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Published in $HURELRORJLD ± which should be cited to refer to this work. Is the recent decrease in airborne Ambrosia pollen in the Milan area due to the accidental introduction of the ragweed leaf beetle Ophraella communa? M. Bonini . B. Sˇikoparija . M. Prentovic´ . G. Cislaghi . P. Colombo . C. Testoni . L. Grewling . S. T. E. Lommen . H. Mu¨ller-Scha¨rer . M. Smith Abstract This study aims to determine whether a pollen data (2000–2013) were examined for trends over significant decrease in airborne concentrations of Am- time and correlated with meteorological data. The brosia pollen witnessed in the north-west of the amount of Ambrosia pollen recorded annually during Province of Milan in Northern Italy could be explained the main flowering period of Ambrosia (August– by environmental factors such as meteorology, or September) was entered into linear regression models whether there is evidence to support the hypothesis that with meteorological data in order to determine whether the decrease was related to the presence of large the amount of airborne Ambrosia pollen recorded in numbers of the oligophagous Ophraella communa leaf 2013 was lower than would normally be expected based beetles that are used as a biological control agent against on the prevailing weather conditions. There were a Ambrosia in other parts of the world. Airborne concen- number of significant correlations between concentra- trations of Ambrosia, Cannabaceae and Urticaceae tions of airborne Ambrosia, Cannabaceae and Urti- caceae pollen, as well as between airborne pollen concentrations and daily and monthly meteorological M. Bonini (&) Á G. Cislaghi Á P. Colombo Á C. Testoni data. The linear regression models greatly overestimat- Department of Medical Prevention, Public Health, Local ed the amount of airborne Ambrosia pollen in 2013. The Health Authority of Milan 1, Parabiago (Mi), Italy http://doc.rero.ch results of the regression analysis support the hypothesis e-mail: [email protected] that the observed decrease in airborne Ambrosia pollen B. Sˇikoparija Á M. Prentovic´ may indeed be related to the presence of large numbers Laboratory for Palynology, Department of Biology and of O. communa in the Milan area, as the drastic decrease Ecology, Faculty of Sciences, University of Novi Sad, in airborne Ambrosia pollen in 2013 cannotbe explained Novi Sad, Serbia by meteorology alone. M. Prentovic´ Department of Oto-Rhino-Laryngology, Research Group Keywords Aerobiology Á Ragweed Á Ophraella Aerobiology and Pollen information, Medical University communa Á Biocontrol agent of Vienna, Vienna, Austria L. Grewling Á M. Smith Laboratory of Aeropalynology, Faculty of Biology, Adam 1 Introduction Mickiewicz University, Poznan´, Poland Ambrosia maritima L. is the only Ambrosia (ragweed) S. T. E. Lommen Á H. Mu¨ller-Scha¨rer Department Biology, University of Fribourg, Fribourg, species native to Europe; three other species of Switzerland Ambrosia (A. psilostachya, A. tenuifolia and A. trifida) 1 were introduced to Europe from North America in should be considered a troublesome introduction or shipments of agricultural products (Smith et al. 2013). whether it is likely to become the first case of a Of these introduced species, the invasive alien successful biological control of an invasive weed in Ambrosia artemisiifolia L. (common or short rag- continental Europe. weed) is the most widely distributed and as such is Ophraella communa is multivoltine in that it considered to be an import weed in agriculture and produces three or four generations per year, with an source of highly allergenic pollen, which causes egg-to-egg generation time of about 4 weeks (Futuy- symptoms of pollen allergy in late summer and ma et al. 1993). Females lay eggs every few days for a autumn and reportedly induces asthma about twice month or more, with the fecundity exceeding 2700 as often as other pollen types (Dahl et al. (1999) and eggs/female (Futuyma et al. 1993; Zhou et al. 2010b). references therein). The survival rate of eggs and larvae is higher, and the The Rhoˆne Valley (France), parts of Northern Italy, development periods shorter, when temperature and the Pannonian Plain (i.e. predominantly Hungary but humidity are increased (Zhou et al. 2010a, b; Zhu et al. also parts of Austria, Bosnia and Herzegovina, Croa- 2012). Both the larva and imago feed on leaves of A. tia, Czech Republic, Romania, Serbia, Slovakia and artemisiifolia (Wan et al. 2009). O. communa can Slovenia) and Ukraine are considered to be the most significantly suppress plant height and the number of important sources of Ambrosia pollen in Europe branches (Guo et al. 2011), and when beetle densities (Smith et al. (2013) references therein). Ambrosia are high enough, it can even kill all Ambrosia plants artemisiifolia is an anemophilous (wind pollinated) (Zhou et al. 2014), thus preventing the production of plant, the pollen grains of which can readily become seeds. Required densities are higher when plants are airborne when conditions are favourable. As with bigger, but