Hostname: page-component-586b7cd67f-rdxmf Total loading time: 0 Render date: 2024-11-29T14:24:59.464Z Has data issue: false hasContentIssue false
  • English
  • Français

Malice at the Gates of Eden: current and future distribution of Agrilus mali threatening wild and domestic apples

Published online by Cambridge University Press:  13 April 2022

Zhaozhi Lu Open the ORCID record for Zhaozhi Lu [Opens in a new window] ,
Xiaoxian Liu ,
Ting Wang ,
Ping Zhang ,
Zhenlin Wang ,
Yanlong Zhang ,
Darren J. Kriticos  and
Myron P. Zalucki
Zhaozhi Lu*
Affiliation:
College of Plant Health and Medicine of Qingdao Agriculture University, Qingdao 266109, China Shandong Engineering Research Center for Environment-Friendly Agricultural Pest Management, College of Plant Health and Medicine, Qingdao Agricultural University, Qingdao 266109, China
Xiaoxian Liu
Affiliation:
Key Laboratory of Biogeography and Bioresource in Arid Land, Xinjiang Institute of Ecology and Geography, Chinese Academy of Sciences, Urumqi, China University of Chinese Academy of Sciences, Beijing 100049, China Research Center for Ecology and Environment of Central Asia, CAS, Urumqi 830011, China
Ting Wang
Affiliation:
College of Plant Health and Medicine of Qingdao Agriculture University, Qingdao 266109, China Shandong Engineering Research Center for Environment-Friendly Agricultural Pest Management, College of Plant Health and Medicine, Qingdao Agricultural University, Qingdao 266109, China
Ping Zhang
Affiliation:
Key Laboratory of Biogeography and Bioresource in Arid Land, Xinjiang Institute of Ecology and Geography, Chinese Academy of Sciences, Urumqi, China University of Chinese Academy of Sciences, Beijing 100049, China Research Center for Ecology and Environment of Central Asia, CAS, Urumqi 830011, China
Zhenlin Wang
Affiliation:
Key Laboratory of Biogeography and Bioresource in Arid Land, Xinjiang Institute of Ecology and Geography, Chinese Academy of Sciences, Urumqi, China University of Chinese Academy of Sciences, Beijing 100049, China Research Center for Ecology and Environment of Central Asia, CAS, Urumqi 830011, China
Yanlong Zhang
Affiliation:
Ecology and Nature Conservation Institute, Chinese Academy of Forestry, Beijing 100091, China
Darren J. Kriticos
Affiliation:
CSIRO Health & Biosecurity, Canberra ACT, Australia 2601 School of Biological Sciences, The University of Queensland, Brisbane, Australia 4072
Myron P. Zalucki
Affiliation:
School of Biological Sciences, The University of Queensland, Brisbane, Australia 4072
*
Author for correspondence: Zhaozhi Lu, Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The apple buprestid, Agrilus mali Matsumura, that was widespread in north-eastern China, was accidently introduced to the wild apple forest ecosystem in mountainous areas of Xinjiang, China. This invasive beetle feeds on domesticated apples and many species of Malus and presents a serious threat to ancestral apple germplasm sources and apple production worldwide. Estimating the potential area at risk of colonization by A. mali is crucial for instigating appropriate preventative management strategies, especially under global warming. We developed a CLIMEX model of A. mali to project this pest's potential distribution under current and future climatic scenarios in 2100 using CSIRO-Mk 3.0 GCM running the SRES A1B emissions scenario. Under current climate, A. mali could potentially invade neighbouring central Asia and eventually the mid-latitude temperate zone, and some subtropical areas and Pampas Steppe in the Southern Hemisphere. This potential distribution encompasses wild apples species, the ancestral germplasm for domesticated apples. With global warming, the potential distribution shifts to higher latitudes, with the potential range expanding slightly, though the overall suitability could decline in both hemispheres. In 2100, the length of the growing season of this pest in the mid-latitude temperature zone could increase by 1–2 weeks, with higher growth rates in most sites compared with current climate in mid-latitudes, at least in China. Our work highlights the need for strategies to prevent the spread of this pest, managing the threats to wild apples in Tian Shan Mountain forests in Central Asia, and commercial apple production globally. We discuss practical management tactics to reduce the spread of this pest and mitigate its impacts.

