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Significance of the Apuseni Mountains (the Carpathians) in the origin and distribution of Central European earthworm fauna

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The earthworm fauna of the Apuseni Mountains is very rich in species, most of them are narrowly distributed endemics. Till now 37 Lumbricidae taxa are known from the Apuseni Mts. of which 13 occur exclusively here. This high number of local endemism is in accordance with the tectonic history of the region. In the southern part, with patchily distributed limestone areas, an accelerated insular-like speciation resulted in presence of many endemic large-bodied Octodrilus species. In the northern volcanic region other endemics such as Dendrobaena sp. nov. and Allolobophora prosselodacica were found. These species show an allopatric distribution with their Carpathian vicariant sister species D. attemsi and A. sturanyi dacidoides respectively. The origin of such Apuseni–Carpathian species pairs is possibly due to the Parathethys transgressions which repeatedly isolated the Carpathians from the Apuseni Mts. in the Tertiary period for a long time. After the final retreat of the Parathetys from the Carpathian Basin some species with larger dispersion capabilities such as Dendrobaena clujensis, Allolobophora sturanyi dacica, Allolobophora mehadiensis etc. migrated to lower altitude hilly and plain habitats forming the so called Dacian faunal element in Central Europe. Our molecular phylogenetic investigations (16S and COI sequences) corroborate this scenario. The high number of endemic species, as well as their distribution patterns places the Apuseni Mts. as a hot-spot of lumbricid earthworms’ diversification and distribution in Central Europe.
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Significance of the Apuseni Mountains (the Carpathians)
in the origin and distribution of Central European
earthworm fauna
(Oligochaeta: Lumbricidae)
Adriana Antonia Pop, Victor V. Pop, Csaba Csuzdi
Abstract. The earthworm fauna of the Apuseni Mountains is very rich in species, most of them
are narrowly distributed endemics. Till now 37 Lumbricidae taxa are known from the Apuseni
Mts. of which 13 occur exclusively here. This high number of local endemism is in accordance
with the tectonic history of the region. In the southern part, with patchily distributed limestone ar-
eas, an accelerated insular-like speciation resulted in presence of many endemic large-bodied Oc-
todrilus species. In the northern volcanic region other endemics such as Dendrobaena sp. nov.
and Allolobophora prosselodacica were found. These species show an allopatric distribution with
their Carpathian vicariant sister species D. attemsi and A. sturanyi dacidoides respectively. The
origin of such Apuseni–Carpathian species pairs is possibly due to the Parathethys transgressions
which repeatedly isolated the Carpathians from the Apuseni Mts. in the Tertiary period for a long
time. After the final retreat of the Parathetys from the Carpathian Basin some species with larger
dispersion capabilities such as Dendrobaena clujensis, Allolobophora sturanyi dacica, Allolobo-
phora mehadiensis etc. migrated to lower altitude hilly and plain habitats forming the so called
Dacian faunal element in Central Europe. Our molecular phylogenetic investigations (16S and
COI sequences) corroborate this scenario. The high number of endemic species, as well as their
distribution patterns places the Apuseni Mts. as a hot-spot of lumbricid earthworms’ diversifica-
tion and distribution in Central Europe.
Key words. Earthworms, Apuseni Mts., the Carpathians, evolution, rDNA, endemisms.
Introduction
The major hypotheses on the origin and distribution of earthworms start with the works of
MICHAELSEN (1903, 1921) who was the first to observe the great disjunctions among differ-
ent terrestrial Oligochaeta families. This is explained by the low dispersal capacity of earth-
worms due to their vulnerable morphological, physiological, and reproductive peculiarities.
Original nuclei of earthworms evolved in a place, isolated from one another, by the tectonic
events which resulted in the creation of barriers such as oceans, seas, mountain chains, etc.
Therefore, families or even genera possess isolated insular-like distribution patterns. These
peculiarities led to an unusually great number of endemic taxa. Due to the lack of fossils, all
hypotheses rely on the actual distribution data and the speculative timing of the tectonic
events with the possible evolution of different phylogenetic earthworm lineages.
There is a general agreement among the specialists that the distribution patterns of en-
demic terrestrial earthworms should be connected to some centres of the tertiary landmasses
A
dvances of the 4th International Oligochaeta Taxonomy Meeting
Zoology in the Middle East, Supplementum 2, 2010: 89–110.
ISSN 0939-7140 © Kasparek Verlag, Heidelberg
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90 Zoology in the Middle East Supplementum 2, 2010
(MICHAELSEN 1921, OMODEO 1952, SIMS 1980, MRŠIĆ 1991). Accordingly, distributional
nuclei of different earthworm taxa were suggested. The last comprehensive zoogeographical
analysis of the family Lumbricidae has recently been presented by CSUZDI & ZICSI (2003).
The present paper deals with the origin and distribution of the earthworm fauna at a
smaller regional scale in the Carpathians and Central Europe. Evidence showing possible
centres of origin as well as dispersal directions of some Octodrilus, Allolobophora and Den-
drobaena species characteristic for this area is given.
Theories on the distribution and palaeogeography of
lumbricid earthworms
With the lack of fossils, we have no, or very little data of the past distribution of earthworms.
Therefore, we have to rely only on present-day evidences. It is admitted that earthworms
spread slowly, stepwise, or are carried by water streams, probably by birds, and certainly by
humans (CAMERON et al. 2007, SCHWERT & DANCE 1979, CSUZDI & ZICSI 2003). Apart from
peregrine earthworms present in different soil types, the majority of species (especially the
endemics) are confined to certain soil types, soil parent material and vegetation (POP 1997).
For instance, some species inhabiting soils developed on limestone usually do not live in
soils developed on acid rocks. Therefore, species inhabiting the patchily distributed lime-
stone areas are isolated or confined to that area by the surrounding acid soils.
