et al. ‘economic entomologists have hitherto treated both E. (2019). The present study identified all the specimens thrax and E. torus as a single species wherever they occur collected from the states of Karnataka, Kerala and together’ (Cock, 2015). Economic impact of E. thrax on Tamil Nadu during 2015-18 as E. torus based on the banana yield was worked out by Waterhouse et al. (1998) characters of female and male genitalia and DNA who extrapolated from several studies on defoliation barcodes. Sympatric occurrence of both E. torus and and fruit loss indicating that more than 16% defoliation E. thrax was observed only in Meghalaya, northeastern will cause loss of yield, and 50% defoliation will cause region, during surveys in 2018, with E. torus being the 28% yield loss. Infestation by E. thrax was found to lead more predominant species. The male (Fig. 3a-d) and to both a serious delay in fruit maturation and reduced female genitalia (Fig. 3e) of representative samples weight of banana bunches (Waterhouse et al., 1998). of E. torus from South India and that of E. thrax from Meghalaya (Fig.3 f-i) are illustrated here. As the name In the aftermath of the recent outbreaks of E. torus E. thrax continues to be used by some authors for the on banana in south India, attempts have been made by species from peninsular India even after the pest has many researchers to formulate management strategies been correctly identified asE. torus (e.g., Irulandi et al., for the pest. Surprisingly, many of these were based 2018), it is advisable to follow Cock’s (2015) precaution on use of insecticides and though biological control “to ensure that voucher specimens are preserved and has been identified as the major management strategy documented for all observations on Erionota spp.”. for E. torus and effective parasitoids have been known (Cock, 2015), systematic attempts have not been Host plants and varietal preference made to document the parasitoids of E. torus in Indian The common name of E. torus is Rounded palm- conditions. This study made intensive efforts to survey redeye and that of E. thrax thrax (the subspecies found and document the natural enemies of E. torus from in India) is Acute palm-redeye (Kunte, 2019), both Southern Indian states Previewduring 2015-18. The natural of which are misnomers as the pests do not feed on enemies of E. torus collected and documented in our palms. Cock (2015) recommended that use of these surveys are reported here with a brief review of the common names for all Erionota spp. should be totally present status of the pest in South India, its seasonal discontinued as they are inappropriate and likely to incidence, varietal preference and management cause confusion in view of the well documented damage strategies in Indian conditions. caused on banana. In the present study, surveys came across E. torus damage on several popular banana Taxonomy cultivars (Musa spp., ) and bird of paradise Evans (1941) described E. torus from Sikkim and (Strelitzia reginae Banks, Strelitziaceae). 20042-- J Poorani A review of the pest status and natural enemy complex of banana skipper Erionota torus Evans in South India and its management 3 J Poorani et al.

Fig. Fig1. Erionota. 1. Erionota spp.: a-c.spp.: Symptoms a-c. Symptoms of damage of ondamage banana; on d-i. banana; Life stages d-i. ofLife E. torusstages: d. of Eggs; E. torus: b.d. NeonateEggs; b. larva: Neonate c. Second larva: instar c. Second larva; d. instar Mature larva; larva; d. e. Mature Pupa; f. larva; Adult e. Pupa; f. Adult.

Fig. 2. Fore wing: a. Erionota thrax; b. E. torus

In the northern districts of Kerala, E. torus was plant infestation) (Sharanabasappa et al., 2016).Guru initially reportedFig. 2. Foreon almost wing :all a. Erionotaruling varieties thrax; of b. bananaE. torus et al. (2018) observed heavy infestation on cv. Mitli cultivated in the area with a preference towards cultivars in Sirsi district, Karnataka. In Andhra Pradesh, the Nendran (Genome type AAB), Njalipoovan (Genome incidence of E. torus was high on cv. Bontha and type AB) and PalayamkodanPreview (Genome type Mysore moderate on cv. Grande Naine (Dr. YSRHU, 2017) AAB) (Soumya et al., 2013; Sivakumar et al., 2014). and on cv. Sugandhalu and Grande Naine (Reddy and The preference may be attributed to leaf characters 1 Hemadri, 2018). In Tamil Nadu, skipper infestation is such as thickness of leaf lamina (Sivakumar et al., now observed by the authors of the present work, on 2014). In Shivamogga, Karnataka, the incidence of E. several popular banana cultivars including Virupakshi torus on cv. Ney Poovan or Puttabaale (AB) and cv. (hill banana), Nendran, Ney Poovan, Grande Naine, Grande Naine (AAA) was observed with significantly Kathali, Chakkai and Rasthali, the first three cultivars greater levels of incidence on Ney Poovan (31.87% being the most affected. Irulandi et al. (2018) reported plant infestation) as compared to Grande Naine (9.65% mean infestation levels of E. torus on various cultivars

