Abstract
Pest populations are mostly regulated by climate, intra- and interspecific competition, natural enemies, and host plant quality. Myzus persicae (Sulzer) (Hemiptera: Aphididae) is a widely adapted aphid in the agroecosystems and is one of the main bell pepper pests. In the present study, we determined the spatial and temporal dynamics and the regulatory factors of M. persicae populations in bell pepper crops. The number of aphids and their natural enemies were evaluated during 2 years in four commercial bell pepper fields. Myzus persicae density data were related to temperature, rainfall, and natural enemies by multiple regression analysis and were then submitted to geostatistical analysis. The density of M. persicae was higher during the plant’s reproductive growth stage. Rainfall, Chrysoperla spp., and Toxomerus spp. regulate M. persicae populations. Initial infestations of this pest occur along the edges of the fields and subsequently spread towards the center. This information is useful for integrated management programs aimed at anticipating periods of higher abundance of M. persicae and identifying arthropods to be prioritized in biological control.
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References
Agrios GN (2018) Economic considerations. In: Mandahar CL (ed) Plant viruses volume II: pathology, 1st edn. CRC Press, Boca Raton, pp 1–22
Akter MS, Siddique SS, Momotaz R, Arifunnahar M, Alam KM, Mohiuddin SJ (2019) Biological control of insect pests of agricultural crops through habitat management was discussed. Journal of Agricultural Chemistry and Environment 8:13
Alvares CA, Stape JL, Sentelhas PC, de Moraes Gonçalves JL, Sparovek G (2013) Köppen’s climate classification map for Brazil. Meteorol Z 22:711–728
Alyokhin A, Drummond FA, Sewell G, Storch RH (2011) Differential effects of weather and natural enemies on coexisting aphid populations. Environ Entomol 40:570–580. https://doi.org/10.1603/EN10176
Amiri-Jami AR, Sadeghi-Namaghi H, Gilbert F (2017) Performance of a predatory hoverfly feeding on Myzus persicae (Hemiptera: Aphididae) reared on two brassicaceous plants varies with ant attendance. Biol Control 105:49–55. https://doi.org/10.1016/j.biocontrol.2016.11.011
Arcaya E, Pérez-Bañón C, Mengual X, Zubcoff-Vallejo JJ, Rojo S (2017) Life table and predation rates of the syrphid fly Allograpta exotica, a control agent of the cowpea aphid Aphis craccivora. Biol Control 115:74–84. https://doi.org/10.1016/j.biocontrol.2017.09.009
Atlihan R, Kaydan B, Özgökçe MS (2004) Feeding activity and life history characteristics of the generalist predator, Chrysoperla carnea (Neuroptera: Chrysopidae) at different prey densities. J Pest Sci 77:17–21. https://doi.org/10.1007/s10340-003-0021-6
Awmack CS, Leather SR (2002) Host plant quality and fecundity in herbivorous insects. Annu Rev Entomol 47:817–844. https://doi.org/10.1146/annurev.ento.47.091201.145300
Barton BT, Ives AR (2014) Direct and indirect effects of warming on aphids, their predators, and ant mutualists. Ecology 95:1479–1484. https://doi.org/10.1890/13-1977.1
Bass C, Puinean AM, Zimmer CT, Denholm I, Field LM, Foster SP, Gutbrod O, Nauen R, Slater R, Williamson MS (2014) The evolution of insecticide resistance in the peach potato aphid, Myzus persicae. Insect Biochem Mol Biol 51:41–51. https://doi.org/10.1016/j.ibmb.2014.05.003
Bernays EA, Chapman RF (2007) Host-plant selection by phytophagous insects vol 2. 1 edn. Springer US, p 312