MICHAELSEN (1903) was the first to recognize the narrow belt of endemic lumbricid
earthworm species in the Northern Hemisphere limited to the regions south of the Quater-
nary ice sheet border. As southern limits, MICHAELSEN indicated natural obstacles as deserts
or seas. He also presumed that the lumbricid earthworms have a Caucasian or Transcauca-
sian origin, later spreading in the Northern Hemisphere, from Japan to Eastern North Amer-
ica. However, POP (1949) doubted MICHAELSEN’s hypothesis showing that even if in Central
and Eastern Europe the northern limit of lumbricid earthworm endemics coincides with the
southern limit of the quaternary ice-cap, this obstacle is not been proven neither for Asia nor
for North America. Moreover, the southern limits of endemic distributions are certainly not
as natural as considered by MICHAELSEN; earthworms have passed the sea barriers between
Europe and Africa, as well as passing or jumping over the large deserted areas of Asia. In
addition, there are no such obstacles to the southward distribution of the earthworms in
North America. Taking into account these facts, POP (1949) concluded that the narrow belt
of endemics is restricted to the Alpine-Carpathian-Himalaya mountain chain together with
the remnants of old mountains located among them, as well as in their close neighborhood.
Thus, the endemic lumbricid earthworms are distributed in the Alleghenies and Appalachians
and in their surroundings in North America, very probable in the Atlas Mts. and highlands of
North Africa, in the Pyrenees, Alps, Carpathians, Balkans, Caucasus, Elbrus, Himalaya and
their southern ramifications as well as in the remnants of the older Hercynian orogeny sys-
tem from Europe. Therefore, lumbricid earthworms should be considered as mountain ani-
mals, which remained living in the above-mentioned mountains, with the exception of some
forms with high adaptation potential. These last forms descended from the mountains spread-
ing on hills and plains where they could even evolve into new taxa; however, most of the
earthworm species in the lowlands are usually peregrine or widely distributed. On the con-
trary, the high altitude forms do not spread off to lower altitudes in spite of the fact that
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Oligochaeta 91
rivers, animals or man could have accidentally carried them. In POP’s opinion, this is the
proof of the mountain origin of earthworms. It is also worth mentioning that even peregrine
species, which are usually distributed in lowlands, were found at very high altitudes as well.
As we have mentioned earlier, most of the hypotheses tend to place the origin of different
earthworm genera and species in some limited areas. MICHAELSEN (1903, 1910) considered
Caucasus and Transcaucasia as centers of origin of the genera Eisenia and Dendrobaena.
Later, MICHAELSEN (1932) and ČERNOSVITOV (1932, 1935) considered the European penin-
sulas as cradles of the Lumbricidae family, namely, the Balkans for Eiseniella and the Apen-
nines and the Iberian peninsula for Allolobophora, followed by their migration to the North,
East, and West.
On the contrary, POP (1949) considered that the lumbricid earthworms have emerged from
their ancestors on the whole range, or almost the whole range, of the youngest mountain
orogenetic system, the Alpine-Carpathian-Himalayan chain and not in restricted cradles.
From these places, some species had migrated to the closely situated Hercynian and volcanic
mountains.
The presence of endemic lumbricid earthworms in eastern North America suggests that the
family emerged on the Euramerican continent, existing in the Cretaceous until the beginning
of the Eocene. During that time, the Northern Hemisphere had suffered repeated fragmenta-
tions, large areas being covered by epicontinental sea-ways. Thus, the distribution area of the
lumbricid earthworms was repeatedly fragmented and reduced. From the isolated terrestrial
areas, the earthworms migrated also to the newly raised landmasses. Consequently, the areas,
which remained sub-aerial during all of the upper Cretaceous and the Tertiary, are inhabited
today by endemic species with only a few immigrants, while the areas recently raised from
waters are populated by different faunal elements.
The present day autochthonous lumbricid earthworms area lying south of the Quaternary
ice border can be divided into four biogeographic domains (Franco-Iberian, Aegean, Tura-
nian, and North American) each with characteristic endemic genera and species (CSUZDI &
ZICSI 2003). The Apuseni Mountains are included in the Aegean domain together with
Europe from the Alps to the Ural Mts., Anatolia, the Levant, and Mesopotamia. This region
is characterized by the presence of genera Octodrilus, Octodriloides, Cernosvitovia, Fitz-
ingeria, and Dendrobaena.
Characterisation of the Apuseni Mountains
The Carpathian Mountains are a range of mountains forming an arc of roughly 1,500 km
across Central and Eastern Europe. The Carpathian chain is usually divided into three major
parts: the Western Carpathians, the Eastern Carpathians, and the Southern Carpathians. The
Carpathians differ from the other alpine-type mountains by their lower altitude, higher frag-
mentation, and presence of large leveled areas, extensive volcanic relief, and the reduced
glaciations. Different patterns of stripes showing more neotectonic movements contribute
also to the peculiarity of the Carpathian Arch (COTEŢ 1973).
Geography. Inside the Carpathian Arch, between the Transylvanian and Pannonian basins
are, as a quite distinct inner bastion, the Apuseni Mountains, known also as the Romanian
Western Carpathians (Fig. 1).
The Apuseni Mountains form an almost circular massif of 100-150 km diameter (about
18,500 km2) of relatively medium height mountains reaching a maximum elevation of
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92 Zoology in the Middle East Supplementum 2, 2010
Fig. 1. Position of the Apuseni Mts. in the Carpathian Arch (partim redrawn after MIHAILESCU 1963).
1849 m (Bihor) and 1836 m (Vladeasa). The high fragmentation of the relief imprint has a
particular “mountain island” character, with several distinct subdivisions of the massif. In
this paper only the clearly distinct central parts of the Apuseni Mts. (north of the Mures and
south of Crisul Repede rivers) are considered, without the smaller Ses and Meses Mts. (north
of Crisul Repede (Fig. 2).
