BIOLOGICAL
CONSERVATION
Biological Conservation 120 (2004) 525–531
www.elsevier.com/locate/biocon
Conservation of Northern European plant diversity:
the correspondence with soil pH
€ Reier, Eva-Liis Tuvi
Meelis P€
artel *, Aveliina Helm, Nele Ingerpuu, Ulle
Institute of Botany and Ecology, University of Tartu, Lai 40, Tartu 51005, Estonia
Received 13 May 2003; received in revised form 23 March 2004; accepted 25 March 2004
Abstract
Effective biodiversity conservation requires an analysis of the existing reserve system. In temperate and boreal regions, plant
diversity has a strong positive association with soil pH. Consequently, in order to protect plant diversity effectively, a relatively large
proportion of protected areas should be on high pH soils. Since biodiversity data are never complete for all taxa, biodiversity
indicators, e.g., threatened species, should be used. We studied soil pH distributions in protected areas in Northern Europe and
tested whether soil pH requirement differs between threatened and non-threatened bryophyte and vascular plant species. As result,
the proportion of high pH soils in protected areas was significantly greater than the proportion of these soils in general. This ensures
that a large regional pool of plant species preferring high pH soils is relatively well protected. Threatened and non-threatened species
in Northern Europe did not differ in their soil pH requirements, but threatened species required a narrower soil pH range than nonthreatened species. Consequently, threatened species diversity can be used for indicating overall plant diversity.
Ó 2004 Elsevier Ltd. All rights reserved.
Keywords: Protected areas; Reserves; Soil acidity; Species richness; Threatened species
1. Introduction
Nature conservation has shifted from single species
protection to biodiversity maintenance (Simberloff,
1998). The principal method of biodiversity conservation is the creation and maintenance of a network of
protected areas (also called parks or reserves), where
negative human influence is considerably limited.
Mostly unproductive or proximal areas without economic importance, grand scenarios, and recreation sites
have historically been set aside for conservation (Pressey, 1994; Margules and Pressey, 2000). Historically,
nature conservation has developed more towards the
protection of animals (Darling, 1964), and especially
birds (Flasbarth, 2001). In contrast, the botanical aspect
has been the leading reason for creating nature reserves
in Sweden (G€
otmark and Nilsson, 1992). How effectively plant diversity is currently incorporated in the
*
Corresponding author. Tel.: +372-7-376234; fax: +372-7-376222.
E-mail address: [email protected] (M. P€artel).
0006-3207/$ - see front matter Ó 2004 Elsevier Ltd. All rights reserved.
doi:10.1016/j.biocon.2004.03.025
system of protected areas in a larger region, is not
generally known.
Several scientific methods for reserve selection have
been reviewed recently (Prendergast et al., 1999; Margules et al., 2002). One principal component of strategies
in systematic conservation planning is the evaluation of
existing reserves (Margules and Pressey, 2000). For example, reserves in the United States ‘‘sample’’ significantly more higher-elevation and unproductive land,
leaving a large proportion of biodiversity only weakly
protected (Scott et al., 2001). Often, however, highquality biodiversity data are lacking and surrogate data
have to be used, for example abiotic environmental data
(Ferrier, 2002).
In Europe, plant diversity is strongly positively related to soil pH (Grime, 1979; Grubb, 1987; Ewald,
2003). In a global-scale study, we have shown that the
soil pH/plant diversity relationship depends on soil type
in regional evolutionary centers (P€artel, 2002). If the
regional evolutionary center is located on low pH
soils (close to the equator), the soil pH/plant diversity
526
M. P€artel et al. / Biological Conservation 120 (2004) 525–531
relationship is mostly negative; if the regional evolutionary center is located on high pH soils (higher latitudes), the soil pH/plant diversity relationship is mostly
positive. Thus, the locally observed soil pH/plant diversity relationship is determined by differences in the
sizes of regional species pools for low and high pH soils
(P€
artel et al., 1996).
