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Basic Appl. Ecol. 4, 493506 (2003) Urban & Fischer Verlag http://www.urbanfischer.

de/journals/baecol

Basic and Applied Ecology

Species indicator values as an important tool in applied plant ecology a review


Martin Diekmann*
Department of Ecology and Evolutionary Biology, Bremen University, Bremen, Germany

Received October 16, 2002 Accepted December 12, 2002

Abstract
Species indicator values, especially those defined by Ellenberg, have been used widely in applied plant ecology, forestry and agriculture. In spite of being criticised by many, there is a growing interest in using them also outside central Europe in order to analyse trends of change in the vegetation and their underlying environmental variables. Various aspects of indicator values are reviewed: their main features, the most important applications (notably the use of weighted site averages), problems and pitfalls of indicator analyses, the relationship between weighted site averages and measurements as well as their extension to other regions. Some aspects are illustrated using data sets of forest plots from S Sweden. Provided that the limitations of indicator values are recognised, these have a high reliability and can complement or, in some cases, replace measurements to determine the values of environmental variables and to monitor their change. Zeigerwerte, besonders die von Ellenberg vorgeschlagenen Zahlen, haben in der Pflanzenkologie, Forst- und Landwirtschaft eine breite Verwendung gefunden. Obwohl viele Wissenschaftler Zeigerwerten kritisch gegenberstehen, werden sie in zunehmendem Mae auch auerhalb Mitteleuropas benutzt, um Vernderungen der Vegetation und der sie bedingenden Umweltfaktoren zu analysieren. Verschiedene Aspekte von Zeigerwerten werden errtert: ihre wichtigsten Merkmale und Anwendungen (insbesondere die Verwendung mittlerer Zeigerwerte), Probleme und Fehlerquellen, die Beziehung zwischen mittleren Zeigerwerten und Messwerten sowie die berprfung und Kalibrierung in Regionen auerhalb Mitteleuropas. Einige dieser Aspekte werden anhand von Datenstzen von Wldern Sd-Schwedens illustriert. Zeigerwerte haben, wenn ihre Begrenzungen bercksichtigt werden, eine hohe Zuverlssigkeit und knnen im Hinblick auf das Monitoring von Umweltvernderungen Messungen ergnzen oder in manchen Fllen sogar ersetzen. Key words: Calibration Ellenbergs indicator values environmental change measurements response curve species optimum weighted average

Introduction
Biological indication can be defined as making use of the specific reactions of organisms to their environment. Farmers have used plants as bio-indicators for thousands of years. Since long also scientists have

made the observation that many plants rather precisely reflect the values of environmental factors. Bio-indicators thus make visible what is not immediately perceptible. Among the main advantages of using plants as bio-indicators instead of conducting measurements are (Zonneveld 1983): (1) Plants represent integrated

*Corresponding author: Martin Diekmann, Department of Ecology and Evolutionary Biology, Bremen University, FB 2, Leobener Strae, D-28359 Bremen, Germany, Phone: +49-421-2183670, Fax: +49-421-2187052, E-mail: mdiekman@uni-bremen.de

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expressions of the values of environmental variables that may strongly fluctuate in time and space, and that therefore cannot be estimated by single measurements. (2) Measurements rely on technical equipment and, consequently, may often need more time and financial effort than simple floristic observations. (3) With no old measurements being available, bio-indicators are indispensable, allowing us to assess the dimension of environmental change. There is general agreement among ecologists that most plants in one way or the other may serve as bioindicators; the quantification of this indication, however, is much disputed. Most controversial are the socalled indicator values reflecting the realised optima of species expressed as ordinal numbers. The first one to develop a quantitative indicator system for vascular plants was the German ecologist Heinz Ellenberg, who, based on preliminary studies from the early 50ies (e.g. Ellenberg 1950), published lists of indicator values (Ellenberg 1974) for most species occurring in western central Europe. The latest edition also includes numbers for bryophytes and lichens (Ellenberg et al. 1992). Alternative lists of indicator values were, for example, proposed for Switzerland (Landolt 1977). Indicator values, especially those developed by Ellenberg, have been used widely by plant ecologists, mainly in central Europe (see Ellenberg et al. 1992; among the more recent publications, e.g. Py sek & Py sek 1995, Koerner et al. 1997, Wamelink et al. 2002), but also in northern Europe (Persson 1981, Diekmann 1994, 1996, Sstad & Moen 1995, Hannerz & Hnell 1997, Brunet et al. 1997, Lawesson 2000), Great Britain (Thompson et al. 1993, Mountford & Chapman 1993, Hill & Carey 1997, Hill et al. 1999, 2000), eastern Europe (Prieditis 1997, Ruprecht & Botta-Dukat 2000) and the Mediterranean region (Celesti Grapow et al. 1993, Bucci & Borghetti 1997). Despite their common application indicator values have been criticised on the following grounds: (1) They are not systematically derived from measurements, but mainly inferred from field experience of plant ecologists, i.e. observations of species occurrences at different sites. They are thus rather subjective, and any data set bias may lead to wrong estimates of habitat quality (kland 1990). (2) The application of indicator values implies an element of circularity: first, the values are derived from the floristic composition of sites for which the values of environmental factors are known or estimated; then, habitat quality is in turn estimated by means of indicator values. (3) Species may shift in their responses, either across geographical gradients (Diekmann & Lawesson 1999) or during their life cycle (Parrish & Bazzaz 1985).

