Abstract
Public health and environmental concerns are increasing the pressure to reduce chemical pesticide usage, thereby requiring management alternatives to control pest damage to crops. Retaining semi-natural habitats within agricultural landscapes is often assumed to be one such alternative, by contributing to boost natural enemy populations and reduce pest abundance and spread. However, these potential benefits might be diluted or counteracted by intensive field management, thus limiting their effectiveness. We test these hypotheses, focusing on olive farming in southern Portugal, where we quantified the abundance of three pests, the olive fruit fly (Bactrocera oleae), olive moth (Prays oleae) and olive psyllid (Euphyllura olivina), and their parasitism and infestation rates in 17 orchards representing an intensification gradient and varying landscape cover by oak woodlands. Fly infestation was lower in more intensive orchards, there were no woodland effects, and parasitism was never detected. Psyllid infestation was also lower in more intensive orchards, but declined with woodland cover in more intensive orchards, while slightly increasing in less intensive ones. Psyllid parasitism rate could not be confidently estimated. Moth infestation declined with woodland cover in the most intensive orchards, while varying little in less intensive orchards. Moth parasitism rate declined with intensification and increased with woodland cover, particularly in less intensive orchards. Infestation by the moth was positively related to its abundance, albeit less so when parasitism rates were higher. Overall, our findings show mixed effects of oak woodlands, although retaining such habitats might still enhance biocontrol potential and reduce pressure by some pests, even under management intensification.
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The datasets generated and analysed during the current study are available from the corresponding author on reasonable request.
References
Albertini A, Pizzolotto R, Petacchi R (2017) Carabid patterns in olive orchards and woody semi-natural habitats: first implications for conservation biological control against Bactrocera oleae. Biocontrol 62:71–83. https://doi.org/10.1007/s10526-016-9780-x
Bakker L, van der Werf W, Bianchi FJJA (2021) No significant effects of insecticide use indicators and landscape variables on biocontrol in field margins. Agric Ecosyst Environ 308:107253. https://doi.org/10.1016/j.agee.2020.107253
Bartón K (2020) MuMIn: multi-model inference. https://CRAN.R-project.org/package=MuMIn
Bates D, Machler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. https://doi.org/10.18637/jss.v067.i01
Bugalho MN, Lecomte X, Gonçalves M et al (2011) Establishing grazing and grazing-excluded patches increases plant and invertebrate diversity in a Mediterranean oak woodland. For Ecol Manag 261:2133–2139. https://doi.org/10.1016/j.foreco.2011.03.009
Chaplin-Kramer R, O’Rourke ME, Blitzer EJ, Kremen C (2011) A meta-analysis of crop pest and natural enemy response to landscape complexity. Ecol Lett 14:922–932. https://doi.org/10.1111/j.1461-0248.2011.01642.x
Costa A, Silva B, Jiménez-Navarro G et al (2020) Structural simplification compromises the potential of common insectivorous bats to provide biocontrol services against the major olive pest Prays oleae. Agric Ecosyst Environ 287:106708. https://doi.org/10.1016/j.agee.2019.106708
Daane KM, Johnson MW (2010) Olive fruit fly: managing an ancient pest in modern times. Annu Rev Entomol 55:151–169. https://doi.org/10.1146/annurev.ento.54.110807.090553
