Abstract
Diversifying crop habitats and controlling arthropod pests by cultivating “secondary plants” alongside a primary crop is a frequently discussed strategy. The effectiveness of using secondary plants to manage pests varies across countries, and is influenced by factors such as the target pest, plant species, experimental design, and climatic conditions. Consequently, we conducted a study investing the impact of intercropping wheat or barley with additional flower strips on controlling aphid pests in white cabbage fields in Japan and Germany.Query Our results in Japan supported the natural enemies hypothesis, leading to a significant reduction in populations of two pest aphids: the green peach aphid, Myzus persicae (Sulzer) (Hemiptera: Aphididae), and the cabbage aphid, Brevicoryne brassicae (L.) (Hemiptera: Aphididae). Furthermore, intercropping and/or flower strips increased the proportions of natural enemies, including hoverfly larvae (Diptera: Syrphidae), ladybirds (Coccinellidae: Coleoptera), and parasitoid wasps (Hymenoptera: Braconidae), relative to the aphids. Hoverfly larvae, due to their high abundance, appeared to be Japan’s most effective aphid suppressors. In contrast, in Germany, intercropping and flower strips did not remarkably suppress aphid populations or enhance the presence of the natural enemies, despite a temporary increase in the population density of hoverfly larvae in intercropping. These disparities between the trials in the two countries may be attributed to variations in regional and local biodiversity. This suggests that using secondary plants for pest control should consider the specificities of local environments.
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References
Almohamad R, Verheggen FJ, Haubruge E (2009) Searching and oviposition behavior of aphidophagous hoverflies (Diptera: Syrphidae): a review. Biotechnol Agron Soc 13:467–481
Aziz M, Mahmood A, Asif M, Ali A (2015) Wheat-based intercropping: a review. J Anim Plant Sci 25:896–907
Bates D, Mächler M, Bolker BM, Walker SC (2015) Fitting linear mixed effects models using lme4. J Stat Softw 67(1):48
Bhatia V, Uniyal PL, Bhattacharya R (2011) Aphid resistance in Brassica crops: challenges, biotechnological progress and emerging possibilities. Biotechnol Adv 29:879–888. https://doi.org/10.1016/j.biotechadv.2011.07.005
Bianchi F, Schellhorn NA, van der Werf W (2009) Predicting the time to colonization of the parasitoid Diadegma semiclausum: the importance of the shape of spatial dispersal kernels for biological control. Biol Control 50:267–274. https://doi.org/10.1016/j.biocontrol.2009.04.014
Brennan EB (2016) Agronomy of strip intercropping broccoli with alyssum for biological control of aphids. Biol Control 97:109–119. https://doi.org/10.1016/j.biocontrol.2016.02.015
Canty A, Ripley BD (2022) boot: Bootstrap R (S-Plus) Functions. R package version 1.3–30
Edwards OR, Franzmann B, Thackray D, Micic S (2008) Insecticide resistance and implications for future aphid management in Australian grains and pastures: a review. Aust J Exp Agric 48:1523–1530
Fidelis EG, do Carmo DD, Santos AA, Farias ED, da Silva RS, Picanço MC, (2018) Coccinellidae, syrphidae and <i>aphidoletes</i> are key mortality factors for <i>myzus persicae</i> in tropical regions: A case study on cabbage crops. Crop Prot 112:288–294. https://doi.org/10.1016/j.cropro.2018.06.015
Finch S, Collier RH (2000) Host-plant selection by insects––a theory based on “appropriate/inappropriate landings” by pest insects of cruciferous plants. Entomol Exp Appl 96:91–102. https://doi.org/10.1046/j.1570-7458.2000.00684.x
Fox J, Weisberg S (2018) An R Companion to Applied Regression, 3rd edn. Sage Publications, Thousand Oaks, CA
