Home / Regular Issue / JTAS Vol. 45 (3) Aug. 2022 / JTAS-2427-2022


Species Composition and DNA Barcoding of Hemipteran Assemblages Throughout Paddy Growing Seasons

Salmah Yaakop, Suliza Sabri, Nur ‘Aimi Kamalia Kamaruddin, Norlaila Nabila Norizam and Muhamad Azmi Mohammed

Pertanika Journal of Tropical Agricultural Science, Volume 45, Issue 3, August 2022

DOI: https://doi.org/10.47836/pjtas.45.3.06

Keywords: COI, genetic, hemipteran, Malaysia, pest, rice, true bugs

Published on: 8 August 2022

Hemipterans are the diverse, abundant, and important pests in the paddy ecosystem due to their piercing and sucking mouthparts that feed on the crop causing significant losses in rice yields. Despite their important roles in the paddy ecosystem, the information on DNA barcode, diversity, and species richness has been occasionally discussed. This study aimed to measure its abundance, species richness, and barcode hemipteran species from the paddy ecosystem. Active sampling was used with two different sampling arrangements in the paddy ecosystem in Sabak Bernam, Selangor, for two different seasons. Hemipterans were collected and identified up to species level morphologically prior to DNA barcoding. The richness and the abundance of species were measured along with the paddy growth phases (vegetative, reproductive, and mature). A total of 2,167 individuals of seven hemipteran species (Cyrtorhinus lividipennis, Leptocorisa oratorius, Nephotettix virescens, Cofana spectra, Sogatella furcifera, Scotinophara coarctata, and Graptostethus sp.) were successfully collected with Shannon-Diversity Index (H’ = 0.4572), Margalef richness index (D = 0.7811), and Evenness Index (E = 0.2257). There was no significant difference (p > 0.05) for species diversity in both seasons. The highest abundance of hemipteran was during the maturity stage (1,543 individuals), followed by the reproductive (591 individuals) and vegetative stages (33 individuals). This study observed a significant difference between the paddy growth for both seasons (p < 0.05). Five hemipteran species namely C. lividipennis, L. oratorius, N. virescens, C. spectra, and S. furcifera, were successfully barcoded with Leptocorisa, the dominant genus. Outcomes from this study suggested that different hemipteran management approaches must be developed to cater to different hemipteran species at different paddy growth stages for a successful and sustainable paddy growing practice in Malaysia.

  • Abdullah, T., Nasruddin, A., & Agus, N. (2017). Populations of rice grain bug, Paraeuscosmetus pallicomis (Hemiptera: Lygaeidae) in weed-free paddy field, weedy paddy field and paddy dykes. Tropical Life Sciences Research, 28(2), 1-7. https://doi.org/10.21315/tlsr2017.28.2.1

  • Ali, M. P., Bari, M. N., Haque, S. S., Kabir, M. M. M., Afrin, S., Nowrin, F., Islam, M. S., & Landis, D. A. (2019). Establishing next-generation pest control services in rice fields: Eco-agriculture. Scientific Reports, 9, 10180. https://doi.org/10.1038/s41598-019-46688-6

  • Altschul, S. F., Gish, W., Miller, W., Myers, E. W., & Lipman, D. J. (1990). Basic local alignment search tool. Journal of Molecular Biology, 215(3), 403-410. https://doi.org/10.1016/S0022-2836(05)80360-2

  • Alves, T. M., Maia, A. H., & Barrigossi, J. A. (2016). Spatial distribution and coexisting patterns of adults and nymphs of Tibraca limbativentris (Hemiptera: Pentatomidae) in paddy rice fields. Environmental Entomology, 45(6), 1505-1514. https://doi.org/10.1093/ee/nvw141

  • Ashrith, K. N., Sreenivas, A. G., Guruprasad, G. S., Hanchinal, S. G., & Chavan, I. (2017). Insect diversity: A comparative study in direct seed and transplanted rice ecosystem. Journal of Entomology and Zoology Studies, 5(6), 762-765.

  • Bambaradeniya, C. N. B., Edirisinghe, J. P., de Silva, D. N., Gunatilleke, C. V. S., Ranawana, K. B., & Wijekoon, S. (2004). Biodiversity associated with an irrigated rice agro-ecosystem in Sri Lanka. Biodiversity and Conservation, 13(9), 1715-1753. https://doi.org/10.1023/B:BIOC.0000029331.92656.de

  • Chandrasekar, K., Muthukrishnan, N., & Soundararajan, R. P. (2017). Ecological engineering cropping methods for enhancing predator, Cyrtorhinus lividipennis (Reuter) and suppression of planthopper, Nilaparvata lugens (Stal) in rice-effect of intercropping system. Journal of Entomology and Zoology Studies, 5(5), 1778-1782.

