2. Metal tolerance in treesThe long

2. Metal tolerance in treesThe long generation time of trees acts to prevent a rapidselection of heavy metal tolerant genotypes, the productionof which is random or induced by the pollutant (Dickinsonet al., 1991). Therefore, tree species are generally not able toadapt to high concentrations of heavy metals in the soil,resulting in the evolution of only a few metal-tolerantecotypes (Kahle, 1993). A characteristic feature of metal￾liferous soils in Europe is the absence of woody and treespecies (Turner, 1994). However, the lack of reportedtoxicity symptoms in trees indicates that their tolerancemechanisms may allow them to withstand higher heavymetal concentrations than agricultural crops (Riddell-Black,1993). Trees that are not especially selected for metaltolerance can generally survive in metal-contaminated soil,albeit usually with a much reduced growth rate (Dickinsonet al., 1992).Restricted location of metals in roots and low uptake intofoliage is the most common resistance trait (Dickinson andLepp, 1997), but true tolerance requires the development ofone or more precise physiological mechanisms with agenetic basis (Dickinson et al., 1991). But the geneticstability of tolerance is questionable, as it can be bothinduced and lost in trees, so their ability to acclimatise tofluctuating stress due to pollution may be very important forthe survival of tree species. Dickinson et al. (1992)described tolerance and survival of plants on metal-conta￾minated soils as arising from ‘‘an orchestrated multiplicityof physiological and biochemical responses, including bothavoidance and true resistance mechanisms’’.The wide genome of trees and facultative tolerance, suchas the redistribution of roots to less contaminated zones ofsoil, allows survival of trees not selected for metal toleranceon polluted soils. Various studies have shown that theacclimation of trees to their soil environment is of consid￾erable importance and may be a significant factor in treesurvival in metal-contaminated soil, although soil fertilitycan be important and mycorrhizal fungi, the hyphae ofwhich can sequester metal ions, may increase metal resist￾ance.Borgega˚rd and Rydin (1989) considered the effects ofheavy metals on root development in birch trees which hadcolonised soil covering copper mine tailings. Tree survivalwas good despite roots penetrating into the spoil; anexample of facultative tolerance in a species, not especially530 I.D. Pulford, C. Watson / Environment International 29 (2003) 529–540selected for metal tolerance, but also not being excludedfrom a substrate containing high heavy metal concentrations. Kopponen et al. (2001) tested the tolerance to Cu andZn in birch clones from metal-contaminated sites whengrown in an artificially contaminated soil. They foundconsiderable variation in the tolerance of samples fromwithin the same population. There was, however, an overallpattern in which tolerance was related to the type ofcontamination at the site from which the clones weresampled, i.e. clones collected from a copper smelter sitegrew better in Cu-contaminated soil than clones from a Znsmelter site, and vice versa. Experiments comparing thegrowth of tree seedlings from trees in metal-polluted anduncontaminated areas failed to demonstrate the existence oftolerance traits (Dickinson et al., 1991), implying that theadaptation of individual mature plants may be the mostsignificant factor which determines the ability to survivepollution. Turner and Dickinson (1993) also showed this.Growth of sycamore seedlings collected at metal-contaminated and control sites, were compared in both metalamended nutrient solutions and reciprocal transplant experiments in soils. Even in contaminated soils, most seedlingssurvived for at least 3 years despite impaired growth,suggesting that some low level of innate tolerance mayexist, but that facultative tolerance, such as the observedproliferation of fine roots in uncontaminated zones of thesoil, is very important. Watmough and Dickinson (1995)summarised this as a strategy of avoiding toxicity, removingselection pressure and negating the necessity for the evolution of tolerance.Acclimation of trees to metal stress has been studiedusing various indices such as cell suspension cultures(Dickinson et al., 1992) and callus cultures (Watmoughand Dickinson, 1995), but seedling growth is the mostcommonly used index, despite their greater sensitivity toadverse conditions than mature trees. Turner and Dickinson(1993) questioned whether studies on seedlings accuratelyreflect the responses of older trees. Mature trees differ fromseedlings in a number of ways, including carbon allocation,canopy structure and the fraction of photosyntheticallyinactive tissue, which increases with age (Turner, 1994).Seedlings are much more sensitive to adverse conditions,le