Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Biological weed control to relieve millions from Ambrosia allergies in Europe

Abstract

Invasive alien species (IAS) can substantially affect ecosystem services and human well-being. However, quantitative assessments of their impact on human health are rare and the benefits of implementing IAS management likely to be underestimated. Here we report the effects of the allergenic plant Ambrosia artemisiifolia on public health in Europe and the potential impact of the accidentally introduced leaf beetle Ophraella communa on the number of patients and healthcare costs. We find that, prior to the establishment of O. communa, some 13.5 million persons suffered from Ambrosia-induced allergies in Europe, causing costs of Euro 7.4 billion annually. Our projections reveal that biological control of A. artemisiifolia will reduce the number of patients by approximately 2.3 million and the health costs by Euro 1.1 billion per year. Our conservative calculations indicate that the currently discussed economic costs of IAS underestimate the real costs and thus also the benefits from biological control.

Introduction

As a consequence of globalisation, the number of biological invasions has substantially increased over the past decades, and new introductions do not appear to be slowing down1. IAS can have multiple effects on biodiversity and ecosystem services2 and incur significant economic costs3,4,5. However, while alien parasites, invertebrates and plants are known to cause public health problems6,7, only a few studies have attempted to quantify their impact on human well-being4,5,8. In a recent review of the economic impacts of invasive insects, Bradshaw et al.4 estimated that the health costs exceed US$6.9 billion per year globally. Yet, studies assesing the impact of invasive species on human health which have been published so far are considered to underestimate the real costs because they are regionally focused, disparate or not grounded in verifiable data4,5. This is of concern, as an accurate information of policy and management about the impact of IAS on human health and the potential savings due to the implementation of mitigation measures is essential to ensure that reasonable resources are invested and actions coordinated in IAS management9.

We apply an interdisciplinary approach to quantify the effects of allergenic pollen produced by common ragweed, Ambrosia artemisiifolia L., on human health in Europe. Common ragweed, a native to North America, has invaded different parts of the world10. In Europe, it is considered invasive in more than 30 countries10 and its spread and impact are likely to increase with changing climate11,12,13. Here we show that, prior to the establishment of the biological control agent Ophraella communa LeSage in 2013, some 13.5 (95% confidence interval (CI) 10.9–14.8) million persons suffered from Ambrosia-induced allergies in Europe, causing economic costs of approximately Euro 7.4 (CI 5.4–8.6) billion annually. Field studies in Italy prove evidence that O. communa can reduce A. artemisiifolia pollen production by 82%. By modelling the number of generations of O. communa across its suitable habitat range in Europe, we project that biological control of A. artemisiifolia will, once the leaf beetle has colonised its environmental niche, reduces the number of patients to approximately 11.2 (CI 8.6–12.9) million and the health costs to Euro 6.4 (CI 4.4–7.5) billion per year. Our estimates of the costs of A. artemisiifolia for public health are considerably higher than what has been reported previously, suggesting that the actual costs of IAS in Europe and the benefits from their management are underestimated.

Results

Effects of Ambrosia artemisiifolia on public health

Based on information from the European pollen monitoring programme, we mapped seasonal total ragweed pollen integrals in Europe during the period 2004–2012, i.e. before the accidental introduction of the North American leaf beetle O. communa. We interpolated data from 296 European pollen monitoring sites to a 10 ×10 km grid and extracted them for the European Union (EU) member states and the non-EU member states that are located within the boundaries of the EU (Fig. 1; Supplementary Note 1; Supplementary Figs. 1, 2; Supplementary Data 1).

Fig. 1: Interpolated seasonal pollen integrals for Ambrosia across Europe.
figure1

a Interpolated seasonal pollen integrals for Ambrosia (number of grains per cubic metre of air) across Europe before the establishment of Ophraella communa (data from 2004–2012). b Seasonal pollen integrals from 296 pollen monitoring stations were used to interpolate ragweed pollen exposure to a 10 × 10 km grid.

Pollen allergens produce clinical symptoms only among previously sensitised persons. Therefore, we mapped ragweed sensitisation rates in Europe by combining data on (a) the overall sensitisation rate among the general population, and (b) the ragweed sensitisation rates among the sensitised population (Supplementary Note 2, Supplementary Data 2). The interpolated map of ragweed sensitisation rates in the European population (Fig. 2) corresponds to that of total seasonal ragweed pollen integrals, with both highest pollen integrals and highest ragweed sensitisation rates found in the Pannonian plain, the Po plain and the Rhône valley. By multiplying the interpolated ragweed sensitisation rates with the European population at a 10 ×10 km grid cell size14, we estimated that currently 23.2 million persons in Europe are ragweed sensitised (Supplementary Data 3, 4). Taking into account that not all persons with a positive allergy test develop symptoms upon contact with the ragweed allergen, we corrected these numbers for clinical relevance15, resulting in an estimated 15.8 million persons in Europe with clinically relevant ragweed sensitisation (Supplementary Data 4). Our estimate is 37% lower than that published by Lake et al.12, which is largely due to our more accurate approach using interpolation of ragweed sensitisation rates based on a large number of geo-referenced locations compared to the region-based approach by Lake et al.12. We then determined the population with clinically relevant sensitisation that was exposed to ragweed pollen prior to the establishment of O. communa (Fig. 1). This approach resulted in a total of approximately 13.5 (CI 10.9–14.8) million persons in Europe, which likely suffered from seasonal ragweed pollen allergy prior to the arrival of O. communa (Supplementary Data 5).