The Apuseni Mts. are distinguished from the rest of the Carpathians by their lower altitude
and higher tectonic and magmatic fragmentation resulting in a tectonic and lithologic mo-
saic. This mosaic aspect is accentuated by the high number of post-tectonic Neogen basins,
the large development of karst, the presence of denudation levels in steps and the large num-
ber of epigenetic valleys. These mountains underwent intensive peneplenisation in direct
connection with lithology, climate, and repeated changes of marine and lake levels. An im-
portant feature of these mountains is the patchily distribution of Triassic and Cretaceous
limestone and dolomites, separated by acid volcanic, metamorphic or sedimentary rocks,
which lead to a patchily distribution of soils and vegetation.
Paleohistory. The Alpine-Carpathian orogeny took place during the Mesozoic-Neozoic in
two steps: (i) a series of rather important Triassic-Jurassic folding in the East, and (ii) an-
other series of Upper Cretaceous – Pliocene folding over the whole area (ŞAULEA 1967). The
second folding stage corresponds to the expansion of angiosperms and the approximate age
of lumbricid earthworms, thus supporting POP’s hypothesis on the wide range mountain
origin of lumbricid earthworms.
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Oligochaeta 93
Fig. 2. Main mountain massifs of the Apuseni Mountains (partim. redrawn after MEICHSNER 2007).
According to the global tectonics (IANOVICI et al. 1976), the Apuseni Mts. have a dual ori-
gin, namely: (i) the northern part has an autochthonous origin as a result of the collision of
the Tisza and Dacia microplates in the Upper Cretaceous, and (ii) the southern part (south of
the Aries River) is supposed to have been formed during the Cretaceous by a subduction
process of the Vardar area when the former sea basin emerged and parts of the Vardar block
rotated and shifted to the current place.
During the Upper Cretaceous, the area of the present Apuseni Mts. was covered by the
Parathethys Sea, so no lumbricid earthworms could have occurred. The land resembling the
present day Apuseni Mts. was achieved in the Sarmatian epoch (Miocene). At this time, the
land of the Apuseni Mts. had lost contact with the Central European mainland but was con-
nected to the Eastern Carpathians.
The land corresponding to the present day Apuseni Mts. suffered real insularity periods
during the Miocene, when the mountain massifs had repeatedly been separated by branches
and transgressions of the Parathetys, Sarmatian, Pannonic, or Transylvanian Lakes; the Para-
thetys finally retreated by the early Pliocene (Fig. 3).
Vegetation. At present, these mountains are covered by the belts of oak (Quercus petraea
agg. 400–600 m alt.), mixed hornbeam-beech (Carpinus betulus, Fagus sylvatica, 600–900
m alt.), beech (Fagus sylvatica, 700–1200 m alt.), mixed beech and spruce forests (F. sylva-
tica, Picea abies, 1000–1200 m alt.) and spruce forests (Picea abies, 1100–1700 m alt.), with
a narrow and fragmented subalpine belt of dwarf Pinus mugo scrubs (1750–1820 m alt.).
Pasture lands (Festuca rubra and Agrostis capillaris, at lower altitudes; Nardus stricta and
Viola declinata at higher altitudes), as well as human settlements are scattered among the
mountains and accentuate/ emphasize the insular-like distribution of biotopes.
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94 Zoology in the Middle East Supplementum 2, 2010
Fig. 3. Paleogeographic evolution of the Romanian Carpathians area. Place of the Apuseni Mts. encircled
(redrawn after VOITESTI 1935, ONCESCU 1959).
Soils. The soil cover of the Apuseni Mts. is very diversified and mosaic-like. Due to the
relative low altitude of these mountains, the high diversity of geologic substrata and the mild
climate in the altitudinal soil sequence does not follow the general Carpathian pattern. Ap-
proximately 60% of the territory is covered by brown, brown-yellowish, and luvic forest
soils, or acid brown soils; approximately 21% of total territory is covered by eubasic or
mesobasic brown soils and 7% by rendzinas. It is important to note that the eu-mesobasic
soils and the rendzinas developed on limestone and dolomites are distributed in patches
within the surrounding areas of acid soils.
These mosaics of the habitats (lithology, soils, and vegetation) have had a decisive role in
the origin and distribution of endemic species by enhancing an insular-like accelerated
speciation process. The clear relationships among earthworms – vegetation and soil, are
evidence of the long co-evolution of the lumbricid earthworm fauna with their specific habi-
tats (POP 1982, 1989, 1997).
The earthworm fauna of the Apuseni Mountains
The earthworm fauna of the Apuseni Mountains is very rich in species, most of them being
narrowly distributed endemics. So far, 37 Lumbricidae taxa are known from the Apuseni
Mts. of which 13 occur exclusively here (Table 1).
The following data prove the highly endemic character of the earthworm fauna from this
relatively small area:
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Oligochaeta 95
Table 1. List of the earthworm species (Lumbricidae) from the Apuseni Mts.
