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DIVERSITY OF HEMIPTERAN FAUNA AND THEIR RELATIVE ABUNDANCE IN RICE ( L.) ECOSYSTEM

Atanu Seni*

* Orissa University of Agriculture and Technology, All India Coordinated Rice Improvement Project, RRTTS, Chiplima, Sambalpur-768025, Odisha, INDIA. E-mail: atanupau@gmail. com; ORCID ID: 0000-0002-1409-8526

[Seni, A. 2021. Diversity of hemipteran insect fauna and their relative abundance in rice (Oryza sativa L.) ecosystem. Munis Entomology & Zoology, 16 (2): 953-961]

ABSTRACT: The study on the hemipteran fauna associated with rice and their abundance at Chiplima, Odisha, India was performed during wet period of 2017 and dry period of 2018. A total of 19 hemipteran insect taxa belonging to eight insect families were recorded in rice ecosystems during the study and prepared their simplified key for easy field identification and monitoring purpose. Among them, eight taxa viz., Nilaparvata lugens (Stal), Sogatella furcifera (Horvath), Nepotettix virescens (Distant), Nephotettix nigropictus (Stal), Nepotettix cincticeps (Uhler), Menida histrio Fabricius, Dolycoris indicus (Stal.), and Leptocoriza oratorius (Fabricius) were most abundant in rice ecosystem. During flowering and milking stages of the crop, pentatomids exhibited greater diversity whereas earhead bugs were common in dry period than wet period, being more prevalent in flowering and dough stages of the rice growth period. One Lygaeidae, Graptostethus servus (Fabricius) was first time recorded on rice.

KEY WORDS: Abundance, key, identification, rice, dry and wet period, hemipteran

Rice (Oryza sativa L.) is one of the world’s most important cereal crops providing a staple food for nearly half of the global population (FAO, 2004). In India, it is cultivated in almost one-fourth of the total cropped area, providing food to about half of the Indian population. It thrives well under varying topographic and hydrologic conditions ranging from rain fed upland to rain fed lowland as well as in deep water condition (Seni et al., 2019). But, introduction and wide adoption of high yielding varieties in India has led to severe incidence of different insect pests. About 300 species of insect pests infest the rice crop at different growth periods and among them only 23 species cause notable damage (Pasalu & Katti, 2006). Among the different insect orders, lepidopteran, hemipteran and dipteran insects cause maximum damage to rice crop (Seni & Naik, 2017a). Within various hemipteran insects, brown plant hopper (BPH); Nilaparvata lugens (Stål), white backed plant hopper (WBPH); Sogatella furcifera (Horvath), earhead bug; Leptocoriza oratorius (Fab.) are the major reasons for huge economic crop losses in rice. Both the nymphs and adults of BPH and WBPH suck the sap from the plant resulting in chlorotic, wilting and drying up of rice plant which is commonly known as ‘hopper-burn’. Generally the yield losses due to hoppers ranges from 10 to 90 percent but if timely control measures are not implemented, there is a possibility of total crop loss within a very short period (Seni & Naik, 2017). Recently, several species of Pentatomidae have caused economic losses in many rice-producing countries (Lupi et al., 2017). In India, rice black bug, Scotinophara bispinosa (: Pentatomidae) causes severe

Munis Entomology & Zoology Mun. Ent. Zool. 954 https://www.munisentzool.org/ 16 (2) (June, 2021) ISSN 1306-3022 © MRG ______damages to the wet-season rice crop in Kuttanadu, Kerala, India (Narayanasamy, 2007; Mashhoor et al., 2013). They cause damage by feeding on kernels in milk and dough stage of maturation, resulting in partially or totally unfilled grains (Pathak & Khan, 1994; Lupi et al., 2017). Damage by pentatomid bugs also helps in the invasion of fungi and bacteria that are responsible for pecky rice, which leads to chalky discoloration around the feeding site (Lupi et al., 2017). Previously, pentatomid bugs were rarely found in rice in Chiplima, Odisha but from 2015 onwards many species of Pentatomidae attack the rice plants. Beside lepidopteran insect, hemipteran causes enormous damage to the rice crop here. For this, the study was intended to document the diversity of hemipteran insect fauna and their abundance in rice fields in west central table land zone of Odisha.