Bolton B (1994) Identification guide to the ant genera of the world. Harvard University Press, Cambridge, Massachusetts, p 232
Brooks SJ (1994) A taxonomic review of the common green lacewing genus Chrysoperla (Neuroptera: Chrysopidae). Bull Br Mus Nat Hist 63:137–210
Canard M (2001) Natural food and feeding habits of lacewings. In: McEwan PK, New TR, Whittington AE (eds) Lacewings in the crop environment, 1st edn. Cambridge University Press, Cambridge, p 564
Canedo-Júnior EO, Santiago GS, Ribas CR, Zurlo LF, Cuissi RG, Souza B, Faria LDB, Rabello AM, Braga DL, Silva E (2018) The effect size of aphid-tending ants in an agricultural tri-trophic system. J Appl Entomol 142:349–358. https://doi.org/10.1111/jen.12475
Chamuene A, Araujo TA, Silva G, Costa TL, Berger PG, Picanco MC (2018) Performance of the natural mortality factors of Aphis gossypii (Hemiptera: Aphididae) as a function of cotton plant variety and phenology. Environ Entomol 47:440–447. https://doi.org/10.1093/ee/nvx205
Charaabi K, Boukhris-Bouhachem S, Makni M, Denholm I (2018) Occurrence of target-site resistance to neonicotinoids in the aphid Myzus persicae in Tunisia, and its status on different host plants. Pest Manag Sci 74:1297–1301. https://doi.org/10.1002/ps.4833
Cibils-Stewart X, Sandercock BK, McCornack BP (2015) Feeding location affects demographic performance of cabbage aphids on winter canola. Entomol Exp Appl 156:149–159. https://doi.org/10.1111/eea.12325
da Silva ÉM, da Silva RS, Rodrigues-Silva N, Milagres CC, Bacci L, Picanço MC (2017) Assessment of the natural control of Neoleucinodes elegantalis in tomato cultivation using ecological life tables. Biocontrol Sci Tech 27:525–538. https://doi.org/10.1080/09583157.2017.1319911
da Silva SEB, França JF, Pareja M (2016) Olfactory response of four aphidophagous insects to aphid- and caterpillar-induced plant volatiles. Arthropod Plant Interact 10:331–340. https://doi.org/10.1007/s11829-016-9436-x
Day RL, Hickman JM, Sprague RI, Wratten SD (2015) Predatory hoverflies increase oviposition in response to colour stimuli offering no reward: implications for biological control. Basic Appl Ecol 16:544–552. https://doi.org/10.1016/j.baae.2015.05.004
Döring TF (2014) How aphids find their host plants, and how they don’t. Ann Appl Biol 165:3–26. https://doi.org/10.1111/aab.12142
FAOSTAT (2017) Food and agriculture Organization of the United Nations. http://www.fao.org/faostat/en/?#data/QC. Accessed 03/24/2019
Fenton B, Kasprowicz L, Malloch G, Pickup J (2010) Reproductive performance of asexual clones of the peach-potato aphid, (Myzus persicae, Homoptera: Aphididae), colonising Scotland in relation to host plant and field ecology. Bull Entomol Res 100:451–460. https://doi.org/10.1017/S0007485309990447
Fernandes MG, Spessoto RR, Degrande PE, Rodrigues TR (2011) Sequential sampling of Aphis gossypii Glover (Hemiptera: Aphididae) and Frankliniella schultzei Trybom (Thysanoptera: Thripidae) on cotton crop. Neotrop Entomol 40:258–263. https://doi.org/10.1590/S1519-566X2011000200016
Ferrante M, Gonzalez E, Lovei GL (2017) Predators do not spill over from forest fragments to maize fields in a landscape mosaic in Central Argentina. Ecol Evol 7:7699–7707. https://doi.org/10.1002/ece3.3247
Filgueira FAR (2008) Novo manual de olericultura: agrotecnologia moderna na produção e comercialização de hortaliças, 3rd edn. Editora UFV, Viçosa, MG, p 421
Galdino TVS, Ferreira DO, Santana Junior PA, Arcanjo LP, Queiroz EA, Sarmento RA, Picanco MC (2017) The role of the beetle Hypocryphalus mangiferae (Coleoptera: Curculionidae) in the spatiotemporal dynamics of mango wilt. J Econ Entomol 110:865–874. https://doi.org/10.1093/jee/tox063
