Abstract
Interspecific interactions (e.g., competition, predation) are core determinants of insect population evolution, geographical distribution, trophic dynamics and ecosystem functioning. Following its recent invasion of eastern Asia, the fall armyworm, Spodoptera frugiperda (Lepidoptera: Noctuidae) co-inhabits maize fields with native lepidopteran herbivores, such as the common cutworm, Spodoptera litura. Here, drawing upon laboratory and field studies, we demonstrate how late-instar S. frugiperda larvae directly prey upon S. litura immature stages and competitively displace them from the maize whorl. Individual maize plants did not mediate the above interactions, with herbivore-damaged leaves not affecting the development rate of either species. In the field, ecological niches of S. frugiperda and S. litura overlapped, with species-specific occupancy rates of whorl-stage leaves (vegetative phase) and ears or tassels (reproductive phase) exceeding 70% and 90%, respectively. Field cage trials showed that S. frugiperda larvae either preyed upon or repelled S. litura larvae from maize plants, routinely resulting in more than 90% mortality of the latter. Field visits and cage studies in Yunnan (SW China) also revealed how—within an approx. 1-year time period—S. frugiperda has become a dominant species in local maize fields and co-infestation of both herbivores on the same plant is rare. Overall, our work shows how the invasive S. frugiperda exhibits a clear competitive advantage over native lepidopterans and could replace certain species within local agroecosystems. This study not only unveils the mechanistic causes of rapid ecological shifts within S. frugiperda-invaded cropping systems, but may also guide subsequent monitoring and management interventions.
Similar content being viewed by others
References
Allison SD, Vitousek PM (2004) Rapid nutrient cycling in leaf litter from invasive plants in Hawai’i. Oecologia 141:612–619. https://doi.org/10.1007/s00442-004-1679-z
Andow DA, Farias JR, Horikoshi RJ, Bernardi D, Nascimento AR, Omoto C (2015) Dynamics of cannibalism in equal-aged cohorts of Spodoptera frugiperda. Ecol Entomol 40:229–236. https://doi.org/10.1111/een.12178
Bascompte J, Stouffer DB (2009) The assembly and disassembly of ecological networks. Philos Trans R Soc Lond B Biol Sci 364:1781–1787. https://doi.org/10.1098/rstb.2008.0226
Bentivenha JPF, Baldin ELL, Hunt TE, Paula-Moraes SV, Blankenship EE (2016) Intraguild competition of three noctuid maize pests. Environ Entomol 45:999–1008. https://doi.org/10.1093/ee/nvw068
Bentivenha JPF, Baldin ELL, Montezano DG, Hunt TE, Paula-Moraes SV (2017) Attack and defense movements involved in the interaction ofSpodoptera frugiperdaand Helicoverpa zea (Lepidoptera: Noctuidae). J Pest Sci 90:433–445. https://doi.org/10.1007/s10340.016.0802
Bentivenha JPF, Montezano DG, Hunt TE, Baldin EL, Peterson JA (2017) Intraguild interactions and behavior of Spodoptera frugiperda and Helicoverpa spp. on maize. Pest Manage Sci 73:2244–2251. https://doi.org/10.1002/ps.4595
Bradshaw CJ, Leroy B, Bellard C, Roiz D, Albert C, Fournier A, Barbet-Massin M, Salles JM, Simard F, Courchamp F (2016) Massive yet grossly underestimated global costs of invasive insects. Nat commun 7:1–8. https://doi.org/10.1038/ncomms12986