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A review of the pest status and natural enemy complex of banana skipper Erionota torus Evans in South India and its management 4 J Poorani et al. in Kanyakumari, Tamil Nadu, ranging from a low of 15, the pest density gradually come down and our 3.16% in cv. Kadali to a high of 47.75% in cv. Matti. observations indicate the pest prefers hilly terrains They found the infestation was low on cv. Kadali, with cooler climates to the plains of South India, many Pachanadan and Karpuravalli, but severe on cv. Matti, parts of which normally experience scorching summers Nendran, Ney Poovan and Red banana and attributed with temperatures ranging from 35oC to upwards of the preference to thickness of leaf lamina. 40oC. The present study observed the pest during the monsoon, post-monsoon and winter seasons (June- Seasonal incidence, crop phenology and influence March) in different parts of South India. In Tamil Nadu of weather factors and Kerala, the pest is mainly confined to the Western Though outbreaks of E. torus were initially Ghats and nearby areas where the conditions appear to be witnessed in several parts of South India during 2012- favourable for the pest. Besides the four southern states,

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Fig. 3. Genitalia of Erionota spp.: a-d. Male genitalia of E. torus: a. Lateral view; b. Ventral view; Figc. .Inner 3. Genitalia aspect of valva;of Erionota d. Aedeagus; spp.: f. Femalea-d. Male genitalia genitalia of E. torus of E.; g-i. torus Male: a.genitalia Lateral of view;E. thrax b.: Ventral g. Ventral view; h. Lateral view; i. Inner aspect of valva; j. Female genitalia of E. thrax. view; c. Inner aspect of valva; d. Aedeagus; f. Female genitalia of E. torus; g-i. Male genitalia of E. thrax: g. Ventral view; h. Lateral view; i. Inner aspect of valva; j. Female genitalia of E. thrax.

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A review of the pest status and natural enemy complex of banana skipper Erionota torus Evans in South India and its management 5 J Poorani et al. the pest has been observed from Sindhudurg, Raigad period (mean infestation of 75.02%) followed by and Ratnagiri districts of Maharashtra (AICRP-Fruits flowering period (45.67%), broad leaf stage (29.58%) 2018; Raju et al., 2019). During the present study, recent and bunch period (1.66%) (Sharanabasappa et al., 2016, surveys in October 2018 in Meghalaya (northeastern 2018). In Shivamogga, Karnataka, incidence of E. region), led to bringing out the co-occurrence of E. torus torus was highly significantly and positively correlated and E. thrax, with E. torus being the more common and with maximum temperature and sunshine hours, but numerically predominant species. significantly negatively correlated with minimum temperature, morning and evening relative humidity In South India, banana is cultivated as a sole crop, and rainfall (Sharanabasappa et al., 2016). intercrop or border crop in and are canut plantations and several other crops and is commonly Natural enemy complex grown in homesteads. Interestingly, skipper infestation Twelve parasitoids attacking the egg, was very high in intercropped banana and isolated plants larval and pupal stages of E. torus were reared and in homesteads and borders rather than mono crop of documented in our surveys during 2015-18 from the banana and within sole crop of banana, the severity states of Tamil Nadu, Kerala and Karnataka in South of infestation was often greater near the borders than India and from Mizoram, Assam and Meghalaya in inside. In northeastern India, skipper infestation was the northeast region. Parasitoids observed from South noticed mainly in homesteads and isolated pockets Karnataka during 2016-18 are listed in Table 1. The (unpublished data). In Kannara, Kerala, the average parasitoids collected in South India were unequivocally plant damage due to skipper was 5-54.5% and the pest associated with E. torus as it was the only species of incidence was observed during February- September, banana skipper identified in all the localities surveyed. 2016 with peak leaf roll formation during the monsoon A brief account of the parasitoids on E. torus is given season (June- August). The pest population declined to herein with illustrations to facilitate their identification. low levels during dry periods (AICRP-Fruits, 2017). In Shivamogga, Karnataka, the pest was active during A. Egg parasitoids August-February and the infestation levels ranged Ooencyrtus pallidipes (Ashmead) (Hymenoptera: from 6.66 to 84.25%. The incidence started in the first Encyrtidae) (Fig.4a-d): The present study observed fortnight of August (8.34% incidence) when the crop it from Kerala, Tamil Nadu and Karnataka as one of was at broadleaf stage and gradually increased with a the major parasitoids of E. torus. The extent of natural peak (84.25%) during the first fortnight of January (pre- parasitism was heavy with 80-100% parasitism of the flowering period) and extended to the flowering period eggs collected from some parts of Karnataka, Tamil (February- March). The pooled data over the years Nadu and Kerala in winter months (December-March). indicated maximum incidence during pre-flowering Three to as many as eight parasitoids were observed Table 1. List of stage-specific parasitoids ofE. torus from South Karnataka (2016-18) Scientific name Stage attacked % parasitism Location Season of Number of activity adults emerged / egg/ larva / pupa Ooencyrtus Egg 14.42–85.89 All locations August- 3-6 pallidipes February Agiommatus sp. Egg >1 Shivamogga August 1 Anastatus sp. PreviewEgg >1 Shivamogga, December- 1 Chamarajanagar January Elasmus Early larval 5–6 Shivamogga, December- 7-9 brevicornis Chamarajanagar, February Chikkamagaluru Senometopia sp. Late Larval 2–3 Shivamogga, September- 1-3 Chikkamagaluru October Winthemia Late Larval Shivamogga, 1-3 sumatrana Chikkamagaluru A review of the pest status and natural enemy complex of banana skipper Erionota torus Evans in South India and its management 6 J Poorani et al.

