Skip to main content
SpringerLink
Log in

Impact of Plant Symbiotic Endophytic Fungus, Aspergillus terreus on Insect Herbivore Spodoptera litura (Fabricius) (Lepidoptera: Noctuidae)

  • Biological Control
  • Published:
Neotropical Entomology Aims and scope Submit manuscript

Abstract

Herbivorous insects are known to be resistant to fungal endophytes that asymptomatically inhabit plant tissues. The insecticidal ability of the endophytic fungus Aspergillus terreus isolated from Catharanthus roseus against Spodoptera litura (Fabricius) was assessed in the current study. The survival and growth of S. litura were adversely impacted by the ethyl acetate extract of endophytic A. terreus. Fungal extract supplemented diet caused 14 to 94% larval mortality in comparison to 2% in control. Additionally, retarded insect growth was observed after ingestion of supplemented diet. The fungal metabolites were also observed to have an inhibitory influence on the adult emergence and reproductive potential of adults. Phytochemical analysis revealed the presence of phenolic compounds in the crude extract of endophytic fungus which may be responsible for toxicity. It was also determined how endophyte-infected cauliflower plants affected S. litura’s survival and growth. Endophyte-infected plants exhibited resistance to S. litura by causing 54% larval mortality and delaying development by 5.2 days. In comparison to uninfected plants, adult emergence, lifespan, fecundity and egg hatchability of insects was significantly decreased on infected plants. There was a significant decrease in relative growth and consumption rates as well as in the efficiency of food conversion, which indicates toxic and antifeedant effect of the fungus on S. litura. This suggests that endophyte-inoculated plants exhibit antibiosis against S. litura. In conclusion, the endophytic fungi having insecticidal activity could be used to develop alternative ecologically safe control strategies.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Data Availability

All data generated and or analyzed during this study are included in this published artilcle.

References

  • Afkhami ME, Rudgers JA (2009) Endophyte-mediated resistance to herbivores depends on herbivore identity in the wild grass Festuca subverticillata. Environ Entomol 38(4):1086–1095

    Article  PubMed  Google Scholar 

  • Alves APC, Corrêa AD, Alves DS, Saczk AA, Lino JB, Carvalho GA (2014) Toxicity of the phenolic extract from jabuticabeira (Myrciaria cauliflora (Mart.) O. Berg) fruit skins on Spodoptera frugiperda. Chil J Agric Res 74(2):200–204

    Article  Google Scholar 

  • Arunthirumeni M, Vinitha G, Shivakumar MS (2023) Antifeedant and larvicidal activity of bioactive compounds isolated from entomopathogenic fungi Penicillium sp. for the control of agricultural and medically important insect pest (Spodoptera litura and Culex quinquefasciatus). Parasitol Int 92:102688

    Article  CAS  PubMed  Google Scholar 

  • Azevedo JL, Maccheroni W Jr, Pereira JO, De Araújo WL (2000) Endophytic microorganisms: a review on insect control and recent advances on tropical plants. Electron J Biotechnol 3(1):15–16

    Article  Google Scholar 

  • Babu SR, Dudwal R, Mahla MK (2018) Field efficacy of newer insecticides against tobacco caterpillar, Spodoptera litura (F.) on soybean. Indian J Entomol 80(3):912–917

    Article  Google Scholar 

  • Ball OJP, Coudron TA, Tapper BA, Davies E, Trently D, Bush LP, Popay AJ (2006) Importance of host plant species, Neotyphodium endophyte isolate, and alkaloids on feeding by Spodoptera frugiperda (Lepidoptera: Noctuidae) larvae. J Econ Entomol 99(4):1462–1473

    Article  CAS  PubMed  Google Scholar 

  • Castillo MA, Moya P, Hernández E, Primo-Yufera E (2000) Susceptibility of Ceratitis capitata Wiedemann (Diptera: Tephritidae) to entomopathogenic fungi and their extracts. Biol Control 19(3):274–282

    Article  Google Scholar 

  • Clement SL, Elberson LR, Bosque-Perez NA, Schotzko DJ (2005) Detrimental and neutral effects of wild barley–Neotyphodium fungal endophyte associations on insect survival. Entomol Exp Appl 114(2):119–125