Gordon RD (1985) The Coccinellidae (Coleoptera) of America north of Mexico. J N Y Entomol Soc 93
Gusmão MR, Picanco MC, Guedes RNC, Galvan TL, Pereira EJG (2006) Economic injury level and sequential sampling plan for Bemisia tabaci in outdoor tomato. J Appl Entomol 130:160–166. https://doi.org/10.1111/j.1439-0418.2005.01032.x
Harmel N, Almohamad R, Fauconnier M-L, Du Jardin P, Verheggen F, Marlier M, Haubruge E, Francis F (2007) Role of terpenes from aphid-infested potato on searching and oviposition behavior of Episyrphus balteatus. Insect Sci 14:57–63. https://doi.org/10.1111/j.1744-7917.2007.00126.x
Hodgson EW, McCornack BP, Tilmon K, Knodel JJ (2012) Management recommendations for soybean aphid (Hemiptera: Aphididae) in the United States. Journal of Integrated Pest Management 3:E1–E10. https://doi.org/10.1603/IPM11019
Inbar M, Gerling D (2008) Plant-mediated interactions between whiteflies, herbivores, and natural enemies. Annu Rev Entomol 53:431–448. https://doi.org/10.1146/annurev.ento.53.032107.122456
Inoue-Nagata AK, Fonseca MEN, Resende RO, Boiteux LS, Monte DC, Dusi AN, de Ávila AC, van der Vlugt RAA (2002) Pepper yellow mosaic virus, a new potyvirus in sweetpepper, Capsicum annuum. Arch Virol 147:849–855. https://doi.org/10.1007/s007050200032
Isaaks E, Srivastava R (1989) An introduction to applied geostatistics. Oxford University Press, New York
Kavallieratos NG, Tomanović Ž, Petrović A, Janković M, Starý P, Yovkova M, Athanassiou CG (2013) Review and key for the identification of parasitoids (Hymenoptera: Braconidae: Aphidiinae) of aphids infesting herbaceous and shrubby ornamental plants in southeastern Europe. Ann Entomol Soc Am 106:294–309. https://doi.org/10.1603/AN12090
Kindlmann P, Dixon AFG, Michaud JP (eds) (2010) Aphid biodiversity under environmental change. Springer Netherlands, Dordrecht, p 191. https://doi.org/10.1007/978-90-481-8601-3
Lai R, You M, Zhu C, Gu G, Lin Z, Liao L, Lin L, Zhong X (2017) Myzus persicae and aphid-transmitted viral disease control via variety intercropping in flue-cured tobacco. Crop Protect 100:157–162. https://doi.org/10.1016/j.cropro.2017.06.021
Layman ML, Lundgren JG (2015) Mutualistic and antagonistic trophic interactions in canola: the role of aphids in shaping pest and predator populations. Biol Control 91:62–70. https://doi.org/10.1016/j.biocontrol.2015.07.008
Lefebvre M, Franck P, Olivares J, Ricard J-M, Mandrin J-F, Lavigne C (2017) Spider predation on rosy apple aphid in conventional, organic and insecticide-free orchards and its impact on aphid populations. Biol Control 104:57–65. https://doi.org/10.1016/j.biocontrol.2016.10.009
Liebhold AM, Rossi RE, Kemp WP (1993) Geostatistics and geographic information systems in applied insect ecology. Annu Rev Entomol 38:303–327. https://doi.org/10.1146/annurev.en.38.010193.001511
Lima CHO, Sarmento RA, Galdino TVS, Pereira PS, Silva J, Souza DJ, Dos Santos GR, Costa TL, Picanco MC (2018) Spatiotemporal dynamics of whitefly Bemisia tabaci (Hemiptera: Aleyrodidae) in commercial watermelon crops. J Econ Entomol 111:1895–1903. https://doi.org/10.1093/jee/toy110
Ludwig M, Schlinkert H, Meyhöfer R (2018) Wind-modulated landscape effects on colonization of Brussels sprouts by insect pests and their syrphid antagonists. Agric For Entomol 20:141–149. https://doi.org/10.1111/afe.12237
