Skip to main content
Log in

Efficacy and emergence of parasitic wasps that attack herbivorous insects on maize and its relatives in their region of origin

  • Original Paper
  • Published:
Arthropod-Plant Interactions Aims and scope Submit manuscript

Abstract

Maize (Zea mays subsp. mays), an important cereal crop worldwide, was domesticated directly from the annual teosinte (Zea mays subsp. parviglumis), and teosintes originated from gamagrass (Tripsacum) plants. Some herbivorous insects of maize began their association on Tripsacum; however, little is known about the interaction between these herbivores and their parasitoids in this ancestral Tripsacum habitat. A field experiment was conducted in the Mesoamerican region of origin of maize, using sentinel eggs of the hopper Dalbulus quinquenotatus on Tripsacum dactyloides, and eggs of the insect pest Dalbulus maidis on annual teosinte, landrace maize, and modern maize. A community of egg parasitoids formed by Anagrus naulti (Mymaridae), Paracentrobia sp., and Pseudoligosita sp. (Trichogrammatidae) was found attacking eggs of both species of hoppers on the tested host plants. The largest abundance of parasitoids adult emergence and rate of parasitism was found in D. quinquenotatus eggs laid on T. dactyloides. The rate of parasitism was similar for the other three treatments: D. maidis on teosinte, landrace maize, and modern maize. In the D. quinquenotatus-Tripsacum treatment, D. maidis-annual teosinte treatment, and D. maidis-hybrid maize treatment more Paracentrobia sp. adults emerged than A. naulti adults. These results suggest that the interaction between hoppers and their egg parasitoids occurs on Tripsacum plants, and probably has been in place since before maize domestication.

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

Access this article

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

Data availability

The data sets generated and analysed during the current study are available from the corresponding author on reasonable request.

Code availability

Analysis were performed using SPSS 12.0 software.

References

  • Benrey B, Callejas A, Rios L, Oyama K, Denno RF (1998) The effects of domestication of Brassica and Phaseolus on the interaction between phytophagous insects and parasitoids. Biol Control 11:130–140

    Article  Google Scholar 

  • Campan E, Benrey B (2004) Behavior and performance of a specialist and a generalist parasitoid. Biol Control 30:220–228

    Article  Google Scholar 

  • Chacon-Torres NM (2020) Efecto de las hormigas sobre la asociación de mutualismo entre Dalbulus quinquenotatus (Hemiptera: Cicadellidae) y sus parasitoides de huevos. Dissertation, Universidad de Guadalajara

  • Chen YH, Welter SC (2003) Confused by domestication: Incongruent behavioral responses of the sunflower month, Homoeosama electellum (Lepidoptera: Pyralidae) and its parasitoid, Dolichogenidea homoeosoma (Hymenoptera: Braconidae), toward wild and domesticated sunflowers. Biol Control 28:180–190

    Article  Google Scholar 

  • Chen YH, Welter SC (2005) Crop domestication disrupts a native tritrophic interaction associated with the sunflower, Helianthus annuus (Asterales: Asteracea). Ecol Entomol 30:673–683

    Article  Google Scholar 

  • Chiappini E, Salerno G, Berzolla A, Lacovone A, Reguzzi MC, Conti E (2012) Role of volatile semiochemicals in host location by the egg parasitoid Anagrus breviphragma. Entomol Exp Appl 144:311–316

    Article  CAS  Google Scholar 

  • de Lange ES, Farnier K, Gaudillat B, Turlings TCJ (2016) Comparing the attraction of two parasitoids to herbivore-induced volatiles of maize and its wild ancestors, the teosintes. Chemoecology 26:33–44

    Article  Google Scholar 

  • Fu Z, Yan J, Zheng Y, Warburton ML, Crouch JH, Li J-S (2010) Nucleotide diversity and molecular evolution of the PSY1gene in Zea mays compared to some other grass species. Theor Appl Genet 120:709–720

    Article  CAS  Google Scholar 

  • Gaillard MDP, Glauser G, Robert CAM, Turlings TCJ (2018) Fine-tuning the plant domestication-reduced defense hypothesis: specialist vs generalist herbivores. New Phytol 217:355–366

