Indiscriminate ingestion of entomopathogenic nematodes and their symbiotic bacteria by Aedes aegypti larvae: a novel strategy to control the vector of Chikungunya, dengue and yellow fever

Indiscriminate ingestion of entomopathogenic nematodes and their symbiotic bacteria by Aedes aegypti larvae: a novel strategy to control the vector of Chikungunya, dengue and yellow fever

Abstract: Third and fourth instar larvae of Aedes aegypti actively ingested entomopathogenic nematodes (EPNs) and their symbiotic bacteria, resulting in larval mortality. All six EPN species evaluated in this study were pathogenic to Ae. aegypti but varied significantly in their virulence. Heterorhabditis bacteriophora and Steinernema carpocapsae were most virulent, H. megidis and S. kraussei showed the least virulence, whereas H. downesi and S. feltiae had intermediate virulence. Larval mortality was dose dependent for all EPN species. When using a dose of 100 infective juveniles (IJs) per larva, H. bacteriophora and S. carpocapsae caused 90%–100% mortality, whereas H. downesi and S. feltiae caused only 40%–60% mortality. Even when using 200 IJs/larva, H. megidis and S. kraussei caused a maximum of 30%–40% mortality. Some of the invasive EPNs were melanized, suggesting a strong humoral defense response by the Aedes larvae. The degree of melanization was quite variable; some EPNs were totally enveloped in a melanin sheath while others were partially coated with melanin. Melanization did not stop the EPN from multiplying and killing the Aedes larvae. IJs released from infected larvae would have the potential to infect healthy mosquito larvae. Also, both bacterial supernatant and bacterial cell suspension of Xenorhabdus nematophila caused >91% larval mortality after 48 h, whereas only the bacterial cell suspension of Photorhabdus laumondii was effective against the mosquito larvae. These data provides useful information on the potential use of EPNs and/or formulated bacterial cell suspensions in the control of the important urban and container-breeding mosquito, Ae. aegypti, and are a starting point for future simulated and actual field studies.Key words: Entomopathogenic nematode (EPN) ingestion, Aedes aegypti, symbiotic bacteria, H. bacteriophora, S. carpocapsae

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  • Alkhaibari AM, Carolino AT, Yavasoglu SI, Maffeis T, Mattoso TC et al. (2016). Metarhizium brunneum blastospore pathogenesis in Aedes aegypti larvae: attack on several fronts accelerates Mortality. PLoS Pathogens 12 (7): e1005715.
  • Boemare N (2002). Biology, Taxonomy, and Systematics of Photorhabdus and Xenorhabdus. In: Gaugler I (editor). Entomopathogenic Nematology. CABI Publishing. New Jersey. pp 57-78.
  • Bowen D, Rocheleau TA, Blackburn M, Andreev O, Golubeva E et al. (1998). Insecticidal toxins from the bacterium Photorhabdus luminescens. Science 280: 2129-2132.
  • Cagnolo SR, Almirón WL (2017). Capacity of the terrestrial entomopathogenic nematode Steinernema rarum (Rhabditida: Steinernematidae) to parasite Culex apicinus larvae (Diptera: Culicidae). Revista de la Sociedad Entomológica Argentina 69: 1-2.
  • Chadee DD (2004). Key premises, a guide to Aedes aegypti (Diptera: Culicidae) surveillance and control. Bulletin of Entomological Research 94: 201-207.
  • Chaudhary MZ, Majeed S, Tayyib M, Javed N, Farzand A et al. (2017). Antagonistic potential of Steinernema kraussei and Heterorhabditis bacteriophora against dengue fever mosquito Aedes aegypti. Journal of Entomology and Zoology Studies 5 (5): 865-869.
  • da Silva OS, Prado GR, da Silva JLR, Silva CE, da Costa M, et al. (2013). Oral toxicity of Photorhabdus luminescens and Xenorhabdus nematophila (Enterobacteriaceae) against Aedes aegypti (Diptera: Culicidae). Parasitology research 112(8): 2891-2896. de Oliveira Cardosoa D, Gomesa VM, Dolinskia C, Souzaa RM (2015). Potential of entomopathogenic nematodes as biocontrol agents of immature stages of Aedes aegypti. Nematoda 2: pe092015.
  • Dilipkumar A, Ramalingam KR, Chinnaperumal K, Govindasamy B, Paramasivam D, et al. (2018). Isolation and growth inhibition potential of entomopathogenic nematodes against three public health important mosquito vectors. Experimental Parasitology 197: 76-84.
