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Oscillation, synchrony, and multi-factor patterns between cereal aphids and parasitoid populations in southern Brazil

Published online by Cambridge University Press:  06 September 2021

Eduardo Engel Open the ORCID record for Eduardo Engel [Opens in a new window] ,
Douglas Lau ,
Wesley A. C. Godoy ,
Mauricio P. B. Pasini ,
José B. Malaquias ,
Carlos D. R. Santos ,
Juliana Pivato  and
Paulo R. V. da S. Pereira
Eduardo Engel*
Affiliation:
Department of Entomology and Acarology, Laboratory of Ecology and Forest Entomology, University of São Paulo, ESALQ, Piracicaba, São Paulo, Brazil
Douglas Lau
Affiliation:
Brazilian Agricultural Research Corporation (Embrapa Trigo), Passo Fundo, Rio Grande do Sul, Brazil
Wesley A. C. Godoy
Affiliation:
Department of Entomology and Acarology, Laboratory of Ecology and Forest Entomology, University of São Paulo, ESALQ, Piracicaba, São Paulo, Brazil
Mauricio P. B. Pasini
Affiliation:
Laboratory of Entomology, University of Cruz Alta-Unicruz, Cruz Alta, Rio Grande do Sul, Brazil
José B. Malaquias
Affiliation:
Department of Biostatistics, Institute of Biosciences – IBB, São Paulo State University (UNESP), Botucatu, São Paulo, Brazil
Carlos D. R. Santos
Affiliation:
Faculty of Agronomy, Postgraduate Program in Plant Science, Federal University of Rio Grande do Sul (UFRGS), Porto Alegre, Rio Grande do Sul, Brasil
Juliana Pivato
Affiliation:
Faculty of Agronomy, Postgraduate Program in Plant Science, Federal University of Rio Grande do Sul (UFRGS), Porto Alegre, Rio Grande do Sul, Brasil
Paulo R. V. da S. Pereira
Affiliation:
Brazilian Agricultural Research Corporation (Embrapa Florestas), Colombo, Paraná, Brazil
*
Author for correspondence: Eduardo Engel, Email: agron.engel@gmail.com
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Abstract

In different parts of the world, aphid populations and their natural enemies are influenced by landscapes and climate. In the Neotropical region, few long-term studies have been conducted, maintaining a gap for comprehension of the effect of meteorological variables on aphid population patterns and their parasitoids in field conditions. This study describes the general patterns of oscillation in cereal winged aphids and their parasitoids, selecting meteorological variables and evaluating their effects on these insects. Aphids exhibit two annual peaks, one in summer–fall transition and the other in winter-spring transition. For parasitoids, the highest annual peak takes place during winter and a second peak occurs in winter–spring transition. Temperature was the principal meteorological regulator of population fluctuation in winged aphids and parasitoids during the year. The favorable temperature range is not the same for aphids and parasitoids. For aphids, temperature increase resulted in population growth, with maximum positive effect at 25°C. Temperature also positively influenced parasitoid populations, but the growth was asymptotic around 20°C. Although rainfall showed no regulatory function on aphid seasonality, it influenced the final number of insects over the year. The response of aphids and parasitoids to temperature has implications for trophic compatibility and regulation of their populations. Such functions should be taken into account in predictive models.