Gómez-Marco F, Urbaneja A, Tena A (2016) A sown grass cover enriched with wild forb plants improves the biological control of aphids in citrus. Basic Appl Ecol 17:210–219. https://doi.org/10.1016/j.baae.2015.10.006
Hahn PG, Cammarano JH (2023) Environmental context and herbivore traits mediate the strength of associational effects in a meta-analysis of crop diversity. J Appl Ecol 60:875–885. https://doi.org/10.1111/1365-2664.14382
Hartwig NL, Ammon HU (2002) 50th Anniversary––invited article––cover crops and living mulches. Weed Sci 50:688–699. https://doi.org/10.1614/0043-1745(2002)050[0688:aiacca]2.0.co;2
Holland JM, Bianchi F, Entling MH, Moonen AC, Smith BM, Jeanneret P (2016) Structure, function and management of semi-natural habitats for conservation biological control: a review of European studies. Pest Manag Sci 72:1638–1651. https://doi.org/10.1002/ps.4318
Horwith B (1985) A role for intercropping in modern agriculture. Bioscience 35:286–291. https://doi.org/10.2307/1309927
Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50:346–363. https://doi.org/10.1002/bimj.200810425
Jamont M, Dubois-Pot C, Jaloux B (2014) Nectar provisioning close to host patches increases parasitoid recruitment, retention and host parasitism. Basic Appl Ecol 15:151–160. https://doi.org/10.1016/j.baae.2014.01.001
Jankowska B, Poniedziałek M, Jędrszczyk E (2009) Effect of intercropping white cabbage with FrenchMarigold (Tagetes patula nana L.) and Pot Marigold (Calendula officinalis L.) on the colonization of plantsby pest insects. Folia Hort 21:95–103. https://doi.org/10.2478/fhort-2013-0129
Köneke A, Uesugi R, Herz A, Tabuchi K, Yoshimura H, Shimoda T, Nagasaka K, Böckmann E (2023) Effects of wheat undersowing and sweet alyssum intercropping on aphid and flea beetle infestation in white cabbage in Germany and Japan. J Plant Dis Prot 130:619–631. https://doi.org/10.1007/s41348-023-00730-y
Landis DA, Wratten SD, Gurr GM (2000) Habitat management to conserve natural enemies of arthropod pests in agriculture. Annu Rev Entomol 45:175–201. https://doi.org/10.1146/annurev.ento.45.1.175
Laubertie EA, Wratten SD, Hemptinne JL (2012) The contribution of potential beneficial insectary plant species to adult hoverfly (Diptera: Syrphidae) fitness. Biol Control 61:1–6. https://doi.org/10.1016/j.biocontrol.2011.12.010
Lopes T, Bodson B, Francis F (2015) Associations of wheat with pea can reduce aphid infestations. Neotrop Entomol 44:286–293. https://doi.org/10.1007/s13744-015-0282-9
Lopes T, Hatt S, Xu QX, Chen JL, Liu Y, Francis F (2016) Wheat (Triticum aestivum L.)-based intercropping systems for biological pest control. Pest Manag Sci 72:2193–2202. https://doi.org/10.1002/ps.4332
Macfadyen S, Davies AP, Zalucki MP (2015) Assessing the impact of arthropod natural enemies on crop pests at the field scale. Insect Sci 22:20–34. https://doi.org/10.1111/1744-7917.12174
Meyling NV, Navntoft S, Philipsen H, Thorup-Kristensen K, Eilenberg J (2013) Natural regulation of Delia radicum in organic cabbage production. Agric Ecosyst Environ 164:183–189. https://doi.org/10.1016/j.agee.2012.09.019
Parolin P, Bresch C, Desneux N, Brun R, Bout A, Boll R, Poncet C (2012) Secondary plants used in biological control: a review. Int J Pest Manage 58:91–100. https://doi.org/10.1080/09670874.2012.659229
Piñero JC, Manandhar R (2015) Effects of increased crop diversity using trap crops, flowering plants, and living mulches on vegetable insect pests. Trends Entomol 11:91–109
Ponti L, Altieri MA, Gutierrez AP (2007) Effects of crop diversification levels and fertilization regimes on abundance of Brevicoryne brassicae (L.) and its parasitization by Diaeretiella rapae (M’Intosh) in broccoli. Agric for Entomol 9:209–214
Prabhakar AK, Roy SP (2010) Evaluation of the consumption rates of dominant coccinellid predators on aphids in north-east bihar. Bioscan 5:491–493
