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Niche analysis of orchids of serpentine and nonserpentine areas: Implications for conservation
a

V. Djordjevi , S. Tsiftsis , D. Lakui & V. Stevanovi


a

Faculty of Biology, Institute of Botany and Botanical Garden, University of Belgrade,


Takovska 43, 11000 Belgrade, Serbia
b

Department of Botany, School of Biology, Aristotle University of Thessaloniki, 54124


Thessaloniki, Greece
Accepted author version posted online: 20 Nov 2014.Published online: 13 Dec 2014.

To cite this article: V. Djordjevi, S. Tsiftsis, D. Lakui & V. Stevanovi (2014): Niche analysis of orchids of serpentine and
non-serpentine areas: Implications for conservation, Plant Biosystems - An International Journal Dealing with all Aspects of
Plant Biology: Official Journal of the Societa Botanica Italiana, DOI: 10.1080/11263504.2014.990534
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Plant Biosystems, 2014


http://dx.doi.org/10.1080/11263504.2014.990534

ORIGINAL ARTICLE

Niche analysis of orchids of serpentine and non-serpentine areas:


Implications for conservation
1, S. TSIFTSIS2, D. LAKUSIC
1, & V. STEVANOVIC
1
V. DJORDJEVIC

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Faculty of Biology, Institute of Botany and Botanical Garden, University of Belgrade, Takovska 43, 11000 Belgrade, Serbia
and 2Department of Botany, School of Biology, Aristotle University of Thessaloniki, 54124 Thessaloniki, Greece

Abstract
Orchids are known for their species richness, intriguing ecology, rarity and the fact that they grow in almost all terrestrial
ecosystems. Although numerous studies about their ecology have been carried out concerning calcareous areas, little is
known about orchids that occur in serpentine habitats. The aim of this study was to investigate the ecological preferences of
orchids in serpentine and non-serpentine areas on the model of the Valjevo Mountain Range (W Serbia). Niche analysis of
orchids was performed using outlying mean index analysis. Data concerning geographical coordinates, altitude, habitat type,
inclination, bedrock type, light regime, soil moisture, acidity, nitrogen and temperature were used as explanatory variables.
Data of 33 orchid taxa from 407 localities were analysed. The most important gradients that govern orchid distribution were
geological bedrock, light regime and temperature. The results have shown that only Anacamptis morio and Gymnadenia
conopsea have statistically significantly larger populations on serpentine compared with non-serpentine bedrocks. This study
highlights the importance of serpentine habitats as orchid habitats, bearing in mind the occurrence of rare species and species
which were found exclusively in serpentine habitats.

Keywords: Orchidaceae, niche analysis, specialists, generalists, serpentine, ecology, conservation

Introduction
Understanding how environmental conditions and
species interactions determine the distribution and
abundance of species is a central problem and a
challenge in ecological and biogeographical research.
In addition, successful species conservation requires
the knowledge of their distribution patterns and
ecological preferences. On a large geographic scale,
patterns of species distributions are determined by
evolutionary and migration history together with
macroclimate. On the other hand, factors such as soil
properties, light regime, meso- and microclimate,
altitude, habitat type, disturbance, biotic factors, and
so on affect distribution and abundance of species on
a regional scale (Diez & Pulliam 2007; Blinova 2008;
Landi et al. 2009; Tsiftsis et al. 2012). The ecological
niche as defined by Hutchinson (1957) is a multidimensional hypervolume, determined by the habitat
gradients and the functional relationship among
species, within which a species maintains a viable
population. Niche analysis is a very useful tool for a

better understanding of the environmental requirements and distribution of species, as well as for
conservation planning (Tsiftsis et al. 2008; Casazza
et al. 2013).
The family Orchidaceae is one of the most speciesrich plant families with ca. 25,000 species distributed
worldwide, but it is most diverse and numerous in the
tropics and subtropics (Whigham & Willems 2003).
With the exception of the poles, extremely dry
deserts, salt marshes, and cultivated agricultural
lands, orchids grow in all terrestrial ecosystems
(Hagsater & Dumont 1996). More than 300 species
have been recorded to occur in Europe, North Africa
and Near East, with most of them distributed in
Mediterranean basin and hinterland (Hagsater &
Dumont 1996). In Serbia, 72 orchid taxa (species
and subspecies) have been recorded (Diklic 1976;
Karadzic et al. 2000; Djordjevic et al. 2010).
Although a few studies provide data on the plant
communities and geological bedrocks in which
individual orchid species occur, generally ecological

Correspondence: V. Djordjevi, Faculty of Biology, Institute of Botany and Botanical Garden, University of Belgrade, Takovska 43, 11000 Belgrade, Serbia.
Tel: 381 11 3244923. Fax: 381 11 3243603. Email: vlakiorhi@yahoo.co.uk
q 2014 Societa` Botanica Italiana

