Do atmospheric events explain the arrival of an invasive ladybird (Harmonia axyridis) in the UK?

Autoři: Pilvi Siljamo aff001;  Kate Ashbrook aff002;  Richard F. Comont aff002;  Carsten Ambelas Skjøth aff002
Působiště autorů: Meteorological Research, Finnish Meteorological Institute, Helsinki, Finland aff001;  School of Science & the Environment, University of Worcester, Worcester, England, United Kingdom aff002
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article
doi: 10.1371/journal.pone.0219335


Species introduced outside their natural range threaten global biodiversity and despite greater awareness of invasive species risks at ports and airports, control measures in place only concern anthropogenic routes of dispersal. Here, we use the Harlequin ladybird, Harmonia axyridis, an invasive species which first established in the UK from continental Europe in 2004, to test whether records from 2004 and 2005 were associated with atmospheric events. We used the atmospheric- chemistry transport model SILAM to model the movement of this species from known distributions in continental Europe and tested whether the predicted atmospheric events were associated with the frequency of ladybird records in the UK. We show that the distribution of this species in the early years of its arrival does not provide substantial evidence for a purely anthropogenic introduction and show instead that atmospheric events can better explain this arrival event. Our results suggest that air flows which may assist dispersal over the English Channel are relatively frequent; ranging from once a week from Belgium and the Netherlands to 1–2 times a week from France over our study period. Given the frequency of these events, we demonstrate that atmospheric-assisted dispersal is a viable route for flying species to cross natural barriers.

Klíčová slova:

Airports – Atmospheric chemistry – Belgium – France – Insect pests – Invasive species – Monte Carlo method – Weather


1. Bellard C, Genovesi P, Jeschke JM. Global patterns in threats to vertebrates by biological invasions. Proc R Soc B Biol Sci. 2016;283: 20152454. doi: 10.1098/rspb.2015.2454 26817767

2. Wittenberg R, Cock MJW, editors. Invasive Alien Species: A Toolkit of Best Prevention and Management Practices. Wallingford: CAB Internationa; 2001.

3. Hulme PE, Bacher S, Kenis M, Klotz S, Kühn I, Minchin D, et al. Grasping at the routes of biological invasions: a framework for integrating pathways into policy. J Appl Ecol. 2008;45: 403–414. doi: 10.1111/j.1365-2664.2007.01442.x

4. Diamond J. “Normal” extinctions of isolated populations. In: Nitecki MH, editor. Extintions. Chigago: Chicago University Press; 1984. pp. 191–246.

5. Millennium Ecosystem Assessment. Ecosystems and Human Well-Being (Synthesis). Washington, DC; 2005. Available:

6. UKNEA. (UK National Ecosystem Assessment), The UK National Ecosystem Assessment: Technical Report). UNEP-WCMC. 2011.

7. Combat Invasive Alien Species–Target 5—Environment—European Commission. [cited 9 Nov 2018]. Available:

8. Pimentel D, McNair S, Janecka J, Wightman J, Simmonds C, O’Connell C, et al. Economic and environmental threats of alien plant, animal, and microbe invasions. Agric Ecosyst Environ. 2001;84: 1–20. doi: 10.1016/S0167-8809(00)00178-X

9. Williams F, Eschen R, Harris A, Djeddour D, Pratt C, Shaw RS, et al. The economic cost of invasive non-native species on Great Britain. Wallingford: CABI; 2010. Available:

10. Lodge DM. Biological invasions: Lessons for ecology. Trends Ecol Evol. 1993;8: 133–137. doi: 10.1016/0169-5347(93)90025-K 21236129

11. Williamson M, Fitter A. The Varying Success of Invaders. Ecology. 1996;77: 1661–1666. doi: 10.2307/2265769

12. Davis MA, Thompson K. Eight ways to be a colonizer: two ways to be an invader: a proposed nomenclature scheme for invasion ecology. Bull Ecol Soc Am. 2000;81: 226–230.