  • Cobblah, M. A., & Den Hollander, J. (1992). Specific differences in immature stages, oviposition sites and hatching patterns in two rice pests, Leptocorisa oratorius (Fabricius) and L. acuta (Thunberg) (Heteroptera: Alydidae). International Journal of Tropical Insect Science, 13(1), 1-6. https://doi.org/10.1017/S1742758400013825

  • Cohen, J. E., Schoenly, K., Heong, K. L., Justo, H., Arida, G., Barrion, A. T., & Litsinger, J. A. (1994). A food web approach to evaluating the effect of insecticide spraying on insect pest population dynamics in a Philippine irrigated rice ecosystem. Journal of Applied Ecology, 31(4), 747-763. https://doi.org/10.2307/2404165

  • Dasgupta, I., Hull, R., Eastop, S., Poggi-Pollini, C., Blakebrough, M., Boulton, M. I., & Davies, J. W. (1991). Rice tungro bacilliform virus DNA independently infects rice after Agrobacterium-mediated transfer. Journal of General Virology, 72(6), 1215-1221. https://doi.org/10.1099/0022-1317-72-6-1215

  • Davis, R. B., Baldauf, S. L., & Mayhew, P. J. (2010). Many hexapod groups originated earlier and withstood extinction events better than previously realized: inferences from supertrees. Proceedings of the Royal Society B: Biological Sciences, 277(1687), 1597-1606. http://doi.org/10.1098/rspb.2009.2299

  • Dong, X., Yi, W., Zheng, C., Zhu, X., Wang, S., Xue, H., Ye, Z., & Bu, W. (2021). Species delimitation of rice seed bugs complex: Insights from mitochondrial genomes and ddRAD‐seq data. Zoologica Scripta, 51(2), 185-198. https://doi.org/10.1111/zsc.12523

  • Folmer, O., Black, M., Hoeh, W., Lutz, R., & Vrijenhoek, R. (1994). DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology, 3(5), 294-299.

  • Hafizal, M. M., & Idris, A. B. (2013). Field population abundance of leafhopper (Homoptera: Cicadelidae) and planthopper (Homoptera: Delphacidae) as affected by rice growth stages. In AIP Conference Proceedings (Vol. 1571, No. 1, pp. 359-362). American Institute of Physics. https://doi.org/10.1063/1.4858683

  • Halim, M., Aman-Zuki, A., Ahmad, S. Z. S., Din, A. M. M., Rahim, A. A., Masri, M. M. M., Zain, B. M. M., & Yaakop, S. (2018). Exploring the abundance and DNA barcode information of eight parasitoid wasps species (Hymenoptera), the natural enemies of the important pest of oil palm, bagworm, Metisa plana (Lepidoptera: Psychidae) toward the biocontrol approach and it’s application in Malaysia. Journal of Asia-Pacific Entomology, 21(4), 1359-1365. https://doi.org/10.1016/j.aspen.2018.10.012

  • Halim, M., Aman-Zuki, A., Mohammed, M. A., & Yaakop, S. (2017). DNA barcoding and relationships of eight ladybugs species (Coleoptera: Coccinellidae) that infesting several crops from Peninsular Malaysia. Journal of Asia-Pacific Entomology, 20(3), 814-820. https://doi.org/10.1016/j.aspen.2017.05.009

  • Hashim, N. A., Abd Aziz, M., Basari, N., Saad, K., Jasmi, A. H., & Ab Hamid, S. (2017). Diversity and guild structure of insects during rice flowering stage at a selected rice field in Penang, Malaysia. Malaysian Applied Biology, 46(3), 161-169.

  • Hebert, P. D., & Gregory, T. R. (2005). The promise of DNA barcoding for taxonomy. Systematic Biology, 54(5), 852-859. https://doi.org/10.1080/10635150500354886

  • Hebert, P. D., Cywinska, A., Ball, S. L., & DeWaard, J. R. (2003). Biological identifications through DNA barcodes. Proceedings of the Royal Society of London. Series B: Biological Sciences, 270(1512), 313-321. https://doi.org/10.1098/rspb.2002.2218

  • International Rice Research Institute. (2022). Pest management: Insects. IRRI. http://www.knowledgebank.irri.org/training/fact-sheets/pest-management/insects

  • Ishizaki, M., Yasuda, T., & Watanabe, T. (2007). Feeding behavior of rice bug Leptocorisa chinensis (Dallas) (Heteroptera: Alydidae) nymphs on rice panicles and rice plant extract. Applied Entomology and Zoology, 42(1), 83-88. https://doi.org/10.1303/aez.2007.83

