Sains Malaysiana 53(1)(2024): 1-10

http://doi.org/10.17576/jsm-2024-5301-01

Molluscicidal Activity of Entomopathogenic Fungus, Metarhizium anisopliae (Hypocreales: Clavicipitaceae) against Golden Apple Snails, Pomacea canaliculata(Architaeniglossa: Ampullariidae)

(Aktiviti Moluskisid Kulat Entomopatogen, Metarhizium anisopliae (Hypocreales: Clavicipitaceae) terhadap Siput Gondang Emas, Pomacea canaliculata (Architaeniglossa: Ampullariidae))

MOHAMAD IKMAL HAKIM ALLAHUDIN¹, ANIS JAZLEENA SYAFIQAH ANN JAISOFI¹, MA NYUK LING¹, THILAHGAVANI NAGAPPAN¹, AZIZ AHMAD¹, NG LEE CHUEN² & WAHIZATUL AFZAN AZMI^1,*

¹Faculty of Science and Marine Environment, Universiti Malaysia Terengganu, 21030 Kuala Nerus, Terengganu, Malaysia

²Faculty of Fishery and Food Science, Universiti Malaysia Terengganu, 21030 Kuala Nerus, Terengganu, Malaysia

Received: 6 March 2023/Accepted: 5 January 2024

Abstract

Golden Apple Snails (GAS, Pomacea canaliculata) is known in Malaysia as one of the world's worst invasive pest species, wreaking havoc on paddy fields by lowering rice yield dramatically. Farmers now employ chemical molluscicides to eliminate GAS, but these are expensive and have serious health and environmental consequences. Biological control agent using entomopathogenic fungus is preferred over chemical molluscicides to control GAS because it is non-toxic, environmentally friendly and cost-effective. This study is aimed to investigate the molluscicidal activity of an entomopathogenic fungus, Metarhizium anisopliae towards GAS adults and eggs. M. anisopliae conidia were subsequently produced into four concentrations (3×10⁴, 3×10⁵, 3×10⁶, and 3×10⁷ conidia/mL) and tested against adults and eggs GAS. The median lethal time (LT₅₀) for the concentration of 3×10⁷ took 5 and 3 days to kill 50% of GAS adults and inhibited 50% of eggs from hatching, respectively. Physiological analysis was also conducted on both GAS adults and eggs. The skin of infected individuals became white and opaque, while internal organs such as the pulmonary sac, digestive tract, and hepatopancreas were visibly destroyed. The colour of GAS eggs turned pale after M. anisopliaeinfestation and resulted in non-viable eggs. This research shows that M. anisopliae is an effective biological control agent for GAS and has the potential to be used as a targeted bio-molluscicide for GAS management.

Keywords: Biopesticide; entomopathogenic fungus; Golden Apple Snail; Pomacea canaliculate; sustainable agriculture

Abstrak

Siput Gondang Emas (GAS, Pomacea canaliculata) dikenali di Malaysia sebagai salah satu spesies haiwan perosak paling bahaya yang mendatangkan bencana kepada sawah-sawah padi dengan mengurangkan hasil tuaian padi secara dramatik. Pesawah kini menggunakan racun moluska kimia untuk menghapuskan GAS, akan tetapi cara ini agak mahal dan mendatangkan kesan yang serius kepada kesihatan dan persekitaran. Kaedah kawalan biologi menggunakan kulat entomopatogen lebih diutamakan berbanding racun moluska kimia bagi mengawal GAS kerana ia tidak toksik, mesra alam dan berkesan kos. Penyelidikan ini bertujuan untuk mengkaji aktiviti moluskisid bagi satu kulat entomopatogen, Metarhizium anisopliae, terhadap siput dewasa dan telur GAS. Konidia M. anisopliae kemudiannya dihasilkan kepada empat kepekatan (3×10⁴, 3×10⁵, 3×10⁶, dan 3×10⁷ konidia/mL) dan diuji ke atas siput dewasa dan telur GAS. Tempoh masa maut median (LT₅₀) bagi kepekatan 3×10⁷ untuk membunuh 50% siput dewasa dan menghalang 50% telur GAS daripada menetas, masing-masing mengambil masa 5 dan 3 hari. Analisis fisiologi juga telah dijalankan bagi kedua-dua siput dewasa dan telur GAS. Kulit individu yang dijangkiti menjadi putih dan legap, manakala organ dalaman seperti kantung pulmonari, saluran penghadaman dan hepatopankreas kelihatan hancur. Warna telur GAS bertukar menjadi pucat setelah dijangkiti M. anisopliaedan mengakibatkan telur-telur itu tidak berdaya hidup. Kajian ini menunjukkan bahawa M. anisopliaemerupakan satu kaedah kawalan biologi yang berkesan untuk GAS dan berpotensi disasarkan sebagai bio-moluskisid untuk pengawalan GAS.

