Abstract
The spatio-temporal dynamics of insect pests in agricultural landscapes involves the potential of species to move, invade, colonise, and establish in different areas. This study revised the dispersal of the important crop pests Diabrotica speciosa Germar and Spodoptera frugiperda (J.E. Smith) by using computational modelling to represent the movement of these polyphagous pests in agricultural mosaics. The findings raise significant questions regarding the dispersal of pests through crops and refuge areas, indicating that understanding pest movement is essential for developing strategies to predict critical infestation levels to assist in pest-management decisions. In addition, our modelling approach can be adapted for other insect species and other cropping systems despite discussing two specific species in the current manuscript. We present an overview of studies, combining experimentation and ecological modelling, discussing the methods used and the importance of studying insect movement as well as the implications for agricultural landscapes in Brazil.
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References
Allen-Perkins A, Estrada E (2019) Mathematical modelling for sustainable aphid control in agriculture via intercropping. Proc R Soc A 475:20190136. https://doi.org/10.1098/rspa.2019.0136
Altieri M (1999) The ecological role of biodiversity in agroecosystems. Agric Ecosyst Environ 74:19–31. https://doi.org/10.1016/S0167-8809(99)00028-6
Andow DA (1991) Vegetational Diversity And Arthropod Population Response. Annu Rev Entomol 36:561–586. https://doi.org/10.1146/annurev.en.36.010191.003021
Andow DA, Farrell SL, Hu Y (2010) Planting patterns of in-field refuges observed for Bt maize in Minnesota. J Econ Entomol 103:1394–1399. https://doi.org/10.1603/EC09201
Arias O, Cordeiro E, Corrêa AS, Domingues FA, Guidolin AS, Omoto C (2019) Population genetic structure and demographic history of Spodoptera frugiperda (Lepidoptera: Noctuidae): implications for insect resistance management programs. Pest Manag Sci 75:2948–2957. https://doi.org/10.1002/ps.5407
Ávila CJ, Parra JRP (2002) Desenvolvimento de Diabrotica speciosa (Germar) (Coleoptera: Chrysomelidae) em diferentes hospedeiros. Ciênc Rural 32(5):739–743. https://doi.org/10.1590/S0103-84782002000500001
Ávila CJ, Parra JRP (2003) Leaf consumption by Diabrotica speciosa (Coleoptera: Chrysomelidae) adults on different host plants. Sci Agric 60(4):789–792. https://doi.org/10.1590/S0103-90162003000400028
Baldin ELL, Lara FM (2001) Attractiveness and leaf consumption by adults of Diabrotica speciosa (Germ.) (Coleoptera: Chrysomelidae) in different squash genotypes. Neotrop Entomol 30:675–679
Baloch MN, Fan J, Haseeb M, Zhang R (2020) Mapping potential distribution of Spodoptera frugiperda (Lepidoptera: Noctuidae) in Central Asia. Insects 11(3):172. https://doi.org/10.3390/insects11030172
Banks JE, Ekbom B (1999) Modelling herbivore movement and colonization: pest management potential of intercropping and trap cropping. Agric For Entomol 1:165–170. https://doi.org/10.1046/j.1461-9563.1999.00022.x
Bascompte J, Solé RV (1998) Effects of habitat destructionin a prey–predator metapopulation model. J Theor Biol 195:383–393
Boudreau M (2013) Diseases in intercropping systems. Annu Rev Phytopathol 51:499–519. https://doi.org/10.1146/annurev-phyto-082712-102246
Brown A (2016) Animal movement. Nat Clim Chang 6:339. https://doi.org/10.1038/nclimate2983
Calil YCD, Ribera L (2019) Brazil’s Agricultural Production and Its Potential as Global Food Supplier. Choices. Available online: http://www.choicesmagazine.org/choices-magazine/theme-articles/theme-overview-the-agricultural-production-potential-of-latin-american-implications-for-global-food-supply-and-trade/brazils-agricultural-production-and-its-potential-as-global-food-supplier
