Folia Geobot DOI 10.1007/s12224-012-9145-x
Can We Distinguish Plant Species that are Rare and Endangered from Other Plants Using Their Biological Traits? Jarmila Gabrielová & Zuzana Münzbergová & Oliver Tackenberg & Jindřich Chrtek
# Institute of Botany, Academy of Sciences of the Czech Republic 2013
Abstract Understanding the factors responsible for species rarity is crucial for effective species conservation. One possible approach to obtaining information about causes of species rarity is to compare rare and common species. We analyzed the biological and ecological traits of critically endangered (CR) plant species of the Czech Republic. We compared the vegetative, generative and ecological traits of CR species with: i) common closely related species (a form of phylogenetic correction), ii) common closely related species sharing the same habitat (i.e., excluding pairs not sharing the same habitat, because many differences in species traits can be caused by adaptation to a specific habitat type) and iii) all plants of the Czech Republic. Information about species traits was mainly obtained from literature and databases. Comparison with common closely related species showed that CR species are smaller, flower for shorter periods, and have higher proportions of selfcompatibility and higher terminal velocities. CR species also differ in their mode of dispersion, and their ecology and distribution. Comparison with species from the same habitat gave similar results. Comparison with the whole flora produced slightly different results, with additional differences in pollination mode and seed mass. The results of all three types of comparison suggest that critically endangered species of
Electronic supplementary material The online version of this article (doi:10.1007/s12224-012-9145-x) contains supplementary material, which is available to authorized users.
J. Gabrielová (*) : Z. Münzbergová Faculty of Science, Department of Botany, Charles University in Prague, Benátská 2, CZ-128 01 Prague, Czech Republic e-mail:
[email protected] Z. Münzbergová : J. Chrtek Institute of Botany, Academy of Sciences of the Czech Republic, Zámek 1, CZ-252 43 Průhonice, Czech Republic O. Tackenberg Institute of Ecology, Evolution and Diversity, Goethe-University Frankfurt, Siesmayerstrasse 70, 603 23 Frankfurt am Main, Germany
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the Czech Republic are small, competitively inferior species, with some differences in the generative part of their life cycle, and occur mainly in open, unproductive habitats. Keywords Central Europe . Life-history traits . Phylogenetically independent contrasts . Red List . Threatened species Plant nomenclature Kubát et al. (2002) Abbreviations CR critically endangered vascular plant species of the Czech Republic IUCN International Union for Conservation of Nature
Introduction Understanding the factors governing the relative abundance and distribution of species remains one of the main issues of ecology (May 1999). Why some species are rare while others are common or even invasive is a question that underlies much of contemporary conservation biology (Gaston 1994; Kunin and Gaston 1997). There are two main approaches to explaining how life history and ecological traits vary among species in relation to rarity and commonness. The first involves the detailed study of the population biology of two or several related, ecologically similar species that vary in abundance (e.g., Fiedler 1987; Byers and Meagher 1997; Witkowski and Lamont 1997; Walck et al. 2001; Münzbergová 2005). Such autecological studies have the potential to provide useful biological information for the conservation and management of rare species (Murray et al. 2002). However, it is simply not feasible to perform such studies for every rare species. In addition, when a single species pair is the focus of study, it is difficult to make generalizations (Bevill and Louda 1999). Hence, the second approach focuses on the relationship between species rarity and selected life-history traits, which are easier to measure and believed to be correlated with important parts of the life cycle (dispersal, establishment and persistence; Weiher et al. 1999). In recent years data on life-history traits have been compiled in extensive databases (e.g., Thompson et al. 1997; Bonn et al. 2000; Klotz et al. 2002; Poschlod et al. 2003; Klimešová and Klimeš 2006; Kleyer et al. 2008; Römermann et al. 2008), which enable the use of this approach within larger sets of species. Comparative studies of species rarity and commonness provide a suitable alternative for rapidly assessing whether there are traits that are characteristic of low-abundance, narrowly distributed or threatened species (Murray et al. 2002). When exploring types of traits within a group of species it is important to be able to distinguish which of the traits are specific characteristics of the species and which are characteristics of a larger set of species within a specific region. A proven way to resolve this problem is by using phylogenetic correction to compare the traits of pairs of closely related species, one of which is rare and the other common (Cotgreave and Pagel 1997). Analysis of the processes involved in producing and maintaining rarity requires a clear definition of rarity (Bevill and Louda 1999). A very simple definition was given by Gaston (1994): “Rare species are regarded as those having low abundance and/or
