Ecophysiological responses of Empetrum nigrum to heavy metal pollution

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Abstract

Chlorophyll, organic (citric and malic acids) and abscisic acid (ABA) contents and stem water potential were measured to indicate possible physiological effects of heavy metal deposition on Empetrum nigrum L. (crowberry). The leaves and stems of E. nigrum were collected at distances of 0.5 and 8 km from the Cu–Ni smelter at Harjavalta, south-west Finland. All the investigated parameters were clearly affected by heavy metal emissions. Chlorophyll contents in the leaves and organic acid contents in the leaves and stems were lower close to the emission source. Generally found increase in organic acid contents with increasing Ni concentrations was not found, which might be due to the lower production of organic acids measured by decreased photosynthesis near the smelter. In contrast, ABA contents in stems and leaves in general, were higher in plants growing 0.5 km from the pollution source. Close to the smelter the stem water potential of E. nigrum was less negative during the day but more negative during the night. These results suggest that smelter emissions have a negative effect on the ecophysiology of E. nigrum even though it is considered to be a tolerant species to heavy metals.

Introduction

Heavy metal emissions are reported to have serious impacts on plants growing in the surroundings of Cu–Ni smelters (Amiro and Courtin, 1981, Helmisaari et al., 1995, Shevtsova, 1998). Many dwarf shrub species are described to grow on severely heavy metal contaminated sites in the vicinity of Cu–Ni smelters in the northern hemisphere (Laaksovirta and Silvola, 1975, Bagatto and Shorthouse, 1991, Shorthouse and Bagatto, 1995, Shevtsova, 1998, Malkonen et al., 1999). The evergreen dwarf shrub Empetrum nigrum L. (crowberry) has a wide ecological amplitude (Bell and Tallis, 1973, Elvebakk and Spjelkavik, 1995), and it survives at a distance of 0.5 km from the Cu–Ni smelter at Harjavalta, south-west (SW) Finland, where almost all other plant species have disappeared (Laaksovirta and Silvola, 1975, Helmisaari et al., 1995). At this site, not only the elevated heavy metal concentrations in the soil (Derome and Lindroos, 1998), but also decreased soil water-holding capacity (Derome and Nieminen, 1998) impairs growing conditions for plants. The metal tolerance mechanism of E. nigrum is not fully known, but one explanation for its survival is the accumulation of high Cu and Ni concentrations in older stems. Thus, E. nigrum is able to restrict the accumulation of Cu and Ni in its younger, growing parts (Helmisaari et al., 1995, Uhlig et al., 2000, Monni et al., 2000). E. nigrum is ericoid mycorrhizal plant and ericoid mycorrhiza of other dwarf shrub species Calluna vulgaris (L.) Hull. roots have been found to have an important role in Cu and Zn tolerance (Bradley et al. 1981, Bradley et al. 1982).

The ecophysiological response of E. nigrum to metals has not been previously investigated, but growth reduction in response to increasing emission levels (Shevtsova, 1998) clearly indicates an ecophysiological impact of heavy metals on E. nigrum. In earlier investigations, chlorophyll, abscisic acid (ABA) and organic acid contents and water potential of plants have been used to indicate plant response to elevated heavy metal levels (Lee et al., 1978, Rauser and Dumbroff, 1981, Angelov et al., 1993, Bishnoi et al., 1993). The photosynthetic rate and chlorophyll concentrations of plants have been found to be decreased by Cu, Ni, Cd and Pb (Lamoreux and Chaney, 1978, Becerril et al., 1989, Angelov et al., 1993, Bishnoi et al., 1993, Pandolfini et al., 1996), and an effect of Ni, Zn and Cd on water relations of plants is reported (Rauser and Dumbroff, 1981, Bishnoi et al., 1993). In experimental studies, stomatal conductance and water potential of the leaves have decreased and the ABA content, which regulates the water status of the plant, increased when plants were exposed to Ni (Rauser and Dumbroff, 1981, Bishnoi et al., 1993). However, also factors other than heavy metals may influence the ABA relations in the plants; higher levels of ABA in the roots and shoots is a typical response to nitrogen deficiency (Goldbach et al., 1975). ABA is also involved in the synthesis of proteins, prevention of precociuous germination, induction of dormancy and abscission of leaves (Marschner, 1995).

