Abstract
The whitefly, Bemisia tabaci, is considered one of the most important pests for tomato Solanum lycopersicum. The population density of this pest varies throughout the year in response to seasonal variation. Studies of seasonality are important to understand the ecological dynamics and insect population in crops and help to identify which seasons have the best climatic conditions for the growth and development of this insect species. In this research, we used CLIMEX to estimate the seasonal abundance of a species in relation to climate over time and species geographical distribution. Therefore, this research is designed to infer the mechanisms affecting population processes, rather than simply provide an empirical description of field observations based on matching patterns of meteorological data. In this research, we identified monthly suitability for Bemisia tabaci, with the climate models, for 12 commercial tomato crop locations through CLIMEX (version 4.0). We observed that B. tabaci displays seasonality with increased abundance in tomato crops during March, April, May, June, October and November (first year) and during March, April, May, September and October (second year) in all monitored areas. During this period, our model demonstrated a strong agreement between B. tabaci density and CLIMEX weekly growth index (GIw), which indicates significant reliability of our model results. Our results may be useful to design sampling and control strategies, in periods and locations when there is high suitability for B. tabaci.
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References
Albergaria NM, Cividanes FJ (2002) Thermal requirements of Bemisia tabaci (Genn.) B-biotype (Hemiptera: Aleyrodidae). Neotrop Entomol 31(3):359–363
Alicai T (1999) Seasonal changes in whitefly numbers and their influence on incidence of sweetpotato chlorotic stunt virus and sweetpotato virus disease in sweetpotato in Uganda. Int. J. Pest Manag. 45(1):51–55
Bacci L, Picanço MC, Moura MF, Della Lucia TM, Semeão AA (2006) Sampling plan for Diaphania spp.(Lepidoptera: Pyralidae) and for hymenopteran parasitoids on cucumber. J Econ Entomol 99(6):2177–2184
Campos WG, Schoereder JH, DeSouza OF (2006) Seasonality in neotropical populations of Plutella xylostella (Lepidoptera): resource availability and migration. Popul Ecol 48(2):151–158
da Silva RS, Kumar L, Shabani F, da Silva EM, da Silva Galdino TV, Picanço MC (2017) Spatio-temporal dynamic climate model for Neoleucinodes elegantalis using CLIMEX. Int J Biometeorol 61(5):785–795
De Villiers M, Hattingh V, Kriticos D (2013) Combining field phenological observations with distribution data to model the potential distribution of the fruit fly Ceratitis rosa Karsch (Diptera: Tephritidae). Bull Entomol Res 103(1):60–73
De Villiers M, Hattingh V, Kriticos DJ, Brunel S, Vayssières J-F, Sinzogan A, Billah M, Mohamed S, Mwatawala M, Abdelgader H (2016) The potential distribution of Bactrocera dorsalis: considering phenology and irrigation patterns. Bull Entomol Res 106(1):19–33
Desneux N, Wajnberg E, Wyckhuys KA, Burgio G, Arpaia S, Narváez-Vasquez CA, González-Cabrera J, Ruescas DC, Tabone E, Frandon J (2010) Biological invasion of European tomato crops by Tuta absoluta: ecology, geographic expansion and prospects for biological control. J Pest Sci 83(3):197–215
Elfekih S, Tay WT, Gordon K, Court LN, De Barro PJ (2018) Standardized molecular diagnostic tool for the identification of cryptic species within the Bemisia tabaci complex. Pest Manag Sci 74(1):170–173
Friedmann M, Lapidot M, Cohen S, Pilowsky M (1998) A novel source of resistance to tomato yellow leaf curl virus exhibiting a symptomless reaction to viral infection. J Am Soc Hortic Sci 123(6):1004–1007
Gerling D (1986) Natural enemies of Bemisia tabaci, biological characteristics and potential as biological control agents: a review. Agric Ecosyst Environ 17(1):99–110. https://doi.org/10.1016/0167-8809(86)90031-9
Gilioli G, Pasquali S, Parisi S, Winter S (2014) Modelling the potential distribution of Bemisia tabaci in Europe in light of the climate change scenario. Pest Manag Sci 70(10):1611–1623
Gontijo P, Picanço M, Pereira E, Martins J, Chediak M, Guedes R (2013) Spatial and temporal variation in the control failure likelihood of the tomato leaf miner, Tuta absoluta. Ann Appl Biol 162(1):50–59
Gottlieb Y, Zchori-Fein E, Mozes-Daube N, Kontsedalov S, Skaljac M, Brumin M, Sobol I, Czosnek H, Vavre F, Fleury F (2010) The transmission efficiency of tomato yellow leaf curl virus by the whitefly Bemisia tabaci is correlated with the presence of a specific symbiotic bacterium species. J Virol 84(18):9310–9317