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V. Djordjevic et al.

studies on orchids in Serbia have not been performed


in the past.
Many of the terrestrial orchids have declined in
abundance and are considered to be rare, threatened,
or endangered, primarily as a result of habitat loss
(Kull & Hutchings 2006). Consequently, a lot of
species are protected by laws and/or are included into
the Red Data Books (Whigham & Willems 2003).
In general, an orchid species is rarer and has a higher
risk of extinction if it has a smaller geographic
distribution and population size, higher specificity of
habitat preferences and the higher level of dependence on pollinators and mycorrhizal symbionts.
Orchids are particularly sensitive to changes in the
balance of ecosystems including changes in organic
matter, light availability, hydrology and competition,
which can affect the survival and the ability of
seedlings to germinate and survive to adulthood
(Swarts & Dixon 2009). Throughout the past
decades, numerous ecological studies have focused
on orchids of calcareous areas, with emphasis on
grassland communities (Barbaro et al. 2003; Kull &
Hutchings 2006; Pierce et al. 2006; Landi et al.
2009), whereas much less research has been carried
out in areas that include other geological types.
Furthermore, it is noteworthy that little is known
about orchids that occur in serpentine habitats.
The term serpentine is used by ecologists, and
refers to ultramafic rocks, principally serpentinite
and peridotite, and the soils derived from them.
Serpentine soils are characterized by low Ca/Mg
ratios, high concentrations of Fe, Ni, Cr and Co, low
nutrient (NPK) levels and poor moisture-holding
capacity. The serpentine flora is characterized by a
relatively high level of endemism and numerous
edaphic ecotypes of species mostly growing on other
bedrock types (Stevanovic et al. 2003), whereas the
vegetation communities are distinct from those of
neighbouring areas, and are usually open, with low
plant cover, low productivity and slow growth rate
(Tzonev et al. 2013).
The main goal of this study was to determine the
ecological preferences of orchids of the Valjevo
Mountain Range (W Serbia). The objectives were: (i)
to determine species niche marginality and breadth,
(ii) to investigate most important ecological gradients
that govern species distribution and separate species
niche and (iii) to explore the relationship between the
population size of orchids of serpentine and nonserpentine habitats.

Materials and methods


Study area
The Valjevo Mountain Range is situated in western
Serbia and includes the mountains Medvednik,

Jablanik, Povlen, Maljen, Suvobor and the region of


Azbukovica, defined by the coordinates 198310 to
208150 E and 438560 to 448150 N. It belongs to the
north-eastern part of the Dinaric Alps, and its
climate can be described as humid temperatecontinental. The study area is dominated by the
following types of geological bedrock: limestone,
dolomite, sandstone, conglomerate, schist, gabbro
and diabase-chert formation, whereas Mts. Maljen
and Suvobor are composed mainly of serpentine
bedrocks (Mojsilovic et al. 1971).
Data collection
In total, data of 33 orchid taxa from 407 localities
were gathered (252 on serpentine and 155 on nonserpentine bedrock types). Data of 29 orchid taxa
from 343 sites were collected during field observations in the period between 1995 and 2013.
In addition, the data set included literature data of 10
taxa from 59 sites (Lintner 1951; Cincovic & Kojic
1956; Pavlovic 1964; Karadzic 1994; Karadzic et al.
2000) and herbarium data of four taxa from five
localities collected from Herbarium of University of
Belgrade. At each locality, data concerning orchid
abundance, geographical coordinates, altitude, habitat type, inclination, geological bedrock, light regime,
soil moisture, acidity, nitrogen and temperature were
recorded.
The identification of orchid taxa was made
according to Delforge (2006) and GIROS (2009),
whereas the nomenclature followed WCSP (2013)
and Molnar et al. (2012).
During field observations, the abundance of
orchids was determined on the basis of counting the
total number of plant specimens (census methodology). Then, the abundance of orchids was
summarized and expressed through a four-point
ordinal scale, used by Tsiftsis et al. (2008), as
follows: (1) 1 5 individuals, (2) 6 20 individuals,
(3) 21 50 individuals, and (4) . 50 individuals.
Literature data, which contained the BraunBlanquet (1964) cover-abundance seven-scale
values, were converted to a scale as follows: (1) r,
(2) , (3) 1 (literature data did not contain 2, 3, 4
and 5 Braun-Blanquet scale values).
Geo-coordinates (longitude, latitude) were transformed into X and Y coordinates. They were used
to explore a spatial differentiation of orchid
distribution.
Plant communities of sites with orchids were
determined by phytosociological sampling according
to the Braun-Blanquet (1964) methodology. Plant
community types were grouped into 11 habitat types
and represented in the analysis as 11 nominal
variables (Table I). Betula pendula forests were
included in Fagus forest type.