Caprio MA, Faver MK, Hankins G (2004) Evaluating the impacts of refuge width on source-sink dynamics between transgenic and nontransgenic cotton. J Insect Sci 4:13. https://doi.org/10.1093/jis/4.1.3
Caprio MA, Parker CD, Schneider JC (2009) Future fitness of female insect pests in temporally stable and unstable habitats and its impact on habitat utility as refuges for insect resistance management. J Insect Sci 9:144. https://doi.org/10.1673/031.009.4401
Caprio MA, Martinez JC, Porter PA, Bynum E (2016) The Impact of Inter-Kernel Movement in the Evolution of Resistance to Dual-Toxin Bt-Corn Varieties in (Lepidoptera: Noctuidae). Journal of Economic Entomology 109(1):307–319
Carrière Y, Dutilleul P, Ellers-Kirk C, Pedersen B, Haller S, Antilla L, Dennehy TJ, Tabashnik BE (2004) Sources, sinks, and the zone of influence of refuges for managing insect resistance to Bt crops. Ecol Appl 14:1615–1623. https://doi.org/10.1890/03-5268
Carroll MW, Head G, Caprio M (2012) When and where a seed mix refuge makes sense for managing insect resistance to Bt plants. Crop Prot 38:74–79. https://doi.org/10.1016/j.cropro.2012.02.015
Cerda H, Wright D (2004) Modeling the spatial and temporal location of refugia to manage resistance in Bt transgenic crops. Agric Ecosyst Environ 102:163–174. https://doi.org/10.1016/j.agee.2003.08.004
Chimonyo VGP, Modi AT, Mabhaudhi T (2015) Perspective on crop modelling in the management of intercropping systems. Arch Agron Soil Sci 61:1511–1529. https://doi.org/10.1080/03650340.2015.1017816
Clark PL, Molina-Ochoa J, Martinelli S, Skoda SR, Isenhour DJ, Lee DJ, Krumm JT, Foster JE (2007) Population variation of the fall armyworm, Spodoptera frugiperda, in the Western Hemisphere. J Insect Sci 7:15. https://doi.org/10.1673/031.007.0501
Common IFB (1990) Moths of Australia. Melbourne University Press, Victoria, p 535
Diekotter T, Crist TO (2003) Quantifying habitat-specific contributions to insect diversity in agricultural mosaic landscapes. Ins Cons Div 6:607-618. https:// doi: https://doi.org/10.1111/icad.12015
Donatelli M, Magarev RD, Bregaglio S, Willocquet L, Whish JPM, Savary S (2017) Modelling the impacts of pests and diseases on agricultural systems. Agric Syst 155:213–224. https://doi.org/10.1016/j.agsy.2017.01.019
Early R, González-Moreno P, Murphy ST, Day R (2018) Forecasting the global extent of invasion of the cereal pest Spodoptera frugiperda, the fall armyworm. NeoBiota 40:25–50. https://doi.org/10.3897/neobiota.40.28165
FAO (2018) Briefing Note on FAO Actions on fall armyworm in Africa. Available in http://www.fao.org/3/a-bt415e.pdf. Accessed on 28 October 2020
Ferreira CP, Godoy WAC (2014) Ecological modelling applied to entomology. Entomology in Focus 1. Springer, Switzerland, p 266
Ferreira CP, Esteva L, Godoy WAC, Cônsoli FL (2014) Landscape diversity influences dispersal and establishment of pest with complex nutritional ecology. Bull Math Biol 76:1747–1761. https://doi.org/10.1007/s11538-014-9975-1
Garcia AG, Godoy WAC (2017) A theoretical approach to analyze the parametric influence on spatial patterns of Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae) Populations. Neotrop Entomol 46(3):283–288. https://doi.org/10.1007/s13744-016-0472-0
Garcia A, Cônsoli FL, Godoy WAC et al (2014) A mathematical approach to simulate spatio-temporal patterns of an insect-pest, the corn rootworm Diabrotica speciosa (Coleoptera: Chrysomelidae) in intercropping systems. Landsc Ecol 29:1531–1540. https://doi.org/10.1007/s10980-014-0073-4
Garcia AG, Ferreira CP, Consoli FL et al (2016) Predicting evolution of insect resistance to transgenic crops in within-field refuge configurations, based on larval movement. Ecol Complex 28:94–103. https://doi.org/10.1016/j.ecocom.2016.07.006