Keywords

Apple buprestidbiosecurityCLIMEXniche modellinguncertainty analysiswild apple
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 112 , Issue 6 , December 2022 , pp. 745 - 757
Check for updates
Copyright
Copyright © Qingdao Agriculture University, 2022. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Aljaryian, R and Kumar, L (2016) Changing global risk of invading greenbug Schizaphis graminum under climate change. Crop Protection 88, 137–148.CrossRefGoogle Scholar
Ayres, MP and Lombardero, MJ (2000) Assessing the consequences of global change for forest disturbance from herbivores and pathogens. Science of the Total Environment 262, 263–286.CrossRefGoogle ScholarPubMed
Baloch, MN, Fan, J, Haseeb, M and Zhang, RZ (2020) Mapping potential distribution of Spodoptera frugiperda (Lepidoptera: Noctuidae) in Central Asia. Insects 11, 172.CrossRefGoogle ScholarPubMed
Battisti, A, Stastny, M, Netherer, S, Robinet, C, Schopf, A, Roques, A and Larsson, S (2005) Expansion of geographic range in the pine processionary moth caused by increased winter temperatures. Ecological Applications 15, 2084–2096.CrossRefGoogle Scholar
Bebber, DP, Ramotowski, MAT and Gurr, SJ (2013) Crop pests and pathogens move polewards in a warming world. Nature Climate Change 3, 985–988.CrossRefGoogle Scholar
Biondi, A, Guedes, RNC, Wan, F and Desneux, N (2018) Ecology, worldwide spread, and management of the invasive south American tomato pinworm, Tuta absoluta: past, present, and future. Annual Review of Entomology 63, 239–258.CrossRefGoogle ScholarPubMed
Bozorov, TA, Luo, Z, Li, X and Zhang, D (2019) Agrilus mali Matsumara (Coleoptera: Buprestidae), a new invasive pest of wild apple in western China: DNA barcoding and life cycle. Ecology and Evolution 9, 1160–1172.CrossRefGoogle ScholarPubMed
Brown, N, Jeger, M, Kirk, S, Williams, D, Xu, X, Pautasso, M and Denman, S (2017) Acute oak decline and Agrilus biguttatus: the co-occurrence of stem bleeding and D-shaped emergence holes in Great Britain. Forests 8, 1–17.CrossRefGoogle Scholar
Chamberlin, TC (1965) The method of multiple working hypotheses. Science (New York, N.Y.) 148, 754–759.CrossRefGoogle ScholarPubMed
Chaves, LF (2016) Globally invasive, withdrawing at home: Aedes albopictus and Aedes japonicus facing the rise of Aedes flavopictus. International Journal of Biometeorology 60, 1727–1738.CrossRefGoogle ScholarPubMed
Cornille, A, Gladieux, P, Smulders, MJM, Roldán-Ruiz, I, Laurens, F, Le Cam, B, Nersesyan, A, Clavel, J, Olonova, M, Feugey, L, Gabrielyan, I, Zhang, XG, Tenaillon, MI and Giraud, T (2012) New insight into the history of domesticated apple: secondary contribution of the European wild apple to the genome of cultivated varieties. PLoS Genetics 8, e1002703.CrossRefGoogle Scholar
Cornille, A, Giraud, T, Bellard, C, Tellier, A, Le Cam, B, Smulders, MJM, Kleinschmit, J, Roldan-Ruiz, I and Gladieux, P (2013) Postglacial recolonization history of the European crab apple (Malus sylvestris Mill.), a wild contributor to the domesticated apple. Molecular Ecology 22, 2249–2263.CrossRefGoogle Scholar
Cui, XN, Liu, DG and Liu, AH (2015) Research progress in integrated management of Agrilus mali. Plant Protection 41, 16–23.Google Scholar
Cui, ZJ, Zhang, YL, Luo, ZH, Ma, HL and Lu, ZZ (2018) Damage of Agrilus mali Matsumura in wild apple forest and its assessment. Arid Zone Research 35, 1153–1159.Google Scholar
Cui, ZJ, Zhang, YL, Zhang, X, Luo, ZH, Zhang, P, Golec, J, Poland, TM, Zalucki, MP, Han, P and Lu, ZZ (2019) Life history and mortality factors of Agrilus mali Matsumura (Coleoptera: Buprestidae) in wild apples in Northwestern China: life history and mortality factors of Agrilus mali Matsumura. Agricultural and Forest Entomology 21, 309–317.CrossRefGoogle Scholar
