Pathogenicity of entomopathogenic fungi to eggs, larvae, and adults and their effects on development of Aedes albopictus
##plugins.themes.bootstrap3.article.sidebar##
Issue
Section
Articles
This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License.
##plugins.themes.bootstrap3.article.main##
Abstract
Abstract. Ramayanti I, Herlinda S, Muslim A, Hasyim H, Anwar C, Suwandi S, Damiri N, Irsan C, Verawaty M. 2023. Pathogenicity of entomopathogenic fungi to eggs, larvae, and adults and their effects on development of Aedes albopictus. Biodiversitas 24: 4766-4774. No information is available on the effect of fungi on the development of Aedes albopictus and the effectiveness of fungi in killing its eggs, larvae, and adults. The aim of this research was to determine the pathogenicity of entomopathogenic fungi on the eggs, larvae, and adults of Ae. albopictus and to investigate the effects of the fungi on the development of Ae. albopictus. The fungal species identified molecularly were Aedes albopictus, Beauveria bassiana, Metarhizium anisopliae, Penicillium citrinum, and Talaromyces diversus. The results showed that entomopathogenic fungi negatively affected the development of Ae. albopictus and could decrease the eggs laid by adult females and shorten adult longevity. M. anisopliae was the most pathogenic fungal species (mortality rate 100%) for eggs, larvae, pupae, and adults of Ae. albopictus. However, B. bassiana, P. citrinum, and T. diversus were also found pathogenic to them. The effect of eggs treated with entomopathogenic fungi negatively affected the larval, pupal, and adult stages of Ae. albopictus. These findings highlighted that M. anisopliae, B. bassiana, P. citrinum, and T. diversus have insecticidal activity against Ae. albopictus eggs, larvae, pupae, and adults. Therefore, further investigation is needed to develop these fungal species into ovicides, larvicides, and adulticides to control Ae. albopictus.
##plugins.themes.bootstrap3.article.details##
References
Akiner MM, Demirci B, Babuadze G, Robert V, Schaffner F. 2016. Spread of the invasive mosquitoes Aedes aegypti and Aedes albopictus in the Black Sea Region increases risk of chikungunya, dengue, and zika outbreaks in Europe. PLoS Neglected Tropical Diseases 10: 1–5. DOI:10.1371/journal.pntd.0004664.
Alkhaibari AM, Carolino AT, Bull JC, Samuels RI, Butt TM. 2017. Differential pathogenicity of Metarhizium blastospores and conidia against larvae of three mosquito species. Journal of Medical Entomology 54: 696–704. DOI:10.1093/jme/tjw223.
Alkhaibari AM, Carolino AT, Yavasoglu SI, Maffeis T, Mattoso TC, Bull JC, Samuels RI, Butt TM. 2016. Metarhizium brunneum blastospore pathogenesis in Aedes aegypti larvae: Attack on several fronts accelerates mortality. PLoS Pathogens 12: 1–19. DOI:10.1371/journal.ppat.1005715.
Blanford S, Jenkins NE, Read AF, Thomas MB. 2012. Evaluating the lethal and pre-lethal effects of a range of fungi against adult Anopheles stephensi mosquitoes. Malaria Journal 11: 1–10. DOI:10.1186/1475-2875-11-365.
Bonizzoni M, Gasperi G, Chen X, James AA. 2014. The invasive mosquito species Aedes albopictus: current knowledge and future perspectives. Trends in Parasitology 29: 460–468. DOI:10.1016/j.pt.2013.07.003.The.
Dhimal M, Gautam I, Joshi HD, O’Hara RB, Ahrens B, Kuch U. 2015. Risk factors for the presence of chikungunya and dengue vectors (Aedes aegypti and Aedes albopictus), their altitudinal distribution and climatic determinants of their abundance in Central Nepal. PLoS Neglected Tropical Diseases 9: 1–20. DOI:10.1371/journal.pntd.0003545.
Farnesi LC, Menna-Barreto RFS, Martins AJ, Valle D, Rezende GL. 2015. Physical features and chitin content of eggs from the mosquito vectors Aedes aegypti, Anopheles aquasalis and Culex quinquefasciatus: Connection with distinct levels of resistance to desiccation. Journal of Insect Physiology 83: 43–52. DOI:10.1016/j.jinsphys.2015.10.006.
Ferreira-De-Lima VH, Lima-Camara TN. 2018. Natural vertical transmission of dengue virus in Aedes aegypti and Aedes albopictus: A systematic review. Parasites and Vectors 11: 1–8. DOI:10.1186/s13071-018-2643-9.
Flor-Weiler LB, Rooney AP, Behle RW, Muturi EJ. 2017. Characterization of Tolypocladium cylindrosporum (Hypocreales: Ophiocordycipitaceae) and its impact against Aedes aegypti and Aedes albopictus eggs at low temperature. Journal of the American Mosquito Control Association 33: 184–192. DOI:10.2987/16-6596R.1.