Can we Distinguish Plant Species that are Rare and Endangered from Other Plants
small ranges”. In practice, this definition is hard to apply, as we need to define the clear meaning of low abundance and small range for a given spatial scale. Bevill and Louda (1999) and Murray et al. (2002) provided an overview of studies that compared the life history and ecological traits of rare and common species. In these studies, rarity was measured as distribution, abundance, threatened status or a combination of these factors (for references see Bevill and Louda 1999 and Murray et al. 2002). Different definitions of rarity in each case may be one of the reasons why there were so few consistent rare–common differences in the review by Murray et al. (2002). Only one plant trait – seed production – distinguished between rare and common species fairly consistently (with lower fecundity in rare species; Murray et al. 2002). Another problem with Gaston`s definition is that rare and endangered species may differ in functional traits, which makes it necessary to clearly distinguish between rarity (which might be natural, cf. Rabinowitz 1981) and endangerment when applying a functional approach (Römermann et al. 2008). Our study focused on critically endangered species from the Red List of rare and endangered vascular plant species of the Czech Republic (IUCN CR category in Procházka 2001). We are aware that this group of species is a relatively heterogeneous mixture of species that was selected using a wide, often subjective, range of criteria. We used this selection as a set of species that are considered rare and of strong conservation interest in the Czech Republic. We compared the traits of CR species with those of species that are closely related to the CR species, but are common (within-pair comparison). For some traits, we also conducted comparisons with common species of the whole flora of the Czech Republic. Comparison with the whole flora (inter-species comparison) gave general information on the traits differentiating CR species from the rest of the Czech flora. In contrast, within-pair comparison has the power to identify causes of species rarity and endangerment. Some differences in species traits between pairs may not be related to species rarity, but to the different habitats occupied by the speices (Prinzing et al. 2008). To take this into account, we also compared a subset of pairs of CR species and their common closely related species occurring in the same habitat. We aimed to answer the following questions: i) Which traits are characteristic of critically endangered (CR) species of the Czech Republic? ii) How do CR species differ from species that are closely related, but common? iii) How do CR species differ from species that are closely related, but common, and share the same habitat type? iv) How do CR species differ from species of the whole flora of the Czech Republic? By making these comparisons, we hope to understand some of the possible causes of rarity of CR species and identify which of the differences are due to the occurrence of the species in different habitat types and to species belonging to different taxonomic categories.
Material and Methods Critically Endangered Species The group of critically endangered (CR) species was based on the Red List of vascular plants of the Czech Republic (Procházka 2001). This category corresponds
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to the CR category of the IUCN. The species belonging to this category were, however, not selected on the basis of some objective criteria (e.g., criteria of IUCN, IUCN 2001). As stated in the methodology of the Red List (Procházka 2001) the list includes taxa that are both very rare and seriously threatened, represented by only one or a few (usually up to five) local populations, confined mostly to habitats endangered by human activities, but sometimes also by natural factors. Populations of these species are mostly not abundant, are often fragmented and isolated, and are formed by individuals that flower only occasionally, rarely bear viable seed or persist in localities only by vegetative means. Taxa whose occurrence exhibits such a pattern are also classified in this category even if they occur in more than five localities, because to conserve their gene pool, a strict limit in the number of localities is of no use. The category also includes taxa that were common or very common in the past but must now be considered rare due to a substantial decrease in the number, size and density of local populations. Some have declined to only 10 % (or even less) of their former occurrence and it can be assumed that this trend will continue. If relevant conservation measures are not implemented immediately to protect taxa in this category (some grow outside protected areas), it is highly probable that under the continuing influence of threatening factors many of them will disappear from the flora of the Czech Republic. The CR category includes 483 species and subspecies (if we take into account additions and corrections from Procházka 2001), and represents 18.9 % of the 2,550 plant species that are autochthonous or archaeophytous in the flora of the Czech Republic (Procházka 2001). This high number of species and the vague definition of this category clearly show that a detailed understanding of the properties of these species will be