Garcia AG, Godoy WAC, Thomas JMG, Nagoshi RN, Meagher RL (2018) Delimiting strategic zones for the development of fall armyworm (Lepidoptera: Noctuidae) on corn in the State of Florida. J Econ Entomol 111:120–126. https://doi.org/10.1093/jee/tox329
Garcia AG, Ferreira CP, Godoy WAC, Meagher RL (2019) A computational model to predict the population dynamics of Spodoptera frugiperda. J Pest Sci 92:429–441. https://doi.org/10.1007/s10340-018-1051-4
Garcia AG, Godoy WAC, Cônsoli FL, Ferreira CP (2020) Modelling movement and stage-specific habitat preferences of a polyphagous insect pest. Mov Ecol 8:13. https://doi.org/10.1186/s40462-020-00198-7
Gilligan CA, Claessen D, van den Bosch F (2005) Spatial and temporal dynamics of gene movements arising from deployment of transgenic crops. In: Wesseler JHH (ed) Environmental costs and benefits of transgenic crops. Springer, New York, pp 143–161
Goergen G, Kumar PL, Sankung SB, Togola A, Tamò 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
Gripenberg S, Morrien E, Cudmore A et al (2007) Resource selection by female moths in a heterogenous environment: what is a poor girl to do? J Anim Ecol 76:854–865. https://doi.org/10.1111/j.1365-2656.2007.01261.x
Haenniger S, Goergen G, Akinbuluma MD, Kunert M, Heckel DG, Unbehend M (2020) Sexual communication of Spodoptera frugiperda from West Africa: adaptation of an invasive species and implications for pest management. Sci Rep 10:2892. https://doi.org/10.1038/s41598-020-59708-7
Hanan J, Prusinkiewicz P, Zalucki M, Sirkin D (2002) Simulation of insect movement with respect to plant architecture and morphogenesis. Comput Electron Agric 35:255–269. https://doi.org/10.1016/S0168-1699(02)00022-4
Hanski I (1999) Metapopulation ecology. Oxford University Press, Oxford, UK, Oxford Series in Ecology and Evolution, p 313
Hardy NB, Otto SP (2014) Specialization and generalization in the diversification of phytophagous insects: tests of the musical chairs and oscillation hypotheses. Proc R Soc B 281:20132960. https://doi.org/10.1098/rspb.2013.2960
Hassanali A, Herren H, Khan ZR, Pickett JA, Woodcock CM (2008) Integrated pest management: the push-pull approach for controlling insect pests and weeds of cereals, and its potential for other agricultural systems including animal husbandry. Philos Trans R Soc B 363:611–621. https://doi.org/10.1098/rstb.2007.2173
Hastings A, Gross LJ (2012) Encyclopedia of theoretical ecology. University of California Press, Berkeley, p 823
Hawkes C (2009) Linking movement behaviour, dispersal and population processes: is individual variation a key? J Anim Ecol 78:894–906. https://doi.org/10.1111/j.1365-2656.2009.01534.x
Holzkämper A, Seppelt R (2007) A generic tool for optimizing land use patterns and landscape structures. Env Mod Software 22:1801–1804. https://doi.org/10.1016/j.envsoft.2007.02.008
Horikoshi RJ, Bernardi D, Bernardi O, Malaquias JB, Okuma DM, Miraldo LL, Amaral FSA, Omoto C (2016) Effective dominance of resistance of Spodoptera frugiperda to Bt maize and cotton varieties: implications for resistance management. Sci Rep 6:34864. https://doi.org/10.1038/srep34864
Huang C, Liu Q, Gou F (2017) Plant growth patterns in a tripartite strip relay intercrop are shaped by asymmetric above ground competition. Field Crop Res 201:41–51. https://doi.org/10.1016/j.fcr.2016.10.021
Janz N (2005) The relationship between habitat selection and preference for adult and larval food resources in the polyphagous butterfly Vanessa cardui (Lepidoptera: Nymphalidae). J Insect Behav 18:767–780. https://doi.org/10.1007/s10905-005-8739-z
Kari JJ (2012) Basic concepts of cellular automata. In: Rozenberg G, Bäck T, Kok JN (eds) Handbook of natural computing. Springer-Verlag, Berlin, pp 3–24. https://doi.org/10.1007/978-3-540-92910-9_1
Kennedy GG, Storer NP (2000) Life systems of polyphagous arthropod pests in temporally unstable cropping systems. Annu Rev Entomol 45:467–493. https://doi.org/10.1146/annurev.ento.45.1.467