Damalas CA (2016) Safe food production with minimum and judicious use of pesticides. In: Selamat J, Iqbal SZ (eds) Food safety. Springer, Cham, pp 43–55
Diez CM, Moral J, Cabello D et al (2016) Cultivar and tree density as key factors in the long-term performance of super high-density olive orchards. Front Plant Sci 7:1–13. https://doi.org/10.3389/fpls.2016.01226
Dimou I, Koutsikopoulos C, Economopoulos AP, Lykakis J (2003) Depth of pupation of the wild olive fruit fly, Bactrocera (Dacus) oleae (Gmel.) (Dipt., Tephritidae), as affected by soil abiotic factors. J Appl Entomol 127:12–17. https://doi.org/10.1046/j.1439-0418.2003.00686.x
Direção Geral de Alimentação e Veterinária (DGAV) (2017) Proteção integrada da cultura da oliveira. https://www.cothn.pt/publicfiles/lfjpcu5ybocfprq2fwooximhwmgu09laxbcoafmw.pdf
Direção-Geral do Território (2015) Carta de Uso e Ocupação do Solo de Portugal Continental para 2015 (COS2015). http://www.dgterritorio.pt/dados_abertos/cos/
Emmerson M, Morales MB, Oñate JJ et al (2016) How agricultural intensification affects biodiversity and ecosystem services. Adv Ecol Res 55:43–97. https://doi.org/10.1016/bs.aecr.2016.08.005
European Commission (2020) A farm to fork strategy for a fair, healthy and environmentally-friendly food system. Communication from the Commission to the European Parliament, the Council, the European Economic and Social Committee, and the Committee of the Regions. COM(2020) 381 final
FAOSTAT (2020) Food and agriculture organization of the United Nations. Statistics Division. https://www.fao.org/faostat/en/#data/QCL. Accessed 17 Feb 2022
Fox J, Weisberg S (2019) An R companion to applied regression. Sage, Thousand Oaks
Galloway AD, Seymour CL, Gaigher R, Pryke JS (2021) Organic farming promotes arthropod predators, but this depends on neighbouring patches of natural vegetation. Agric Ecosyst Environ 310:107295. https://doi.org/10.1016/j.agee.2020.107295
Garantonakis N, Varikou K, Markakis E et al (2016) Interaction between Bactrocera oleae (Diptera: Tephritidae) infestation and fruit mineral element content in Olea europaea (Lamiales: Oleaceae) cultivars of global interest. Appl Entomol Zool 51:257–265. https://doi.org/10.1007/s13355-016-0397-4
Gariepy TD, Haye T, Zhang J (2014) A molecular diagnostic tool for the preliminary assessment of host-parasitoid associations in biological control programmes for a new invasive pest. Mol Ecol 23:3912–3924. https://doi.org/10.1111/mec.12515
Gonçalves FM, Rodrigues MC, Pereira JA et al (2012) Natural mortality of immature stages of Bactrocera oleae (Diptera: Tephritidae) in traditional olive groves from north-eastern Portugal. Biocontrol Sci Technol 22:837–854. https://doi.org/10.1080/09583157.2012.691959
Gonzalez D, Cabral JA, Torres L, Santos M (2015) A cohort-based modelling approach for managing olive moth Prays oleae (Bernard, 1788) populations in olive orchards. Ecol Modell 296:46–56. https://doi.org/10.1016/j.ecolmodel.2014.10.012
Harrison XA (2015) A comparison of observation-level random effect and beta-binomial models for modelling overdispersion in Binomial data in ecology and evolution. PeerJ. https://doi.org/10.7717/peerj.1114
Hartig F (2022) DHARMa: residual diagnostics for hierarchical (multi-level/mixed) regression models. R package version 0.4.6. https://CRAN.R-project.org/package=DHARMa
Herrera JM, Silva B, Jiménez-Navarro G et al (2021) A food web approach reveals the vulnerability of biocontrol services by birds and bats to landscape modification at regional scale. Sci Rep 11:23662. https://doi.org/10.1038/s41598-021-02768-0