No. Taxon Distribution type Mts Apuseni
Allolobophora Eisen, 1873
1 Allolobophora chlorotica (Sav., 1826) Peregrine
2 Allolobophora leoni (Mich., 1891) Transaegean
3 Allolobophora mehadiensis oreophila V.V. Pop, 1978 Dacian endemic Strict endemic
4 Allolobophora prosellodacica Csuzdi & V. V. Pop, 2008 Dacian endemic Strict endemic
5 Allolobophora sturanyi dacica (Pop, 1938) Dacian endemic
6 Allolobophora zarandensis V. V. Pop, 1978 Dacian endemic Strict endemic
Aporrectodea Örley, 1885
7 Aporrectodea caliginosa (Sav., 1826) Peregrine
8 Aporrectodea georgii Mich., 1890 Atlanto-Medit.
9 Aporrectodea rosea (Sav., 1826) Peregrine
Dendrobaena Eisen, 1873
10 Dendrobaena attemsi (Michaelsen, 1902) Balkanic-Alpine
11 Dendrobaena byblica (Rosa, 1893) Circum-Medit.
12 Dendrobaena clujensis Pop, 1938 Dacian endemic
13 Dendrobaena octaedra (Sav., 1826) Peregrine
14 Dendrobaena sp. nov. Dacian endemic Strict endemic
Dendrodrilus Omodeo, 1956
15 Dendrodrilus rubidus rubidus (Sav., 1826) Peregrine
16 Dendrodrilus rubidus subrubicundus (Eisen, 1873) Peregrine
Eisenia Malm, 1877
17 Eisenia fetida (Sav., 1826) Peregrine
18 Eisenia spelea (Rosa, 1901) Central European
19 Eisenia lucens (Waga, 1857) Central European
Eiseniella Michaelsen, 1900
20 Eiseniella tetraedra (Sav., 1826) Peregrine
Fitzingeria Zicsi, 1978
21 Fitzingeria platyura montana (Černosvitov, 1932) Central European
Lumbricus Linnaeus, 1758
22 Lumbricus polyphemus (Fitzinger, 1833) Central European
23 Lumbricus rubellus Hoffmeister, 1843 Peregrine
24 Lumbricus terrestris Linnaeus, 1758 Peregrine
Octodrilus Omodeo, 1956
25 Octodrilus aporus V. V. Pop, 1989 Dacian endemic Strict endemic
26 Octodrilus bihariensis bihariensis V. V. Pop, 1989 Dacian endemic Strict endemic
27 Octodrilus bihariensis rendzinicola V. V. Pop, 1989 Dacian endemic Strict endemic
28 Octodrilus c. compromissus Zicsi & V. V. Pop, 1984 Dacian endemic
29 Octodrilus compromissus minimus V. V. Pop, 1989 Dacian endemic Strict endemic
30 Octodrilus exacystis exacystis (Rosa, 1896) Dacian endemic
31 Octodrilus exacystis meziadensis V. V. Pop, 1989 Dacian endemic Strict endemic
32 Octodrilus exacystis oresbius V. V. Pop, 1989 Dacian endemic Strict endemic
33 Octodrilus frivaldszkyi (Örley, 1885) Dacian endemic Strict endemic
34 Octodrilus ophiomorphus V. V. Pop, 1989 Dacian endemic Strict endemic
35 Octodrilus permagnus V. V. Pop, 1989 Dacian endemic Strict endemic
Octolasion Örley, 1885
36 Octolasion lacteum (Örley, 1881) Peregrine
Proctodrilus Zicsi, 1985
37 Proctodrilus antipai (Mich., 1891) Central European
TOTAL 17 endemics 13 strict endem.
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96 Zoology in the Middle East Supplementum 2, 2010
Table 2. Distribution types of Lumbricide species from the Apuseni Mts.
Distribution type No. %
1 Dacian endemics 17 45.9
2 Peregrine 11 29.7
3 Central European 1 13.5
4 Circum-Mediterranean 1 2.7
5 Balkanic-Alpine 1 2.7
6 Atlanto-Mediterranean 1 2.7
7 Transaegean 1 2.7
Total species 37 100
70% of the total 37 lumbricid earthworm taxa found in the Apuseni Mts. have small
distribution areas and are confined to the Carpathians or to Central Europe;
this fauna represents 51 % of the total 77 species and subspecies found in Romania;
and 39 % from the total 96 species and subspecies found in the Carpathian Basin;
17 taxa are endemics in the western part of Romania and eastern part of Hungary;
13 are strict endemics, confined to the Apuseni Mts.
The endemic species belong to the genera Octodrilus (10 taxa), Allolobophora (4 taxa),
and Dendrobaena (2 taxa). It is important to notice the absence of Cernosvitovia and Octo-
driloides species which are present by several elements in the Romanian or the Carpathian
Basin fauna.
This high number of local endemism is in accordance with the tectonic history of the re-
gion. In the southern part, with patchily distributed limestone areas an accelerated insular-
like speciation resulted in many endemic large-bodied Octodrilus species. In the northern
volcanic part, other endemics such as Dendrobaena sp. nov. and Allolobophora prosselo-
dacica were found. These species showed an allopatric distribution with their Carpathian
vicariant sister species D. attemsi and A. sturanyi dacidoides, respectively. The origin of
such Apuseni–Carpathian species pairs is possibly due to the Parathetys transgressions,
which repeatedly isolated the Carpathians from the Apuseni Mts. during the Miocene. After
final retreat of the Parathetys from the Carpathian Basin some species with larger dispersion
capabilities, such as Dendrobaena clujensis, Allolobophora sturanyi dacica, Allolobophora
mehadiensis etc., migrated to lower altitude hilly and plain habitats forming the so called
Dacian faunal element in Central Europe.
Ecological researches in the Carpathians, including the Apuseni Mts., show that the struc-
ture of the earthworm communities follows several quite well defined patterns (POP 1985,
1997). These researches also show clear relationships among the species’ structure of earth-
worm communities, vegetation, soil types, lithology, geology, and altitude. These relation-
ships are stricter for the endemic species. Thus, almost all strict endemic Octodrilus taxa are
calcophilous and confined to rendzinas and eubasic brown soils developed on limestone or
dolomite. To the contrary, the endemic Allolobophora and Dendrobaena species are distrib-
uted in acid brown soils developed on acid metamorphic or volcanic rocks. All endemic taxa
are found at relatively high altitude, in the montane and subalpine belts of the Apuseni Mts.
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Oligochaeta 97
Origin and distribution of the endemic earthworms
in the Apuseni Mts.