Knowing the differences in plant species pool sizes for
low and high pH soils in Europe, it would be desirable
that the areas with high pH soils are proportionally
more protected to maintain regional plant diversity effectively. In reality, there may be the opposite tendency,
since high pH soils are often extensively used for agriculture (Ramankutty et al., 2002), and reserves may
more often be on acid soils (bogs, forests on leached
soils, granite rock habitats). The lack of protection of
high pH soil areas would be a clear indication of a threat
to regional plant diversity.
Most of the soils at higher latitudes are acidic, leaving
few habitats for the relatively large pool of species preferring high pH soils (P€
artel, 2002). The lack of suitable
habitats may be one cause of species rarity. Anthropogenic acidification has been considered to be a serious
threat for many rare plants typical of intermediate pH
soils (Bobbink et al., 1998). Several studies have shown
that rare plant species are concentrated on high pH
soils, for example in the Sheffield region (Hodgson,
1986), Estonia (Kull et al., 2002), Swedish forests (Gustafsson, 1994), and grasslands of the Netherlands
(Roem and Berendse, 2000). An additional aspect is the
broadness of species’ soil pH requirement. According to
the work of Rabinowitz (1981), habitat specificity is one
criteria of rarity. For example, rare species had a narrow
ecological range in the floras of Sheffield (Hodgson,
1986) and Finland (Lahti et al., 1991).
Biodiversity is a relatively new indicator of nature
conservation value (Haila and Kouki, 1994). In contrast, presence of threatened species has been used in
reserve selection for a long time. Threatened species can
serve as indicators of overall diversity if they share
similar requirements with non-threatened species, e.g.,
they do not have higher soil pH requirements than nonthreatened species. Comparison of soil pH preferences
of threatened and non-threatened species using raw lists
of species gives information about the current trait
patterns, but, due to phylogenetical relationships
between species, it is biased to reveal causality. Grytnes
et al. (1999) showed that rare and common species of
Fennoscandia are not taxonomically equally distributed.
Moreover, species’ soil pH preference showed significant
phylogenetic conservatism: it depends on the legacy
from species’ ancestors, not only on species’ own adaptations (Prinzing et al., 2001). Causal relationships
between rarity and soil pH preference or its broadness
can be revealed correctly with methods which consider
species’ phylogenetical relations (Silvertown and Dodd,
1996; Eriksson and Jakobsson, 1998; Tofts and Silvertown, 2000; P€artel et al., 2001).
Our aims were to test for Northern Europe: (i) whether protected areas are more probably located on high
pH soils; (ii) whether threatened plant species have
higher soil pH requirements than non-threatened species
and (iii) whether threatened species have more restricted
soil pH preference than non-threatened species.
2. Methods
We limited our study to Northern Europe for several reasons. First, this area has the same postglacial
history: species colonized it after the smelting of land
ice. Second, the strength of the soil pH/plant diversity
relationship increases with latitude and is stronger in
Northern Europe than in southern parts (P€artel, 2002).
In addition, compared to Western and Central Europe
the human population density is lower and plant diversity relations to environmental factors are probably
less modified by direct human influence. Third, information about threatened species is available, since local Red Data Books cover all parts of Northern
Europe.
We used data from Denmark, Estonia, Finland,
Latvia, Lithuania, Norway and Sweden, and Russian
administrative districts (republic of Karelia, and regions
of St. Petersburg, Murmansk, Novgorod and Pskov),
hereafter all referred as countries. For each country, we
found the proportion of high pH soils from the global
0:5° 0:5° data set of soil pH properties for top 30 cm,
achieved as median of measurements in water:soil suspension of 1:1 to 1:5 (Batjes, 1997). High pH was determined for a 0:5° 0:5° area if it had soils with
pH > 5.5, corresponding to the generally accepted
boundary between acidic and non-acidic soils (P€
artel,
2002).
We extracted coordinates and areas for 1213 protected sites from the Nationally Designated Protected
Areas Database of the United Nations Environment
Programme and the World Conservation Monitoring
Centre (http://www.unep-wcmc.org, data acquired 01.