Gabarty A, Salem HM, Fouda MA, Abas AA, Ibrahim AA. 2014. Pathogencity induced by the entomopathogenic fungi Beauveria bassiana and Metarhizium anisopliae in Agrotis ipsilon (Hufn.). J Radiat Res Appl Sci 7: 95–100. DOI:doi.org/10.1016/j.jrras.2013.12.004.
Greenfield BPJ, Peace A, Evans H, Dudley E, Ansari MA, Butt TM. 2015. Identification of Metarhizium strains highly efficacious against Aedes, Anopheles and Culex larvae. Biocontrol Science and Technology 25: 487–502. DOI:10.1080/09583157.2014.989813.
Gustianingtyas M, Herlinda S, Suwandi, Suparman, Hamidson H, Hasbi, Setiawan A, Verawaty M, Elfita, Arsi. 2020. Toxicity of entomopathogenic fungal culture filtrate of lowland and highland soil of South Sumatra (Indonesia) against Spodoptera litura larvae. Biodiversitas 21: 1839–1849. DOI:10.13057/biodiv/d210510.
Hamid PH, Prastowo J, Ghiffari A, Taubert A, Hermosilla C. 2017. Aedes aegypti resistance development to commonly used insecticides in Jakarta, Indonesia. PLoS ONE 12: 1–11. DOI:10.1371/journal.pone.0189680.
Herlinda S, Efendi RA, Suharjo R, Hasbi, Setiawan A, Elfita, Verawaty M. 2020. New emerging entomopathogenic fungi isolated from soil in South Sumatra (Indonesia) and their filtrate and conidial insecticidal activity against Spodoptera litura. Biodiversitas 21: 5102–5113. DOI:10.13057/biodiv/d211115.
Hussain A, Tian M-Y, He Y-R, Ahmed S. 2009. Entomopathogenic fungi disturbed the larval growth and feeding performance of Ocinara varians (Lepidoptera: Bombycidae) larvae. Insect Science 16: 511–517. DOI:10.1111/j.1744-7917.2009.01272.x.
Kalvnadi E, Mirmoayedi A, Alizadeh M, Pourian HR. 2018. Sub-lethal concentrations of the entomopathogenic fungus, Beauveria bassiana increase fitness costs of Helicoverpa armigera (Lepidoptera: Noctuidae) offspring. Journal of Invertebrate Pathology 158: 32–42. DOI:10.1016/j.jip.2018.08.012.
Kauffman E, Payne A, Franke MA, Schmid MA, Harris E, Kramer LD. 2017. Rearing of Culex spp. and Aedes spp. mosquitoes. Bio Protoc 7: 1–25. DOI:10.21769/BioProtoc.2542.Rearing.
Lee J, Ryu JS. 2019. Current status of parasite infections in Indonesia: A literature review. Korean Journal of Parasitology 57: 329–339. DOI:10.3347/kjp.2019.57.4.329.
Lee JY, Woo RM, Choi CJ, Shin TY, Gwak WS, Woo SD. 2019. Beauveria bassiana for the simultaneous control of Aedes albopictus and Culex pipiens mosquito adults shows high conidia persistence and productivity. AMB Express 9: 1–9. DOI:10.1186/s13568-019-0933-z.
Leles RN, D’Alessandro WB, Luz C. 2012. Effects of Metarhizium anisopliae conidia mixed with soil against the eggs of Aedes aegypti. Parasitology Research 110: 1579–1582. DOI:10.1007/s00436-011-2666-z.
Lestari YA, Verawaty M, Herlinda S. 2022. Development of Spodoptera frugiperda fed on young maize plant’s fresh leaves inoculated with endophytic fungi from South Sumatra, Indonesia. Biodiversitas 23: 5056–5063. DOI:10.13057/biodiv/d231012.
Lopez DC, Sword GA. 2015. The endophytic fungal entomopathogens Beauveria bassiana and Purpureocillium lilacinum enhance the growth of cultivated cotton (Gossypium hirsutum) and negatively affect survival of the cotton bollworm (Helicoverpa zea). Biological Control 89: 53–60. DOI:10.1016/j.biocontrol.2015.03.010.
Luz C, Mnyone LL, Russell TL. 2011. Survival of anopheline eggs and their susceptibility to infection with Metarhizium anisopliae and Beauveria bassiana under laboratory conditions. Parasitology Research 109: 751–758. DOI:10.1007/s00436-011-2318-3.
Mancillas-Paredes JM, Hernández-Sánchez H, Jaramillo-Flores ME, García-Gutiérrez C. 2019. Proteases and chitinases induced in Beauveria bassiana during infection by Zabrotes subfasciatus. Southwestern Entomol 44: 125–137. DOI:10.3958/059.044.0114.
