Impact of nickel mining in New Caledonia assessed by compositional data analysis of lichens
© The Author(s) 2016
Received: 15 June 2016
Accepted: 11 November 2016
Published: 28 November 2016
The aim of this study is to explore the use of lichens as biomonitors of the impact of nickel mining and ore treatment on the atmosphere in the New Caledonian archipelago (South Pacific Ocean); both activities emitting also Co, Cr and possibly Fe. Metal contents were analysed in thirty-four epiphytic lichens, collected in the vicinity of the potential sources, and in places free from known historical mining. The highest Ni, Co, and Cr concentrations were, as expected, observed in lichens collected near ore deposits or treatment areas. The elemental composition in the lichens was explored by multivariate analysis, after appropriately transforming the variables (i.e. using compositional data analysis). The sample score of the first principal component (PC1) makes the largest (positive) multiplicative contribution to the log-ratios of metals originating from mining activities (Ni, Cr, Co) divided by Ti. The PC1 scores are used here as a surrogate of pollution levels related to mining and metallurgical activity. They can be viewed as synthetic indicators mapped to provide valuable information for the management and protection of ecosystems or, as a first step, to select locations where air filtration units could be installed, in the future, for air quality monitoring. However, as this approach drastically simplifies the problem, supplying a broadly efficient picture but little detail, recognizing the different sources of contamination may be difficult, more particularly when their chemical differences are subtle. It conveys only relative information: about ratios, not levels, and is therefore recommended as a preliminary step, in combination with close examination of raw concentration levels of lichens. Further validation using conventional air-monitoring by filter units should also prove beneficial.
Nickel exploitation began in the archipelago of New Caledonia (South Pacific Ocean), soon after the discovery by Jules Garnier in 1864 of nickel silicates, called garnierite. Ever since, the economic life of the island has beaten to the rhythm of nickel demand. Nickel mining is now becoming the largest employer in New Caledonia (more than 7500 employees in 2015). When exploitation first began, high-grade veins of garnierite (6–7% Ni), identifiable by their green colour, were extracted. Miners were soon interested by other lateritic horizons that developed on ultramafic weathered rocks. These nickel-enriched soils are located near the surface, so opencast mining was preferred. For such an approach, vegetation and top soil are first removed, and ore is extracted and transported by trucks on unpaved roads or by belt conveyors to loading zones or to ore treatment plants. All these operations are expected to release into the atmosphere huge amounts of dust enriched in trace metals (Chakraborty et al. 2002; Huertas et al. 2012), known to affect human health: it can lead to respiratory dysfunction, cardiovascular disease and cancer (International Agency for Research on Cancer 1990; Andersen et al. 1996; Harrison and Yin 2000; Menvielle et al. 2003). Nickel mining and ore treatments are known to have deleterious effects on the quality of the New Caledonian environment by degrading natural ecosystems (Bramwell 2011; Kettle et al. 2007; Losfeld et al. 2015), forests (Jaffré et al. 1977), and the lagoon (Gunkel-Grillon et al. 2014; Hédouin et al. 2007). Furthermore, the smallest dust particles can be spread over very long distances, far from emission sources. The impact of mining on the surroundings and the geographical dispersion of metals are often estimated using atmospheric filtration units covering the territory of interest. The filters are frequently changed because meteorological conditions (humidity, wind strength and direction variability, etc.) drastically affect the quality and quantity of dust material collected. This procedure is commonly used as a reference method, but remains costly and time consuming. Yet, at least for preliminary screening, some alternatives do exist. They are based on the biomonitoring capabilities of some organisms or organic material, such as tree rings, peat deposit, mosses or epiphytic lichens (Aslan et al. 2012; Balabanova et al. 2013a; Boamponsem et al. 2010; Mihaljevič et al. 2008; Monna et al. 2012; Richter et al. 2007; Spiro et al. 2004). Epiphytic lichens are symbiotic organisms, composed of fungi and algae. They have the ability to absorb and accumulate metals, through wet and dry deposition, without symptoms, at least up to a certain level (see the seminal work from