Fig. 2: Interpolated percentage of ragweed sensitised persons in the European population.
figure2

a Interpolated percentage of ragweed sensitised persons in the European population. b Geographic distribution of studies assessing overall sensitisation rates among the general population in Europe. Size of points indicates overall sensitisation rates (%) among the persons tested. c Geographic distribution of studies assessing ragweed sensitisation rates among the sensitised human population in Europe. Size of points indicates ragweed sensitisation rates (%) among the sensitised persons tested. Studies are based on ragweed specific skin prick tests or circulating ragweed specific IgE tests.

To validate the estimated number of patients suffering from ragweed pollen allergy, we compared our European-wide assessment with detailed healthcare data from the Rhône-Alpes region in southeastern France16 (www.auvergne-rhone-alpes.ars.sante.fr/; Supplementary Data 6). For each of the region’s 313 communities, we calculated the average number of persons which got reimbursed for purchasing anti-allergy or anti-asthma medication during the ragweed flowering season and related them to the average seasonal total ragweed pollen integrals in the communities (the period from 2007 to 2015; Supplementary Figs. 3, 4). We found that seasonal total ragweed pollen counts were significantly correlated with the number of patients, with a 10% decrease in the seasonal total ragweed pollen counts resulting in an 8.4% reduction in the number of patients (Supplementary Fig. 5). With our interpolation approach used at the European level, we estimated that the average proportion of affected patients in the 313 communities in the Rhône-Alpes region was 3.2% (SD 2.2). This figure is similar to the proportion of the population in the communities receiving reimbursements for anti-allergy or anti-asthma medication (2.9%, SD 1.0). Thus, our approach to estimate the number of persons suffering from ragweed pollen allergy appears to be reasonably accurate.

To estimate the European-wide economic costs due to ragweed pollen allergy prior to the establishment of O. communa, we estimated European-wide treatment costs per patient and year based on the cost estimates summarised by Bullock et al.17 for nine European countries. The annual treatment costs varied between Euro 8.30 (for antihistamines in the Czech Republic) and Euro 8,060 (for treatment of asthma in Switzerland), with median treatment costs of Euro 565 per patient and year (Supplementary Note 3). To also account for socio-economic costs, we used the ratio between medical expenses and absence from work calculated for the Rhône-Alpes region (18.5%, Supplementary Data 6). This resulted in estimated annual costs of Euro 670 per patient, a lower and thus a more conservative estimate than the median costs for seasonal allergic rhinitis in Europe (Euro 964 per patient and year18). By weighting the treatment and lost work time costs at the country level using purchasing power parity (PPP)-adjusted health expenditures per capita for 2015, we found that the overall economic costs amount to approximately Euro 7.4 (CI 5.4–8.6) billion per year in Europe (Supplementary Note 3; Supplementary Data 7). Our cost estimates are approximately 8-fold higher than those presented by Bullock et al.17, which is only partly explained by their lower estimate of the medical treatment costs per patient (Euro 303). More importantly, Bullock et al.’s17 estimates of the number of people affected by ragweed allergy in Europe (between 0.84 and 4.18 million). Our calculations rely on an extensive dataset of observed pollen integrals and on a geospatial approach for calculating total number of patients in Europe using a large dataset of observed sensitisation rates. This suggest that our approach is more accurate concerning exposure and that previous numbers of patients have been substantially underestimated. This is supported by the fact that the healthcare data from the Rhône-Alpes region indicate that in this region alone some 200,000 persons per year received reimbursement for purchasing anti-allergy or anti-asthma medication during the ragweed flowering season16.

Projected impact of Ophraella communa

The establishment of O. communa in Europe in 2013 raised the question whether this leaf beetle, which is mass-reared and actively distributed in China for biological control of A. artemisiifolia19, might also contribute to the sustainable management of this plant invader in Europe20. In Northern Italy, where the beetle was first detected, up to 100% of A. artemisiifolia plants are attacked with damage levels high enough to completely prevent flowering of most ragweed plants20. Pollen monitoring studies in the Milan area revealed that the substantial drop in airborne ragweed pollen concentrations since the establishment of O. communa cannot be explained by meteorological factors21.

To assess whether the reduction in airborne Ambrosia pollen concentrations in Northern Italy indeed reflects the impact of O. communa on pollen production of A. artemisiifolia plants, we conducted a field experiment in the Po plain during which O. communa was excluded in replicated plots at two of three study sites. We found that O. communa reduced pollen production on average by 82% (73–100%; Fig. 3), which well corresponds to the drop in airborne pollen concentrations recorded in the Milano area since the establishment of this beetle21 (Supplementary Fig. 6). Hence, our findings support the notion that the observed drop in Ambrosia pollen integrals in Northern Italy is caused by O. communa.

