Abstract
Insect herbivores frequently must balance host plant quality and the risk of attack by their natural enemies when making oviposition decisions. Yet, which factor is more important remains unresolved in plant–insect ecology. Here, we report the oviposition preference and larval performance of the brassicaceous specialist Plutella xylostella, in the context of plant quality (cabbage Brassica oleracea vs. mustard B. juncea) and associated natural enemies. Despite the greater larval weight and adult lifespan on cabbage, ovipositing females strongly preferred mustard. Both the egg parasitoid Trichogrammatoidea bactrae and the larval ectoparasitoid Bracon brevicornis are more likely to attack P. xylostella that feed on cabbage; thus, mustard represents enemy-reduced space from these two parasitoids. However, larval diet had no impact on the parasitism rate of specialist Cotesia vestalis. Feeding on mustard improved larval immune responses. The total hemocyte number, diversity, and phenoloxidase activity were higher in mustard-fed larvae which increased their survival against the entomopathogen, Bacillus thuringiensis. Interestingly, host plants altered the larval body odor profile. Mustard-fed larvae emitted allyl isothiocyanate (AITC) and butyl isothiocyanate (BITC) while cabbage-fed larvae emitted dimethyl disulphide (DMDS) and dimethyl trisulphide (DMTS) that served as short-range cues for larval parasitoids. For B. brevicornis, host body odor guided oviposition choice was crucial as their fitness was affected by the host larval diet. Although C. vestalis showed a clear preference towards volatiles emitted by mustard fed larvae, their fitness was unaltered. Taken together, our results illustrate that P. xylostella prefers to lay eggs on mustard plants providing enemy-reduced space from some, but not all, natural enemies.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data Availability Statement
Data are deposited in the Dryad Digital Repository. https://doi.org/10.5061/dryad.fttdz08tk (Ghosh et al. 2021).
References
Aartsma Y, Bianchi FJ, van der Werf W, Poelman EH, Dicke M (2017) Herbivore-induced plant volatiles and tritrophic interactions across spatial scales. New Phytol 216:1054–1063. https://doi.org/10.1111/nph.14475
Badenes-Pérez FR, Shelton AM, Nault BA (2004) Evaluating trap crops for diamondback moth, Plutella xylostella (Lepidoptera: Plutellidae). J Econ Entomol 97:1365–1372. https://doi.org/10.1093/jee/97.4.1365
Bandoly M, Grichnik R, Hilker M, Steppuhn A (2016) Priming of anti-herbivore defence in Nicotiana attenuata by insect oviposition: herbivore-specific effects. Plant Cell Environ 39:848–859. https://doi.org/10.1111/pce.12677
Bartea CM, Casacci LP, Bonelli S, Zampollo S, Barbero F (2020) Chemical, physiological and molecular responses of host plants to lepidopteran egg-laying. Front Plant Sci 10:1768. https://doi.org/10.3389/fpls.2019.01768
Bukovinsky T, Poelman EH, Gols R, Prekatsakis G, Vet LEM, Harvey JA, Dicke M (2009) Consequences of constitutive and induced variation in plant nutritional quality for immune defence of a herbivore against parasitism. Oecologia 160:299–308. https://doi.org/10.1007/s00442-009-1308-y
Charleston DS, Kfir R (2000) The possibility of using Indian mustard, Brassica juncea, as a trap crop for the diamondback moth, Plutella xylostella, in South Africa. J Crop Prot 19:455–460. https://doi.org/10.1016/S0261-2194(00)00037-5
Dicke M (2009) Behavioural and community ecology of plants that cry for help. Plant Cell Environ 32:654–665. https://doi.org/10.1111/j.1365-3040.2008.01913.x
Drezen JM, Bézier A, Burke GR, Strand MR (2022) Bracoviruses, ichnoviruses, and virus-like particles from parasitoid wasps retain many features of their virus ancestors. Curr Opin Insect Sci 49:93–100. https://doi.org/10.1016/j.cois.2021.12.003