01.2003). For each protected site, we determined whether it is located on low or high pH soils using the global
data set (Fig. 1). For each country, we calculated how
large a proportion of protected sites are on high pH
soils.
Using country as a replicate, we used the dependent
sample t-test to check whether the proportion of protected areas on high pH soil is higher than the proportion of high pH soil in that particular country. The
countries had contrasting sizes and densities of protected areas, but using proportions eliminated these
differences. Establishment of protected sites is mostly a
local decision and a country is the best spatial limitation
M. P€artel et al. / Biological Conservation 120 (2004) 525–531
527
Using the same species pairs we also checked whether
threatened plant species were more likely to prefer
narrowly defined soil pH and non-threatened species a
wider range (i.e., are they indifferent regarding soil pH).
For bryophyte species, none of the species from the
pairs had indifferent status and the test was not used.
For vascular plants, we compiled 2 2 tables (threatened/non-threatened and specified pH preference/indifferent) and used one-tailed Fisher Exact Test.
Additionally, we performed Wilcoxon-matched pairs
test to check if this pattern is significant over all countries (comparing the number of indifferent species
among threatened and non-threatened taxa).
Since repeated tests were made with species pairs for
each country (n ¼ 12), Bonferroni correction was used
for P -levels and a result was considered significant at
P < 0:004.
for such nature conservation studies (Griffin, 1999;
Smith et al., 2003).
Threatened vascular plant species were determined
from the Red Data Books of each particular country:
Denmark (Stoltze and Pihl, 1998), Estonia (Lilleleht,
1998), Finland (Rassi et al., 2000), Karelia (Ivanter and
Kuznetsov, 1995), Latvia (Anon., 1997), Lithuania
(Anon., 2000), Murmansk (Andreev and Makarova,
1990), Norway (Lein, 1992), Novgorod (Tzvelev,
2000a), Pskov (Tzvelev, 2000a), St. Petersburg (Tzvelev,
2000b), Sweden (G€
ardenfors, 2000). For bryophytes,
European Red Data Book is available (ECCB, 1995),
but we extracted only those species which are distributed
in Northern Europe (S€
oderstr€
om et al., 1996).
Species’ soil pH preferences were taken from Ellenberg et al. (1991) reaction values. For each species, ordinal values 1–9 or indifferent (x) are provided.
Ellenberg data were elaborated mainly for Central Europe, but it has been shown to work well in Scandinavia
(Diekmann, 1995; Dupre and Diekmann, 1998), Estonia
(P€artel et al., 1996, 1999, 2001) and North-West Russia
(Maslov, 1989, 1990).
We compared species’ soil pH preferences among
congeneric threatened and non-threatened species pairs
to eliminate the effect of phylogeny (for methods, see
P€
artel et al., 2001). If there were more than one choice
for the congeneric species pairs, the species that was
alphabetically first in the flora of particular country was
selected. Wilcoxon-matched pairs test was used to check
whether threatened species require higher soil pH than
the non-threatened species. Species pairs containing
species with indifferent soil pH requirements were
omitted from this analysis.
3. Results
In Northern Europe, both high and low pH soils are
present (Fig. 1). In different countries, however, both the
overall proportion of high pH soils and the proportion
of high pH soils in protected areas vary from almost
zero to almost one (Fig. 2). Using countries as replicates,
significantly higher proportions of protected areas were
located on high pH soils compared to the overall proportion of high pH soils in a particular country (t ¼
2:3, df ¼ 11, P ¼ 0:044).
The number of congeneric species pairs for each
country ranged from 14 to 78 (Table 1). Soil pH preference did not differ between threatened and nonthreatened species in any country except for Norway,
where threatened species required higher pH than nonthreatened. This result, however, became nonsignificant
after Bonferroni correction.
1.0
Proportion of high pH soils
in protected areas
Fig. 1. Map of nature conservation areas in Northern Europe (dots).
Shaded areas show high pH soils (pH > 5.5).