13. Manchester SJ, Bullock JM. The impacts of non-native species on UK biodiversity and the effectiveness of control. J Appl Ecol. 2000;37: 845–864. doi: 10.1046/j.1365-2664.2000.00538.x

14. Roy HE, Peyton J, Aldridge DC, Bantock T, Blackburn TT, Britton R, et al. Horizon scanning for invasive alien species with the potential to threaten biodiversity in Great Britain. Glob Chang Biol. 2014;20: 3859–3871. doi: 10.1111/gcb.12603 24839235

15. Turbelin AJ, Malamud BD, Francis RA. Mapping the global state of invasive alien species: patterns of invasion and policy responses. Glob Ecol Biogeogr. 2017;26: 78–92. doi: 10.1111/geb.12517

16. Lacasella F, Marta S, Singh A, Stack Whitney K, Hamilton K, Townsend P, et al. From pest data to abundance-based risk maps combining eco-physiological knowledge, weather, and habitat variability. Ecol Appl. 2017;27: 575–588. doi: 10.1002/eap.1467 27859850

17. Hulme PE. Climate change and biological invasions: evidence, expectations, and response options. Biol Rev. 2017;92: 1297–1313. doi: 10.1111/brv.12282 27241717

18. Roy HE, Hesketh H, Purse B V., Eilenberg J, Santini A, Scalera R, et al. Alien Pathogens on the Horizon: Opportunities for Predicting their Threat to Wildlife. Conserv Lett. 2017;10: 477–484. doi: 10.1111/conl.12297

19. Dick JTA, Laverty C, Lennon JJ, Barrios-O’Neill D, Mensink PJ, Robert Britton J, et al. Invader Relative Impact Potential: a new metric to understand and predict the ecological impacts of existing, emerging and future invasive alien species. Souza L, editor. J Appl Ecol. 2017;54: 1259–1267. doi: 10.1111/1365-2664.12849

20. Rejmánek M. Invasive plants: approaches and predictions. Austral Ecol. 2000;25: 497–506. doi: 10.1046/j.1442-9993.2000.01080.x

21. Branch GM, Nina Steffani C. Can we predict the effects of alien species? A case-history of the invasion of South Africa by Mytilus galloprovincialis (Lamarck). J Exp Mar Bio Ecol. 2004;300: 189–215. doi: 10.1016/J.JEMBE.2003.12.007

22. THUILLER W, RICHARDSON DM, PYSEK P, MIDGLEY GF, HUGHES GO, ROUGET M. Niche-based modelling as a tool for predicting the risk of alien plant invasions at a global scale. Glob Chang Biol. 2005;11: 2234–2250. doi: 10.1111/j.1365-2486.2005.001018.x

23. Kolar CS, Lodge DM. Ecological predictions and risk assessment for alien fishes in North America. Science. 2002;298: 1233–6. doi: 10.1126/science.1075753 12424378

24. Early R, Bradley BA, Dukes JS, Lawler JJ, Olden JD, Blumenthal DM, et al. Global threats from invasive alien species in the twenty-first century and national response capacities. Nat Commun. 2016;7: 12485. doi: 10.1038/ncomms12485 27549569

25. van Lenteren JC, Loomans AJM, Babendreier D, Bigler F. Harmonia axyridis: an environmental risk assessment for Northwest Europe. From Biological Control to Invasion: the Ladybird Harmonia axyridis as a Model Species. Dordrecht: Springer Netherlands; 2007. pp. 37–54. doi: 10.1007/978-1-4020-6939-0_4

26. Robinet C, Liebhold AM. Dispersal polymorphism in an invasive forest pest affects its ability to establish. Ecol Appl. 2009;19: 1935–1943. Available: doi: 10.1890/08-1971.1 19831081

27. Essl F, Dullinger S, Rabitsch W, Hulme PE, Hülber K, Jarošík V, et al. Socioeconomic legacy yields an invasion debt. Proc Natl Acad Sci U S A. 2011;108: 203–7. doi: 10.1073/pnas.1011728108 21173227

28. Roy HE, Brown PMJ, Adriaens T, Berkvens N, Borges I, Clusella-Trullas S, et al. The harlequin ladybird, Harmonia axyridis: global perspectives on invasion history and ecology. Biol Invasions. 2016;18: 997–1044. doi: 10.1007/s10530-016-1077-6

