Eur. J. Entomol. 115: 703-707, 2018 | DOI: 10.14411/eje.2018.069
Effect of aphid abundance and urbanization on the abundance of Harmonia axyridis (Coleoptera: Coccinellidae)Original article
- Crop Research Institute, Drnovska 507, CZ-16106 Praha 6 - Ruzyně, Czech Republic; e-mails: honek@vurv.cz, martinkova@vurv.cz, strobach@vurv.cz
The factors that affect the local distribution of the invasive Harmonia axyridis are not yet completely resolved. Hypotheses predicting positive and independent effects of prey abundance and degree of urbanization on the adult abundance of this species in Central Europe were tested. Populations of H. axyridis were sampled in a period when it was most abundant, by sweeping lime trees (Tilia spp.) at 28 sites along a 20 km transect across urban (western Prague) and surrounding rural areas. The sites differed in aphid abundance (number of Eucallipterus tiliae per 100 sweeps) and degree of urbanization (percentage of the surrounding area within a 500 m radius covered by impervious human constructions). Multiple linear regression analysis of log-transformed data revealed that abundance of H. axyridis (number of adults per 100 sweeps) increased significantly with both aphid abundance (P = 0.015) and urbanization (P = 0.045). The positive relationship between degree of urbanization and abundance of H. axyridis was thus not a side effect of variation in aphid abundance, which was also greater in urban than rural areas. The effect of urbanization might constrict the habitat available to H. axyridis and force this species to aggregate in urban green "refugia". These results point to a plurality of factors that determine coccinellid abundance at natural sites.
Keywords: Aphididae, Eucallipterus tiliae, Coleoptera, Coccinellidae, Harmonia axyridis, Tilia, tree, abundance, distribution, population, urbanization
Received: October 17, 2018; Revised: November 29, 2018; Accepted: November 29, 2018; Published online: December 17, 2018 Show citation
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References
- Adriaens T., San Martin y Gomez G. & Maes D. 2008: Invasion history, habitat preferences and phenology of the invasive ladybird Harmonia axyridis in Belgium. - BioControl 53: 69-88.
Go to original source... - Andrade R., Bateman H.L. & Kang Y. 2017: Seasonality and land cover characteristics drive aphid dynamics in an arid city. - J. Arid. Environ. 144: 12-20.
Go to original source... - Bidinger K., Lötters S., Rödder D. & Veith M. 2012: Species distribution models for the alien invasive Asian Harlequin ladybird (Harmonia axyridis). - J. Appl. Entomol. 136: 109-123.
Go to original source... - Brown P.M.J., Adriaens T., Bathon H., Cuppen J., Goldarazena A., Hägg T., Kenis M., Klausnitzer B.E.M., Kovar I., Loomans A.J.M. et al. 2008: Harmonia axyridis in Europe: spread and distribution of a non-native coccinellid. - BioControl 53: 5-21.
Go to original source... - Brown P.M.J., Thomas C.E., Lombaert E., Jeffries D.L., Estoup A. & Lawson Handley L.J. 2011: The global spread of Harmonia axyridis (Coleoptera: Coccinellidae): distribution, dispersal and routes of invasion. - BioControl 56: 623-641.
Go to original source... - Ceryngier P. & Romanowski J. 2017: Harmonia axyridis (Pallas, 1773) (Coleoptera: Coccinellidae) and its parasite in south-western Bulgaria and northern Greece. - Bioinvasions Rec. 6: 307-310.
Go to original source... - Colares F., Michaud J.P., Bain C.L. & Torres J.B. 2015: Recruitment of aphidophagous arthropods to sorghum plants infested with Melanaphis sacchari and Schizaphis graminum (Hemiptera: Aphididae). - Biol. Contr. 90: 16-24.
Go to original source... - Fluckiger W. & Braun S. 1999: Stress factors of urban trees and their relevance for vigour and predisposition for parasite attacks. In Lemattre M., Lemattre P. & Lemaire F. (eds): Proceeding of the International Symposium on Urban Tree Health, Paris, France, September 22, 1997. - Acta Horticulturae 496: 325-334.
Go to original source... - Gardiner M.M., Prajzner S.P., Burkman C.E., Albro S. & Grewal P.S. 2014: Vacant land conversion to community gardens: influences on generalist arthropod predators and biocontrol services in urban greenspaces. - Urban Ecosyst. 17: 101-122.