    Article  Google Scholar 

  • Delvas N, Bauce É, Labbé C, Ollevier T, Bélanger R (2011) Phenolic compounds that confer resistance to spruce budworm. Entomol Exp Appl 141(1):35–44

    Article  CAS  Google Scholar 

  • Edriss AE, Satti AA, Alabjar ZA (2012) Preliminary studies on phytochemicals and larvicidal effects of Acacia nilotica L. extracts against Anopheles arabiensis Patton. Sci Res Essays 7(50):4253–4258

    Google Scholar 

  • Elango D, Manikandan V, Jayanthi P, Velmurugan P, Balamuralikrishnan B, Ravi AV, Shivakumar MS (2020) Selection and characterization of extracellular enzyme production by an endophytic fungi Aspergillus sojae and its bio-efficacy analysis against cotton leaf worm, Spodoptera Litura. Curr Plant Biol 23:100153

    Article  Google Scholar 

  • El-Sayed AS, Moustafa AH, Hussein HA, El-Sheikh AA, El-Shafey SN, Fathy NA, Enan GA (2020) Potential insecticidal activity of Sarocladium strictum, an endophyte of Cynanchum acutum, against Spodoptera littoralis, a polyphagous insect pest. Biocatal Agric Biotechnol 24:101524

    Article  Google Scholar 

  • Flonc B, Barbercheck M, Ahmad I (2021) Observations on the relationships between endophytic Metarhizium robertsii, Spodoptera frugiperda (Lepidoptera: Noctuidae), and maize. Pathogens 10(6):713

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gange AC, Eschen R, Wearn JA, Thawer A, Sutton BC (2012) Differential effects of foliar endophytic fungi on insect herbivores attacking a herbaceous plant. Oecologia 168:1023–1031

    Article  PubMed  Google Scholar 

  • Golla SK, Rajasekhar P, Akbar SM, Sharma HC (2018) Proteolytic activity in the midgut of Helicoverpa armigera (Noctuidae: Lepidoptera) larvae fed on wild relatives of chickpea, Cicer arietinum. J Econ Entomol 111(5):2409–2415

    Article  CAS  PubMed  Google Scholar 

  • Gonthier DJ, Sullivan TJ, Brown KL, Wurtzel B, Lawal R, VandenOever K, Bultman TL (2008) Stroma-forming endophyte Epichloë glyceriae provides wound-inducible herbivore resistance to its grass host. Oikos 117(4):629–633

    Article  Google Scholar 

  • Guo Z, Gai C, Cai C, Chen L, Liu S, Zeng Y, Dai H (2017) Metabolites with insecticidal activity from Aspergillus fumigatus JRJ111048 isolated from mangrove plant Acrostichum specioum endemic to Hainan Island. Mar Drugs 15(12):381

    Article  PubMed  PubMed Central  Google Scholar 

  • Hammon KE, Faeth SH (1993) Ecology of plant-herbivore communities: a fungal component? J Nat Toxins 1(3):197–208

    Article  Google Scholar 

  • Hartley SE, Gange AC (2009) Impacts of plant symbiotic fungi on insect herbivores: mutualism in a multitrophic context. Annu Rev Entomol 54:323–342

    Article  CAS  PubMed  Google Scholar 

  • Ioannidis P, Buer B, Ilias A, Kaforou S, Aivaliotis M, Orfanoudaki G, Denecke S (2022) A spatiotemporal atlas of the lepidopteran pest Helicoverpa armigera midgut provides insights into nutrient processing and pH regulation. BMC Genom 23(1):1–12

    Article  Google Scholar 

  • Jallow MF, Dugassa-Gobena D, Vidal S (2004) Indirect interaction between an unspecialized endophytic fungus and a polyphagous moth. Basic and Applied Ecology 5(2):183–191

    Article  Google Scholar 

  • Jallow MF, Dugassa-Gobena D, Vidal S (2008) Influence of an endophytic fungus on host plant selection by a polyphagous moth via volatile spectrum changes. Arthropod-Plant Interact 2:53–62