Martins JC, Picanco MC, Silva RS, Gonring AH, Galdino TVdS, Guedes RN (2018) Assessing the spatial distribution of Tuta absoluta (Lepidoptera: Gelechiidae) eggs in open-field tomato cultivation through geostatistical analysis. Pest Manag Sci 74:30–36. https://doi.org/10.1002/ps.4664
Matheron G (1963) Principles of geostatistics. Econ Geol 58:1246–1266. https://doi.org/10.2113/gsecongeo.58.8.1246
Murphy PA, Sternitzke HS (1979) Growth and yield estimation for loblolly pine in the West Gulf. Res. Pap. SO-154. New Orleans, LA: U.S. Department of Agriculture, Forest Service, southern Forest Experiment Station. 12 p. 154
Nyasani JO, Meyhöfer R, Subramanian S, Poehling HM (2013) Seasonal abundance of western flower thrips and its natural enemies in different French bean agroecosystems in Kenya. J Pest Sci 86:515–523. https://doi.org/10.1007/s10340-013-0491-0
Pedigo LP, Rice ME (2014) Entomology and pest management. 6th edn. Waveland Press Inc., Long Grove, Illinois, p 784
Pereira PS, Sarmento RA, Galdino TV, Lima CH, Dos Santos FA, Silva J, Dos Santos GR, Picanco MC (2017) Economic injury levels and sequential sampling plans for Frankliniella schultzei in watermelon crops. Pest Manag Sci 73:1438–1445. https://doi.org/10.1002/ps.4475
Riolo MA, Rohani P, Hunter MD (2015) Local variation in plant quality influences large-scale population dynamics. Oikos 124:1160–1170. https://doi.org/10.1111/oik.01759
Robertson GP (2008) GS+: Geostatistics for the environmental sciences user’s guide, 7.0 edn.,
Rodrigues-Silva N, de Oliveira CS, de Sá FE, de Souza TC, Martins JC, Picanço MC (2017) Relative importance of natural enemies and abiotic factors as sources of regulation of mealybugs (Hemiptera: Pseudococcidae) in Brazilian coffee plantations. Ann Appl Biol 171:303–315. https://doi.org/10.1111/aab.12373
Rosado JF, Picanço MC, Sarmento RA, da Silva RS, Pedro-Neto M, Carvalho MA, Erasmo EAL, Silva LCR (2015) Seasonal variation in the populations of Polyphagotarsonemus latus and Tetranychus bastosi in physic nut (Jatropha curcas) plantations. Exp Appl Acarol 66:415–426. https://doi.org/10.1007/s10493-015-9911-6
Roubinet E, Birkhofer K, Malsher G, Staudacher K, Ekbom B, Traugott M, Jonsson M (2017) Diet of generalist predators reflects effects of cropping period and farming system on extra- and intraguild prey. Ecol Appl 27:1167–1177. https://doi.org/10.1002/eap.1510
Rusch A, Valantin-Morison M, Sarthou JP, Roger-Estrade J (2013) Effect of crop management and landscape context on insect pest populations and crop damage. Agric Ecosyst Environ 166:118–125. https://doi.org/10.1016/j.agee.2011.05.004
Salamanca J, Pareja M, Rodriguez-Saona C, Resende ALS, Souza B (2015) Behavioral responses of adult lacewings, Chrysoperla externa, to a rose–aphid–coriander complex. Biol Control 80:103–112. https://doi.org/10.1016/j.biocontrol.2014.10.003
SAS II (2009) Procedures Guide, 9.2 edn., Cary, NC
Schröder ML, Glinwood R, Ignell R, Krüger K (2016) The role of visual and olfactory plant cues in aphid behaviour and the development of non-persistent virus management strategies. Arthropod Plant Interact 11:1–13. https://doi.org/10.1007/s11829-016-9463-7
Semeão AA, Martins JC, Picanco MC, Chediak M, da Silva EM, Silva GA (2012) Seasonal variation of natural mortality factors of the guava psyllid Triozoida limbata. Bull Entomol Res 102:719–729. https://doi.org/10.1017/S0007485312000338
Silva GA, Picanco MC, Bacci L, Crespo AL, Rosado JF, Guedes RN (2011) Control failure likelihood and spatial dependence of insecticide resistance in the tomato pinworm, Tuta absoluta. Pest Manag Sci 67:913–920. https://doi.org/10.1002/ps.2131
