Abstract
In temperate regions, generalist insect pests are expected to use multiple habitats and host plant species over the different seasons. Landscape composition and configuration can also provide a diversity of thermal resources and host plants that can modify insect activity and movement. Here, we described the seasonal spatial distribution of a destructive invasive pest, spotted wing drosophila (SWD), along a gradient of landscape composition (i.e. proportion of forest habitat) and configuration (i.e. length of forest edge). We selected a triplet of habitat patches (forest, vineyard and grassland) in 17 landscapes in North-eastern Italy characterised by different proportions of forest and forest edge length and monitored pest activity density for 1 year. We found that during the cold season, SWD mostly occupied forest habitats, which were suitable overwintering sites due to ideal microclimatic conditions. During plant-growing season, SWD occurred equally in the three habitats, probably due to warmer temperatures in open areas as well as high food and host availability. In summer, when high temperatures can be limiting, landscapes with large forest edge length presented an increase in activity density compared to landscapes with less amount of edges, irrespective of the total cover of forest. Large edge length indicated landscapes with high contact zones between forest and open habitats, probably favouring spillover of individuals in SWD. In the light of these results, pest control in crop fields located in landscapes with complex configurations can be particularly challenging. The high density in non-crop habitats suggests that this invasive species can have pervasive impact also on wild plant species occurring in semi-natural and natural habitats.
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References
Akaike H (2011) Akaike’s information criterion. In: International encyclopedia of statistical science. Springer, Berlin, pp 25–25. https://doi.org/10.1007/978-3-642-04898-2_110
Andersen JL, Manenti T, Sørensen JG, Macmillan H, Loeschcke V, Overgaard J (2015) How to assess Drosophila cold tolerance: chill coma temperature and lower lethal temperature are the best predictors of cold distribution limits. Funct Ecol 29:55–65. https://doi.org/10.1111/1365-2435.12310
Asplen MK, Anfora G, Biondi A, Choi DS, Chu D, Daane KM, Gibert P, Gutierrez A, Hoelmer K, Hutchison W, Isaacs R, Jiang ZL, Kárpáti Z, Kimura MT, Pascual M, Philips CR, Plantamp C, Ponti L, Vétek G, Vogt H, Walton VM, Yu Y, Zappalà L, Desneux N (2015) Invasion biology of spotted wing drosophila (Drosophila suzukii): a global perspective and future priorities. J Pest Sci 88:469–494. https://doi.org/10.1007/s10340-015-0681-z
Barton K (2016) MuMIn: multi-model inference. R package version 1.15.1. 1:18
Bellamy DE, Sisterson MS, Walse SS (2013) Quantifying host potentials: indexing postharvest fresh fruits for spotted wing drosophila, Drosophila suzukii. PLoS ONE 8:e61227. https://doi.org/10.1371/journal.pone.0061227
Berger JS, Birkhofer K, Hanson HI, Hedlund K (2018) Landscape configuration affects herbivore–parasitoid communities in oilseed rape. J Pest Sci 91:1093–1105. https://doi.org/10.1007/s10340-018-0965-1
Bianchi FJJA, Booij CJH, Tscharntke T (2006) Sustainable pest regulation in agricultural landscapes: a review on landscape composition, biodiversity and natural pest control. Proc Biol Sci 273:1715–1727. https://doi.org/10.1098/rspb.2006.3530
Bianchi FJJA, Goedhart PW, Baveco JM (2008) Enhanced pest control in cabbage crops near forest in the Netherlands. Landsc Ecol 23:595–602. https://doi.org/10.1007/s10980-008-9219-6
Biondi A, Traugott M, Desneux N (2016) Special issue on Drosophila suzukii: from global invasion to sustainable control. J Pest Sci 89:603–604