Nylander 1866, and for reviews of recent studies, Conti and Cecchetti 2001; Szczepaniak and Biziuk 2003). Their nutrient uptake therefore relies exclusively on air constituents, since they have neither roots nor cuticles. Concerning absorption of metals, three main mechanisms have been invoked: intercellular absorption by an exchange process, intercellular accumulation, and entrapment of metal-rich particles (Richardson 1995; Szczepaniak and Biziuk 2003). The respective role of these processes is, however, not fully understood, all the more since metal contents in thalli seem to experience periods both of accumulation and release, related to several environmental factors. In any case, it has been demonstrated that lichens are good biomonitors of trace elements, as their thalli concentrations are correlated with those in their surrounding environment (Conti 2008). The sampling of these organisms is inexpensive and easy (when thalli are abundant), in any case free from heavy logistics. Furthermore, it can be problematic to compare concentrations from different individuals, even within the same species, because biomonitors may be affected by several internal factors, such as body morphology, age, and exposure (Carignan et al. 2002; Doucet and Carignan 2001; Kinalioglu et al. 2010; Senhou et al. 2002). That is why, instead of examining absolute concentration levels, some authors have proposed normalizing concentrations of potentially anthropogenic elements by a single chosen reference element, exclusively of crustal origin, such as titanium, aluminium or a lanthanide (i.e. all metal concentrations are divided, for instance, by those of Ti, the normalizing element used in the following, Goix et al. 2013; Monna et al. 2012). This can be viewed as the first step towards the so-called enrichment factor (EF) calculation, which aims at detecting, in combination with other tools, which elements are enriched in relation to local soils or earth crust (Agnan et al. 2013; Aničić et al. 2009; Aslan et al. 2012; Cloquet et al. 2015). The only difference is that there is no final normalization by local reference values or, more simply, by those of the upper continental crust (e.g. Wedepohl 1995).
Although convenient, and most of the time efficient (Bergamaschi et al. 2002; Nyarko et al. 2006), the normalization of concentrations of potentially anthropogenic elements by a single chosen reference element (e.g. Metals/Ti or Metals/Al), or possibly by the sum of reference elements (e.g. Metals/(Ti + Al)), presents an unavoidable drawback: the use of new ratio-based variables with the same element(s) as denominator is mathematically inadequate for all statistics based on correlations (see Pearson 1896; Kim 1999, for a complete discussion, and Monna et al. 2006 for a debatable use of multivariate statistics on such ratio data). The use of [metal/Ti] or [metal/(Ti + Al)] ratios are still mathematically correct when correlations are not computed (only sites are compared), but the geochemical signals carried by all other pairwise ratios (e.g. Ni/Cr, Co/Zn, etc.) are not really taken into account, although they may contain subtle information about the origin of the metals.
The compositional data are by nature closed because the sum of all components, including those not measured, is constrained (to 1, or to 100%). The covariance structure of such a dataset is necessarily biased (Filzmoser et al. 2009a, b), so that most multivariate techniques become doubtful without a proper transformation. Undeniable progress has, however, been made since the 1980s to open the dataset and to remove problems related to spurious inter-element correlations (Aitchison 1982; Van der Weijden 2002). The data are, with these new techniques, treated as a whole, allowing each inter-elemental ratio to be examined (Van den Boogaart and Tolosana-Delgado 2013).
In the present study, elemental concentrations in Co, Cr, Ni, Fe, Cu, Zn and Ti were analysed in more than 30 epiphytic lichens collected in New Caledonia, at various distances from modern mining activities, and from an ore treatment plant in Noumea, from within the city, and from areas free from any known historical mining. Ti is supposedly of crustal origin and used as reference, Cu and Zn have potentially an industrial/domestic origin, while Ni, Co, Cr and, to a lesser extent, Fe are especially targeted, because they are expected to be emitted by mining and metallurgical activity. The objective of this study is therefore to evaluate the potential of lichens as biomonitors of air quality in the context of Ni mining and ore treatment. Compositional data analyses were used to compute a synthetic index summarising the local degree of contamination related to mining and metallurgy.