29. Hodek I, Honěk A. Ecology of Coccinellidae. Dordrecht: Springer Netherlands; 1996. doi: 10.1007/978-94-017-1349-8

30. Raak-van den Berg CL, Hemerik L, de Jong PW, van Lenteren JC. Mode of overwintering of invasive Harmonia axyridis in the Netherlands. BioControl. 2012;57: 71–84. doi: 10.1007/s10526-011-9394-2

31. Roy HE, Brown PMJ. Ten years of invasion: Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) in Britain. Ecol Entomol. 2015;40: 336–348. doi: 10.1111/een.12203 26435571

32. Roy HE, Adriaens T, Isaac NJB, Kenis M, Onkelinx T, Martin GS, et al. Invasive alien predator causes rapid declines of native European ladybirds. Divers Distrib. 2012;18: 717–725. doi: 10.1111/j.1472-4642.2012.00883.x

33. Brown PMJ, Thomas CE, Lombaert E, Jeffries DL, Estoup A, Lawson Handley L-J. The global spread of Harmonia axyridis (Coleoptera: Coccinellidae): distribution, dispersal and routes of invasion. BioControl. 2011;56: 623–641. doi: 10.1007/s10526-011-9379-1

34. Brown PMJ, Roy HE, Rothery P, Roy DB, Ware RL, Majerus MEN. Harmonia axyridis in Great Britain: analysis of the spread and distribution of a non-native coccinellid. BioControl. 2008;53: 55–67. doi: 10.1007/s10526-007-9124-y

35. Kukkonen J, Olsson T, Schultz DM, Baklanov A, Klein T, Miranda AI, et al. A review of operational, regional-scale, chemical weather forecasting models in Europe. Atmos Chem Phys. 2012;12: 1–87. doi: 10.5194/acp-12-1-2012

36. Stohl A, Seibert P, Wotawa G, Arnold D, Burkhart JF, Eckhardt S, et al. Xenon-133 and caesium-137 releases into the atmosphere from the Fukushima Dai-ichi nuclear power plant: determination of the source term, atmospheric dispersion, and deposition. Atmos Chem Phys. 2012;12: 2313–2343. doi: 10.5194/acp-12-2313-2012

37. Sofiev M, Berger U, Prank M, Vira J, Arteta J, Belmonte J, et al. MACC regional multi-model ensemble simulations of birch pollen dispersion in Europe. Atmos Chem Phys. 2015;15: 8115–8130. doi: 10.5194/acp-15-8115-2015

38. Leskinen M, Markkula I, Koistinen J, Pylkkö P, Ooperi S, Siljamo P, et al. Pest insect immigration warning by an atmospheric dispersion model, weather radars and traps. J Appl Entomol. 2011;135: 55–67. doi: 10.1111/j.1439-0418.2009.01480.x

39. Roy H, Brown P, Frost R, Poland R. Ladybirds (Coccinellidae) of Britain and Ireland. BRC Atlases SP3. Centre for Ecology & Hydrology Natural Environment Research Council (NERC); 2011. Available:

40. Brown PMJ, Adriaens T, Bathon H, Cuppen J, Goldarazena A, Hägg T, et al. Harmonia axyridis in Europe: spread and distribution of a non-native coccinellid. BioControl. 2008;53: 5–21. doi: 10.1007/s10526-007-9132-y

41. Comont RF, Ashbrook K. Evaluating promotional approaches for citizen science biological recording: bumblebees as a group versus Harmonia axyridis as a flagship for ladybirds. BioControl. 2017;62: 309–318. doi: 10.1007/s10526-016-9771-y

42. Baddeley A, Rubak E, Turner R. Spatial point patterns: methodology and applications with R. Available:

43. Juhász L, Hochmair HH. Where to catch ‘em all?–a geographic analysis of Pokémon Go locations. Geo-spatial Inf Sci. 2017;20: 241–251. doi: 10.1080/10095020.2017.1368200