    Article  Google Scholar 

  • Karthi S, Vaideki K, Shivakumar MS, Ponsankar A, Thanigaivel A, Chellappandian M, Senthil-Nathan S (2018) Effect of Aspergillus flavus on the mortality and activity of antioxidant enzymes of Spodoptera litura Fab. (Lepidoptera: Noctuidae) larvae. Pestic Biochem Phys 149:54–60

    Article  CAS  Google Scholar 

  • Kaur HP, Singh B, Kaur A, Kaur S (2013) Antifeedent and toxic activity of endophytic Alternaria alternata against tobacco caterpillar Spodoptera litura. J Pest Sci 86:543–550

    Article  Google Scholar 

  • Kaur M, Chadha P, Kaur S, Kaur A, Kaur R, Yadav AK, Kaur R (2018) Schizophyllum commune induced genotoxic and cytotoxic effects in Spodoptera litura. Sci Rep 8(1):4693

    Article  PubMed  PubMed Central  Google Scholar 

  • Kaur T, Kaur J, Kaur A, Kaur S (2016) Larvicidal and growth inhibitory effects of endophytic Aspergillus niger on a polyphagous pest, Spodoptera litura. Phytoparasitica 44:465–476

    Article  Google Scholar 

  • Kaur T (2020) Fungal endophyte-host plant interactions: role in sustainable agriculture. Sustainable Crop Production 211

  • Kaur T, Singh B, Kaur A, Kaur S (2015) Endophyte-mediated interactions between cauliflower, the herbivore Spodoptera litura, and the ectoparasitoid Bracon hebetor. Oecologia 179:487–494

    Article  PubMed  Google Scholar 

  • Kebede D, Alemu T, Tefera T (2022) Endophytic potential and larvicidal efficacy of entomopathogenic fungi against the spotted stem borer, chilo partellus. Psyche: A Journal of Entomology 2022

  • Khan AL, Hamayun M, Kang SM (2012) Endophytic fungal association via gibberellins and indole acetic acid can improve plant growth potential in abiotic stress: an example of Paecilomyces formosus LHL10. BMC Microbiol 12:3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    Article  CAS  PubMed  Google Scholar 

  • Koul O, Shankar JS, Mehta N, Taneja SC, Tripathi AK, Dhar KL (1997) Bioefficacy of crude extracts of Aglaia species (Meliaceae) and some active fractions against lepidopteran larvae. J Appl Entomol 121(1–5):245–248

    Article  Google Scholar 

  • Kumar A, Purohit AK (2020) Biological control and need of a strategic shift in plant disease management. Plant Defence: Biological Control 119-133

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33(7):1870–1874

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Larone MT (2002) Medically important fungi. A guide to identification 4:270–274

    Google Scholar 

  • 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 Journal of Biological Diversity 23(10)

  • Mantzoukas S, Grammatikopoulos G (2020) The effect of three entomopathogenic endophytes of the sweet sorghum on the growth and feeding performance of its pest, Sesamia nonagrioides larvae, and their efficacy under field conditions. J Crop Prot 127:104952

    Article  CAS  Google Scholar 

  • Marques TR, Caetano AA, Alves DS, Ramos VDO, Simao AA, Carvalho GA, Correa AD (2016) Malpighia emarginata DC. bagasse acetone extract: Phenolic compounds and their effect on Spodoptera frugiperda (JE Smith)(Lepidoptera: Noctuidae). Chil J Agric Res 76(1):55–61

    Article  Google Scholar 

  • Martinez SS, Van Emden HF (2001) Growth disruption, abnormalities and mortality of Spodoptera littoralis (Boisduval) (Lepidoptera: Noctuidae) caused by azadirachtin. Neotrop Entomol 30:113–125

    Article  CAS  Google Scholar 

  • Maxmen A (2013) Crop pests: under attack. Nature 501(7468):S15–S17

    Article  CAS  PubMed  Google Scholar 

  • Mayur B, Sandesh S, Shruti S, Sung-Yum S (2010) Antioxidant and α-glucosidase inhibitory properties of Carpesium abrotanoides L. J Med Plants Res 4(15):1547–1553