Lamp WO, Zhao L (1993) Prediction and manipulation of movement by polyphagous, highly mobile pests! J Agric Entomol 10:267–281
Lima EABF, Ferreira CP, Godoy WAC (2009) Ecological modeling and pest population management: a possible and necessary connection in a changing world. Neotrop Entomol 38:699–707. https://doi.org/10.1590/s1519-566×2009000600001
Macfadyen S, Davies AP, Zalucki MP (2015) Assessing the impact of arthropod natural enemies on crop pests at the field scale. Insects 22:20–34. https://doi.org/10.1111/1744-7917.12174
Machado EP, dos S. Rodrigues Junior GL, Führ FM et al (2020) Cross-crop resistance of Spodoptera frugiperda selected on Bt maize to genetically-modified soybean expressing Cry1Ac and Cry1F proteins in Brazil. Sci Rep 10:10080. https://doi.org/10.1038/s41598-020-67339-1
Maitra S, Palai JB, Manasa P, Kumar DP (2019) Potential of intercropping system in sustaining crop productivity. JAEB 12:39–45. https://doi.org/10.30954/0974-1712.03.2019.7
Malaquias JB, Godoy WAC, Garcia AG, Ramalho FS, Omoto C (2017) Larval dispersal of Spodoptera frugiperda strains on Bt cotton: a model for understanding resistance evolution and consequences for its management. Sci Rep 7:16109. https://doi.org/10.1038/s41598-017-16094-x
Malaquias JB, Caprio MA, Godoy WAC, Omoto C, Ramalho FS, Pachú JKS (2020) Experimental and theoretical landscape influences on Spodoptera frugiperda movement and resistance evolution in contaminated refuge areas of Bt cotton. J Pest Sci 93:329–340. https://doi.org/10.1007/s10340-019-01145-1
Malaquias JB, Godoy WAC, Caprio MA et al. (2021) Evolutionary process modelling with Bayesian inference of Spodoptera frugiperda ballooning and walking dispersal on Bt and non-Bt cotton plants mixture. Entomol Exp Appl (in press)
Marques GBC, Ávila CJ, Parra JRP (1999) Danos Causados por Larvas e Adultos de Diabrotica speciosa (Coleoptera: Chrysomelidae) em Milho. Pesqui Agropecu Bras 34:1983–1986. https://doi.org/10.1590/S0100-204X1999001100002
Martinez JC, Caprio MA, Friedenberg NA (2018) Density dependence and growth rate: evolutionary effects on resistance development to Bt (Bacillus thuringiensis). J Econ Entomol 111:382–390. https://doi.org/10.1093/jee/tox323
Mazzi D, Dorn S (2012) Movement of insect pests in agricultural landscapes. Ann Appl Biol 160:97–113. https://doi.org/10.1111/j.1744-7348.2012.00533.x
Meehan TD, Werling BP, Landis DA, Gratton C (2011) Agricultural landscape simplification and insecticide use in the Midwestern United States. PNAS 12:11500–11505. https://doi.org/10.1073/pnas.1100751108
Moorcroft PR (2012) Mechanistic approaches to understanding and predicting mammalian space use: recent advances, future directions. J Mammal 93:903–916
Murray JD (2003) Mathematical biology II: Spatial models and biomedical applications. 3rd Ed. Interdisciplinary Applied Mathematics Series 18. Springer-Verlag, New York, p 838
Nagoshi RN, Meagher RL (2004) Seasonal distribution of fall armyworm (Lepidoptera: Noctuidae) host strains in agricultural and turf grass habitats. Environ Entomol 33:881–889. https://doi.org/10.1603/0046-225X-33.4.881
Nair SS, Kang SJ, Zhang XS, Miguez FE, Izaurralde RC, Wullschleger SD (2012) Bioenergy crop models: descriptionschallenges. Glob Change Biol Bioenergy. 4:620–633. https://doi.org/10.1111/j.1757-1707.2012.01166.x
Nakweya G (2020) Global actions needed to combat fall armyworm. Available online: https:// www.scidev.net/sub-saharan-africa/farming/news/global-actions-combat-fall-armyworm.Html (accessed on 1 February 2020)
Nathan R, Getz WM, Revilla E, Holyoak M, Kadmon R, Saltz D, Smouse PE (2008) A movement ecology paradigm for unifying organismal movement research. Proc Natl Acad Sci U S A 105(49):19052–19059. https://doi.org/10.1073/pnas.0800375105