Two sites directly related to nickel mining and smelting were more particularly targeted in this study. The first is the Poro mine, situated on the east coast, one of the oldest still active extraction sites (Fig. 1c). The second is the metallurgical ore factory of Doniambo, located in Noumea (Fig. 1d). It was established in 1910 on an isolated, 7 ha site, far away from the town of Noumea in its past configuration. Today, this site covers 250 ha. It is surrounded by many industrial areas, the Noumea harbour and, more problematically, several residential zones set up following the considerable extension of the regional capital, Noumea, which now counts 100,000 inhabitants. About 3.5 million tons of ores per year, extracted from several mines all over Grande Terre, and transported by tankers, are treated in this pyrometallurgical plant. The proximity of the Doniambo plant to the capital generates environmental atmospheric issues for residents, in terms of (i) SO2 levels, a pollutant emitted from the fuel power plant powering the energy-consuming pyrometallurgical operations, and (ii) nickel-enriched PM10 (particulate matter with a diameter below 10 µm) released from the plant. The situation is such that atmospheric pollution levels are given with the TV weather forecast.
Thirty-four epiphytic lichen thalli belonging to the Parmeliaceae family were collected in New Caledonia in March 2012 from around the Poro mine (PORO, n = 8), and the Noumea peninsula (NOU, n = 15). Several additional lichens were also collected from the countryside between these two sites (COUN, n = 11), far from any known historical mining sites or potentially polluting human activities (Fig. 1b–d). Lichens were collected exclusively from tree trunks, always at least 1.5 m above ground level, by means of pre-cleaned plastic knives. Sometimes, lichens were moistened with Milli-Q water to facilitate their removal from the trunks. Any tree bark fragments collected with thalli were systematically eliminated. The samples were immediately stored in hermetically closed plastic bags.
Quality control of the analyses
LOD (µg g−1)
BCR 482 (µg g−1)
NIST 1547 (µg g−1)
Body metal concentrations in lichens (in µg g−1, except iron content in %w/w)
Once it has been demonstrated that there is a difference between at least one pair of group population means, multiple comparisons can be performed using Hotelling T2 tests, along with Bonferroni corrections, as usual.
Data preparation, transformations, statistical procedure and plot drawings used the free R software (R Core Team 2008), with the FactoMineR (Lê et al. 2008), compositions (Van den Boogaart and Tolosana-Delgado 2008), hotteling (Curran 2013) and ggplot2 packages (Wickham 2009). Mapping used the Quantum GIS free software (QGIS Development Team 2010).
Results and discussion
Elemental concentrations in lichens
Concentrations in lichens, together with the geometric means of the three groups (NOU, PORO and COUN), are reported in Table 2. They vary widely, covering 2 or 3 orders of magnitude. Such huge variability is rather unusual in environmental studies dealing with lichens, where differences of one or two orders of magnitude are more common (Goix et al. 2013; Zvěřina et al. 2014). As expected, the highest Co, Cr and Ni concentrations (above 100, 1000 and 3000 µg g−1, respectively) are observed in two of the Poro samples (PORO #28 and #32), and close to the Doniambo plant (NOU #16) (Table 2). Maximum Zn and Cu contents are recorded at Noumea (NOU #13 and #19). For comparison, the Co, Cr, and Ni concentrations reported for lichens collected close to an open-pit olivine mine in Greenland (Søndergaard 2013) were about one or two orders of magnitude lower than those observed at Poro, but comparable with our COUN samples. Although, at first sight, the overall picture drawn from absolute concentrations seems to be reliable, a non-negligible part of the variations observed in the Co, Cr and Ni concentrations might also be due to body morphology, age, and exposure of individuals, as suggested by the huge variations in Ti contents, an element assumed of crustal origin. Rather than normalizing all metals to a single crustal element (e.g. Ti), and hence comparing the sites, a compositional data analysis approach was preferred here.
Compositional data analysis
The first two axes of the covariance biplot computed after a clr-transformation of the dataset explain 82.5% of the total variability (57.8 and 24.7% respectively), a value reasonably high for D = 7 parts (Fig. 2). This representation must, however, be interpreted differently from the traditional biplot originally proposed by Gabriel (1971), because all the components are somehow intermixed during the clr-transformation. Its key reading is the link between two variable arrow heads, which approximates the standard deviation of their corresponding log-ratios (see Aitchison and Greenacre 2002; Van den Boogaart and Tolosana-Delgado 2013 for more details about compositional biplots). The mining elements (Ni, Co, Cr), and to a lesser extent Fe, plot relatively close to each other (i.e. their links are short). They therefore present relatively constant log-ratios, while the largest links observed between [Ni, Co, Cr] and Ti, on the one hand, and between Zn and Cu, on the other hand, indicate the most relative variations across the lichens. Interestingly, the orthogonality between these links underlines the absence of correlation between their corresponding log-ratios (e.g. Zn/Cu is not correlated with Ni/Ti).
