Abstract
Successful pest management using parasitoids requires careful evaluation of host-parasitoid interactions. Here, we report the performance of larval ecto-parasitoid wasp, Bracon brevicornis (Wesmael) on important agricultural pests, Spodoptera litura (Fabricius) and S. frugiperda (J.E. Smith). Biology of B. brevicornis was studied on different host instars under laboratory and cage setup. In no-choice assay, the parasitoid development was highest on fifth-instar S. litura larvae as the wasp laid ~ 253 eggs with 62% hatching, 76% pupae formation and 78% adult emergence. Similarly, these parameters were highest on fifth instar S. frugiperda larvae (293 eggs, 57% hatching, 80% pupae formation, 70% adult emergence). In two-choice assay, B. brevicornis preferred fourth or fifth over third instar larvae of both hosts. Successful parasitism depends on host paralysis and suppression of host immunity. B. brevicornis interaction downregulated cellular immunity of both hosts as shown by reduced hemocyte viability and spreading. The percent parasitism rate of B. brevicornis was unaltered in the presence of host plant, Zea mays in cage study. 76 and 84% parasitism was observed on fifth-instar larvae of S. litura and S. frugiperda, respectively. We evaluated the performance of B. brevicornis as a biocontrol agent on S. frugiperda in maize field. Our results show 54% average reduction in infestation after release of B. brevicornis. Taken together, we report the performance of B. brevicornis on important insect pests for the first time in laboratory and field conditions. Our findings indicate that B. brevicornis is a promising candidate for integrated pest management.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Bakr RF, Gesraha MA, Guneidy NA, Farag NA, Ebeid AR, Elbehery HH, Abou-Ellail M (2014) Biological studies on Bracon brevicornis (Hymenoptera: Braconidae) reared on different host larvae. Egypt Acad J Biol Sci 7(2):89–95. https://doi.org/10.21608/eajbsa.2014.13138
Brodeur J, Vet LEM (1995) Relationships between parasitoid and host range and host defense: a comparative study of egg encapsulation in two related parasitoid species. Physiol Entomol 20:7–12. https://doi.org/10.1111/j.1365-3032.1995.tb00794.x
Brown ES, Dewhurst CF (1975) The genus Spodoptera (Lepidoptera, Noctuidae) in Africa and the Near East. Bull Entomol Res 65(2):221–262. https://doi.org/10.1017/S0007485300005939
Charnov EL, Skinner SW (1985) Complementary approaches to the understanding of parasitoid oviposition decisions. Environ Entomol 14:383–391. https://doi.org/10.1093/ee/14.4.383
Cheng T, Wu J, Wu Y, Chilukuri RV, Huang L, Yamamoto K, Feng L, Li W, Chen Z, Guo H, Liu J, Li S, Wang X, Peng L, Liu D, Guo Y, Fu B, Li Z, Liu C, Chen Y, Tomar A, Hilliou F, Montagné N, Jacquin-Joly E, d’Alençon E, Seth RK, Bhatnagar RK, Jouraku A, Shiotsuki T, Kadono-Okuda K, Promboon A, Smagghe G, Arunkumar KP, Kishino H, Goldsmith MR, Feng Q, Xia Q, Mita K (2017) Genomic adaptation to polyphagy and insecticides in a major East Asian noctuid pest. Nat Ecol Evol 1:1747–1756. https://doi.org/10.1038/s41559-017-0314-4
Day R, Abrahams P, Bateman M, Beale T, Clottey V, Cock M, Colmenarez Y, Corniani N, Early R, Godwin J, GomezJ MPG, Murphy ST, Oppong-Mensah B, Phiri N, Pratt C, Silvestri S, Witt A (2017) Fall Armyworm: impacts and implications for Africa. Outlooks Pest Manag 28:196–201. https://doi.org/10.1564/v28_oct_02