Go to original source... - Grez A.A., Zaviezo T., Hernandez J., Rodriguez-San Pedro A. & Acuna P. 2014: The heterogeneity and composition of agricultural landscapes influence native and exotic coccinellids in alfalfa fields. - Agr. Forest Entomol. 16: 382-390.
Go to original source... - Hanks L.M. & Denno R.F. 1993: Natural enemies and plant water relations influence the distribution of armored scale insect. - Ecology 74: 1081-1091.
Go to original source... - Hironori Y. & Katsuhiro S. 1997: Cannibalism and interspecific predation in two predatory ladybirds in relation to prey abundance in the field. - Entomophaga 42: 153-163.
Go to original source... - Hodek I. & Evans E.W. 2012: Food relationships. In Hodek I., van Emden H.F. & Honek A. (eds): Ecology and Behaviour of the Ladybird Beetles (Coccinellidae). Wiley-Blackwell, Chichester, pp. 141-274.
Go to original source... - Honek A. 2012: Distribution and habitats. In Hodek I., van Emden H.F. & Honek A. (eds): Ecology and Behaviour of the Ladybird Beetles (Coccinellidae). Wiley-Blackwell, Chichester, pp. 110-139.
Go to original source... - Honek A., Martinkova Z. & Dixon A.F.G. 2015: Detecting seasonal variation in composition of adult Coccinellidae communities. - Ecol. Entomol. 40: 543-552.
Go to original source... - Honek A., Dixon A.F.G., Soares A.O., Skuhrovec J. & Martinkova Z. 2017: Spatial and temporal changes in the abundance and composition of ladybird (Coleoptera: Coccinellidae) communities. - Curr. Opin. Insect Sci. 14: 61-67.
Go to original source... - Honek A., Martinkova Z., Roy H.E., Dixon A.F.G., Skuhrovec J., Pekár S. & Brabec M. 2018: Differences in the phenology of Harmonia axyridis (Coleoptera: Coccinellidae) and native coccinellids in Central Europe. - Environ. Entomol. [in press] doi: 10.1093/ee/nvy173.
Go to original source... - Jovicic I., Radonjic A. & Petrovic-Obradovic O. 2016: Aphids (Hemiptera: Aphididae) on alfalfa and their coccinellid predators in Serbia: seasonal abundance. - Acta Zool. Bulg. 68: 581-587.
- Korotayev B.A. 2013: On high abundance of the harlequin lady beetle Harmonia axyridis (Pall.) (Coleoptera, Coccinellidae) in the plains of the north western Caucasus, Russia. - Entomol. Rev. 92: 856-858.
- Kovar I. 2007: Coccinellidae. In Löbl I. & Smetana A. (eds): Catalogue of Palaearctic Coleoptera. Vol. 4. Apollo Books, Stenstrup, pp. 568-631.
- Latibari M.H., Moravvej G., Namaghi H.S. & Khormizi M.Z. 2016: Coccinellid biodiversity on the coniferous trees Thuja orientalis and Pinus mugo in urban landscape of Mashhad, Razavi Khorasan Province, Iran. - Egypt. J. Biol. Pest Contr. 26: 419-421.
- Lu Z.B., Shi P.J., Reddy G.V.P., Li L.M., Men X.Y. & Ge F. 2015: Nonparametric estimation of interspecific spatio-temporal niche separation between two lady beetles (Coleoptera: Coccinellidae) in Bt cotton fields. - Ann. Entomol. Soc. Am. 108: 807-813.
Go to original source... - Mackos-Iwaszko E., Lubiarz M. & Karczmarz K. 2015: The impact of urban conditions on the occurrence of aphids on Acer platanoides L. - Acta Sci. Polon. Hort. Cult. 14: 189-207.
- Mukwevho V.O., Pryke J.S. & Roets F. 2017: Habitat preferences of the invasive harlequin ladybeetle Harmonia axyridis (Coleoptera: Coccinellidae) in the western Cape Province, South Africa. - Afr. Entomol. 25: 86-97.
Go to original source... - Osawa N. 2000: Population field studies on the aphidophagous ladybird beetle Harmonia axyridis (Coleoptera: Coccinellidae): resource tracking and population characteristics. - Popul. Ecol. 42: 115-127.
Go to original source... - Osawa N. 2005: The effect of prey availability on ovarian development and oosorption in the ladybird beetle Harmonia axyridis (Coleoptera: Coccinellidae). - Eur. J. Entomol. 102: 503-511.
Go to original source... - Osawa N. 2011: Ecology of Harmonia axyridis in natural habitats within its native range. - BioControl 56: 613-621.