(4) Using indicator values may prevent us from conducting measurements. Nevertheless, indicator values enjoy an unbroken popularity, simply because they appear to reflect habitat quality well in many situations (see below). The pros and cons of indicator values were listed by Dierschke (1994). This paper will review some of their main features and discuss the above points of criticism. It focuses on Ellenbergs indicator values for those four environmental factors that are of particular interest to ecologists when site conditions are to be estimated: light (L), soil moisture (M), soil reaction/pH (R) and soil nitrogen (N).

Features of indicator species


Species response curves It has often been hypothesised (and occasionally shown) that the abundances of species along environmental gradients approximate bell-shaped curves with single peaks (the optima or modes), resembling Gaussian distribution curves (Gauch 1982). Species behaving in this way would be suitable bio-indicators, but it is now recognised that the model is an oversimplification and hardly applicable but to a few taxa (kland 1990). However, to serve as an indicator species it is basically sufficient to show either a unimodal or monotonically increasing or decreasing response along a gradient. The majority of species appear to have unimodal responses (kland 1990, Lawesson & Oksanen 2002), provided that the ecological variable in question is an important (dominant) one, that the -diversity of the data set is large enough, and that the distribution of sample plots over the environmental gradient is not too uneven (kland 1986). In a model data set comprising 467 sample plots of deciduous forest on mineral soil from S Sweden (for more details, see Diekmann & Falkengren-Grerup 1998), about 72% of all species showed a significant unimodal or monotone response along the pH gradient. Most species that could not be fitted by Gaussian regression were either rare or showed a bimodal behaviour such as Melica nutans. The species optima estimated from the Gaussian response models were highly correlated with the indicator values for pH (R2 = 0.480, P < 0.001, n = 110). These results correspond well to the study by Ejrns (2000) who found 76% of all species in dry grasslands of Denmark to have significant linear, monotone or unimodal responses to pH. The large majority of Danish woodland species studied by Lawesson & Oksanen (2002) also showed unimodal or skewed unimodal responses. Good indicator species should, apart from having de-

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fined optima, also show small Gaussian tolerances t, or, more generally, narrow amplitudes around the optimum (see ter Braak & Looman 1986, Lawesson & Oksanen 2002). Practical considerations Low abundance and limited geographical distribution considerably reduce a species suitability as bio-indicator. Of course, a low abundance may be the result of exceptional habitat conditions to which the species is confined; then, its rarity simply reflects the rarity of a particular environment. However, often rarity is caused by other factors than habitat quality alone, such as poor dispersal capacity or low germination rate. The absence of a species thus is a less reliable indicator than its presence! The best indicators should neither be too rare nor too common. Another crucial practical point is whether the species is easy to identify or not. Systematically complex species groups (such as the Rubus fruticosus aggregate, cf. Weber 1992) are therefore less suitable as indicators.

Ecological applications of indicator values


Weighted averages Many species together allow a more precise and reliable indication than a single species, because the overlap of ecological tolerances of many species is smaller than the ecological amplitude of a single species. Therefore species inventories (relevs, quadrats) form the basis of most applications of indicator values. Let rij be the response of species i in sample plot j, and xi the indicator value of species i. Then the easiest way to estimate the value of an environmental variable is to calculate a weighted average of all values of those species present in the plot (absent species and those lacking indicator values are disregarded): n Weighted average =
i=1

n
i=1

(rij * xi) / rij

In the large majority of studies applying indicator values the above formula was used. Weighted averages are surrogates of the values of environmental variables and can be translated into the real values if the relationship between these averages and measured values is known. The estimation of site conditions from the species assemblage at a site is a form of calibration (kland 1990). The most common application of indicator values is the comparison of weighted averages (or their means) between different plant community types. The sites can