Niche analysis of orchids

Table I. Habitat types and plant communities in which orchids were recorded.
Habitat type

Plant communities

Arrhenatheretalia elatioris grasslands

Arrhenatheretum elatioris, Festuco rubrae-Agrostetum capillaris, Cynosuretum cristati,


Rhinantho-Cynosuretum cristati
Fagetum montanum, Abieti-Fagetum, Betuletum pendulae
Bromo-Danthonietum calycinae, Danthonietum calycinae, Chrysopogonetum grylli,
Festucetum valesiacae, Koelerietum montanae
Deschampsietum caespitosae, Holcetum lanati, Agrostio-Juncetum effusi, Juncetum inflexi,
Calthaetum palustris, Phragmitetum communis, Scirpetum sylvatici
Molinietum coeruleae, Molinio-Deschampsietum coespitosae, Molinio-Nardetum strictae
Nardetum strictae
Helleboro odori-Querco-Ostryetum, Orno-Ostryetum carpinifoliae
Pinetum nigrae, Pinetum nigrae-sylvestris
Pinus sylvestris forests
Querco-Carpinetum betuli
Quercetum frainetto-cerris, Quercetum cerris, Quercetum montanum

Fagus forests
Festuco-Brometea grasslands

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Marshes and hygrophilous meadows


Molinion coeruleae grasslands
Nardetalia strictae grasslands
Ostrya forests
Pinus nigra forests
Pinus sylvestris forests
Querco-Carpinetum betuli forests
Quercus forests

Geological bedrock types were determined on the


basis of field observations and the geological map of
the study area in a 1:100,000 scale (Mojsilovic et al.
1971). The following three bedrock types were
distinguished and treated as three nominal variables:
(1) diabases and spilites, (2) limestone, and (3)
serpentine.
The light regime was expressed in the scale, on
the basis of field observation as follows: (1) shadow,
(2) half-shadow and (3) open light regime.
Soil moisture was assessed by soil moisture
monitoring in the field. Scale of soil moisture was
as follows: (1) dry, (2) moderate and (3) moist.
Soil acidity, soil richness in available nitrogen and
temperature of habitat were determined using the
indicator values of edificator and dominant species
within plant communities (Kojic et al. 1997). For
each plant community, we have calculated the
indicator values, and then we made the scale of the
values. Soil acidity scale was: (1) slightly basic, (2)
neutral, (3) slightly acidic and (4) acidic. The scale
of soil richness in available nitrogen was as follows: (1)
oligotrophic, (2) intermediate group between
oligotrophic and mesotrophic, (3) mesotrophic and
(4) eu-mesotrophic. The temperature scale was: (1)
thermophilous, (2) intermediate group between
mesothermophilous and thermophilous, (3) mesothermophilous and (4) intermediate group between
frigothermophilous and mesothermophilous.
Data analysis
To explore how the orchid composition of the
collecting localities is influenced by the explanatory
variables, we used the outlying mean index (OMI)
analysis as described by Doledec et al. (2000). To do
that, two data sets were used; the first data set
consisted of the species data, and included orchid
taxa recorded at least twice in each collecting locality
together with their abundance (Ophrys insectifera was

excluded from the analysis because it was recorded


just once). The second data set consisted of the
explanatory variables: geographical coordinates,
altitude, habitat type, inclination, bedrock type,
light regime, soil moisture, acidity, nitrogen and
temperature.
The OMI analysis has been designed to
investigate which ecological factors are most important for community structure and to separate species
niches according to their OMI, i.e. species marginality (Doledec et al. 2000). It measures the distance
between the mean habitat conditions used by a
species and the mean habitat conditions of the
sampling area. Low values of the OMI index mean
that species have non-marginal niches, i.e. grow in
typical habitat types of a region, whereas high values
of the OMI index indicate that species have marginal
niches (grow in atypical habitat types of a region).
Furthermore, the OMI analysis provides an index of
tolerance or niche breadth. It measures the amplitude of the distribution of each species across
measured environmental conditions. Species that
get high values of species tolerance have distribution
across habitats with widely varying environmental
conditions (generalist species), and those that get low
values have distribution across habitat with limited
range of conditions (specialist species). Groups of
species were determined by partitioning applied to
the table of species scores. The centre of gravity of
each group was first computed, and each point was
associated with the closest centre of gravity.
To test the statistical significance of the marginality of each species, a random permutation test with
10,000 permutations was used.
To explore the significance in orchid populations
of serpentine, as a geological bedrock type, against
the non-serpentine, we used the non-parametric
Mann Whitney U test. Population sizes, using
census data, of each taxon recorded in serpentine
and non-serpentine localities were compared (i)

V. Djordjevic et al.

independently of the habitat type and (ii) only for the


non-forest habitats.
The OMI analysis and the species partitioning
were performed with the ADE-4 software (Thioulouse
et al. 1997), whereas Pearsons correlation coefficients
between the environmental variables and the first three
OMI axes and the MannWhitney U tests were
calculated using PASW Statistic 18 software (SPSS,
Inc., Chicago, IL, USA).