required to set up efficient conservation measures. Selection of Common Closely Related Species To remove the effect of phylogeny from the data, we compared CR species with closely related species that are common in the Czech Republic. To select these species, we used published phylogenetic reconstructions of appropriate groups of species (mainly genera). If there was no such study (about 60 % of cases), we considered the newest generally accepted within-genus division based on non-molecular traits (morphology, chromosome number, traits of pollen grains, secondary metabolites). Initially we planned to include only species that are not endangered in the Czech Republic. However, using this condition led to very few species pairs. We thus included 29 near threatened (NT) and 51 vulnerable (VU) species according to the Red List of vascular plants of the Czech Republic (Procházka 2001). In total we obtained 206 species pairs (see Table S1 in Electronic Supplementary Material). The remaining 277 CR species have no common close relative in the Czech Republic, or else the close relative is also critically or strongly endangered or extinct. Species Traits Data The data on species traits were obtained from the literature (Ellenberg et al. 1992; Hejný and Slavík 1988, 1990, 1992; Slavík 1995, 1997, 2000; Kubát et al. 2002; Slavík and Štěpánková 2004) and databases (Thompson et al. 1997; Bonn et al. 2000; Klotz et al. 2002; Poschlod et al. 2003; Klimešová and Klimeš 2006; Kleyer et al.
Can we Distinguish Plant Species that are Rare and Endangered from Other Plants
2008), covering five main groups of traits: vegetative, generative, seed traits, ecology and distribution. A basic overview of all traits is given in Table 1, and a detailed explanation of the categories and sources is given in Appendix S1 in Electronic Supplementary Material. For a small set of species (see Table S1 in Electronic Supplementary Material), some species traits were measured experimentally, e.g., seed mass, seed shape, terminal velocity and seed bank longevity. We followed the methodology described by Knevel et al. (2005). For selected species traits (see Table 1), we also compared CR species with the whole flora, according to the checklist of the Czech flora (Danihelka et al. 2007). CR and extinct species and species of unclear taxonomic status were excluded. We obtained a list of 3,263 species and subspecies. Statistical Analyses To test for differences in quantitative characteristics we performed a paired t-test or Wilcoxon signed-rank test (comparison of CR vs common) and a one-way ANOVA or Kruskal-Wallis test (comparison of CR vs whole flora). To test for differences in categorical characteristics we used a contingency table and a χ2 test. Differences in categorical characteristics that were coded as percentages (in cases in which one species may occur in more than one category, e.g., altitudinal level, pollination vector) were tested using canonical correspondence analysis (CCA, with species traits as “species” and single species as “samples”). When comparing CR species with closely related common species, “species pair” was used as a covariate and the significance was tested using randomization within blocks defined by these covariates. In this way, the test performed using CCA was conceptually similar to a paired t-test, i.e., it also compared traits between CR and common species within the pair. Unlike the t-tests, the CCA analysis is performed via permutation, a quasistatistical method. For this reason, it is not possible to extend statistical inferences to the whole nature as is the case in parametric statistical methods. The results for traits tested by t-test are thus of a different type than those obtained in the CCA. As parametric tests cannot be performed in CCA, we checked what would happen if we used permutation instead of a parametric test for the data tested via the t-test. The results were qualitatively the same in both cases. We thus suggest that combining the results obtained using the two different approaches is not a major problem when interpreting our results. Analyses were performed in S-PLUS 2000 (MathSoft, Inc. 2000) and CANOCO (ter Braak and Šmilauer 1998). Some differences in species characteristics of closely related species may be caused by adaptation to different habitat types. To explore this, we divided the species into nine groups according to their habitat type (streams and water bodies, wetlands and riverine vegetation, springs and mires, cliffs and boulder scree, treeless alpine habitats, secondary grasslands and heathlands, scrub, forests, and habitats strongly influenced or created by man; categories after Chytrý et al. 2001). We then selected the pairs of CR and common species that occur at least partly in the same habitat type. We obtained a subset of 149 species pairs. As we conducted many separate comparisons of traits that are intercorrelated, we constructed a correlation matrix for traits for which we found a significant difference. This matrix is too large to present here; however, in general only the expected
J. Gabrielová et al. Table 1 Differences in species traits between critically endangered (CR) plant species of the Czech Republic and common species, common species from the same habitat type and the whole flora of the Czech Republic Traits
Test
All pairs n
Same habitat type
CR vs the whole flora
P-value n
P-value
n
P-value
2027
n.s.
