FLOWERING PLANTS AND ENTOMOPHAGOUS ARTHROPODS IN THE AGRICULTURAL LANDSCAPE: A PRACTISE-ORIENTED SUMMARY OF A COMPLEX RELATIONSHIP

Zhizhi WANG, Pu TANG, Min SHI, Jianhua HUANG, Xuexin CHEN

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Front. Agr. Sci. Eng. ›› 2022, Vol. 9 ›› Issue (1) : 63-74. DOI: 10.15302/J-FASE-2021427
REVIEW
REVIEW

FLOWERING PLANTS AND ENTOMOPHAGOUS ARTHROPODS IN THE AGRICULTURAL LANDSCAPE: A PRACTISE-ORIENTED SUMMARY OF A COMPLEX RELATIONSHIP

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Highlights

● Most entomophagous arthropods consume nectar or pollen as alternative diets.

● The attractive of floral resource with different traits varies in a wide degree.

● Floral resource plays positive effects on not only entomophagous insects but also agricultural biodiversity, multiple ecosystem services and crop production.

Abstract

There is a growing demand for high-quality agricultural products and more countries have adopted landscape management by sowing flowering plants in agricultural fields as an important branch of conservation biological control. However, there has been less concern over the interactions and trade-offs between floral plants and entomophagous arthropods. This paper review progress in pollen/nectar feeding habits of entomophagous insects including parasitoids and predators which are important natural enemies of crop pests in agricultural fields. Factors that influence the preference of different guilds of natural enemies are reviewed to guide the selection of flowering plants in conservation biological control practices. Most studies find that floral resources have positive effects on both biological traits of natural enemies and their abundance and diversity, and this is believed to contribute greatly to pest control. Furthermore, the potential impacts of floral resources on crop yields are also discussed with an emphasis on a guild of entomophagous insects that provides both pest control and pollination services.

Graphical abstract

Keywords

ecosystem services / flowering plants / natural enemies / nectar / pollen

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Zhizhi WANG, Pu TANG, Min SHI, Jianhua HUANG, Xuexin CHEN. FLOWERING PLANTS AND ENTOMOPHAGOUS ARTHROPODS IN THE AGRICULTURAL LANDSCAPE: A PRACTISE-ORIENTED SUMMARY OF A COMPLEX RELATIONSHIP. Front. Agr. Sci. Eng., 2022, 9(1): 63‒74 https://doi.org/10.15302/J-FASE-2021427