Deutsch, C, Tewksbury, JJ, Huey, RB, Sheldon, KS, Ghalambor, CK, Haak, DC and Martin, PR (2008) Impacts of climate warming on terrestrial ectotherms across latitude. Proceedings of the National Academy of Sciences of the USA 105, 6668–6672.CrossRefGoogle ScholarPubMed
Digirolomo, MF, Jendek, E, Grebennikov, VV and Nakladal, O (2019) First North American record of an unnamed West Palaearctic Agrilus (Coleoptera: Buprestidae) infesting European beech (Fagus sylvatica) in New York City, USA. European Journal of Entomology 116, 244–252.CrossRefGoogle Scholar
Dodds, KJ, Hanavan, RP and DiGirolomo, MF (2017) Firewood collected after a catastrophic wind event: the bark beetle (Scolytinae) and woodborer (Buprestidae, Cerambycidae) community present over a 3-year period. Agricultural & Forest Entomology 19, 309–320.CrossRefGoogle Scholar
Duan, JJ, Tim, W, Phil, T, Kristi, L and Lelito, JP (2013) Effects of ambient temperature on egg and larval development of the invasive emerald ash borer (Coleoptera: Buprestidae): implications for laboratory rearing. Journal of Economic Entomology 106, 2101–2108.CrossRefGoogle ScholarPubMed
Duan, JJ, Schmude, JM and Larson, KM (2021) Effects of low temperature exposure on diapause, development, and reproductive fitness of the emerald ash borer (Coleoptera: Buprestidae): implications for voltinism and laboratory rearing. Journal of Economic Entomology 114, 201–208.CrossRefGoogle ScholarPubMed
Engelkes, T, Morrieen, E, Verhoeven, KJF, Bezemer, TM, Biere, A, Harvey, JA, McIntyre, LM, Tamis, WLM and van der Putten, WH (2008) Successful range-expanding plants experience less above-ground and below-ground enemy impact. Nature 456, 946–948.CrossRefGoogle ScholarPubMed
Foster, JR, Townsend, PA and Mladenoff, DJ (2013) Mapping asynchrony between gypsy moth egg-hatch and forest leaf-out: putting the phenological window hypothesis in a spatial context. Forest Ecology and Management 287, 67–76.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
Gillard, M, Thiebaut, G, Deleu, C and Leroy, B (2017) Present and future distribution of three aquatic plants taxa across the world: decrease in native and increase in invasive ranges. Biological Invasions 19, 2159–2170.CrossRefGoogle Scholar
Goergen, G, Kumar, PL, Sankung, SB, Togola, A and Tamo, M (2016) First report of outbreaks of the fall armyworm Spodoptera frugiperda (J E Smith) (Lepidoptera, Noctuidae), a new alien invasive pest in west and central Africa. PLoS ONE 11, 1–9.CrossRefGoogle Scholar
Guichard, S, Guis, H, Tran, A, Garros, C, Balenghien, T and Kriticos, DJ (2014) Worldwide niche and future potential distribution of Culicoides imicola, a major vector of bluetongue and African horse sickness viruses. PLoS ONE 9, e112491.CrossRefGoogle Scholar
Haack, RA and Benjamin, DM (1982) The biology and ecology of the twolined chestnut borer, Agrilus bilineatus (Coleoptera: Buprestidae), on oaks, Quercus spp., in Wisconsin. Canadian Entomologist 114, 385–396.CrossRefGoogle Scholar
Haack, RA, Petrice, TR and Wiedenhoeft, AC (2010) Incidence of bark- and wood-boring insects in firewood: a survey at Michigan's Mackinac bridge. Journal of Economic Entomology 103, 1682–1692.CrossRefGoogle ScholarPubMed
Harris, SA, Robinson, JP and Juniper, BE (2002) Genetic clues to the origin of the apple. Trends in Genetics 18, 426–430.CrossRefGoogle Scholar
Hortal J, Jiménez-Valverde A, Gómez JF, Lobo JM and Baselga A (2008) Historical bias in biodiversity inventories affects the observed environmental niche of the species. Oikos 6, 847–858.CrossRefGoogle Scholar