1808
–***
1485
n.s.
Vegetative traits Life form
CCA 206
n.s.
149
n.s.
Life span
CCA 206
n.s.
149
n.s.
Mean plant height
W
205
–***
149
–***
Leaf distribution along the stem χ2
132
n.s.
95
n.s.
Leaf persistence
χ2
122
n.s.
87
n.s.
Leaf anatomy
CCA 106
n.s.
77
n.s.
Specific leaf area (SLA)
W
63
n.s.
48
n.s.
Clonality†
χ2
57–87 n.s.
44–66
n.s.
Duration of flowering
W
206
–***
149
–**
Beginning of flowering
W
206
+**
149
n.s.
End of flowering
W
206
+**
149
+**
Type of reproduction
χ2
131
n.s.
95
n.s.
Dicliny
CCA 130
n.s.
94
n.s.
Dichogamy
CCA 92
m.s.
61
n.s.
Pollination mode
CCA 165
n.s.
117
n.s.
1675
*
Self-compatibility
χ2
101
*
78
*
1233
***
Floral rewards
χ2
42
n.s.
31
n.s.
t
81
+m.s.
53
+*
1236
n.s.
Generative traits
Seed traits Terminal velocity Seed mass
W
70
n.s.
51
n.s.
1333
–***
Seed shape
t
78
n.s.
55
n.s.
1190
n.s.
Dispersal type
CCA 141
*
96
m.s.
1177
**
LDD vs SDD
W
141
n.s.
96
n.s.
1177
n.s.
Seed production
W
44
n.s.
31
n.s.
Seed bank longevity index
W
23
n.s.
20
n.s.
690
n.s.
1560
**
+***
Ecology Grime’s csr scheme
CCA 123
**
85
**
Urbanity
χ
***
84
***
Hemeroby
CCA 118
**
83
**
Number of hemerobic levels
W
118
n.s.
83
n.s.
Ell. ind. values - light
W
123
+*
89
n.s.
1796
Ell. ind. values - temperature
W
87
+m.s.
64
+*
1564
n.s.
Ell. ind. values - continentality
W
101
m.s.
70
n.s.
1628
n.s.
2
120
Ell. ind. values - moisture
W
113
n.s.
83
n.s.
1444
+***
Ell. ind. values - soil reaction
W
92
+*
66
+**
1550
n.s.
Ell. ind. values - nitrogen
W
104
–***
74
–*
1690
–***
Can we Distinguish Plant Species that are Rare and Endangered from Other Plants Table 1 (continued) Traits
Test
All pairs n
Same habitat type P-value n
P-value
CR vs the whole flora n
P-value
Distribution Altitudinal level
CCA 193
**
123
**
Number of floristic zones
W
128
–***
91
–***
Number of floristic regions
W
129
–*
91
–**
Habitat type
CCA 206
**
*** – P≤0.001, ** – P<0.01, * – P<0.05, m.s. – marginally significant (P<0.1), n.s. – not significant; + – CR species have higher values for a given trait; – – CR species have lower values; without sign – significant differences for factors; empty fields – not tested for differences. Test: CCA – canonical correspondence analysis, t – paired t-test/one-way ANOVA, W – Wilcoxon signed-rank test/Kruskal-Wallis test, χ2 – contingency table with χ2 test. LDD vs SDD – long- vs short-distance dispersal. † – Clonality: many traits from Klimešová and Klimeš (2006), all differences not significant, thereby not shown (see also Appendix S1 in Electronic Supplementary Material).