  • Edmunds C, Wilding CS, Rae R (2020). Pathogenicity and environmental tolerance of commercial and UK native entomopathogenic nematodes (Steinernema and Heterorhabditis spp.) to the larvae of mosquitoes (Aedes aegypti and Ochlerotatus detritus). International Journal of Pest Management 1-9.
  • Forst S, Dowds B, Boemare N, Stackebrandt E (1997). Xenorhabdus and Photorhabdus spp.: bugs that kill bugs. Annual Review of Microbiology 51: 47-72.
  • Georgis R, Koppenhofer AM, Lacey LA, Berlair G, Duncan LW et al. (2006). Successes and failures in the use of parasitic nematodes for pest control. Biological Control 38: 103-123.
  • Goodrich-Blair H, Clarke DJ (2007). Mutualism and pathogenesis in Xenorhabdus and Photorhabdus: two roads to the same destination. Molecular Microbiology 64: 260-268.
  • Gubler DJ, Clark GG (1994). Community-based integrated control of Aedes aegypti: a brief overview of current programs. American Journal of Tropical Medicine and Hygiene 50: 50-60.
  • Gubler DJ (2002). Epidemic dengue/dengue hemorrhagic fever as a public health, social and economic problem in the 21st century. Trends in Microbiology 10: 100-03.
  • Guzman MG (2005). Deciphering dengue: The Cuban experience. Science. 309: 1495-1497.
  • Hazir S, Shapiro-Ilan DI, Bock CH, Hazir C, Leite LG et al. (2016). Relative potency of culture supernatants of Xenorhabdus and Photorhabdus spp. on growth of some fungal phytopathogens. European Journal of Plant Pathology 146: 369-381.
  • Higgs S (2006). The 2005–2006 Chikungunya epidemic in the Indian Ocean. Vector-Borne and Zoonotic Diseases 6: 115-116.
  • Hominick WM (2002). Biogeography. In: Gaugler, R. (Ed.). Entomopathogenic Nematology. Wallingford, UK: CABI Publishing. pp. 115-143.
  • Kaya HK, Stock SP (1997). Techniques in insect nematology. In: Lacey LA (editor). Manual of Techniques Insect Pathology. Academic Press, London, UK. pp. 281-324.
  • Kim HG, Alston DG (2008). Potential of Two Entomopathogenic Nematodes for Suppression of Plum Curculio (Conotrachelus nenuphar, Coleoptera: Curculionidae) Life Stages in Northern Climates. Environmental Entomology 37: 1272-1279.
  • Liu WT, Chen TL, Hou RF, Chen CC, Tu WC (2020). The invasion and encapsulation of the entomopathogenic nematode, steinernema abbasi, in Aedes albopictus (Diptera: Culicidae) larvae. Insects 11(12): 832.
  • MacKenzie JS, Gubler DJ, Petersen LR (2004). Emerging flaviviruses: the spread and resurgence of Japanese encephalitis, West Nile, and dengue viruses. Nature Medicine 10: 98-107.
  • Molta NB, Hominick WM (1989). Dose and time response assessments of Heterorhabditis heliothidis and Steinernema feltiae (Nem.: Rhabditida) against Aedes aegypti larvae. Entomophaga 34: 485-493.
  • Monath TP (2005). Yellow fever vaccine. Expert Review of Vaccines 4: 553-574.
  • Nappi AJ, Vass E (2001). Cytotoxic reactions associated with insect immunity. Advances in Experimental Medicine and Biology 484: 329-348.
  • Owuama CI (2001). Entomopathogenic symbiotic bacteria, Xenorhabdus and Photorhabdus of nematodes. World Journal of Microbiology and Biotechnology 17: 505-515.
  • Patil PB, Gorman KJ, Dasgupta SK, Reddy KV, Barwale SR et al. (2018). Self-limiting OX513A Aedes aegypti demonstrate full susceptibility to currently used insecticidal chemistries as compared to Indian wild-type Aedes aegypti. Psyche 2018.
  • Peschiutta ML, Cagnolo SR, Almirón WR (2014). Susceptibility of larvae of Aedes aegypti (Linnaeus) (Diptera: Culicidae) to entomopathogenic nematode Heterorhabditis bacteriophora (Poinar) (Rhabditida: Heterorhabditidae). Revista de la Sociedad Entomológica Argentina 73 (3-4): 99-108.
  • Peters A, Ehlers R-U (1997). Encapsulation of the entomopathogenic nematode Steinernema feltiae in Tipula oleracea. Journal of Invertebrate Pathology 69: 218-222.