Mnyone LL, Kirby MJ, Mpingwa MW, Lwetoijera DW, Knols BGJ, Takken W, Koenraadt CJM, Russell TL. 2011. Infection of Anopheles gambiae mosquitoes with entomopathogenic fungi: Effect of host age and blood-feeding status. Parasitology Research 108: 317–322. DOI:10.1007/s00436-010-2064-y.
Nugroho SS, Mujiyono M, Setiyaningsih R, Garjito TA, Ali RSM. 2019. New species checklist and distribution data of Aedes and Verrallina mosquitoes (Diptera: Culicidae) of Indonesia. Vektora 11: 111–120. DOI:10.22435/vk.v11i2.1462.
Nur Athen MH, Nazri CD, Siti Nazrina C. 2020. Bioassay studies on the reaction of Aedes aegypti & Aedes albopictus (Diptera: Culicidae) on different attractants. Saudi Journal of Biological Sciences 27: 2691–2700. DOI:10.1016/j.sjbs.2020.06.016.
Ortiz-Urquiza A, Keyhani NO. 2013. Action on the surface: Entomopathogenic fungi versus the insect cuticle. Insects 4: 357–374. DOI:10.3390/insects4030357.
Peach DAH, Matthews BJ. 2022. The invasive mosquitoes of Canada: An entomological, medical, and veterinary review. American Journal of Tropical Medicine and Hygiene 107: 231–244. DOI:10.4269/ajtmh.21-0167.
Quintero-Zapata I, Flores-González MS, Luna-Santillana EJ, Arroyo-González N, Gandarilla-Pacheco FL. 2022. Late effects of Beauveria bassiana on larval stages of Aedes aegypti Linneo, 1762 (Diptera: Culicidae). Brazilian Journal of Biology 82: 1–8. DOI:10.1590/1519-6984.237789.
Ramayanti I, Herlinda S, Muslim A, Hasyim H. 2022. First report of entomopathogenic fungi from South Sumatra (Indonesia): pathogenicity to egg, larvae, and adult of Culex quinquefasciatus. Biodiversitas 23: 5695–5702. DOI:10.13057/biodiv/d231120.
Ramayanti I, Herlinda S, Muslim A, Hasyim H. 2023. Entomopathogenic fungi from South Sumatra (Indonesia) pathogenicity to egg, larvae, and adult of Aedes aegypti. Hayati Journal of Biosciences 30: 35–47. DOI:10.4308/hjb.30.1.35-47.
Rezza G. 2014. Dengue and Chikungunya: Long-distance spread and outbreaks in naïve areas. Pathogens and Global Health 108: 349–355. DOI:10.1179/2047773214Y.0000000163.
Shoukat RF, Hassan B, Shakeel M, Zafar J, Li S, Freed S, Xu X, Jin F. 2020. Pathogenicity and transgenerational effects of Metarhizium anisopliae on the demographic parameters of Aedes albopictus (Culicidae: Diptera). Journal of Medical Entomology 57: 677–685. DOI:10.1093/jme/tjz236.
Snetselaar J, Andriessen R, Suer RA, Osinga AJ, Knols BG, Farenhorst M. 2014. Development and evaluation of a novel contamination device that targets multiple life-stages of Aedes aegypti. Parasites and Vectors 7: 1–10. DOI:10.1186/1756-3305-7-200.
Suwandi S, Junita A, Suparman S, Umayah A, Hamidson H, Muslim A, Irsan C. 2018. Curative activity of watery fermented compost extract as a bark treatment against tapping panel dryness. The Open Agriculture Journal 12: 74–83. DOI:10.2174/1874331501812010074.
Valero-Jiménez CA, Debets AJM, Van Kan JAL, Schoustra SE, Takken W, Zwaan BJ, Koenraadt CJM. 2014. Natural variation in virulence of the entomopathogenic fungus Beauveria bassiana against malaria mosquitoes. Malaria Journal 13: 1–8. DOI:10.1186/1475-2875-13-479.
Vivekanandhan P, Kavitha T, Karthi S, Senthil-Nathan S, Shivakumar MS. 2018. Toxicity of Beauveria bassiana-28 mycelial extracts on larvae of Culex quinquefasciatus mosquito (Diptera: Culicidae). Int J Environ Res Public Health 15: 1–11. DOI:10.3390/ijerph15030440.
Vivekanandhan P, Swathy K, Murugan AC, Krutmuang P. 2022. Insecticidal efficacy of Metarhizium anisopliae derived chemical constituents against disease?vector mosquitoes. Journal of Fungi 8: 1–12. DOI:10.3390/jof8030300.
