Critical Review pubs.acs.org/est
Challenges in Tracing the Fate and Effects of Atmospheric Polycyclic Aromatic Hydrocarbon Deposition in Vascular Plants Dorine Desalme,† Philippe Binet, and Geneviève Chiapusio* UMR CNRS-UFC 6249 ChronoEnvironnement, Université de Franche Comté BP 71427, 25 211 Montbéliard, France ABSTRACT: Polycyclic aromatic hydrocarbons (PAHs) are ubiquitous organic pollutants that raise environmental concerns because of their toxicity. Their accumulation in vascular plants conditions harmful consequences to human health because of their position in the food chain. Consequently, understanding how atmospheric PAHs are taken up in plant tissues is crucial for risk assessment. In this review we synthesize current knowledge about PAH atmospheric deposition, accumulation in both gymnosperms and angiosperms, mechanisms of transfer, and ecological and physiological effects. PAHs emitted in the atmosphere partition between gas and particulate phases and undergo atmospheric deposition on shoots and soil. Most PAH concentration data from vascular plant leaves suggest that contamination occurs by both direct (air-leaf) and indirect (air-soil-root) pathways. Experimental studies demonstrate that PAHs affect plant growth, interfering with plant carbon allocation and root symbioses. Photosynthesis remains the most studied physiological process affected by PAHs. Among scientific challenges, identifying specific physiological transfer mechanisms and improving the understanding of plant-symbiont interactions in relation to PAH pollution remain pivotal for both fundamental and applied environmental sciences.
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INTRODUCTION Polycyclic aromatic hydrocarbons (PAHs) are a large class of toxic, mutagenic, and carcinogenic organic pollutants emitted to the atmosphere by incomplete combustion of biomass or fossil fuels.1 As semivolatile chemicals, they partition in the atmosphere between the gaseous and the particulate phase and can be transported in the atmosphere over long distances according to their specific physicochemical characteristics. Human exposure to PAHs occurs mainly through ingestion of contaminated food rather than through inhalation or skin contact.2 Since plants provide the exposure route to higher trophic levels as primary food producers, atmospheric PAH transfer and biological effects on plants constitute crucial steps which must be considered in PAH transfer through the food chain.3 Clearly, increased understanding vascular plant uptake and accumulation of PAHs from the environment has considerable implications for risk assessments. Nonvascular plants, especially bryophytes, have been used as biomonitors because of their wide geographic distribution and uptake of atmospheric PAHs by simple diffusion through their exchange surface with the air.4−9 Nevertheless, vascular plants dominate the plant kingdom given their highly adapted morphology, anatomy, and reproductive capacity which collectively account for their expansion. The leaf cuticle and vascular tissues offer particularly adapted structures for life in atmospheric conditions but also for PAH uptake. In natural conditions, contamination of vascular plants by PAHs is the © 2013 American Chemical Society
result of the root/shoot uptake of PAHs which have been previously deposited on soil/leaf surfaces. PAH concentrations measured in the same plant species, whether gymnosperm or angiosperm, vary according to location, enabling the use of vascular plant leaves for biomonitoring. Biomonitoring studies produce ranges of PAH concentrations in plant leaves that range from 4000 ng g−1 dry weight. The effects of atmospheric PAHs on plants vary according to the PAHs in question, their ambient concentration, exposure time, and species-specific plant characters that modulate physiological mechanisms of uptake. The scope of this review is to synthesize current knowledge about the transfer and the biological effects of atmospheric PAHs in vascular plants. With this aim, this review focuses on (1) atmospheric deposition of PAHs, (2) concentrations recovered in in situ vegetation, (3) mechanisms of PAH uptake, and (4) biological and physiological effects of PAHs in vascular plants. Finally, we identify remaining challenges and future research requirements to more fully understand the scope of plant-PAH interactions. Received: Revised: Accepted: Published: 3967