Nguyen HDD, Nansen C (2018) Edge-biased distributions of insects. A review Agron Sustain Dev 38:11. https://doi.org/10.1007/s13593-018-0488-4
Okubo A (1980) Diffusion and Ecological Problems: Mathematical Models. (Biomathematics, Vol. 10.) Springer-Verlag, Berlin-Heidelberg-New York, p. 254
Paiva IG, Auad AM, Veríssimo BA, Silveira LCP (2020) Differences in the insect fauna associated to a monocultural pasture and a silvopasture in Southeastern Brazil. Sci Rep 10:12112. https://doi.org/10.1038/s41598-020-68973-5
Peñalver-Cruz A, Alvarez-Baca JK, Alfaro-Tapia A, Gontijo L, Lavandero B (2019) Manipulation of agricultural habitats to improve conservation biological control in South America. Neotrop Entomol 48:875–898. https://doi.org/10.1007/s13744-019-00725-1
Pereira PAA, Martha GB, Santana CA et al (2012) The development of Brazilian agriculture: future technological challenges and opportunities. Agric Food Secur 1:4. https://doi.org/10.1186/2048-7010-1-4
Prowell DP, McMichael M, Silvain JF (2004) Multilocus genetic analysis of host use, introgression, and speciation in host strains of fall armyworm (Lepidoptera: Noctuidae). Ann Entomol Soc Am 97:1034–1044. https://doi.org/10.1603/0013-8746(2004)097[1034:mgaohu]2.0.co;2
Quisenberry SS (1991) Fall armyworm (Lepidoptera: Noctuidae) host strain reproductive compatibility. Fla Entomol 74:194–199
Radcliffe EB, Ragsdale DW (2002) Aphid-transmitted potato viruses: the importance of understanding vector biology. Am J Potato Res 79:353–386. https://doi.org/10.1007/BF02870173
Richardson EB, Troczka BJ, Gutbrod O, Davies TGE, Nauen R (2020) Diamide resistance: 10 years of lessons from lepidopteran pests. J Pest Sci 93:911–928. https://doi.org/10.1007/s10340-020-01220-y
Rodrigues LAD, Varriale MC, Godoy WAC, Mistro DC (2014) Coupled map lattice model for insects and spreadable substances. In: Ferreira CP, Godoy WAC (eds) Ecological modelling applied to entomology. Entomology in Focus vol 1. Springer, Cham, https://doi.org/10.1007/978-3-319-06877-0_7, pp 141–169
Sage RF, Monson RK (1998) C4 plant biology. Academic Press, London, UK, p 594
Sarate PJ, Tamhane VA, Kotkar HM (2012) Developmental and digestive flexibilities in the midgut of a polyphagous pest, the cotton bollworm, Helicoverpa armigera. J Insect Sci 12:42–16. https://doi.org/10.1673/031.012.4201
Scheirs J, De Bruyn L (2002) Integrating optimal foraging and optimal oviposition theory in plant-insect research. Oikos 96:187–191. https://doi.org/10.1034/j.1600-0706.2002.960121.x
Scheirs J, De Bruyn L, Verhagen R (2000) Optimization of adult performance determines host choice in a grass miner. Proc R Soc Lond B 267:2065–2069. https://doi.org/10.1098/rspb.2000.1250
Silva DM, Bueno AF, Andrade KS et al (2017) Biology and nutrition of Spodoptera frugiperda (Lepidoptera: Noctuidae) fed on different food sources. Sci Agric 74:18–31. https://doi.org/10.1590/1678-992x-2015-0160
Sisterson MS, Carrière Y, Dennehy TJ, Tabashnik BE (2005) Evolution of resistance to transgenic crops: interaction between insect movement and field distribution. J Econ Entomol 98:1751–1762. https://doi.org/10.1093/jee/98.6.1751
Smouse PE, Focardi S, Moorcroft PR, Kie JG, Forester JG, Morales JM (2010) Stochastic modelling of animal movement. Phil Trans R Soc B Biol Sci 365(1550):2201–2211. https://doi.org/10.1098/rstb.2010.0078
Song BZ, Wu HY, Kong Y, Zhang J, du YL, Hu JH, Yao YC (2010) Effects of intercropping with aromatic plants on the diversity and structure of an arthropod community in a pear orchard. BioControl 55:741-751. https:// doi: https://doi.org/10.1007/s10526-010-9301-2
Staudacher K, Schallhart N, Thalinger B, Wallinger C, Juen A, Traugott M (2013) Plant diversity affects behavior of generalist root herbivores, reduces crop damage, and enhances crop yield. Ecol Appl 23:1135–1145. https://doi.org/10.1890/13-0018.1