  • Phong TV, Nam VS (1999). Key breeding sites of dengue vectors in Hanoi, Vietnam, 1994-1997. Dengue Bulletin. 23.
  • Poinar GO Jr, Kaul HN (1982). Parasitism of the mosquito Culex pipiens by the nematode Heterorhabditis bacteriophora Journal of Invertebrate Pathology 39: 382-387.
  • Power KT, An R, Grewal PS (2009). Effectiveness of Heterohabditis bacteriophora strain GPS11 applications targeted against different instars of the Japanese beetle Popillia japonica. Biological Control 48: 232-236.
  • Reiter P, Nathan MB (2001). Guidelines for assessing the efficacy of insecticidal space sprays for control of the dengue vector Aedes aegypti. In: World Health Organization, document WHO/CDS/ CPE/PVC/2001.1, Geneva, Switzerland.
  • Rodri´guez MM, Bisset JA, Ferna´ndez D (2007). Levels of insecticide resistance and resistance mechanisms in Aedes aegypti from some Latin American countries. Journal of American Mosquito Control Association 23: 420-429.
  • Shapiro-Ilan D, Hazir S, Glazer I (2020). Advances in use of entomopathogenic nematodes in IPM. In Kogan M, Higley L, (eds.). Integrated management of insect pests: current and future developments. Burleigh Dodds Science Publishing.
  • Shapiro-Ilan DI, Hazir S, Glazer I (2017). Basic and Applied Research: Entomopathogenic Nematodes. In: Lacey LA (editor). Microbial Control of Insect and Mite Pests, From Theory to Practice. Academic Press, San Diego, USA.
  • Scholte EJ., Takken W, Knols BG (2007). Infection of adult Aedes aegypti and Ae. albopictus mosquitoes with the entomopathogenic fungus Metarhizium anisopliae. Acta Tropica 102: 151-158.
  • Silva HHG, Silva IG, Lira KS (1999). Adaptação do Aedes aegypti em criadouros artificiais com água poluída. do Aedes aegypti em criadouros artificiais com água poluída. Entomologia Vectos 6: 383-389.
  • Toksoz S, Saruhan I (2018). Efficacy of entomopathogenic nematode isolates from Turkey and Kyrgyzstan against the larvae of the mosquito species Culex pipiens L. (Diptera: Culicidae) under laboratory conditions. Egyptian Journal of Biological Pest Control 28 (1): 1-5.
  • Vitta A, Thimpoo P, Meesil W, Yimthin T, Fukruksa C et al. (2018). Larvicidal activity of Xenorhabdus and Photorhabdus bacteria against Aedes aegypti and Aedes albopictus. Asian Pacific Journal of Tropical Biomedicine 8 (1): 31.
  • Walgate R (1994). Biological control of vectors. In: Walgate, R. (Editor). Tropical disease research: progress 1975-94; highlights 1993-94. Twelfth programme report of the UNDP/World Bank/WHO Special Programme for Research and Training in Tropical Diseases (TDR). WHO Publishers. pp 151.
  • Wang Y, Campbell JF, Gaugler R (1995). Infection of entomopathogenic nematode Steinernema glaseri and Heterorhabditis bacteriophora against Popillia japonica (Coleoptera: Scarabaeidae) larvae. Journal of Invertebrate Pathology 66: 178-184.
  • Wagutu GK, Mwangi W, Waturu CN (2017). Entomopathogenic bacteria: Xenorhabdus spp and Photorhabdus spp from Steinernema karii and Heterorhabditis indica for the control of mosquito larvae. Journal of Agriculture, Science and Technology 18 (2): 21-38.
  • Welch HE, Bronskill JF (1962). Parasitism of mosquito larvae by the nematode DD-136 (Nematodea: Neoplectanidae). Canadian Journal of Zoology 40: 1263-1268.
  • World Health Organization, (2009). Dengue and dengue haemorrhagic fever, Fact sheet Nº 117. WHO Media Centre.
  • World Health Organization (2021), Dengue and the severe dengue.
  • Zheng Z, Zhan J, Chen L, Chen H, Cheng S (2021). Global, regional, and national dengue burden from 1990 to 2017: A systematic analysis based on the global burden of disease study 2017. EClinicalMedicine 32: 100712.
Turkish Journal of Zoology-Cover
  • ISSN: 1300-0179
  • Yayın Aralığı: Yılda 6 Sayı
  • Yayıncı: TÜBİTAK
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