Fig. Fig.4. Egg 4. Eggparasitoids parasitoids of Erionota of Erionota spp.: spp.: a, b.a, b.Eggs Eggs parasitized parasitized by by Ooencyrtus Ooencyrtus pallidipes pallidipes;; c, d. Ooencyrtusc, d. Ooencyrtus pallidipes pallidipes; e, f. Agiommatus; e, f. Agiommatus sp. parasitizing sp. parasitizing E. torus E. eggs.torus eggs to emerge from each egg. This species was introduced torus eggs by O. pallidipes was observed in selected in and Mauritius for the control of skipper localities in five districts of Karnataka during 2016-17 (Cock 2015) and it appears to be the most common and and 2017-18. In all the locations surveyed, per cent widespread parasitoid of E. torus in Karnataka, Kerala plant infestation, number of larvae/ plant and per cent and Tamil Nadu. This parasitoid was also reared from parasitism by O. pallidipes were found to increase parasitized eggs collected from Assam and Meghalaya. gradually from the post-monsoon season and peaked in Ooencyrtus erionotae Ferriere, a species considered winter (Table 2). Mean egg parasitism by O. pallidipes to be synonymous with O. pallidipes (Noyes, 2018), in these localities was 15.17-26.70% in 2016-17 and had been earlier known fromPreview India (Karnataka, Assam 17.55-39.48% in 2017-18 (Table 2) and the extent of and Andhra Pradesh) on other lepidopteran hosts parasitism was as high as 83.84% in Shivamogga and (Hayat and Subba Rao, 1981; Hayat, 1986). Gupta and 4 85.89% in Davanagere during February 2018. In Tamil Sharanabasappa (2016) observed O. pallidipes from Nadu also, randomly collected egg masses of E. torus Karnataka and natural parasitism observed was 80-82% showed high levels of parasitism (60-100%) in 2016-17 in Shivamogga district. (unpublished data). These observations clearly indicate O. pallidipes is the most effective parasitoid of E. torus Eggs of a mixed population of Erionota spp. in South India and it appears to have a wide distribution from Meghalaya were found to be parasitized by O. in India or probably spread on its own along with the pallidipes in October 2018. Natural parasitism of E. host insect to different localities in South India as no A review of the pest status and natural enemy complex of banana skipper Erionota torus Evans in South India and its management 7 J Poorani et al. deliberate attempts have been made to use biological in Karnataka. Despite repeated attempts, females of control agents against E. torusin India. this parasitoid could not be collected. Male specimens collected from Erionota sp. on banana from Mizoram Agiommatus sp. (Hymenoptera: Pteromalidae) were found to be close to two species, A. paria (Fig. 4e, f): An undetermined species of Agiommatus (Motschulsky) and A. geethae Sureshan and Narendran (Fig. 4e, f) was observed to parasitize E. torus eggs and the species identity could not be confirmed without