MATERIALS AND METHODS

Experimental Site The study was conducted in the experimental farm of Regional Research and Technology Transfer Station (OUAT), Chiplima, Sambalpur, Odisha, during 2017 wet and 2018 dry period of rice crop. The Station is situated at 20021’ N latitude and 80055’E longitude in Dhankauda block of Sambalpur district under west central table land zone of Odisha, India at an altitude of 178.8 m above MSL. The climate of the area is warm sub humid.

Experimental details The experiment was conducted in 1000 sq. m area with rice variety MTU- 7029. The variety was sown in the third week of July and transplanting was done after 25 days of sowing at 20 cm x 15 cm hill spacing in wet season. But, in case of dry season variety was sown in January. All the agronomic practices were followed except plant protection measures during crop growth period. Observations on the incidence of hemipteran insects were recorded on rice hills present in one meter square area randomly at 6 spots at 10 days interval. The observation were taken from 10 days after transplanting to harvesting stage and sampling of the hemipteran insects were also conducted during that period to determine their species composition. The samples were collected by adopting the methods of sweeping. Sweeping were done between 7.30 a.m. to 11.00 a.m. from rice fields during rice growth period. Then hemipteran insects were identified using available keys and guides from the various references (such as Dale, 1994; Barrion & Litsinger, 1994; Pathak & Khan, 1994; Biswas et al., 2014; Ghosh, 2008; Datta et al., 1985; Sheikh et al., 2017; Salini & Viraktamath, 2015; Das et al., 2017).

Statistical analysis Numbers of different hemipteran insects were pooled over months (July-May) to know the abundance of different insects in rice. One way Analysis of Variance (ANOVA) test was followed to find out the difference in the population of different hemipteran insects in different months and significant differences were determined by using Tukey’s Honest Significant Difference (HSD) test at probability level P ˂ 0.05 by using SPSS 16 statistical package.

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RESULTS

Incidence of hemipteran insect fauna A total of 19 hemipteran insect taxa belonging to eight insect families were documented from the rice fields studied at west central table land zone of Odisha (Table 1). Among them, eight taxa viz., Nilaparvata lugens (Stal), Sogatella furcifera (Horvath), Nepotettix virescens (Distant), Nephotettix nigropictus (Stal), Nephotettix cincticeps (Uhler), Menida histrio Fabricius, Dolycoris indicus (Stal.), and Leptocoriza oratorius (Fabricius) were abundant in rice ecosystem at Chiplima (Table 3). A higher species richness of hemipteran bugs were observed during the milking and grain ripening stages of the rice crop (Tables 2, 3, 4 and Fig. 1).

Table 1. List of Hemipteran insect with their families found in rice at west central table land zone of Odisha.

Insect Family Insects name Cicadellidae Nephotettix virescens (Distant), N. nigropictus (Stal), N. cincticeps (Uhler), Cofana spectra Distant, C. unimaculata (Signoret) Hecalus porrectus Walker Recilia dorsalis (Motschulsky) Delphacidae Nilapervata lugens (Stal) Sogatella furcifera (Horvath) perpusilla (Walker) Pentatomidae Nezara viridula (Lin.) Eysarcoris ventralis Westw Menida histrio Fabricius Dolycoris indicusStal Coreidae Cletus puntiger (Dallas) Alydidae Leptocorisa oratorious (Fabricius) Riptortus linearis (Fabricius) Lygaeidae Graptostethus servus (Fabricius) Miridae Cyrtorhinus lividipennis Reuter

Table 2. Hemipteran insect associated with different growth stages of rice.