References

[1]
Bommarco R, Kleijn D, Potts S G. Ecological intensification: harnessing ecosystem services for food security. Trends in Ecology & Evolution, 2013, 28( 4): 230–238
CrossRef Google scholar
[2]
Wäckers F L, Romeis J, van Rijn P. Nectar and pollen feeding by insect herbivores and implications for multitrophic interactions. Annual Review of Entomology, 2007, 52( 1): 301–323
CrossRef Google scholar
[3]
Jervis M A, Kidd N A C, Heimpel G E. Parasitoid adult feeding behaviour and biocontrol—a review. Biocontrol News and Information, 1996, 17( 1): 11N–26N
[4]
Roy R, Schmitt A J, Thomas J B, Carter C J. Review: Nectar biology: From molecules to ecosystems. Plant Science, 2017, 262 : 148–164
CrossRef Google scholar
[5]
Gurr G M, Wratten S D, Landis D A, You M. Habitat management to suppress pest populations: progress and prospects. Annual Review of Entomology, 2017, 62( 1): 91–109
CrossRef Google scholar
[6]
WackersF L, Van Rijn P C J. Pick and mix: selecting flowering plants to meet the requirements of target biological control insects. In: Gurr G M, Wratten S D, Snyder W E, Read D M Y, eds. Biodiversity and Insect Pests: Key Issues for Sustainable Management. Blackwell: Wiley, 2012, 139–165
[7]
Alhadidi S N, Fowler M S, Griffin J N. Functional diversity of predators and parasitoids does not explain aphid biocontrol efficiency. BioControl, 2019, 64( 3): 303–313
CrossRef Google scholar
[8]
Letourneau D K, Jedlicka J A, Bothwell S G, Moreno C R. Effects of natural enemy biodiversity on the suppression of arthropod herbivores in terrestrial ecosystems. Annual Review of Ecology, Evolution, and Systematics, 2009, 40( 1): 573–592
CrossRef Google scholar
[9]
Imbert C, Papaix J, Husson L, Warlop F, Lavigne C. Pests, but not predators, increase in mixed fruit tree-vegetable plots compared to control vegetable plots in a Mediterranean climate. Agroforestry Systems, 2020, 94( 2): 627–638
CrossRef Google scholar
[10]
Bigger D S, Chaney W E. Effects of Iberis umbellata (Brassicaceae) on insect pests of cabbage and on potential biological control agents. Environmental Entomology, 1998, 27( 1): 161–167
CrossRef Google scholar
[11]
Zhao J Z, Ayers G S, Grafius E J, Stehr F W. Effects of neighboring nectar-producing plants on populations of pest Lepidoptera and their parasitoids in broccoli plantings. Great Lakes Entomologist, 1992, 25( 4): 253–258
[12]
Lavandero B I, Wratten S D, Didham R K, Gurr G M. Increasing floral diversity for selective enhancement of biological control agents: a double-edged sward. Basic and Applied Ecology, 2006, 7( 3): 236–243
CrossRef Google scholar
[13]
Rand T A, Titus E F, Waters D K. Do floral resources benefit the herbivorous sawfly, Cephus cinctus (Hymenoptera: Cephidae), a major pest of wheat in North America. Journal of Economic Entomology, 2019, 112( 2): 565–570
CrossRef Google scholar
[14]
Baggen L R, Gurr G M, Meats A. Flowers in tri-trophic systems: mechanisms allowing selective exploitation by insect natural enemies for conservation biological control. Entomologia Experimentalis et Applicata, 1999, 91( 1): 155–161
CrossRef Google scholar
[15]
Wardhaugh C W. How many species of arthropods visit flowers. Arthropod-Plant Interactions, 2015, 9( 6): 547–565
CrossRef Google scholar
[16]
Pfannenstiel R S, Patt J M. Feeding on nectar and honeydew sugars improves survivorship of two nocturnal cursorial spiders. Biological Control, 2012, 63( 3): 231–236
CrossRef Google scholar
[17]
Van Rijn P C J, Tanigoshi L K. Pollen as food for the predatory mites Iphiseius degenerans and Neoseiulus cucumeris (Acari: Phytoseiidae): dietary range and life history. Experimental & Applied Acarology, 1999, 23( 10): 785–802
CrossRef Google scholar
[18]
Tixier M S. Predatory mites (Acari: Phytoseiidae) in agro-ecosystems and conservation biological control: a review and explorative approach for forecasting plant-predatory mite interactions and mite dispersal. Frontiers in Ecology and Evolution, 2018, 6 : 192
