Climate-change-induced range shifts of three allergenic ragweeds (Ambrosia L.) in Europe and their potential impact on human health

Introduction

Climate is one of the most important determinants of species distributions at regional and global scales (Parmesan & Yohe, 2003; Burrows et al., 2011). Human-induced climate change is affecting global vegetation patterns, ecosystem functions and the distribution range of multiple terrestrial and aquatic species (Cramer et al., 2001; Gonzalez et al., 2010). One dramatic effect of climate change is the shift in species distribution range and phenological interactions (Parmesan & Yohe, 2003; Visser & Both, 2005), which can change the pollen season and lead to increases in local pollen production (Rogers et al., 2006). Allergic responses such as rhinitis (hayfever) and asthma, caused by plant pollen are therefore globally an increasing public health concern (Albertine et al., 2014; Essl et al., 2015; Hamaoui-Laguel et al., 2015; Schindler et al., 2015).

Among allergenic plants, ragweeds (Ambrosia L., Asteraceae) are considered to be among the most potent aeroallergens. Ambrosia is distributed from Mexico to Canada and contains at least 40 species (Essl et al., 2015). Ragweed species flower from July to October and each plant is able to produce millions of wind-dispersed pollen grains that may be transported over long distances, with reports ranging to over 1,000 km (Belmonte et al., 2000; Bullock et al., 2013; Hamaoui-Laguel et al., 2015). Ragweed pollen is a significant cause of allergic reactions (Frenz, 2001; Ziska et al., 2011). The threshold for provoking allergic rhinitis in ragweed pollen sensitized patients is below 20 grains m⁻³, and in sensitive patients be as low as 1–5 grains m⁻³ (Déchamp et al., 1997; Šikoparija et al., 2009) compared to 50 grass pollen grains (Davies & Smith, 1973). Ragweed pollen furthermore induces asthma about twice as often as other types of pollen (Skjøth et al., 2010). In this regard, common ragweed (A. artemisiifolia), perennial ragweed (A. psilostachya) and giant ragweed (A. trifida) are of special concern as they rank among the most widespread allergenic plants (Bassett & Crompton, 1982; Ghosh et al., 1994; Rich, 1994; Frenz, 2001). The medical cost of allergies in the United States is estimated to an annual cost in excess of $18 billion a year (Centers for Disease Control and Prevention, 2011). Ragweed is the major cause of late summer allergic rhinitis (hay fever) in the United States and Canada (Arbes Jr et al., 2005), and is also a significant problem in Southern and Southeastern Europe where allergy is the most common chronic disease (Papadopoulos et al., 2012). Estimated medical costs of ragweed-related allergies are substantial in the affected countries. In Hungary, where 25% of the population is allergic to ragweed, Kazinczi et al. (2008) estimated the annual cost to exceed €110 million per year; in Austria Gerber et al. (2011) put the cost around €88 million per year (for a comprehensive review, see Task 5 in Bullock et al. (2013)).

Ragweed populations remain relatively rare in Northern Europe, where low autumn temperatures prevent ragweed species from flowering and reaching reproductive maturity (Chapman et al., 2014). However, global warming is predicted to facilitate a northwards expansion of ragweed species (Storkey et al., 2014; Essl et al., 2015). This can accelerate the establishment and pollen production of self-propagating ragweed populations, and extend the local pollen season in regions currently climatically unsuitable (Gerber et al., 2011; Cunze, Leiblein & Tackenberg, 2013). Increasing amounts of anthropogenically released carbon dioxide (CO₂) also has the potential to increase pollen production (Sheffield, Weinberger & Kinney, 2011). Studies have shown an increase of up to 61% in ragweed pollen production in a CO₂ enriched atmosphere, both in climate-controlled greenhouses and in field based experiments (Ziska et al., 2003; Rogers et al., 2006). Furthermore, Patz & Olson (2006) described how especially plants in urban areas are exposed to elevated CO₂ concentrations, i.e., from industry and dense traffic. Cities are therefore prone to a disproportionate increase in ragweed pollen production, with serious consequences for public health (Ziska et al., 2003). This raises concern about the consequences of the increasing frequency of which ragweed species have been registered across continental Europe, where they are now considered bioinvaders (Fernández-Llamazares et al., 2012). Over future decades, ragweed may become a major source of pollen allergy in Northern Europe, with severe medical and economic implications (Bullock et al., 2013).

In this paper, we use species distribution modeling (SDM) to explore which areas of Europe are most susceptible to successful invasion of common ragweed, perennial ragweed and giant ragweed by year 2100 under two different IPCC climate scenarios (RCP 6.0 and RCP 8.5). We show that all three ragweed species are expected to expand and shift their potential distribution across Europe by year 2100, and that ragweed species by the end of the century may cause large-scale health related impacts on the European continent.

Methods

Results

Based on all data points from the native range (Table 1), the median AUC values ranged from 0.80 to 0.82, depending on the species, indicating ‘good’ performance (AUC > 0.8) of all models for all three species (Table 2).