Keywords

Aphididaebiological controlBraconidaecommunity ecologypopulation dynamicstrophic levels
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 112 , Issue 2 , April 2022 , pp. 143 - 150
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Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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References

Akaike, H (1973) Information theory and an extension of the maximum likelihood principle. (BN Petrov and F Csaki, Eds.), Budapest, Hungary CL – 2nd International Symposium on Information Theory, Tsahkadsor, Armenia, USSR, September 2–8, 1971: Akadémiai Kiadó, pp. 267–281.Google Scholar
Alford, L, Andrade, TO, Georges, R, Burel, F and Van Baaren, J (2014) Could behaviour and not physiological thermal tolerance determine winter survival of aphids in cereal fields? PLoS ONE 9, 1–16.CrossRefGoogle Scholar
Andrade, TO, Krespi, L, Bonnardot, V, van Baaren, J and Outreman, Y (2016) Impact of change in winter strategy of one parasitoid species on the diversity and function of a guild of parasitoids. Oecologia 180, 877–888.CrossRefGoogle ScholarPubMed
Auad, AM, Alves, SO, Carvalho, CA, Silva, DM, Resende, TT and Veríssimo, BA (2009) The impact of temperature on biological aspects and life table of Rhopalosiphum padi (Hemiptera: Aphididae) fed with signal grass. Florida Entomologist 92, 569–577.CrossRefGoogle Scholar
Basheer, A, Aslan, L and Asaad, R (2014) Effect of constant temperatures on the development of the aphid parasitoid species, Diaeretiella rapae (M'intosh) (Hymenoptera: Aphidiidae). Egyptian Journal of Biological Pest Control 24, 1–5.Google Scholar
Bell, JR, Alderson, L, Izera D, Kruger T, Parker S, Pickup J, Shortall CR, Taylor MS, Verrier P and Harrington, R (2015) Long-term phenological trends, species accumulation rates, aphid traits and climate: five decades of change in migrating aphids. Journal of Animal Ecology 84, 21–34.CrossRefGoogle ScholarPubMed
Brewer, MJ, Peairs, FB and Elliott, NC (2019) Invasive cereal aphids of North America: ecology and pest management. Annual Review of Entomology 64, 73–93.CrossRefGoogle ScholarPubMed
Carvalho, FJ, de Santana, DG and Sampaio, MV (2020) Modeling overdispersion, autocorrelation, and zero-inflated count data via generalized additive models and Bayesian statistics in an aphid population study. Neotropical Entomology 49, 40–51.CrossRefGoogle Scholar
Chamuene, A, Araújo, TA, Silva, G, Costa, TL, Berger, PG and Picanço, MC (2018) Performance of the natural mortality factors of Aphis gossypii (hemiptera: Aphididae) as a function of cotton plant variety and phenology. Environmental Entomology 47, 440–447.CrossRefGoogle ScholarPubMed
Dedryver, CA, Le Ralec, A and Fabre, F (2010) The conflicting relationships between aphids and men: a review of aphid damage and control strategies. Comptes Rendus – Biologies 333, 539–553.CrossRefGoogle ScholarPubMed
Fidelis, EG, Farias, ES, Lopes, MC, Sousa, FF, Zanuncio, JC and Picanço, MC (2019) Contributions of climate, plant phenology and natural enemies to the seasonal variation of aphids on cabbage. Journal of Applied Entomology 143, 365–370.CrossRefGoogle Scholar
Finlay, KJ and Luck, JE (2011) Response of the bird cherry-oat aphid (Rhopalosiphum padi) to climate change in relation to its pest status, vectoring potential and function in a crop-vector-virus pathosystem. Agriculture, Ecosystems and Environment 144, 405–421.CrossRefGoogle Scholar
Furlong, MJ and Zalucki, MP (2017) Climate change and biological control: the consequences of increasing temperatures on host–parasitoid interactions. Current Opinion in Insect Science 20, 39–44.CrossRefGoogle ScholarPubMed
Harrington, R, Clark, SJ, Welham, SJ, Verrier, PJ, Denholm, CH, Hullé, M, Maurice, D, Rounsevell, MD and Cocu, N (2007) Environmental change and the phenology of European aphids. Global Change Biology 13, 1550–1564.CrossRefGoogle Scholar