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Results
The results of the OMI analysis are presented in
Table II. In total, 25 orchid taxa showed a significant
marginality, suggesting a considerable influence of
the selected environmental variables on species
distribution. The other seven taxa that did not show
significant marginality were those recorded in a small
number of localities. The relatively low values of the
residual tolerance indicate that the selected environmental variables strongly affect the distribution of the
orchids of the study area (Table II).

The first three axes of the OMI analysis were used,


which accounted for 70.83% (43.96% for the first,
16.36% for the second and 10.52% for the third axis)
of the total explained variability. According to
Pearsons correlations, the first axis was highly and
significantly correlated with serpentine bedrock, limestone bedrock, light regime, Molinion coeruleae grasslands, nitrogen availability and acidity (20.66, 0.60,
20.59, 20.55, 0.52 and 20.51, respectively; Figure 1;
Table III). The second axis was highly and significantly
correlated with temperature, Fagus forests, light
regime, soil moisture and Festuco-Brometea grasslands
(20.67, 0.58, 20.54, 0.54 and 20.52, respectively;
Figure 1; Table III). The third axis was highly and
significantly correlated with Quercus forests, latitude,
longitude and Arrhenatheretalia elatioris grasslands
(20.67, 0.53, 20.51 and 0.51, respectively). All the
explanatory variables used in the analysis, except for
the marshes and hygrophilous meadows, were significantly correlated with at least one of the three OMI
axes, whereas many of them were significantly
correlated with all three axes (Table III).

Table II. Niche parameters of orchid species of the Valjevo Mountain Range and their substrate preferences.
Taxon

Code

Occ

Inertia

OMI (%)

T1 (%)

T2 (%)

Num

Anacamptis coriophora
Anacamptis morio
Anacamptis papilionacea
Anacamptis pyramidalis
Cephalanthera damasonium
Cephalanthera longifolia
Cephalanthera rubra
Dactylorhiza incarnata
Dactylorhiza maculata subsp. maculata
Dactylorhiza maculata subsp. transsilvanica
Dactylorhiza saccifera
Dactylorhiza sambucina
Epipactis atrorubens
Epipactis helleborine
Epipactis microphylla
Epipactis palustris
Epipactis purpurata
Gymnadenia conopsea
Himantoglossum jankae
Limodorum abortivum
Neotinea tridentata
Neotinea ustulata
Neottia nidus-avis
Neottia ovata
Ophrys insectifera
Ophrys scolopax subsp. cornuta
Orchis mascula
Orchis purpurea
Orchis simia
Platanthera bifolia
Platanthera chlorantha
Spiranthes spiralis
Traunsteinera globosa

Anaccori
Anacmori
Anacpapi
Anacpyra
Cephdama
Cephlong
Cephrubr
Dactinca
Dactmama
Dactmatr
Dactsacc
Dactsamb
Epipatro
Epiphell
Epipmicr
Epippalu
Epippurp
Gymncono
Himajank
Limoabor
Neottrid
Neotustu
Neotnidu
Neotovat
Ophrinse
Ophrscco
Orchmasc
Orchpurp
Orchsimi
Platbifo
Platchlo
Spirspir
Trauglob

22
87
2
8
15
23
6
6
3
29
13
34
5
36
5
2
2
143
2
22
8
18
43
7
1
2
2
2
6
63
2
2
4

13.14
18.57
24.51
15.25
28.46
27.88
25.49
37.37
40.18
30.55
24.87
39.11
31.99
34.59
35.47
46.83
62.62
18.60
34.31
22.78
15.44
19.46
27.52
18.29

2.76
2.59
17.65
9.21
7.05
7.99
10.73
16.52
40.10
11.92
5.56
10.65
31.35
8.65
22.25
46.32
62.20
2.24
34.03
11.85
10.02
3.27
8.67
5.26

0.31
1.31
0.01
0.76
1.82
2.40
1.69
2.15
0.00
5.01
1.01
9.48
0.00
1.89
4.10
0.00
0.01
1.21
0.01
1.43
0.12
0.43
2.14
0.49