CrossRef Google scholar
[19]
Villa M, Somavilla I, Santos S A P, Lopez-Saez J A, Pereira J A. Pollen feeding habits of Chrysoperla carnea s. l. adults in the olive grove agroecosystem. Agriculture, Ecosystems & Environment, 2019, 283 : 106573
CrossRef Google scholar
[20]
Haslett J R. Interpreting patterns of resource utilization: randomness and selectivity in pollen feeding by adult hoverflies. Oecologia, 1989, 78( 4): 433–442
CrossRef Google scholar
[21]
Bertrand C, Eckerter P W, Ammann L, Entling M H, Gobet E, Herzog F, Mestre L, Tinner W, Albrecht M. Seasonal shifts and complementary use of pollen sources by two bees, a lacewing and a ladybeetle species in European agricultural landscapes. Journal of Applied Ecology, 2019, 56( 11): 2431–2442
CrossRef Google scholar
[22]
Almeida L M, Correa G H, Giorgi J A, Grossi P C. New record of predatory ladybird beetle (Coleoptera, Coccinellidae) feeding on extrafloral nectaries. Revista Brasileira de Entomologia, 2011, 55( 3): 447–450
CrossRef Google scholar
[23]
Guillermo-Ferreira R, Cardoso-Leite R, Gandolfo R. First observation of alternative food usage (extrafloral nectar) by the assassin bug Atopozelus opsimus (Hemiptera, Reduviidae). Revista Brasileira de Entomologia, 2012, 56( 4): 489–491
CrossRef Google scholar
[24]
LundgrenJ G. The functions of non-prey foods in the diets of entomophagous species. In: Lundgren J G, ed. Relationships of Natural Enemies and Non-prey Foods. Dordrecht: Springer, 2009, 1–14
[25]
Infante F, Ortiz J A, Solis-Montero L, Mound L A, Vega F E. Thrips (Thysanoptera) of coffee flowers. Annals of the Entomological Society of America, 2017, 110( 3): 329–336
CrossRef Google scholar
[26]
Beckman N, Hurd L E. Pollen feeding and fitness in praying mantids: the vegetarian side of a tritrophic predator. Environmental Entomology, 2003, 32( 4): 881–885
CrossRef Google scholar
[27]
De Sousa M F, Fernandes M G, Mota T A. Biology of Trichogramma pretiosum (Hymenoptera: Trichogrammatidae) fed transgenic maize pollen. Florida Entomologist, 2017, 100( 3): 653–656
CrossRef Google scholar
[28]
Gómez J M, Zamora R. Pollination by ants: consequences of the quantitative effects on a mutualistic system. Oecologia, 1992, 91( 3): 410–418
CrossRef Google scholar
[29]
Junker R R, Blüthgen N. Floral scents repel facultative flower visitors, but attract obligate ones. Annals of Botany, 2010, 105( 5): 777–782
CrossRef Google scholar
[30]
Jervis M A, Kidd N A C, Fitton M G, Huddleston T, Dawah H A. Flower-visiting by Hymenopteran parasitoids. Journal of Natural History, 1993, 27( 1): 67–105
CrossRef Google scholar
[31]
Zhang G R, Zimmermann O, Hassan S A. Pollen as a source of food for egg parasitoids of the genus Trichogramma (Hymenoptera: Trichogrammatidae). Biocontrol Science and Technology, 2004, 14( 2): 201–209
CrossRef Google scholar
[32]
Soyelu O J. Suitability of a novel diet for a parasitic wasp, Cotesia plutellae. Journal of Insect Science, 2013, 13( 86): 8601
CrossRef Google scholar
[33]
McMurtry J A, Croft B A. Life-styles of Phytoseiid mites and their roles in biological control. Annual Review of Entomology, 1997, 42( 1): 291–321
CrossRef Google scholar
[34]
Jervis M A, Heimpel G E, Ferns P N, Harvey J A, Kidd N A C. Life-history strategies in parasitoid wasps: a comparative analysis of ‘ovigeny’. Journal of Animal Ecology, 2001, 70( 3): 442–458
CrossRef Google scholar
[35]
Zhang Y, Yang N, Wang J, Wan F. Effect of six carbohydrate sources on the longevity of a whitefly parasitoid Eretmocerus hayati (Hymenoptera: Aphelinidae). Journal of Asia-Pacific Entomology, 2014, 17( 4): 723–728
CrossRef Google scholar
[36]