Holloway, P, Kudenko, D and Bell, JR (2018) Dynamic selection of environmental variables to improve the prediction of aphid phenology: a machine learning approach. Ecological Indicators 88, 512–521.CrossRefGoogle Scholar
Honek, A, Martinkova, Z, Saska, P and Dixon, AFG (2018) Aphids (Homoptera: Aphididae) on winter wheat: predicting maximum abundance of Metopolophium dirhodum. Journal of Economic Entomology 111, 1751–1759.CrossRefGoogle ScholarPubMed
Jerbi-Elayed, M, Lebdi-Grissa, K, Le Goff, G and Hance, T (2015) Influence of temperature on flight, walking and oviposition capacities of two aphid parasitoid species (Hymenoptera: Aphidiinae). Journal of Insect Behavior 28, 157–166.CrossRefGoogle Scholar
Jonsson, M, Buckley, HL, Case, BS, Wratten, SD, Hale, RJ and Didham, RK (2012) Agricultural intensification drives landscape-context effects on host-parasitoid interactions in agroecosystems. Journal of Applied Ecology 49, 706–714.Google Scholar
Kaiser, HF (1974) An index of factorial simplicity. Psychometrika 39, 31–36.CrossRefGoogle Scholar
Lê, S, Josse, J and Husson, F (2008) FactoMineR: an R package for multivariate analysis. Journal of Statistical Software 25, 1–18.CrossRefGoogle Scholar
Leslie, TW, Van Der Werf, W, Bianchi, FJJA and Honěk, A (2009) Population dynamics of cereal aphids: influence of a shared predator and weather. Agricultural and Forest Entomology 11, 73–82.CrossRefGoogle Scholar
Malaquias, JB, Ramalho, FS, Dias, CTDS, Brugger, BP, Lira, ACS, Wilcken, CF, Pachú, JKS and Zanucio, JC (2017) Multivariate approach to quantitative analysis of Aphis gossypii Glover (Hemiptera: Aphididae) and their natural enemy populations at different cotton spacings. Scientific Reports 7, 1–11.CrossRefGoogle ScholarPubMed
MAPA (2008) Portaria no 43/2008. Regionalização para épocas de semeadura de trigo e triticale Estado do Rio Grande do Sul.Google Scholar
Meisner, MH, Harmon, JP and Ives, AR (2014) Temperature effects on long-term population dynamics in a parasitoid-host system. Ecological Monographs 84, 457–476.CrossRefGoogle Scholar
Moiroux, J, Boivin, G and Brodeur, J (2015) Temperature influences host instar selection in an aphid parasitoid: support for the relative fitness rule. Biological Journal of the Linnean Society 115, 792–801.CrossRefGoogle Scholar
Ovaskainen, O, Skorokhodova, S, Yakovleva, M, Sukhov, A, Kutenkov, A, Kutenkova, N, Shcherbakov, A, Meyke, E and Delgado, DMM (2013) Community-level phenological response to climate change. Proceedings of the National Academy of Sciences of the USA 110, 13434–13439.CrossRefGoogle ScholarPubMed
Parizoto, G, Rebonatto, A, Schons, J and Lau, D (2013) Barley yellow dwarf virus-PAV in Brazil: seasonal fluctuation and biological characteristics. Tropical Plant Pathology 38, 11–19.CrossRefGoogle Scholar
Pennachio, F (1989) The Italian species of the genus Aphidius Nees (Hymenoptera, Braconidae, Aphidiinae). Bollettino Del Laboratorio Di Entomologia Agraria Filippo Silvestri 46, 75–106.Google Scholar
Pereira, PRVDS, Salvatori, JR and Lau, D (2009) Identificação de adultos ápteros e alados das principais espécies de afídeos (Hemiptera: Aphididae) associadas a cereais de inverno no Brasil. Passo Fundo: Embrapa Trigo, (December), 17.Google Scholar
Pérez, N, Seco, MV, Valenciano, JB and Lorenzana, A (2007) Use of suction-trap and moericke traps for monitoring the migration of damson-hop aphid (Phorodon humuli) (Hemiptera, aphididae). New Zealand Journal of Crop and Horticultural Science 35, 455–461.CrossRefGoogle Scholar
Rebonatto, A, Salvadori, JR and Lau, D (2015) Temporal changes in cereal aphids (Hemiptera: Aphididae) populations in Northern Rio Grande do Sul, Brazil. Journal of Agricultural Science 7, 71–78.CrossRefGoogle Scholar
Santos, CDRD, Sampaio, MV, Lau, D, Redaelli, LR, Jahnke, S, Pivato, J and Carvalho, FJ (2019) Taxonomic status and population oscillations of Aphidius colemani species group (Hymenoptera: Braconidae) in Southern Brazil. Neotropical Entomology 48, 983–991.CrossRefGoogle Scholar