44. Sofiev M, Siljamo P, Valkama I, Ilvonen M, Kukkonen J. A dispersion modelling system SILAM and its evaluation against ETEX data. Atmos Environ. 2006;40: 674–685. doi: 10.1016/j.atmosenv.2005.09.069

45. Sofiev M, Vira J, Kouznetsov R, Prank M, Soares J, Genikhovich E. Construction of the SILAM Eulerian atmospheric dispersion model based on the advection algorithm of Michael Galperin. Geosci Model Dev. 2015;8: 3497–3522. doi: 10.5194/gmd-8-3497-2015

46. Paatero J, Vira J, Siitari-Kauppi M, Hatakka J, Holmén K, Viisanen Y. Airborne fission products in the high Arctic after the Fukushima nuclear accident. J Environ Radioact. 2012;114: 41–47. doi: 10.1016/j.jenvrad.2011.12.027 22300482

47. Saarnio K, Aurela M, Timonen H, Saarikoski S, Teinilä K, Mäkelä T, et al. Chemical composition of fine particles in fresh smoke plumes from boreal wild-land fires in Europe. Sci Total Environ. 2010;408: 2527–2542. doi: 10.1016/j.scitotenv.2010.03.010 20359735

48. Vira J, Carboni E, Grainger RG, Sofiev M. Variational assimilation of IASI SO<sub>2</sub> plume height and total column retrievals in the 2010 eruption of Eyjafjallajökull using the SILAM v5.3 chemistry transport model. Geosci Model Dev. 2017;10: 1985 doi: 10.5194/gmd-10-1985-2017

49. Sofiev M, Siljamo P, Ranta H, Rantio-Lehtimäki A. Towards numerical forecasting of long-range air transport of birch pollen: theoretical considerations and a feasibility study. Int J Biometeorol. 2006;50: 392–402. doi: 10.1007/s00484-006-0027-x 16596367

50. Siljamo P, Sofiev M, Filatova E, Grewling Ł, Jäger S, Khoreva E, et al. A numerical model of birch pollen emission and dispersion in the atmosphere. Model evaluation and sensitivity analysis. Int J Biometeorol. 2013;57: 125–36. doi: 10.1007/s00484-012-0539-5 22434484

51. Sofiev M, Siljamo P, Ranta H, Linkosalo T, Jaeger S, Rasmussen A, et al. A numerical model of birch pollen emission and dispersion in the atmosphere. Description of the emission module. Int J Biometeorol. 2013;57: 45–58. doi: 10.1007/s00484-012-0532-z 22410824

52. Sofiev M, Berger U, Prank M, Vira J, Arteta J, Belmonte J, et al. MACC regional multi-model ensemble simulations of birch pollen dispersion in Europe. Atmos Chem Phys. 2015;15: 8115–8130. doi: 10.5194/acp-15-8115-2015

53. Sofiev M, Ritenberga O, Albertini R, Arteta J, Belmonte J, Bernstein CG, et al. Multi-model ensemble simulations of olive pollen distribution in Europe in 2014: current status and outlook. Atmos Chem Phys. 2017;17: 12341–12360. doi: 10.5194/acp-17-12341-2017

54. Karl M, Jonson JE, Uppstu A, Aulinger A, Prank M, Sofiev M, et al. Effects of ship emissions on air quality in the Baltic Sea region simulated with three different chemistry transport models. Atmos Chem Phys. 2019;19: 7019–7053. doi: 10.5194/acp-19-7019-2019

55. Petersen AK, Brasseur GP, Bouarar I, Flemming J, Gauss M, Jiang F, et al. Ensemble forecasts of air quality in eastern China–Part 2: Evaluation of the MarcoPolo–Panda prediction system, version 1. Geosci Model Dev. 2019;12: 1241–1266. doi: 10.5194/gmd-12-1241-2019

56. Veriankaitė L, Siljamo P, Sofiev M, Šaulienė I, Kukkonen J. Modelling analysis of source regions of long-range transported birch pollen that influences allergenic seasons in Lithuania. Aerobiologia (Bologna). 2010;26: 47–62. doi: 10.1007/s10453-009-9142-6