R_Core_Team (2022) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Rodríguez-Gasol N, Alins G, Veronesi ER, Wratten S (2020) The ecology of predatory hoverflies as ecosystem-service providers in agricultural systems. Biol Control 151:104405
Root RB (1973) Organization of a plant-arthropod association in simple and diverse habitats: the fauna of collards (Brassica oleracea). Ecol Monogr 43:95–120. https://doi.org/10.2307/1942161
Safarzoda S, Bahlai CA, Fox AF, Landis DA (2014) The role of natural enemy foraging guilds in controlling cereal aphids in michigan wheat. PLoS ONE 9:17. https://doi.org/10.1371/journal.pone.0114230
Sarwar M (2011) Effects of wheat and barley intercropping ecosystem on the prevalence of aphid Hemiptera: Aphididae population in canola Brassica napus L. crop. Biol Divers Conserv 4:11–16
Scott SM, Barlow CA (1990) Effect of hunger on the allocation of time among pea-plants by the larvae of an aphidophagous hover fly, Eupeodes corollae [Dipt, Syrphidae]. Entomophaga 35:163–172. https://doi.org/10.1007/bf02374790
Sheehan W (1986) Response by specialist and generalist natural enemies to agroecosystem diversification—a selective review. Environ Entomol 15:456–461. https://doi.org/10.1093/ee/15.3.456
Sileshi G (2006) Selecting the right statistical model for analysis of insect count data by using information theoretic measures. Bull Entomol Res 96:479–488. https://doi.org/10.1079/ber2006449
Singh R, Ellis PR, Pink DAC, Phelps K (1994) An investigation of the resistance to cabbage aphid in brassica species. Ann Appl Biol 125:457–465. https://doi.org/10.1111/j.1744-7348.1994.tb04983.x
Soh BSB, Kekeunou S, Nanga SN, Dongmo M, Rachid H (2018) Effect of temperature on the biological parameters of the cabbage aphid Brevicoryne brassicae. Ecol Evol 8:11819–11832. https://doi.org/10.1002/ece3.4639
Tenhumberg B (1995) Estimating predatory efficiency of Episyrphus balteatus (Diptera: Syrphidae) in cereal fields. Environ Entomol 24:687–691. https://doi.org/10.1093/ee/24.3.687
Thomson LJ, Macfadyen S, Hoffmann AA (2010) Predicting the effects of climate change on natural enemies of agricultural pests. Biol Control 52:296–306. https://doi.org/10.1016/j.biocontrol.2009.01.022
Uesugi R, Konishi-Furihata R, Tabuchi K, Yoshimura H, Shimoda T (2023) Predacious natural enemies associated with suppression of onion thrips, Thrips tabaci (Thysanoptera: Thripidae), in intercropped onion-barley agroecosystems. Environ Entomol 52:183–196. https://doi.org/10.1093/ee/nvad014
Vidal S (1997) Factors influencing the population dynamics of Brevicoryne brassicae in undersown brussels sprouts. Biol Agric Hortic 15:285–295. https://doi.org/10.1080/01448765.1997.9755204
White AJ, Wratten SD, Berry NA, Weigmann U (1995) Habitat manipulation to enhance biological control of brassica pests by hover flies (Diptera: Syrphidae). J Econ Entomol 88:1171–1176. https://doi.org/10.1093/jee/88.5.1171
Xu QX, Hatt S, Lopes T, Zhang Y, Bodson B, Chen J, Francis F (2018) A push-pull strategy to control aphids combines intercropping with semiochemical releases. J Pest Sci 91:93–103. https://doi.org/10.1007/s10340-017-0888-2
Zytynska SE, Eicher M, Fahle R, Weisser WW (2021) Effect of flower identity and diversity on reducing aphid populations via natural enemy communities. Ecol Evol 11:18434–18445. https://doi.org/10.1002/ece3.8432
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Uesugi, R., Köneke, A., Sekine, T. et al. Intercropping and flower strips to enhance natural enemies and control aphids: a comparative study in cabbage fields of Japan and Germany. Appl Entomol Zool 59, 173–183 (2024). https://doi.org/10.1007/s13355-024-00867-8
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DOI: https://doi.org/10.1007/s13355-024-00867-8