Future species distribution in Europe

In Europe, all models predicted that climatically suitable areas for ragweed will become more widespread on the continent by year 2100 (following IPCC climate change scenarios RCP 6.0 and RCP 8.5) (Fig. 1). At present, the ragweed ‘high allergy risk’ (HAR) areas are found mostly in Southern Europe (Fig. 1 and Fig. S4). The models show a substantial increase of HAR areas across Europe by 2100 (Table 3). For common ragweed the HAR areas with maximum habitat suitability increased 100% (RCP 6.0) and 45% (RCP 8.5), respectively, with most new areas located in Northern (e.g., Denmark, United Kingdom) and Eastern Europe (e.g., the Baltic countries) (Fig. 1 and Table 3). For perennial ragweed models predicted an increase of 127% (RCP 6.0) and 189% (RCP 8.5), with new areas located across most of Central and Eastern Europe (Fig. 1 and Table 3). For giant ragweed, the HAR area increased by 97% for the RCP 6.0 projections but decreased by 69% for the RCP 8.5 projections. New habitats occurred especially in Russia, the Baltic countries and Southeastern Europe (Fig. 1 and Table 3).

Table 3:

The area (km²) in future ‘high allergy risk’ (HAR) areas of common ragweed (Ambrosia artemisiifolia), perennial ragweed (A. psilostachya) and giant ragweed (A. trifida) in Europe under current and future climate (year 2100) conditions assuming RCP 6.0 and RCP 8.5 climate change scenarios (IPCC, 2014).

Species	Highest habitat suitability (km2)
	Current	RCP 6.0	RCP 8.5
Common ragweed	89,460	178,960	129,320
Perennial ragweed	41,660	52,760	78,650
Giant ragweed	38,220	75,290	26,530

DOI: 10.7717/peerj.3104/table-3

Effects of environmental variables

The jackknife evaluation procedure suggested that GDD was the most important predictor for all three species. T_min was the second most important variable for perennial and giant ragweed, and WBAL was the second most important variable for common ragweed (Table 4 and Fig. S5). The response of the variables showed somewhat different tendencies (Fig. 2). Habitat suitability for all species tended to increase with GDD. Species showed similar response to T_min. Habitat suitability of common ragweed and giant ragweed showed a similar increasing response to WBAL, whereas habitat suitability for perennial ragweed showed a hump-shaped relationship with WBAL values ranging from ca. −1,000 to 1,000 mm. Across species, WBAL had the strongest impact for common ragweed (Table 4). All species had their highest estimated habitat suitability for T_min values ranging from approximately −30 to 10 °C (Fig. 2). MESS comparison of the environmental factors in Europe indicated very little extrapolation outside the range of the native conditions. Specifically, more than 99% of grid cells for both the present-day and future climate conditions fell within the range of the native climate conditions (Fig. S6).

Table 4:

Explanatory power of three climate variable (growing degree days, GDD; minimum temperature, T_min; water balance, WBAL) deviated from the jackknife analysis on native range models of 15 replicates.

Original jackknife analysis output of the model are found in Fig. S5.

Parameter	Species
	Common ragweed	Perennial ragweed	Giant ragweed
GDD	0.425	0.456	0.548
Tmin	0.215	0.306	0.252
WBAL	0.36	0.238	0.2

DOI: 10.7717/peerj.3104/table-4

Discussion

Understanding the future distribution of allergenic plant species is crucial for predicting the consequences of the associated health related issues. Our study shows that three allergenic ragweed species have considerable potential to successfully expand their distribution range in Europe by the end of the century. The predicted ‘high allergy risk’ (HAR) areas, i.e., areas with climatic conditions corresponding to the highest quartile (25%) of present day habitat suitability for each of the three species, may expand extensively in Europe, depending on species and future climate change (RCP 6.0/8.5) scenarios (Table 3).

Our results for common ragweed agree with those of Cunze, Leiblein & Tackenberg (2013) in predicting an increased habitat suitability of common ragweed in Europe, particularly towards Northern and Eastern Europe. These authors, however, did not quantify the extent of the increase in areas where allergenic problems may be expected as a consequence of climatic changes. The majority of ragweed-studies so far have exclusively investigated common ragweed. However, considering that pollen of ragweed species is morphologically similar and give similar allergenic reactions (Frenz, 2001; Ziska et al., 2011; Sikoparija et al., 2016), it is important to consider multiple ragweed species and climate scenarios when predicting future increases in habitat suitability of allergenic ragweeds. Specifically, depending on the species and RCP used, our models estimated a change in ragweed HAR areas ranging from a loss of 11,690 km² (giant ragweed, RCP 8.5) to an increase of 89,500 km² (common ragweed RCP 6.0), affecting in particular Great Britain, Denmark, Sweden and the Baltic countries. Surprisingly, the more severe climate change scenario (RCP 8.5) did not facilitate an expansion of ragweeds further north compared to the milder scenario (RCP 6.0). In fact, the largest extent of suitable habitats was found under RCP 6.0 for both common and giant ragweed. We note that the northward expansion of ragweed species will be controlled by biological constraints in addition to climate variables (Deen, Hunt & Swanton, 1998). For instance, ragweeds are short-day plants and their flowering is induced by a dark period of approximately eight hours (Deen, Hunt & Swanton, 1998). Ragweeds are also sensitive to frost, and will not continue to flower when temperatures drop below freezing (Deen, Hunt & Swanton, 1998). In Northern Europe, growing season length and dark period duration may become insufficient for ragweed species to reproduce despite relatively favorable climatic conditions. Additionally, the lower extent of high habitat suitability for these species under RCP 8.5 could also be associated with drought. We found that both common and giant ragweed perform well under relatively wet conditions, whereas perennial ragweed performs better in drier habitats (Fig. 2). Prolonged drought and dry periods are increasingly expected under RCP 8.5, hence water scarcity provides one potential explanation why perennial ragweed will become most abundant under RCP 8.5 compared to both common and giant ragweed. Overall, we recommend that further work examining ragweed species distributions may be improved by considering important non-climatic variables including, for example, day length.