    Google Scholar 

  • Mousavi SS, Karami A (2022) Application of Endophyte microbes for production of secondary metabolites. Appl Environ Microbiol 1–37

  • Nathan SS (2006) Effects of Melia azedarach on nutritional physiology and enzyme activities of the rice leaffolder Cnaphalocrocis medinalis (Guenée) (Lepidoptera: Pyralidae). Pestic Biochem Phys 84(2):98–108

    Article  CAS  Google Scholar 

  • Nathan SS, Chung PG, Murugan K (2005) Effect of biopesticides applied separately or together on nutritional indices of the rice leaffolder Cnaphalocrocis medinalis. Phytoparasitica 33:187–195

    Article  Google Scholar 

  • Nathan SS, Kalaivani K (2005) Efficacy of nucleopolyhedrovirus and azadirachtin on Spodoptera litura Fabricius (Lepidoptera: Noctuidae). Biol Control 34(1):93–98

    Article  CAS  Google Scholar 

  • Ouaba J, Tchuinkam T, Waïmane A, Magara HJO, Niassy S, Meutchieye F (2022) Lepidopterans of economic importance in Cameroon: A systematic review. J Agric Food Res 8:100286

    Google Scholar 

  • Raps A, Vidal S (1998) Indirect effects of an unspecialized endophytic fungus on specialized plant–herbivorous insect interactions. Oecologia 114:541–547

    Article  CAS  PubMed  Google Scholar 

  • Russo ML, Jaber LR, Scorsetti AC, Vianna F, Cabello MN, Pelizza SA (2021) Effect of entomopathogenic fungi introduced as corn endophytes on the development, reproduction, and food preference of the invasive fall armyworm Spodoptera frugiperda. J Pest Sci 94:859–870

    Article  CAS  Google Scholar 

  • Russo ML, Scorsetti AC, Vianna MF, Allegrucci N, Ferreri NA, Cabello MN, Pelizza SA (2019) Effects of endophytic Beauveria bassiana (Ascomycota: Hypocreales) on biological, reproductive parameters and food preference of the soybean pest Helicoverpa gelotopoeon. Journal of King Saud University-Science 31(4):1077–1082

    Article  Google Scholar 

  • Senthilkumar N, Murugesan S, Babu DS (2014) Metabolite profiling of the extracts of endophytic fungi of entomopathogenic significance, Aspergillus flavus and Nigrospora sphaerica isolated from tropical tree species of India, Tectona grandis L. J Agric Life Sci 1(1)

  • Senthil-Nathan S (2013) Physiological and biochemical effect of neem and other Meliaceae plants secondary metabolites against Lepidopteran insects. Front Physiol 4:359

    Article  PubMed  PubMed Central  Google Scholar 

  • Sharma M, Chadha BS, Kaur M, Ghatora SK, Saini HS (2008) Molecular characterization of multiple xylanase producing thermophilic/thermotolerant fungi isolated from composting materials. Lett Appl Microbiol 46(5):526–535

    Article  CAS  PubMed  Google Scholar 

  • Shymanovich T, Faeth SH (2018) Anti-insect defenses of Achnatherum robustum (sleepygrass) provided by two Epichloë endophyte species. Entomol Exp Appl 166(6):474–482

    Article  CAS  Google Scholar 

  • Singh B, Dhaliwal RS, Kumar P, Singh A (2021) Insecticidal activity of a proteinaceous α-glycosidase inhibitor isolated from an endophytic Aspergillus awamori and its biosafety evaluation. Physiol Mol Plant Pathol 116:101707

    Article  CAS  Google Scholar 

  • Singh B, Kaur T, Kaur S, Manhas RK, Kaur A (2016) Insecticidal potential of an endophytic Cladosporium velox against Spodoptera litura mediated through inhibition of alpha glycosidases. Pestic Biochem Physiol 131:46–52