Xiong S, Yu K, Yao H, Wang F, Fang Q, Song Q, Ye G. Effects of sugar sources on adult longevity, survival and related gene expression in an endoparasitoid, Pteromalus puparum (Hymenoptera: Pteromalidae). Pest Management Science, 2021, 77( 3): 1282–1291
CrossRef Google scholar
[37]
Sheng S, Zhang X R, Zheng Y, Wang J, Zhou Y, Liao C W, Wang J, Wu F A. Effect of six sugars on the longevity, oviposition performance and nutrition accumulation in an endoparasitoid, Meteorus pulchricornis (Hymenoptera: Braconidae). Journal of Asia-Pacific Entomology, 2019, 22( 1): 263–268
CrossRef Google scholar
[38]
IrvinN A, Hoddle M S, CastleS J. The effect of resource provisioning and sugar composition of foods on longevity of three Gonatocerus spp., egg parasitoids of Homalodisca vitripennis. Biological Control, 2007, 40(1): 69–79
[39]
Pandey S, Rahman A, Gurr G M. Australian native flowering plants enhance the longevity of three parasitoids of brassica pests. Entomologia Experimentalis et Applicata, 2018, 166( 4): 265–276
CrossRef Google scholar
[40]
Kai L, Zhu P Y, Lu Z X, Chen G H, Zhang J M, Lu Y B, Lu Y H. Effects of sesame nectar on longevity and fecundity of seven Lepidoptera and survival of four parasitoid species commonly found in agricultural ecosystems. Journal of Integrative Agriculture, 2017, 16( 11): 2534–2546
CrossRef Google scholar
[41]
Stapel J O, Cortesero A M, De Moraes C M, Tumlinson J H, Joe Lewis W. Extrafloral nectar, honeydew, and sucrose effects on searching behavior and efficiency of Microplitis croceipes (Hymenoptera: Braconidae) in cotton. Environmental Entomology, 1997, 26( 3): 617–623
CrossRef Google scholar
[42]
Heimpel G E. Linking parasitoid nectar feeding and dispersal in conservation biological control. Biological Control, 2019, 132 : 36–41
CrossRef Google scholar
[43]
Araj S E, Wratten S, Lister A, Buckley H, Ghabeish I. Searching behavior of an aphid parasitoid and its hyperparasitoid with and without floral nectar. Biological Control, 2011, 57( 2): 79–84
CrossRef Google scholar
[44]
Siekmann G, Keller M A, Tenhumberg B. The sweet tooth of adult parasitoid Cotesia rubecula: ignoring hosts for nectar?. Journal of Insect Behavior, 2004, 17( 4): 459–476
CrossRef Google scholar
[45]
Tylianakis J M, Tscharntke T, Lewis O T. Habitat modification alters the structure of tropical host-parasitoid food webs. Nature, 2007, 445( 7124): 202–205
CrossRef Google scholar
[46]
Araj S E, Wratten S, Lister A, Buckley H. Adding floral nectar resources to improve biological control: potential pitfalls of the fourth trophic level. Basic and Applied Ecology, 2009, 10( 6): 554–562
CrossRef Google scholar
[47]
Ramsden M W, Menéndez R, Leather S R, Wäckers F. Optimizing field margins for biocontrol services: the relative role of aphid abundance, annual floral resources, and overwinter habitat in enhancing aphid natural enemies. Agriculture, Ecosystems & Environment, 2015, 199 : 94–104
CrossRef Google scholar
[48]
HeimpelG E, Jervis M A. Does floral nectar improve biological control by parasitoids? In: Wackers F L, van Rijn P C J, Bruin J, eds. Plant-provided Food for Carnivorous Insects: Protective Mutualism and ItsApplications. Cambridge: Cambridge University Press, 2005, 267–304
[49]
Rodríguez-Gasol N, Alins G, Veronesi E R, Wratten S. The ecology of predatory hoverflies as ecosystem-service providers in agricultural systems. Biological Control, 2020, 151 : 104405
CrossRef Google scholar
[50]
van Rijn P C J, Wackers F L. Nectar accessibility determines fitness, flower choice and abundance of hoverflies that provide natural pest control. Journal of Applied Ecology, 2016, 53( 3): 925–933
CrossRef Google scholar
[51]
van Rijn P C J, Kooijman J, Wackers F L. The contribution of floral resources and honeydew to the performance of predatory hoverflies (Diptera: Syrphidae). Biological Control, 2013, 67( 1): 32–38
CrossRef Google scholar
[52]
