Short Communication
Vehicle-derived ultrafine particulate contaminating bees and bee products

https://doi.org/10.1016/j.scitotenv.2020.141700Get rights and content

Highlights

  • SEM/EDX analysis of UFP on bees reveals nature, morphology and mineral composition

  • Areas of intense traffic in Northern Italy are contaminated by metal-based dust.

  • UFP are exclusively made of Fe oxides/hydroxides and baryte.

  • Baryte and iron are common constituents of the braking systems of vehicles.

  • Honey and pollen display PM contamination, showing potential UFP exposure to bees.

Abstract

Despite adverse health effects, ultrafine particulate matter (UFP), i.e., PM less than 0.1 μm in diameter, is an emerging pollutant not subject to regulation. UFP may cause both lung inflammation and cardiopulmonary disease and may enter the brain directly via the olfactory bulb, affecting the nervous system. In highly urbanized environments, diesel and gasoline vehicles are among the major sources of UFP including combustion-generated solid particle pollutant and metal-based particles. Metal-based UFP are of much concern, as they may promote inflammation and DNA damage via oxidative stress with generation of free radicals and reactive oxygen species (ROS).

We used the honeybee as an alternative sampling system of UFP in an area of the Po Valley (Northern Italy), which is subject to intense traffic. Worker bees are widely recognised as efficient samplers of air pollutants, including airborne PM. During flight and foraging activity, pubescence of the bees promotes the accumulation of electrical charge on the body's surface, enhancing attraction to air pollutants.

Bees living near the main Italian highway, the Autostrada A1, displayed a contamination of nanosized Fe-oxides/hydroxides and baryte. Sources of Fe-bearing and baryte ultrafine particles are primarily the vehicles speeding on the motorway.

Pollen collected by forager bees and honey produced by the bee colony displayed contamination by nanosized Fe-oxides/hydroxides and baryte. Such a contamination exposes pollinators and humans to UFP ingestion, endangering the safety of food produced at traffic-influenced sites.

Given the global spread of traffic, our findings suggest that exposure and environmental impact of ultrafine Fe-oxides/hydroxides and baryte are potentially ubiquitous, although usually overlooked in environmental policy discussions.

Introduction

Vehicular traffic is responsible for the emission of a significant amount of airborne particulate matter (PM), a complex mixture of airborne chemical components, commonly classified by a particle size up to 10 μm (PM10). PM toxicity depends on morphology, chemical composition, and dimension of the dust, with ultrafine PM (UFP; PM less than 0.1 μm in diameter) able to penetrate deeply into the lungs and enter blood circulation. UFP may cause both lung inflammation and cardiopulmonary disease and may enter the brain directly via the olfactory bulb, affecting the nervous system (Brook et al., 2010; Maher et al., 2016; Bencsik et al., 2018). Metal-based particles are of much concern, as they may promote inflammation and DNA damage via oxidative stress caused by generation of free radicals and reactive oxygen species (ROS) (Dashtipour et al., 2015; Soltani et al., 2018; Jan et al., 2020). Neurological disorders such as Alzheimer's and Parkinson's disease are associated to metal-based UFP exposure (Maher et al., 2016). Despite the known adverse health effects to humans at a low-level dose exposure (Lanphear, 2017), UFP is not subject to regulations, while limits for the protection of human health are available for PM10 and PM2.5 (Directive 2008/50/EC of the European Parliament and of the Council of 21st May 2008 on ambient air quality and cleaner air for Europe). Such limits are expressed as mass per unit volume of atmospheric air with no specific indication on the chemical nature of the particles.

In highly urbanized environments, vehicular traffic is a steady source of ultrafine metal-based particles (Liati et al., 2018). Relatively few studies investigate the chemical and physical-structural characteristics of such PM while the great majority of them deals with particle counting (Liati et al., 2018). The honey bee is a well-known indicator of environmental pollution (Perugini et al., 2011; van der Steen et al., 2012; Zarić et al., 2018a, Zarić et al., 2018b). Recently, it has been demonstrated that each single forager bee acts as an efficient mobile sampler of airborne PM (Negri et al., 2015; Pellecchia and Negri, 2018). During the flight and foraging activity, the pubescence of the bees promotes accumulation of electrical charges on the surface of the body due to friction with the air (Vaknin et al., 2000). The charges enhance attraction of airborne particles, including pollen for pollination and pollutants (Vaknin et al., 2000; Bonmatin et al., 2015). Airborne PM attached to the bee's body is typically up to 10 μm in diameter and can be analysed by size, morphology, and chemical composition using a scanning electron microscope (SEM) coupled with energy dispersive X-ray fluorescence (EDX) (Negri et al., 2015; Pellecchia and Negri, 2018). SEM/EDX is a powerful, fast, and non-destructive technique, and the information given by the morphology and composition of particles leads to particle identification and classification (Negri et al., 2015; Pellecchia and Negri, 2018).