be small sample plots (such as relevs) or large grid squares (e.g. Godefroid 2001). A list of mean averages for all phytosociological alliances and associations of S Germany was published by Bcker et al. (1983). Weighted averages have served to, for example, analyse floristic data by means of ordination (Persson 1981, Diekmann 1994, Bucci & Borghetti 1997, Ewald 1999a, Wohlgemuth et al. 1999, van Dobben et al. 1999, van Rossum et al. 1999, Brunet et al. 2000), compare the ecological conditions between large towns and their surroundings (Durwen et al. 1984a), characterise the flora of different grid squares (Durwen et al. 1984b), compile the size of the regional species pool for various plant communities (Prtel et al. 1996, Dupr 2000), predict the occurrence of vascular plants (Dupr & Diekmann 1998) or lichens (Nimis & Martellos 2002), characterise the ecology of species found in seed banks (Bossuyt & Hermy 2001), assess the humus form of forests (Mller 1997) or define the environment for butterflies (Oostermeijer & van Swaay 1998). Weighted averages can further be used to: Determine the ecological behaviour of species by fitting their response curves to sites with different weighted averages (for similar approaches, see Reif et al. 1985, Schmidt 2000). This indirect determination of species responses has been applied occasionally (Diekmann 1996) and can be used to calibrate the original indicator values (see below). Analyse floristic changes by comparing old and new vegetation samples in permanent or semi-permanent plots. If we record a change in weighted averages, we may assume that this change results from an environmental change. In this way indicator values have served to monitor the effects of drainage (ter Braak & Wiertz 1994) and re-wetting (Oomes et al. 1996), atmospheric pollution by acidifying substances and nitrogen (Kuhn et al. 1987, Rost-Siebert & Jahn 1988, Brger 1991, Rodenkirchen 1992, Thimonier et al. 1992, 1994, Diekmann & Dupr 1997, Diekmann et al. 1999, van Dobben et al. 1999), eutrophication of wetlands (Ruthsatz 1998), forest management or succession (Persson 1980, Brunet et al. 1997), primary succession on islands (Rydin & Borgegrd 1991), etc. Interpret spatial side-by-side patterns by arranging them into temporal sequences. For example, geographical differences in weighted averages between regions with different nitrogen deposition levels can be interpreted as effects of a temporal change (Brkenhielm & Qinghong 1995, Diekmann et al. 1999). Soil acidity patterns around trees in forests are likely to be caused by acid rain and subsequent stem flow of acid water (Jochheim 1985, Wittig et al. 1985). Reconstruct historical site conditions by calculating weighted averages on the basis of former species assemblages from, for example, lake sediments. Exam-

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ples of such palaeo-ecological studies include the use of diatom algae for the reconstruction of lake acidification (Flower 1986, ter Braak & van Dam 1989, Birks et al. 1990) and the use of bryophytes for the analysis of changes in the environment of the LateGlacial (Jonsgard & Birks 1995). An application not depending on the calculation of weighted averages is the compilation of indicator spectra (for example, see Fig. 1a), i.e. histograms showing the frequency distribution of indicator values in single sites, communities or whole floras (Durwen et al. 1984a, Durwen & von Ruville 1984, Ellenberg 1992, Dierschke 1994). By plotting the proportion of threatened species in different indicator value classes, Ellenberg (1983) demonstrated that the highest share of endangered taxa was found among species with high light and low nitrogen scores that are confined to open, infertile sites such as calcareous grasslands. Also environmental change can be deduced from comparing indicator spectra between two points in time (Dierschke & Wittig 1991). How to calculate weighted averages? It has been discussed repeatedly that applying strictly mathematical criteria the calculation of weighted averages of Ellenberg indicator values is not appropriate, considering the ordinal nature of the values. Median indicator values were proposed as a statistically more sound alternative (Mller 1987, 1992, Kowarik & Seidling 1989). Yet, the majority of plant ecologists calculate weighted averages because they appear to work well. Mean and median values usually do not differ much, except in some species-poor community types. If they do, an indicator value spectrum may reveal what the problem is. Of course, weighted averages do not always properly reflect the current environmental conditions (see below), but then also the median is not reliable. According to ter Braak & Gremmen (1987) the shapes of the species response curves are far more important than the ordinal character of the values. When calculating weighted averages another choice has to be made: should the responses of species (rij) be entered as presence/absence (qualitative) data or, if available, as abundance (quantitative) data? (for detailed discussions of this problem, see Bcker et al. 1983, Kowarik & Seidling 1989, Diekmann 1995) Most researchers have preferred qualitative data, reasoning that a species abundance is not only dependent on environmental site conditions, but also on its specific growth form. Clonal species often occur in large populations, whereas other species usually grow solitary; both, however, may have the same indicative value. In general, the choice of either qualitative or quantitative data may depend on:

The habitat type. In species-rich vegetation types such as deciduous forests and meadows, both approaches give similar results (usually differing less than 0.2 units; Diekmann 1995, Kowarik & Seidling 1989). In species-poor habitats and when single species attain dominance as in Phragmites reeds, the differences are larger, and abundance data may give more reliable results (Diekmann 1995, Ellenberg 1992). The environmental variable. The light climate in forests, for example, may be better reflected by species abundances, as true forest species usually attain higher cover than accidentally occurring species of more open habitats (Diekmann 1995). The type of ecological study. In monitoring studies based on the comparison of historical and recent plots, abundance data sometimes should be avoided. First, if the sampling at the two occasions was carried

Fig. 1. Frequency distribution of indicator values for reaction (indicator spectrum) of species encountered in two forest sites on land, S Sweden. a) Elmash forest (weighted average: 6.8); b) pine forest on limestone (weighted average: 4.9).