Fatouros NE, Lucas-Barbosa D, Weldegergis BT, Pashalidou FG, van Loon JJ, Dicke M (2012) Plant volatiles induced by herbivore egg deposition affect insects of different trophic levels. PLoS One 7:e43607. https://doi.org/10.1371/journal.pone.0043607
Fox LR, Eisenbach J (1992) Contrary choices: possible exploitation of enemy-free space by herbivorous insects in cultivated vs. wild crucifers. Oecologia 89:574–579. https://doi.org/10.1007/BF00317166
Furlong MJ, Shi ZH, Liu SS, Zalucki MP (2004) Evaluation of the impact of natural enemies on Plutella xylostella L. (Lepidoptera: Yponomeutidae) populations on commercial Brassica farms. Agri for Entomol 6:311–322. https://doi.org/10.1111/j.1461-9555.2004.00228.x
Garvey MA, Creighton JC, Kaplan I (2020) Tritrophic interactions reinforce a negative preference-performance relationship in the tobacco hornworm Manduca sexta. Ecol Entomol 45:783–794. https://doi.org/10.1111/een.12852
Gasmi L, Martínez-Solís M, Frattini A, Ye M, Collado MC, Turlings TC, Erb M, Herrero S (2019) Can herbivore-induced volatiles protect plants by increasing the herbivores’ susceptibility to natural pathogens? Appl Environ Microbiol 85:e01468-e1518. https://doi.org/10.1128/AEM.01468-18
Gauld ID, Gaston KJ, Janzen DH (1992) Plant allelochemicals, tritrophic interactions and the anomalous diversity of tropical parasitoids: the “nasty” host hypothesis. Oikos 65:353–357. https://doi.org/10.2307/3545032
Ghosh E, Venkatesan R (2019) Plant volatiles modulate immune responses of Spodoptera litura. J Chem Ecol 45:715–724. https://doi.org/10.1007/s10886-019-01091-3
Ghosh E, Sasidharan A, Ode PJ, Venkatesan R (2021) Oviposition preference is regulated by volatiles, immune status and enemy-free space in Plutella xylostella – parasitoid interaction, Dryad, dataset. https://doi.org/10.5061/dryad.fttdz08tk
Grzywacz D, Rossbach A, Rauf A, Russell DA, Srinivasan R, Shelton AM (2010) Current control methods for diamondback moth and other brassica insect pests and the prospects for improved management with lepidopteran-resistant Bt vegetable brassicas in Asia and Africa. Crop Protect 29:68–79. https://doi.org/10.1016/j.cropro.2009.08.009
Hansen AC, Glassmire AE, Dyer LA, Smilanich AM (2017) Patterns in parasitism frequency explained by diet and immunity. Ecography 40:803–805
Heil M (2008) Indirect defence via tritrophic interactions. New Phytol 178:41–61. https://doi.org/10.1111/j.1469-8137.2007.02330.x
Hilker M, Fatouros NE (2015) Plant responses to insect egg deposition. Annu Rev Entomol 60:493–515. https://doi.org/10.1146/annurev-ento-010814-020620
Hilker M, Fatouros NE (2016) Resisting the onset of herbivore attack: plants perceive and respond to insect eggs. Curr Opin Plant Biol 32:9–16. https://doi.org/10.1016/j.pbi.2016.05.003
Hopkins RJ, van Dam NM, van Loon JJA (2009) Role of glucosinolates in insect-plant relationships and multitrophic interactions. Annu Rev Entomol 54:57–83. https://doi.org/10.1146/annurev.ento.54.110807.090623
Jalali SK, Rabindra RJ, Rao NS, Dasan CB (2003) Mass production of trichogrammatids and chrysopids. Project Directorate of Biological Control, Bangalore, India. pp, 16
Jeffries MJ, Lawton JH (1984) Enemy free space and the structure of ecological communities. Biol J Linn Soc 23:269–286. https://doi.org/10.1111/j.1095-8312.1984.tb00145.x
Kaplan I, Carrillo J, Garvey M, Ode PJ (2016) Indirect plant-parasitoid interactions mediated by changes in herbivore physiology. Curr Opin Insect Sci 14:112–119. https://doi.org/10.1016/j.cois.2016.03.004
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 7:89–95. https://doi.org/10.21608/eajbsa.2014.13138
Klemola N, Klemola T, Rantala MJ, Ruuhola T (2007) Natural host-plant quality affects immune defence of an insect herbivore. Entomol Exp Appl 123:167–176. https://doi.org/10.1111/j.1570-7458.2007.00533.x