Dhir BCM, Mohapatra HK, Senapathi B (1992) Assessment of crop loss in groundnut due to tobacco caterpillar, Spodoptera litura (F.). Indian J Plant Prot 20:215–217
Feltwell J (1982) Large white butterfly: the biology, biochemistry and physiology of P. brassicae (L.). W. Junk, The Hague, p 273
Firake DM, Behere GT (2020) Natural mortality of invasive fall armyworm, Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae) in maize agroecosystems of North-East India. Biol Control 148:104303–104310. https://doi.org/10.1016/j.biocontrol.2020.104303
Ghosh E, Venkatesan R (2019) Plant volatiles modulate immune responses of Spodoptera litura. J Chem Ecol 45(8):715–724. https://doi.org/10.1007/s10886-019-01091-3
Girling RD, Stewart-Jones A, Dherbecourt J, Staley JT, Wright DJ, Poppy GM (2011) Parasitoids select plants more heavily infested with their caterpillar hosts: a new approach to aid interpretation of plant headspace volatiles. Proc Biol Sci 278:2646–2653. https://doi.org/10.1098/rspb.2010.2725
Godfray HCJ (1994) Parasitoids: behavior and evolutionary ecology. Princeton University Press, Princeton
Goergen G, Kumar PL, Sankung SB, Togola A, Tamo M (2016) First report of outbreaks of the fall armyworm Spodoptera frugiperda (J E Smith) (Lepidoptera, Noctuidae), a new alien invasive pest in West and Central Africa. PLoS ONE 11:e0165632. https://doi.org/10.1371/journal.pone.0165632
Gols R, Bukovinszky T, van Dam NM, Dicke M, Bullock JM, Harvey JA (2008) Performance of generalist and specialist herbivores and their endoparasitoids differs on cultivated and wild Brassica populations. J Chem Ecol 34:132–143. https://doi.org/10.1007/s10886-008-9429-z
Gupta A, Soujanya PL, VAN Achterberg C, Sekhar JC (2020) Coccygidium transcaspicum (Kokujev) (Hymenoptera: Braconidae) parasitizing larvae of invasive pest Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae) in India. Zootaxa. 4750(2). https://doi.org/10.11646/zootaxa.4750.2.13
Jervis MA, Ellers J, Harvey JA (2007) Resource acquisition, allocation, and utilization in parasitoid reproductive strategies. Annu Rev Entomol 53:361–385. https://doi.org/10.1146/annurev.ento.53.103106.093433
Kant R, Minor MA, Trewick SA (2012) Fitness gain in a koinobiont parasitoid Diaeretiella rapae (Hymenoptera: Aphidiidae) by parasitising hosts of different ages. J Asia Pac Entomol 15:83–87. https://doi.org/10.1016/j.aspen.2011.08.011
Kares EA, Ebaid GH, El-Sappagh IA (2009) Biological studies on the larval parasitoid species Bracon brevicornis Wesm. (Hymenoptera: Braconidae), reared on different insect hosts. Egypt J Biol Pest Control 19:165–168. https://doi.org/10.21608/eajbsa.2014.13138
Kenis M, Du Plessis H, Van den Berg J, Ba MN, Goergen G, Kwadjo KE, Baoua I, Tefera T, Buddie A, Cafà G, Offord L (2019) Telenomus remus, a candidate parasitoid for the biological control of Spodoptera frugiperda in Africa, is already present on the continent. Insects 10:92. https://doi.org/10.3390/insects10040092
Khan MAZ, Liang QF, Maria MSM, Liu TX (2016) Effect of temperature on functional response of Aphidius gifuensis (Hymenoptera: Braconidae) parasitizing Myzus persicae (Hemiptera: Aphididae). Florida Entomol 99:696–702. https://doi.org/10.1653/024.099.0419