10.07
14.68
6.85
5.27
19.59
17.48
13.07
18.70
0.08
13.62
18.30
18.98
0.64
24.05
9.12
0.51
0.40
15.15
0.27
9.49
5.30
15.77
16.71
12.54

159
0
1233 (ns)
189
1
0
120
59
2
0
29
0
0
0
1
12
1
0
83
0
23
117
0
1314 (ns)

31.75
25.20
36.67
35.07
27.04
18.06
15.67
14.39

21.53
18.55
36.38
24.27
3.48
18.04
9.27
10.39

1.80
0.35
0.01
0.74
3.60
0.00
0.21
0.04

8.42
6.30
0.29
10.06
19.95
0.02
6.19
3.96

745 (ns)
1713 (ns)
57
0
0
1162 (ns)
5630 (ns)
989 (ns)

Note: Occ, occurrences; Inertia, total variability; OMI, outlying mean index (%); T1, species tolerance (%); T2, residual tolerance (%);
Num, number of random permutations; S, serpentine; L, limestone; D, diabases and spilites.

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Niche analysis of orchids

Figure 1. Canonical weights of the environmental variables. The relative importance of each variable in the analysis is showed by the length of
the arrow, whereas the direction of the arrow indicates between-variables correlations; for the abbreviations of environmental variables, see
Table III.

The positions of orchid species along the first two


OMI axes are presented in Figure 2. The species
were partitioned in five ecological groups based on
their scores.
One group consists of species of Molinion grasslands, Nardetalia grasslands, marshes and hygrophilous meadows, mainly occurring on serpentine
geological bedrock. At the same time, these are the
species of habitats with high soil moisture and high
acidity: Dactylorhiza incarnata, D. maculata
subsp. maculata, D. maculata subsp. transsilvanica,
D. sambucina and Platanthera bifolia. In this group,
Platanthera chlorantha, which occurs in Pinus sylvestris
forests, is included as well.

The second group consists of species inhabiting


forests, as those of Fagus and/or Quercus, as well as
those of Querco-Carpinetum. The species Epipactis
purpurata grows exclusively, whereas Epipactis helleborine and Neottia nidus-avis inhabit mainly Fagus forests.
Cephalanthera damasonium and C. longifolia occur in
Fagus, Quercus, Querco-Carpinetum, Ostrya, Pinus
sylvestris and Pinus nigra forests. Cephalanthera rubra
appears in Fagus, Ostrya and Quercus forests, whereas
Orchis mascula occurs in Fagus forests and Arrhenatheretalia grasslands. The orchids of this group occur
mainly on non-serpentine geological bedrocks.
The third group consists of light-demanding
species of Festuco-Brometea grasslands and/or Arrhe-

V. Djordjevic et al.

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Table III. Pearsons correlation coefficients between the environmental variables and the first three axes of OMI analysis.
Environmental variables

Code

Latitude
Longitude
Altitude
Arrhenatheretalia elatioris grasslands
Fagus forests
Festuco-Brometea grasslands
Marshes and hygrophilous meadows
Molinion coeruleae grasslands
Nardetalia strictae grasslands
Ostrya forests
Pinus nigra forests
Pinus sylvetris forests
Querco-Carpinetum betuli forests
Quercus forests
Inclination
Diabases and spilites
Limestone
Serpentine
Light Regime
Soil moisture
Acidity
Nitrogen
Temperature

LAT
LON
ALT
Arrhenatheretalia
Fagus
Festuco-Brometea
Marshes
Molinion
Nardetalia
Ostrya
Pinus nigra
Pinus sylvetris
Querco-Carpinetum
Quercus
Inclination
Diabases
Limestone
Serpentine
Light
Moisture
Acidity
Nitrogen
Temp

OMI axis 1

OMI axis 2

OMI axis 3

0.45**
20.31**
20.49**
20.02ns
0.37**
20.30**
20.05ns
20.55**
20.23**
0.38**
0.04ns
20.15**
0.29**
0.23**
0.36**
0.22**
0.60**
20.66**
20.59**
20.40**
20.51**
0.52**
0.38**

20.32**
0.46**
20.06ns
20.24**
0.58**
20.52**
0.08ns
0.37**
0.21**
20.26**
20.07ns
0.20**
0.05ns
0.08ns
20.22**
0.39**
20.44**
0.31**
20.54**
0.54**
0.30**
0.13*
20.67**

0.53**
20.51**
0.38**
0.51**
0.28**
20.16**
0.02ns
20.03ns
0.10*
0.01ns
20.20**
20.01ns
0.07ns
20.67**
0.32**
0.14**
0.26**
20.30**
0.06ns
0.12*
0.43**
0.38**
20.33**