PinheiroL A, Torres L, RaimundoJ, SantosS A P. Effect of seven species of the family Asteraceae on longevity and nutrient levels of Episyrphus balteatus. BioControl, 2013, 58(6): 797–806
[53]
Laubertie E A, Wratten S D, Hemptinne J L. The contribution of potential beneficial insectary plant species to adult hoverfly (Diptera: Syrphidae) fitness. Biological Control, 2012, 61( 1): 1–6
CrossRef Google scholar
[54]
PinheiroL A, Torres L M, RaimundoJ, SantosS A P. Effects of pollen, sugars and honeydew on lifespan and nutrient levels of Episyrphus balteatus. BioControl, 2015, 60(1): 47–47
[55]
Branquart E, Hemptinne J L. Development of ovaries, allometry of reproductive traits and fecundity of Episyrphus balteatus (Diptera: Syrphidae). European Journal of Entomology, 2000, 97( 2): 165–170
CrossRef Google scholar
[56]
Ambrosino M D, Luna J M, Jepson P C, Wratten S D. Relative frequencies of visits to selected insectary plants by predatory hoverflies (Diptera: Syrphidae), other beneficial insects, and herbivores. Environmental Entomology, 2006, 35( 2): 394–400
CrossRef Google scholar
[57]
Colley M R, Luna J M. Relative attractiveness of potential beneficial insectary plants to aphidophagous hoverflies (Diptera: Syrphidae). Environmental Entomology, 2000, 29( 5): 1054–1059
CrossRef Google scholar
[58]
Haenke S, Scheid B, Schaefer M, Tscharntke T, Thies C. Increasing syrphid fly diversity and density in sown flower strips within simple vs. complex landscapes. Journal of Applied Ecology, 2009, 46( 5): 1106–1114
CrossRef Google scholar
[59]
Ramsden M, Menendez R, Leather S, Wackers F. Do natural enemies really make a difference? Field scale impacts of parasitoid wasps and hoverfly larvae on cereal aphid populations. Agricultural and Forest Entomology, 2017, 19( 2): 139–145
CrossRef Google scholar
[60]
Xiu C, Xu B, Pan H, Zhang W, Yang Y, Lu Y. Volatiles from Sophora japonica flowers attract Harmonia axyridis adults (Coleoptera: Coccinellidae). Journal of Integrative Agriculture, 2019, 18( 4): 873–883
CrossRef Google scholar
[61]
Togni P H B, Venzon M, Muniz C A, Martins E F, Pallini A, Sujii E R. Mechanisms underlying the innate attraction of an aphidophagous coccinellid to coriander plants: implications for conservation biological control. Biological Control, 2016, 92 : 77–84
CrossRef Google scholar
[62]
He X Q, Sigsgaard L. A floral diet increases the longevity of the coccinellid Adalia bipunctata but does not allow molting or reproduction. Frontiers in Ecology and Evolution, 2019, 7 : 6
CrossRef Google scholar
[63]
Gonzalez D, Nave A, Goncalves F, Nunes F M, Campos M, Torres L. Higher longevity and fecundity of Chrysoperla carnea, a predator of olive pests, on some native flowering Mediterranean plants. Agronomy for Sustainable Development, 2016, 36( 2): 30
CrossRef Google scholar
[64]
Zhu P, Lu Z, Heong K, Chen G, Zheng X, Xu H, Yang Y, Nicol H I, Gurr G M. Selection of nectar plants for use in ecological engineering to promote biological control of rice pests by the predatory bug, Cyrtorhinus lividipennis (Heteroptera: Miridae). PLoS One, 2014, 9( 9): e108669
CrossRef Google scholar
[65]
Mendoza J E, Balanza V, Cifuentes D, Bielza P. Genetic improvement of Orius laevigatus for better fitness feeding on pollen. Journal of Pest Science, 2021, 94( 3): 729–742
CrossRef Google scholar
[66]
Benhadi-Marin J, Pereira J A, Sousa J P, Santos S A P. Spiders actively choose and feed on nutritious non-prey food resources. Biological Control, 2019, 129 : 187–194
CrossRef Google scholar
[67]
Hinds J, Barbercheck M E. Diversified floral provisioning enhances performance of the generalist predator, Orius insidiosus (Hemiptera: Anthocoridae). Biological Control, 2020, 149 : 104313
CrossRef Google scholar
[68]
Li G Y, Zhang Z Q. Can supplementary food (pollen) modulate the functional response of a generalist predatory mite (Neoseiulus cucumeris) to its prey (Tetranychus urticae)?. BioControl, 2020, 65( 2): 165–174