Kugimiya S, Shimoda T, Tabata J, Takabayashi J (2010) Present or past herbivory: a screening of volatiles released from Brassica rapa under caterpillar attacks as attractants for the solitary parasitoid, Cotesia vestalis. J Chem Ecol 36:620–628. https://doi.org/10.1007/s10886-010-9802-6
Li J, Coudron TA, Pan W, Liu X, Lu Z, Zhang Q (2006) Host age preference of Microplitis mediator (Hymenoptera: Braconidae), an endoparasitoid of Mythimna separata (Lepidoptera: Noctuidae). Biol Control 39:257–261. https://doi.org/10.1016/j.biocontrol.2006.09.002
Li XW, Niu YQ, Liu TX (2014) The performance of Oomyzus sokolowskii (Hymenoptera: Eulophidae) parasitizing Plutella xylostella (Lepidoptera: Plutellidae) on different host plants. Appl Entomol Zool 49:67–75. https://doi.org/10.1007/s13355-013-0225-z
Malesios GA, Prophetou-Athanasiadou DA (2014) Development of the parasitoid Bracon brevicornis on different larval instars (L2–L5) of the Indian meal moth Plodia interpunctella. Entomol Hell 23:59–64. https://doi.org/10.12681/eh.11537
Mattiacci L, Dicke M (1995) Host searching behaviour of Cotesia glomerata, a larval parasitoid of Pieris brassicae: Infochemical use in the selection of the most profitable caterpillar instars. Entomol Exp Appl 76:39–50. https://doi.org/10.1007/BF01995321
Natikar PK, Balikai RA (2015) Screening of different varieties of soybean for their ovipositional preference to Spodoptera litura (Fabricius) under field conditions. J Exp Zool India 18(2):975–977
Pan MZ, Wang L, Zhang CY, Zhang LX, Liu TX (2017) The influence of feeding and host deprivation on egg load and reproduction of an aphid parasitoid, Aphidius gifuensis (Hymenoptera: Braconidae). Appl Entomol Zool 52:255–263. https://doi.org/10.1007/s13355-016-0474-8
Pogue MG (2002) A world revision of the genus Spodoptera Guenee (Lepidoptera: Noctuidae). Mem Am Entomol Soc 43:1–202
Prasanna BM, Huesing JE, Regina Eddy R, Peschke VM (2018) Fall Armyworm in Africa: a guide for integrated pest management. vii, México. CIMMYT, USAID
Qian C, Liu Y, Fang Q, Min-Li Y, Liu SS, Ye GY, Li YM (2013) Venom of the ectoparasitoid, Nasonia vitripennis, influences gene expression in Musca domestica hemocytes. Arch Insect Biochem Physiol 83(4):211–231. https://doi.org/10.1002/arch.21107
Quicke DLJ (2015) The braconid and ichneumonid parasitoid wasps: biology, systematics, evolution and ecology. Wiley, Oxford
R Development Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Rao NBC, Nischala A, Ramanandam G, Maheswarappa HG (2018) Biological suppression of coconut black headed caterpillar Opisina arenosella outbreak in East Godavari district of Andhra Pradesh-eco friendly technology. Curr Sci 115(8):1588–1594. https://doi.org/10.18520/cs/v1151i8/1588-1594
Sarfraz M, Dosdall LM, Keddie BA (2009) Host plant nutritional quality affects the performance of the parasitoid Diadegma insulare. Biol Control 51:34–41. https://doi.org/10.1016/j.biocontrol.2009.07.004
Scholler M, Flinn PW, Grieshop MJ, Zdarkova E (2006) Biological control of stored product pests. In: Heaps JW (ed) Insect management for food storage and processing, 2nd edn. AACC International, St. Paul, pp 67–87
Sharanabasappa KCM, Asokan R, MahadevaSwamy HM, Maruti MS, Pavithra HB, Hegde K, Navi S, Prabhu ST, Georgen G (2018) First report of the Fall armyworm, Spodoptera frugiperda (J E Smith) (Lepidoptera: Noctuidae), an alien invasive pest on maize in India. Pest Mana Hortic Ecosyst 24:23–29