Note: **p , 0.01; *p , 0.05; ns, non-significant.

natheretalia elatioris grasslands: Anacamptis coriophora, A. morio, A. pyramidalis, Gymnadenia conopsea,


Neotinea tridentata, Neotinea ustulata, Neottia ovata,
Spiranthes spiralis and Traunsteinera globosa. In this
group, Epipactis atrorubens is included as well, which
inhabits Pinus nigra forests.
The fourth group includes species that occur
exclusively in limestone habitats. From these species,
Himantoglossum jankae is found exclusively in Ostrya
forests; Ophrys scolopax subsp. cornuta grows in
Festuco-Brometea grasslands and Ostrya forests;
Epipactis microphylla inhabits Ostrya and Fagus
forests; Anacamptis papilionacea grows in Arrhenatheretalia elatioris and Festuco-Brometea grasslands,
whereas Orchis simia grows in Ostrya and Quercus
forests.
The last recognized species group includes the
species that occur in habitats that are close to the
average habitat conditions of the study area. These
species are: Dactylorhiza saccifera, Epipactis palustris,
Limodorum abortivum and Orchis purpurea. Although
Epipactis palustris and Orchis purpurea have been
classified in this species group, due to their small
number of records, E. palustris should be classified in
the first group because of the ecological connection
with the other species of the marshes and hygrophilous meadows, whereas O. purpurea should be
included in the second group.
The substrate preferences of orchids are presented in Table II. The most species-rich substrate is
limestone with 25 taxa, followed by serpentine (21

taxa) and finally diabases and spilites (5 taxa).


Species and subspecies found only on non-serpentine
bedrock types were: Anacamptis papilionacea, Cephalanthera rubra, Epipactis microphylla, E. purpurata,
Himantoglossum jankae, Ophrys insectifera, O. scolopax
subsp. cornuta, Orchis mascula, O. purpurea, O. simia
and Traunsteinera globosa, whereas those found only
on serpentine were Dactylorhiza maculata
subsp. maculata, D. maculata subsp. transsilvanica,
Epipactis atrorubens, E. palustris, Neotinea tridentata,
Neottia ovata, and Platanthera chlorantha.
The Mann Whitney U test showed that only
Anacamptis morio and Gymnadenia conopsea have
statistically significantly larger populations on serpentine compared with non-serpentine bedrock
types. This was found when the comparison was
performed for all the habitats (both forest and nonforest habitats), as well as only for non-forest habitats
(grasslands and marshes; p , 0.001 in both cases).

Discussion
Specialists and generalists
Orchid taxa tend to be relatively common close to the
centre of their geographical distribution, whereas
they become rarest near their distribution edges
(Pfeifer et al. 2010). This, in part, is the result of the
special ecological requirements of each taxon.
The results of the OMI analysis (Figure 2;
Table II) allow us to separate two major categories of

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Niche analysis of orchids

Figure 2. Weighted positions of the species along the first two axes of the OMI analysis. Species with high marginality are located far from
origin, and those with low marginality are located near the origin; for the abbreviations of taxon names, see Table II.

orchid taxa. The first category consists of taxa with


narrow range of ecological requirements (specialists).
This category includes the following taxa: Epipactis
purpurata, E. palustris, E. atrorubens, Dactylorhiza
maculata subsp. maculata, Orchis purpurea, O. simia,
Himantoglossum jankae, Anacamptis papilionacea,
Ophrys scolopax subsp. cornuta, Platanthera chlorantha, and Traunsteinera globosa. These taxa have
marginal niches and narrow niche breadth (Table II).
The second category includes generalist taxa, which
are those occurring across a wide range of habitat
types with widely varying conditions. This category
includes Dactylorhiza saccifera, Gymnadenia conopsea,
Anacamptis morio, Neotinea ustulata, Neottia ovata,

Cephalanthera damasonium, C. longifolia, Epipactis


helleborine, Platanthera bifolia and Neottia nidus-avis.
The intermediate group between specialists and
generalists includes other orchid species of the study
area. Similarly, Tsiftsis et al. (2008) found that
Epipactis palustris is one of the specialists in NE
Greece, whereas generalists include Dactylorhiza
saccifera, Neottia ovata, Platanthera bifolia, Epipactis
helleborine, Cephalanthera longifolia and Neottia
nidus-avis.
Our results also reveal differences in the
separation of specialist and generalist orchids from
those from other regions. This, in particular,
concerns the orchid Platanthera chlorantha and

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V. Djordjevic et al.