Buntin GD (1986) A review of plant response to fall armyworm, Spodoptera frugiperda (J. E. Smith), injury in selected field and forage crops. Fla Entomol 69:549–559. https://doi.org/10.2307/3495389
Burkness EC, Dively GP, Patton T, Morey AC, Hutchison WD (2010) Novel Vip3A Bacillus thuringiensis (Bt) maize approaches high dose efficacy against Helicoverpa zea (Lepidoptera: Noctuidae) under field conditions: implications for resistance management. GM Crops 1:337–343. https://doi.org/10.4161/gmcr.1.5.14765
CABI (2016) Spodoptera frugiperda (fall armyworm). CAB International, Wallingford
Chapman JW, Williams T, Escribano A, Primitivo C, Cave RD, Dave G (1999) Fitness consequences of cannibalism in the fall armyworm, Spodoptera frugiperda. Behav Ecol 10:298–303. https://doi.org/10.1093/beheco/10.3.298
Chapman JW, Williams T, Martínez AM, Cisneros J, Caballero P, Cave RD, Goulson D (2000) Does cannibalism in Spodoptera frugiperda (Lepidoptera: Noctuidae) reduce the risk of predation? Behav Ecol Sociobiol 48:321–327. https://doi.org/10.1007/s002650000237
Chen Q, Duan Y, Hou YH, Chen L, Fan ZY (2020) Morphological characteristics of Spodoptera frugiperda in comparison with three other common Noctuidae species at maize filling stage. Plant Prot 46:34–41. https://doi.org/10.16688/j.zwbh.2019509
Chu D, Pan HP, Guo D, Tao YL, Liu BM, Zhang YJ (2012) Ecological processes and mechanisms of invasion of the alien whitefly Bemisia tabaci biotype Q in China. Acta Entomol Sin 55:1399–1405. https://doi.org/10.16380/j.kcxb.2012.12.010
Courchamp F, Fournier A, Bellard C, Bertelsmeier C, Bonnaud E, Jeschke JM, Russell JC (2017) Invasion biology: specific problems and possible solutions. Trends Ecol Evol 32:13–22. https://doi.org/10.1016/j.tree.2016.11.001
Crowder DW, Snyder WE (2010) Eating their way to the top? Mechanisms underlying the success of invasive insect generalist predators. Biol Invasions 12:2857–2876. https://doi.org/10.1023/A:1001712500451
De Lange ES, Laplanche D, Guo H, Xu W, Turlings TCJ (2020) Spodoptera frugiperda caterpillars suppress herbivore-induced volatile emissions in maize. J Chem Ecol 46:344–360. https://doi.org/10.1007/s10886-020-01153-x
Denno RF, Mcclure MS, Ott JR (1995) Interspecific interactions in phytophagous insects: competition reexamined and resurrected. Annu Rev Entomol 40:297–331. https://doi.org/10.1146/annurev.en.40.010195.001501
Díaz S, Settele J, Brondízio E, Ngo H, Guèze M, Agard J, Arneth A, Balvanera P, Brauman K, Butchart S, Chan K (2019) Summary for policymakers of the global assessment report on biodiversity and ecosystem services of the intergovernmental science-policy platform on biodiversity and ecosystem services. Popul Dev Rev 45:665–686. https://doi.org/10.1111/padr.12283
Ding J, Mack RN, Lu P, Ren M, Huang H (2008) China’s booming economy is sparking and accelerating biological invasions. Bioscience 58:317–324. https://doi.org/10.1641/B580407
Durrett R, Levin S (1998) Spatial aspects of interspecific competition. Theor Popul Biol 53:30–43. https://doi.org/10.1006/tpbi.1997.1338
Ekesi S, Billah MK, Nderitu PW (2009) Evidence for competitive displacement of Ceratitis cosyra by the invasive fruit fly Bactrocera invadens (Diptera: Tephritidae) on mango and mechanisms contributing to the displacement. J Econ Entomol 102:981–991. https://doi.org/10.1603/029.102.0317