In the present paper, honeybees were used as an alternative sampling system of UFP in the peri-urban area of the City of Parma (Po Valley, Northern Italy). The Po Valley is one of the most important industrial and agricultural areas in Italy and Europe, characterized by a high population density and a low level of air quality (Marcazzan et al., 2001). According to source apportionment studies, PM10 and PM2.5 in the Po Valley in the warm season mainly originate from traffic and agriculture (Marcazzan et al., 2001; Pietrogrande et al., 2016; Pozzer et al., 2019). In the City of Parma, the fixed monitoring network of airborne pollutants consists of a few stations of the Regional Environmental Protection Agency (ARPAE) (http://www.arpae.it/), located in different domains (e.g., urban trafficked sites, rural and industrial areas). Higher concentrations of PM2.5 are usually displayed in colder months than in warmer months; however, annual mean values are always below the limit set by the Directive 2008/50/EC (i.e. an annual mean value of 20 μg/m3 based on a 3-year average). Mean values of approximately 40 μg/m3 were displayed in the winter months of 2017 with a peak concentration in February, and approximately 15 μg/m3 in the warmer months (http://www.arpae.it/). However, no data are available on the nature and chemical composition of the particles. In this work, SEM/EDX analysis of UFP collected by forager bees provided information on the nature, morphology and mineralogical composition of the ultrafine fraction of PM present in the area. Analysis performed on honey and bee pollen demonstrated the potential for UFP to enter the food chain and to expose pollinators to UFP ingestion.

Section snippets

Area of investigation

In February 2017, a beehive for PM monitoring was placed in a lawn in the peri-urban area of the City of Parma. Parma is located in the middle of the Po Valley (Northern Italy), an alluvial sedimentary plain of Pliocene and quaternary age, which lies between the Northern Apennine and the Southern Alps. Alluvial deposits of the area include silty clays and sandy silts from the Taro River and the Parma stream, which originate from numerous Flysch formations of the Apennine that feed the alluvial

Results and discussion

While all negative controls did not display any PM contamination (Suppl. Fig. 1), the wings of the bees from the monitoring station showed a contamination of inorganic dust typically less than 10 μm. While PM up to 5 μm were mostly of natural origin (i.e. soil-derived clay minerals), UFP was exclusively made of Fe-oxides/hydroxides (occasionally with traces of Cu and/or Ti) and baryte, a barium sulphate (Fig. 1, Fig. 2). Additionally, bee pollen collected from the hindlegs of insects (Fig. 1,

Conclusion

By using the honeybee as an alternative natural and inexpensive sampling system of UFP, we demonstrate that areas subject to intense traffic are contaminated by metal-based dust, primarily originating from vehicular traffic. Additionally, honey and pollen displayed contamination by the PM; thus, demonstrating the potential for UFP to enter the food chain and to expose pollinators to UFP ingestion.

Given the global spread of traffic, the exposure to ultrafine Fe-oxides/hydroxides and baryte is

CRediT authorship contribution statement

Giulia Papa: Investigation, Writing - review & editing. Giancarlo Capitani: Investigation. Ettore Capri: Funding acquisition, Writing - review & editing. Marco Pellecchia: Conceptualization, Methodology, Investigation, Writing - review & editing. Ilaria Negri: Conceptualization, Methodology, Funding acquisition, Writing - review & editing.

Declaration of competing interest

I declare no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgments

This project has been funded with a support from the ECORESILIENTE project of Università Cattolica del Sacro Cuore (E.C. and I.N.). G.P. was partially supported by the Doctoral School on the Agro-Food System (Agrisystem) of the Università Cattolica del Sacro Cuore (Italy). Special thanks to Liceo Ulivi of Parma and Comune di Parma for supporting beekeeping activity during the educational project “Che aria tira”. We thank Dr. Antonia Desiante for her support in data collection, and Dr. Paolo

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