Hoelmer KA, Kirk AA, Pickett CH et al (2011) Prospects for improving biological control of olive fruit fly, Bactrocera oleae (Diptera: Tephritidae), with introduced parasitoids (Hymenoptera). Biocontrol Sci Technol 21:1005–1025. https://doi.org/10.1080/09583157.2011.594951
Holland JM, Douma JC, Crowley L et al (2017) Semi-natural habitats support biological control, pollination and soil conservation in Europe. A review. Agron Sustain Dev 37:31. https://doi.org/10.1007/s13593-017-0434-x
Karp DS, Chaplin-Kramer R, Meehan TD et al (2018) Crop pests and predators exhibit inconsistent responses to surrounding landscape composition. Proc Natl Acad Sci USA 115:E7863–E7870. https://doi.org/10.1073/pnas.1800042115
Lê S, Josse J, Husson F (2008) FactoMineR: an R package for multivariate analysis. J Stat Softw 25:1–18. https://doi.org/10.18637/jss.v025.i01
Lee R, den Uyl R, Runhaar H (2020) Assessment of policy instruments for pesticide use reduction in Europe; learning from a systematic literature review. Crop Prot 126:104929. https://doi.org/10.1016/j.cropro.2019.104929
Lefcheck JS (2016) piecewiseSEM: piecewise structural equation modelling in r for ecology, evolution, and systematics. Methods Ecol Evol 7:573–579. https://doi.org/10.1111/2041-210X.12512
Malheiro R, Casal S, Baptista P, Pereira JA (2015) A review of Bactrocera oleae (Rossi) impact in olive products: from the tree to the table. Trends Food Sci Technol 44:226–242. https://doi.org/10.1016/j.tifs.2015.04.009
Martínez-Núñez C, Rey PJ, Manzaneda AJ et al (2020) Direct and indirect effects of agricultural practices, landscape complexity and climate on insectivorous birds, pest abundance and damage in olive groves. Agric Ecosyst Environ 304:107145. https://doi.org/10.1016/j.agee.2020.107145
Martínez-Núñez C, Rey PJ, Manzaneda AJ et al (2021) Insectivorous birds are not effective pest control agents in olive groves. Basic Appl Ecol 56:270–280. https://doi.org/10.1016/j.baae.2021.08.006
Mata VA, da Silva LP, Veríssimo J et al (2021) Combining DNA metabarcoding and ecological networks to inform conservation biocontrol by small vertebrate predators. Ecol Appl 31:1–15. https://doi.org/10.1002/eap.2457
Miranda MA, Miquel M, Terrassa J et al (2008) Parasitism of Bactrocera oleae (Diptera; Tephritidae) by Psyttalia concolor (Hymenoptera; Braconidae) in the Balearic Islands (Spain). J Appl Entomol 132:798–805. https://doi.org/10.1111/j.1439-0418.2008.01358.x
Moreno A, Rescia AJ, Pascual S, Ortega M (2022) Methodological approach to spatial analysis of agricultural pest dispersal in olive landscapes. Environ Monit Assess. https://doi.org/10.1007/s10661-022-10068-x
Morgado R, Santana J, Porto M et al (2020) A Mediterranean silent spring? The effects of olive farming intensification on breeding bird communities. Agric Ecosyst Environ 288:106694. https://doi.org/10.1016/j.agee.2019.106694
Morgado R, Pedroso R, Porto M et al (2021) Preserving wintering frugivorous birds in agro-ecosystems under land use change: lessons from intensive and super-intensive olive orchards. J Appl Ecol 58:2975–2986. https://doi.org/10.1111/1365-2664.14029
Morgado R, Ribeiro PF, Santos JL et al (2022) Drivers of irrigated olive grove expansion in Mediterranean landscapes and associated biodiversity impacts. Landsc Urban Plan 225:104429. https://doi.org/10.1016/j.landurbplan.2022.104429
Morris TI, Campos M, Kidd NAC, Symondson WOC (1999) What is consuming Prays oleae (Bernard) (Lep.: Yponomeutidae) and when: a serological solution? Crop Prot 18:17–22. https://doi.org/10.1016/S0261-2194(98)00083-0