Blitzer EJ, Dormann CF, Holzschuh A, Klein AM, Rand TA, Tscharntke T (2012) Spillover of functionally important organisms between managed and natural habitats. Agric Ecosyst Environ 146:34–43. https://doi.org/10.1016/j.agee.2011.09.005
Block W, Baust JG, Franks F, Johnston IA, Bale J (1990) Cold tolerance of insects and other arthropods [and discussion]. Philos Trans R Soc B Biol Sci 326:613–633. https://doi.org/10.1098/rstb.1990.0035
Burgess L (1981) Winter sampling to determine overwintering sites and estimate density of adult flea beetle pests of rape (Coleoptera: Chrysomelidae). Can Entomol 113:441–447. https://doi.org/10.4039/Ent113441-5
Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer, Berlin
Burnham KP, Anderson DR (2004) Multimodel inference. Understanding AIC and BIC in model selection. Sociol Methods Res 33:261–304. https://doi.org/10.1177/0049124104268644
Cahenzli F, Bühlmann I, Daniel C, Fahrentrapp J (2018) The distance between forests and crops affects the abundance of Drosophila suzukii during fruit ripening, but not during harvest. Environ Entomol. https://doi.org/10.1093/ee/nvy116
Calabria G, Máca J, Bächli G, Serra L, Pascual M (2012) First records of the potential pest species Drosophila suzukii (Diptera: Drosophilidae) in Europe. J Appl Entomol 136:139–147. https://doi.org/10.1111/j.1439-0418.2010.01583.x
Chabert S, Allemand R, Poyet M, Eslin P, Gilbert P (2012) Ability of European parasitoids (Hymenoptera) to control a new invasive Asiatic pest, Drosophila suzukii. Biol Control 63:40–47. https://doi.org/10.1016/j.biocontrol.2012.05.005
Daane KM, Wang X, Biondi A, Miller B, Miller JC, Riedl H, Shearer PW, Guerrieri E, Giorgini M, Buffington M, van Achterberg K, Song Y, Kang T, Yi H, Jung C, Dong Woon Lee DW, Chung B, Hoelmer KA, Walton VM (2016) First exploration of parasitoids of Drosophila suzukii in South Korea as potential classical biological agents. J Pest Sci 89:823–835. https://doi.org/10.1007/s10340-016-0740-0
Deutsch CA, Tewksbury JJ, Huey RB, Sheldon KS, Ghalambor CK, Haak DC, Martin PR (2008) Impacts of climate warming on terrestrial ectotherms across latitude. Proc Natl Acad Sci USA 105:6668–6672. https://doi.org/10.1073/pnas.0709472105
Duflot R, Georges R, Ernoult A, Aviron S, Burel F (2014) Landscape heterogeneity as an ecological filter of species traits. Acta Oecol 56:19–26. https://doi.org/10.1016/j.actao.2014.01.004
Enriquez T, Colinet H (2017) Basal tolerance to heat and cold exposure of the spotted wing drosophila, Drosophila suzukii. PeerJ 5:e3112. https://doi.org/10.7717/peerj.3112
Ewers RM, Didham RK (2008) Pervasive impact of large-scale edge effects on a beetle community. Proc Natl Acad Sci 105:5426–5429. https://doi.org/10.1073/pnas.0800460105
Fahrig L (2003) Effects of habitat fragmentation on biodiversity. Annu Rev Ecol Evol Syst 34:487–515. https://doi.org/10.1146/annurev.ecolsys.34.011802.132419
Gelman A (2008) Scaling regression inputs by dividing by two standard deviations. Stat Med 27:2865–2873. https://doi.org/10.1002/sim.3107
González E, Salvo A, Defagó MT, Valladares G (2016) A moveable feast: insects moving at the forest-crop interface are affected by crop phenology and the amount of forest in the landscape. PLoS ONE 11:1–19. https://doi.org/10.1371/journal.pone.0158836
Google Inc. © (2017) Google Earth Pro
Gravesen E, Toft S (1987) Grass fields as reservoirs for polyphagous predators (Arthropoda) of aphids (Homopt., Aphididae). J Appl Entomol 104:461–473. https://doi.org/10.1111/j.1439-0418.1987.tb00547.x
Hamby KA, Bellamy DE, Chiu JC, Lee JC, Walton VM, Wiman NG, York RM, Biondi A (2016) Biotic and abiotic factors impacting development, behavior, phenology, and reproductive biology of Drosophila suzukii. J Pest Sci 89:605–619. https://doi.org/10.1007/s10340-016-0756-5