Accelerated insular-like speciation in Octodrilus
The presence of 11 closely related Octodrilus taxa on the relative small territory of the
Apuseni Mts. was explained by POP (1994) by a process of accelerated insular-like speci-
ation. This hypothesis was based both on factual and theoretical premises. It is widely ac-
cepted that geographical speciation means the genetic reconstruction of an animal population
during a period of spatial isolation. MAYR (1971) showed that geographical barriers may be
considered “any area inadequate for a species to inhabit it, which serves as barriers for its
distribution” and also that “vegetation belts have proved to be as important barriers as moun-
tain chains or valleys”. In MAYR’s conception, regions which could be regarded as insular
from whatever point of view always display an active speciation, while continental regions
display speciation only where physiological or climatic barriers bring about discontinuities
between populations. It is stated that any factor favoring isolation and reducing the gene-
flow accelerate speciation.
Considering that the notion of biological species defined by reproductive isolation is
hardly applicable to hermaphrodite, parthenogenetic organisms, theoretically any isolated
earthworm population may be considered as evolving distinctly; when their morphological
differences are obvious, these populations may be considered as independent species as well.
The following data should be considered as factual proofs of the process of accelerated insu-
lar-like speciation in the case of the Octodrilus species found in the Apuseni Mts.:
high stenobiontism of endemic species, confined to limestone or dolomite areas;
very low variability of morphological characters in the Octodrilus genus;
low dispersal ability of earthworms;
rather small size of population enhancing the probability of quick genetic changes;
patchily distribution of limestone and dolomite in the Apuseni Mts., isolated by larger
areas of acid rocks, leading to the insularity of habitats, i.e., soils developed on these cal-
careous “islands” are separated from each other by more acid soils developed on acid
rocks under different forest or vegetation types.
Accordingly, the insularly isolated Octodrilus populations should be considered as distinct
species. This process is also supported by the timing of the above discussed orogenetic proc-
esses and earthworm-vegetation coevolution. STEPHENSON (1930) suggested that the adap-
tive radiation in terrestrial annelids had taken place in the Cretaceous, together with the
spreading of the angiosperms. This coevolution was improved during the Tertiary and
reached the present status in the Quaternary. The endemic Octodrilus species in the Apuseni
Mts. are confined to beech and beech-hornbeam forests with rendzina or eubasic brown
forest soils developed on limestone and dolomites. A few are found under neighbouring
grassland areas, too.
It is generally accepted that all plant species of the postglacial forests were already formed
in the Tertiary. The hornbeam (Carpinus betulus) period is considered as being particular for
the South Eastern Carpathians (BOSCAIU 1987). The sub-boreal forests preceded and thus
facilitated the development of beech (Fagus sylvatica) forests.
The positive correlation among Lumbricidae communities-vegetation-soil observed nowa-
days support the idea that these major components of a terrestrial environment have had a
long coevolution (BOUCHÉ 1971, POP 1982).
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98 Zoology in the Middle East Supplementum 2, 2010
Fig. 4. Distribution of Octodrilus aporus, O. ophiomorphus and O. permagnus.
It is also accepted that many plant species survived the Ice Ages in their native place. The
existence of glacial refuges in the Balkan Peninsula was proved by SERCELIJ (1970). Such
refuges could have been situated in the Apuseni Mts., especially in the limestone areas. The
existences of glacial refuges seem to have been conditioned mostly by the characteristics of
the limestone substratum and by local relief and less by the continental thermal zonality
(BOSCAIU 1987). Therefore, it is most probable that the Octodrilus species could survive the
Quaternary ice age (which is not really proved in the Apuseni Mts.) just in the refuges with
hornbeam forests in the limestone areas.
Distribution of Octodrilus endemics
Two kinds of Octodrilus species were found in the Apuseni Mts, namely, monotypic and
polytypic taxa, which differ in their distributional patterns as well.
(1) The monotypic Octodrilus species (frivaldszkyi, aporus, permagnus, ophiomorphus)
possess rather narrow areas, strictly confined to the patchily distributed limestone islands
(Figs 4-5). Thus, O. frivaldszkyi was found only in the central karstic Bihar Mts. and in the
very closely situated Codru Moma Mts. O. aporus was found only in a limestone massif near
Abrud, O. permagnus in 3 centers and ophiomorphus in two centers in the Metaliferi and
Trascau Mountains (Fig. 5).
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Oligochaeta 99
Fig. 5. Distribution of Octodrilus compromissus and O. frivaldszkyi.
(2) The distribution of the polytypic O. exacystis, and O. compromissus, is more complex,
with several overlaps. These species are found also in the hilly parts of Transylvania while
O. compromissus also occur in the eastern part of Hungary (Fig. 5).
The subspecies of O. compromissus and O. exacystis were erected by POP (1989, 1991) on
morphological differences proved by means of numerical taxonomy and by differences in
their habitats. These species occur in very different soil types, developing on limestone and
acid rocks as well. Larger ecological valences permitted their greater distribution from the
original mountain to the hilly biotopes. From O. bihariensis the nomino-typical smaller
subspecies O. b. bihariensis was found only in grasslands, while the larger O. b. rendzinicola
was found only in forest biotopes (Fig. 6).
Geological and palinological studies (FONTUGNEC et al. 2002) show that the Apuseni Mts.
were slightly affected by the Quaternary glaciations. During the last cold and dry periods the
complex relief with a large extension of karstic zone permitted the persistence of sheltered
areas where trees of the present day forests could survive.