In general, plants possess physiological mechanisms that enable them to resist elevated heavy metal concentrations in their substrate (Antonovics et al., 1971, Baker, 1981, Baker, 1987, Woolhouse, 1983). Heavy metal tolerance of plants is species- and metal-specific and plants can either detoxify metals by binding them with organic acids, proteins or other ligands (Lee et al., 1978, Rauser and Curvetto, 1980, Godbold et al., 1984), or accumulate the metals in different plant parts or cell organelles (Reilly, 1969, Bringezu et al., 1999). Many plant species which are tolerant to Cu or Ni (Lee et al., 1978, Rauser, 1984) or to both Cu and Ni are found (Hogan and Rauser, 1979). However, the tolerance of these two metals is usually achieved by two different mechanisms. Organic acids play a central role in detoxifying metals in Ni- and Zn-accumulating plants (Ernst, 1975, Mathys, 1977, Lee et al., 1978, Yang et al., 1997), while Cu forms complexes with proteins and amino acids (Rauser, 1984).

The aim of this study was to investigate the general ecophysiology of E. nigrum, and to determine the responses of E. nigrum to heavy metal pollution by measuring physiological parameters. Chlorophyll contents of leaves were used as an indicator for physiological stress, because photosynthesis has been found to decrease due to elevated concentrations of Cu and Ni. Organic acids were measured to find out if there is any connection between organic acid contents and Ni resistance. To indicate the previously described connection between Cu, Ni and desiccation stress, the stem water potential and abscisic acid contents of E. nigrum leaves and stems were studied.

Section snippets

The Harjavalta smelter area

The shoots of E. nigrum were collected at distances of 0.5 and 8 km to the south-east (SE) of the Cu–Ni smelter at Harjavalta, SW Finland. The Cu smelter was established in 1945 and the Ni smelter in 1960. Sulphur dioxide and heavy metals have been emitted into the environment for the past 40–60 years. The deposition of metals near the smelter was considerably reduced in the 1990s after a taller stack was built and electrostatic filters installed (Rantalahti, 1995). The prevailing wind

Chlorophyll contents

Plant chlorophyll (a+b) contents were lower at 0.5 than at 8 km, and the differences between the means were statistically significant through the whole season (P<0.05) (Fig. 1a). The means of the chlorophyll (a+b) contents varied between 1.9 and 3.2 μmol chlorophyll g−1 dry wt. and were the lowest in October compared to the other sampling dates. The chlorophyll a/b ratio, was generally lower at a distance of 8 km than at 0.5 km, and the difference between the means at two distances was

Discussion

Chlorophyll contents in the leaves of E. nigrum were, in general, within the range reported for unpolluted locations in Swedish Lapland for Empetrum nigrum subsp. hermaphroditum (Michelsen et al., 1996). However, at the 0.5 km site, the chlorophyll contents in E. nigrum were 15–30% lower than the values for plants growing at 8 km. Similar decreases in chlorophyll contents have been reported for several broadleaved species exposed to metals (Angelov et al., 1993, Bishnoi et al., 1993). The

Conclusions

Our results indicate that heavy metal pollution has negative effects on E. nigrum. The decreased contents of chlorophyll pigments and organic acids and increased ABA contents indicate a reduction in the physiological activity of E. nigrum near to the pollution source. Although E. nigrum is known to be one of the most tolerant species near Cu–Ni smelters in the northern hemisphere (Helmisaari et al., 1995, Uhlig et al., 2000) and to accumulate high concentrations of Cu and Ni in its living parts

Acknowledgements

We would like to thank the staff of the Finnish Forest Research Institute, the Department of Plant Physiology and Microbiology, University of Tromsø, and the Department of Physiological Ecology of Plants, University of Tübingen, for helping with the practical aspects of this study. Olavi Junttila and Maija Salemaa made critical comments on the manuscript and John Derome revised the English. The work was funded by Maj and Tor Nessling Foundation and NorFA.

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