    Article  CAS  Google Scholar 

  • Garvery M, Creighton C, Kaplan I (2020) Pepper domestication enhances parasitoid recruitment to herbivore-damaged plants. Arthropod Plant Interact 14:695–703

    Article  Google Scholar 

  • Gault CM, Kremling KA, Bucklers ES (2018) Tripsacum de novo transcriptome assemblies reveal parallel gene evolution with maize after ancient polyploidy. Plant Genome 11(3):1–13

    Article  Google Scholar 

  • Gols R, Bukovinszky T, van Dam M, Dicke M, Bullock JM, Harvery JA (2008) Performance of generalist and specialist herbivores and their endoparasitoids differs on cultivated and wild Brassica populations. J Chem Ecol 34:132–143

    Article  CAS  Google Scholar 

  • Heady SE, Nault LR (1984) Leafhopper egg microfilaments (Homoptera: Cicadellidae). Ann Entomol Soc Am 77:610–615

    Article  Google Scholar 

  • Heady SE, Madden LV, Nault LR (1985) Oviposition behavior of Dalbulus leafhoppers (Homoptera: Cicadellidae). Ann Entom Soc Am 78:723–727

    Article  Google Scholar 

  • Larsen KJ, Heady SE, Nault LR (1992) Influence of ants (Hymenoptera: Formicidae) on honeydew excretion and escape behaviors in a myrmecophile, Dalbulus quinquenotatus (Homoptera: Cicadellidae), and its congeners. J Insect Behav 5:109–122

    Article  Google Scholar 

  • Larson SR, Doebley J (1994) Restriction site variation in the chloroplast genome of Tripsacum (Poaceae): Phylogeny and rates of sequence evolution. Syst Bot 19:21–34

    Article  Google Scholar 

  • Li X, Garvey M, Kaplan J, Li B, Carrillo J (2018) Domestication of tomato has reduced the attraction of herbivore natural enemies to pest-damaged plants. Agric For Entomol 20:390–401

    Article  Google Scholar 

  • Matsuoka Y, Vigouroux Y, Goodman MM, Sanchez GJ, Buckler E, Doebley J (2002) A single domestication for maize shown by multilocus microsatellite genotyping. Proc Natl Acad Sci USA 99:6080–6084

    Article  CAS  Google Scholar 

  • Mills N (2010) Egg parasitoids in biological control and integrated pest management. In: Consoli F, Parra J, Zucchi R (eds) Egg parasitoids in agroecosystem with emphasis on Trichogramma, vol 9. Springer, New York, pp 389–411

    Google Scholar 

  • Moya-Raygoza G (2016) Effect of herbivore insect pest age on fecundity and attractiveness to egg parasitoids in maize and its wild relative teosinte. Ann Entomol Soc Am 109:724–729

    Article  Google Scholar 

  • Moya-Raygoza G (2019) Biological control of the leafhopper Dalbulus maidis in corn throughout the Americas: interactions among phytoplasma-insect vector-parasitoids. In: Olivier CY, Dumonceaux TJ, Pérez-López E (eds) Sustainable management of phytoplasma diseases in crops grown in the tropical belts. Sustainability in plant and crop protection, vol 12. Springer, Champ, pp 203–218

  • Moya-Raygoza G, Triapitsyn SV (2015) Egg parasitoids (Hymenoptera: Mymaridae and Trichogrammatidae) of Dalbulus quinquenotatus (Hemiptera: Cicadellidae), with description of a new species of Anagrus (Mymaridae) from Mexico. Ann Entomol Soc Am 108:289–298

    Article  Google Scholar 

  • Mutyambai DM, Bruce TJA, Midega CAO, Woodcock CM, Caulfield JC, Van Den Berg J, Pickett JA, Khan ZR (2015) Responses of parasitoids to volatiles induced by Chilo pertellus oviposition on teosintes, a wild ancestor of maize. J Chem Ecol 41:323–329

    Article  CAS  Google Scholar 

  • Nault LR (1990) Evolution of an insect pest: maize and the corn leafhopper, a case study. Maydica 35:165–175

    Google Scholar 

  • Nault LR, Delong DM (1980) Evidence for co-evolution of leafhoppers in the genus Dalbulus (Cicadellidae: Homoptera) with maize and its ancestors. Ann Entomol Soc Am 73:349–353