December 7, 2012 March 12, 2013 March 20, 2013 April 5, 2013 dx.doi.org/10.1021/es304964b | Environ. Sci. Technol. 2013, 47, 3967−3981
Environmental Science & Technology
Critical Review
Table 1. Compilation of Data about the Partitioning of Six PAHs (Anthracene, Phenanthrene, Chrysene, Pyrene, Benzo(A)Pyrene, And Benzo(k)fluoranthene) between Gaseous and Particulate Phases in the Atmosphere from Selected In Situ Studiesa physico-chemical properties −1
−1
gas-particle partitioning −1
3
MW (g mol )
Sw (mg L )
Log Kow
KH (Pa m mol )
% gas
% particle
ref
anthracene
178
0.045
4.54
3.96
99.0% 83−100% 100.0%
1.0% 0−17% 0.0%
11 12 13
phenanthrene
178
1.1
4.57
3.24
99.0% 96−100% 92.6% 87.6%
1.0% 0−4% 7.4% 12.4%
11 12 13 14
pyrene
202
0.132
5.18
0.92
95.5% 73−98% 91.4% 38.6%
4.5% 2−27% 8.6% 61.4%
11 12 13 14
chrysene
228
0.0018
5.86
0.065
48.4% 21−81% 87.5%
51.6% 19−79% 12.5%
11 12 13
benzo[a]pyrene
252
0.0038
6.04
0.046
8.0% 0−19% 22.5% 0%
92.0% 81−100% 77.5% 100%
11 12 13 14
benzo[k]fluoranthene
252
0.0008
6.00
0.016
5.0% 0−20% 15.0% 8.7%
95.0% 80−100% 85.0% 91.3%
11 12 13 14
PAH
a
MW: Molecular weight; Sw: solubility in water; Kow: octanol/water partitioning coefficient; KH: Henry’s constant. Physico-chemical properties were obtained from Mackay et al.15.
Table 2. General Synthesis about the Partitioning of PAHs between Gaseous and Particulate Phase in the Atmosphere
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PAHs
number of benzenic rings
log Koa
% gas
% particle
primary process of deposition
light PAHs intermediate PAHs heavy PAHs
2−3 rings 4 rings >4 rings
11
80−100 20−100 0−20
0−20 0−80 80−100
gas deposition gas and particle depositions particle deposition
atmospheric transport and chemical transformations.12,16 The gas-particle partition coefficient (Kp, m3 μg−1) is defined as
ATMOSPHERIC DEPOSITION OF PAHs
Following atmospheric transport over variable distances and possible attendant transformations, PAHs are deposited on land and water surfaces either through dry or wet deposition.10 Since PAHs are only poorly water-soluble, wet depositionthat is, solubilization in rainwater and fogis limited and most PAHs are consequently deposited through dry deposition of gases and particles. Particle-bound and gaseous PAHs undergo different fates because of their different properties and the range of environmental constraints for deposition. Atmospheric PAH Physicochemical Characteristics. Atmospheric deposition of PAHs depends on PAH physicochemical properties. As semivolatile chemicals, PAHs partition between the gaseous and the particulate phases according to their individual physicochemical properties (Table 1). The partitioning of semivolatile organic compounds between gaseous and particulate phase in the atmosphere is a defining process concerning their potential to undergo long-range
K p = (Cp/TSP)/Ca
(1)
where Cp (ng m−3) and Ca (ng m−3) are the concentrations of the compound in the particulate and the gaseous phases at the equilibrium state, respectively; and TSP (μg m−3) is the total suspended particulate matter concentration. In actual fact, it has been well documented that Kp is mostly related to the octanol/air partitioning coefficient (Koa) which depends on molecular weight and on the temperature:17 Koa = Kow /KH
(2)
where Kow is the octanol−water partitioning coefficient and KH is the Henry’s constant. The higher Koa is, the more abundant the compound will be in the particulate phase. Based on their Koa, PAHs are schematically classified into three categories18 (Table 2). Light PAHs (two and three benzene rings) with log Koa< 8.5 exist mainly in vapor phase, whereas heavy PAHs (more than 3968
dx.doi.org/10.1021/es304964b | Environ. Sci. Technol. 2013, 47, 3967−3981
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Table 3. PAH Accumulation in Needles of Selected Gymnosperms species
country
location
number of studied PAHs
Cedrus deodara Picea abies Pinus halepensis Pinus halepensis Pinus massoniana Pinus massoniana Pinus massoniana Pinus massoniana Pinus nigra Pinus nigra Pinus nigra Pinus nigra Pinus nigra Pinus nigra Pinus nigra Pinus nigra Pinus pinaster Pinus pinaster Pinus pinaster