57. Wainwright CE, Stepanian PM, Reynolds DR, Reynolds AM. The movement of small insects in the convective boundary layer: linking patterns to processes. Sci Rep. 2017;7: 5438. doi: 10.1038/s41598-017-04503-0 28710446

58. Chapman JW, Reynolds DR, Mouritsen H, Hill JK, Riley JR, Sivell D, et al. Wind Selection and Drift Compensation Optimize Migratory Pathways in a High-Flying Moth. Curr Biol. 2008;18: 514–518. doi: 10.1016/j.cub.2008.02.080 18394893

59. Cardé RT. Insect Migration: Do Migrant Moths Know Where They Are Heading? Curr Biol. 2008;18: R472–R474. doi: 10.1016/j.cub.2008.04.018 18522818

60. Dingle H, Drake VA. What Is Migration? Bioscience. 2007;57: 113–121. doi: 10.1641/B570206

61. Chapman JW, Reynolds DR, Wilson K. Long-range seasonal migration in insects: mechanisms, evolutionary drivers and ecological consequences. Ecol Lett. 2015;18: 287–302. doi: 10.1111/ele.12407 25611117

62. Wu Q-L, Hu G, Westbrook JK, Sword GA, Zhai B-P. An Advanced Numerical Trajectory Model Tracks a Corn Earworm Moth Migration Event in Texas, USA. Insects. 2018;9: 115. doi: 10.3390/insects9030115 30189679


64. Showers WB, Keaster AJ, Raulston JR, Hendrix WH, Derrick ME, McCorcle MD, et al. Mechanism of Southward Migration of a Noctuid Moth [Agrotis Ipsilon (Hufnagel)]: A Complete Migrant. Ecology. 1993;74: 2303–2314. doi: 10.2307/1939583

65. Srygley RB, Dudley R. Optimal strategies for insects migrating in the flight boundary layer: mechanisms and consequences. Integr Comp Biol. 2007;48: 119–133. doi: 10.1093/icb/icn011 21669778

66. Grez AA, Rand TA, Zaviezo T, Castillo-Serey F. Land use intensification differentially benefits alien over native predators in agricultural landscape mosaics. Bradley B, editor. Divers Distrib. 2013;19: 749–759. doi: 10.1111/ddi.12027

67. Jeffries DL, Chapman J, Roy HE, Humphries S, Harrington R, Brown PMJ, et al. Characteristics and Drivers of High-Altitude Ladybird Flight: Insights from Vertical-Looking Entomological Radar. Warrant EJ, editor. PLoS One. 2013;8: e82278. doi: 10.1371/journal.pone.0082278 24367512

68. Johnson C. Migrationand dispersal of insects by flight. By Johnson C. G. London (Methuen). London: Methuen; 1969. doi: 10.1002/qj.49709640721

69. Brown PMJ, Roy DB, Harrower C, Dean HJ, Rorke SL, Roy HE. Spread of a model invasive alien species, the harlequin ladybird Harmonia axyridis in Britain and Ireland. Sci Data. 2018;5: 180239. doi: 10.1038/sdata.2018.239 30351305

70. Camacho-Cervantes M, Ortega-Iturriaga A, del-Val E. From effective biocontrol agent to successful invader: the harlequin ladybird (Harmonia axyridis) as an example of good ideas that could go wrong. PeerJ. 2017;5: e3296. doi: 10.7717/peerj.3296 28533958

71. Alford AV. Potential problems posed by non-indigenous terrestrial flatworms in the United Kingdom. Pedobiologia (Jena). 1998;42: 574–578.

72. Fox R, Conrad KF, Parsons MS, Warren MS, Woiwod I. The state of Britain’s larger moths. Wareham, Dorset: Butterfly Conservation and Rothamsted Research; 2006. Available:

73. Roy H, Lewington R, Brown P. Field Guide to the Ladybirds of Great Britain and Ireland. Bloomsbury Wildlife; 2018. Available:

74. Walter A, Bliss P, Moritz RFA, Moritz RFA. The wasp spider Argiope bruennichi (Arachnida, Araneidae): ballooning is not an obligate life history phase. J Arachnol. 2005;33: 516–522. doi: 10.1636/04-78.1

75. Gardiner T. Macropterism of Roesel’s Bushcricket Metrioptera roeselii in Relation to Climate Change and Landscape Structure in Eastern England. J Orthoptera Res. 2009;18: 95–102. doi: 10.1665/034.018.0110

76. Vickery VR. Factors governing the Distribution and Dispersal of the Recently Introduced Grasshopper, Metrioptera roeselii (Hgb.) (Orthoptera:Ensifera. Ann la Société Entomol Québec. 1965;10: 165–172.