Stage Insects Nursery Nephotettix virescens, Nephotettix nigropictus Tillering Sogatella furcifera, Nilaparvata lugens, Nephotettix virescens, Nephotettix nigropictus, Nephotettix cincticeps, Hecalus porrectus, Cofana unimaculata, Recilia dorsalis, Cofana spectra, Pyrilla perpusilla Booting Sogatella furcifera, Nilaparvata lugens, Recilia dorsalis, Cofana spectra, Nephotettix virescens, Nephotettix nigropictus, Nephotettix cincticeps, Hecalus porrectus, Cofana unimaculata, Cyrtorhinus lividipennis, Pyrilla perpusilla Flowering Sogatella furcifera, Nilaparvata lugens, Recilia dorsalis, Cofana spectra, Nezara viridula, Eysarcoris ventralis, Menida histrio, Dolycoris indicus, Cyrtorhinus lividipennis, Nephotettix virescens, Nephotettix nigropictus Nephotettix cincticeps, Hecalus porrectus, Cofana unimaculata, Pyrilla perpusilla

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Milking Sogatella furcifera, Nilaparvata lugens, Recilia dorsalis, Cofana spectra, Nezara viridula, Eysarcoris ventralis, Menida histrio, Dolycoris indicus, Leptocorisa oratorius, Cyrtorhinus lividipennis, Nephotettix virescens, Nephotettix nigropictus, Nephotettix cincticeps, Hecalus porrectus, Cofana unimaculata, Cletus puntiger, Riptortus linearis, Graptostethus servus Ripening Sogatella furcifera, Nilaparvata lugens, Recilia dorsalis, Cofana spectra, Nezara viridula, Eysarcoris ventralis, Menida histrio, Dolycoris indicus, Leptocoris oratorius, Cyrtorhinus lividipennis, Nephotettix virescens, Nephotettix nigropictus, Nephotettix cincticeps, Hecalus porrectus, Cofana unimaculata, Cletus puntiger, Riptortus linearis, Graptostethus servus Harvesting Nephotettix virescens, Nephotettix nigropictus, Nephotettix cincticeps, Leptocorisa oratorius

Table 3. Incidence of different hemipteran insect families* in rice during 2017-18.

Month Cicadellidae Delphacidae Alydidae Pentatomidae 2017 July 4.00 (2.12)d 0.00 (0.71)g 0.00 (0.71)d 0.00 (0.71)d Aug. 8.95 (3.07)cd 5.33 (2.41)efg 0.00 (0.71)d 0.00 (0.71)d Sep. 17.46 (4.24)bc 18.67 (4.38)ef 0.00 (0.71)d 0.00 (0.71)d Oct. 66.83 (8.20)a 163.50 (12.81)cd 0.00 (0.71)d 1.46 (1.40)bc Nov. 51.0 (7.18)a 739.50 (27.20)a 3.37 (1.97)c 4.79 (2.30)ab Dec. 27.83 (5.32)b 224.83 (15.01)c 6.50 (2.64)b 5.05 (2.35)ab 2018 Feb. 3.83 (2.08)d 1.67 (1.47)fg 0.00 (0.71)d 0.00 (0.71)d March 30.21 (5.54)b 22.85 (4.83)e 0.00 (0.71)d 0.00 (0.71)d April 70.25 (8.41)a 100.46 (10.05)d 4.00 (2.12)c 1.67 (1.47)bc May 29.08 (5.44)b 436.97 (20.91)b 10.33 (3.29)a 10.33 (3.29)a *Mean number of insects in a family per meter square. Figures in parentheses are square root transformed values Mean in each column with different alphabets indicate a significant difference in their abundance in different months (P<0.05, ANOVA, Tukeys HSD)

Table 4. Incidence of different hemipteran insect families* in rice during 2017-18.