St. Petersburg
Norway
Denmark
Estonia
0.8
Sweden
Pskov
0.6
1
:1
Lithuania
0.4
Murmansk
0.2
Latvia
Finland
Karelia
Novgorod
0.0
0.0
0.2
0.4
0.6
0.8
Proportion of high pH soils in country
1.0
Fig. 2. Proportion of high pH soils in Northern European countries
and their conservation areas. Significantly more protected areas are
located on high pH soils.
528
M. P€artel et al. / Biological Conservation 120 (2004) 525–531
Table 1
Mean Ellenberg reaction value for threatened and non-threatened species from congeneric species pairs for Northern European countries
Threatened
Non-threatened
n
T
Z
P
Vascular plants
Denmark
Estonia
Finland
Karelia
Latvia
Lithuania
Murmansk
Norway
Novgorod
Pskov
St. Petersburg
Sweden
6.09
6.31
6.31
6.35
5.83
6.48
6.00
6.60
6.71
6.32
5.72
6.37
6.14
6.55
5.96
5.74
6.22
6.62
5.36
5.69
6.42
6.38
6.03
6.31
35
58
48
34
59
50
14
35
24
34
29
78
177.0
266.5
253.5
101.0
453.5
389.5
42.5
106.5
74.5
212.5
112.5
1014.0
0.29
1.04
1.48
1.89
1.17
0.28
0.63
2.40
0.82
0.11
0.45
0.17
0.773
0.296
0.139
0.058
0.242
0.783
0.530
0.016
0.409
0.914
0.649
0.862
Bryophytes
4.92
4.90
50
385.0
0.34
0.737
Difference is tested by Wilcoxon-matched pairs test. None of these tests remains significant after Bonferroni correction.
Table 2
Counts of indifferent and specific Ellenberg reaction values among threatened and non-threatened congeneric plant species pairs in Northern Europe
Indifferent
Denmark
Estonia
Finland
Karelia
Latvia
Lithuania
Murmansk
Norway
Novgorod
Pskov
St. Petersburg
Sweden
P
Specific
Threatened
Non-threatened
Threatened
Non-threatened
3
13
3
3
5
5
4
5
0
2
1
8
11
29
12
12
26
19
5
14
12
16
18
24
45
83
60
45
82
66
18
48
36
49
46
98
37
67
51
36
61
52
17
39
36
35
29
82
0.020
0.004*
0.013
0.011
<0.001*
<0.001*
0.050
0.020
<0.001*
<0.001*
<0.001*
0.002*
Significances according to Fisher Exact test. An asterisk marks significant tests after Bonferroni correction.
Broad pH requirement was always less common
among threatened species than among non-threatened
(Table 2). After Bonferroni correction most of the tests
remained significant. Using country as a replicate, Wilcoxon-matched pairs test revealed that this pattern is
significant within the region (n ¼ 12, T ¼ 0:00, Z ¼ 3:1,
P ¼ 0:002).
4. Discussion
In Northern Europe, the proportion of high pH soils
in protected areas was significantly larger than the
proportion of these soils in general. This ensures that the
large regional pool of plant species preferring high pH
soils is relatively well protected. The requirement of
threatened species in Northern Europe was not more
biased towards high pH soils than non-threatened species. Consequently, number of threatened species can be
successfully used as indicator of overall biodiversity
level.
For Swedish protected areas, besides political reasons, botanical criteria (presence of rare or endangered
species and plant communities, many plant species)
have been the most frequently applied scientific aspect
in reserve selection, because professional botanists were
widely involved in this process (G€
otmark and Nilsson,
1992). This is certainly not true for all Northern European countries. In Sweden the proportion of high pH
soils is less than 40%, but more than 80% of protected
land is on high pH soils (Fig. 2). Swedish data can be
used in Northern Europe as a standard, against which
the representation of botanical aspects in the nature
conservation systems of other countries can be
checked. Indeed, the general trend is clearly showing
that high pH soils with potentially high plant diversity
are well protected throughout Northern Europe
(Fig. 2).