CrossRef Google scholar
[69]
Tsuchida Y, Masui S. Effects of providing pollen to Euseius sojaensis or Amblyseius eharai (Acari: Phytoseiidae) on populations of the pink citrus rust mite, Aculops pelekassi (Acari: Eriophyidae). Applied Entomology and Zoology, 2020, 55( 2): 241–248
CrossRef Google scholar
[70]
Balmer O, Pfiffner L, Schied J, Willareth M, Leimgruber A, Luka H, Traugott M. Noncrop flowering plants restore top-down herbivore control in agricultural fields. Ecology and Evolution, 2013, 3( 8): 2634–2646
CrossRef Google scholar
[71]
Yong T H. Nectar-feeding by a predatory ambush bug (Heteroptera: Phymatidae) that hunts on flowers. Annals of the Entomological Society of America, 2003, 96( 5): 643–651
CrossRef Google scholar
[72]
LabbéR M, GagnierD, KosticA, ShippL. The function of supplemental foods for improved crop establishment of generalist predators Orius insidiosus and Dicyphus hesperus. Scientific Reports, 2018, 8(1): 17790
[73]
Miall J H, Abram P K, Cappuccino N, Bennett A M R, Fernandez-Triana J L, Gibson G A P, Mason P G. Addition of nectar sources affects a parasitoid community without improving pest suppression. Journal of Pest Science, 2021, 94( 2): 335–347
CrossRef Google scholar
[74]
Pellissier M E, Jabbour R. Herbivore and parasitoid insects respond differently to annual and perennial floral strips in an alfalfa ecosystem. Biological Control, 2018, 123 : 28–35
CrossRef Google scholar
[75]
JuddW S, Campbell C S, KelloggE A, StevensP F, Donoghue M J. Plant systematics: a phylogenetic approach. 4th ed. Oxford University Press, 2015
[76]
Fiedler A K, Landis D A, Wratten S D. Maximizing ecosystem services from conservation biological control: the role of habitat management. Biological Control, 2008, 45( 2): 254–271
CrossRef Google scholar
[77]
Tooker J F, Hanks L M. Flowering plant hosts of adult Hymenopteran parasitoids of central Illinois. Annals of the Entomological Society of America, 2000, 93( 3): 580–588
CrossRef Google scholar
[78]
Tooker J F, Hauser M, Hanks L M. Floral host plants of Syrphidae and Tachinidae (Diptera) of central Illinois. Annals of the Entomological Society of America, 2006, 99( 1): 96–112
CrossRef Google scholar
[79]
Al-Doghairi M A, Cranshaw W S. Surveys on visitation of flowering landscape plants by common biological control agents in Colorado. Journal of the Kansas Entomological Society, 1999, 72( 2): 190–196
[80]
Sivinski J, Wahl D, Holler T, Al Dobai S, Sivinski R. Conserving natural enemies with flowering plants: estimating floral attractiveness to parasitic Hymenoptera and attraction’s relationship to flower and plant morphology. Biological Control, 2011, 58( 3): 208–214
CrossRef Google scholar
[81]
Li S, Jaworski C C, Hatt S, Zhang F, Desneux N, Wang S. Flower strips adjacent to greenhouses help reduce pest populations and insecticide applications inside organic commercial greenhouses. Journal of Pest Science, 2021, 94( 3): 679–689
CrossRef Google scholar
[82]
Hatt S, Uyttenbroeck R, Lopes T, Chen J L, Piqueray J, Monty A, Francis F. Effect of flower traits and hosts on the abundance of parasitoids in perennial multiple species wildflower strips sown within oilseed rape (Brassica napus) crops. Arthropod-Plant Interactions, 2018, 12( 6): 787–797
CrossRef Google scholar
[83]
Hatt S, Uyttenbroeck R, Lopes T, Mouchon P, Chen J, Piqueray J, Monty A, Francis F. Do flower mixtures with high functional diversity enhance aphid predators in wildflower strips?. European Journal of Entomology, 2017, 114 : 66–76
CrossRef Google scholar
[84]
Arnó J, Oveja M F, Gabarra R. Selection of flowering plants to enhance the biological control of Tuta absoluta using parasitoids. Biological Control, 2018, 122 : 41–50
CrossRef Google scholar
[85]