Fig. 3: Impact of Ophraella communa on Ambrosia artemisiifolia pollen production.
figure3

Estimated Ambrosia artemisiifolia raceme density per year at three study sites in Northern Italy in the presence and absence of Ophraella communa. CO = Corbetta; GR = Grugliasco; MA = Magnago. GR- and MA- indicate plots from which O. communa was excluded by spraying insecticides. At Corbetta permission for insecticide application was not obtained. Boxplots represent the variation across plots within treatment and site, with the black dot as the median, the boxes representing the quartiles, the whiskers 1.5 times the interquartile range and the yellow dots the data points.

To estimate the potential impact of O. communa on ragweed pollen integrals at the European level, we developed species distribution models for A. artemisiifolia and O. communa based on worldwide occurrences and bioclimatic variables (Fig. 4; Supplementary Fig. 7). We conducted a field cage experiment along an altitudinal gradient in Northern Italy and determined an average growing degree days (GDD) value of 288.7 (Supplementary Data 8) for one generation of O. communa. This value was incorporated into the species distribution model to map the number of generations which O. communa is likely to complete across its environmental niche in Europe (Fig. 4). We then quantified the potential impact of O. communa on ragweed pollen integrals by matching the number of generations of the beetle with the interpolated seasonal pollen integrals (Supplementary Note 1). Based on the association between seasonal total pollen integrals and relative number of patients determined for the Rhône-Alpes region (Supplementary Fig. 5), we projected O. communa to reduce the number of patients to approximately 11.2 (CI 8.6–12.9) million once it will have colonised its entire environmental niche in Europe. This corresponds to an average reduction in the number of patients by 2.3 million (16.9%; Supplementary Fig. 8, Supplementary Data 5). Correspondingly, the approximated yearly economic costs are, when accounting for PPP among countries, projected to drop to Euro 6.4 (CI 4.4–7.5) billion. This reduction results in economic savings of approximately Euro 1.1 billion annually (Supplementary Data 7). Besides Northern Italy, where the beetle has already significantly reduced airborne pollen concentrations, our projections suggest that people in countries of the Balkan Peninsula will benefit most from the establishment of O. communa (Figs. 2 and 4; Supplementary Data 5).

Fig. 4: Modelled distribution of Ambrosia artemisiifolia and Ophraella communa in Europe.
figure4

The modelled distribution range of Ophraella communa includes the expected number of generations per year.

Discussion

Our study provides evidence that the impacts of common ragweed on human health and the economy are so far highly underestimated, but that biological control by O. communa might mitigate these impacts in parts of Europe. So far, host specificity studies with closely related crops, ornamentals and native endangered species indicate no significant negative impact of O. communa on non-target plants under field conditions20,22. The results of our interdisciplinary study justify a comprehensive risk:benefit assessment of O. communa, also regarding a possible deliberate distribution of this leaf beetle across the climatically suitable areas in Europe.

Estimates of the economic impact of biological invasions have provided important input in policy and management at the national and international level3,23. Our estimate of the costs incurred by A. artemisiifolia is in a similar range as the currently discussed overall economic costs of IAS in Europe24 (Euro 12 billion per year). We propose that future assessments of economic impacts of IAS should more thoroughly consider costs related to human health.

Methods

Ragweed pollen exposure map

The estimates of ragweed pollen exposure in Europe are based on the best available information on long-term exposure to Ambrosia pollen for the period from 2004 to 2012. The data were obtained from published work of the mean seasonal total Ambrosia pollen integrals from 296 observational sites found in most large urban regions of Europe (Fig. 1b). We incorporated data from all sites where seasonal pollen integrals cover at least five years in order to secure sufficient data points near and outside the main invasion fronts of A. artemisiifolia (Supplementary Note 1). The final dataset with 296 calibration points for Ambrosia pollen exposure both within and outside the EU was interpolated to a 10 × 10 km2 grid using the common European Geographical Reference System (GCS_ETRS_1989). The gridded data were then extracted for the study area which covers 42 countries within Europe and includes EU27 and the bordering non-EU member countries Albania, Serbia, Macedonia, Bosnia-Herzegovina, Kosovo, Montenegro, Iceland, Norway and Switzerland (Supplementary Fig. 1).

Map of ragweed sensitisation among the European population

The map of ragweed sensitisation rates among the population in Europe is based on a combination of two types of published studies: (a) overall sensitisation rates among the general population obtained from medical centres and (b) ragweed sensitisation rates among sensitised patients collected from medical centres. A thorough review of all European studies was conducted and all peer-reviewed studies based on skin prick and circulating specific Immunoglobulin E (IgE) testing were included, while questionnaire studies were excluded. The review provided 50 data sets on the sensitisation rate among the general population and 80 data sets on ragweed sensitisation among the sensitised population (Figs. 2b, 2c; Supplementary Note 2; Supplementary Data 2).

The two data sets (50 areas and 102 areas) were then interpolated to a 10 × 10 km grid using the common European Geographical reference system (GCS_ETRS_1989). After that, the gridded data were extracted for the study area. Resulting Ambrosia sensitisation rates among the European population were then calculated by multiplying the gridded overall sensitisation rates among the population with the ragweed sensitisation rates among sensitised persons. We used natural breaks in the data to classify the exposure and population data (Figs. 1 and 2). Considering that only a proportion of patients with positive skin prick test reactions express symptoms, we calculated the clinically relevant sensitised population by multiplying the ragweed sensitised population with the clinically relevant ragweed sensitisation rates at the country level15. When determining the population with clinically relevant sensitisation that was exposed to ragweed pollen prior to the establishment of O. communa, we excluded all locations with very low seasonal ragweed pollen estimates (<10 grains per cubic metre during the pollen season12).