Shylesha AN, Jalali SK, Gupta A, Varshney R, Venkatesan T, Shetty P, Ojha R, Ganiger PC, Navik O, Subaharan K, Bakthavatsalam N, Ballal CR (2018) Studies on new invasive pest Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae) and its natural enemies. J Biol Control 32(3):1–7. https://doi.org/10.18311/jbc/2018/21707
Sisay B, Simiyu J, Malusi P, Likhayo P, Mendesil E, Elibariki N, Wakgiri M, Ayalew G, Tefera T (2018) First report of fall armyworm, Spodoptera frugiperda (Lepidoptera:Noctuidae), natural enemies from Africa. J Appl Entomol 142(8):800–804. https://doi.org/10.1111/jen.12534
Srinivasan T, Chandrikamohan (2017) Population growth potential of Bracon brevicornis Wesmael (Braconidae: Hymenoptera): A life table analysis. Acta Phytopathol Entomol Hung 52:123–129. https://doi.org/10.1556/038.52.2017.010
Stoepler TM, Lill JT, Murphy SM (2011) Cascading effects of host size and host plant species on parasitoid resource allocation. Ecol Entomol 36:724–735. https://doi.org/10.1111/j.1365-2311.2011.01322.x
Suby SB, Soujanya PL, Yadava P, Patil J, Subaharan K, Prasad GS, Babu KS, Jat SL, Yathish KR, Vadassery J, Kalia VK, Bakthavatsalam N, Shekhar JC, Rakshit S (2020) Invasion of fall armyworm (Spodoptera frugiperda) in India: nature, distribution, management and potential impact. Curr Sci 119(1):44–51. https://doi.org/10.18520/cs/v119/i1/44-51
Temerak SA (1984) Suitability of five lepidopteran host insects to the ectolarval parasitoid, Bracon brevicornis Wesmael. Z Angew Entomol 97:210–213. https://doi.org/10.1111/j.1439-0418.1984.tb03739.x
Teng ZW, Xu G, Gan SY, Chen X, Fang Q, Ye GY (2016) Effects of the endoparasitoid Cotesia chilonis (Hymenoptera: Braconidae) parasitism, venom, and calyx fluid on cellular and humoral immunity of its host Chilo suppressalis (Lepidoptera: Crambidae) larvae. J Insect Physiol 85:46–56. https://doi.org/10.1016/j.jinsphys.2015.11.014
Weis AE, Abrahamson WG (1985) Potential selective pressures by parasitoids on a plant-herbivore interaction. Ecology 66:1261–1269. https://doi.org/10.2307/1939179
Wiedenmann RN, Smith JW, Darnell PO (1992) Laboratory rearing and biology of the parasite Cotesia flavipes (Hymenoptera: Braconidae) using Diatraea saccharalis (Lepidoptera: Pyralidae) as a host. Environ Entomol 21:1160–1167. https://doi.org/10.1093/ee/21.5.1160
Yang L, Wan B, Wang B-B, Liu M-M, Fang Q, Song Q-S, Ye G-Y (2019) The Pupal Ectoparasitoid Pachycrepoideus vindemmiae regulates cellular and humoral immunity of host DROSOPHILA melanogaster. Front Physiol 10:1282. https://doi.org/10.3389/fphys.2019.01282
Acknowledgments
Funding from NCBS, Max Planck Gesellschaft (Partner Group Program), DBT-NER grant and Ramanujan Fellowship is acknowledged. The authors thank Indian Council of Agricultural Research, New Delhi, for research support and Dr. Sane lab, NCBS, for parasitoid behavior recording. The authors thank TNAU for initial culture of B. brevicornis. The authors acknowledge Dr. kavitha Isvaran, IISc and Pankaj Kumar Chauhan for their input in statistical analysis.
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by Blas Lavandero.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Ghosh, E., Varshney, R. & Venkatesan, R. Performance of larval parasitoid, Bracon brevicornis on two Spodoptera hosts: implication in bio-control of Spodoptera frugiperda. J Pest Sci 95, 435–446 (2022). https://doi.org/10.1007/s10340-021-01385-0
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10340-021-01385-0