other sub-Mediterranean or Mediterranean taxa


(Orchis purpurea and Himantoglossum jankae). Tsiftsis
et al. (2008) found that these three species belong to
the group of generalists in NE Greece, which may be
attributed to the Mediterranean climate and the
favourable habitat conditions in that region.
In contrast, the generalists of the study area
Cephalanthera damasonium, C. longifolia and Neottia
ovata were determined as specialists in Crete (Tsiftsis
et al. 2011). In addition, the levels of specialization of
some high-altitude orchids or those that prefer wet
habitats (Epipactis palustris, Dactylorhiza incarnata,
D. sambucina and Gymnadenia conopsea) were lower
than those determined for NE Greece (Tsiftsis et al.
2008). This may be explained by the greater influence
of humid and continental climate in the study area.
Conversely, some of the Mediterranean and subMediterranean species of the study area (Anacamptis
papilionacea, Orchis simia and Epipactis microphylla)
have higher levels of specialization than in NE Greece.
These results suggest that orchid species have a higher
level of specialization if they are more distant from the
centre of their distribution area.
Environmental gradients
The results show that the most important gradients
that govern distribution of orchids are defined by
geological bedrock, light regime and temperature.
The geological bedrock gradient (OMI axis 1)
separates serpentine and non-serpentine species.
Serpentine gradient was positively correlated with
light regime, Molinion coeruleae grasslands and acidity,
and negatively correlated with limestone gradient and
nitrogen gradient. Limestone gradient was positively
correlated with the inclination gradient.
The light regime gradient (OMI axis 1) separates
the species of open light regime, and the species of
shadow and half-shadow light condition. The habitat
types follow light regime gradient along OMI axis 1,
and separate forest species and non-forest species.
The nitrogen gradient (OMI axis 1) separates
oligotrophic and oligo-mesotrophic species from
mesotrophic and eu-mesotrophic, whereas the acidity
gradient separates species of slightly acidic to neutral
soils and species of neutral to slightly basic soils.
The temperature gradient (OMI axis 2) separates
frigo-mesothermophilous and mesothermophilous
orchid species, with species that are mesothermophilous thermophilous
and
thermophilous.
In addition, the moisture gradient (OMI axis 2)
separates species that grow on wet or moderate moist
soils and species that grow on dry or moderate moist
soils. Consequently, the first OMI axis can be
regarded as a complex gradient of geological
substrates and of the factors related to them (e.g.
acidity), as well as light regime. The second axis can

be regarded as a complex gradient of temperature


gradient and soil moisture.
The results of this study are in accordance with
the results of previous studies, which showed that the
important factors in determining the distribution
patterns and abundance of orchids are: geological
types and soil properties (Dijk et al. 1997; Tsiftsis
et al. 2008, 2012), light regime (Abernethy 2002;
Diez & Pulliam 2007), habitat types (Barbaro et al.
2003; Tsiftsis et al. 2008; Landi et al. 2009), nutrient
content (Tsiftsis et al. 2008, 2012), soil reaction
(Tsiftsis et al. 2008; Landi et al. 2009), temperature
(Barbaro et al. 2003; Blinova 2008) and soil moisture
(Diez & Pulliam 2007).
Our results do not indicate an important role of
altitude in orchid distribution in the study area,
although it has been found among the most
important factors that define the distribution of
orchids in the Vercors Natural Park (Barbaro et al.
2003), NE Greece (Tsiftsis et al. 2008), Crete
(Tsiftsis et al. 2011), and on Reunion Island
(Jacquemyn et al. 2007). Although the altitudinal
range of the localities of the study area was about
1000 m (220 1298 m), the altitude has not been
found as an important factor because most of the
records were made at a relatively small altitudinal
range (mean ^ SD: 867 ^ 245).
Importance of serpentine habitats
The results of this study demonstrate the significance
of serpentine habitats as orchid habitats, bearing in
mind the large populations of Anacamptis morio and
Gymnadenia conopsea, the occurrence of rare species
(Dactylorhiza maculata both subspecies and
Epipactis palustris), as well as the occurrence of the
populations of species which were found exclusively
on serpentine. All orchid species found on serpentine
can be considered as serpentine-facultative plants,
considering that most of them have been characterized as species of calcareous substrates (Delforge
2006; Vakhrameeva et al. 2008; GIROS 2009).
The occurrence of the orchids on serpentine
bedrock may be explained by several factors.
Primarily, it could be attributed to the specific
physico-chemical properties of serpentine soils. They
favour open vegetation with generally lower levels of
competition between plants. This situation seems to
suit the light-demanding orchids having low competitive ability. For example, Anacamptis morio is
intolerant to shade and is outcompeted by larger
growing herbs, and its level of genetic variation and
reproductive fitness is positively affected by nutrient
poor and dry conditions (Hornemann et al. 2012).
Furthermore, Dressler (1981) noted that orchids are
closer to stress-tolerator group, whereas Hagsater
and Dumont (1996) stated that they belong to the