Relationship between seasonal Ambrosia pollen integrals and patient numbers

The relationship between the seasonal Ambrosia pollen integrals and the number of patients was calculated with information from the database compiled by the ‘Agence régionale de santé Auvergne-Rhône-Alpes’ (www.auvergne-rhone-alpes.ars.sante.fr/) on health costs related to common ragweed allergies in the Rhône-Alpes region. The Rhône-Alpes region, which is since 1 January 2016 part of the new region Auvergne-Rhône-Alpes, lies in southeastern France and covers an area of 43’700 km2 with approximately 6.5 million inhabitants. The Rhône Valley, which runs north-south through the Rhône-Alpes region, reports the highest common ragweed infestation rates in France10 and, together with the Pannonian plain and Northern Italy, also the highest rates in Europe25.

Since 2007, the Regional Health Agency, in association with the National Aerobiological Monitoring Network, has been collecting data on the annual health costs of ragweed allergies in the Rhône-Alpes region26. These cost calculations are based on the consumption of medical care and medical goods by persons affiliated to the general health insurance scheme and cover 98.9% of all patients. The included costs relate to allergy medication, doctor consultations, allergy tests, oral desensitisation treatments and sick leave when linked to the prescription of anti-allergy drugs during ragweed flowering season (see Supplementary Data 3 for further explanations). The relationship between total seasonal ragweed pollen integrals and number of patients was calculated for the period 2007–2015 using data from all 313 communities in the Rhône-Alpes region (Supplementary Fig. 5). The number of patients is defined as the number of persons receiving reimbursement through the general health insurance scheme for purchasing anti-allergy or anti-asthma medication to treat allergies during the ragweed pollen season from July 7 to October 2126.

We interpolated the community-level pollen exposure from pollen data for 62 monitoring sites in France (Supplementary Fig. 3), using the same approach as for the calculation at the European level. Instead of interpolating the annual total pollen integrals at the grid-cell level, we used the community centroid as the central point for interpolation. We found the highest exposure in the area around Lyon and the area on both sides of the river Rhone which is consistent with the habitat preferences of the plant27 (see Supplementary Fig. 4).

The method for estimating the number of patients is likely to represent the lower bound of the overall effect since only those persons were included which were reimbursed for the consumption of allergy-related medication.

Besides A. artemisiifolia, some other plant species flowering in late summer or autumn also possess allergenic pollen, which may theoretically pose some challenges for allergy epidemiological studies. However, in southeastern France, the two other ragweed species (Ambrosia trifida L. and A. psilostachya DC.) are rare. Moreover, peak flowering of allergenic mugwort species, such as Artemisia vulgaris L., A. absinthium L. and A. verlotiorum Lamotte, is before and after the peak flowering season of common ragweed, and the season of airborne Artemisia pollen hardly overlaps with the season of airborne Ambrosia pollen28. Moreover, seasonal pollen integrals for Artemisia pollen are far lower in southeastern France (Supplementary Fig. 4b) and northern Italy (Supplementary Fig. 6d) than those for A. artemisiifolia and thus only marginally contribute to the consumption of allergy-related medication in these regions (Supplementary Note 3).

To obtain an estimate of the treatment effect, we averaged the total seasonal pollen integrals and the number of patients for each community and the period 2007–2015. We then log-transformed the data and estimated the relationship without a constant using the linear least squares approach. This approach forces the regression to go through the origin which is a necessary condition for modelling the causal relationship between pollen counts and patient numbers. Overall, the specified regression model fits the data well and explains a significant share of variation (Supplementary Fig. 5).

Impact of O. communa on pollen production

In 2014, we selected three sites in northern Italy where A. artemisiifolia and O. communa co-occurred (Corbetta: N45.4709 E8.9368, Magnago: N45.5707 E8.7855, Grugliasco: N45.0654 E7.5923). Half of each site was assigned to experimental exclusion of O. communa in an experimental block design, except for the site in Corbetta for which we did not obtain permission to apply insecticides. In each site-treatment combination, 14 permanent plots of 0.5 × 0.5 m2 were installed covering the range of Ambrosia densities in June 2014 after ragweed had successfully established, and ensuring similar densities across treatments within sites. Starting in July 2014, beetles were experimentally excluded from the blocks assigned by the biweekly application of insecticides while control blocks in these sites were treated with water only. In 2015 and 2016, treatments started in May (corresponding to the period where the first beetle generation of offspring from the overwintering adults develops) and lasted until O. communa disappeared from the sites in autumn. The insecticide treatment constituted of spraying three insecticides (including two contact insecticides and a systemic insecticide; for further details see Lommen et al.29). This method has no direct effects on seed and pollen output or pollen allergenicity of A. artemisiifolia29.