Huang, L, Tang, J, Chen, C, He, H, Gao, Y and Xue, F (2020) Diapause incidence and critical day length of Asian corn borer (Ostrinia furnacalis) populations exhibit a latitudinal cline in both pure and hybrid strains. Journal of Pest Science 93, 559–568.CrossRefGoogle Scholar
Hulme, PE (2017) Climate change and biological invasions: evidence, expectations, and response options. Biological Reviews 92, 1297–1313.CrossRefGoogle ScholarPubMed
Jacobi, WR, Hardin, JG, Goodrich, BA and Cleaver, CM (2012) Retail firewood can transport live tree pests. Journal of Economic Entomology 105, 1645–1658.CrossRefGoogle ScholarPubMed
Jaric, I, Heger, T, Monzon, FC, Jeschke, JM, Kowarik, I, Mcconkey, KR, Pysek, P, Sagouis, A and Essl, F (2019) Crypticity in biological invasions. Trends in Ecology and Evolution 34, 291–302.CrossRefGoogle ScholarPubMed
Kimura, MT (1988) Interspecific and geographic variation of diapause intensity and seasonal adaptation in the Drosophila auraria species complex (Diptera: Drosophilidae). Functional Ecology 2, 177–183.CrossRefGoogle Scholar
Kistner, EJ (2017) Climate change impacts on the potential distribution and abundance of the brown marmorated stink bug (Hemiptera: Pentatomidae) with special reference to North America and Europe. Environmental Entomology 46, 1212–1224.CrossRefGoogle ScholarPubMed
Kovacs, KF, Haight, RG, McCullough, DG, Mercader, RJ, Siegert, NW and Liebhold, AM (2010) Cost of potential emerald ash borer damage in U.S. communities, 2009–2019. Ecological Economics 69, 569–578.CrossRefGoogle Scholar
Koveos, DS, Kroon, A and Veerman, A (1993) Geographic variation of diapause intensity in the spider mite Tetranychus urticae. Physiological Entomology 18, 50–56.CrossRefGoogle Scholar
Kriticos, DJ, Sutherst, RW, Brown, JR, Adkins, SW and Maywald, GF (2003) Climate change and biotic invasions: a case history of a tropical woody vine. Biological Invasions 5, 147–165.CrossRefGoogle Scholar
Kriticos, DJ, Watt, MS, Potter, KJB, Manning, LK, Alexander, NS and Tallent-Halsell, N (2011) Managing invasive weeds under climate change: considering the current and potential future distribution of Buddleja davidii. Weed Research 51, 85–96.CrossRefGoogle Scholar
Kriticos, DJ, Webber, BL, Leriche, A, Ota, N, Macadam, I, Bathols, J and Scott, JK (2012) CliMond: global high-resolution historical and future scenario climate surfaces for bioclimatic modelling. Methods in Ecology and Evolution 3, 53–64.CrossRefGoogle Scholar
Kriticos, DJ, Agathe, L, Palmer, DJ, Cook, DC, Brockerhoff, EG, Stephens, AEA, Watt, MS and Alex, SM (2013) Linking climate suitability, spread rates and host-impact when estimating the potential costs of invasive pests. PLoS ONE 8, e54861.CrossRefGoogle ScholarPubMed
Kriticos, DJ, Ota, N, Hutchison, WD, Beddow, J, Walsh, T, Tay, WT, Borchert, DM, Paula-Moreas, SV, Czepak, C and Zalucki, MP (2015) The potential distribution of invading Helicoverpa armigera in North America: is it just a matter of time? PLoS ONE 10, e0119618.CrossRefGoogle ScholarPubMed
Kriticos, DJ, Kean, JM, Phillips, CB, Senay, SD, Acosta, H and Haye, T (2017) The potential global distribution of the brown marmorated stink bug, Halyomorpha halys, a critical threat to plant biosecurity. Journal of Pest Science 90, 1033–1043.CrossRefGoogle Scholar
Kriticos, DJ, Darnell, RE, Yonow, T, Ota, N, Boykin, LM, Sutherst, RW, Parry, HR, Mugerwa, H, Maruthi, MN, Seal, S, Colvin, J, Macfadyen, SA, Kalyebi, A, Hulthen, A and De Barro, PJ (2020) Improving climate suitability for Bemisia tabaci in East and Central Africa correlates with increased prevalence of whiteflies and cassava diseases. Scientific Reports 10, 22049.CrossRefGoogle Scholar