    Article  Google Scholar 

  • Pitre HN (1970) Notes on the life history of Dalbulus maidis on gama grass and plant susceptibility to the corn stunt disease agent. J Econ Entomol 63:1661–1662

    Article  Google Scholar 

  • Qi J, Malook S, Shen G, Gao L, Zhang C, Li J, Zhang J, Wang L, Wu J (2018) Current understanding of maize and rice defense against insect herbivores. Plant Divers 40:189–195

    Article  Google Scholar 

  • Ross-Ibarra J, Teneillon M, Gaut BS (2009) Historical divergence and gene flow in the genus Zea. Genetics 181:1399–1413

    Article  CAS  Google Scholar 

  • Rowen E, Kaplan I (2016) Eco-evolutionary factors drive induced plant volatiles: a meta-analysis. New Phytol 210:284–294

    Article  CAS  Google Scholar 

  • Sann C, Theodorou P, Heong KL, Villareal S, Settele J, Vidal S, Westphal C (2018) Hopper parasitoids do not significantly benefit from non-crop habitats in rice production landscapes. Agric Ecosyst Environ 254:224–232

    Article  Google Scholar 

  • Tamiru A, Bruce TJA, Woodcock CM, Caulfield JC, Midega CAO, Ogol CKPO, Mayon P, Birkett MA, Pickett JA, Khan ZR (2011) Maize landraces recruit egg and larval parasitoids in response to egg deposition by a herbivore. Ecol Lett 14:1075–1083

    Article  Google Scholar 

  • Tamiru A, Bruce TJA, Richter A, Woodcock CM, Midega CAO, Degenhardt J, Kelemus S, Pickett JA, Khan ZR (2017) A maize landrace that emits defenses volatiles in response to herbivore eggs possesses a strongly inducible terpene synthase gene. Ecol Evol 7:2835–2845

    Article  Google Scholar 

  • Tena A, Wäckers FL, Heimpel GE, Urbaneja A, Pekas A (2016) Parasitoid nutritional ecology in a community context: the importance of honeydew and implications for biological control. Curr Opin Insect Sci 14:100–104

    Article  Google Scholar 

  • Turlings TCJ, Erb M (2018) Tritrophic interactions mediated by herbivore-induced plant volatiles: mechanisms, ecological relevance, and application potential. Annu Rev Entomol 63:433–452

    Article  CAS  Google Scholar 

  • Virla EG, Coll Araoz MV, Luft Albarracin E (2021) Estimation of direct damage to maize seedlings by the corn leafhopper, Dalbulus maidis (Hemiptera: Cicadellidae), under different watering regimes. B Entomol Res. https://doi.org/10.1017/S0007485321000079

    Article  Google Scholar 

  • Wäckers FL, van Rijn PCJ, Heimpel GE (2008) Honeydew as a food source for natural enemies: making the best of a bad meal? Biol Control 45:176–184

    Article  Google Scholar 

  • Weiss MR (2006) Defecation behavior and ecology of insects. Ann Rev Entomol 51:635–661

    Article  CAS  Google Scholar 

Download references

Acknowledgments

I thank Dr. Claudia S. Copeland (Cape Diem Biomedical Writing and Editing) for editing the manuscript.

Funding

No funding was received for conducting this study.

Author information

Authors and Affiliations

Authors

Contributions

GMR: conceived, designed and executed this study and wrote the manuscript. No other person is entitled to authorship.

Corresponding author

Correspondence to Gustavo Moya-Raygoza.

Ethics declarations

Conflict of interest

The author GMR declares that he has no conflicts of interest.

Consent for publication

The author GMR is consent for publication.

Ethical approval

This article does not contains any studies with animals (vertebrates) performed by the author.

Additional information

Handling Editor: Miriama Malcicka.

Publisher's Note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Moya-Raygoza, G. Efficacy and emergence of parasitic wasps that attack herbivorous insects on maize and its relatives in their region of origin. Arthropod-Plant Interactions 15, 409–415 (2021). https://doi.org/10.1007/s11829-021-09818-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11829-021-09818-4

Keywords

Navigation