correlations were observed – particularly those between ecological and distributional characteristics (e.g., between Ellenberg indicator values and hemeroby, urbanity, habitat type and altitude; between csr-strategy and hemeroby etc.). There were only a few correlations among biological traits and between biological traits and ecology (e.g., between terminal velocity and anemochory, mean height and Ellenberg indicator value for reaction or between anemogamy and urbanophilic level of urbanity). The differences between the CR species and the whole flora could theoretically be because CR species are overrepresented in some families, but underrepresented in others. To explore this possibility we performed a randomization test. We thus asked whether the number of CR species belonging to a given family could result from random sampling from the total dataset (all vascular plants of the Czech Republic). Specifically, we randomly sampled a given number of species (corresponding to the number of CR species) from the whole flora of the Czech Republic. In each step we recorded whether the number of species in each family in this random sample was equal to, or higher or lower than the real number of CR species in the given family. We repeated such random sampling 1,000 times. For each family, we derived an empirical P-value indicating the probability that the number of CR species belonging to a given family could be due to random sampling from the total dataset or that the number of species in the family is higher or lower than expected (two-sided test with α=0.05).
Results Comparison of Traits between CR Species and Their More Common Close Relatives Within the group of vegetative traits, we found significant differences in mean plant height – CR species are shorter than common species (Fig. 1a). There are no differences in life form, distribution of leaves along the stem, leaf duration, leaf anatomy or
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Fig. 1 Differences in quantitative traits of critically endangered (CR) species of the Czech Republic and their common close relatives: a mean plant height (n=205, P<0.001); b duration of flowering (n=206, P<0.001)
clonality (Table 1). Comparison of generative traits revealed significant differences in the duration of flowering – CR species start to flower later and finish flowering earlier than common species, and thus the duration of flowering is shorter (Fig. 1b). Species also differ in the proportion of self-compatibility – CR species are significantly more often self-compatible and less often self-incompatible than common species (Fig. 2). There are no differences in the type of reproduction, dicliny, dichogamy, pollination mode or floral reward (Table 1). CR and common species also differ significantly in their mode of dispersal. There is a higher proportion of epizoochory and hydrochory and a lower proportion of endozoochory and hemerochory in CR species in comparison with common species (Fig. 3). However, there is no difference in the proportion of long- and short-distance dispersal. There is a marginally significant difference in terminal velocity – CR species have higher terminal velocities than common species. The CR and common species do not differ in seed mass, seed shape or seed bank longevity index.
Can we Distinguish Plant Species that are Rare and Endangered from Other Plants
Fig. 2 Differences in proportion of self-compatibility between critically endangered (CR) and common closely related species of the Czech Republic. SC – self-compatible, SI – self-incompatible, SI/SC – intermediate (n=101, P=0.04)
CR and common species differ in a number of ecological characteristics. There are fewer c-strategists and more s-strategists among CR species (if we decode the intermediate strategies – cs, cr, sr and csr in the main three categories c-s-r using a fuzzy coding approach). There are more urbanophobic species among CR species compared with common species (81.7 % vs 52.5 %). Surprisingly, there is also a higher proportion of urbanophilic species (species that occur only in urban areas) among CR species (3.3 % vs 0.8 %). There is a higher proportion of ahemerobic (7.6 % vs 2.4 %) and oligohemerobic (38.1 % vs 31.1 %) species (species that occur in habitats without or with only slight human impact) among CR species. However, there is no difference in the number of hemerobic levels between CR and common species (i.e., the species do not differ in their “ecological amplitude”). Comparison of the Ellenberg indicator values showed that CR species have significantly higher requirements for light (Fig. 4a) and temperature (marginally
Fig. 3 Differences in dispersal type between critically endangered (CR) species of the Czech Republic and their common close relatives (n=141, P=0.028). Anemo – anemochory (dispersal by wind), hydro – hydrochory (dispersal by surface currents of water), epizoo – epizoochory (adhesive dispersal), endozoo – endozoochory (dispersal after digestion), hemero – hemerochory (dispersal by man). All types are methods of long-distance dispersal. Others – short-distance dispersal
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Fig. 4 Differences in Ellenberg indicator values between critically endangered (CR) species of the Czech Republic and their common close relatives: a Ellenberg indicator values for light (n=123, P=0.01); b Ellenberg indicator values for nitrogen (n=104, P<0.001)
significant difference), are more basophilous, and have lower requirements for nitrogen (often interpreted as nutrients, Schaffers and Sýkora 2000; Fig. 4b) than common species. CR and common species differ in all compared characteristics associated with distribution. CR species occur significantly more often in sub-alpine habitats (i.e., above 1,300 m a.s.l.) and in the lower elevations of the Czech Republic (200–400 m a.s.l.). CR species also have smaller geographical ranges measured as the number of floristic zones and floristic regions. CR and common species also differ in their distribution in different habitat types (Fig. 5). The results of the comparisons between species pairs from the same habitat type were generally consistent with the results of the comparisons between all CR and common species. Only the differences in the beginning of flowering and the Ellenberg indicator value for light were not significant in this case, and the differences in dispersal type were only marginally significant (Table 1).