Kumar, C, Singh, SK, Pramanick, KK, Verma, MK, Srivastav, M, Singh, R, Bharadwaj, C and Naga, KC (2018) Morphological and biochemical diversity among the Malus species including indigenous Himalayan wild apples. Scientia Horticulturae 233, 204–219.CrossRefGoogle Scholar
Lehmann, P, Lyytinen, A, Piiroinen, S and Lindström, L (2015) Latitudinal differences in diapause related photoperiodic responses of European Colorado potato beetles (Leptinotarsa decemlineata). Evolutionary Ecology 29, 269–282.CrossRefGoogle Scholar
Li, ML and Zhang, ZQ (2017) Discussion on biology and life history associated with Agrilus mali Matsumura. Journal of Northwest Forestry University 32, 139–146.Google Scholar
Li, ZY, Feng, X, Liu, SS, You, M and Furlong, MJ (2016) Biology, ecology, and management of the diamondback moth in China. Annual Review of Entomology 61, 277–296.CrossRefGoogle ScholarPubMed
Li, X, Wu, MF, Ma, J, Gao, BY, Wu, QL, Chen, AD, Liu, J, Jiang, YY, Zhai, BP, Early, R, Chapman, JW and Hu, G (2020) Prediction of migratory routes of the invasive fall armyworm in eastern China using a trajectory analytical approach. Pest Management Science 76, 454–463.CrossRefGoogle ScholarPubMed
Liu, AH (2010) Biology and Ecology of Agrilus mali and its Dominant Natural Enemies in Wild Fruit Forests in Xinjiang. Xinjiang: China Xinjiang Agricultural University.Google Scholar
Logan, JA, Reniere, J and Powell, JA (2003) Assessing the impacts of global climate change on forest pests. Frontiers in Ecology 1, 130–137.CrossRefGoogle Scholar
Mathers, HM (2005) Screening Malus seedlings for cold hardiness. Hortscience A Publication of the American Society for Horticultural Science 40, 318–322.Google Scholar
Nakicenovic, N, Alcamo, J, Grubler, A, Riahi, K, Roehrl, RA, Rogner, H-H and Victor, N (2000) Special Report on Emissions Scenarios: A Special Report of Working Group III of the Intergovernmental Panel on Climate Change. Cambridge, UK: Cambridge University, Press.Google Scholar
Olfert, O, Weiss, RM and Kriticos, D (2011) Application of general circulation models to assess the potential impact of climate change on potential distribution and relative abundance of Melanoplus sanguinipes (Fabricius) (Orthoptera: Acrididae) in North America. Psyche: A Journal of Entomology 2011, 1–9.CrossRefGoogle Scholar
Parmesan, C, Ryrholm, N, Stefanescu, C, Hill, JK, Thomas, CD, Descimon, H, Huntley, B, Kaila, L, Kullberg, J, Tammaru, T, Tennent, WJ, Thomas, JA and Warren, M (1999) Poleward shifts in geographical ranges of butterfly species associated with regional warming. Nature 399, 579–583.CrossRefGoogle Scholar
Pimentel, D, Lach, L, Zuniga, R and Morrison, D (2000) Environmental and economic costs of nonindigenous species in the United States. Bioscience 50, 53–65.CrossRefGoogle Scholar
Poland, TM and Mccullough, DG (2006) Emerald ash borer: invasion of the urban forest and the threat to North America's ash resource. Journal of Forestry 104, 118–124.Google Scholar
Poole, EM, Ulyshen, MD, Horn, S, Cram, M, Olatinwo, R and Fraedrich, S (2019) Biology and distribution of Agrilus macer LeConte (Coleoptera: Buprestidae), a species associated with sugarberry (Celtis laevigata Willd.) mortality in the southeastern USA. Annals of Forest Science 76, 1–14.CrossRefGoogle Scholar
Singer, MC and Parmesan, C (2010) Phenological asynchrony between herbivorous insects and their hosts: signal of climate change or pre-existing adaptive strategy? Philosophical Transactions of the Royal Society of London 365, 3161–3176.CrossRefGoogle ScholarPubMed