Grávalos C, Fernández E, Belando A, Moreno I, Ros C, Bielza P (2015) Cross-resistance and baseline susceptibility of Mediterranean strains of Bemisia tabaci to cyantraniliprole. Pest Manag Sci 71(7):1030–1036
Gusmão M, Picanço M, Guedes R, Galvan T, Pereira E (2006) Economic injury level and sequential sampling plan for Bemisia tabaci in outdoor tomato. J Appl Entomol 130(3):160–166
Gusmao MR (2000) Avaliação de vetores de viroses, predadores e parasitóides e plano de amostragem para mosca-branca em tomateiro. Universidade Federal de Viçosa
Gusmão MR, Picanço MC, Zanuncio JC, Silva DJH, Barrigossi JAF (2005) Standardised sampling plan for Bemisia tabaci (Homoptera: Aleyrodidae) in outdoor tomatoes. Sci Hortic 103(4):403–412. https://doi.org/10.1016/j.scienta.2004.04.005
Han P, Desneux N, Michel T, Le Bot J, Seassau A, Wajnberg E, Amiens-Desneux E, Lavoir A-V (2016) Does plant cultivar difference modify the bottom-up effects of resource limitation on plant-insect herbivore interactions? J Chem Ecol 42(12):1293–1303
Harris I, Jones P (2017) CRU TS4. 00: Climatic Research Unit (CRU) Time-Series (TS) version 4.00 of high resolution gridded data of month-by-month variation in climate (Jan. 1901–Dec. 2015). Centre for Environmental Data Analysis 25
Heuvelink E (2005) Tomatoes, vol 13. CABI,
Hirano K, Budiyanto E, Winarni S (1993) Biological characteristics and forecasting outbreaks of the whitefly, Bemisia tabaci, a vector of virus diseases in soybean fields. ASPAC Food & Fertilizer Technology Center
Horowitz AR, Ishaaya I (2014) Dynamics of biotypes B and Q of the whitefly Bemisia tabaci and its impact on insecticide resistance. Pest Manag Sci 70(10):1568–1572
Imenes S, Campos T, Takematsu A, Bergmann E, Silva M (1992) Efeito do manejo integrado na população de pragas e inimigos naturais na produção de tomate estaqueado. Arq Inst Biol 59:1–7
Jafarbeigi F (2014) Sublethal effects of some botanical and chemical insecticides on the cotton whitefly, Bemisia tabaci (Hem: Aleyrodidae). Arthropods 3(3):127
Jones JB Jr (2007) Tomato plant culture: in the field, greenhouse, and home garden. CRC
Kriticos DJ, Maywald GF, Yonow T, Zurcher EJ, Herrmann NI, Sutherst R (2015) Exploring the effects of climate on plants, animals and diseases. CLIMEX Version 4:184
Lapidot M, Friedmann M, Lachman O, Yehezkel A, Nahon S, Cohen S, Pilowsky M (1997) Comparison of resistance level to tomato yellow leaf curl virus among commercial cultivars and breeding lines. Plant Dis 81(12):1425–1428
Leite GLD, Picanço M, Guedes RNC, Ecole CC (2006) Factors affecting the attack rate of Bemisia tabaci on cucumber. Pesq Agrop Brasileira 41(8):1241–1245
Lima CH, Sarmento RA, Pereira PS, Galdino TV, Santos FA, Silva J, Picanço MC (2017) Feasible sampling plan for Bemisia tabaci control decision-making in watermelon fields. Pest Manag Sci 73:2345–2352
Luan J-B, Chen W, Hasegawa DK, Simmons AM, Wintermantel WM, Ling K-S, Fei Z, Liu S-S, Douglas AE (2015) Metabolic coevolution in the bacterial symbiosis of whiteflies and related plant sap-feeding insects. Genome Biol Evol 7(9):2635–2647
McKenzie CL, Kumar V, Palmer CL, Oetting RD, Osborne LS (2014) Chemical class rotations for control of Bemisia tabaci (Hemiptera: Aleyrodidae) on poinsettia and their effect on cryptic species population composition. Pest Manag Sci 70(10):1573–1587
Moraes CP, Foerster LA (2015) Thermal requirements, fertility, and number of generations of Neoleucinodes elegantalis (Guenée) (Lepidoptera: Crambidae). Neotrop Entomol:1–7 GBIF.org (2nd May 2017) GBIF Occurrence Download https://doi.org/10.15468/dl.mwb31k
Morales FJ, Jones PG (2004) The ecology and epidemiology of whitefly-transmitted viruses in Latin America. Virus Res 100(1):57–65 https://doi.org/10.1016/j.virusres.2003.12.014
Munyuli T, Kalimba Y, Mulangane EK, Mukadi TT, Ilunga MT, Mukendi RT (2017) Interaction of the fluctuation of the population density of sweet potato pests with changes in farming practices, climate and physical environments: a 11-year preliminary observation from South-Kivu Province, Eastern DRCongo. Open Agriculture 2(1):495–530
Naranjo SE, Castle SJ, De Barro PJ, Liu S-S (2009) Population dynamics, demography, dispersal and spread of Bemisia tabaci. In: Bemisia: bionomics and management of a global pest. Springer, pp 185–226
Naranjo SE, Ellsworth PC (2005) Mortality dynamics and population regulation in Bemisia tabaci. Entomol Exp Appl 116(2):93–108
Navas-Castillo J, Fiallo-Olivé E, Sánchez-Campos S (2011) Emerging virus diseases transmitted by whiteflies. Annu Rev Phytopathol 49:219–248