Soares, JRS, da Silva Paes, J, de Araújo, VCR, de Araújo, TA, Ramos, RS, Picanço, MC and Zanucio, JC (2020) Spatiotemporal dynamics and natural mortality factors of Myzus persicae (Sulzer) (Hemiptera: Aphididae) in bell pepper crops. Neotropical Entomology 49(3), 445–455. doi: 10.1007/s13744-020-00761-2CrossRefGoogle Scholar
Starý, P and Lukáš, J (2009) Aphid parasitoids and their tritrophic associations in Slovakia (Hymenoptera: Braconidae, Aphidiinae). Bratislava: Folia Hymenopterologica Slovaca 1, 1–63.Google Scholar
Tomanović, Ž, Kavallieratos, NG, Starý, P, Athanassiou, CG, Žikic, V, Petrovic-Obradovic, O and Sarlis, GP (2003) Aphidius nees aphid parasitoids (Hymenoptera, Braconidae, Aphidiinae) in Serbia and Montenegro: tritrophic associations and key. Acta Entomologica Serbica 8, 15–39.Google Scholar
Tomanovic, Ž, Petrovic, A, Mitrovic, M, Kavallieratos, NG, Starý, P, Rakhshani, E, Rakhshanipour, M, Popovic, A, Shukshuk, AH and Ivanovic, A (2014) Molecular and morphological variability within the Aphidius colemani group with redescription of Aphidius platensis Brethes (Hymenoptera: Braconidae: Aphidiinae). Bulletin of Entomological Research 104, 552–565. doi: 10.1017/S0007485314000327CrossRefGoogle Scholar
Tomanović, Ž, Mitrovic, M, Petrovic, A, Kavallieratos, NG, Zikic, V, Ivanovic, A, Rakhshani, E, Starý, P and Vorbugue, C (2018) Revision of the European Lysiphlebus species (Hymenoptera: Braconidae: Aphidiinae) on the basis of COI and 28SD2 molecular markers and morphology. Arthropod Systematics & Phylogeny 76(2), 179–213.Google Scholar
Tougeron, K, Damien, M, Lann, CL, Brodeur, J and van Baaren, J (2018) Rapid responses of winter aphid-parasitoid communities to climate warming. Frontiers in Ecology and Evolution 6, 1–9.CrossRefGoogle Scholar
Tougeron, K, Brodeur, J, Le Lann, C and van Baaren, J (2019) How climate change affects the seasonal ecology of insect parasitoids. Ecological Entomology 45(2), 167–181. doi: 10.1111/een.12792CrossRefGoogle Scholar
Valério, DA, Tres, A, Tetto, AF, Soares, RV and Wendling, WT (2018) Holdridge life zone classification for the southern Brazilian state ‘Rio grande do sul’. Ciencia Florestal 28, 1776–1788.CrossRefGoogle Scholar
Van den Eynde, R, Van Leeuwen, T and Haesaert, G (2020) Identifying drivers of spatio-temporal dynamics in barley yellow dwarf virus epidemiology as a critical factor in disease control. Pest Management Science 76, 2548–2556. doi: 10.1002/ps.5851CrossRefGoogle ScholarPubMed
Wang, L, Hui, C, Sandhu, HS, Li, Z and Zhao, Z (2015) Population dynamics and associated factors of cereal aphids and armyworms under global change. Scientific Reports 5, 1–8.Google ScholarPubMed
Werner, CM, Stuble, KL, Groves, AM and Young, TP (2020) Year effects: interannual variation as a driver of community assembly dynamics. Ecology 101, 0–2.CrossRefGoogle ScholarPubMed
Wiest, R, Salvadori, JR, Fernandes, JMC, Lau, D, Pavan, W, Zanini, W, Toebe, J and Lazzaretti, AT (2020) Population growth of Rhopalosiphum padi under different thermalregimes: an agent-based model approach. Agricultural and Forest Entomology 23, 59–69. doi: 10.1111/afe.12404CrossRefGoogle Scholar
Wood, S (2017) Generalized Additive Models: An Introduction with R, 2ed. Boca Raton: Chapman & Hall/CRC, pp. 1–467.CrossRefGoogle Scholar
Yang, F, Xu, L, Wu, YK, Wang, Q, Yao, ZW, Žikić, V, Tomanović, Z, Ferrer-Suay, M, Selfa, J, Pujade-Villar, J, Traugott, M, Desneux, N, Lu, YH and Guo, YY (2017) Species composition and seasonal dynamics of aphid parasitoids and hyperparasitoids in wheat fields in northern China. Scientific Reports 7, 1–9. doi: 10.1038/s41598-017-14441-6Google ScholarPubMed
Zhao, ZH and Reddy, GVP (2019) Semi-natural habitats mediate influence of inter-annual landscape variation on cereal aphid-parasitic wasp system in an agricultural landscape. Biological Control 128, 17–23.CrossRefGoogle Scholar