China - Dalian Province Germany - Cologne Spain - Ebro River Italy - Sicily China - Guangdong Province China - Guangdong Province China - Guangdong Province China - Guangdong Province Spain - Ebro River USA - Ohio Germany - Cologne Germany - Cologne Germany - Cologne Germany - Cologne Italy Germany - Cologne Portugal Portugal Portugal
U U R+U U R U U U R+U U R R U U R+U R+U R U R+U
14 17 16 15 16 16 16 16 16 16 3-ring 3-ring 3-ring 3-ring 9 16 16 16 16
Pinus Pinus Pinus Pinus Pinus
pinaster pinea pinea pinea pinea
Italy Spain - Ebro River Portugal Portugal Portugal
R+U R+U R U R+U
9 16 16 16 16
Pinus Pinus Pinus Pinus Pinus Pinus Pinus Pinus Pinus Pinus Pinus Pinus Pinus Pinus Pinus
pinea strobus strobus strobus strobus strobus sylvestris sylvestris sylvestris sylvestris sylvestris sylvestris sylvestris taeda thunbergii
Italy- Sicily U.S. - Ohio U.S. - Idaho U.S. - Idaho U.S. U.S. - Indiana Germany - Cologne Poland Czech Republic Czech Republic Argentina and Germany Argentina and Germany UK U.S. - Texas China - Liaoning Province
U U R U R+U U U R R U R U R+U U U
15 16 10 10 18 11 17 16 16 16 5 5 16 20 14
PAHs PAHs PAHs PAHs
∑PAH in planta
ref
490−3,241 8−61 63−808 400−1,000 1,045 ± 115 1,144 ± 484 1,927 ± 955 1,565 ± 91 55−363 2,543−6,111 60−300 400−600 600−700 1,000−1,500 12−507 51−455 96 ± 30 866 ± 304 90 ± 50b 1,212 ± 436c 10−817 77−350 188 ± 117 337 ± 153 71 ± 33b 514 ± 317d 300− 700 127−589 64−141 137−859 370 ± 110 600−1,600 98−121 194−224 0.3−18,590 300−19,251 113−333 196−4,399 19−3,090 209−2,226 66−1,650
31 32 33 34 35 35 35 35 33 36 37 37 37 37 38 39 40 40 41 38 33 40 40 41 34 36 42 42 27 28 32 43 44 44 45 45 46 47 48
Range (min-max) or mean ± standard deviation. All concentrations are expressed in ng g‑1dry weight. R: rural, semirural and remote sites; U: urban, suburban, and industrial sites. bNew year needle. c3 year needles. d2 year needles.
a
four benzene rings) with log Koa > 11 are mostly associated with particulates; intermediate PAHs (four-ringed PAHs, e.g., pyrene and chrysene) have log Koa between 8.5 and 11 and hence are partitioned between the gaseous and particulate phases. Particle Bound and Gaseous PAH Deposition. Deposition of particle-bound PAHs mostly depends on the gravity law and the direction of dominant winds. Then, their atmospheric concentrations generally decrease with the distance to emission sources,19,20 and these PAHs are subject to dissipation in the atmosphere through photodegradation as well as chemical reactions with ozone and nitrate radicals.21 On the other hand, gaseous PAHs can undergo long-range transport in the atmosphere because they may be issued from primary sources of emission, for example, industrial combustions, domestic home heating and vehicle exhausts, but also
from secondary sources, for example, contaminated soil or plants from which they volatilize depending on the temperature. Deposition of gaseous PAHs is thus almost independent of the distance to emission sources and gaseous PAHs are likely to be found in remote sites located away from any emission source.22 As a result, gaseous PAHs dominate the total mixture of PAHs in air in a range of environments (i.e., in rural, suburban, or urban areas).23 However, gaseous PAHs are subjected to radical attack by reaction with ozone, hydroxyl and nitrate radicals. Atmospheric deposition of both particle-bound and gaseous PAHs are time-dependent because atmospheric PAH concentrations vary at several time-scales (daily, seasonal, interannual cycles).11,23−25 In temperate regions of the northern hemisphere, concentrations of PAHs are higher in winter, because of increased emissions of sources (e.g., home heating)25 and the 3969
dx.doi.org/10.1021/es304964b | Environ. Sci. Technol. 2013, 47, 3967−3981
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Table 4. PAH Accumulation in Leaves of Selected Angiosperms species
country
location
number of studied PAHs
∑PAH in planta
ref
Acer saccarum Acer saccarum Acer saccarum Acer saccarum Allium ascalonicumb Allium porrum Brassica oleacera Brassica oleracea Brassica oleracea Brassica rapa Calotropis gigantea Chichorium endivia Chrysanthemum coronarium Colocasia esculentab Corylus avellana Daucus carotab Daucus carotab Festuca ovina Ficus benghalensis Fraxinus excelsior Holcus lanatus Lactuca sativa Lactuca sativa Lolium perenne Pisum sativum Quercus ilex Quercus ilex Quercus ilex Quercus ilex Quercus robur, Q. petrea and intermediate Raphanus sativusb Trifolium repens Zea mays Zea mays