even plants that were only experimentally other wind-pollinated plants, such as those belonging exposed to the beetles when they were already over to the Cannabaceae and Urticaceae families that 90 cm tall were successfully killed prior to seed flower at around the same time as Ambrosia, pollen production (Zhou et al. 2014). In addition, O. release and dispersal is aided by high temperature and communa has high dispersal potential (Tanaka and low relative humidity (Dahl et al. (2013) and refer- Yamanaka 2009). The flight distance has been ences therein). estimated to be approximately 25 km/day, with Ophraella communa LeSage 1986 (Coleoptera: potential range expansion of 329 km/year (Yamamura Chrysomelidae) is an oligophagous leaf beetle that et al. 2007; Tanaka and Yamanaka 2009). Taking into feeds on various plants species belonging to the tribe account the selective host-feeding preferences, high Heliantheae (Asteraceae), including A. artemisiifolia fecundity and dispersal potential, it is suggested that (Futuyma and MCCafferty 1990; Palmer and Goeden O. communa may be a potential biological control http://doc.rero.ch 1991). The beetle originates from North America agent against A. artemisiifolia (Teshler et al. 2002) (Futuyma and MCCafferty 1990) and has been although Ophraella slobodkini was a preferred candi- (accidentally) introduced to a number of other areas date species for the biological control of A. artemisi- worldwide, including Europe, where it was first ifolia in Europe, because it exclusively feeds on detected in 2013 (Takizawa et al. 1999; Meng and Li Ambrosia (Gerber et al. 2011). 2005;Mu¨ller-Scha¨rer et al. 2014). Despite extensive Ophraella communa beetles were observed feeding host-specificity tests carried out over the past two on Ambrosia artemisiifolia plants in several regions of decades (reviewed by Zhou et al. (2011)), there Northern Italy, especially near Milan (Bosio et al. remains a controversial debate mainly on whether 2014;Mu¨ller-Scha¨rer et al. 2014), during the summer the beetle can attack and damage sunflower, of 2013. The beetle was found on all observed ragweed Helianthus annuus L., in the field (cf. Mu¨ller-Scha¨rer populations. Individual A. artemisiifolia plants har- et al. (2014) and references therein). Therefore, host- boured up to over a hundred beetles, and many plants specificity tests both under quarantine and open-field were completely defoliated before the end of the conditions in Switzerland and Northern Italy and season (Mu¨ller-Scha¨rer et al. 2014). At the same time, including various sunflower varieties and Ambrosia it was noticed that routine pollen-monitoring stations species are presently underway (H. Mu¨ller-Scha¨rer, situated in three towns of the north-west area of the unpublished results) to decide on whether this beetle Province of Milan were recording less Ambrosia 2 pollen than usual. This study aims to determine examined, Ambrosia, Cannabaceae and Urticaceae, whether the observed decrease in airborne concentra- are routinely monitored. tions of Ambrosia pollen can be explained by The amount of Ambrosia pollen recorded annually environmental factors such as meteorology that are during the main flowering period of Ambrosia (August– known to strongly affect pollen release and dispersal, September) is presented (Annual Ambrosia Pollen— or whether there is evidence to support the hypothesis AAP). The mean AAP of all three sites combined was that the decrease was related to the presence of O. also examined and termed ‘‘Milan area’’. In addition, the communa in the area. amounts of Cannabaceae pollen (Annual Cannabaceae Pollen—ACP) and Urticaceae pollen (Annual Urti- caceae Pollen—AUP) recorded during August–Septem- 2 Materials and methods ber at Legnano were included in the study as these taxa contain species that flower in August–September. As a 2.1 Airborne pollen data result, the amount of these pollen types in the air can be assumed to be influenced by similar meteorological Daily average pollen concentrations were collected at factors as Ambrosia. We therefore hypothesised that if three sites in the north-west area of the Province of airborne Cannabaceae and Urticaceae pollen concen- Milan, Northern Italy, from 2000 to 2013 (Fig. 1). trations do not follow a similar trend as Ambrosia pollen, Pollen data were collected by volumetric spore trap of i.e. the ACP and AUP did not decrease in the same way the Hirst design (Hirst 1952). The pollen-monitoring as AAP, then weather conditions during the period of sites were the towns of Legnano (ITMIL6), Magenta pollen release are unlikely to be the main factor affecting (ITMAGE) and Rho (ITRHO1). Legnano is the closest airborne Ambrosia pollen concentrations. This would pollen-monitoring site to the meteorological stations, provide support for the hypothesis that the observed and so pollen data from this site were used throughout decrease in AAP was due to the presence of O. communa the analysis. Legnano is also the only pollen-monitor- in the area, rather than meteorology.

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