VAM populations in relation to grass invasion associated with forest decline

Spruce stands in Northern Bohemia forests, damaged to various degrees by industrial pollution, have shown establishment of grass cover following tree defoliation. Populations of vesicular-arbuscular mycorrhizal (VAM) fungi were studied under this grass cover in four permanent plots with spruce under different levels of pollution stress. Soil and root samples were collected in April and June within each plot as follows: (1) sites without grass, (2) sites with initial stages of grass invasion, and (3) sites with fully developed grass cover. In all plots, the highest number of propagules were recovered from samples taken from sites having full grass cover. Mycorrhizal infection of grass was highest in the plot with the severest pollution damage and lowest in the least damaged plot. The development of grass cover and VAM infection of grass increased with tree defoliation caused by air pollution.     

Interactions of Trametes versicolor, Coriolopsis rigida and the arbuscular mycorrhizal fungus Glomus deserticola on the copper tolerance of Eucalyptus globulus

The presence of high levels of Cu in soil decreases the shoot and root dry weights of Eucalyptus globulus. However, higher plant tolerance of Cu has been observed in the presence of the arbuscular mycorrhizal (AM) fungus Glomus deserticola. The hyphal length of G. deserticola was sensitive to low Cu concentrations, and the percentage of AM root colonisation and the metabolic activity of the AM fungus were also decreased by Cu. Therefore, a direct effect of Cu on the development of the AM fungus inside and outside the root cannot be ruled out. E. globulus colonised by G. deserticola had higher metal concentrations in the roots and shoots than do non-mycorrhizal plants; however, the absence of a higher root to shoot metal ratio in the mycorrhizal plants (1.70 ± 0.11) indicated that G. deserticola did not play a filtering/sequestering role against Cu. The saprobe fungi Coriolopsis rigida and Trametes versicolor were able to remove Cu ions from the asparagine–glucose growth media. However, plants inoculated with C. rigida and T. versicolor did not accumulate more Cu than non-inoculated controls, and the growth of the plant was not increased in the presence of these fungi. However, C. rigida increased the shoot dry weight, AM root length colonisation, and metabolic mycelial activity of plants colonised with G. deserticola in the presence of Cu; only this saprobe-AM fungus combination increased the tolerance of E. globulus to Cu. Inoculation with G. deserticola and C. rigida increased the E. globulus Cu uptake to levels reached by hyperaccumulative plants.     

Changes in elemental uptake and arbuscular mycorrhizal colonisation during the life cycle of Thlaspi praecox Wulfen

Elemental uptake and arbuscular mycorrhizal (AM) colonisation were studied during the life cycle of field collected Cd/Zn hyperaccumulating Thlaspi praecox (Brassicaceae). Plant biomass and tissue concentrations of Cd, Pb, Zn, Fe and Ni were found to vary during development, while no variation in P, K, Ca, Mn and Cu tissue concentrations were observed. The lowest Cd bioaccumulation in rosette leaves (BAF(RL)) observed during seeding was partially attributed to lower translocation from roots to rosette leaves and partially to high translocation to stalks, indicating a high Cd mobility to reproductive tissues, in line with our previous studies. The highest intensity of AM colonisation (M%) was observed in the flowering phase and was accompanied by increased root Cd, Zn, Pb and Fe contents. In addition, a positive correlation between AM colonisation and Fe contents in rosette leaves was found. The results indicate developmental dependence of AM formation, accompanied by selective changes in nutrient acquisition in T. praecox that are related to increased plant needs, and the protective role of AM colonisation on metal polluted sites during the reproductive period.     

Microbial processes in the rhizosphere soil of a heavy metals-contaminated Mediterranean salt marsh: a facilitating role of AM fungi

We investigated the relationship of the zonal pattern followed by the vegetation in a polluted Mediterranean salt marsh, in semiarid south-eastern Spain, with the microbiological and biochemical properties (labile C fractions, oxidoreductases and hydrolases) of the rhizosphere soil of two halophyte species, Arthrocnemum macrostachyum and Sarcocornia fruticosa, and with the degree of arbuscular mycorrhizal (AM) colonisation in their rhizospheres. Levels of plant biomass and cover were inversely related to heavy metal contents and salinity. The concentrations of Fe, Cu, Mn and Pb extracted with DTPA hardly varied among the different zones of the salt marsh. The dehydrogenase and phosphatase activities, the soluble C and water-soluble carbohydrates concentrations and the extent of root colonisation were greater in the salt marsh zones of lower soil salinity and lower metal concentration. Urease and beta-glucosidase activities were not detected in the salt marsh. Plant biomass and cover showed positive relationships with mycorrhizal colonisation (R=0.773, P<0.001; R=0.874, P<0.001, respectively). Mycorrhizal colonisation was negatively correlated with the contents of Pb and Zn in plant tissues. This work supports the view that reduced plant uptake of toxic metals, particularly lead, could be involved in the beneficial effects of AM fungi on plant development in Mediterranean salt marshes contaminated with mining wastes.     

Pollution resistance of mountain birch, Betula pubescens subsp. czerepanovii, near the copper-nickel smelter: natural selection or phenotypic acclimation?

Mountain birch, Betula pubescens subsp. czerepanovii (Orlova) Hamet-Ahti, is one of the very few woody plants surviving in the heavily polluted industrial barrens of the Kola Peninsula, north-western Russia. The present study was designed to find out whether long-lasting pollution impact caused selection of resistant birch genotypes, and to investigate possible trade-offs between pollution resistance and performance by exploring growth of birch seedlings in the different environments. In the reciprocal planting experiments, progenies of birches from polluted sites performed slightly better in the polluted environment (in terms of survival, leaf number, and leaf size) than progenies of birches from clean sites; and vice versa, in the clean environment progenies of birches from polluted sites performed slightly worse than progenies of birches from clean sites. However, this pattern was detected only in some of statistical tests, while the majority of comparisons showed no genotype or genotype by environment effects. Although some of the results indicate that long-lasting pollution impact may have increased pollution resistance of the affected populations by elimination of sensitive genotypes (survival selection), this conclusion should be considered tentative. The resistance did not reach the level sufficient to assure re-colonisation of polluted habitats: progenies of all trees completely died on the contaminated soils by the end of the first growth season. Therefore persistence of mountain birch populations near the strong polluters may be transient, being explained not only by higher resistance of the survivors, but also by phenotypic acclimatisation of mature trees to gradual increase in pollution.     

Colonisation of a Zn, Cd and Pb hyperaccumulator Thlaspi praecox Wulfen with indigenous arbuscular mycorrhizal fungal mixture induces changes in heavy metal and nutrient uptake

Plants of the Zn, Cd and Pb hyperaccumulator Thlaspi praecox Wulfen (Brassicaceae) inoculated or not with indigenous arbuscular mycorrhizal (AM) fungal mixture were grown in a highly Cd, Zn and Pb contaminated substrate in order to evaluate the functionality of symbiosis and assess the possible impact of AM colonisation on heavy metal uptake and tolerance. The results suggest AM development in the metal hyperaccumulating T. praecox is favoured at elevated nutrient demands, e.g. during the reproductive period. AM colonisation parameters positively correlated with total soil Cd and Pb. Colonised plants showed significantly improved nutrient and a decreased Cd and Zn uptake as revealed by TRXRF, thus confirming the functionality of the symbiosis. Reduced heavy metal uptake, especially at higher soil metal contents, indicates a changed metal tolerance strategy in colonised T. praecox plants. This is to our knowledge the first report on AM colonisation of the Zn, Cd and Pb hyperaccumulator T. praecox in a greenhouse experiment.     

Reproduction of mountain birch along a strong pollution gradient near Monchegorsk, Northwestern Russia

We explored effects of severe pollution on sexual reproduction of mountain birch, Betula pubescens subsp. czerepanovii, by counting catkins on sample branches and weighing both somatic and generative structures of both short and long shoots from birches growing at 21 sites around large nickel-copper smelter at Monchegorsk, Northwestern Russia. Proportion of reproducing trees, production of catkins, shoot and catkin weight, as well as the relative difference in weight of somatic structures of generative and vegetative shoots, were generally independent of pollution load; in 2003 birches growing in industrial barrens produced more catkins than birches growing in unpolluted forests. Thus, we found no support for the hypothesis that reproductive allocation should decrease with decrease in environmental capacity. Absence of adverse effects might indicate that long-lasting pollution impact already eliminated the most sensitive individuals from the affected birch populations.     

A modified glass bead compartment cultivation system for studies on nutrient and trace metal uptake by arbuscular mycorrhiza

A modified glass bead compartment cultivation system is described in which glass beads continue to be used in the hyphal compartment but are replaced by coarse river sand in the compartments for host plant roots and mycorrhizal hyphae. Arbuscular mycorrhizal (AM) associations were established using two host plant species, maize (Zea mays L.) and red clover (Trifolium pratense L.) and two AM fungi, Glomus mosseae and G. versiforme. When the standard and modified cultivation systems were compared, the new method yielded much more fungal tissue in the hyphal compartment. Using G. versiforme as the fungal symbiont, up to 30 mg of fungal dry matter (DM) was recovered from the hyphal compartment of mycorrhizal maize and about 6 mg from red clover. Multi-element analysis was conducted on samples of host plant roots and shoots and on harvested fungal biomass. Concentrations of P, Cu and Zn were much higher in the fungal biomass than in the roots or shoots of the host plants but fungal concentrations of K, Ca, Mg, Fe and Mn were similar to or lower than those in the plants. There were also significant differences in nutrient concentrations between the two AM fungi and these may be related to differences in their proportions of extraradical mycelium to spores. The high affinity of the fungal mycelium for Zn was very striking and is discussed in relation to the potential use of arbuscular mycorrhiza in the phytoremediation of Zn-polluted soils.     

Zn, Cd and Pb accumulation and arbuscular mycorrhizal colonisation of pennycress Thlaspi praecox Wulf. (Brassicaceae) from the vicinity of a lead mine and smelter in Slovenia

Significant hyperaccumulation of Zn, Cd and Pb in field samples of Thlaspi praecox Wulf. collected from a heavy metal polluted area in Slovenia was found, with maximal shoot concentrations of 14,590 mg kg(-1) Zn, 5960 mg kg(-1) Cd and 3500 mg kg(-1) Pb. Shoot/root ratios of 9.6 for Zn and 5.6 for Cd show that the metals were preferentially transported to the shoots. Shoot bioaccumulation factors exceeded total soil Cd levels 75-fold and total soil Zn levels 20-fold, further supporting the hyperaccumulation of Cd and Zn. Eighty percent of Pb was retained in roots, thus indicating exclusion as a tolerance strategy for Pb. Low level colonisation with arbuscular mycorrhizal fungi (AMF) of a Paris type was observed at the polluted site, whereas at the non-polluted site Arum type colonisation was more common. To our knowledge this is the first report of Cd hyperaccumulation and AMF colonisation in metal hyperaccumulating T. praecox.     

Testing nickel tolerance of Sorghastrum nutans and its associated soil microbial community from serpentine and prairie soils

Ecotypes of Sorghastrum nutans from a naturally metalliferous serpentine grassland and the tallgrass prairie were assessed for Ni tolerance and their utility in remediation of Ni-polluted soils. Plants were inoculated with serpentine arbuscular mycorrhizal (AM) root inoculum or whole soil microbial communities, originating from either prairie or serpentine, to test their effects on plant performance in the presence of Ni. Serpentine plants had marginally higher Ni tolerance as indicated by higher survival. Ni reduced plant biomass and AM root colonization for both ecotypes. The serpentine AM fungi and whole microbial community treatments decreased plant biomass relative to uninoculated plants, while the prairie microbial community had no effect. Differences in how the soil communities affect plant performance were not reflected in patterns of root colonization by AM fungi. Thus, serpentine plants may be suited for reclamation of Ni-polluted soils, but AM fungi that occur on serpentine do not improve Ni tolerance.     

Inoculation with arbuscular mycorrhizal fungi and addition of composted olive-mill waste enhance plant establishment and soil properties in the regeneration of a heavy metal-polluted environment

A greenhouse experiment was carried out in order to investigate the effects of arbuscular mycorrhizal (AM) fungi inoculation and the use of composted olive waste (COW) in the establishment of Tetraclinis articulata and soil properties in a heavy metal-polluted soil. The treatments assayed were as follows: AM?+?0 % COW, AM?+?1 % COW, and AM?+?3 % COW. The higher doses of COW in combination with AM fungi increased shoot and root biomass production of T. articulata by 96 and 60 %, respectively. These treatments trended to improve the soil properties evaluated, highlighting the C compounds and N as well as the microbiological activities. In relation to the metal translocation in T. articulata, doses of COW applied decreased the Cr, Ni, and Pb contents in shoot, as well as Cr and As in root, although the most of them reached low levels and far from phytotoxic. The COW amendment aided Glomus mosseae-inoculated T. articulata plants to thrive in contaminated soil, mainly through an improvement in both nutrients uptake, mainly P and soil microbial function. In addition, the combined use of AM fungi plus COW could be a feasible strategy to be incorporated in phytoremediation programs because it promotes soil properties, a better performance of plants for supporting the stress in heavy metal-contaminated soils derived from the mining process, and also can be a good way for olive-mill waste disposal.     

The role of arbuscular mycorrhiza in zinc uptake by red clover growing in a calcareous soil spiked with various quantities of zinc

Three pot experiments were conducted to investigate the role of arbuscular mycorrhiza (AM) in Zn uptake by red clover. Plants inoculated with Glomus mosseae and uninoculated controls were grown in a sterile calcareous soil in 'Plexiglas' (Acrylic) containers with two nylon net partitions (30 microm mesh) to separate the central root zone from the two outer hyphal zones. The effects of mycorrhiza on plant growth and Zn uptake changed dramatically with increasing Zn addition level (range 0-1200 mg kg(-1)) in the root zone. With Zn addition levels <300 mg kg(-1), added Zn did not affect plant yield and above the critical level plant yield gradually decreased but was always higher for mycorrhizal than for controls. Below the critical Zn application rate (50 mg kg(-1)), Zn uptake was enhanced while above this level Zn translocation to the shoots decreased. At all Zn addition levels, mycorrhizal colonization increased Zn absorption and accumulation in the roots, and this may help to explain the alleviation of Zn toxicity at high Zn application rates. As expected, AM colonization enhanced P nutrition and hence yield at all added Zn levels studied. Efforts were made to obtain direct evidence for hyphal contribution to Zn uptake by applying both Zn to the hyphal growth zone and additional P to the root zone to avoid the 'growth dilution effect'. The data demonstrate that mycorrhizal hyphae could absorb Zn directly from the soil and then transfer it to the plant roots. The hyphal contribution to Zn uptake by the host plant reached its maximum value at the Zn addition level of 50 mg kg(-1), in which Zn uptake via the extramatrical hyphae comprised 22% of total uptake, thus confirming the critical Zn application level found previously.     

Saprobe fungi decreased the sensitivity to the toxic effect of dry olive mill residue on arbuscular mycorrhizal plants

We studied the influence of olive mill dry residue (DOR) treated with saprobe fungi on growth of tomato and alfalfa colonized by Glomus deserticola. The application of 25g kg(-1) of dry DOR to soil decreased the shoot and root dry weight of tomato and alfalfa. Plants were more sensitive to the toxicity of DOR when colonized with the arbuscular mycorrhizal (AM) fungi. The sensitivity of both plants to the toxicity of DOR differed according to whether they were colonized by G. deserticola or by indigenous AM fungi. The phytotoxicity of DOR towards tomato and alfalfa was decreased by incubation the residue before planting with saprobe fungi for 20wk. The beneficial effects of AM fungi on plant growth added with DOR incubated with saprobe fungi depend of the type of the plant and AM fungi. The contribution of AM fungi to the beneficial effect of DOR incubated with saprobe fungi varied according to the type of the plant and AM fungi. G. deserticola increased the shoot and root dry weight of plants when they were grown in the presence of DOR incubated with saprobe fungi for 20wk. The beneficial effect of saprobe fungi on the dry weight and the level of AM mycorrhization of plants seem to be related to the decrease caused by these fungi in the phenol concentration in DOR. However, the toxicity of DOR due to substances other than phenols can not be ignored. The use of certain saprobe and AM fungi allows the possibility of using DOR as an organic fertilizer.     

Influence of arbuscular mycorrhizal fungi on the growth and nutrient status of bermudagrass grown in alkaline bauxite processing residue

A nursery experiment was conducted to evaluate the potential role of arbuscular mycorrhizal (AM) fungi in encouraging the vegetation cover on bauxite residue (red mud) sites. An alkali tolerant bermudagrass (Cynodon dactylon) adapted to local conditions were grown in red mud with different amendments with and without AM fungi to assess mycorrhizal effects on plant growth, mineral nutrition, metal uptake and neutralization of bauxite residue. Inoculation of AM fungi significantly increased the plant growth, nutrient uptake and reduced Fe, Al accumulation in plant tissue and also improved the soil physico-chemical and biochemical properties. Gypsum and sludge amended treatments inoculated with AM fungi had maximum biomass, nutrient uptake and reduced accumulation of metals. The neutralization of red mud was significant in presence of AM fungi than control. The experiment provided evidence for the potential use of bermudagrass in combination with AM fungi for ecological restoration of bauxite residue sites.     

Atmospheric pollution in an urban environment by tree bark biomonitoring--part I: trace element analysis

Tree bark has been shown to be a useful biomonitor of past air quality because it accumulates atmospheric particulate matter (PM) in its outermost structure. Trace element concentrations of tree bark of more than 73 trees allow to elucidate the impact of past atmospheric pollution on the urban environment of the cities of Strasbourg and Kehl in the Rhine Valley. Compared to the upper continental crust (UCC) tree barks are strongly enriched in Mn, Ni, Cu, Zn, Cd and Pb. To assess the degree of pollution of the different sites in the cities, a geoaccumulation index I_geo was applied. Global pollution by V, Ni, Cr, Sb, Sn and Pb was observed in barks sampled close to traffic axes. Cr, Mo, Cd pollution principally occurred in the industrial area. A total geoaccumulation index I_GEO-tot was defined; it is based on the total of the investigated elements and allows to evaluate the global pollution of the studied environment by assembling the I_geo indices on a pollution map.     

Zinc accumulation in Solanum nigrum is enhanced by different arbuscular mycorrhizal fungi

Solanum nigrum was found to proliferate in sediments with high levels of metal pollution. The effect of Zn on plant growth and tissue metal accumulation was assessed. The response of the plant to the inoculation with four different isolates of arbuscular mycorrhizal fungi (AMF) (Glomus sp. BEG140, Glomus claroideum, Glomus mosseae and Glomus intraradices) was studied. While the isolates of AMF did not have a significant (P<0.05) influence on mycorrhizal colonisation, increasing Zn concentration to high levels (500 and 1000 mgkg(-1)) induced significant (P<0.05) decrease of the AMF colonisation. In general, the presence of AMF did not affect the growth and biomass of S. nigrum individuals. However, the level of metal in the matrix affected S. nigrum growth; plants grown at 100 mgkg(-1) had significantly (P<0.05) lower leaf, stem, root and total biomass than control ones and plants growing at 500 and 1000 mgkg(-1) had the significantly (P<0.05) lowest biomass. Plants inoculated with the AMF G. claroideum and G. intraradices presented significantly (P<0.05) higher Zn accumulation in all plant tissues. In general, the stem tissues had the higher Zn content while the leaves registered the lowest values, which indicate a high translocation of the metal. AMF inoculation had no significant (P<0.05) influence on the metal translocation within the plant. This study suggests that inoculation with the AMF G. claroideum or G. intraradices, can enhance the Zn accumulation in the tissues of S. nigrum, not affecting the plant translocation capacities.     

Vegetational and mycorrhizal successions at a metal polluted site: Indications for the direction of phytostabilisation?

Plant communities on plots with different metal pollution levels were compared in a field study in order to select the most suitable plant species for the direction of secondary succession toward the targeted grassland vegetation. The vegetational succession showed a gradual increase in plant cover and the number of plant species on the less polluted locations. Two predominant grass species Calamagrostis varia and Sesleria caerulea were selected for phytostabilisation, but a severely reduced seed germination capacity obstructed their use in practice. The mycorrhizal succession showed a gradual replacement of non-mycorrhizal with mycorrhizal plant species. Similar levels of arbuscular mycorrhizal colonisation of a particular plant species may be developed within each growing season regardless of the levels of pollution, with the exception of vesicle/intraradical spore formation. The results suggest that lower overall mycorrhizal colonisation levels and increased vesicle/spore formation may be a part of a mycorrhizal strategy at the most polluted locations.     

Structural responses of Daucus carota root-organ cultures and the arbuscular mycorrhizal fungus, Glomus intraradices, to 12 pharmaceuticals

Pharmaceuticals and personal care products may enter the terrestrial environment through the amendment of agricultural soils with manure or biosolids with potential impacts on beneficial soil microbe populations. The beneficial symbiotic relationship between most plant species and arbuscular mycorrhizal fungi is a primary determinant of plant health and soil fertility. As such, there is increasing recognition of the need to study the impacts of anthropogenic stressors on plant-microbe interactions in soil ecotoxicology studies and risk assessment. A case study exploring the use of root-organ cultures to evaluate the effects of 12 common veterinary and human-use pharmaceuticals on the arbuscular mycorrhizal fungus, Glomus intraradices grown on Daucus carota root-organ cultures is presented. The bioassays were conducted over a 28-day exposure period at concentrations up to 1000mugl(-1). Root length and the fungal endpoints of hyphal growth and spore production were evaluated weekly during the study. Sulfamethoxazole and atorvastatin were the most phytotoxic compounds with EC(50) values of 45mugl(-1) and 65mugl(-1), respectively. Three compounds exhibited selective mycotoxicity, whereby the fungal symbiont was adversely affected at concentrations significantly less than that calculated for root length. The EC(50) for G. intraradices hyphal length was 45mugl(-1) for doxycycline, while carbamazepine and 17-alpha-ethynyl estradiol targeted spore production with EC(50) values of 113 and 116mugl(-1), respectively. The assay results indicate that the root lengths responded quickly to the presence of phytotoxic pharmaceuticals in the culture medium. Hyphal length is a sensitive endpoint after 21 days exposure, while spore production requires 28 days exposure before significant differences could be detected. Root-organ cultures provide an effective means to evaluate chemical stressors on arbuscular mycorrhizal fungi and can be used to screen for root-based phytotoxicity.     

Effects of nitrogen with and without acidified sulphur on an ectomycorrhizal community in a Sitka spruce (Picea sitchensis Bong. Carr) forest

This preliminary study investigated the effects of enhanced nitrogen (NH4NO3 at 48 kg ha(-1) y(-1)), sulphur (Na2SO4 at 50 kg ha(-1) y(-1)), acidified nitrogen and sulphur (H2SO4 + NH4NO3) at pre-stated doses (pH 2.5), and acidified nitrogen and sulphur deposition at double these doses on the ectomycorrhizal community associated with a 13-year-old Sitka spruce (Picea sitchensis) forest. Sulphur deposition had little impact on below ground ectomycorrhizal diversity, but stimulated sporocarp production. Nitrogen inputs increased below ground colonisation compared to acidified nitrogen and sulphur, largely due to an increase in Tylospora fibrillosa colonisation. Sporocarp production and ectomycorrhizal root colonisation by Lactarius rufus were reduced in the nitrogen treated plots. These observations suggest that nitrogen deposition to a young plantation may suppress ectomycorrhizal fungi producing large sporocarps. It is proposed that enhanced nitrogen deposition increases ectomycorrhizal nitrogen assimilation, consuming more carbon and leaving less for extrametrical mycelium and sporocarp development.     

Occurrence of spruce bark beetles in forest stands at different levels of air pollution stress

The spruce bark beetle, Ips typographus (L.) is the most serious pest of mature spruce stands, mainly Norway spruce, Picea abies (L.) Karst. throughout Eurasia. A complex of weather-related events and other environmental stresses are reported to predispose spruce stands to bark beetle attack and subsequent tree mortality; however the possible role of industrial pollution as a predisposing factor to attack by this species is poorly understood. The abundance and dynamics of I. typographus populations was evaluated in 60-80 year old Norway spruce stands occurring on 10 x 50 ha sites in five countries within the Carpathian range that were selected in proximity to established ozone measurement sites. Data were recorded on several parameters including the volume of infested trees, captures of adult beetles in pheromone traps, number of attacks, and the presence and relative abundance of associated bark beetle species. In several cases, stands adjacent to sites with higher ozone values were associated with higher bark beetle populations. The volume of sanitary cuttings, a reflection of tree mortality, and the mean daily capture of beetles in pheromone traps were significantly higher at sites where the O(3) level was higher. However, the mean infestation density on trees was higher in plots associated with lower O(3) levels. Captures of beetles in pheromone traps and infestation densities were higher in the zone above 800 m. However, none of the relationships was conclusive, suggesting that spruce bark beetle dynamics are driven by a complex interaction of biotic and abiotic factors and not by a single parameter such as air pollution.