U.S. - Bloomington U.S. U.S. U.S. China - Guangdong province Greece - Thessaloniki China - Guangdong Province Greece - Thessaloniki Spain - Galicia China - Guangdong province India Greece - Thessaloniki China - Guangdong province China - Guangdong province United Kingdom China - Guangdong province Greece - Thessaloniki England India - Varanasi United Kingdom England China - Guangdong province Greece - Thessaloniki England China - Guangdong province Italy - Caserta Italy - Naples Italy - Campania region Italy - Palermo United-Kingdom China - Guangdong province England U.S. Spain - Galicia
U R U U U U U U U U U U U U U U U R U U R U U R U U U U R+U U U R R+U U
11 18 18 18 16 17 16 17 11 16 18 17 16 16 23 16 17 16 NS 23 16 16 17 16 16 16 27 16 17 23 16 16 18 11
500−1,100 220 ± 52 510 ± 100 1,600 ± 210 577 72−116 450 25−108 4 451 372−4,362 112−239 945 199 72 ± 9 412 48−94 136−510 630−3,358 28 ± 2 120−730 957 40−294 100−900 611 1,270−3,900 393−2,100 500−2,000 92−1,454 41 ± 4 264 130−940 27 ± 2 2
28 27 27 27 49 3 49 3 50 49 51 3 49 49 13 49 3 12 52 13 12 49 3 12 49 53 54 55 56 13 49 12 27 50
a Range (min-max) or mean ± standard deviation. All concentrations are expressed in ng g−1dry weight. R: rural, semirural and remote sites/U: urban, suburban, and industrial sites. NS: not specified. bConcentrations in edible part, i.e., in roots or in tubers.
weight. Second, the diversity of the number of PAHs considered into the assays varies from one, generally the BaP; up to sixteen, the U.S. Environmental Protection Agency priority PAHs; or even more (Tables 3 and 4). Finally, data obtained from various locations differ greatly on the global scale (different country, continent, or hemisphere) in addition to local scale differentiation (industrial, urban, suburban, or semirural areas). For example, the quantification of PAHs in Pinus nigra needles has enabled the distinction of industrial sites (1000−1500 ng g−1), Cologne city (600−700 ng g−1), smaller towns (400−600 ng g−1), and rural sites (60−300 ng g−1).37 In Acer saccarum leaves sampled in the USA, PAH concentrations were in average 220, 510 and 1,600 ng g−1 in rural, suburban and urban areas, respectively.27 Nevertheless, whatever the location of the experimental zone, PAH recovery from vegetation is noted in both gymnosperm and angiosperms taxa. PAHs Recovered in Vascular Plants: Biomonitoring. More than 20 vascular plants species belonging to Gymnosperms and Angiosperms have been used to monitor atmospheric concentrations of PAHs. No comparable data exist for the Pteridophytes. The PAH concentrations recovered in Gymnosperm needles or in Angiosperm leaves can be
shift in their gas/particle distribution resulted in a seasonality effect for particle-bound PAHs only.11
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PAH RECOVERY IN VASCULAR PLANTS IN ENVIRONMENTAL CONDITIONS The Biomonitoring Context. Biomonitoring is based on the sampling of leaves of indigenous vegetation from different sites in order to compare the susceptibility of these sites to be contaminated by atmospheric pollution.10,26,27 It has long been known that vegetation accumulates atmospheric organic pollutants such as PAHs in their leaves, generally in proportions that correlate with atmospheric concentrations.1,3,27−30 Even if complementary physicochemical measurements are performed using passive and active sampling protocols, biomonitoring remains necessary for estimating the range of atmospheric PAHs recovered in vegetation. Many data concerning PAH accumulation by plant leaves are available in the literature but among these results, it remains difficult to make direct comparisons between studies because of data heterogeneity. First, values of PAH concentrations recovered in leaves are expressed in different units such as μg g−1 fresh weight or μg g−1 dry weight or μg g−1 lipid or μg cm−2. The most frequently used unit remains per dry 3970
dx.doi.org/10.1021/es304964b | Environ. Sci. Technol. 2013, 47, 3967−3981
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Figure 1. PAH exposure pathways for in situ vascular plants.