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out by different persons, inter-observer differences in cover estimation may distort the analysis (Sykes et al. 1983). Second, there is a marked fluctuation in species abundance between years caused by annual changes in weather conditions, which may be observed also in rather stable community types such as forests (Brunet & Tyler 2000, Caroe et al. 2000). On the other hand, an environmental change may first manifest itself in altered species abundances and not in appearances or disappearances. The conclusion that can be drawn from the presence-absence vs. abundance debate is that the results with few exceptions do not differ much. Multi-layered vegetation types such as forests create specific problems (see discussion in Kowarik & Seidling 1989): How should the weighted averages be calculated by using all species in a site, or by considering only those in the field layer? Trees and, to a lesser extent, shrubs are often planted; partly, they root in deeper soil layers and exploit another environment than herbaceous species. Woody species may also show ontogenetic shifts in their responses to the environment during their early life stages (Kowarik & Seidling 1989, Diekmann 1994). Species of the bottom layer, on the other hand, are often valuable indicators (e.g. Stetzka 1994), especially in habitats with a high share of bryophytes or lichens, for example mires and sandy heaths. Indicator values of bryophytes have rarely been tested in vegetation types dominated by vascular plants (but see Diekmann 1995, Schaffers & Sykora 2000). Pitfalls Weighted averages may, in certain circumstances, be unreliable, and one has to be aware when this might be the case. The following problems should be kept in mind: Sample plots should be as homogeneous as possible, otherwise the results may be misleading or even nonsense. A mire plot containing both hummocks and hollows will have a weighted average for moisture that does not reflect the water level of any part of the plot except for a small transitional zone between the two mire elements. However, sometimes heterogeneity is not so obvious: in Fennoscandian pine forests with an acid humus layer on limestone bedrock there is often a mixture of basiphilous and acidicolous species. Whereas an indicator value spectrum for pH demonstrates this well, a weighted average does not (Fig. 1b). If the environmental gradient is short, weighted averages will not differ much between plots and be more affected by random spatial fluctuation in species composition than by any underlying gradient. The differences between weighted averages then have a limit-

ed or no ecological meaning. An example: 20 sample plots of 1 m2 each were placed along a transect in a deciduous forest on land, S Sweden, that appeared to be very homogeneous in respect to both topography and vegetation. Relative light intensity and the weighted averages for light were unrelated both to plot position and to each other (Fig. 2), i.e. it seems highly unlikely that the variation in weighted averages reflects actual environmental differences between the plots. Note, however, that the coefficient of variation for the light measurements (0.13) was larger than that for the weighted averages (0.05). Within-site variance of indicator values was also studied by Ewald (1999b). In areas strongly affected by human impact, new habitats are created, changing the competitive relationships between species. Some species may extend their realised responses due to competitive release. This applies, for example, to Poa palustris in ruderal communities of large cities (Kowarik & Seidling 1989). In heavily grazed or trampled communities the vegetation does not primarily indicate specific soil conditions, but mainly reflects the disturbance regime. In such cases indicator values should first be calibrated (Briemle 1997) or not be used at all. If there is a sudden environmental shift, species changes often limp behind. A drained alder swamp forest will only slowly develop a vegetation typical for more mesic forest sites, because many swamp species may survive for decades even in the new site conditions, and because new species need time to disperse and establish. Dzwonko (2001) showed that indicator values were less good predictors of habitat conditions in recent than in ancient forests.

Fig. 2. Fluctuation in light across a transect of 20 sample plots of 1 m2 each in a deciduous forest on land, S Sweden. Light was measured as relative light intensity (proportion of photosynthetically active radiation in the forest interior to the open, in percent) or estimated as weighted averages of the indicator values for light. Both variables were unrelated to plot position (R2 = 0.090, P = 0.197, n = 20 and R2 = 0.124, P = 0.127, respectively) and to each other (R2 = 0.085, P = 0.211).