Table 2. Incidence of E. torus and extent of egg parasitism by Ooencyrtus pallidipes in Karnataka (2016-17, 2017-18)

Place Month % plant infestation Number of larvae/ Total number of % parasitism plant eggs observed 2016-17 2017-18 2016-17 2017-18 2016-17 2017-18 2016-17 2017-18 Shivamogga June 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 District July 0.00 0.00 0.00 0.00 61 82 0.00 0.00 (Shivamogga August 17.25 26.40 1.54 2.55 141 152 0.00 0.00 taluk) September 25.14 43.86 2.52 4.05 394 617 0.00 14.42 October 34.12 50.25 3.12 4.50 524 705 14.50 22.12 November 48.14 58.65 3.62 5.82 768 1191 24.60 47.43 December 56.78 63.47 4.20 4.54 860 1128 29.76 59.75 January 54.64 54.40 3.42 4.17 710 1029 36.33 65.30 February 48.25 40.25 2.36 2.42 521 520 38.57 83.84 March 21.20 - 0.25 - 13 - 46.15 - Mean 30.55 37.47 2.10 3.11 399.20 602.66 18.99 32.54 Davanagere June 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 District (Honnali July 0.00 0.00 0.00 0.00 36 31 0.00 0.00 and Chennagiri August 15.65 16.82 1.64 1.25 163 42 0.00 0.00 taluks) September 28.55 23.25 2.52 2.22 415 352 13.01 21.87 October 40.94 35.55 2.83 3.45 431 469 24.59 28.35 November 51.82 47.36 3.56 3.94 816 1150 31.61 47.21 December 54.71 56.48 4.10 4.32 825 1228 42.42 53.25 January 51.25 44.10 2.42 2.25 768 1018 47.13 61.10 February 46.84 32.62 1.22 1.02 436 312 52.75 85.89 March 24.23 - 0.22 18 - 55.55 - Mean 31.39 28.46 1.85 2.05 390.80 511.33 26.70 33.07 Chitradurga June 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 District July 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 (Holalkere and August 0.00 0.00 0.00 0.00 16 0.00 0.00 0.00 Chitradurga taluks) SeptemberPreview10.23 0.00 0.56 0.00 98 14 0.00 0.00 October 12.84 15.64 0.92 1.33 126 106 8.73 0.00 November 18.98 21.14 1.54 1.95 186 253 15.05 21.73 December 28.44 28.65 2.11 2.34 237 412 24.47 29.61 January 32.74 24.36 2.64 2.85 212 325 28.77 50.46 February 30.32 19.54 1.10 1.21 182 146 31.86 56.16 March 12.65 - 0.14 - 7 - 42.85 - Mean 14.62 12.14 0.90 1.07 106.40 139.55 15.17 17.55 A review of the pest status and natural enemy complex of banana skipper Erionota torus Evans in South India and its management 8 J Poorani et al.