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Niche analysis of orchids


group between ruderal and stress-tolerant plants
according to Grime (1979) theory, suggesting that
some orchid species can inhabit stressful serpentine
habitats.
Moreover, mycorrhiza probably makes orchids
tolerant to the high concentration of heavy metals.
Jurkiewicz et al. (2001) found that mycorrhizal fungi
play an important role in the separation and
detoxification of heavy metals in orchid Epipactis
atrorubens, in which the accumulation of heavy
metals and biofiltration occur in roots.
Although serpentine habitats are often referenced
as habitats with xeric conditions, wet and dry
serpentine habitats may be differentiated in the
study area. Wet serpentine habitats host orchids of
the first species group, whereas dry and semi-dry
serpentine habitats include orchids of the third
species group. Specific features of serpentine
substrates are manifested only in case of skeletal
soils. However, when the soils are moist, peaty or well
developed, their specificity is significantly reduced,
due to migration of the ions and increasing humus
layer. In those cases, the features of these soils
become similar to those of non-serpentine.
Conservation implications
In this study, the priorities for orchid conservation
are determined primarily on the basis of the results of
the niche analysis, i.e. species niche marginality and
breadth, as well as the size of their populations.
In addition, the amplitude of species geographical
distribution and conservation status of their habitats
are taken into account.
The first conservation priority should concern
Epipactis purpurata, considering that this is the single
record of this species in the central Balkans and one
of the southernmost populations in SE Europe
(Djordjevic et al. 2010). Special attention should be
given to the species growing only in limestone
habitats, especially those that inhabit the lower and
middle altitude grasslands. These habitats, even
including those at high altitudes, are strongly
influenced by human activities in the study area,
primarily by the conversion into agricultural lands.
Consequently, the populations of Anacamptis papilionacea, Orchis mascula, Ophrys scolopax
subsp. cornuta, and Traunsteinera globosa should be
expected to diminish gradually. Similarly, Kull and
Hutchings (2006) showed that orchids of calcareous
habitats have a high level of decline in Estonia and
the UK, suggesting the importance of the conservation of these habitats. Our results showed that the
limestone forests of a Tertiary relict Ostrya carpinifolia are an important orchid habitat that is not
strongly influenced by anthropogenic factors and
includes some specialists.

Another conservation priority should concern


orchid species that grow in hygrophilous grasslands
and marshes. Dactylorhiza maculata is a rare species
of southeastern Europe, whereas D. maculata
subsp. transsilvanica is an endemic of the Carpathians
and the Balkans (Vakhrameeva et al. 2008),
suggesting their high conservation values. These two
taxa were found mainly in Molinion coeruleae grasslands that are influenced by grazing, mowing, tourism
and urbanization. However, the fact that grazing has
led to the expansion of Nardus stricta in the
community Molinietum coeruleae seems favourable
for orchids because in this case, the orchids have a
large population size. In addition, the results of
Janeckova et al. (2006) showed that the regular annual
mowing, especially late in the season, is necessary for
optimal performance of many Dactylorhiza species.
The last conservation priority should concern
orchid species of serpentine Festuco-Brometea grasslands. The results showed that these grasslands are an
important orchid habitat due to the presence of many
species that are otherwise characteristic of calcareous
grasslands. In most cases, these habitats were not
altered into agricultural land and are characterized by
the absence of agricultural practices and, therefore,
have temporal and spatial continuity. This situation
seems to be favourable for the development of large
orchid populations. Silvertown et al. (1994) showed
that fertilization strongly decreased population size of
Anacamptis morio in Flanders and the Netherlands,
whereas Meekers et al. (2012) noted that agricultural
intensification, ploughing of old fields, overgrazing and
drainage are the major causes of decline of Gymnadenia
conopsea. This may explain why the populations of
these two species are significantly larger in serpentine
grasslands than in limestone habitats.
In conclusion, niche analysis showed that the
geological bedrocks (serpentine and non-serpentine)
and factors related to them were the main factors for
determination of orchid distribution in the study
area. Serpentine areas could be considered as an
orchid refuge free from the strong anthropogenic
pressure recorded in the surrounding limestone
areas. Our results confirm the general statement
that agricultural intensification is one of the main
factors that impact on orchid decline (Barbaro et al.
2003; Kull & Hutchings 2006). Future studies
should demonstrate which mechanisms orchids use
to manage the stressful serpentine conditions, and
whether the serpentine habitats constitute possible
orchid reserves for the future.
Funding
This work was supported by the Ministry of
Education, Science and Technological Development
of the Republic of Serbia [grant number 173030].

10

V. Djordjevic et al.

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