Kata kunci: Kulat entomopatogen; pertanian mampan; Pomacea canaliculata; racun perosak bio; Siput Gondang Emas

REFERENCES

Abdullah, A.N. & Reyhan, M. 2017. Karakterisasi dan identifikasi senyawa aktif ekstrak pigmen telor keong mas. Jurnal Pengolahan dan Perikanan Indonesia 20: 286-295.

Azmi, W.A., Khoo, S.C., Ng, L.C., Baharuddin, N., Aziz, A.A. & Ma, N.L. 2022. The current trend in biological control approaches in the mitigation of golden apple snail Poamcea spp. Biological Control 175: 105060.

Dai, L., Wang, W., Dong, X., Hu, R. & Nan, X. 2011. Molluscicidal activity of cardiac glycosides from Nerium indicum against Pomacea canaliculata and its implications for the mechanisms of toxicity. Environmental Toxicology and Pharmacology 32(2): 226-232.

Damborenea, C., Brusa, F. & Negrete, L. 2017. Symbionts and diseases associated with invasive apple snails. In Biology and Management of Invasive Apple Snails, edited by Joshi, R.C., Robert, H.C. & Sebastian, L.C. Nueva Ecija: Philippine Rice Research Institute. pp. 73-97.

Dotaona, R., Wilson, B.A.L., Stevens, M.M., Holloway, J. & Ash, G.J. 2017. Chronic effects and horizontal transmission of Metarhizium anisopliae strain QS155 infection in the sweet potato weevil, Cylas formicarius (Coleoptera: Brentidae). Biological Control 114: 24-29.

Duarte, G.F., Rodrigues, J., Fernandes, É.K.K., Humber, R.A. & Luz, C. 2015. New insights into the amphibious life of Biomphalaria glabrata and susceptibility of its egg masses to fungal infection. Journal of Invertebrate Pathology 125: 31-36.

El-Sahn, O.M.N. & Shairra, S.A. 2012. Efficiency of Metarhizium anisopliae var acridum and certain chemical compounds on garden snails, Cornu aspersum (= Helix aspersa). Journal of the Egyptian-German Society of Zoology 64: 103-111.

Gohar, A.A., Maatooq, G.T., Gadara, S.R., Aboelmaaty, W.S. & El-Shazly, A.M. 2014. Molluscicidal activity of the methanol extract of Callistemon viminalis (Sol. ex Gaertner) G.Don ex loudon fruits, bark and leaves against Biomphalaria alexandrina snails. The Iranian Journal of Pharmaceutical Research 13(2): 505-514.

Grace, L.E.L., Jamilah, M.S., Mohd Farid, A. & Wahizatul, A.A. 2017. Entomopathogenic fungi isolated from the soil of Terengganu, Malaysia as potential bio-pesticides against the red palm weevil, Rhynchophorus ferrugineus. Journal of Sustainability Science Management 12: 71-79.

Hasyierah, N.M.S., Arbain, D., Zulkali, M.M.D., Pilus, N. & Rohaina, N. 2012. Distribution and management of Pomacea canaliculata in the northern region of Malaysia: Mini review. Procedia APCBEE 2: 129-134.

Joshi, R.C., Martín, R.S., Saez-Navarrete, C., Alarcon, J., Sainz, J., Antolin, M.M., Martin, A.R., & Sebastian, L.S. 2008. Efficacy of quinoa (Chenopodium quinoa) saponins against golden apple snail (Pomacea canaliculata) in the Philippines under laboratory conditions. Crop Protection 27(3-5): 553-557.

Kasim, N.M., Ahmad, M.H., Shaharudin, A.B., Naidu, B.M., Chan, Y.Y. & Aris, T. 2018. Food choices among Malaysian adults: Findings from Malaysian adults’ nutrition survey (MANS) 2003 and MANS 2014. Malaysian Journal of Nutrition 24(1): 63-75.

Ke, W., Lin, X., Yu, Z., Sun, Q. & Zhang, Q. 2017. Molluscicidal activity and physiological toxicity of Macleaya cordata alkaloids components on snail Oncomelania hupensis. Pesticide Biochemistry and Physiology 143: 111-115.

Leemon, D.M. & Jonsson, N.N. 2008. Laboratory studies on Australian isolates of Metarhizium anisopliae as a biopesticide for the cattle tick Boophilus microplus. Journal of Invertebrate Pathology 97(1): 40-49.