If we admit our hypothesis on the endemic Octodrilus speciation in the Apuseni Mts., we
could admit as well similar processes happening in comparable situations in other European
mountains, such as the Alps and Dinara Mts. These three mountain massifs with large lime-
stone areas, were born approximately at the same time with the Alpine-Carpathic orogeny,
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100 Zoology in the Middle East Supplementum 2, 2010
Fig. 6. Distribution of Octodrilus exacystis, O. b. bihariensis and O. b. rendzinicola.
and similarly hold high numbers of endemic Octodrilus and Octodriloides species, namely:
in the Apuseni Mts., 11 endemic Octodrilus taxa were described (ÖRLEY 1885, ZICSI &
POP 1984, POP 1989);
in the southern limestone Alps (Tessin, Karawankas), 15 endemic Octodriloides species
were described (ZICSI 1969, 1970, 1971, 1986);
in the Dinara karst areas about 20 endemic Octodrilus species were described (ZICSI
1986, MRŠIĆ 1991).
All these data seem to prove the existence of the three speciation centres: the limestone
area in the Apuseni Mts. (the Carpathians) and the Dinara Mts. for the genus Octodrilus and
the southern limestone Alps for the genus Octodriloides. The high resemblance among some
large Octodrilus species from the Dinara Mts., Octodrilus mima, O. tergestinus, O. sloveni-
cus and O. permagnus, Oc. ophiomorphus, O. frivaldszkyi from the Apuseni Mts. may be
due to a convergent evolution in relatively similar environments from a common Octodrilus
ancestor carried by the eastward shifting Vardar block.
Origin and distribution of Allolobophora endemics
Till now 6 Allolobophora taxa (5 species and 1 subspecies) were recorded in the Apuseni
Mts. of which 4 are Dacian endemics (Table 1). Their distribution follows the pattern
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Oligochaeta 101
Fig. 7. Distribution of Allolobophora zarandensis and A. mehadiensis oreophila.
observed in Octodrilus, namely the monotypic species are narrowly distributed endemics
recorded only in the Apuseni Mts, while the polytypic species with a larger distribution area
spread also to the lower altitude Transylvanian hilly plain and in the eastern part of the Pan-
nonian plain.
Until now, Allolobophora zarandensis had been found only in a restricted area in acid
soils under beech-hornbeam forests of the low altitude Zarand Mts. (Fig. 7). Its biogeograhic
position is quite intriguing because to its morphology highly resembles Allolobophora fer-
nandae Graff, 1957 known only from Portugal. No interjacent localities have been recorded
so far. Allolobophora mehadiensis oreophila described from the southern part of the Apuseni
Mts. (Fig. 7) is the mountain subspecies of the nominal Allolobophora mehadiensis Rosa,
1895, which is very characteristic for quite a large area in the south-western part of Roma-
nia, and the eastern parts of Hungary and Serbia. Its possible origin can be placed at the
Apuseni Mts., nevertheless, the mountains south of Mures River (Poiana Rusca, Aninei and
Semenicului Mts.) could not be totally excluded.
Allolobophora prosellodacica is a Dacian endemics found only in the northern part of the
Apuseni Mts., in the Vladeasa massif in acid brown soils developed on volcanic rocks (Fig.
8). It is highly probable that this species belongs to a common evolutionary lineage with the
closely resembling A. sturanyi dacica. Having narrower ecological valences, this species
remained in the mountains while A. s. dacica migrated to lower altitudes, too.
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102 Zoology in the Middle East Supplementum 2, 2010
Fig. 8. Distribution of Allolobophora prosellodacica and A. sturanyi dacica.
Allolobophora sturanyi dacica is a very characteristic endemic species in the Transylva-
nian hilly plain and the eastern part of the Pannonian plain. It is distributed in the southern
part of the Apuseni Mts., south of the Aries River, in the lower hornbeam and oak forest
belts (Fig. 8). We recently clarified the taxonomy of this species. It was described by POP in
1938 as a subspecies of Allolobophora dugesi, and later considered as an independent spe-
cies (BOUCHÉ & QIU 2000, CSUZDI & ZICSI 2003, POP 1978, ZICSI 1991). However, we have
now placed it as a subspecies of Allolobophora sturanyi (Rosa, 1895) (CSUZDI & POP 2008).
Origin and distribution of Dendrobaena endemics
Out of the five Dendrobaena species found till now in the Apuseni Mts, two are endemics
(Fig. 9). D. clujensis is a Dacian endemics, characteristic for the northern autochthonous part
of Apuseni Mts. both under forest and grassland vegetation. The species is found frequently
also in the hilly Transylvanian Plain to the Pannonian Plain. It is a robust species, of moun-
tain origin, which subsequently invaded different forest and grassland habitats in hilly and
even plain areas. The species probably has a common origin with the Balkanic-Alpine-
Carpathian D. alpina species group.
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Oligochaeta 103
Fig. 9. Distribution of Dendrobaena clujensis and D. sp. nov.
Dendrobaena sp. nov. belongs to the Dendrobaena alpina species group to which it was
attributed for a long time by POP et al. (2007). Its distribution is confined to the Vladeasa
massif, a northern volcanic part of the Apuseni Mts. It is very characteristic and abundant in
the higher altitude spruce forests and subalpine Pinus mugo scrubs; the species was never
found in grasslands. Recent, unpublished taxonomic revision shows that this species is a
vicariant with D. attemsi and D. alpina found in the higher altitude Carpathians.
Lumbricidae dispersion from the Apuseni Mts. towards lower altitude habitats
A majority of the lumbricid earthworm species dealt with here are narrowly distributed en-
demics, confined to the Apuseni Mountains, found in relatively small and patchily distrib-
uted areas. Only a few species, seemingly with wider ecological tolerance and higher
adaptability, spread off towards lower altitude habitats. The distribution nuclei and the pre-
sumable spreading directions of the endemic species are discussed below.
The genera Allolobophora and Dendrobaena seem to include several narrowly distributed
endemic species, or at the most, endemics with larger distribution areas in quite different
habitat types. It seems that the species included in these two genera are genetically more
tolerant to environmental conditions.