Can we Distinguish Plant Species that are Rare and Endangered from Other Plants
Fig. 5 Distribution of critically endangered (CR) species of the Czech Republic and their common close relatives among different habitat types. V – streams and water bodies, M – wetlands and riverine vegetation, R – springs and mires, S – cliffs and boulder screes, A – treeless alpine habitats, T – secondary grasslands and heathlands, K – scrub, L – forests, X – habitats strongly influenced or created by man (n=206, P=0.004)
Comparison of Traits between CR Species and Species of the Whole Flora of the Czech Republic The comparison of selected traits of CR species and the whole flora of the Czech Republic confirmed some of the above-mentioned findings (differences in mean plant height, self-compatibility, Grime’s CSR scheme, Ellenberg indicator values for light and nitrogen), and revealed some additional trends. The additional trends include differences in pollination mode (Fig. 6). Differences in dispersal type remained significant, but the trend was inconsistent with the results of the comparison between CR and common species. In agreement with the previous comparison, there is a higher proportion of epizoochory and hydrochory in CR species. However, the comparison with common species showed a lower proportion of anemochory in CR species (18.7 % vs 19.5 %). In comparison with species of the whole flora, CR species tend to be much more anemochorous (21.5 % vs 12.1 %) and have significantly lighter seeds. Another new trend is that of higher indicator values
Fig. 6 Differences in pollination mode between critically endangered (CR) species of the Czech Republic and species of the whole flora (n=1675, P=0.028)
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for moisture in CR species, meaning that CR species are more hygrophilic. The differences in temperature and soil reaction between CR species and species of the whole flora, however, were not significant. CR species occur in 83 families out of 173 families of the whole flora of the Czech Republic. In six families, the number of CR species is significantly less than expected by random sampling from the whole flora (Alliaceae, Brassicaceae, Onagraceae, Polygonaceae, Rosaceae and Solanaceae). In nine families, the number of species is significantly higher than expected by random sampling from the whole flora (Aspleniaceae, Asteraceae, Caryophylaceae, Gentianaceae, Isoëtaceae, Lentibulariaceae, Orchidaceae, Orobanchaceae and Santalaceae).
Discussion Comparison of traits between CR and common species showed many differences in their ecology and distribution and relatively few differences in their biological traits. However, there were some differences in generative traits – CR species flower for a shorter period each year, beginning to flower later and finishing flowering earlier than common species. This result is consistent with the findings of Lahti et al. (1991) and Gustafsson (1994). The effectiveness and success of pollination may depend on the length of the flowering period, so CR species may be at a disadvantage in this aspect of reproductive biology. However, as suggested by Lahti et al. (1991), this pattern may also arise due to methodological problems: the small population size and restricted geographical distribution of the threatened taxa tends to reduce the variance in the phenology of flowering observed in the field and thus reported in databases. There are also many high altitude species among the CR species, and these generally begin flowering later and flower for a shorter period than species from lower elevations. Small, peripheral and isolated populations or species from islands are often reported to be more self-compatible than species that are common or grow in the center of their distributional range, leading to reproductive assurance in these populations/species (e.g., Baker 1955; Stebbins 1957; Barrett 1996; Schoen et al. 1996; Fausto et al. 2001; Busch 2005). We confirmed these findings for rare and threatened species in our study, showing more self-compatible taxa in CR species in comparison to common species and taxa of the whole flora of the Czech Republic. This suggests that CR species have developed characteristics that make them less dependent on pollinator services for their reproductive success, with self-compatibility reducing their reliance on pollinators whose presence and quality may be unreliable (Kunin and Schmida 1997). Long-term crossing of closely related individuals, however, can cause inbreeding depression leading to the overall lower fitness of these individuals (Meffe and Carroll 1994). In accordance with Kelly and Woodward (1996), Cadotte and Lovett-Doust (2002) and Pilgrim et al. (2004) we found significant differences in pollination mode in comparison with the whole flora, with more entomogamy, and less anemogamy and autogamy among CR species. The prevalence of entomogamy in rare species could be explained as a “cost of mutualism” when the association with a specialized pollinator constrains the area that the particular species can colonize (Kelly 1996).