Haro-Barchin E, Scheper J, Ganuza C, De Groot GA, Colombari F, van Kats R, Kleijn D (2018) Landscape-scale forest cover increases the abundance of Drosophila suzukii and parasitoid wasps. Basic Appl, Ecol
Hauser M (2011) A historic account of the invasion of Drosophila suzukii (Matsumura) (Diptera: Drosophilidae) in the continental United States, with remarks on their identification. Pest Manag Sci 67:1352–1357. https://doi.org/10.1002/ps.2265
Hennig EI, Mazzi D (2018) Spotted wing drosophila in sweet cherry orchards in relation to forest characteristics, bycatch, and resource availability. Insects 9:118. https://doi.org/10.3390/insects9030118
Hermann A, Brunner N, Hann P, Wrbka T, Kromp B (2013) Correlations between wireworm damages in potato fields and landscape structure at different scales. J Pest Sci 86:41–51. https://doi.org/10.1007/s10340-012-0444-z
Hodkinson ID (2005) Terrestrial insects along elevation gradients: species and community responses to altitude. Biol Rev 80:489–513. https://doi.org/10.1017/S1464793105006767
Ioriatti C, Walton V, Dalton D, Anfora G, Grassi A, Maistri S, Mazzoni V (2015) Drosophila suzukii (Diptera: Drosophilidae) and its potential impact to wine grapes during harvest in two cool climate wine grape production regions. J Econ Entomol 108:1148–1155. https://doi.org/10.1093/jee/tov042
Karp DS, Chaplin-Kramer R, Meehan TD, Martin EA et al (2018) Crop pests and predators exhibit inconsistent responses to surrounding landscape composition. Proc Natl Acad Sci. https://doi.org/10.1073/pnas.1800042115
Kenis M, Tonina L, Eschen R, van der Sluis B, Sancassani M, Mori N, Haye T, Helsen H (2016) Non-crop plants used as hosts by Drosophila suzukii in Europe. J Pest Sci 89:735–748. https://doi.org/10.1007/s10340-016-0755-6
Kimura MT (1988) Adaptations to temperate climates and evolution of overwintering strategies in the Drosophila melanogaster species group. Evolution (N Y) 42:1288–1297. https://doi.org/10.2307/2409012
Klick J, Yang WQ, Walton VM, Dalton DT, Hagler JR, Dreves AJ, Lee JC, Bruck DJ (2016) Distribution and activity of Drosophila suzukii in cultivated raspberry and surrounding vegetation. J Appl Entomol 140:37–46. https://doi.org/10.1111/jen.12234
Knoll V, Ellenbroek T, Romeis J, Collatz J (2017) Seasonal and regional presence of hymenopteran parasitoids of Drosophila in Switzerland and their ability to parasitize the invasive Drosophila suzukii. Sci Rep 7:1–11. https://doi.org/10.1038/srep40697
Lee JC, Bruck DJ, Dreves AJ, Ioriatti C, Vogt H, Baufeld P (2011) In focus: spotted wing drosophila, Drosophila suzukii, across perspectives. Pest Manag Sci 67:1349–1351. https://doi.org/10.1002/ps.2271
Lukacs PM, Burnham KP, Anderson DR (2010) Model selection bias and Freedman’s paradox. Ann Inst Stat Math 62:117–125. https://doi.org/10.1007/s10463-009-0234-4
Marino PC, Landis DA (1996) Effect of landscape structure on parasitoid diversity and parasitism in agroecosystems. Ecol Appl 6:276–284
McGarigal K, Cushman SA, Ene E (2012) FRAGSTATS v4: spatial pattern analysis program for categorical and continuous maps. University of Massachusetts, Amherst. https://www.umass.edu/landeco
Mitsui H, Beppu K, Kimura MT (2010) Seasonal life cycles and resource uses of flower- and fruit-feeding drosophilid flies (Diptera: Drosophilidae) in central Japan. Entomol Sci 13:60–67. https://doi.org/10.1111/j.1479-8298.2010.00372.x
Nicholls CI, Parrella M, Altieri MA (2001) The effects of a vegetational corridor on the abundance and dispersal of insect biodiversity within a northern California organic vineyard. Landsc Ecol 16:133–146. https://doi.org/10.1023/A:1011128222867
Pelton E, Gratton C, Isaacs R, van Timmeren S, Blanton A, Guédot C (2016) Earlier activity of Drosophila suzukii in high woodland landscapes but relative abundance is unaffected. J Pest Sci 89:725–733. https://doi.org/10.1007/s10340-016-0733-z