Muneret L, Thiéry D, Joubard B, Rusch A (2018) Deployment of organic farming at a landscape scale maintains low pest infestation and high crop productivity levels in vineyards. J Appl Ecol 55:1516–1525. https://doi.org/10.1111/1365-2664.13034
Nardi F, Carapelli A, Dallai R et al (2005) Population structure and colonization history of the olive fly, Bactrocera oleae (Diptera, Tephritidae). Mol Ecol 14:2729–2738. https://doi.org/10.1111/j.1365-294X.2005.02610.x
Ortega M, Pascual S (2014) Spatio-temporal analysis of the relationship between landscape structure and the olive fruit fly Bactrocera oleae (Diptera: Tephritidae). Agric for Entomol 16:14–23. https://doi.org/10.1111/afe.12030
Ortega M, Moreno N, Fernández CE, Pascual S (2022) Olive landscape affects Bactrocera oleae abundance, movement and infestation. Agronomy 12:1–15. https://doi.org/10.3390/agronomy12010004
Paredes D, Cayuela L, Gurr GM, Campos M (2013) Effect of non-crop vegetation types on conservation biological control of pests in olive groves. PeerJ 1:e116. https://doi.org/10.7717/peerj.116
Paredes D, Karp DS, Chaplin-Kramer R et al (2019) Natural habitat increases natural pest control in olive groves: economic implications. J Pest Sci 92:1111–1121. https://doi.org/10.1007/s10340-019-01104-w
Picchi MS, Bocci G, Petacchi R, Entling MH (2016) Effects of local and landscape factors on spiders and olive fruit flies. Agric Ecosyst Environ 222:138–147. https://doi.org/10.1016/j.agee.2016.01.045
Pinto-Correia T, Ribeiro N, Sá-Sousa P (2011) Introducing the montado, the cork and holm oak agroforestry system of Southern Portugal. Agrofor Syst 82:99–104. https://doi.org/10.1007/s10457-011-9388-1
Rand TA, Waters DK, Blodgett SL et al (2014) Increased area of a highly suitable host crop increases herbivore pressure in intensified agricultural landscapes. Agric Ecosyst Environ 186:135–143. https://doi.org/10.1016/j.agee.2014.01.022
R Core Team (2022) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Ricci B, Lavigne C, Alignier A et al (2019) Local pesticide use intensity conditions landscape effects on biological pest control. Proc R Soc B Biol Sci. https://doi.org/10.1098/rspb.2018.2898
Riggi LGA, Bommarco R (2019) Subsidy type and quality determine direction and strength of trophic cascades in arthropod food webs in agroecosystems. J Appl Ecol 56:1982–1991. https://doi.org/10.1111/1365-2664.13444
Rodríguez-Cohard JC, Sánchez-Martínez JD, Garrido-Almonacid A (2020) Strategic responses of the European olive-growing territories to the challenge of globalization. Eur Plan Stud 28:2261–2283. https://doi.org/10.1080/09654313.2020.1716691
Santos SAP, Pereira JA, Torres LM, Nogueira AJA (2007) Evaluation of the effects, on canopy arthropods, of two agricultural management systems to control pests in olive groves from north-east of Portugal. Chemosphere 67:131–139. https://doi.org/10.1016/j.chemosphere.2006.09.014
Shipley B (2009) Confirmatory path analysis in a generalized multilevel context. Ecology 90:363–368. https://doi.org/10.1890/08-1034.1
Silveira A, Ferrão J, Muñoz-Rojas J et al (2018) The sustainability of agricultural intensification in the early 21st century: insights from the olive oil production in Alentejo (Southern Portugal). Changing Societies: Legacies and Challenges. The Diverse Worlds of Sustainability, pp 247–275. https://doi.org/10.31447/ics9789726715054.10
Skouras PJ, Margaritopoulos JT, Seraphides NA et al (2007) Organophosphate resistance in olive fruit fly, Bactrocera oleae, populations in Greece and Cyprus. Pest Manag Sci 63:42–48. https://doi.org/10.1002/ps.1306