M. P€artel et al. / Biological Conservation 120 (2004) 525–531
There are very few examples where a similar approach has been used elsewhere. For example, rare
plants and threatened calcareous communities were
successfully identified for conservational purposes from
soil and geological data in Kentucky, USA (Mann et al.,
1999). It is economically easier to make nature reserves
in sparsely populated mountains or bogs than in agricultural landscapes, which are often characterized by
high pH soils (Ramankutty et al., 2002). Lack of economic value, and the existence of scenic and recreational
values have been the prevailing selection criteria of
protected areas in most countries (Pressey, 1994). Further analyses are needed for other regions with higher
population density (e.g., Western and Central Europe,
Northern America).
Threatened and non-threatened plant species in
Northern Europe did not differ in their soil pH requirements (Table 1). This is in agreement with our
previous studies on Estonian threatened and nonthreatened bryophytes (Ingerpuu and Vellak, 1995) and
Estonian calcareous grassland common (core) and rare
(satellite) species (P€
artel et al., 2001). Our results, however, do not contradict several works that claim that
most rare species in Europe require high pH soils
(Hodgson, 1986; Nilsson and G€
otmark, 1992; Gustafsson, 1994; Roem and Berendse, 2000). Most European
threatened species do require high pH soils, but this is
also the case for non-threatened species. Thus, we have
to reject our initial hypothesis that shortage of high pH
soils in Northern Europe causes rarity and is a threat for
plant species. A further decrease of high pH sites,
however, may become a threat for plant diversity in
Northern Europe. For example, a decrease in local plant
diversity has been described in Europe due to acidification by pollution (Bobbink et al., 1998) and natural
mire succession (Gunnarsson et al., 2000).
When selecting conservation areas for biodiversity
protection, all taxa cannot be recorded from all sites,
and biodiversity indicators should be used (Hansson,
2001). Red List species are monitored more commonly
than other species. Our results suggest that threatened
species can be used as indicators for total plant diversity,
and establishment of nature reserves in areas with many
threatened species also protects the overall species pool.
In addition, the requirements of vascular plants and
bryophytes regarding soil pH were not different, and one
taxonomic group can be used as an indicator for the
other group. The correlations between the species richnesses of bryophytes and vascular plants were positive in
several forest and mire community types (Ingerpuu
et al., 2001).
Threatened vascular plant species require more restricted soil pH while non-threatened species tolerate a
broader range of soil pH (Table 2). In a comparison of
threatened and non-threatened vascular plant species in
Finland, the threatened species had more specialized
529
edaphic requirements (Lahti et al., 1991). Likewise,
habitat specificity was the most frequent form of plant
rarity in Norway (Sætersdal, 1994). Habitat specificity is
a widely used criterion for defining rare species (Rabinowitz, 1981). Restricted habitat specificity is characteristic of 59% of British vascular plants (Rabinowitz et
al., 1986) and of 67% of vascular plants in Estonian
grasslands (Ingerpuu, 2002). We were not able to estimate whether threatened bryophytes had a narrower
requirement for soil reaction since none of the bryophyte species from 50 pairs were indicated as indifferent.
Thus, both rare and common bryophyte species probably have relatively well-defined soil pH requirements
compared to vascular plants. Using taxonomically related rare and common moss species, Cleavitt (2001)
observed no differences in the range of substrate pH
preferences. Among Estonian grassland bryophytes,
72% showed restricted habitat specificity (Ingerpuu,
2002). Consequently, in order to protect a wide array of
threatened species, it is important to have reserves not
only on high pH soils but also on low pH soils.
The protection of European biological and landscape
diversity is not satisfactory at the present moment
(Haslett, 2002). The plant diversity conservation in
Northern Europe is at least on the right tracks according
to the soil pH/plant diversity relationship (P€artel, 2002).
Our positive results, however, do not mean that the
present network of protected areas in Northern Europe
is sufficient. Several other aspects should be considered,
especially both positive and negative human influence.
Nevertheless, this work is an example of how to examine
a system of protected areas in regard to the relationships
between biodiversity and abiotic factors.
Acknowledgements
This work was supported by Estonian Science
Foundation grants for M.P. (4597 and 5503), N.I.
€
(5452) and U.R.
(5815).
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