Chikkamagaluru June 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 District (Kadur, July 0.00 21.85 0.00 1.85 10 235 0.00 22.97 Tarikere and August 10.25 23.00 0.78 1.88 95 266 0.00 27.06 Birur taluks) September 12.64 26.28 1.24 2.26 256 346 0.00 33.52 October 22.35 25.44 2.54 2.54 321 464 12.14 37.28 November 33.41 28.45 2.91 2.95 462 853 19.69 53.81 December 41.58 32.14 3.44 2.18 685 985 28.32 55.02 January 42.32 30.56 2.84 2.00 550 886 33.81 61.06 February 36.46 20.92 1.76 1.54 485 260 37.93 64.61 March 23.41 - 0.16 - 16 - 43.75 - Mean 22.24 22.88 1.56 1.91 288 477.22 17.56 39.48 Chamarajanagar June 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 District July 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 (Chamarajanagar August 0.00 0.00 0.00 0.00 23 26 0.00 0.00 taluk) September 10.23 15.62 0.72 1.12 132 230 0.00 26.95 October 16.74 20.64 1.21 1.64 286 405 10.83 42.46 November 20.31 23.74 1.87 1.98 413 452 16.46 46.90 December 31.67 30.56 2.38 2.46 547 528 27.97 48.10 January 36.66 40.82 2.76 2.52 532 446 35.52 55.60 February 34.89 35.24 0.88 1.02 454 330 42.73 65.15 March 18.62 - 0.18 - 10 - 50 - Mean 16.91 18.51 1.00 1.19 239.70 339.55 18.35 31.67 examining associated females (P.M. Sureshan, in litt.). B. Larval parasitoids Agiommatus sumatraensis Crawford (1911) and A. Elasmus brevicornis Gahan (Hymenoptera: erionotus Huang (1986) are known to parasitize the Eulophidae) (Fig. 5a-c): Elasmus brevicornis had been eggs of E. thrax and E. torus, respectively. known as the most common early larval parasitoid in surveys conducted in Tamil Nadu (Fig. 5a-c) and it Anastatus sp. (Hymenoptera: Eupelmidae): An appears to be a major controlling factor as it parasitizes unidentified species ofAnastatus was found to parasitize the early larval stages by up to 25%. From each the eggs of E. torus in Shivamogga and Chamarajanagar parasitized host collected in Tamil Nadu, 6-11 adult (Karnataka) at very low levels (less than 1%). parasitoids were observed to emerge (unpublished Tetrastichus sp. (Hymenoptera: Eulophidae): data). Specimens reared on E. torus from Kerala were Specimens of an in determinate species of Tetrastichus also examined. The parasitoid was identified using the were collected on the eggs of Erionota sp. from description and key to Indian Elasmus by Verma et al. Mizoram. There is no mention of Tetrastichus as an egg (2002).The female (Fig. 5d, e) and male (Fig. 5f) of E. parasitoid of both E. torus and E. thrax and this appears brevicornis are illustrated herein. Thompson (1955) to be a new record. and Strakhova and Yefremova (2013) observed it as a larval parasitoid of E. thrax and Cock (2015) noted that Telenomus sp. (Hymenoptera:Preview Platygastridae): it is a polyphagous, facultative hyper parasitoid. It had Specimens reared from the eggs of E. torus received also been known as a hyper parasitoid of Pediobius sp. for identification from Karnataka were identified (Noyes, 2018). However, Verma et al. (2002) mentioned as Telenomus sp. and this appears to be rare as the that Elasmus species are primary parasitoids of larvae present study could not observe it from any of the other and prepupae of various Lepidoptera. Another species, surveyed locations in South India. Telenomus sp. nr. Elasmus philippinensis Ashmead had been known as a attaci is the only platygastrid egg parasitoid observed parasitoid of E. thrax and E. torus from Philippines and on E. thrax from Sabah (Syed 1971). Taiwan, respectively (Cock 2015). Both are known to be A review of the pest status and natural enemy complex of banana skipper Erionota torus Evans in South India and its management 9 J Poorani et al.

FigFig.. 5. 5.Elasmus Elasmus brevicornis, brevicornis, an early an larval early parasitoid larval ofparasitoid E. torus: a. Larvaeof E. torusemerging: a. from Larvae E. torus emerging; b, c. Pupae from of E. E. torus; b, c. Pupaebrevicornis of E. brevicornis; d. Female, dorsal; d. view;Female, e. Female, dorsal lateral view; view; e.f. Male,Female, lateral lateral view. view; f. Male, distributedlateral view. in India (Verma et al., 2002; Noyes, 2018). parasitoid from early instar larvae of E. torus collected Verma et al. (2002) stated that E. brevicornis was very from Tamil Nadu and examined conspecific specimens closely related to E. philippinensis and it could not be from Kerala. The specimens appear to be close to P. reliably distinguished from the latter, hence it is likely elasmi, which belongs to the crassicornis-group of that they could be synonymous. species as defined by Cao et al. (2017) and are different from P. erionotae Kerrich (1973), a widely observed Fig 7 before Pediobius sp.Fig nr.. elasmi5. Elasmus (Ashmead) brevicornis, (Hymenoptera: an early larval parasitoidegg parasitoid of E. torus of: E.a. Larvaethrax in emerging Southeast from Asia E. by several Fig 6 Eulophidae) (Fig.7a,torus; b,b) :c. The Pupae present of E. brevicornisstudy reared; d. this Female, workers dorsal view; (Cock, e. Female, 2015), lateralwhich view; belongs f. Male, to the pyrgo- reference lateral view. Preview