Feng HQ, Wu XF, Wu B, Wu KM (2009) Seasonal migration of Helicoverpa armigera (Lepidoptera: Noctuidae) over the Bohai Sea. J Econ Entomol 102:95–104. https://doi.org/10.1603/029.102.0114
Ferlian O, Eisenhauer N, Aguirrebengoa M, Camara M, Ramirez-Rojas I, Santos F, Tanalgo K, Thakur MP (2018) Invasive earthworms erode soil biodiversity: a meta - analysis. J Anim Eco 87:162–172. https://doi.org/10.1111/1365-2656.12746
Fischer MJ, Havill NP, Brewster CC, Davis GA, Salom SM, Kok LT (2015) Field assessment of hybridization between Laricobius nigrinus and L. rubidus, predators of Adelgidae. Biol Control 82:1–6. https://doi.org/10.1016/j.biocontrol.2014.12.002
Frost CM, Peralta G, Rand TA, Didham RK, Varsani A, Tylianakis JM (2016) Apparent competition drives community-wide parasitism rates and changes in host abundance across ecosystem boundaries. Nat Commun 7:1–12. https://doi.org/10.1038/ncomms12644
Giga DP, Canheo JC Sr (1993) Competition between Prostephanus truncatus (Horn) and Sitophilus zeamais (Motsch.) in maize at two temperatures. J Stored Prod Res 29:63–70. https://doi.org/10.1016/0022-474X(93)90023-W
Glauser G, Marti G, Villard N, Doyen GA, Wolfender JL, Turlings TCJ, Erb M (2011) Induction and detoxification of maize 1,4-benzoxazin-3-ones by insect herbivores. Plant J 68:901–911. https://doi.org/10.1111/j.1365-313X.2011.04740.x
Goergen G, Kumar PL, Sankung SB, Togola A, Tamò M (2016) First report of outbreaks of the fall armyworm Spodoptera frugiperda (JE 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
Gordy JW, Leonard BR, Blouin D, Davis JA, Stout MJ (2015) Comparative effectiveness of potential elicitors of plant resistance against Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae) in four crop plants. PLoS ONE 10:e0136689. https://doi.org/10.1371/journal.pone.0136689
Guo J, Jing D, Tai H, Zhang A, He K, Wang Z (2019) Morphological characteristics of Spodoptera frugiperdain comparison with three other lepidopteran species with similar injury characteristics and morphology in cornfields. Plant Prot 45:7–12. https://doi.org/10.16688/j.zwbh.2019080
He LM, Ge SS, Chen YC, Wu QL, Jiang YY, Wu KM (2019) The developmental threshold temperature, effective accumulated temperature and prediction model of developmental duration of fall armyworm, Spodoptera frugiperda. Plant Prot 45:18–26. https://doi.org/10.16688/j.zwbh.2019409
Holt RD, Bonsall MB (2017) Apparent competition. Annu Rev Ecol Evol Syst 48:447–471. https://doi.org/10.1016/B978-0-12-809633-8.12264-2
Hurlbert SH (1978) The measurement of niche overlap and some relatives. Ecology 59:67–77. https://doi.org/10.2307/1936632
Jiang Y, Liu J, Xie MC, Li YH, Yang JJ, Zhang ML, Qiu K (2019) Observation on law of diffusion damage of Spodoptera frugiperda in China in 2019. Plant Prot 45:10–19. https://doi.org/10.16688/j.zwbh.2019539
Jonsson M, Wratten SD, Landis DA, Tompkins JML, Cullen R (2010) Habitat manipulation to mitigate the impacts of invasive arthropod pests. Biol Invasions 12:2933–2945. https://doi.org/10.1007/s10530-010-9737-4
Kenis M, Auger-Rozenberg MA, Roques A, Timms L, Péré C, Cock MJ, Settele J, Augustin S, Lopez-Vaamonde C (2009) Ecological effects of invasive alien insects. Biol Invasions 11:21–45. https://doi.org/10.1007/s10530-008-9318-y