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104 Zoology in the Middle East Supplementum 2, 2010
Admitting that the majority of earthworm species have mountainous origins, or at least
mountain ancestors, it is probable that their different distribution patterns due to their nar-
rower or wider ecological tolerances are genetically determined. Some species remained
confined to high altitude biotopes; others conquered hilly or even plain biotopes as well.
Their distribution ability is reflected by some of the main morphological characteristics.
Thus, red pigmented earthworms theoretically have the advantage of being more protected
against the killing effect of solar ultraviolet radiations. Carried downstream by rivers, these
forms should have more survival chances (D. clujensis, which is also a rather robust) than
the unpigmented or slightly pigmented species (such as D. alpina, D. attemsi, and D. sp.
nov.)
Robust earthworms need deep soils, or somehow protected habitats. The large or very
large Octodrilus species were found in mountain rendzinas of eubasic brown soils developed
on limestone or dolomite. These are rather shallow, very rocky but very loose soils, evolved
under forest vegetation (mostly Carpinus betulus and Fagus sylvatica), habitats which offer
good protection, a lot of food, as well as moving-digging conditions. Absence of these large
species in the neighbouring grassland areas with the same soil types, but usually compacted
by grazing animals, shows that they do not tolerate neither compacted nor exposed soils.
Another restriction agent in grassland can be the lack of suitable leaf litter which may consti-
tute the main food-type of the large-bodied earthworms (ZICSI 1981).
Peregrine lumbricid earthworm species invasion in the Apuseni Mts.
The earthworm fauna of the Apuseni Mts., constituted in geologic times, may be threatened
by drastic changes in the natural environment due to different present-day human activities.
The clear cutting of mountain natural forests and airborne soil pollution could affect local
earthworm species, especially the endemic ones with narrower ecological valences. More
resistant peregrine species could replace local species. In the Apuseni Mts., cases of Lumbri-
cus terrestris invasions substituting endemic Dendrobaena clujensis populations have yet
been recorded (POP & POP 2006). Moreover, in highly polluted areas, an almost total disap-
pearance of earthworm fauna was observed (POP 1987). The most threatened populations are
the small populations of large Octodrilus species from limestone areas, where in the case of
clear cutting forests these species have no chances of survival.
Lumbricidae evolutionary lineages in the Apuseni Mountains
proved by molecular approach
Our molecular phylogenetic investigations (16S and COI sequences) on lumbricid earth-
worms corroborate the above presented scenarios. The high number and area patterns of
endemic species place the Apuseni Mts. as a hot-spot of lumbricid earthworm diversification
and distribution in Central Europe. As an example, some molecular phylogenetic trees show-
ing clear relations between evolutionary lineages and distribution areas in the Octodrilus and
Dendrobaena alpina group species are selected (POP et al. 2008, CSUZDI et al. 2005).
The species of the genus Octodrilus (including the Octodriloides species) can be grouped
into two major clades according to the number (2 versus 5, 6, 7 or 8) of spermathecae pairs
(POP 1989, 1991), and subdivided further into secondary lineages according to the 5, 6, 7
pairs of spermathecae. Molecular groupings in clades fit not only the morphological classes,
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Oligochaeta 105
Fig. 10. Combined 16S rDNA and COI neighbour joining tree constructed for Octodrilus, Octodriloides and
Octolasion species. 2p, 5p, 6p, 7p – lineages defined by pairs of spermathecae. Shaded species distributed in
the Carpathians and the Carpathian-basin (redrawn from CSUZDI & POP 2007a).
but also the biogeographical groupings of Octodrilus species in the Dacian and Alpine-
Balkanic and peregrine elements respectively (CSUZDI & POP 2007, POP et al. 2008)
(Fig. 10). Molecular data provided relevant information on species origin and phylogenetic
relatedness for the Dendrobaena alpina species group also (CSUZDI et al. 2005). Branching
pattern of clades in the molecular phylogenetic trees clearly distinguishes D. alpina and
separates Dendrobaena sp. nov. from the closely related D. attemsi. The clades fit the bio-
geographical grouping as well, not only in Alpine-Carpathians-Balkanic elements, but even
inside the Carpathian branch elements separating D. a. alteclitellata from the nominate sub-
species (Fig. 11).
Paleohistorical aspects
The high number of endemics and the patterns of their present day distribution, as we stated
above, prove the important role of the Apuseni Mountains in the origin and distribution of
the Central European lumbricid earthworm fauna. The timing of this process and neo-
endemic character of the Octodrilus species from the Apuseni Mountains was tentatively
explained by POP (1994) by a process of accelerated insular-like speciation. According to
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106 Zoology in the Middle East Supplementum 2, 2010
Fig. 11. Neighbour joining bootstrap tree based on 16S rDNA analysis, constructed for Dendrobaena species
from the Carpathians (from CSUZDI & POP 2007a). Dark grey shaded areas are Carpathian; light grey are
Dacian species.
this hypothesis, these Octodrilus species are relatively new and young species, evolving in
situ from a common ancestor which occurred in the former territory of the Apuseni Mts. It is
probable that after a radiant evolution by splitting of the common ancestor, each isolate had
its own “in situ” evolution. The close morphological similarities of the endemic Octodrilus
species as well their similar ecological requirements sustain the hypothesis of their origin
and evolution on small mountain areas, which suffered repeatedly isolations and amalgama-
tion during different geological periods.
The high probability of this event is also supported by the existence of other similar Octo-
drilus species groupings in the southern limestone Alps and in the Dinara Mountains, respec-
tively. The branching pattern of their morphological and evolutionary trees (see above) cor-
roborated with their distribution areas clearly showing the existence of these genetic centers,
or evolutionary hot spots in the Central European Mountains.
If the process could happen in the Octodrilus genus, we could accept the same kind of
evolution in the other genera, such as Allolobophora and Dendrobaena, with many endemic
species in this area.