As a proxy for the yearly pollen production per plot30, we estimated the total raceme length rper plot in 2015 and 2016 following \(r = n \, \ast \, m \, \ast e^{v \, \ast \, \beta + \alpha }\), where \(n\) is the total number of A. artemisiifolia plants in the plot at the end of the season in September (excluding the new seedlings that had just appeared in Magnago in 2015 and which did not produce pollen anymore), \(m\) is the fraction of these A. artemisiifolia that had matured per site-treatment combination (as a proxy for the fraction of plants that had produced racemes), \(v\) is the mean log-transformed volume of the matured A. artemisiifolia in the plot (based on all or a sample of ca. 10 plants measured in the plot (N = 47 plots), or the site-treatment mean if no plants in the specific plot had been measured (N = 23 plots)), and \(\alpha\) and \(\beta\) are the intercept and the slope, respectively, of the linear relationship between the log-transformed total raceme length and the log-transformed volume of individual matured A. artemisiifolia, as assessed by a sample of 21 plants taken outside of the plots per site-treatment combination. The analysis excluded plots that contained no A. artemisiifolia plants in 2014 (as these may represent the absence of a soil seed bank), and all plots in one block in Grugliasco where grasses dominated and suppressed ragweed occurrence after 2014. As too few mature plants were available in Corbetta and Magnago in 2016, the respective raceme-volume relationships from 2015 were used instead. The estimated raceme lengths per plot were rescaled to represent racemes per square metre.

Since many plots were estimated to produce a raceme length of 0 (i.e. no racemes), we took a hurdle-model approach for the statistical analysis of the effect of treatment on the raceme length per plot. As in 2016 none of the control plots and all of the insecticide-treated plots produced racemes, we could only do this for the data from 2015. We first assessed the effect of treatment on the probability of a plot producing racemes in 2015 by a generalised linear mixed effect model (GLMER) with treatment as a fixed effect, site as a random effect, and a binomial error distribution, tested against the corresponding null-model. For those plots producing racemes in 2015, we then similarly assessed the effect of treatment on the total length of racemes produced by a GLMER with treatment as a fixed effect, site as a random effect, and a Poisson error distribution with a log-link, which was tested against the corresponding null-model. The models were then used to obtain fitted estimates of the probability to produce racemes and the total length of racemes produced for each treatment, and their product was an estimate of the density of racemes produced (in cm per m2).

In 2015 the insecticide treatment increased the probability of a plot to produce racemes from 0.26 (95% CI = 0.14–0.42) to 0.84 (95% CI = 0.37-0.98; χ12 = 17.496, p < 0.001). When considering plots with raceme production, insecticide-treated plots produced significantly higher densities of racemes than control plots (fitted average 905 cm/m2 versus 260 cm/m2, respectively; χ12 = 6573, p < 0.001). As mentioned above, in 2016 only insecticide-treated plots produced racemes (Fig. 3).

Species distribution models for A. artemisiifolia and O. communa

We collected occurrence data for A. artemisiifolia and O. communa worldwide from the literature, from online resources and from additional occurrence sources (see Appendix S2 in Sun et al.13). In summary, we used WORLDCLIM current climate data (developed by Hijmans et al.31) at 5-min spatial resolution to derive a set of meaningful predictors that are considered critical to plant or insect physiological function and survival of both species. The final model for A. artemisiifolia included annual mean temperature, isothermality, temperature seasonality, max temperature of warmest month, min temperature of coldest month, temperature annual range, mean temperature of driest quarter and an approximation of GDD based on monthly average temperatures (Thom’s formula). The final model for O. communa included max temperature of warmest month, temperature annual range, mean temperature of driest quarter, mean temperature of coldest quarter, precipitation of wettest month, precipitation of wettest quarter, precipitation of driest quarter, precipitation of coldest quarter and standard insect growing degree days (GDD > 13.3 °C as the minimum development threshold temperature for all immature stages according to Zhou et al.32)13. We modelled the current potential distribution for each species in Europe using the integrative modelling framework Biomod2 R-package33. The combination of different modelling techniques generating an ensemble of predictions is proposed as an optimal solution for dealing with the uncertainties of extrapolation34. Generalised linear models (GLM), generalised boosting models (GBM), random forest (RF), and maximum entropy (MAXENT) were therefore calibrated on a random sample of the initial data (80%) and tested on the remaining data sets (20%) with both the receiver-operating characteristic curve (ROC) and the true skill statistic (TSS). We then estimated their area under the curve (AUC) that evaluates the discriminatory power of model predictions. Above techniques were chosen because they have proven to presently be among the most effective species distribution models35. Duplicated presences within a raster pixel were removed. As only occurrences were available, random pseudo-absences were generated36 to fill the absence component of models. The entire training-evaluation procedure was repeated 100 times (25 times for each model), using a different set of calibrated presences and absences within each iteration to ensure robustness of the predictions and provide uncertainty estimates37. A stacked assemblage of predictions across individual models including mean, inferior confidence interval, superior confidence interval of both A. artemisiifolia and O. communa were generated. The suitability of species distributions of two species were then binary-transformed using species-specific thresholds maximising the rate of the number of corrected predicted presences to number of false absences (i.e., to transform the probabilities of presence into presence and absence). Based on these thresholds, we also binary-transformed all confidence interval predictions (Supplementary Fig. 7), which were later used for uncertainty estimation. In our models, AUC ranged from 0.87 to 0.96 across the two species and four model types, which provided useful information for an analysis of climate suitability through modelling of the species distributions. Finally, the overlap maps of O. communa on its host plant A. artemisiifolia that we used for later computations were produced based on their binary mean distribution maps, binary lower confidence interval maps and binary upper confidence interval maps (BIOMOD_EnsembleModeling function in Biomod2)13.