Krebs CJ (2014) Ecological Methodology, 3rd ed (in preparation). https://www.zoology.ubc.ca/~krebs/books.html
Lach L (2005) Interference and exploitation competition of three nectar-thieving invasive ant species. Insect Soc 52:257–262. https://doi.org/10.1007/s00040-005-0807-z
Li WJ, Wang L, Jaworski CC, Yang F, Liu B, Jiang YY, Lu YH, Wu KM, Desneux N (2020) The outbreaks of nontarget mirid bugs promote arthropod pest suppression in Bt cotton agroecosystems. Plant Biotechnol J 18:322–324. https://doi.org/10.1111/pbi.13233
Liu SS, De Barro PJ, Xu J, Luan JB, Zang LS, Ruan YM, Wan FH (2007) Asymmetric mating interactions drive widespread invasion and displacement in a whitefly. Science 318:1769–1772. https://doi.org/10.1126/science.1149887
Liu B, Yang L, Yang Y, Lu Y (2016) Influence of landscape diversity and composition on the parasitism of cotton bollworm eggs in maize. PLoS ONE 11:e0149476. https://doi.org/10.1371/journal.pone.0149476
Lu YH, Liang GM (2016) Research advance on the succession of insect pest complex in Bt crop ecosystem. Plant Prot 42:7–11. https://doi.org/10.3969/j.issn.0529-1542.2016.01.002
Lu Y, Wu K, Jiang Y, Guo Y, Desneux N (2012) Widespread adoption of Bt cotton and insecticide decrease promotes biocontrol services. Nature 487:362–365. https://doi.org/10.1038/nature11153
Luginbill P (1928) The fall armyworm. USDA Technol Bull 34:91. https://doi.org/10.1007/s00467-004-1436-x
Ma J, Lin JT, Chen HJ, Hu XN (2009) The potential role of interspecific competition in fruit fly invasions. J Environ Entomol 31:361–364. https://doi.org/10.3969/j.issn1674-0858.2009.04.011
May RM (1975) Some notes on estimating the competition matrix. Ecology 56:737–741. https://doi.org/10.2307/1935511
Michael R, Turlings TCJ (2008) Induction of systemic acquired resistance in Zea mays also enhances the plant’s attractiveness to parasitoids. Biol Control 46:178–186. https://doi.org/10.1016/j.biocontrol.2008.04.012
Montezano DG, Specht A, Sosa-Gòmez DR, Roque-Specht VF, Sousa-Silva JC, Paula-Moraes SV, Peterson JA, Hunt TE (2018) Host plants of Spodoptera frugiperda (Lepidoptera: Noctuidae) in the Americas. Afr Entomol 26:286–301. https://doi.org/10.4001/003.026.0286
Nielsen RL (2019) Determining corn leaf stages. Purdue University. https://www.agry.purdue.edu/ext/corn/news/timeless/VStageMethods.html
Nuessly GS, Hartstack AW, Witz JA, Sterling WL (1991) Dislodgement of Heliothis zea (Lepidoptera: Noctuidae) eggs from cotton due to rain and wind: a predictive model. Ecol Model 55:89–102. https://doi.org/10.1016/0304-3800(91)90067-B
Paini DR, Sheppard AW, Cook DC, De Barro PJ, Worner SP, Thomas MB (2016) Global threat to agriculture from invasive species. Proc Natl Acad Sci USA 113:7575–7579. https://doi.org/10.1073/pnas.1602205113
Qin HG, Wang DD, Ding J, Huang RH, Ye ZX (2006) Host plants of Spodoptera litura. Acta Agric Jiangxi 5:51–58. https://doi.org/10.19386/j.cnki.jxnyxb.2006.05.017
Ray S, Alves P, Ahmad I, Gaffoor I (2016) Turnabout is fair play: herbivory-induced plant chitinases excreted in fall armyworm frass suppress herbivore defenses in maize. Plant Physiol 171:694–706. https://doi.org/10.1104/pp.15.01854
Schoener TW (1983) Field experiments on interspecific competition. Am Nat 122:240–285. https://doi.org/10.1086/284133