Fig. 6. Acropimpla sp., a new ichneumonid parasitoid of E. torus: a. Parasitoid larva on E. Fig. 6. Acropimpla sp., a new ichneumonid parasitoid of E. torus: a. Parasitoid larva on E. torus larva;torus Figb.. larva;6.Parasitoid Acropimpla b. Parasitoid pupa sp., pupa a insidenew inside ichneumonid silkensilken cocoon; cocoon; parasitoid c. Parasitoid c.of ParasitoidE. pupa; torus d.: a.Female, Parasitoid pupa; dorsal d. larva view.Female, on E. dorsal view. torus larva; b. Parasitoid pupa inside silken cocoon; c. Parasitoid pupa; d. Female, dorsal view.

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A review of the pest status and natural enemy complex of banana skipper Erionota torus Evans in South India and its management 10 J Poorani et al. group of species (Cao et al., 2017). Cock (2015) in (Hymenoptera: Ichneumonidae) (Fig. 6): A specimen Fig. 6 after his review of parasitoids of Erionota spp. mentions of Acropimpla was reared from a third instar larva of Fig 7 Refer- that Pediobius elasmi is a hyper parasitoid of Cotesia E. torus collected at Thadiyankudisai, Lower Pulney ence erionotae (Wilkinson). Our observations indicate it Hills, Tamil Nadu. It appears to be close to Acropimpla could be a possible hyper parasitoid of E. brevicornis. nigroscutis (Cameron), the only species of this genus All the specimens reared by us were from early instar known from India at present, but more specimens larvae and not from eggs. and studies are needed to establish its identity. This constitutes a new host-parasitoid association as there Tetrastichus sp. (Hymenoptera: Eulophidae) is no other published record on the occurrence of (Fig.7c):Specimens of an indeterminate species of Acropimpla as a parasitoid of E. torus. Tetrastichus were collected from the early instar larvae of E. torus from Tamil Nadu, which were probably Cotesia sp. (Hymenoptera: Braconidae): The hyper parasitoids. Cock’s (2015) review does not present study reared a species of Cotesia from a solitary include any Tetrastichus spp. as larval parasitoids of cocoon formed from an early stage larva of E. torus and Erionota spp. and this is a new record for E. torus. frequently collected solitary cocoons of Microgastrinae (Braconidae) in association with E. torus in Kerala and Acropimpla sp. nr. nigroscutis (Cameron) Tamil Nadu, none of which yielded adults. Cotesia

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Fig.Fig .7. 7. Natural Natural enemies enemies of Erionota of Erionota spp.: spp.:a, b. Pediobiusa, b. Pediobius sp., a larval sp., aparasitoid larval parasitoid of E. torus of; c. E. Tetrastichus torus; c. Tetrastichussp., a pupal parasitoid sp., a pupal of E. parasitoidtorus; d. Brachymeria of E. torus lasus,; d. Brachymeriaa pupal parasitoid lasus, of Erionota a pupal spp.;parasitoid e, f. Leaf of Erionota spp.; e, rollsf. Leaf of Erionota rolls of spp.Erionota showing spp. characteristic showing characteristic signs of bird predationsigns of bird predation.

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A review of the pest status and natural enemy complex of banana skipper Erionota torus Evans in South India and its management 11 J Poorani et al. erionotae (Wilkinson), a gregarious larval parasitoid, In northeastern India, tachinid parasitism of Erionota has been successfully used in controlling Erionota spp. spp. was commonly observed on a much larger scale. in different parts of the world (Cock, 2015), but did not In Shivamogga, Karnataka, two tachinid parasitoids, come across any gregarious microgastrine braconid in Senometopia sp. and Winthemia sumatrana (Townsend) our surveys. were encountered as larval parasitoids and their activity started from the second fortnight of September (0.62%) Tachinid parasitoids of E. torus (Diptera: and peaked during the second fortnight of November ) (Fig. 8): Low levels of parasitism of later (7.25%) and later gradually declined till the second instar larvae and pupae of E. torus by tachinids (Fig. fortnight of January (0.62%). The maximum activity 8a-d) was observed at various locations in South India. of parasitoids were noticed during pre-flowering period

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Fig. 8. Tachinid parasitoids of Erionota spp.: a. Tachinid parasitoid on skipper larva; b–d Puparia of tachinid Fig. 8. Tachinid parasitoidsparasitoids ofof Erionota Erionota spp.; spp.: e. Senometopia a. Tachinid sp.; parasitoidf. Winthemia on sp. skipper larva; b–d Puparia of tachinid parasitoids of Erionota spp.; e. Senometopia sp.; f. Winthemia sp.