Can we Distinguish Plant Species that are Rare and Endangered from Other Plants
It also indicates the greater sensitivity of entomogamous species to environmental changes and habitat degradation. Significant differences were only observed in comparisons with the whole flora possibly because pollination mode is an evolutionarily stable trait (Eriksson and Bremer 1992; Dodd et al. 1999), and is consistent with Lahti et al. (1991), who also found no significant differences between rare and closely related common species in terms of pollination mode. The results of the comparison of seed traits varied depending on whether the comparison was between CR and common species or the whole flora. Comparison with common species indicated that CR species might show limited wind dispersal (significantly higher values of terminal velocity). However, no such difference was detected in comparison with the whole flora. Conversely, the results showed a significantly lower seed mass and a higher proportion of anemochory in CR species in the comparison with the whole flora. The absence of a difference in seed mass in comparison with common species could be because seed mass is an evolutionary stable trait, the variation of which among species is associated with taxonomy such as family membership (Leishman et al. 2000) and is thus similar between species from the same genus. Differences between species within species pairs were thus not expected. The results of comparison with the whole flora may also be influenced by the CR species being small, competitively inferior species that have lighter seeds (e.g., Peat and Fitter 1994) that are better dispersed by wind. Interestingly, other studies found no significant differences in the dispersal abilities of rare and/or endangered species (Lahti et al. 1991; Kelly 1996, Kelly and Woodward 1996; Hegde and Ellstrand 1999) or any differences in seed mass (Edwards and Westoby 1996; Eriksson and Jakobsson 1998; Thompson et al. 1999). However, species from high elevations, which were overrepresented in this study, show significant differences in terminal velocities when compared to lowland species, at least when species from habitats with closed vegetation cover are included in the analysis (Tackenberg and Stöcklin 2008). Many studies on rare–common species pairs found that rare species produce fewer seeds (e.g., Banks 1980; Byers and Meagher 1997; Pirie et al. 2000; Walck et al. 2001); authors of studies of larger sets of species came to the same conclusion (Eriksson and Jakobsson 1998; Cadotte and Lovett-Doust 2002; Lavergne et al. 2004; Pilgrim et al. 2004). However we found no significant difference in seed production between CR and common closely related species. This may be due to the insufficient quality and paucity of available data for seed production in the LEDA traitbase used as the source of our data. Comparison of hemeroby (Klotz et al. 2002) in CR species with common closely related species demonstrated that CR species occur significantly more often in habitats without any or with only slight human impact, which is consistent with the expectation that CR species are negatively influenced by modern human activities. However, not all CR species are restricted to habitats with low hemeroby. Several CR species, such as Hypochaeris glabra, Rumex palustris, Sagina nodosa, Sagina subulata, Viola kitaibeliana and Trifolium striatum in fact grow across a wide range of hemerobic levels. A similar result was obtained in the comparison of urbanity. Many CR species are urbanophobic, however there is also a higher proportion of urbanophilic species (e.g., Artemisia scoparia, Bromus squarrosus, Eragrostis pilosa and Herniaria hirsuta) compared to common species.