Sharanabasappa D, Kalleshwaraswamy CM, Asokan R, Swamy HM, Maruthi MS, Pavithra HB, Hegbe K, Navi S, Prabhu ST, Goergen GE (2018) First report of the fall armyworm, Spodoptera frugiperda (JE Smith) (Lepidoptera: Noctuidae) an alien invasive pest on maize in India. Pest Manag Hortic Ecosyst 24:23–29
Shi BC, Lu H, Gong YJ, Wei SJ, Kang ZJ (2009) The identification and prevention of Spodoptera litura. China Veg 19:18–19. https://doi.org/10.19386/j.cnki.jxnyxb.2006.05.017
Silva RBD, Corrêa AS, Della Lucia TMC, Pereira AIA, Cruz I, Zanuncio JC (2012) Does the aggressiveness of the prey modify the attack behavior of the predator Supputius cincticeps (Stål) (Hemiptera, Pentatomidae)? Rev Bras Entomol 56:244–248. https://doi.org/10.1590/S0085-56262012005000031
Søgaard Jørgensen P, Aktipis CA, Brown Z, Carriere Y (2018) Antibiotic and pesticide susceptibility and the Anthropocene operating space. Nat Sustain 1:632–641. https://doi.org/10.1038/s41893-018-0164-3
Sokame BM, Subramanian S, Kilalo DC, Juma G, Paul-André C (2020) Larval dispersal of the invasive fall armyworm, Spodoptera frugiperda, the exotic stemborer Chilo partellus, and indigenous maize stemborers in Africa. Entomol Exp Appl 168:323–331. https://doi.org/10.1111/eea.12899
Sparks AN (1979) A review of the biology of the fall armyworm. Fla Entomol 62(2):82–87. https://doi.org/10.2307/3494083
Stout MJ, Riggio MR, Yang Y (2009) Direct induced resistance in Oryza sativa to Spodoptera frugiperda. Environ Entomol 38:1174–1181. https://doi.org/10.1603/022.038.0426
Sun X, Hu C, Jia H, Wu Q, Shen X, Zhao S, Jiang Y, Wu K (2019) Case study on the first immigration of fall armyworm Spodoptera frugiperda invading into China. J Integr Agric 18:2–10. https://doi.org/10.1016/S2095-3119(19)62839-X
Tu YG, Wu KM, Xue FS, Lu YH (2010) Laboratory evaluation of flight activity of the common cutworm, Spodoptera litura (Lepidoptera: Noctuidae). Insect Sci 17:53–59. https://doi.org/10.1111/j.1744-7917.2009.01281.x
Turlings TCJ, Lengwiler UB, Bernasconi ML, Wechsler D (1998) Timing of induced volatile emissions in maize seedlings. Planta 207:146–152. https://doi.org/10.2307/23385423
Van Driesche RG, Carruthers RI, Center T, Hoddle MS, Hough-Goldstein J, Morin L, Smith L, Wagner DL, Blossey B, Brancatini V, Casagrande R (2010) Classical biological control for the protection of natural ecosystems. Biol Control 54:2–33. https://doi.org/10.1016/j.biocontrol.2010.03.003
Varella AC, Menezes-Netto AC, de Souza Alonso JD, Caixeta DF, Peterson RK, Fernandes OA (2015) Mortality dynamics of Spodoptera frugiperda (Lepidoptera: Noctuidae) immatures in maize. PLoS ONE 10:e0130437. https://doi.org/10.1371/journal.pone.0130437
Wang ZY, Wang XM (2019) Current status management strategies for corn pests and diseases in China. Plant Prot 45:1–11. https://doi.org/10.16688/j.zwbh.2018442
Wang H, Reitz SR, Xiang J, Smagghe G, Lei Z (2014) Does temperature-mediated reproductive success drive the direction of species displacement in two invasive species of leafminer fly? PLoS ONE 9:e0098761. https://doi.org/10.1371/journal.pone.0098761
Wu KM (2020) Management strategies of fall army worm (Spodoptera frugiperda) in China. Plant Prot 46:1–5. https://doi.org/10.16688/j.zwbh.2020088
Wu KM, Guo YY (2005) The evolution of cotton pest management practices in China. Annu Rev Entomol 50:31–52. https://doi.org/10.1146/annurev.ento.50.071803.130349