Month Miridae Coreidae Lygaeidae Lophopidae 2017 July 0.00 (0.71)d 0.00 (0.71)a 0.00 (0.71)c 0.00 (0.71)a Aug. 0.00 (0.71)d 0.00 (0.71)a 0.00 (0.71)c 0.00 (0.71)a Sep. 0.05 (1.00)d 0.00 (0.71)a 0.00 (0.71)c 0.00 (1.00)a Oct. 18.33 (4.34)c 0.50 (1.00)a 0.05 (0.74)b 0.22 (0.85)a Nov. 94.17 (9.73)a 0.50 (1.00)a 0.50 (1.00)ab 0.38 (0.94)a Dec. 46.33 (6.84)b 0.17 (0.82)a 0.83 (1.15)a 0.00 (0.71)a 2018 Feb. 0.00 (0.71)d 0.00 (0.71)a 0.00 (0.71)c 0.00 (0.71)a March 1.50 (1.41)d 0.00 (0.71)a 0.00 (0.71)c 0.00 (0.71)a April 8.33 (2.97)c 0.00 (0.71)a 0.00 (0.71)c 0.22 (0.85)a May 38.17 (6.22)b 0.50 (1.00)a 0.72 (1.10)ab 0.05 (0.74)a *Mean number of insects in a family per meter square. Figures in parentheses are square root transformed values Mean in each column with different alphabets indicate a significant difference in their abundance in different months (P<0.05, ANOVA, Tukeys HSD)

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Figure 1. Number of insect families collected by sweep net during the sampling period from July, 2017 to May, 2018.

The study revealed that Delphacidae family of hemipteran insects were most abundant from tillering stage to crop maturity stage of rice growth period (F=166.69, df=9, p<0.05) and insects belonging to cicadellidae family were present throughout the rice growth period (F=54.57, df=9, p<0.05). Among delphacids, N. lugens and S. furcifera were prevalent species in both the wet and dry seasons. The population of both N. lugens and S. furcifera were reached to 24 to 65 per hill in November month of 2017 whereas in dry period of 2018 it reached to 18 to 46 per hill in the month of May. In cicadellids; most abundant species were Nephotettix virescens, N. cincticeps and N. nigropictus and their population was significantly higher in October in wet season and April in dry season. The mirid bug, Cyrtorhinus lividipennis Reuter, is a predator of plant and leafhopper eggs found in large numbers in November last week in wet season, and in May in dry period (F=103.55, df=9, p<0.05). Among alydidae, earhead bug; L. oratorius was most predominant and appeared from milky stage to grain maturity stage of rice growth period and they were more abundant in dry season (7-15 numbers/m2 in May 2018 whereas in wet season, 2017 it was found only 3-8/m2 in November) in comparison to wet season (F=99.201, df=9, p<0.05). In lygaeidae, Graptostethus servus (Fabricius) was first time observed in rice field during milking stage of rice. It is also first record from rice. It was observed that four species of pentatomidae attacked the rice crop at Chiplima, Odisha. They were; Nezara viridula (Lin.), Eysarcoris ventralis Westwood, Menida histrio Fabricius and Dolycoris indicus Stal. In dry season, they infested rice crop from the April to May months in flowering to ripening stage (F=12.43, df=9, p<0.05). But, in wet season, they were found in rice fields during the October to December months and most abundant species were M. histrio and D. indicus. In wet season their numbers were 1-8/m2 in December whereas in dry season their number was 5- 14/m2 in May. Other hemipteran insect belonging Coreidae and Lophopidae families were less in numbers and were not significantly different between the months.

Taxonomic keys for easy field identification Simplified taxonomic key prepared for various hemipteran insect infesting rice (Fig. 2) are given below.