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The statistical distributions of indicator values for different variables are not independent of each other, because some community types with particular combinations of environmental conditions are more species-rich than others (Bcker et al. 1983). For example, species with high R and low N values are overrepresented in central Europe due to the high species richness of infertile, calcareous grasslands in this region; in contrast, there are hardly any species with both low L and low N values, because dark, nutrientpoor forests are species-poor (Dupr et al. 2002). For example, pH and light in forests often are negatively correlated (for the weighted averages for R and L in the model data set: r = 0.539, P < 0.001, n = 467). Let us assume a deciduous forest exposed to strong atmospheric deposition suffering from both acidification and eutrophication. When comparing the weighted averages for R between old and new data, acidification is not always indicated, because natural forest succession and eutrophication may lead to a denser tree canopy, outshading many acido-tolerant, but light-demanding species with low R values (cf. BrgerArndt 1994). Finally, it must be remembered that weighted averages do not always reflect current environmental conditions at a site, but may indicate conditions of critical periods for the plants. Weighted averages for light in deciduous forests are low, because only shadetolerant species with low indicator values for light survive in the dark forest interior in summer. Of course, these averages are useless as light predictors in spring. Some wetland habitats such as shallow depressions can periodically dry out in summer which is not reflected by the high averages for soil moisture. The latter was taken into account by the Ellenberg system in adding special signs to the indicator values for moisture for those species that are often found on soils with a highly fluctuating water table or on periodically inundated sites.

is that the correlation between weighted averages and measured values may not always be linear and that some values must be transformed (e.g. Schaffers & Sykora 2000), which is crucial if the regression line is to be used for predicting the actual values of environmental variables. Wamelink et al. (2002) showed that the lines of the regressions of weighted averages for R on pH and of weighted averages for moisture on groundwater level differed significantly between phytosociological classes, i.e. the values of the averages partly depend on the type of vegetation studied. This means that (a) the weighted averages may be biased, (b) one cannot calculate weighted averages and then predict the environmental value at a site without knowing the exact regression line for the vegetation in question, and (c) one should not compare weighted averages between much different vegetation types. Soil pH Soil pH is easier to measure than most other variables and does not vary as much over the year as soil water or light. Figure 3a shows a highly significant linear correlation between indicated and measured values. Given the regression equation the soil pH at each site can be deduced from the corresponding weighted averages. A close relationship between indicated and measured pH was found in many studies (Table 1). Schaffers & Sykora (2000) showed, however, that this relationship is usually curvilinear, i.e. at pH (KCl/CaCl) >5.0 the weighted averages do not change much with increasing pH (also supported by Fig. 3a). In other words, using such averages as a surrogate for soil pH may be inappropriate when high-pH soils are studied. This is probably caused by the narrow pH tolerances of species with high pH optima (Schaffers & Sykora 2000). However, Wamelink et al. (2002) in a large data set including more than 3000 plots from The Netherlands found a close relationship between indicated and measured values of pH without any evidence for non-linearity. Soil pH is no plant nutrient per se, but affects the general nutrient status and the available amounts of other elements in the soil. Some of these are much better correlated to the weighted averages for R than pH, notably the amount or saturation of exchangeable Ca2+, total calcium content and base saturation (Table 1). Schaffers & Sykora (2000) in an extensive review on this matter proposed to better refer to Ellenberg indicator values for reaction as calcium values. Soil moisture Correlations of weighted averages for soil moisture with measured values are surprisingly rare. Basically

Indicator values and measurements


To know how reliable indicator values and their averages are they should be related to measured values. This is not as easy as it seems. If the correlation between weighted averages and measured values is close, we conclude that the indicator values for the variable in question work well. If the correlation is weak, we may instead conclude that the values perform poorly, but we may equally well deduce that the environmental parameter measured is the wrong one. In other words, it is not clear what variable is indicated best, because species occurrences are integrated responses related to more than one parameter. Another problem

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three parameters were used to assess the reliability of the indicator values for moisture: groundwater level, moisture content and pF-value. All have proved to correlate well with weighted averages, unless the gradient was too short (Table 1). Ertsen et al. (1998) showed that soil texture is important for the relationship between vegetation and groundwater level. Therefore Schaffers & Sykora (2000) expected moisture content and pF values to perform better, but so far there is little evidence. The authors as well as Diekmann (1995) emphasised that the lowest values of the measured parameters give slightly better correlations with weighted averages than average values, indicating that the plants susceptibility to periodical or occasional drought is more important to their long-term performance in the field than their tolerance of occasional periods of high soil moisture (Schaffers & Sykora 2000). The correlation between moisture parameters and indicator values is in greater detail discussed by Ellenberg (1992).