Ning W, Shi X, Liu B, Pan H, Wei W, Zeng Y, Sun X, Xie W, Wang S, Wu Q (2015) Transmission of tomato yellow leaf curl virus by Bemisia tabaci as affected by whitefly sex and biotype. Sci Rep 5:10744
Oliveira C, Auad A, Mendes S, Frizzas M (2014) Crop losses and the economic impact of insect pests on Brazilian agriculture. Crop Prot 56:50–54
Papayiannis LC, Iacovides TA, Katis N, Brown J (2010) Differentiation of tomato yellow leaf curl virus and tomato yellow leaf curl Sardinia virus using real-time TaqMan® PCR. J Virol Methods 165(2):238–245
Pedigo LP, Rice ME (2014) Entomology and pest management. Waveland
Pereira E, Picanço M, Bacci L, Crespo A, Guedes R (2007) Seasonal mortality factors of the coffee leafminer, Leucoptera coffeella. Bull Entomol Res 97(4):421–432
Queiroz PR, Lima LH, Sujii ER, Monnerat RG (2017) Description of the molecular profiles of Bemisia tabaci (Hemiptera: Aleyrodidae) in different crops and locations in Brazil. Journal of Entomology and Nematology 9(5):36–45
Queiroz PR, Martins ES, Klautau N, Lima L, Praça L, Monnerat RG (2016) Identification of the B, Q, and native Brazilian biotypes of the Bemisia tabaci species complex using scar markers. Pesq Agrop Brasileira 51(5):555–562
Ramos RS, Kumar L, Shabani F, Picanço MC (2018) Mapping global risk levels of Bemisia tabaci in areas of suitability for open field tomato cultivation under current and future climates. PLoS One 13(6):e0198925. https://doi.org/10.1371/journal.pone.0198925
Rosenzweig C, Iglesias A, Yang X, Epstein PR, Chivian E (2001) Climate change and extreme weather events; implications for food production, plant diseases, and pests. Glob. Chang. Hum. Health 2 (2):90–104
Simmons AM, Harrison HF, LING KS (2008) Forty-nine new host plant species for Bemisia tabaci (Hemiptera: Aleyrodidae). Entomol Sci 11(4):385–390
Stansly PA, McKenzie CL (2008) Fourth international Bemisia workshop international whitefly genomics workshop December 3–8, 2006, Duck Key, Florida, USA. J Insect Sci 8(4):1–54
Sutherst RW, Constable F, Finlay KJ, Harrington R, Luck J, Zalucki MP (2011) Adapting to crop pest and pathogen risks under a changing climate. Wiley Interdiscip Rev Clim Chang 2(2):220–237
Togni PH, Laumann RA, Medeiros MA, Sujii ER (2010) Odour masking of tomato volatiles by coriander volatiles in host plant selection of Bemisia tabaci biotype B. Entomol Exp Appl 136(2):164–173
Tomar S, Malik SSK (2017) Life parameters of whitefly (Bemisia tabaci, Genn.) on different host plants. Indian J Sci Res 16(1):34–37
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(6):e0130437
Xie W, Q-s M, Q-j W, S-l W, Yang X, N-n Y, Li R-m, X-g J, H-p P, B-m L (2012) Pyrosequencing the Bemisia tabaci transcriptome reveals a highly diverse bacterial community and a robust system for insecticide resistance. PLoS One 7(4):e35181
Zidon R, Tsueda H, Morin E, Morin S (2016) Projecting pest population dynamics under global warming: the combined effect of inter-and intra-annual variations. Ecol Appl 26(4):1198–1210
Acknowledgements
The simulations were carried out using the computational facilities at UNE. Mr. Phillip John Villani (B.A. from the University of Melbourne, Australia) revised and corrected the English language used in this manuscript.
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This research was supported by the National Council for Scientific and Technological Development (Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq)) and financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) of Brazil (Finance Code 001), the Minas Gerais State Foundation for Research Aid (FAPEMIG) and the School of Environmental and Rural Science of the University of New England (UNE), Armidale, Australia.
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RSR, RSS and MCP conceived of and designed the research. TAA, RSS and RSR contributed to conducting the experiments and acquiring the data. RSR analysed the data and wrote the manuscript with support from LK. LK and FS made the critical revisions (providing language help and writing assistance). LK and MCP made the critical revisions and approved the final version. All authors reviewed and approved the final manuscript.
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Ramos, R.S., Kumar, L., Shabani, F. et al. Climate model for seasonal variation in Bemisia tabaci using CLIMEX in tomato crops. Int J Biometeorol 63, 281–291 (2019). https://doi.org/10.1007/s00484-018-01661-2
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DOI: https://doi.org/10.1007/s00484-018-01661-2