Vontas J, Kioulos E, Pavlidi N, Morou E, della Torre A, Ranson H. 2012. Insecticide resistance in the major dengue vectors Aedes albopictus and Aedes aegypti. Pesticide Biochemistry and Physiology 104: 126–131. DOI:10.1016/j.pestbp.2012.05.008.
Wu H-H, Wang C-Y, Teng H-J, Lin C, Lu L-C, Jian S-W, Chang N-T, Wen T-H, Wu J-W, Liu D-P, Lin L-J, Norris DE, Wu H-S. 2013. A dengue vector surveillance by human population-stratified ovitrap survey for Aedes (Diptera: Culicidae) adult and egg collections in high dengue-risk areas of Taiwan. Population and Community Ecology 50: 261–269. DOI:10.1603/ME11263.
Yuliani DM, Hadi UK, Soviana S, Retnani EB. 2021. Habitat characteristic and density of larva Aedes albopictus in Curug, Tangerang District, Banten Province, Indonesia 2018. Biodiversitas 22: 5350–5357. DOI:10.13057/biodiv/d221216.
Most read articles by the same author(s)
- RAHMAT PRATAMA, AHMAD MUSLIM, SUWANDI SUWANDI, SUPARMAN SHK, First report of Ceratocystis fimbriata causing wilt disease of soursop in South Sumatra, Indonesia , Biodiversitas Journal of Biological Diversity: Vol. 24 No. 12 (2023)
- SUWANDI SUWANDI, MONICA ALESIA, RUDI PUTRA MUNANDAR, RAHMAD FADLI, SUPARMAN SUPARMAN, CHANDRA IRSAN, A. MUSLIM, The suppression of Ganoderma boninense on oil palm under mixed planting with taro plants , Biodiversitas Journal of Biological Diversity: Vol. 25 No. 3 (2024)
- YUWINDA AYU LESTARI, MARIESKA VERAWATY, SITI HERLINDA, Development of Spodoptera frugiperda fed on young maize plant’s fresh leaves inoculated with endophytic fungi from South Sumatra, Indonesia , Biodiversitas Journal of Biological Diversity: Vol. 23 No. 10 (2022)
- DETYA ROSA FADDILAH, MARIESKA VERAWATY, SITI HERLINDA, Growth of fall armyworm, Spodoptera frugiperda J.E. Smith (Lepidoptera: Noctuidae) fed on young maize colonized with endophytic fungus Beauveria bassiana from South Sumatra, Indonesia , Biodiversitas Journal of Biological Diversity: Vol. 23 No. 12 (2022)
- ERISE ANGGRAINI, TIYAS SETIAWATI, SITI HERLINDA, CHANDRA IRSAN, MULAWARMAN, NUNI GOFAR, A. MUSLIM, WEI HONG LAU, Identification of the nettle caterpillar in smallholding oil palm plantation cultivated on peatland in Ogan Ilir, South Sumatra, Indonesia , Biodiversitas Journal of Biological Diversity: Vol. 26 No. 1 (2025)
- SITI HERLINDA, MIMMA GUSTIANINGTYAS, SUWANDI SUWANDI, RADIX SUHARJO, JELLY MILINIA PUSPITA SARI, SUPARMAN, HARMAN HAMIDSON, HAMZAH HASYIM, Endophytic fungi from South Sumatra (Indonesia) in seed-treated corn suppressing Spodoptera frugiperda growth , Biodiversitas Journal of Biological Diversity: Vol. 23 No. 11 (2022)
- BENI RAHMAD, NURHAYATI DAMIRI, ZAZILI HANAFIAH, DESSY ADRIANI, LAILA HANUM, Food source diversity and honey production in stingless bee meliponiculture, Ogan Komering Ulu Timur, South Sumatra, Indonesia , Biodiversitas Journal of Biological Diversity: Vol. 25 No. 6 (2024)
- JELLY MILINIA PUSPITA SARI, SITI HERLINDA, SUWANDI SUWANDI, ELFITA, Effect of endophytic entomopathogenic fungal conidia and blastospores induced in maize plants by seed inoculation on Spodoptera frugiperda immune response and mortality , Biodiversitas Journal of Biological Diversity: Vol. 24 No. 10 (2023)
- ERISE ANGGRAINI, TESSIA MASNITA SINAGA, CHANDRA IRSAN, SITI HERLINDA, AHMAD MUSLIM, HARMAN HAMIDSON, MARLIN SEFRILA, ASTUTI KURNIANINGSIH, DESI ARYANI, MIRZA ANTONI, ZAHLUL IKHSAN, Insects found in different ages of coconut viridis variety in Sri Tiga Village, Banyuasin District, South Sumatra, Indonesia , Biodiversitas Journal of Biological Diversity: Vol. 25 No. 8 (2024)