  • Kainoh, Y., Shimizu, K., Maru, S., & Tamaki, Y. (1980). Host-finding behavior of the rice bug, Leptocorisa chinensis Dallas (Hemiptera: Coreidae), with special reference to diel patterns of aggregation and feeding on rice plant. Applied Entomology and Zoology, 15(3), 225-233. https://doi.org/10.1303/aez.15.225

  • Kim, H., Baek, S., & Lee, J. H. (2017). Temperature-dependent development and oviposition models on Chinensis dallas (Hemiptera: Alydidae). Journal of Asia-Pacific Entomology, 21(1), 244-251. https://doi.org/10.1016/j.aspen.2017.12.006

  • Malipatil, M. B., Gao, C. Q., & Eow, L. X. (2020). Australian Lygaeoidea (Heteroptera) of economic importance identification of families, tribes and representative genera. Department of Jobs, Precints and Regions.

  • Meeran, M., Fathima, S., Priya, S., Arivoli, S., & Tennyson, S. (2021). Assessment of insect diversity in paddy fields of Uthamapalayam, Theni district, Tamil Nadu, India. Journal of Wildlife and Biodiversity, 5(2), 88-98. https://doi.org/10.22120/jwb.2020.135814.1183

  • Namara, R. E., Weligamage, P., & Barker, R. (2003). Prospects for adopting system of rice intensification in Sri Lanka: A socioeconomic assessment. International Water Management Institute.

  • Nasiruddin, M., & Roy, R. C. (2012). Rice field insect pests during the rice growing seasons in two areas of Hathazari, Chittagong. Bangladesh Journal of Zoology, 40(1), 89-100. https://doi.org/10.3329/bjz.v40i1.12898

  • Ooi, A. C. (2015). Common insect pests of rice and their natural biological control. UTAR Institutional Repository. http://eprints.utar.edu.my/id/eprint/1681

  • Paterson, H. E. H. (1991). The recognition of cryptic species among economically important insects. In M. P. Zalucki (Ed.), Heliothis: Research methods and prospects (pp. 1-10). Springer. https://doi.org/10.1007/978-1-4612-3016-8_1

  • Pathak, M. D., & Khan, Z. R. (1994). Insect pest of rice. International Rice Research Institute.

  • Rambaut, A. (2009). FigTree v1. 3.1. http://tree.bio.ed.ac.uk/software/figtree/

  • Rashid, M. M., Ahmed, N., Jahan, M., Islam, K. S., Nansen, C., Willers, J. L., & Ali, M. P. (2017). Higher fertilizer inputs increase fitness traits of brown planthopper in rice. Scientific Reports, 7, 4719. https://doi.org/10.1038/s41598-017-05023-7

  • Rattanapun, W. (2013). Biology of rice bug Leptocorisa oratorius (Fabricius) (Hemiptera: Alydidae), population change and alternative host plants. Communication in Agricultural and Applied Biological Sciences, 78(2), 193-197.

  • Razali, R., Yaakop, S., Abdullah, M., Ghazali, S. Z., & Aman-Zuki, A. (2015). Insect species composition in an under SRI management in Tanjung Karang, Selangor, Malaysia. Malaysian Applied Biology Journal, 44(4), 73-80.

  • Reissig, W. H., Heinrichs, E. A., Litsinger, J. A., Moody, K., Fiedler, L., Mew, T. W., & Barrion, A. T. (1986). Illustrated guide to integrated pest management in rice in tropical Asia. International Rice Research Institute.

  • Rosenthal, L. M., Larsson, K. H., Branco, S., Chung, J. A., Glassman, S. I., Liao, H. L., Peay, K. G., Smith, D. P., Talbot, J. M., Taylor, J. W., Vellinga, E. C., Vilgalys, R., & Bruns, T. D. (2017). Survey of corticioid fungi in North American pinaceous forests reveals hyperdiversity, underpopulated sequence databases, and species that are potentially ectomycorrhizal. Mycologia, 109(1), 115-127. https://doi.org/10.1080/00275514.2017.1281677

  • Rothschild, G. H. L. (1970). Observations on the ecology of the rice-ear bug Leptocorisa oratorius (F.) (Hemiptera: Alydidae) in Sarawak (Malaysian Borneo). Journal of Applied Ecology, 7(1), 147-167. https://doi.org/10.2307/2401616

  • Saunders, M. E., Peisley, R. K., Rader, R., & Luck, G. W. (2016). Pollinators, pests, and predators: Recognizing ecological trade-offs in agroecosystems. Ambio, 45(1), 4-14. https://doi.org/10.1007/s13280-015-0696-y

  • Savolainen, V., Cowan, R. S., Vogler, A. P., Roderick, G. K., & Lane, R. (2005). Towards writing the encyclopaedia of life: an introduction to DNA barcoding. Philosophical Transactions of the Royal Society B: Biological Sciences, 360(1462), 1805-1811. https://doi.org/10.1098/rstb.2005.1730

  • Schaefer, C. W. (2004). Key to the genera of new world Alydidae (Hemiptera: Heteroptera). Proceedings of the Entomological Society of Washington, 106(2), 280-287.