Soil nitrogen From an applied point of view, the indication of soil nitrogen appears to be particularly useful, because nitrogen is the most important macro-nutrient in terrestrial ecosystems, and because it appears to be more difficult to measure than soil pH or moisture. Three types of measured parameters can be distinguished: actual measurements of nitrogen (content, mineralisation, C/N ratio), measurements of other soil nutrients (such as K or P) and vegetation-derived parameters (biomass, N concentration of leaves; Table 1). There is no clear evidence which factor is indicated best by the indicator values for nitrogen, but the following can be generalised: Total amounts or mineralisation rates of N are weakly indicated by weighted averages, as they are less important than the rates of either NO3 or NH4+ (Fig. 3b). Other nutrients (P, K) are equally well indicated by weighted averages as the amounts or mineralisation rates of NO3 or NH4+. Vegetation-derived parameters, especially biomass, are best correlated with weighted averages for nitrogen, indicating that the nitrogen values do not just reflect the species responses to this variable, but effectively integrate the supply of several nutrients and other parameters related to the potential of the sites to produce biomass. In fact, the results support the suggestion to better refer to the nitrogen values as productivity values (Ellenberg 1992, Hill & Carey 1997, Schaffers & Sykora 2000). An interesting result reported by Schaffers & Sykora (2000) was that some of the relationships between indicated and measured parameters tended to have a sigmoid shape. This is probably not a coincidence, because also in the Swedish model data set, there was an S-curved relation between the weighted averages for nitrogen and percent mineralised NO3 in the soil. This logistic function is likely to be caused by the sudden shift from no nitrification to predominantly nitrification at a certain pH level (see also Diekmann et al. 1999). Light Although light is one of the most important environmental variables for plants, measurements of light and even more so their correlation with weighted averages for light are scarce (Table 1). The reliability of Ellenberg indicator values for light compared to the above variables is therefore difficult to assess. The most promising way to measure the light climate in plant communities appears to be the determination of relative light intensity (Diekmann 1995). In forests

Fig. 3. Relationship between weighted averages of indicator values (weighted by cover-abundance) and measurements of soil variables using the model data set of 467 deciduous forest sites from S Sweden. a) Weighted averages for reaction (R) vs. pH (KCl); b) weighted averages for nitrogen (N) vs. total mineralisation rate of nitrogen (N-tot).

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Table 1. Measured parameters that were correlated with the weighted averages of plant species indicator values for soil reaction, moisture, nitrogen and light. In the correlation column it is assessed how close the different (partly transformed) parameters were related to the particular average as reported in the literature (++, close positive correlation; +, positive correlation; , weak or no correlation). Parameter Soil reaction pH (H2O), pH (KCl) or pH (CaCl2) Correlation + (Persson 1980, Degorski 1982, Lawesson & Mark 2000, Wamelink et al. 2002, Lawesson, unpubl. results) + (Rodenkirchen 1982) + (Ellenberg 1992, Herzberger & Karrer 1992, Seidling & Rohner 1993, Diekmann 1995, Hill & Carey 1997, Ertsen et al. 1998, Schaffers & Sykora 2000, Diekmann, unpubl. results) ++ (Degorski 1982, Seidling & Rohner 1993, Schaffers & Sykora 2000) ++ (Seidling & Rohner 1993) ++ (Schaffers & Sykora 2000) ++ (Degorski 1982, Schaffers & Sykora 2000, Lawesson, unpubl. results) ++ (Schaffers & Sykora 2000) ++ + ++ ++ + + ++ ++ + + + + + + + + + + + + + + ++ + + + + + ++ ++ ++ + (Schaffers & Sykora 2000) (Ertsen et al. 1998, Wamelink et al. 2002) (Schaffers & Sykora 2000) (Schaffers & Sykora 2000) (Schaffers & Sykora 2000) (Diekmann 1995) (Lawesson, unpubl. results) (Schaffers & Sykora 2000) (Schaffers & Sykora 2000) (Schaffers & Sykora 2000) (Schaffers & Sykora 2000) (Ellenberg 1992) (Lawesson, unpubl. results) (Vevle & Aase 1980, Schaffers & Sykora 2000) (Hill & Carey 1997, Ertsen et al. 1998) (Hill & Carey 1997) (Diekmann, unpubl. results) (Ellenberg 1992) (Schaffers & Sykora 2000) (Diekmann, unpubl. results) (Schaffers & Sykora 2000) (Lawesson, unpubl. results) (Schaffers & Sykora 2000) (Schaffers & Sykora 2000) (Rodenkirchen 1982, Ellenberg 1992) (Schaffers & Sykora 2000, Diekmann, unpubl. results) (Diekmann, unpubl. results) (Diekmann, unpubl. results) (Diekmann, unpubl. results) (Hill & Carey 1997, Ertsen et al. 1998) (Ertsen et al. 1998, Schaffers & Sykora 2000) (Lawesson, unpubl. results) (Ertsen et al. 1998) (Hill & Carey 1997, Schaffers & Sykora 2000) (Lawesson, unpubl. results) (Lawesson, unpubl. results) (Boller-Elmer 1977, Briemle 1986) (Melman et al. 1988, Hill & Carey 1997, Ertsen et al. 1998, Schaffers & Sykora 2000) (Ertsen et al. 1998, Schaffers & Sykora 2000) (Thompson et al. 1993) (Schaffers & Sykora 2000) Remarks