Staentzel, C, Combroux, I, Barillier, A, Grac, C, Chanez, E and Beisel, J (2019) Effects of a river restoration project along the Old Rhine River (France-Germany): response of macroinvertebrate communities. Ecological Engineering 127, 114–124.CrossRefGoogle Scholar
Sun, YZ, Liang, YY and Sun, H (1979) Studies apple buprestid (Agrilus mali Mats.) in Shanxi. Journal of Northwest A & F University (Natural Science Edition) 2, 47–56.Google Scholar
Sutherst, RW and Maywald, GF (1985) A computerised system for matching climates in ecology. Agriculture Ecosystems & Environment 13, 281–299.CrossRefGoogle Scholar
Sutherst, RW, Baker, RHA, Coakley, SM, Harrington, R and Scherm, H (2007) Pests Under Global Change – Meeting Your Future Landlords? New York: Springer, Berlin Heidelberg.CrossRefGoogle Scholar
Tao, Y, Li, Q, Chen, X, Philippe, DM, Xue, Y, Liu, Y, Zhao, TB and Li, LH (2019) Spatiotemporal variability of the precipitation concentration and diversity in Central Asia. Atmospheric Research 241, 1–28.Google Scholar
Taylor, KE, Stouffer, RJ and Meehl, GA (2012) An overview of CMIP5 and the experiment design. Bulletin of the American Meteorological Society 93, 485–498.CrossRefGoogle Scholar
Velasco, R, Zharkikh, A, Affourtit, J, Dhingra, A, Cestaro, A, Kalyanaraman, A, Fontana, P, Bhatnagar, SK, Troggio, M and Pruss, D (2010) The genome of the domesticated apple (Malus × domestica Borkh.). Nature Genetics 42, 833–839.CrossRefGoogle ScholarPubMed
Virkkala, R and Lehikoinen, A (2014) Patterns of climate-induced density shifts of species: poleward shifts faster in northern boreal birds than in southern birds. Global Change Biology 20, 2995–3003.CrossRefGoogle ScholarPubMed
Vitousek, PM, Dantonio, CM, Loope, LL, Rejmanek, M and Westbrooks, R (1997) Introduced species: a significant component of human-caused global change. New Zealand Journal of Ecology 21, 1–16.Google Scholar
Walther, GR, Post, E, Convey, P, Menzel, A, Parmesan, C, Beebee, TJC, Fromentin, JM, Hoegh-Guldberg, O and Bairlein, F (2002) Ecological responses to recent climate change. Nature 416, 389–395.CrossRefGoogle ScholarPubMed
Wang, ZY, Zhang, YL, Yang, ZQ and Wang, XY (2013) Determination of larval instars of Agrilus mali Matsumura (Coleoptera: Buprestidae). Forest Research 26, 786–789.Google Scholar
Yi, ZH, Liu, DG, Cui, XN and Shang, ZM (2016) Morphology and ultrastructure of antennal sensilla in male and female Agrilus mali (Coleoptera: Buprestidae). Journal of Insect Science 16, 86, 81–10.CrossRefGoogle ScholarPubMed
Zhang, ZQ, Jiao, S, Li, XH and Li, ML (2018) Bacterial and fungal gut communities of Agrilus mali at different developmental stages and fed different diets. Scientific Reports 8, 1–11.Google ScholarPubMed
Zhang, P, Lu, ZZ, Zhang, X, Zhao, XP, Zhang, YG, Tanabeko, G, Bagila, M, Zhanera, A and Cui, ZJ (2019) Age structure of Malus sieversii population in Ili of Xinjiang and Kazakhstan. Arid Zone Research 36, 844–853.Google Scholar
Zhang, P, Cui, ZJ, Xu, H, Ali, A and Lu, ZZ (2020) Thirst or malnutrition: the impacts of invasive insect Agrilus mali on the physiological status of wild apple tree. Forests 11, 440.CrossRefGoogle Scholar
Zhang, X, Zhang, YL, Zhang, P, Cui, ZJ, Han, P, Gao, GZ, Poland, TM, Zalucki, MP and Lu, ZZ (2021) Agrilus mali Matsumura (Coleoptera: Buprestidae) density and damage in wild apple Malus sieversii (Rosales: Rosaceae) forests in Central Eurasia under four different management strategies. Entomologia Generalis 41, 257–266.CrossRefGoogle Scholar
Supplementary material: File

Lu et al. supplementary material

Lu et al. supplementary material

Download Lu et al. supplementary material(File)
File 23.1 MB