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A review of the pest status and natural enemy complex of banana skipper Erionota torus Evans in South India and its management 12 J Poorani et al. with a mean of 3.27% parasitization by Senometopia as high as 50to 10% within a month in Kerala and it sp. and W. sumatrana (Sharanabasappa et al., 2018). was so effective that no other management options were Winthemia sumatranahad been known as a pupal resorted to. The red ant Oecophylla smaragdina and parasitoid of E. torus in Japan by Shima (1996) and as a spiders also have been observed as feeding on different parasitoid of E. torus from Karnataka (Sharanabasappa stages of the pest in Karnataka (Sharanbasappa et al., et al., 2018). Senometopia sp.was reared from the 2016). mature larva collected in Lower Pulney Hills, Tamil Nadu. Two tachinid parasitoids of E. torus including Management Exorista japonica (Townsend) and an unidentified Efficacy of insecticides and microbials:Padmanaban species were listed by Cock (2015) in his list of natural (2015), Sharanabasappa (2017), Irulandi et al. (2018) enemies of E. torus. A species of Drino (Palexorista) and Guru et al. (2018) evaluated the efficacy of various was also found to parasitize the late larval stages of E. insecticides and microbials such as Beauveria bassiana torus in Tamil Nadu. against E. torusin different parts of Tamil Nadu and Karnataka. Foliar application of insecticides such C. Pupal parasitoids as chlorpyriphos, profenophos, chlorantraniliprole, Brachymeria lasus (Walker) (Hymenoptera: cyantraniliprole and combinations of lambda Chalcididae) (Fig.7d): It is a common parasitoid cyhalothrin+dichlorvos, chlorpyriphos+dicholorvos collected in association with many lepidopteran pupae and profenophos+dichlorvos have been found to be in India and the specimens examined by us were effective in controlling E. torus in different states of reared from the pupae of E. torus collected in Kerala South India (Padmanaban, 2015; Sharanabasappa et al., and also from larvae of undetermined Erionota sp. 2016; AICRP-Fruits, 2017; Irulandi et al., 2018; Guru from Meghalaya. Species of Brachymeria are known et al., 2018).Padmanaban (2015) and Irulandi et al. to parasitize the pupae of a variety of lepidopteran (2018) found B. bassiana as an effective and affordable hosts (Narendran, 1989). Narendran (1986) listed four solution for managing E. torus as it had persistent species, Brachymeria albotibialis (Ashmead), B. lasus, activity, particularly under highly humid conditions in B. euploeae (Westwood), and B. thracis (Crawford), banana plantations and it has proven efficacy against the as parasitoids of E. thrax/ E. torus in his catalogue of pseudostem weevil (Odoiporus longicollis (Olivier)), Oriental Chalcididae. which is a major pest of banana.