The number of generations of O. communa across the potential distribution in Europe was estimated by experimentally assessing the temperature-dependent developmental time of O. communa along an altitudinal gradient in the Southern Alps, approximately 50 km north of the Milan area. The five field sites were set up on sun-exposed grasslands or in private gardens at 130 m (in the Po plain), 250 m, 480 m, 700 m and 1230 m. Greenhouse-reared, potted A. artemisiifolia plants were exposed to female O. communa in a field cage set up at the lowest elevation. Plants with freshly laid egg batches were individually covered with a gauze bag, firmly attached to the pot with an elastic ribbon, and transferred within 48 h after oviposition to one of the five field sites in a randomised order. At the field site, A. artemisiifolia plants were placed within a 1 × 1 × 2 m gauze cage, dug together with the pots into the soil and regularly watered. Two cohorts of 5–8 plants each were transferred to the five field sites, with the exception of the highest site, which only received plants from the second cohort. The first cohort was set up between 29 June and 2 July 2016 and the second cohort between 8 and 10 August 2016. Each field site was visited at least once a week to record the presence of beetle life stages on each A. artemisiifolia plant. Based on the field study, we calculated an average GDD > 13.3°32 of 288.7 for the period from the egg stage to adult emergence of O. communa (Supplementary Data 8). This value closely corresponds to the GDD reported for O. communa by Zhou et al.32 which was based on growth chamber experiments with constant temperature regimes (307.2). We then used the GDD calculated from our field experiment to map the number of generations of O. communa in relation to the climatic conditions within its potential distribution range in Europe.

Impact of O. communa on airborne Ambrosia pollen concentration in Europe

To quantify the potential impact of O. communa on seasonal pollen integrals in Europe, we exploited retrospective data from northern Italy. We used data on ragweed pollen concentration (number of pollen per cubic metre of air) with a daily resolution for three monitoring sites in the Milan area for the period 2004–2018. The sites are located in proximity (less than 30 km) to the Malpensa airport, where the beetle was initially detected in 2013. Because common ragweed was already established in all potential habitats before the beetle’s arrival, we can calculate the pre-treatment exposure and compare it with the post-treatment exposure. For this purpose, we first obtained a measure of the average daily pollen integral for each station during the two periods and then calculated the average of pollen integrals over the three monitoring sites. Supplementary Fig. 6 shows the average impact of O. communa on daily pollen integrals in the Milan metropolitan area. The average impact of the beetle on ragweed pollen exposure is 86.3%, which implies that the average pollen integrals dropped from 46.2 to 7.5 pollen grains per cubic metre of air. We used this information to estimate the empirical reduction function of pollen concentration due to O. communa. For this purpose, we cumulated the daily pollen integrals before the arrival (2004-2012) and calculated the reduction in pollen concentration at the respective level of pollen concentration in the pre-arrival period. The impact of the beetle is stronger for the lower range of annual pollen concentration (above 90%) and levels out at 83.7% for the higher range (Supplementary Fig. 6b). In terms of human exposure to ragweed pollen, this resulted in a reduction of the number of days with ragweed pollen and reduced pollen integral during days with ragweed pollen (Supplementary Fig. 6c).

In Northern Italy, the population density of O. communa and the feeding damage increased significantly in August, which corresponds with the end of the beetle’s third generation. We thus assumed that all projected areas with at least three beetle generations face the same reduction in total seasonal ragweed pollen integrals as in the Milan area (86%; Supplementary Figs. 6a and 8). For areas with one or two generations we assumed a reduction in seasonal Ambrosia pollen integrals by 30%, due to a likewise reduction in plant densities by early feeding damage that is not compensated for during the growing season (Lommen, unpubl. results). For all other areas, we assumed no effect of O. communa on seasonal Ambrosia pollen integrals.

Reporting summary

Further information on research design is available in the Nature Research Reporting Summary linked to this article.

Data availability

The source data underlying Fig. 3 and Supplementary Fig. 6 are provided as a Source Data file. All data sets linked to spatial data sets have been deposited in https://eprints.worc.ac.uk/7124/ and can be made available upon request. The data that support the analysis of the percent persons suffering from ragweed allergies in the Rhône-Alpes region are available from the French Network of Aerobiological Monitoring (RNSA) but restrictions apply to the availability of these data, which were used under written agreement for the current study, and so are publicly not available. Data are however available from M. Thibaudon upon reasonable request and with permission of RNSA.

Code availability

All R, Stata, and ArcGIS codes necessary to produce the results here can be made available upon request.

References

  1. 1.

    Seebens, H. et al. No saturation in the accumulation of alien species worldwide. Nat. Commun. 8, 14435 (2017).

    CAS  ADS  Article  Google Scholar 

  2. 2.

    Vilà, M. & Hulme, P. (eds) Impact of Biological Invasions on Ecosystem Services Vol. 12 (Springer, Cham, 2017).