Liang, K., Zhang, J.E., Fangm L., Zhao, B., Luo, M., Parajuli, P. & Ouyang, Y. 2013. The biological control of Pomacea canaliculata population by rice-duck mutualism in paddy fields. Biocontrol Sci. Tech. 23: 674-690.

Liu, C., Zhang, Y., Ren, Y., Wang, H., Li, S., Jiang, F., Yin, L., Qiao, X., Zhang, G., Qian, W., Liu, B. & Fan, W. 2018. The genome of the golden apple snail Pomacea canaliculata provides insight into stress tolerance and invasive adaptation. GigaScience 7(9). https://doi.org/10.1093/gigascience/giy101

Noorshilawati, A.A., Nur Suraya, A. & Siti Rosiyyah, S. 2020. Molluscicidal activity of Ipomoea batatas leaf extracts against Pomacea canaliculata(Golden apple snail). Food Research 4(5): 131-137.

Nur Suraya, A., Noorshilawati, A.A. & Rosminah, M. 2017. Molluscicidal activity of Entada rheedii stem bark methanolic extract against paddy pest Pomacea canaliculata(golden apple snail. Malaysian Journal of Analytical Science 21(1): 46-51.

Rahim, K.A.A. & Joshi, R.C. 2019. The current status of invasive apple snails, Pomacea spp., in Malaysia: A short review. Agriculture for Development 37: 58-63.

Ramle, M., Mohd Basri, W., Norman, K., Siti Ramlah, A.A. & Noor Hisham, H. 2016. Research into the commercialization of Metarhizium anisopliae (Hyphomycetes) for biocontrol of the rhinoceros beetle, Oryctes rhinoceros (Scarabaeidae) in oil palm. Journal of Oil Palm Research 18: 37-49.

Reddy, G.V.P., Zhao, Z. & Humber, R.A. 2014. Laboratory and field efficacy of entomopathogenic fungi for the management of the sweet potato weevil, Cylas formicarius (Coleoptera: Brentidae). Journal of Invertebrate Pathology 122: 10-15.

Resh, V.H. & Rosenberg, D.M. 2015. Economic aspects of freshwater invertebrates. In Thorp and Covich’s Freshwater Invertebrates: Ecology and General Biology, 4th ed., edited by Thorp, J., Rogers, D.C. Elsevier. pp. 93-109.

Schneiker, J., Weisser, W.W., Settele, J., Nguyen, V.S., Bustamante, J.V., Marquez, L. & Türke, M. 2016. Is there hope for sustainable management of golden apple snails, a major invasive pest in irrigated rice? NJAS - Wagen. Journal of Life Science 79: 11-21.

Shen, X., Wang, Z., Liu, L. & Zou, Z. 2018. Molluscicidal activity of Solidago canadensisL. extracts on the snail Pomacea canaliculataLam. Pesticide Biochemistry and Physiology 149: 104-112.

Su, S.T. 2006. Evaluation of different species of fish for biological control of golden apple snail Pomacea canaliculata (Lamarck) in rice. Crop Protection 25(9): 1004-1012.

Sun, J., Fuxa, J.R. & Henderson, G. 2003. Effects of virulence, sporulation, and temperature on Metarhizium anisopliae and Beauveria bassiana laboratory transmission in Coptotermes formosanus. Journal of Invertebrate Pathology 84: 38-46.

Teo, S.S. & Hamsein, N.N. 2017. The apple snail Pomacea canaliculata in East Malaysia – past, present and future. In Biology and Management of Invasive Apple Snails, edited by Joshi, R.C., Cowie, R.H. & Sebastian L.S. Nueva Ecija: Philippine Rice Research Institute. pp 197-208.

Tulloch, M. 1976. The genus Metarhizium. Transactions of British Mycology Society 66(3): 407-411.

Xu, Y., Li, A.J., Li, K., Qin, J. & Li, H. 2017. Effects of glyphosate-based herbicides on survival, development and growth of invasive snail (Pomacea canaliculata). Aquatic Toxicology 193: 136-143.

Yahaya, H., Amzah, B., Sivapragasam, A., Nordin, M., Muhamad Hisham, M.N. & Misrudin, H. 2017. Invasive apple snails in Malaysia. In Biology and Management of Invasive Apple Snails. 2nd ed., edited by Joshi, R.C., Cowie, R.H. & Sebastian L.S. Nueva Ecija: Philippine Rice Research Institute. pp. 187-613.

*Corresponding author; email: wahizatul@umt.edu.my