Wu KM, Lu YH, Feng HQ, Jiang YY, Zhao JZ (2008) Suppression of cotton bollworm in multiple crops in China in areas with Bt toxin-containing cotton. Science 321:1676–1678. https://doi.org/10.1126/science.1160550
Wu HH, Huang MS, Lei CL, Wan P (2016) The spatial-temporal distribution of Spodoptera litura in China. J Anhui Agric Sci 44:142–144. https://doi.org/10.13989/j.cnki.0517-6611.2016.09.049
Wyckhuys KAG, Wongtiem P, Rauf A, Thancharoen A, Heimpel GE, Le NT, Fanani MZ, Gurr GM, Lundgren JG, Burra DD, Palao LK (2018) Continental-scale suppression of an invasive pest by a host-specific parasitoid underlines both environmental and economic benefits of arthropod biological control. Peer J 6:e5796. https://doi.org/10.7717/peerj.5796
Wyckhuys KAG, Zhang W, Prager SD, Kramer DB, Delaquis E, Gonzalez CE, Van der Werf W (2018) Biological control of an invasive pest eases pressures on global commodity markets. Environ Res Lett 13:094005. https://doi.org/10.1088/1748-9326/aad8f0
Yang L, Xu L, Liu B, Zhang Q, Pan Y, Li Q, Li H, Lu Y (2019) Non-crop habitats promote the abundance of predatory ladybeetles in maize fields in the agricultural landscape of northern China. Agric Ecosyst Environ 277:44–52. https://doi.org/10.1016/j.agee.2019.03.008
Zanuncio JC, Silva CADD, Lima ERD, Pereira FF, Ramalho FDS, Serrão JE (2008) Predation rate of Spodoptera frugiperda (Lepidoptera: Noctuidae) larvae with and without defense by Podisus nigrispinus (Heteroptera: Pentatomidae). Braz Arch Biol Tech 51:121–125. https://doi.org/10.1590/S1516-89132008000100015
Zhang SM, Zhao YX (1996) The Geographical Distribution of agricultural and forest insects in China. China Agriculture Press, Beijing
Zhang L, Liu B, Jiang YY, Liu J, Wu KM, Xiao YT (2019) Molecular characterization analysis of fall armyworm populations in China. Plant Prot 45:20–27. https://doi.org/10.16688/j.zwbh.2019296
Zhao S, Luo Q, Sun X, Yang X, Jiang Y, Wu K (2019) Comparison of morphological and biological characteristics between Spodoptera frugiperda and Spodoptera litura. China Plant Prot 39:26–35
Zhou A, Liang G, Lu Y, Zeng L, Xu Y (2014) Interspecific competition between the red imported fire ant, Solenopsis invicta Buren and ghost ant, Tapinoma Melanocephalum Fabricius for honeydew resources produced by an invasive mealybug, Phenacoccus solenopsis Tinsiley. Arthropod-Plant Interact 8:469–474. https://doi.org/10.1007/s11829.014.9324.1
Acknowledgements
This work was supported by the National Key R&D Program of China [2019YFD0300102]; the Central Public-interest Scientific Institution Basal Research Fund, China [CAASZDRW202007]; and the National Modern Agricultural Industry Technology System Construction Fund Project of China [CARS-15-19].
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors have declared that they have no conflict of interest.
Ethical approval
This article does not contain any studies with human participants or animals performed by any of the authors.
Additional information
Communicated by Mattias Jonsson .
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Song, Y., Yang, X., Zhang, H. et al. Interference competition and predation between invasive and native herbivores in maize. J Pest Sci 94, 1053–1063 (2021). https://doi.org/10.1007/s10340-021-01347-6
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10340-021-01347-6