In addition to a geographical increase in areas with high climate suitability, a warmer climate may facilitate flowering and pollen production in areas where flowering and seed maturation currently is limited by low temperatures. Thus, allergenic pollen load could also be intensified within the current realized range of the three ragweed species. These changes impose substantial health related risks, as evident from current HAR areas in Southern Europe. For example, a prick-test study of ragweed allergens showed levels of pollen-allergic patients ranging from 30–40% in the Rhône Valley (France), to 70% in Northern Italy and more than 80% in Hungary (Rybnícek & Jäger, 2001). Another health related concern is cross-reactivity between species within the genus Ambrosia as well as with other allergenic species, such as mugwort (Artemisia L.) species (White & Bernstein, 2003; D’Amato et al., 2007). This combined with the late flowering of ragweeds, that will prolong the local pollen season (D’Amato et al., 2007; Vogl et al., 2008), are likely to entail medical and socio-economical implications for the public in novel HAR areas.

In the context of allergenic plants, urban areas are of main concern due to their high population densities (higher exposure risk) and elevated CO₂ concentrations that are known to facilitate biomass and pollen production (Ziska et al., 2003). Our models indicate that future ragweed HAR areas will overlap with major cities in Europe including St. Petersburg, Hamburg and Paris. Ragweeds future distribution may therefore affect large populations across Europe. A higher overall abundance of ragweed species also increases the risk of long-distance transport of allergenic pollen (Grewling et al., 2016). Ragweed pollen can disperse 100’s of kilometers (Bullock et al., 2013), thus affecting allergic persons in areas without established ragweed populations. This has already been shown using complex cluster backward trajectories (Makra et al., 2016), and Hamaoui-Laguel et al. (2015) estimated that airborne ragweed pollen concentration will increase about four times by 2050, dispersing pollen across large regions of Europe. The low atmospheric concentration of ragweed pollen necessary to induce allergic reactions in sensitive patients (∼5 grains m⁻³) (Déchamp et al., 1997) combined with the long-distance wind dispersal potential, makes urban ragweed populations important sources for pollen induced allergies across large spatial areas (Belmonte et al., 2000; Essl et al., 2015; Hamaoui-Laguel et al., 2015).

While the results of this study can inform future management strategies addressing climate change and increasing human disturbance, there is a need to acknowledge the caveats embedded in all climate model studies (Araujo & Guisan, 2006). For instance, our model does not take into consideration anthropogenic factors like disturbance, land use and propagule pressure, which will be crucial in controlling range filling within the potential range set by the climatic variables. Including such parameters in future model-work will allow us to expand knowledge and predictability of the distribution of invasive allergenic species (Chapman et al., 2016). Local adaptation is another parameter that may affect the distribution of species and their response to climate change. Intra-population local adaption has been shown to allow species to survive in otherwise unfavorable conditions (Li et al., 2015). Thus, incorporation of physiological performance/phenology of ragweed throughout their distribution would be beneficial in future work to estimate range expansion at regional or local scales (Chapman et al., 2014). For now, our results demonstrate that future climate changes could result in a large expansion of Ambrosia related allergy problems in Europe, unless precautionary efforts are made to limit further expansion of the three species across Europe (Pearson, 2007; Webber et al., 2011; Chapman et al., 2016). In Northern and Eastern Europe, focus should primarily be on restricting further invasion and establishment of ragweed (Dullinger et al., 2009; Cunze, Leiblein & Tackenberg, 2013; Storkey et al., 2014). The most important factor for successful invasion by ragweed is propagule pressure, both in terms of number of introductions and number of propagules released (Lockwood, Cassey & Blackburn, 2005; Gladieux et al., 2011). Ragweeds are species that propagate exclusively by seeds. Long-distance dispersal of ragweed seeds is mostly dependent on anthropogenic forces, including import of contaminated birdseeds and crops (e.g., maize and soya beans), transport of contaminated soil, and seed infested agricultural machines (Essl et al., 2015; Chapman et al., 2016). Seeds may remain dormant for as long as 40 years (Bassett & Crompton, 1975) if conditions are unfavorable, calling for a long term effort in controlling ragweed invasion. All these aspects illustrate the importance of cross-countries management planning in order to prevent and control future spread of these allergenic bioinvaders.

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