J. Gabrielová et al.
In the comparison with common species as well as with the whole flora of the Czech Republic, CR species were found to be significantly shorter than the more common species. This is consistent with the results of Hegde and Ellstrand (1999), Lavergne et al. (2004) and Pilgrim et al. (2004). Plant height is associated with competitive vigour, plant fecundity and generation time after disturbance (Knevel et al. 2005), suggesting that the CR species are competitively weaker than their common congeners. The lower competitive ability of CR species was also evident in the comparison of csr-strategy, with a lower proportion of c-strategists among CR species. CR species are thus often species of early successional stages, which, during the process of succession, are overgrown by stronger competitors or occur in habitats with high levels of stress. These findings were confirmed by comparison of Ellenberg indicator values (Ellenberg et al. 1992). Comparison with common closely related species suggested that CR species occur significantly more often in open, calcareous, warm and nutrient-poor habitats. Comparison with the whole flora indicated that CR species occur significantly more often in calcareous, nutrient-poor and humid habitats. Despite some inconsistency in the results based on the two types of comparison, both indicate that CR species are competitively weak and are thus forced into unsuitable habitats. Nutrient-poor habitats are endangered by eutrophication over the whole of Europe, leading to high levels of endangerment of species in these habitats (e.g., Ratcliffe 1984; Fischer and Stöcklin 1997; Bakker and Berendse 1999). Comparison of the occurrence of CR and common species at different altitudinal levels and in different types of habitat also illustrated the problem of rarity and the endangerment of habitats in the Czech Republic in which CR species tend to occur. Many CR species are restricted to high elevations, and treeless alpine habitats, the extent of which is limited in the Czech Republic. The markedly lower distribution of CR species in forests and scrub is particularly interesting. This probably reflects the fact that forests and scrub are common in the Czech Republic (Härtel et al. 2009). CR species have, in comparison to common closely related species, a smaller geographical range based on rough data available in the BiolFlor database (Klotz et al. 2002). This indicates that the CR status of species in the Red Lists of the Czech Republic is correlated with “natural” rarity defined by the extent of their area of distribution. Limitations of the Study In our study, we compared traits that are available in databases, as have many previous studies that compared larger number of traits. Using this approach allows comparison of a large number of traits for a large number of species, resulting in tests with high statistical power. The information in the databases, however, could contain mistakes, and values of traits measured for individuals of a species growing, for example, in Great Britain, may not completely correspond to values for the same species growing in the Czech Republic. In addition the set of traits and species available from databases is limited and some rare-common differences may occur on a finer scale than we could capture based on the available data. Furthermore, differences in single life-history traits do not necessarily mean differences in overall population dynamics (Münzbergová 2005). It would thus be useful to link the results
Can we Distinguish Plant Species that are Rare and Endangered from Other Plants
of such extensive studies comparing single life-history traits with more detailed data on the life cycle of a few selected species. Our dataset is also limited because information about individual traits was missing for many species (for each trait we had information for a slightly different subset of species). We also carried out many separate comparisons of traits that are mutually correlated. While it would definitely be interesting to carry out the analyses with all traits combined, such analysis is unfortunately not possible due to the many missing values and low number of species with data on all traits. The method of pair-wise comparison used in our study is one of the simplest versions of phylogenetic correction (Felsenstein 1985). Recently, more sophisticated techniques based on complete phylogeny have been developed (e.g., Díaz-Uriarte and Garland 1998; Martins and Hansen 1999; Rheindt et al. 2004; Rohlf 2006; Webb et al. 2008). Such an approach, however, requires a fully resolved phylogeny, which is not available for the flora of the Czech Republic, and thus a pair-wise comparison was the method of choice in our case. The disadvantage of this method is that in some cases there was no suitable species pair available and thus species without pairs had to be removed from the analyses. In some cases (10 %), we used the same common species as the closest common congeners for more than one CR species. While this represents a kind of pseudoreplication, we believe that including these did not cause major problems. Excluding such pairs did not affect the results. The division into nine basic habitat types in the comparison of species sharing the same habitats was relatively crude, but finer classification was not available for all species. If available, this would lead to the exclusion of most of the species pairs from such a comparison. Hence, even if the results of the comparison of CR and common species are similar to the results of the comparison of congeneric pairs sharing the same habitats, we cannot rule out the possibility that the differences in traits of closely related species revealed in our study were due to adaptation to different habitat types. Acknowledgments We thank A. Bucharová, P. Dostál, V. Hadincová, Z. Hroudová, V. Latzel, J. Knappová, P. Petřík, H. Skálová and two anonymous reviewers for helpful comments on the manuscript. This study was supported by grant VaV 2B06178 and institutional research grants RVO 67985939 and MSMT. JG was supported by 206-08-H049, OT by the DFG (TA 311-3), and BIK-F within the LOEWEinitiative of Hesse’s Ministry of Higher Education, Research and the Arts.
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