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Cicadellidae Body green in colour, length 4.5-4.7 mm, vertex without band, forewings with distinct black spot that does not touch claval suture and apical portion black in colour...... ………………………………………………………………………………………………...... Nephotettix virescens Body green in colour, length 3.6-4.3 mm, vertex round with black submerginal band, anterior margin of pronotum with a black marking. Inner margin of clavous black in colour, forewings with distinct wedge shaped black marks touch the claval suture and apical portion black in colour……………………………………………………………………………Nephotettix nigropictus Body green in colour, length 4.5-4.65 mm, vertex round, no black spot present on forewing but apex portion grayish black in colour, last abdominal segment bears bead like band………. …………………………………….……………………………………………………………..Nephotettix cincticeps Body white in colour, length 9.1-10 mm, vertex rounded with 4 black spots, 3 spots in one row at base of vertex, forewings grayish white with prominent veins…...... Cofana spectra Body pale green in colour, length 5-6.6 mm, vertex and pronotum light green, 3 spots present on vertex in transverse series, forewings grayish white with veins………………………… ……………..……………………………………………………………………………………….Cofana unimaculata Adults are greenish yellow, length 4.7-5.4 mm, vertex with 4 longitudinal yellow lines, pronotum with 6 and 3 lines present on scutellum, forewing light green in colour with veins………………………………………………………………………………………………….Hecalus porrectus Adults are white in colour, length 3-3.55 mm, eyes red, vertex and pronotum white in colour, forewings with dark brown longitudinal zigzag band……….………………Recilia dorsalis Delphacidae Adults are brownish yellow, length 3.5-5 mm, pronotum pale brownish yellow, tegmina subhyaline with yellowish tint, veins smoky brown, an elongate black spot at apex of clavus.. …………………………………………….………………………………………………………….Nilapervata lugens Adults are light brownish yellow, length 3.3-5 mm, pronotum white medially with two punctured dots, mesonotum black in colour and apex region yellowish white, tegmina hyaline with brownish yellow vein, abdomen black, legs pale yellow……….Sogetella furcifera Alydidae Adult body cylindrical, brownish in colour, length 14-17.5 mm, pronotum with distinct central carinate line, dorsal abdomen reddish brown in colour while ventrolateral margins pale greenish yellow in colour, with brownish black spot…………………Leptocorisa oratorious Adults are slender dark cinnamon brown in colour, length 14-16.5 mm, apical half of 2nd and 3rd and whole 1st antennal segments dark reddish brown, lateral side of whole insect with a broad longitudinal yellowish band……………………………………………….………..Riptortus linearis Miridae Adults are green in colour, length 2.8-3.2 mm, apex of 1st antennal segment greenish yellow, hemelytra and legs greenish, longitudinal median line of scutellum black, all tibiae yellow in colour……………………………………………………………………………………….Cyrtorhinus lividipennis Pentatomidae Body green, shield shaped, length 11.8-16.7 mm, antennae green, apically brownish, three small white spots present on the front edge of the scutellum……………………...Nezara viridula Adult head with 4 black longitudinal lines, length 6.3-8.2 mm, scutellum with white mark in each basal angle and the apical region reddish ochraceous in colour, wings apical region reddish ochraceous with a black spot………………………………………………………...Menida histrio Adult head narrow, scutellum not hump shaped, length 9.5-10.6 mm, head yellow or orange yellow mottled with cluster of black spots, scutellum apex pale yellow, disk of scutellum with Y shaped mark pale ochraceous……………………………………………………………..Dolycoris indicus Adults are black or dark brown with ochraceous spots, length 5-6.5 mm, head shorter than breadth, three small yellow spots on the front edge of the scutellum, scutellum is broadly rounded apex and extending well beyond half of abdomen, tylus with a thin yellow longitudinal stripe………………………………………………………..………………….Eysarcoris ventralis Lophopidae Adults are straw in colour with long pointed snout and prominent red eyes, length 18.6-20.5 mm, wings are folded on the abdomen in the shape of a roof, legs are pale yellow in colour…. …………………………………………………………………………………………………………..Pyrilla perpusilla