Nafziger T D Jr, Fadamiro H Y. Suitability of some farmscaping plants as nectar sources for the parasitoid wasp, Microplitis croceipes (Hymenoptera: Braconidae): effects on longevity and body nutrients. Biological Control, 2011, 56( 3): 225–229
CrossRef Google scholar
[86]
Hogg B N, Nelson E H, Mills N J, Daane K M. Floral resources enhance aphid suppression by a hoverfly. Entomologia Experimentalis et Applicata, 2011, 141( 2): 138–144
CrossRef Google scholar
[87]
Ribeiro A L, Gontijo L M. Alyssum flowers promote biological control of collard pests. BioControl, 2017, 62( 2): 185–196
CrossRef Google scholar
[88]
Gurr G M, Lu Z, Zheng X, Xu H, Zhu P, Chen G, Yao X, Cheng J, Zhu Z, Catindig J L, Villareal S, Van Chien H, Cuong Q, Channoo C, Chengwattana N, Lan L P, Hai H, Chaiwong J, Nicol H I, Perovic D J, Wratten S D, Heong K L. Multi-country evidence that crop diversification promotes ecological intensification of agriculture. Nature Plants, 2016, 2( 3): 16014
CrossRef Google scholar
[89]
Cahenzli F, Pfiffner L, Daniel C. Reduced crop damage by self-regulation of aphids in an ecologically enriched, insecticide-free apple orchard. Agronomy for Sustainable Development, 2017, 37( 6): 65
CrossRef Google scholar
[90]
Campbell A J, Wilby A, Sutton P, Wäckers F. Getting more power from your flowers: multi-functional flower strips enhance pollinators and pest control agents in apple orchards. Insects, 2017, 8( 3): 101
CrossRef Google scholar
[91]
Le Gal A, Robert C, Accatino F, Claessen D, Lecomte J. Modelling the interactions between landscape structure and spatio-temporal dynamics of pest natural enemies: implications for conservation biological control. Ecological Modelling, 2020, 420 : 108912
CrossRef Google scholar
[92]
Wyckhuys K, Sanchez-Bayo F, Aebi A, van Lexmond M B, Bonmatin J M, Goulson D, Mitchell E. Stay true to integrated pest management. Science, 2021, 371( 6525): 133
[93]
Rader R, Cunningham S A, Howlett B G, Inouye D W. Non-bee insects as visitors and pollinators of crops: biology, ecology, and management. Annual Review of Entomology, 2020, 65( 1): 391–407
CrossRef Google scholar
[94]
Tschumi M, Albrecht M, Collatz J, Dubsky V, Entling M H, Najar-Rodriguez A J, Jacot K. Tailored flower strips promote natural enemy biodiversity and pest control in potato crops. Journal of Applied Ecology, 2016, 53( 4): 1169–1176
CrossRef Google scholar
[95]
Pekas A, De Craecker I, Boonen S, Wackers F L, Moerkens R. One stone; two birds: concurrent pest control and pollination services provided by aphidophagous hoverflies. Biological Control, 2020, 149 : 104328
CrossRef Google scholar
[96]
Kleijn D, Bommarco R, Fijen T P M, Garibaldi L A, Potts S G, van der Putten W H. Ecological Intensification: bridging the gap between science and practice. Trends in Ecology & Evolution, 2019, 34( 2): 154–166
CrossRef Google scholar

Acknowledgements

This work was jointly supported by the National Key Research and Development Program of China (2019YFD0300100), the Key Program of the National Natural Science Foundation of China (31630060), the Key International Joint Research Program of the National Natural Science Foundation of China (31920103005), the Key Research and Development Program of Zhejiang Province (2021C02045), the Fundamental Research Funds for the Central Universities, and the Special Research Fund for Distinguished Scholars of Zhejiang Province (2018R51004).

Compliance with ethics guidelines

Zhizhi Wang, Pu Tang, Min Shi, Jianhua Huang, and Xuexin Chen declare that they have no conflicts of interest or financial conflicts to disclose. This article does not contain any study with human or animal subjects performed by any of the authors.

RIGHTS & PERMISSIONS

The Author(s) 2021. Published by Higher Education Press. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0)
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