Lampert EC, Bowers MD (2015) Incompatibility between plant-derived defensive chemistry and immune response of two sphingid herbivores. J Chem Ecol 41:85–92. https://doi.org/10.1007/s10886-014-0532-z
Lee KP, Cory JS, Wilson K, Raubenheimer D, Simpson SJ (2006) Flexible diet choice offsets protein costs of pathogen resistance in a caterpillar. Proc Roy Soc B 273:823–829. https://doi.org/10.1098/rspb.2005.3385
Li Q, Eigenbrode SD, Stringam GR, Thiagarajah MR (2000) Feeding and growth of Plutella xylostella and Spodoptera eridania on Brassica juncea with varying glucosinolate concentrations and myrosinase activities. J Chem Ecol 26:2401–2419. https://doi.org/10.1023/A:1005535129399
McCormick AC, Unsicker SB, Gershenzon J (2012) The speciality of herbivore induced plant volatiles in attracting herbivore enemies. Trends Plant Sci 17:303–310. https://doi.org/10.1016/j.tplants.2012.03.012
Milonas PG, Anastasaki E, Partsinevelos G (2019) Oviposition-induced volatiles affect electrophysiological and behavioral responses of egg parasitoids. Insects 10:437. https://doi.org/10.3390/insects10120437
Muller K, Vogelweith F, Thiéry D, Moret Y, Moreau J (2015) Immune benefits from alternative host plants could maintain polyphagy in a phytophagous insect. Oecologia 177:467–475. https://doi.org/10.1007/s00442-014-3097-1
Nishida R (2002) Sequestration of defensive substances from plants by Lepidoptera. Annu Rev Entomol 47:57–92. https://doi.org/10.1146/annurev.ento.47.091201.145121
Ode PJ (2006) Plant chemistry and natural enemy fitness: effects on herbivore and natural enemy interactions. Annu Rev Entomol 51:163–185. https://doi.org/10.1146/annurev.ento.51.110104.151110
Ode PJ (2019) Plant toxins and parasitoid trophic ecology. Curr Opin Insect Sci 32:118–123. https://doi.org/10.1016/j.cois.2019.01.007
Ojala K, Julkunen-Tiitto R, Lindström L, Mappes J (2005) Diet affects the immune defence and life-history traits of an arctiid moth Parasemia plantaginis. Evol Ecol Res 7:1153–1170. https://doi.org/10.1002/ece3.7802
Oudenhove L, Mailleret L, Fauvergue X (2017) Infochemical use and dietary specialization in parasitoids: a meta-analysis. Ecol Evol 7:4804–4811. https://doi.org/10.1002/ece3.2888
Pennachio F, Strand MR (2006) Evolution of developmental strategies in parasitic Hymenoptera. Annu Rev Entomol 51:233–258. https://doi.org/10.1146/annurev.ento.51.110104.151029
Petschenka G, Agrawal AA (2016) How herbivores coopt plant defenses: natural selection, specialization, and sequestration. Curr Opin Insect Sci 14:17–24. https://doi.org/10.1016/j.cois.2015.12.004
Randlkofer B, Obermaier E, Hilker M, Meiners T (2010) Vegetation complexity—the influence of plant species diversity and plant structures on plant chemical complexity and arthropods. Basic Appl Ecol 11:383–395. https://doi.org/10.1016/j.baae.2010.03.003
Ratzka A, Vogel H, Kliebenstein DJ, Mitchell-Olds T, Kroymann J (2002) Disarming the mustard oil bomb. PNAS 99:11223–11228. https://doi.org/10.1073/pnas.172112899
Renwick JAA, Haribal M, Gouinguene S, Stadler E (2006) Isothiocyanates stimulating oviposition by the diamondback moth, Plutella xylostella. J Chem Ecol 32:755–766. https://doi.org/10.1007/s10886-006-9036-9
Reudler JH, Biere A, Harvey JA, van Nouhuys S (2011) Differential performance of a specialist and two generalist herbivores and their parasitoids on Plantago lanceolata. J Chem Ecol 37:765–778. https://doi.org/10.1007/s10886-011-9983-7
Sang JP, Minchinton IR, Johnstone PK, Truscott RJW (1984) Glucosinolate profiles in the seed, root and leaf tissue of cabbage, mustard, rapeseed, radish and swede. Can J Plant Sci 64:77–93. https://doi.org/10.4141/cjps84-011
Schoonhoven LM, van Loon JJA, Dicke M (2005) Insect-plant biology, 2nd edn. Oxford University Press, Oxford
Singer MS, Carrière Y, Theuring C, Hartmann T (2004) Disentangling food quality from resistance against parasitoids: diet choice by a generalist caterpillar. Am Nat 164:423–429. https://doi.org/10.1086/423152