Go to original source... - Ovchinnikova A.A., Ovchinnikov A.N., Dolgovskaya M.Y.U., Reznik S.Ya. & Belyakova N.A. 2016: Trophic induction of diapause in native and invasive populations of Harmonia axyridis (Coleoptera: Coccinellidae). - Eur. J. Entomol. 113: 469-475.
Go to original source... - Philpott S.M. & Bichier P. 2017: Local and landscape drivers of predation services in urban gardens. - Ecol. Appl. 27: 966-976.
Go to original source... - Poutsma J., Loomans A.J.M., Aukema B. & Heijerman T. 2008: Predicting the potential geographical distribution of the harlequin ladybird, Harmonia axyridis, using the CLIMEX model. - BioControl 53: 103-125.
Go to original source... - Rocha E.A. & Fellowes M.D.E. 2018: Does urbanization explain differences in interactions between an insect herbivore and its natural enemies and mutualists? - Urban Ecosyst. 21: 405-417.
Go to original source... - Rocha E.A., Souza E.N.F., Bleakley L.A.D., Burley C., Mott J.L., Rue-Glutting G. & Fellowes M.D.E. 2018: Influence of urbanisation and plants on the diversity and abundance of aphids and their ladybird and hoverfly predators in domestic gardens. - Eur. J. Entomol 115: 140-149.
Go to original source... - Roy H.E., Brown P.M.J., Adriaens T., Berkvens N., Borges I., Clusella Trullas S., Comont R., De Clercq P., Eschen R., Estoup A. et al. 2016: The harlequin ladybird, Harmonia axyridis: global perspectives on invasion history and ecology. - Biol. Invas. 18: 997-1044.
Go to original source... - Seagraves M.P. 2009: Lady beetle oviposition behavior in response to the trophic environment. - Biol. Contr. 51: 313-322.
Go to original source... - Sienkiewicz-Paderewska D., Dmuchowski W., Baczewska A.H., Bragoszewska P. & Gozdowski D. 2017: The effect of salt stress on lime aphid abundance on Crimean linden (Tilia 'Euchlora') leaves. - Urban For. Urban Green. 21: 74-79.
Go to original source... - Sloggett J.J. 2017: Harmonia axyridis (Coleoptera: Coccinellidae): smelling the rat in native ladybird declines. - Eur. J. Entomol. 114: 455-461.
Go to original source... - Soares A.O., Honek A., Martinkova Z., Skuhrovec J., Cardoso P. & Borges I. 2017: Harmonia axyridis did not establish in the Azores: the role of species richness, intraguild interactions and resource availability. - BioControl 62: 423-434.
Go to original source... - Systat Software Inc. 2006: SigmaStat 3.5. Systat Software Inc. Point Richmond, CA
- Tomov R., Trencheva K., Trenchev G. & Kenis M. 2009: The Multicolored invasive Asian ladybird Harmonia axyridis (Pallas, 1773) (Coleoptera: Coccinellidae) new to the fauna of Bulgaria. - Acta Zool. Bulgar. 61: 307-311.
- Ukrainsky A.S. & Orlova-Bienkowskaja M.J. 2014: Expansion of Harmonia axyridis Pallas (Coleoptera: Coccinellidae) to European Russia and adjacent regions. - Biol. Invas. 16: 1003-1008.
Go to original source... - Veran S., Piry S., Ternois V., Meynard C.N., Facon B. & Estoup A. 2016: Modeling spatial expansion of invasive alien species: relative contributions of environmental and anthropogenic factors to the spreading of the harlequin ladybird in France. - Ecography 39: 665-675.
Go to original source... - Viglasova S., Nedved O., Zach P., Kulfan J., Parak M., Honek A., Martinkova Z. & Roy H.E. 2017: Species assemblages of ladybirds including the harlequin ladybird Harmonia axyridis: a comparison at large spatial scale in urban habitats. - BioControl 62: 409-421.
Go to original source... - Wagner L.S., Fenoglio M.S. & Salvo A. 2017: Alien species numerically dominate natural enemy communities in urban habitats: a preliminary study. - J. Entomol. Res. Soc. 19: 31-42.
Go to original source... - With K.A., Pavuk D.M., Worchuck J.L., Oates R.K. & Fisher J.L. 2002: Threshold effects of landscape structure on biological control in agroecosystems. - Ecol. Appl. 12: 52-65.
Go to original source... - Zakharov I.A. 2015: [Harmonia in Moscow.] - Priroda 2015: 92-93 [in Russian].
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