Tabashnik BE, Carrière Y (2017) Surge in insect resistance to transgenic crops and prospects for sustainability. Nat Biotechnol 35:926–935. https://doi.org/10.1038/nbt.3974
Tabashnik BE, Brévault T, Carrière Y (2013) Insect resistance to Bt crops: lessons from the first billion acres. Nat Biotechnol 31:510–521. https://doi.org/10.1038/nbt.2597
Thacker JRM (2002) An introduction to arthropod pest control. Cambridge University Press, Cambridge, UK, p 343
Tonnang HEZ, Hervé BDB, Biber-Freudenberger L, Salifu D, Subramanian S, Ngowi VB, Guimapi RYA, Anani B, Kakmeni FMM, Affognon H, Niassy S, Landmann T, Ndjomatchoua FT, Pedro SA, Johansson T, Tanga CM, Nana P, Fiaboe KM, Mohamed SF, Maniania NK, Nedorezov LV, Ekesi S, Borgemeister C (2017) Advances in crop insect modelling methods—towards a whole system approach. Ecol Model 354:88–103. https://doi.org/10.1016/j.ecolmodel.2017.03.015
Tscharntke T, Klein AM, Kruess A, Steffan-Dewenter I, Thies C (2005) Landscape perspectives on agricultural intensification and biodiversity – ecosystem service management. Ecol Lett 8:857–874. https://doi.org/10.1111/j.1461-0248.2005.00782.x
Turner MG, Gardner RH, O’Neill RV (2001) Landscape ecology in theory and practice: pattern and process. Springer, New York, p 401
Turchin P (1998) Quantitative analysis of movement measuring and modeling population redistribution of plants and animals. Sinauer Associates, p 396
USDA (2020) Oilseeds and products annual. Report Number: BR2020-0011. United States Department of Agriculture Foreign Agricultural Service, Brasília, Brazil
Walsh GC (2003) Host range and reproductive traits of Diabrotica speciosa (Germar) and Diabrotica viridula (F.) (Coleoptera: Chrysomelidae), two species of South American pest rootworms, with notes on other species of Diabroticina. Environ Entomol 32(2):276–285. https://doi.org/10.1603/0046-225X-32.2.276
Walsh GC, Ávila CJ, Cabrera N et al (2020) Biology and management of pest Diabrotica species in South America. Insects 11:421. https://doi.org/10.3390/insects11070421
Westbrook JK, Nagoshi RN, Meagher RL, Fleischer SJ, Jairam S (2016) Modeling seasonal migration of fall armyworm moths. Int J Biometeorol 60:255–267. https://doi.org/10.1007/s00484-015-1022-x
Xiao Y, Wu K (2019) Recent progress on the interaction between insects and Bacillus thuringiensis crops. Philos Trans R Soc B 374:20180316. https://doi.org/10.1098/rstb.2018.0316
Xiao H, Ye X, Xu H, Mei Y, Yang Y, Chen Yang Y, Liu T, Yu Y, Yang W, Lu Z, Li F (2020) The genetic adaptations of fall armyworm facilitated its rapid global dispersal and invasion. Molecular Ecology Resources 20(4):1050–1068
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AGG and JBM hold fellowships awarded by FAPESP (2019/26071-8) and FAPESP (2017/05953-7), respectively. The project also received grant 2014/16609-7 from FAPESP.
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All authors contributed to the study conception and design. Data were collected and analysed by Adriano Gomes Garcia, José Bruno Malaquias, and Claudia Pio Ferreira. The first draft of the manuscript was written by Wesley Augusto Conde Godoy. Maysa Pereira Tomé, Igor Daniel Weber, Adriano Gomes Garcia, and Wesley Augusto Conde Godoy analysed and organised the text flow, reviewed the bibliography, and contributed to the discussion in the context of agricultural landscape ecology. All authors commented on previous versions of the manuscript, and read and approved the final manuscript.
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Garcia, A.G., Malaquias, J.B., Ferreira, C.P. et al. Ecological Modelling of Insect Movement in Cropping Systems. Neotrop Entomol 50, 321–334 (2021). https://doi.org/10.1007/s13744-021-00869-z
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DOI: https://doi.org/10.1007/s13744-021-00869-z