  3. 3.

    Pimentel, D., Zuniga, R. & Morrison, D. Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecol. Econ. 52, 273–288 (2005).

    Article  Google Scholar 

  4. 4.

    Bradshaw, C. J. et al. Massive yet grossly underestimated global costs of invasive insects. Nat. Commun. 7, 12986 (2016).

    CAS  ADS  Article  Google Scholar 

  5. 5.

    Schindler, S., Staska, B., Adam, M., Rabitsch, W. & Essl, F. Alien species and public health impacts in Europe: a literature review. NeoBiota 27, 1–23 (2015).

    Article  Google Scholar 

  6. 6.

    Jones, K. E. et al. Global trends in emerging infectious diseases. Nature 451, 990–993 (2008).

    CAS  ADS  Article  Google Scholar 

  7. 7.

    Hulme, P. E. Invasive species challenge the global response to emerging diseases. Trends Parasitol. 30, 267–270 (2014).

    Article  Google Scholar 

  8. 8.

    Mazza, G., Tricarico, E., Genovesi, P. & Gherardi, F. Biological invaders are threats to human health: an overview. Ethol. Ecol. Evol. 26, 112–129 (2014).

    Article  Google Scholar 

  9. 9.

    Epanchin‐Niell, R. S. & Hastings, A. Controlling established invaders: integrating economics and spread dynamics to determine optimal management. Ecol. Lett. 13, 528–541 (2010).

    Article  Google Scholar 

  10. 10.

    Essl, F. et al. Biological flora of the British Isles: Ambrosia artemisiifolia. J. Ecol. 103, 1069–1098 (2015).

    Article  Google Scholar 

  11. 11.

    Hamaoui-Laguel, L. et al. Effects of climate change and seed dispersal on airborne ragweed pollen loads in Europe. Nat. Clim. Change 5, 766–771 (2015).

    ADS  Article  Google Scholar 

  12. 12.

    Lake, I. R. et al. Climate change and future pollen allergy in Europe. Environ. Health Persp. 125, 385–391 (2017).

    Article  Google Scholar 

  13. 13.

    Sun, Y. et al. Climatic suitability ranking of biological control candidates: a biogeographic approach for ragweed management in. Eur. Ecosphere 8, e01731 (2017).

    Article  Google Scholar 

  14. 14.

    Center for International Earth Science Information Network (2016) Gridded Population of the World, Version 4 (GPWv4): Population Count Adjusted to Match 2015. Revision of UN WPP Country Totals. Palisades, NY: NASA Socioeconomic Data and Applications Center (SEDAC). https://doi.org/10.7927/H4SF2T42 (2016).

  15. 15.

    Burbach, G. J. et al. GA2LEN skin test study II: clinical relevance of inhalant allergen sensitizations in Europe. Allergy 64, 1507–1515 (2009).

    CAS  Article  Google Scholar 

  16. 16.

    Mouttet, R. et al. Estimating economic benefits of biological control of Ambrosia artemisiifolia by Ophraella communa in southeastern France. Basic Appl. Ecol. 33, 14–24 (2018).

    Article  Google Scholar 

  17. 17.

    Bullock, J. et al. Assessing and Controlling the Spread and the Effects of Common Ragweed in Europe (ENV.B2/ETU/2010/0037) Final Report (European Commission, 2012).

  18. 18.

    Linneberg, A. et al. Burden of allergic respiratory disease: a systematic review. Clin. Mol. Allergy 14, 12 (2016).

    CAS  Article  Google Scholar 

  19. 19.

    Guo, J.-Y. et al. Control efficiency of leaf beetle, Ophraella communa, on the invasive common ragweed, Ambrosia artemisiifolia, at different growing stages. Bioc. Sci. Technol. 21, 1049–1063 (2011).

    Article  Google Scholar 

  20. 20.

    Müller-Schärer, H. et al. Ophraella communa, the ragweed leaf beetle, has successfully landed in Europe: fortunate coincidence or threat? Weed Res. 54, 109–119 (2014).

    Article  Google Scholar 

  21. 21.

    Bonini, M. et al. A follow-up study examining airborne Ambrosia pollen in the Milan area in 2014 in relation to the accidental introduction of the ragweed leaf beetle Ophraella communa. Aerobiologia 32, 371–374 (2016).

    Article  Google Scholar 

  22. 22.

    Müller-Schärer, H. et al. Cross-fertilizing weed science and plant invasion science to improve efficient management: a European challenge. Basic Appl. Ecol. 33, 1–13 (2018).

    Article  Google Scholar 

  23. 23.

    Katsanevakis, S. et al. Implementing the European policies for alien species: networking. Sci., Partnersh. a complex Environ. Manag. Biol. Inv. 4, 3–6 (2013).

    Google Scholar 

  24. 24.

    Kettunen et al. Technical Support to EU Strategy on Invasive Species (IAS)—Assessment of the Impacts of IAS in Europe and the EU (Final Module Report for the European Commission) (Institute for European Environmental Policy (IEEP), 2009).

  25. 25.

    Šikoparija, B. et al. Spatial and temporal variations in airborne Ambrosia pollen in. Eur. Aerobiologia 33, 181–189 (2017).