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Coreidae Adults are 9.7-11.6 mm long, head narrower and shorter than pronotum, forewings pale brown in colour with white spots, humeri longer, protruded laterally and sharply pointed…………………………………………………………………………………………………Cletus punctiger Lygaeidae Adults are pale red in colour, length 8.8-9.7 mm, large black spot on the lateral area of each sterna segment, leg, antennae and rostrum are black in colour, rostrum reaching posterior coxae……………………………………………………..……………………………………..Graptostethus servus

Figure 2. 1; Dolycoris indicus 2; Nezara viridula 3; Menida histrio 4; Eysarcoris ventralis 5; Nephotettix virescens 6; Graptostethus servus 7; Cletus puntiger 8; Nephotettix nigropictus 9; Leptocorisa oratorius 10; Sogatella furcifera 11; Nilaparvata lugens 12; Riptortus linearis 13; Cofana spectra 14; Recilia dorsalis 15; Cyrtorhinus lividipennis 16; Cofana unimaculata 17; Hecalus porrectus 18; Nephotettix cincticeps.

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DISCUSSION

The study revealed that Delphacidae family of hemipteran insect were most prevalent from tillering stage to crop maturity stage of rice growth period. This finding is in accordance with the finding of Seni & Naik (2017) whom reported that N. lugens and S. furcifera were the serious pests of rice in Hirakud command area situated at west central table land zone of Odisha. In our study, highest number of insect genus (4) belongs to both Pentatomidae and Cicadellidae family followed by delphacidae and alydidae with each having (2). Although same genus numbers were found in both Pentatomidae and Cicadellidae family but maximum species (7 spp.) were observed in Cicadellidae family. Among cicadellidae except Nephotettix virescens, N. nigropictus and Cofana spectra insects, N. cincticeps, C. unimaculata, Hecalus porrectus, Recilia dorsalis were first time reported from here in rice ecosystem. But in pentatomidae insects, four species (N. viridula, E. ventralis, M. histrio and D. indicus) were observed infesting rice crop. Although, previously some pentatomidae bugs were observed in rice in coastal zone of Odisha (Gupta et al., 1989) but the mentioned bugs were first time recorded from west central table land zone of Odisha. Bambaradeniya & Edirisinghe (2008) studied the species composition, structure and abundance of guilds in rice ecosystem in Sri Lanka and found that majority of the insect species belonged to the order hymenoptera (81 species in 26 families) followed by Lepidoptera (58 species in 7 families), coleopteran (40 species in 8 families), hemiptera (38 species in 17 families) and diptera consists of 21 species in 11 families in rice ecosystem. They further observed that among hemipteran insects most dominated families were Cicadellidae (10 spp.) and Pentatomidae (7 spp.). Earhead bug; L. oratorius was more prevalent in rice crop from milky stage to grain maturity stage at Chiplima and this finding is in conformity with the findings of Chakraborty & Chatterjee (2002) whom observed that earhead bug, L. acuta on rice was high during panicle formation when the temperature was 27o to 340 C and the relative humidity was 85 to 90 per cent. Ghosh et al., 2016 studied the diversity of insects present in the rice fields in Burdwan district, West Bengal, India and observed that among hemipteran insects, green leaf hopper (Nephotettix sp) and gandhi bug (Leptocorisa sp.) were the major pests in rice. The incidence of Graptostethus servus was a new record on rice. Pentatomidae insects were more prevalent in flowering, milking and ripening stages of the rice crop at Chiplima. Kandiben (2008) also observed that pentatomid bugs were abundant in flowering and dough stages of the rice growth period. Other insects belonging to Coreidae, Alydidae and Lygaeidae families were observed in milking stage to ripening stage of rice but their numbers were very less. Insects belonging to Coreidae and Lophopidae families were not significantly different among different months of rice growth period. Our findings are also in accordance with Marques et al. (2000) who mentioned that in particular stage of a crop growth period, some group of insects present abundantly than other group of insects. This information on the incidence of hemipteran insect fauna and their simplified taxonomic key would be very useful for easy identification and monitoring in field and which ultimately helps in formulating suitable management practices in case of their outbreak.

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LITERATURE CITED

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