  • Shariff, S., Ibrahim, N.J., Md-Zain, B.M., Idris, A.B., Suhana, Y., Roff, M.N., & Yaakop, S. (2014). Multiplex PCR in determination of Opiinae parasitoids of fruit flies, Bactrocera sp., infesting star fruit and guava. Journal of Insect Science, 14, 7. https://doi.org/10.1093/jis/14.1.7

  • Siwi, S. S., & van Doesburg, P. H. (1984). Leptocorisa Latreille in Indonesia (Heteroptera, Coreidae, Alydinae). Zoologische Mededelingen, 58(7), 117-129.

  • Song, N., Liang, A. P., & Bu, C. P. (2012). A molecular phylogeny of Hemiptera inferred from mitochondrial genome sequences. PLOS One, 7(11), e48778. https://doi.org/10.1371/journal.pone.0048778

  • Su, J. Q., Ding, L. J., Xue, K., Yao, H. Y., Quensen, J., Bai, S. J., Wei, W. X., Wu, J. S., Zhou, J., Tiedje, J. M., & Zhu, Y. G. (2015). Long-term balanced fertilization increases the soil microbial functional diversity in a phosphorus-limited paddy soil. Molecular Ecology, 24(1), 136-150. https://doi.org/10.1111/mec.13010

  • Sulaiman, N., Isahak, A., Sahid, I.B., & Maimon, A. (2013). Diversity of pest and non-pest insects in an organic paddy field cultivated under the System of Rice Intensification (SRI): A case study in Lubok China, Melaka, Malaysia. Journal of Food Agriculture and Environment, 11(3), 2861-2865.

  • Sweet, M. H. (2000). Seed and chinch bugs (Lygaeoidea). In C. W. Schaefer & A. R. Panizzi (Eds.), Heteroptera of economic importance (pp. 143-264). CRC Press. https://doi.org/10.1201/9781420041859.ch6

  • Swofford, D. L. (2003). PAUP*. Phylogenetic Analysis Using Parsimony (* and other methods) (version 4.0b10). Sinauer Associates.

  • Tahir, H. M., Noor, A., Mehmood, S., Sherawat, S. M., & Qazi, M. A. (2018). Evaluating the accuracy of morphological identification of insect pests of rice crops using DNA barcoding. Mitochondrial DNA Part B, 3(2), 1220-1224. https://doi.org/10.1080/23802359.2018.1532334

  • Torres, M. A. J., Lumansoc, J., & Demayo, C. G. (2010). Variability in head shapes in three populations of the Rice Bug Leptocorisa oratorius (Fabricius) (Hemiptera: Alydidae). Egyptian Academic Journal of Biological Sciences. A, Entomology, 3(1), 173-184. https://doi.org/10.21608/eajbsa.2010.15252

  • Triplehorn, C. A., Johnson, N. F., & Borror, D. J. (2005). Borror and DeLong’s introduction to the study of insects (7th ed.). Thomson Brooks/Cole.

  • Yaakop, S., David-Dass, A., Shaharuddin, U. S., Sabri, S., Badrulisham, A. S., & Zain Che-Radziah, C. M. (2020). Species richness of leaf roller and stem borers (Lepidoptera) associated with different paddy growth and first documentation of its DNA barcode. Pertanika Journal of Tropical Agricultural Science, 43(4), 523-535. https://doi.org/10.47836/pjtas.43.4.08

  • Yashiro, T., & Sanada-Morimura, S. (2021). A rapid multiplex PCR assay for species identification of Asian rice planthoppers (Hemiptera: Delphacidae) and its application to early-instar nymphs in paddy fields. PLOS One, 16(4), e0250471. https://doi.org/10.1371/journal.pone.0250471

  • Zhang, J., Zheng, X., Jian, H., Qin, X., Yuan, F., & Zhang. R. (2013). Arthropod biodiversity and community structures of organic rice ecosystems in Guangdong province, China. Florida Entomologist, 96(1), 1-9. https://doi.org/10.1653/024.096.0101

ISSN 0128-7702

e-ISSN 2231-8534

Article ID


Download Full Article PDF

Share this article

Recent Articles