of food.50 Recently, Wang et al.49 estimated that the consumption of vegetables grown near e-waste sites should be avoided .
divided into two main groups, those found in rural area (including semirural and remote sites) and those from urban area (including suburban and industrial sites) (Tables 3 and 4). At individual sampling sites, PAH concentrations recovered from vascular plant shoots are highly variable between plant species.3,13,32,33,57 For Gymnosperms, Pinus represents the dominant genus selected for biomonitoring of atmospheric pollution by PAHs, with data available for several species such as P. nigra, P. sylvestris, P. strobus, P. pinaster, P. pinea, P. massoniana sampled from various countries and areas (Table 3). Moreover, PAHs accumulate into pine needles over time, as shown by Ratola et al.41 who found that two-year old needles had twice the PAH concentration of needles of the year. Pines needles have then advantages over Angiosperm leaves because of their ability to accumulate PAHs year-round and also because of their differentiation in terms of yearly growth. For Angiosperms, biomonitoring of atmospheric PAH concentrations includes the use of leaves of deciduous trees (Acer, Quercus, Ficus, Fraxinus, Corylus genus), vegetables (L. sativa, B. oleacera, P. sativum), cereals (Z. mais), and grassland species (F. ovina, H. lanatus, T. repens, and L. perenne) (Table 4). Surprisingly, few data are available for the same genus or species. Vegetables and grassland species have been selected to better assess the risks of PAH transfer into the food chain, especially when the sites present potential risks (proximity of emission sources, emissions after accidental releases). As an example, the analyses of PAH concentrations in vegetables located near a chemical factory highlighted the major contribution of an accidental fire event to the contamination
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UPTAKE OF ATMOSPHERIC PAHs BY VASCULAR PLANTS PAH Exposure Pathways for In Situ Vascular Plants. In ecosystems and agrosystems, plants are exposed to atmospheric pollution by PAHs from the atmosphere but also from the soil.3,30 Therefore, PAH concentrations recovered in vascular plants in situ represent integrative concentrations of two PAH exposure pathways, one pathway from the air to leaves (direct contamination, air-plant pathway) and the other from the air to roots, passing through the soil compartment (indirect contamination, air-soil-plant pathway) (Figure 1). The global fate of atmospheric PAHs in plants, that is, the proportions between the two pathways, is known. Direct transfer of PAHs, that is, foliar uptake, is assumed to be the major contributing pathway for plant contamination when plants grow in nonpolluted soils (10−100 mg PAH kg−1 dry soil).60 In many cases, once pollutants enter plant tissues, they can migrate from root to shoot and from shoot to root, depending on the chemical and physiological processes occurring within the plant. Contributions from Experiments under Controlled Conditions. Most experiments performed under controlled conditions generally distinguish contamination pathways and some studies have attempted to study them in parallel. As an example, the two-photon excitation microscopy technique (TPEM) enables the direct observation of PAHs in intact plant tissues thanks to their fluorescence properties.61,62 Leaf uptake of atmospheric PAHs has been simulated by spraying aqueous or solvent solutions containing PAHs directly on leaves, and devices have been designed to generate atmospheric pollution under controlled conditions. Large exposure chambers (>1m3) have been developed to examine the effects of environmental variables such as temperature, humidity and light,63 and to determine the physicochemical properties of PAHs involved in the PAH partitioning between air and plants.64,65 In general, smaller exposure chambers (