77. Kumschick S, Fronzek S, Entling MH, Nentwig W. Rapid spread of the wasp spider Argiope bruennichi across Europe: a consequence of climate change? Clim Change. 2011;109: 319–329. doi: 10.1007/s10584-011-0139-0

78. Krehenwinkel H, Tautz D. Northern range expansion of European populations of the wasp spider Argiope bruennichi is associated with global warming-correlated genetic admixture and population-specific temperature adaptations. Mol Ecol. 2013;22: 2232–2248. doi: 10.1111/mec.12223 23496675

79. Hulme PE, Roy DB, Cunha T, Larsson T-B. A pan-European inventory of alien species: rationale, implementation and implications for managing biological invasions. DAISIE, Handbook of Alien Species in Europe. Dordrecht: Springer Netherlands; 2009. pp. 1–14. doi: 10.1007/978-1-4020-8280-1

80. Facon B, Crespin L, Loiseau A, Lombaert E, Magro A, Estoup A. Can things get worse when an invasive species hybridizes? The harlequin ladybird Harmonia axyridis in France as a case study. Evol Appl. 2011;4: 71–88. doi: 10.1111/j.1752-4571.2010.00134.x 25567954

81. Lawson Handley L-J, Estoup A, Evans DM, Thomas CE, Lombaert E, Facon B, et al. Ecological genetics of invasive alien species. BioControl. 2011;56: 409–428. doi: 10.1007/s10526-011-9386-2

82. ESTOUP A GUILLEMAUD T. Reconstructing routes of invasion using genetic data: why, how and so what? Mol Ecol. 2010;19: 4113–4130. doi: 10.1111/j.1365-294X.2010.04773.x 20723048

83. MUIRHEAD JR, GRAY DK, KELLY DW, ELLIS SM, HEATH DD, MACISAAC HJ. Identifying the source of species invasions: sampling intensity vs. genetic diversity. Mol Ecol. 2008;17: 1020–1035. doi: 10.1111/j.1365-294X.2008.03669.x 18261046

84. Comont RF, Roy HE, Harrington R, Shortall CR, Purse B V. Ecological correlates of local extinction and colonisation in the British ladybird beetles (Coleoptera: Coccinellidae). Biol Invasions. 2014;16: 1805–1817. doi: 10.1007/s10530-013-0628-3

85. López S, González M, Goldarazena A. Vespa velutina Lepeletier, 1836 (Hymenoptera: Vespidae): first records in Iberian Peninsula. EPPO Bull. 2011;41: 439–441. doi: 10.1111/j.1365-2338.2011.02513.x

86. Grosso-Silva J, Maia M. Vespa velutina Lepeletier, 1836 (Hymenoptera, Vespidae), new species for Portugal. Arq Entomolóxicos. 2012; 53–54. Available:

87. Rome Q. Spread of the invasive hornet Vespa velutina Lepeletier, 1836, in Europe in 2012 (Hym., Vespidae). Bull Soc Entomol Fr. 2013;118: 21–22. Available:

88. CABI. Vespa velutina (Asian Hornet). In: Invasive Species Compendium [Internet]. 2018. Available:

89. Monceau K, Bonnard O, Thiéry D. Vespa velutina: a new invasive predator of honeybees in Europe. J Pest Sci (2004). 2014;87: 1–16. doi: 10.1007/s10340-013-0537-3

90. Asian Hornet, Vespa velutina—GB non-native species secretariat. [cited 8 Nov 2018]. Available:

91. Asian hornet: UK sightings in 2018—GOV.UK. [cited 7 Jun 2019]. Available:

Článek vyšel v časopise


2020 Číslo 1