Snyder WE, Ives AR (2003) Interactions between specialist and generalist natural enemies: parasitoids, predators, and pea aphid biocontrol. Ecology 84:91–107. https://doi.org/10.1890/0012-9658(2003)084[0091:IBSAGN]2.0.CO;2
Stevens M, Lacomme C (2017) Transmission of plant viruses. In: van Emden HF, Harrington R (eds) Aphid as crop pests, 2nd edn. CABI, Wallingford, United Kindom, pp 323–361
Thompson FC (1999) Contributions on Entomology, International vol 3. A key to the genera of the flower flies (Diptera: Syrphidae) of the neotropical region including descriptions of new genera and species and a glossary of taxonomic terms used. Associated Publishers, Gainesville, FL, p 30
Triplehorn CA, Johnson NF (2015) Estudo dos insetos. 2 edn. Cengage Learning, p 766
Verheggen FJ, Arnaud L, Bartram S, Gohy M, Haubruge E (2008) Aphid and plant volatiles induce oviposition in an aphidophagous hoverfly. J Chem Ecol 34:301–307. https://doi.org/10.1007/s10886-008-9434-2
Voudouris CC, Williamson MS, Skouras PJ, Kati AN, Sahinoglou AJ, Margaritopoulos JT (2017) Evolution of imidacloprid resistance in Myzus persicae in Greece and susceptibility data for spirotetramat. Pest Manag Sci 73:1804–1812. https://doi.org/10.1002/ps.4539
Welch KD, Whitney TD, Harwood JD (2016) Non-pest prey do not disrupt aphid predation by a web-building spider. Bull Entomol Res 106:91–98. https://doi.org/10.1017/S0007485315000875
Whitfield AE, Falk BW, Rotenberg D (2015) Insect vector-mediated transmission of plant viruses. Virology 479-480:278–289. https://doi.org/10.1016/j.virol.2015.03.026
Yao I (2014) Costs and constraints in aphid-ant mutualism. Ecol Res 29:383–391. https://doi.org/10.1007/s11284-014-1151-4
Zhang Y, Wang L, Wu K, Wyckhuys KAG, Heimpel GE (2008) Flight performance of the soybean aphid, Aphis glycines (Hemiptera: Aphididae) under different temperature and humidity regimens. Environ Entomol 37:301–306. https://doi.org/10.1093/ee/37.2.301
Zust T, Agrawal AA (2016) Mechanisms and evolution of plant resistance to aphids. Nat Plants 2:15206. https://doi.org/10.1038/nplants.2015.206
Acknowledgments
We would like to thank Mr. Phillip Villani (University of Melbourne, Australia) for revising the English writing, and professor Laércio Zambolim (Universidade Federal de Viçosa) for identifying the entomopathogen species.
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We are grateful for the financial support provided by the National Council of Scientific and Technological Development (CNPq), the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001, and the Minas Gerais State Foundation for Research Aid (FAPEMIG).
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JRSS, VCRA, RSR, TAA, and MCP contributed to the study conception and design. Material preparation, data collection, and analysis were performed by JRSS, JSP, VCRA, TAA, and RSR. The first draft of the manuscript was written by JRSS and corrected by JCZ. All authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
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Soares, J.R.S., da Silva Paes, J., de Araújo, V.C.R. et al. Spatiotemporal Dynamics and Natural Mortality Factors of Myzus persicae (Sulzer) (Hemiptera: Aphididae) in Bell Pepper Crops. Neotrop Entomol 49, 445–455 (2020). https://doi.org/10.1007/s13744-020-00761-2
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DOI: https://doi.org/10.1007/s13744-020-00761-2