Singer MS, Mace KC, Bernays EA (2009) Self-medication as adaptive plasticity: increased ingestion of plant toxins by parasitized caterpillars. PLoS One 4:e4796. https://doi.org/10.1371/journal.pone.0004796
Smilanich AM, Dyer LA, Chambers JQ, Bowers MD (2009) Immunological cost of chemical defence and the evolution of herbivore diet breadth. Ecol Lett 12:612–621. https://doi.org/10.1111/j.1461-0248.2009.01309.x
Smilanich AM, Mason PA, Sprung L, Chase TR, Singer MS (2011) Complex effects of parasitoids on pharmacophagy and diet choice of a polyphagous caterpillar. Oecologia 165:995–1005. https://doi.org/10.1007/s00442-010-1803-1
Srinivasan K, Moorthy PK (1992) Development and adoption of integrated pest management for major pests of cabbage using Indian mustard as a trap crop. In 2nd International Workshop on the Diamondback Moth and other Cruciferous Pests. Asian Vegetable Research and Development Center, Taipei, Taiwan, pp, 511–521.
Stamp N (2001) Enemy-free space via host plant chemistry and dispersion: assessing the influence of tri-trophic interactions. Oecologia 128:153–163. https://doi.org/10.1007/s004420100679
Videla M, Valladares GR, Salvo A (2012) Choosing between good and better: optimal oviposition drives host plant selection when parents and offspring agree on best resources. Oecologia 169:743–751. https://doi.org/10.1007/s00442-011-2231-6
Vinson SB (1976) Host selection by insect parasitoids. Annu Rev Entomol 21:109–133. https://doi.org/10.1146/annurev.en.21.010176.000545
Vogelweith F, Thiéry D, Quaglietti B, Moret Y, Moreau J (2011) Host plant variation plastically impacts different traits of the immune system of a phytophagous insect. Funct Ecol 25:1241–1247. https://doi.org/10.1111/j.1365-2435.2011.01911.x
Yen GC, Wei QK (1993) Myrosinase activity and total glucosinolate content of cruciferous vegetables, and some properties of cabbage myrosinase in Taiwan. J Sci Food Agric 61:471–475. https://doi.org/10.1002/jsfa.2740610415
Zhang PJ, Lu YB, Zalucki MP, Liu SS (2012) Relationship between adult oviposition preference and larval performance of the diamondback moth, Plutella xylostella. J Pest Sci 85:247–252. https://doi.org/10.1007/s10340-012-0425-2
Acknowledgements
The authors thank Dr. Radhika Reddy for her inputs in volatile analysis and Mudrika Singhal for assisting in the study initially. The authors also thank the National Bureau of Agricultural Insect Resources, Bengaluru for providing insects. NCBS central imaging and flow cytometry facility is gratefully acknowledged. This work was supported by grants from the Department of Science and Technology (Early Career Award, Ramanujan Fellowship), Max Planck Society (DST-Max Planck Partner group program) and Department of Biotechnology.
Funding
This work was supported by funds from the Department of Science and Technology (Early Career Award, Ramanujan Fellowship), Max Planck Society (Max Planck Partner group program) and Department of Biotechnology to RV.
Author information
Authors and Affiliations
Contributions
RV and EG conceived the study. RV obtained funding and supervised the project. EG designed and performed the experiments, and EG and PO conducted the statistical analyses. AM performed the volatile analysis and contributed to performance assays. EG, PO, and RV wrote the manuscript with inputs from AM.
Corresponding author
Ethics declarations
Competing Interests
The authors declare no competing interests.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Ghosh, E., Sasidharan, A., Ode, P.J. et al. Oviposition Preference and Performance of a Specialist Herbivore Is Modulated by Natural Enemies, Larval Odors, and Immune Status. J Chem Ecol 48, 670–682 (2022). https://doi.org/10.1007/s10886-022-01363-5
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10886-022-01363-5