    Article  CAS  PubMed  Google Scholar 

  • Singh B, Thakur A, Kaur S, Chadha BS, Kaur A (2012) Acetylcholinesterase inhibitory potential and insecticidal activity of an endophytic Alternaria sp. from Ricinus communis. Appl Biochem Biotechnol 168:991–1002

    Article  CAS  PubMed  Google Scholar 

  • Sinha KK, Choudhary AK, Kumari P (2016) Entomopathogenic fungi. Ecofriendly pest management for food security. Academic Press, pp 475–505

    Chapter  Google Scholar 

  • Strobel G, Daisy B (2003) Bioprospecting for microbial endophytes and their natural products. Microbiol Mol Biol Rev 67(4):491–502

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tan RX, Zou WX (2001) Endophytes: a rich source of functional metabolites. Nat Prod Rep 18(4):448–459

    Article  CAS  PubMed  Google Scholar 

  • Thakur A, Kaur S, Kaur A, Singh V (2012) Detrimental effects of endophytic fungus Nigrospora sp. on survival and development of Spodoptera litura. Biocontrol Sci Technol 22(2):151–161

    Article  Google Scholar 

  • Thakur A, Kaur S, Kaur A, Singh V (2013a) Enhanced resistance to Spodoptera litura in endophyte infected cauliflower plants. Environ Entomol 42(2):240–246

    Article  PubMed  Google Scholar 

  • Thakur A, Singh V, Kaur A, Kaur S (2013b) Insecticidal potential of an endophytic fungus, Cladosporium uredinicola, against Spodoptera litura. Phytoparasitica 41:373–382

    Article  Google Scholar 

  • Tintjer T, Rudgers JA (2006) Grass–herbivore interactions altered by strains of a native endophyte. New Phytol 170(3):513–521

    Article  PubMed  Google Scholar 

  • Tong H, Su Q, Zhou X, Bai L (2013) Field resistance of Spodoptera litura (Lepidoptera: Noctuidae) to organophosphates, pyrethroids, carbamates and four newer chemistry insecticides in Hunan, China. J Pest Sci 86:599–609

    Article  Google Scholar 

  • van Lenteren JC, Bolckmans K, Köhl J, Ravensberg WJ, Urbaneja A (2018) Biological control using invertebrates and microorganisms: plenty of new opportunities. Biocontrol 63:39–59

    Article  Google Scholar 

  • Waksmundzka-Hajnos M, Sherma J, Kowalska T (2008) Thin layer chromatography in phytochemistry. CRC Press

    Book  Google Scholar 

  • Wu J, Li J, Zhang C, Yu X, Cuthbertson AG, Ali S (2020) Biological impact and enzyme activities of Spodoptera litura (Lepidoptera: Noctuidae) in response to synergistic action of matrine and Beauveria brongniartii. Front Physiol 11:584405

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang BC (1994) Index of economically important Lepidoptera. Cab International

    Google Scholar 

Download references

Funding

Financial assistance received from University Grants Commission (UGC), New Delhi, India [F. No. – 43–568/2014(SR)], is duly acknowledged.

Author information

Authors and Affiliations

  1. Department of Zoology, Guru Nanak Dev University, Amritsar, Punjab, India

    Surbjit Singh & Sanehdeep Kaur

  2. Department of Microbiology, Guru Nanak Dev University, Amritsar, Punjab, India

    Rajvir Kaur & Amarjeet Kaur

Authors
  1. Surbjit Singh
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sanehdeep Kaur
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rajvir Kaur
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Amarjeet Kaur
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

SS, AK and SK conceived and designed the experiments, SS performed the experiments. AK helps in the identification of fungus. The data obtained was analyzed by SS, AK and SK. SS wrote the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Sanehdeep Kaur.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Additional information

Edited by Khalid Haddi

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Singh, S., Kaur, S., Kaur, R. et al. Impact of Plant Symbiotic Endophytic Fungus, Aspergillus terreus on Insect Herbivore Spodoptera litura (Fabricius) (Lepidoptera: Noctuidae). Neotrop Entomol 52, 932–944 (2023). https://doi.org/10.1007/s13744-023-01070-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13744-023-01070-0

Keywords

Search

Navigation