Pelton E, Gratton C, Guédot C (2017) Susceptibility of cold hardy grapes to Drosophila suzukii (Diptera: Drosophilidae). J Appl Entomol 141:644–652. https://doi.org/10.1111/jen.12384
Poyet M, Le Roux V, Gibert P, Meirland A, Prévost G, Eslin P, Chabrerie O (2015) The wide potential trophic niche of the asiatic fruit fly Drosophila suzukii: the key of its invasion success in temperate Europe? PLoS ONE 10:e0142785. https://doi.org/10.1371/journal.pone.0142785
QGIS Development Team (2014) Quantum GIS geographic information system
R Core Team (2018) R: a language and environment for statistical computing
Rolland C (2003) Spatial and seasonal variations of air temperature lapse rates in alpine regions. J Clim 16:1032–1046. https://doi.org/10.1175/1520-0442(2003)016%3c1032:SASVOA%3e2.0.CO;2
Rossi Stacconi MV, Kaur R, Mazzoni V, Ometto L, Grassi A, Gottardello A, Rota-Stabelli O, Anfora G (2016) Multiple lines of evidence for reproductive winter diapause in the invasive pest Drosophila suzukii: useful clues for control strategies. J Pest Sci 89:689–700. https://doi.org/10.1007/s10340-016-0753-8
Rossi Stacconi MV, Panel A, Baser N, Ioriatti C, Pantezzi T, Anfora G (2017) Comparative life history traits of indigenous Italian parasitoids of Drosophila suzukii and their effectiveness at different temperatures. Biol Control 112:20–27. https://doi.org/10.1016/j.biocontrol.2017.06.003
Sakai M (2005) Cherry Drosophila suzukii, in primary color pest and disease encyclopedia. In: Rural Culture Association Japan (ed) Apples, cherries, European pears and walnuts, 2nd edn. Rural Culture Association Japan, Tokyo, pp 489–492
Santoiemma G, Fioretto D, Corcos D, Mori N, Marini L (2018a) Spatial synchrony in Drosophila suzukii population dynamics along elevational gradients. Ecol Entomol. https://doi.org/10.1111/en.12688
Santoiemma G, Mori N, Tonina L, Marini L (2018b) Semi-natural habitats boost Drosophila suzukii populations and crop damage in sweet cherry. Agric Ecosyst Environ 257:152–158. https://doi.org/10.1016/j.agee.2018.02.013
Scheffers BR, Edwards DP, Diesmos A, Williams SE, Evans TA (2014) Microhabitats reduce animal’s exposure to climate extremes. Glob Chang Biol 20:495–503. https://doi.org/10.1111/gcb.12439
Schellhorn NA, Bianchi FJJA, Hsu CL (2014) Movement of entomophagous arthropods in agricultural landscapes: links to pest suppression. Annu Rev Entomol 59:559–581. https://doi.org/10.1146/annurev-ento-011613-161952
Sears MW, Angilletta MJ (2015) Costs and benefits of thermoregulation revisited: both the heterogeneity and spatial structure of temperature drive energetic costs. Am Nat 185:E94–E102. https://doi.org/10.1086/680008
Shearer PW, West JD, Walton VM, Brown PH, Svetec N, Chiu JC (2016) Seasonal cues induce phenotypic plasticity of Drosophila suzukii to enhance winter survival. BMC Ecol 16:11. https://doi.org/10.1186/s12898-016-0070-3
Sivakoff FS, Rosenheim JA, Dutilleul P, Carrière Y (2013) Influence of the surrounding landscape on crop colonization by a polyphagous insect pest. Entomol Exp Appl 149:11–21. https://doi.org/10.1111/eea.12101
Steingröver EG, Geertsema W, van Wingerden WKRE (2010) Designing agricultural landscapes for natural pest control: a transdisciplinary approach in the Hoeksche Waard (The Netherlands). Landsc Ecol 25:825–838. https://doi.org/10.1007/s10980-010-9489-7
Stephens AR, Asplen MK, Hutchison WD, Venette RC (2015) Cold hardiness of winter-acclimated Drosophila suzukii (Diptera: Drosophilidae) adults. Environ Entomol 44:1619–1626. https://doi.org/10.1093/ee/nvv134
Tait G, Grassi A, Pfab F, Crava CM, Dalton DT, Magarey R, Ometto L, Vezzulli S, Rossi Stacconi MV, Gottardello A, Pugliese A, Firrao G, Walton VM, Anfora G (2018) Large-scale spatial dynamics of Drosophila suzukii in Trentino, Italy. J Pest Sci 91:1213–1224. https://doi.org/10.1007/s10340-018-0985-x