    Article  Google Scholar 

  26. 26.

    A. R. S. Rhône-Alpes. Deuxième rapport sur l’ambroisie en région Rhône-Alpes: Analyse des données environnementales et médico-économiques. http://wd043.lerelaisinternet.com/pdf/Ambroisie2.pdf (2011).

  27. 27.

    Chauvel, B., Dessaint, F., Cardinal-Legrand, C. & Bretagnolle, F. The historical spread of Ambrosia artemisiifolia L. in France from herbarium records. J. Biogeogr. 33, 665–673 (2006).

    Article  Google Scholar 

  28. 28.

    D’Amato, G. et al. Pollen-related allergy in Europe. Allergy 53, 567–578 (1998).

    Article  Google Scholar 

  29. 29.

    Lommen, S. T. et al. Direct effects of insecticides on common ragweed-implications for natural enemy exclusion trials. J. Pestic. Sci. 43, 36–40 (2018).

    CAS  Article  Google Scholar 

  30. 30.

    Lommen, S. T. et al. Explaining variability in the production of seed and allergenic pollen by invasive Ambrosia artemisiifolia across Europe. Biol. Inv. 20, 1475–1491 (2018).

    Article  Google Scholar 

  31. 31.

    Hijmans, R. J. et al. Very high resolution interpolated climate surfaces for global land areas. Int. J. Climatol. 25, 1965–1978 (2005).

    Article  Google Scholar 

  32. 32.

    Zhou, Z. S., Guo, J. Y., Chen, H. S. & Wan, F. H. Effects of temperature on survival, development, longevity, and fecundity of Ophraella communa (Coleoptera: Chrysomelidae), a potential biological control agent against Ambrosia artemisiifolia (Asterales: Asteraceae). Env. Entomol. 39, 1021–1027 (2010).

    Article  Google Scholar 

  33. 33.

    Thuiller, W., Georges, D., Engler, R. & Breiner, F. biomod2: Ensemble platform for species distribution modeling. R package version 3.3-7. Retrieved from https://cran.r-project.org/web/packages/biomod2/index.html (2016).

  34. 34.

    Araujo, M. & New, M. Ensemble forecasting of species distributions. Trends Ecol. Evol. 22, 42–47 (2007).

    Article  Google Scholar 

  35. 35.

    Elith, J. et al. Novel methods improve prediction of species’ distributions from occurrence data. Ecography 29, 129–151 (2006).

    Article  Google Scholar 

  36. 36.

    Graham, C. H. et al. New developments in museum-based informatics and applications in bio- diversity analysis. Trends Ecol. Evol. 19, 497–503 (2004).

    Article  Google Scholar 

  37. 37.

    Broennimann, O. & Guisan, A. Predicting current and future biological invasions: both native and invaded ranges matter. Biol. Lett. 4, 585–589 (2008).

    Article  Google Scholar 

Download references

Acknowledgements

This study was coordinated within the framework of the EU COST Action FA1203 “Sustainable management of Ambrosia artemisiifolia across Europe (SMARTER)” (http://www.cost.eu/COST_Actions/fa/FA1203?parties). We acknowledge financial support from the Swiss State Secretariat for Education, Research and Innovation (C14.0063 to US and C13.0146 to HMS), the Swiss National Science Foundation (#31003A_166448 to HMS), the Swiss Federal Office for the Environment (13.0098.KP/M323-0760 to HMS) and that for Agriculture (1062-62,200 to HMS) and the EU COST Action SMARTER. Urs Schaffner was supported by CABI with core financial support from its member countries (see http://www.cabi.org/about-cabi/who-we-work-with/key-donors/). Carsten A. Skjøth was supported by European Commission through a Marie Curie Career Integration Grant (Project ID CIG631745 and Acronym SUPREME), Yan Sun by an Advanced Postdoc Mobility fellowship from the Swiss National Science Foundation (P300PA_161014), Branko Šikoparija was supported by the Ministry of Education, Science and Technological Development of the Republic of Serbia and Suzanne T. Lommen received funding from the European Union’s Horizon 2020 research and innovation programme under the Marie Skłodowska-Curie grant agreement No 786624. We thank Teja Tscharntke and Ragan Callaway for commenting on an earlier version of the manuscript.

Author information

Affiliations

Authors

Contributions

The study was conceptualised by U.S., S.S. and H.M.S.; S.S. coordinated data collection and data analysis, with support from C.A.S., L.A.D.W., Y.S., M.B., G.K., B.S., M.T., U.S. and H.M.S.; The field study on the impact of O. communa on pollen production was designed, executed and analysed by S.T.L., the species distribution modelling by Y.S., and the demographic study by B.A.A.; U.S. wrote the first draft of the paper, and all authors contributed to writing subsequent versions.

Corresponding author

Correspondence to Heinz Müller-Schärer.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Peer review information Nature Communications thanks the anonymous reviewer(s) for their contribution to the peer review of this work. Peer reviewer reports are available.

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Source data

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Schaffner, U., Steinbach, S., Sun, Y. et al. Biological weed control to relieve millions from Ambrosia allergies in Europe. Nat Commun 11, 1745 (2020). https://doi.org/10.1038/s41467-020-15586-1

Download citation

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing