Evaluating trivalent chromium toxicity on wild terrestrial and wetland plants
Graphical abstract
Species sensitivity ranks using EC25s for the tested wild species, crops [bold], and trees [underlined] exposed to Cr3+ in artificial soil during the concentration-response experiments. Of the 32 species tested, nine species required stratification and were thus initially exposed to chromium either immediately after stratification [A] or during stratification [B]. Only species exhibiting effects are included.
Introduction
Mining of chromium and its use in industrial activities, including alloy and stainless steel production, leather tanning, pulp and paper manufacturing, wood preservation, and other chemical and metallurgical processes, have raised worldwide concerns due to the risk of environmental contamination and possible effects on the food chain, from primary producers to humans (Dhal et al., 2013). The world-leading countries in chromium mining are South Africa, Kazakhstan, India and China (ICDA, 2011). In Northern Ontario, Canada, extensive and high grade chromite (FeCr2O4) deposits were discovered in the Ring of Fire region (latitude 52°57′N, longitude 87°22′W) (Fig. 1).
The most stable and commonly found forms of chromium in nature are trivalent (Cr3+) and hexavalent (Cr6+), which have differing physical and chemical characteristics. Hexavalent chromium is more soluble and can be easily transferred within and between environments (Fendorf, 1995). Sources of both forms of chromium vary: Cr3+ is abundantly present in chromite, while Cr6+ naturally exists in crocoite (Zayed and Terry, 2003).
The average level of chromium in soil worldwide is around 10–100 mg kg−1 with a mean of 60 mg kg−1 and depends on the bedrock (Kabata-Pendias, 2011, Alloway, 2013). The acceptable level in soil for the protection of environmental and human health has been estimated at 64 mg kg−1 (CCME, 2015). However, major anthropogenic pollution can alter the normal environmental concentrations. For instance, the background level in Manitoba, Canada, was 30 mg kg−1 while it was 718 mg kg−1 near a wood treatment facility (Pawlisz et al., 1997). In Dartmouth, Nova Scotia, Canada, levels reached 5000 mg kg−1 in soil close to a wood preservation factory (Bamwoya et al., 1991 cited in Pawlisz et al., 1997). In the St. Mary's River system, levels exceeding 328,000 mg kg−1 were detected in soils and 40,000 mg kg−1 in sediments near a tannery facility in Michigan, a superfund site (USEPA, 1992). Likewise, levels of 630 mg kg−1 were measured in the tannery effluent-contaminated soil in Pakistan (Khan, 2001) and up to 2700 mg kg−1 in India (Raju and Tandon, 1999). The Welland Canal in Ontario, Canada, contains concentrations beyond 5120 mg kg−1 downstream of steel industries (Pawlisz et al., 1997). Chromium was also found in the air in Canada (1–545 μg m−3), with the main sources being industrial emissions (Pawlisz et al., 1997).
Chromium is not an essential nutrient for plants but Cr3+ is required in trace amounts in animals (Bluskov et al., 2005, Panda and Choudhury, 2005). A few studies have shown that chromium in relatively small quantities may promote plant productivity (Zayed and Terry, 2003, Prasad et al., 2010). However, it has also been shown that both Cr3+ and Cr6+ caused delays in seed germination, reduced photosynthesis and biomass, chlorosis, necrosis, and eventually death in crops (Davies et al., 2002, Panda and Choudhury, 2005, Lopez-Luna et al., 2009). Antagonistic interactions or interference may occur between chromium and other essential nutrients, including calcium (Scoccianti et al., 2006), iron (Schmidt, 1996), phosphorus, potassium (Davies et al., 2002), manganese, zinc, and possibly copper (Abreu et al., 2002). Chromium is known to affect metabolic processes via oxidative stress causing chloroplast and pigment alterations (Panda and Choudhury, 2005, Scoccianti et al., 2006). Many studies have shown that chromium suppresses the function and regulation of several proteins (Panda and Choudhury, 2005, Labra et al., 2006, Dotaniya et al., 2014), including antioxidant enzymes (Sinha et al., 2005), and causes chromosomal impairments within plant tissues (Zou et al., 2006, Kranner and Colville, 2011).
Phytotoxicity of chromium (mostly Cr6+) to juvenile plants has been studied in crops and species of economic value within controlled experimental environments, often under hydroponic conditions (Zou et al., 2006, Prasad et al., 2010, Stasinos and Zabetakis, 2013). Other, but fewer, studies have shown that chromium (Cr3+ and Cr6+) was detrimental to seed germination in experiments also involving crops (Scoccianti et al., 2006, Labra et al., 2006, Amin et al., 2013, Dotaniya et al., 2014), and large differences in sensitivity were often found. For instance, Lopez-Luna et al. (2009) found decreases in germination of both Sorghum bicolor × Sorghum sudanense L. and Triticum aestivum L. grown in soil and exposed to Cr3+ at >500 mg kg−1 concentrations, yet germination of Avena sativa L. was not affected below 4000 mg kg−1.
The seed stage is an important component of plant reproduction and dispersal, and for survival in unfavourable conditions. A soil seedbank is a collection of buried, dormant seeds found naturally in soils. Seeds can remain intact and viable in soils for several years awaiting optimal germination conditions (i.e. soil moisture and oxygen content, temperature, light) (Brändel, 2006, Honda, 2008). Most importantly, soil seedbanks constitute sources for vegetation recovery and restoration following natural or anthropogenic disturbances (Armesto and Pickett, 1985, Klimkowska et al., 2010). Seeds can be affected by soil and water contamination arising from persistent man-made disturbances which may have direct effects on seedbank compositions.
There is a dearth of toxicological studies dealing with native species shaping natural communities (Olszyk et al., 2008, Prasad et al., 2010). With regards to chromium, many studies were more concerned with the effects of Cr6+ on economically important species (Zou et al., 2006, Labra et al., 2006, Kranner and Colville, 2011), since Cr6+ is more harmful at lower concentrations compared to Cr3+. However, mining of chromite ore is associated with Cr3+ contamination. It is important to understand how plants cope with heavy metal pollution in order to identify species with the highest sensitivity to chromium and then be able to predict impacts at the individual, population, and community levels. The overall objective of this study was to perform concentration-response tests to determine chromium toxicity on a range of plants with diverse ecological characteristics (i.e. taxonomic group, growth habit, and habitat). Seeds were exposed to a suite of chromium (Cr3+) concentrations, including natural environmental levels and those simulating different levels of contamination that may originate from anthropogenic activities. Two experiments were conducted: one using seeds grown in artificial soil (experiment 1) and the second with seeds present in the seedbank from soils collected near the Ring of Fire region (experiment 2). The objectives of these experiments were to assess the effects of Cr3+ on seed germination, early seedling health, and soil seedbanks.
Section snippets
Methods
Experiment 1 was conducted between October 2013 and October 2014. Soil samples for experiment 2 were collected in Nibinamik (Summer Beaver) traditional/reserve territory, Northern Ontario (Fig. 1), in September 2014 and the seedbank study was performed between October 2014 and April 2015. Both experiments were conducted in growth chambers (Conviron, PGW36, Winnipeg, Manitoba) situated at the National Wildlife Research Centre (Environment and Climate Change Canada), Ottawa, Canada. Artificial
Results
The measured levels of total chromium in dosed artificial soil were slightly higher than the expected (nominal) levels, most notably in control soils where natural background levels were detected (Fig. S1, Table S2). Likewise, the background level of total chromium in soils collected for the seedbank study was 26.4 ± 5.9 mg kg−1 (Table S2). The background levels of other metals in the control artificial soil and soils from Nibinamik were found to be below accepted levels (Table S2). Therefore,
Effect of chromium (Cr3+) on plants
In natural environments with active chromium mining, sensitive species may be outcompeted by other tolerant species and could disappear. This study with artificial soil demonstrated that low levels of Cr3+ (250 mg kg−1) adversely affected the germination of seven species (22% of all species tested) from six families (33% of all families), while higher levels (500 and 1000 mg kg−1) affected 22 and 30 species (69% and 94%), respectively, from 16 families (89%). The seedbank study confirmed the
Acknowledgements
We wish to thank the Chief and Band Council members of the Nibinamik community for giving the authors permission to enter their traditional land and collect soil samples during the field work season. Thanks to Carly Casey and Simon Gräfe for laboratory assistance, and Sara Rodney for valuable information on statistical analyses and SAS software. Map in Fig. 1 created in ArcView version 10.3 with the help of Lukas Mundy. This work was funded by Environment and Climate Change Canada and by the
References (71)
- et al.
Effect of chromium on seed germination, seedling growth and yield of peas
Agric. Ecosyst. Environ.
(1993) - et al.
Chemical and microbial remediation of hexavalent chromium from contaminated soil and mining/metallurgical solid waste: a review
J. Hazard Mater.
(2013) Surface reactions of chromium in soils and waters
Geoderma
(1995)Relationships between chromium biomagnification ratio, accumulation factor, and mycorrhizae in plants growing on tannery effluent-polluted soil
Environ. Int.
(2001)- et al.
Chromium occurrence in the environment and methods of its speciation
Environ. Pollut.
(2000) - et al.
Metals and seeds: biochemical and molecular implications and their significance for seed germination
Environ. Exp. Bot.
(2011) - et al.
Zea mays L. protein changes in response to potassium dichromate treatments
Chemosphere
(2006) - et al.
Effects of heavy metals on seed germination and early seedling growth of Arabidopsis thaliana
Plant Growth Regul.
(2005) - et al.
Toxicity assessment of soil amended with tannery sludge, trivalent chromium, and hexavalent chromium, using wheat, oat and sorghum plants
J. Hazard Mater.
(2009) - et al.
The biochemistry of environmental heavy metal uptake by plants: implications for the food chain
Int. J. Biochem. Cell B
(2009)