Tochen S, Dalton DT, Wiman N, Hamm C, Shearer PW, Walton VM (2014) Temperature-related development and population parameters for Drosophila suzukii (Diptera: Drosophilidae) on cherry and blueberry. Environ Entomol 43:501–510. https://doi.org/10.1603/EN13200
Tochen S, Walton VM, Lee JC (2016a) Impact of floral feeding on adult Drosophila suzukii survival and nutrient status. J Pest Sci 89:793–802. https://doi.org/10.1007/s10340-016-0762-7
Tochen S, Woltz JM, Dalton DT, Lee JC, Wiman NG, Walton VM (2016b) Humidity affects populations of Drosophila suzukii (Diptera: Drosophilidae) in blueberry. J Appl Entomol 140:47–57. https://doi.org/10.1111/jen.12247
Tonina L, Grassi A, Caruso S, Mori N, Gottardello A, Anfora G, Giomi F, Vaccari G, Ioratti C (2017) Comparison of attractants for monitoring Drosophila suzukii in sweet cherry orchards in Italy. J Appl Entomol. https://doi.org/10.1111/jen.12416
Tonina L, Mori N, Sancassani M, Dall’Ara P, Marini L (2018) Spillover of Drosophila suzukii between noncrop and crop areas: implications for pest management. Agric For Entomol. https://doi.org/10.1111/afe.12290
Tscharntke T, Rand TA, Bianchi FJJA (2005) The landscape context of trophic interactions: insect spillover across the crop-noncrop interface. Ann Zool Fennici 42:421–432. https://doi.org/10.2307/23735887
Tscharntke T, Karp DS, Chaplin-Kramer R, Batáry P 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
Walsh DB, Bolda MP, Goodhue RE, Dreves AJ, Lee JC, Bruck DJ, Walton VM, O’Neal SD, Zalom FG (2011) Drosophila suzukii (Diptera: Drosophilidae): invasive pest of ripening soft fruit expanding its geographic range and damage potential. J Integr Pest Manag 2:1–7. https://doi.org/10.1603/IPM10010
Wang XG, Stewart TJ, Biondi A, Chavez BA, Ingels C, Caprile J, Grant JA, Walton VM, Daane KM (2016) Population dynamics and ecology of Drosophila suzukii in Central California. J Pest Sci 89:701–712. https://doi.org/10.1007/s10340-016-0747-6
Wiman NG, Walton VM, Dalton DT, Anfora G et al (2014) Integrating temperature-dependent life table data into a matrix projection model for Drosophila suzukii population estimation. PLoS ONE 9:e106909. https://doi.org/10.1371/journal.pone.0106909
Wiman NG, Dalton DT, Anfora G, Biondi A et al (2016) Drosophila suzukii population response to environment and management strategies. J Pest Sci 89:653–665. https://doi.org/10.1007/s10340-016-0757-4
Woltz JM, Lee JC (2017) Pupation behavior and larval and pupal biocontrol of Drosophila suzukii in the field. Biol Control 110:62–69. https://doi.org/10.1016/j.biocontrol.2017.04.007
Wong JS, Cave AC, Lightle DM, Wf Mahaffee, Naranjo SE, Wiman NG, Woltz JM, Lee JC et al (2018) Drosophila suzukii flight performance reduced by starvation but not affected by humidity. J Pest Sci 91:1269–1278. https://doi.org/10.1007/s10340-018-1013-x
Acknowledgements
We are grateful to the farmers who allowed us to carry out the experiments on their land. We thank Bioibérica S.A. Company and Michele Brardinelli for providing Suzukii Trap® attractant. We thank three anonymous reviewers for providing insightful comments that improved the manuscript.
Funding
This work was supported by the European Union’s Seventh Framework Programme for Research, Technological Development and Demonstration, DROPSA [Grant Number 613678]. GS received a grant from Aldo Gini Foundation (Padova).
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Santoiemma, G., Trivellato, F., Caloi, V. et al. Habitat preference of Drosophila suzukii across heterogeneous landscapes. J Pest Sci 92, 485–494 (2019). https://doi.org/10.1007/s10340-018-1052-3
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DOI: https://doi.org/10.1007/s10340-018-1052-3