Sow A, Brévault T, Benoit L et al (2019) Deciphering host-parasitoid interactions and parasitism rates of crop pests using DNA metabarcoding. Sci Rep 9:1–12. https://doi.org/10.1038/s41598-019-40243-z
Tamburini G, De Simone S, Sigura M et al (2016) Conservation tillage mitigates the negative effect of landscape simplification on biological control. J Appl Ecol 53:233–241. https://doi.org/10.1111/1365-2664.12544
Thies C, Roschewitz I, Tscharntke T (2005) The landscape context of cereal aphid–parasitoid interactions. Proc R Soc B Biol Sci 272:203–210. https://doi.org/10.1098/rspb.2004.2902
Tilman D, Clark M (2014) Global diets link environmental sustainability and human health. Nature 515:518–522. https://doi.org/10.1038/nature13959
Tscharntke T, Karp DS, Chaplin-Kramer R et al (2016) When natural habitat fails to enhance biological pest control: five hypotheses. Biol Conserv 204:449–458. https://doi.org/10.1016/j.biocon.2016.10.001
Vasconcelos S, Pina S, Herrera JM et al (2022) Canopy arthropod declines along a gradient of olive farming intensification. Sci Rep 12:17273. https://doi.org/10.1038/s41598-022-21480-1
Veres A, Petit S, Conord C, Lavigne C (2013) Does landscape composition affect pest abundance and their control by natural enemies? A review. Agric Ecosyst Environ 166:110–117. https://doi.org/10.1016/j.agee.2011.05.027
Villa M, Santos SAP, Mexia A et al (2016) Ground cover management affects parasitism of Prays oleae (Bernard). Biol Control 96:72–77. https://doi.org/10.1016/j.biocontrol.2016.01.012
Wang XG, Nadel H, Johnson MW et al (2009) Crop domestication relaxes both top-down and bottom-up effects on a specialist herbivore. Basic Appl Ecol 10:216–227. https://doi.org/10.1016/j.baae.2008.06.003
Wittwer RA, Bender SF, Hartman K et al (2021) Organic and conservation agriculture promote ecosystem multifunctionality. Sci Adv 7:1–13. https://doi.org/10.1126/sciadv.abg6995
Zuur AF, Hilbe JM, Ieno EN (2013) Beginner’s guide to GLM and GLMM with R: a frequentist and Bayesian perspective for ecologists. Highland Statistics Ltd, Aberdeenshire
Acknowledgements
We are grateful to the landowners and managers for granting us access to the surveyed orchards, to Mar Ferrer Suay for confirming the identity of a charipine wasp, Miguel Porto for advice on statistical analysis, and Juan Pablo Cancela for the pest drawings.
Funding
This study was funded by the Portuguese Foundation for Science and Technology (FCT) under PTDC/AAG-REC/6480/2014. SV, RH, JMH, FM, BS and GJ-N were supported by FCT Grants/Contracts SFRH/BD/121388/2016, UID/BIA/04004/2021, IF/00001/2015, IF/01053/2015, SFRH/BD/137803/2018 and SFRH/BD/133017/2017, respectively. JMH is currently granted with a María Zambrano contract (University of Cádiz, Ministry of Universities, Recovery, Transformation, and Resilience Plan – Funded by the European Union – Next Generation EU). PB was supported by EDP Biodiversity Chair and MJ by SLU Centre for Biological Control. Work was co-funded by the Project NORTE-01-0246-FEDER-000063, supported by Norte Portugal Regional Operational Programme (NORTE2020), under the PORTUGAL 2020 Partnership Agreement, through the European Regional Development Fund (ERDF).
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Vasconcelos, S., Pina, S., Jonsson, M. et al. Mixed effects of oak woodlands on biocontrol potential and pest pressure in olive orchards under management intensification. J Pest Sci 97, 355–368 (2024). https://doi.org/10.1007/s10340-023-01634-4
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DOI: https://doi.org/10.1007/s10340-023-01634-4