only low-pH sites non-linear

Base saturation/S-value Al/Ca-ratio Ca2+ saturation Ca2+ amount Total calcium Soil moisture Average annual groundwater Mean spring groundwater Average highest groundwater Average lowest groundwater Soil moisture content Aver. annual moisture content Aver. lowest moisture content Aver. highest moisture content Highest pF values Number of days with low pF Mean soil depth Soil nitrogen Total N Total C or organic matter C/N ratio Mineral N (NO3 + NH4+) Mineral NO3 % NO3 Total mineralisation rate Ammonification rate Nitrification rate Nitrification ratio Total P Available PO43 Total K Available/exchangeable K+ Exchangeable Mg Biomass/standing crop N accumulation of plants Foliar N concentration Tissue N concentration Light Relative light intensity

gradient short slightly non-linear

weak at low C/N weak at high C/N slightly sigmoid

(Rodenkirchen 1982) + (Diekmann 1995)

few measurements

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canopy cover has occasionally been used as an indirect measure of light intensity (Brunet et al. 2000). As for the soil variables, the goodness of correlation between indicated and measured light values is highly dependent on the length of the gradient considered. If the light gradient is short (as in Fig. 2 showing fluctuation but no systematic change), the relation will be weak. If, on the other hand, the gradient is large, for example, extending from open grassland to dark forest, the relation will be close, even if the light values were not very accurate. In general, the performance of indicator is probably best assessed by using data sets including moderately long gradients.

Calibration
General Ellenbergs indicator values were created and are primarily valid for central Europe, more precisely western Germany. How appropriate is the system outside the region for which is was defined? Although the indicator values have been used widely (and successfully) across many areas, it is likely that they become less reliable when moving away from central Europe, because the climatic conditions and floras become increasingly different. Therefore one of the most important tasks has been to extend and calibrate the values to new regions by correcting for regional deviations and by assigning new values to local species. Attempts to calibrate indicator values to new regions have been based on simple observations of single species (Kowarik & Seidling 1989, Herzberger & Karrer 1992, Gustafsson 1994), large vegetation data sets or measurements of environmental variables. Calibration with large vegetation data sets Extensions of indicator values on the basis of vegetation data proceed from the assumption that the Ellenberg system as such is definite or true, but needs to be refined for a minority of species. A simple approach to calibrating indicator values was introduced by Zlyomi (1989) and also applied by Diekmann (1995). The basic idea is to, first, calculate weighted averages of all sites in a data set and, then, determine the ecological responses of species by calculating their constancy in sites with different weighted averages. If the optimum of a response (curve) deviates from the original indicator value, a new value can be assigned (if certain conditions are met, such as a minimum frequency of the species; cf. Diekmann 1995). Ter Braak & Gremmen (1987) tested the internal consistency of moisture values by means of weighted averaging and Gaussian logit regression and concluded that about 20% of the

tested species deviated in their responses from the original indicator values. A somewhat different method was proposed by van der Maarel (1993) who assigned new scores on the basis of average values for sociological-ecological groups. A more advanced technique was introduced by Hill et al. (2000) who re-predicted indicator values for Britain by an algorithm of two-way weighted averaging, followed by local regression, based on a large data set of more than 14,000 quadrats. The authors pointed at many discrepancies between original and re-predicted values and published a list including 1791 taxa for which extended values are given (Hill et al. 1999). This approach basically allows to assign improved scores to all species, irrespective of their tolerances relative to the environmental variables. Species tolerances were calculated by, for example, Diekmann (1995), ter Braak & Gremmen (1987) and Roy et al. (2000), offering a possibility to identify wide-amplitude species that may be excluded from the analysis or calibration. In conclusion, it must be remembered that it is impossible to improve the values in a statistically sound way on the basis of floristic data only (ter Braak & Gremmen 1987). Calibration with measured environmental variables A statistically better and perhaps more convincing way to improve indicator values is to relate them to measurements, although this seems impossible to achieve for all species of a flora and all variables. The basic idea is to determine where along the environmental gradient the species have their optima, to order the species according to these optima and to re-assign new values if the species original indicator value appear to be wrong (see, e.g. Kunzmann et al. 1990). In general, the approach of identifying response curves of species along a gradient by means of weighted averaging or Gaussian logistic regression is suitable to identify species optima and amplitudes (ter Braak & Looman 1986, Storm 1996, Wierda et al. 1997). If tolerance values are known, it is possible to distinguish more objectively between good indicator species and indifferent species (see also ter Braak & Gremmen 1987). In a study of Swedish deciduous forests, Diekmann & FalkengrenGrerup (1998) calculated weighted averages for nitrate and ammonium based on soil nitrogen mineralisation rates and combined these in linear models to construct functional nitrogen indices for species. In general these were closely related to Ellenbergs nitrogen values, but for some species the indices disagreed. Measurements of plant performance in response to different levels of ammonium and nitrate were also used by Wamelink et al. (1998) to calibrate the indicator values for nitrogen. The authors used a different ap-