The three previously defined groups of lichens can be distinguished mainly by PC1 (Fig. 2). The PORO samples plot on the right of the diagram (positive side of PC1), while COUN samples plot on the left (negative side of PC1). The NOU samples lie between the two other groups. Although this structure is clearly visible, it worth noting that multivariate analysis of variance (MANOVA) can also be applied in less trivial cases. The MANOVA indicates that at least one group appears to be significantly different from the others (p < 10−6). Multiple pairwise Hotelling T2 tests indicate that each group is significantly different from the others (p < 10−4), even after Bonferroni correction (Holm 1979).
Impact levels and geographical dispersion
The PC2 sample scores, which mainly depict the log ratio of Zn/Cu, are not very informative here, because the three groups of samples (NOU, COUN and PORO) do not exhibit any significant difference concerning this variable, neither in terms of mean, nor in terms of variance (Fig. 2).
Although the results are fully coherent in their present form, the addition (or suppression) of elements may drastically modify the outputs of the multivariate analysis. The environmental question must therefore always be kept in mind, so that only those elements supposed to be of interest are processed; the sought-after signals might otherwise be obscured. The transformations required to process the compositional data properly mean that the original concentration values are no longer directly present. This loss of contact can be a serious problem in certain studies, such as those undertaken for ecotoxicological evaluation, where the knowledge of pollutant levels is of paramount importance. The compositional biplot conveys only relative information because of the compositional structure of the data, so that loadings cannot be interpreted separately, but only as pairs or groups of variables. Such grouping may make the overall picture less easy to understand. It is therefore strongly recommended to use compositional data analyses as a complement to the traditional approach (which consists in closely examining raw concentration levels in lichens, possibly also using concentration normalization), when mapping a synthetic contamination index, or for in-depth studies of the associations between variables, or between individuals.
Our results demonstrate that epiphytic lichens, at least those belonging to the Parmeliaceae family, can be used as biomonitors for air quality assessment in a Ni mining context. As expected, raw Ni, Co, Cr concentrations in lichen bodies are high, even extremely high, close to the mine and to the ore treatment plant. Concentrations decrease as distance from these infrastructures increases. In our case, the sample scores for the first principal component, computed after appropriate transformation, can be used as an overall environmental indicator. The PC1 includes all the main elements emitted into the atmosphere during Ni extraction and treatment. This approach may provide valuable information for the management and protection of ecosystems, highlighting those areas most contaminated by mining activity, and identifying the best sites for the installation of costly filtration units, for continued air quality monitoring. However, as the synthetic index drawn from PC1 drastically simplifies the problem by providing a broad picture, it may also preclude the differentiation of sources, when their compositional differences are subtle. Applying compositional data analyses in combination with close examination of raw data from lichens is therefore recommended, because contact with their absolute values is lost during the statistical analysis. Although the results of this study indicate that lichens can be used beneficially for assessing atmospheric dispersion of Ni in the surroundings of mining and metallurgical activities, further study in an area where air quality or atmospheric deposition data are also available would be useful to evaluate more precisely the performances of the approach described here.
CD, BB and FM collected the samples; PL, RL and FM performed the chemical analyses. CP wrote the first draft. All authors contributed equally to the scientific discussion and approved the final manuscript. We are grateful to the two anonymous reviewers whose judicious comments have greatly improved the manuscript. All authors read and approved the final manuscript.
The authors declare that they have no competing interests.
This work was funded by the CNRT (French National Center for Technological Research) (www.cnrt.nc) “Nickel and its environment”, Noumea, New Caledonia (5PS2013-CNRT.UNIV.BORDEAUX/DMML15042015). The French Ministry of Research funded the Ph.D. fellowship of Camille Pasquet.
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