Unidentified Tachinidae: Cock (2015) listed the Guru et al. (2018) evaluated different insecticides tachinid pupal parasitoids of E. thrax and E. torus. and microbial pesticides such as Metarhizium rileyi Soumya et al. (2013) observed the occurrence of an (=Nomuraea rileyi), M. anisopliae and B. bassiana unidentified species of tachinid parasitizing the pupae individually and in combination against E. torus in Sirsi, of banana skipper (reported as E. thrax). The present Karnataka, and found the microbials were less effective study observed an unidentified tachinid pupal parasitoid than chemical insecticides against the skipperbutopined of Erionota sp. from Meghalaya. that M. rileyi and M. anisopliae in combination with neem oil could be recommended for controlling the D. Insect and bird predators skipper. Bacillus thuringiensis application (3ml/l, Heavy bird predation on medium to large sized 1x108 cfu) was also found to be efficacious against larvae, mainly the latter, was observed in many parts E. torus. Application of azadirachtin andneem oil- of Tamil Nadu, Karnataka and Kerala, which appears based botanical insecticides was recommended by to be a major regulatory factor of E. torus. Large leaf the Department of Agriculture, Kerala (Soumya et al., rolls harbouring mediumPreview to full grown larvae are 2013). However, chemical control does not appear to apparently preferred by birds, which feed on the larvae be a viable and feasible solution for managing E. torus inside by tearing them open (Fig. 7e, f). Crow pheasant in the field as the skipper larvae remain sheltered inside (Centropussinensis), house crow (Corvus splendens), leaf rolls and feed from inside. It is also quite likely that Indian tree pie (Dendrocitta vagabunda), and white- the dense powdery coating on older larvae may protect headed babbler (Turdoides affinis) have been reported the larvae against insecticides. Besides, effective and by various authors as avian predators of E. torus targeted application of insecticides is near impossible in (Sivakumar et al., 2014; Sharanabasappa et al., 2016). very tall cultivars such as hill banana and Red Banana Sivakumar et al. (2014) observed that bird predation (among the most preferred banana cultivars by E. torus) brought down the infestation levels of the skipper from which are more than 3.5-4.5 m high. A review of the pest status and natural enemy complex of banana skipper Erionota torus Evans in South India and its management 13 J Poorani et al.

Biological control: Biological control appears to India, particularly the plains, appear to be largely be the best option for managing E. torusin view of contained now due to the activity of natural enemies the semi-perennial nature of the banana ecosystem as and unfavourable hot weather. At present, the pest is banana crop has a very long duration (15-18 months) confined to the cooler climes of the Western Ghats and and farmers in South India traditionally go for two or adjoining areas conducive for its development. Mapping even three ratoons after the mother crop (‘plant crop’). its geographic range vis-à-vis E. thrax, its closest relative Cock (2015) reviewed the parasitoids of E. torus and and documenting all the stage-specific parasitoids are E. thrax and observed that ‘good taxonomy, a critical required in the event of possible outbreaks in future. It factor to success in biological control programmes, is imperative to study the factors that caused the sudden does not appear to be a limiting factor in the case of explosion in its population and monitor further spread Erionota spp. as both seem to be attacked by the same from its present restricted pockets of distribution in set of parasitoids’. At present, the distribution ranges peninsular Indiainto new areas. In the areas where E. of E. thrax and E. torus are not clearly mapped and torus is found, avoiding indiscriminate use of broad- studies on host preference are lacking in regions where spectrum insecticides to conserve its natural enemies both species coexist. In the northeastregion of India, appears to be the best option for containing the pest. where both species coexist, it is not clear whether host associations were correctly observed for parasitoids ACKNOWLEDGEMENTS in view of the difficulty in separating the two hosts by Thanks are due to Dr. S. Uma, Director, ICAR- economic entomologists. NRCB, Trichy, for the facilities provided to carry In the present study, O. pallidipes and B. lasus from out this work; Dr. Prakash Patil, Project Co-ordinator the northeast region where both species of Erionota are (ICAR-AICRP-Fruits) for his support and help; Dr. sympatric and from South India, where only E. torus P.M. Sureshan, ZSI, Calicut, for confirming and was known. In Mauritius, where E. torus was introduced commenting on the identity of Agiommatus; and Dr. and wrongly identified as E. thrax, successful control H.M. Yeshwanth, UAS, Bangalore, for permitting the was achieved by introducing parasitoids of E. thrax use of his photo of Agiommatus in this paper. from Sabah (Cock, 2015). Also, this study, documents REFERENCES the natural enemies associated with E. torus without any ambiguity as the host identity was established beyond AICRP-Fruits. 2017-18. 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Economic benefits to Papua Conference on Technological Challenges and Human Resources New Guinea and Australia from the biological control of banana for Climate Smart Horticulture – Issues and Strategies. May 28-31 skipper (Erionota thrax). ACIAR Project CS2/1988/ 002-C. 2014, Navsari Agricultural University, Navsari, Gujarat. Impact Assessment Series 12. Australian Centre for International Agricultural Research, ACIAR, Canberra, Australia. 36 pp. (Manuscript Received: February, 2020; Revised: May, 2020; Accepted: May, 2020; Online Published: May, 2020) Online published (Preview) in www.entosocindia.org Ref. No. 20042