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Diekmann

proach in first constructing species optima which then were regressed on the nitrogen values to identify deviating species. A related approach was used by Lawesson & Mark (2000) for the calibration of reaction values in Denmark. Schaffers & Sykora (2000) carried out a sophisticated analysis by calculating species optima relative to the three edaphic variables for different plant communities in The Netherlands. The authors realised the problem of uneven sampling distribution (see also ter Braak & Looman 1986, Diekmann 1995) and introduced an extra weighting factor. The species optima were highly positively correlated to Ellenberg values, but the regression of new on old values justified the adjustment of some of the original indicator values. Species adjustments All attempts to improve Ellenberg indicator values or to extend them to other regions have resulted in new or adjusted values. The larger the deviation between original and new value is, the more likely it becomes that this difference is not only caused by a sampling bias (for a discussion, see Hill et al. 2000), but a real shift in species response. The number of deviations depends on the approach used for calibration: if the procedure is based on sample plots from a particular type of vegetation (for example, forests, see Diekmann & Falkengren-Grerup 1998), the differences are likely to be more and larger, but only applicable to the vegetation type in question. Hill et al. (2000) in Britain

found the original values for light and moisture to work comparatively well, whereas many improvements had to be made for the reaction and nitrogen values (a difference of 2 or more for about 14% and 13% of the species). Table 2 lists a number of publications from different European regions that include calibrations of Ellenberg values; it also shows how these are related to each other. Except in one case where only six species were in common, the adjustments were significantly correlated between regions. This means that the direction of change generally was the same: for example, the improved soil reaction values for Galium verum were lower than the original values both in Britain (Hill et al. 1999), Denmark (Lawesson & Mark 2000) and Sweden (Diekmann, unpubl. results). The correlation of improvements was particularly high between Britain and The Netherlands which are climatically quite similar.

Conclusions
In response to the criticism that is often raised against indicator values (see above), some conclusions may be drawn: (1) Indicator values are subjective, but if they coincide with the optima of species response curves, they have an objective biological meaning. However, any bias in the data set used for the estimation of indicator

Table 2. Comparison of calibrations of species indicator values for the variables soil moisture (M), reaction/pH (R) and nitrogen (N) as reported in the literature. The calibrated data for the different regions were entered as positive (new value > original Ellenberg value) or negative numbers (new value < original Ellenberg value) and correlated to each other. Pearson correlation coefficient and significance probabilities (***, P < 0.001; **, P < 0.01; *, P < 0.05; ns, P > 0.05) are given above the diagonal, the number of species considered in the correlation below the diagonal. The higher the correlation coefficients are, the better coincide the two calibrations in question. ( = not enough data available, the calibrations considered different variables.) Lawesson, unpubl. results, Faroe Islands Lawesson, unpubl. results, Faroe Islands Hill et al. (1999), Britain Hill et al. (1999), Britain M: 0.442 *** R: 0.594 *** N: 0.601 *** Schaffers & Sykora (2000), The Netherlands Lawesson & Mark (2000), Denmark Diekmann, unpubl. data, Sweden R: 0.719 ** Diekmann & Falkengren-Grerup (1998), Sweden N: 0.369 ns

M: 70 R: 48 N: 54

M: 0.749 ** R: 0.928 *** N: 0.885 *

R: 0.755 ***

R: 0.344 ***

N: 0.435 ***

Schaffers & Sykora (2000), The Netherlands Lawesson & Mark (2000), Denmark Diekmann, unpubl. results Diekmann & Falkengren-Greup (1998), Sweden

M: 11 R: 15 N: 6 R: 31 R: 161 N: 66

R: 14 N: 6

R: 18

R: 0.779 ***

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values (regarding, for example, the distribution of measured values and the spectrum of community types) will give a wrong estimate and distort the analysis. (2) If indicator values are estimated or calibrated on the basis of environmental measurements, circular reasoning is avoided. They are supported by the close correlation between weighted averages and measurements of various variables. (3) Shifts in species responses along climatic and geographical gradients should be met by calibrating the original values and extending the system to other regions. The indicative value of species may also differ between different vegetation types. (4) Whenever possible, measurements should be made and accompanied by indicator value analysis.
Acknowledgements. The author is grateful to Cecilia Dupr and Jonas E. Lawesson for valuable comments on an earlier draft of this review. Two anonymous reviewers helped to improve the paper.

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