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Oligochaeta 107
Regarding the timing of these processes, because of the lack of fossils, we should rely only
on the rather approximate age of their habitat. Considering the age and history of the
Apuseni Mts we should admit that the ancestors of these species could not colonize this area
before 30-40 million years ago. This relatively short time seems not to be enough for speci-
ation in earthworms (OMODEO 1952, 2000). Nevertheless, taking into account the accelerated
insular-like speciation process happening in isolated mountain areas, we could presume that
the earthworm fauna of the Apuseni Mountains had evolved more rapidly.
Conclusions
The Apuseni Mountains hold a very rich and characteristic earthworm fauna. Currently, 37
lumbricid taxa, among them 17 Dacian endemics, were recorded from this relatively small
area. The existence of many endemic earthworm species in the Apuseni Mts. in comparison
with surrounding lower altitude habitats proves the highly probable mountain origin of lum-
bricid earthworm species in Central Europe. Nearby habitats developed on Neogene depos-
its, such as the Pannonian Plain, have practically no endemic earthworms; mostly peregrine
forms, carried by human activity, are found. In the nearby hilly areas several mountain spe-
cies (sometimes reaching the fringe of the Pannonian Plain also) are found as well, showing
the most probable downhill expansion of the Dacian endemics.
Monotypic species seem to be narrowly distributed endemics, originated and confined to
higher mountain areas, while polytypic species with wider ecological tolerances also spread
to lower altitude habitats.
Spreading off the mountain earthworms to lower altitude habitats seems to be facilitated
by genetically determined morpho-ecological peculiarities. Therefore, stenobiontic species
with narrow ecological tolerances remain confined to mountain habitats and do not survive
downhill transport. For instance, the small unpigmented and fragile species of the Dendro-
baena alpina group are never found below the altitudinal belt of under the coniferous or
mixed beach-spruce forests. Red pigmented species, such as Dendrobaena clujensis, more
protected against solar radiation, seem to have more survival capabilities when accidentally
transported from mountain to lower altitude habitats enhancing the enlargement of their
distribution area.
Molecular data (16S DNA and COI) corroborate morphological and bio-geographical sce-
narios of mountain origin and subsequent radiation of several central European earthworm
lineages.
The high number of endemics, the distinct evolutionary lineages, and the distribution pat-
tern, places the Apuseni Mts. as a hot-spot of the lumbricid earthworm origin, diversification
and distribution in the central Europe.
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Author’s addresses: Adriana Antonia Pop, Institute of Zoology, Technical University Darmstadt,
Germany and Institute of Pharmacy and Molecular Biotechnology, Ruprecht Karls University, Heidel-
berg, Germany. – Victor V. Pop, Institute of Biological Research, Cluj-Napoca, Romania. – Csaba
Csuzdi, Systematic Zoology Research Group of the Hungarian Academy of Sciences and the Hungar-
ian Natural History Museum, Hungary. – E-mail: csuzdi@nhmus.hu.
Downloaded by [Csaba Csuzdi] at 01:39 01 March 2013
... Several studies indicate that "the South-Eastern Carpathians have a significantly higher proportion of endemic taxa than the Western Carpathians" (Kliment et al., 2016;Mráz and Ronikier, 2016), for some taxonomic groups is highlighted importance of Apuseni Mountains that were spatially isolated since the Tertiary from the main Carpathian arc by the Transylvanian Basin and Pannonia (Mráz and Ronikier, 2016;Pop et al., 2010). These aspects are not reflected in the HD species hotspot patterns identified in this paper. ...
... We showed that rare species contribute less to the diversity of species in individual grid cells than common or abundant species. In addition, published studies often refer to invertebrate groups that are not represented or poorly represented in annexes of the Habitats Directive, i.e. earthworms (Pop et al., 2010), aquatic insects (Bálint et al., 2011), spiders (Gajdoš et al., 2014). Thus, the species of these groups are not reflected in the results of this study. ...
... The present list of earthworms of Bosnia & Herzegovina includes 49 species, belonging to 12 genera (Table 2), with Dendrobaena being the species-richest genus (11), followed by Aporrectodea (8), Octodrilus (7) and Allolobophora (6). Following the distribution types given by several authors (Mršić 1991;Omodeo & Rota 1991;Csuzdi & Zicsi 2003;Pop et al. 2010;Csuzdi et al. 2011), our zoogeographic analysis has shown the presence of 9 different types of distribution: Peregrine, endemics (Balkan and Dacian endemics), Trans-Aegean, Central European, Balkanic-Alpine, Alpine-Dinaric, Illyric (western Balkans), Circum-Mediterranean, Atlanto-Mediterranean (Table 2). Аlmost one third of all species are either peregrines (14 species, 28.57%) or endemics (13 species, 26.53%). ...
... In Bosnia & Herzegovina, only the subspecies sturanyi dacidoides was not found. Octodrilus gradinescui (Pop, 1938) belongs to the Dacian endemics, which distribution center is considered to be the Apuseni Mts. in Romania (Pop et al. 2010). According to data present in the existing literature (Zajonc 1981;Csuzdi & Zicsi 2003;Stojanović & Milutinović, 2014), this species has also been found in Slovakia, Ukraine, Hungary and Serbia. ...
Article
In this paper, a list of the earthworm fauna of Bosnia & Herzegovina (Oligochaeta: Lumbricidae) is presented, including literature data, unpublished data from our collection and new data from the field. In this list, earthworm diversity, general ecology, their distribution and zoogeographical types are presented as well. The currently known earthworm fauna of Bosnia & Herzegovina is comprised of 49 species belonging to 12 genera, with Dendrobaena being the species-richest genus (11). Our zoogeographic analysis has shown presence of 9 different types of distribution. Аlmost one third of all species represent either peregrines (14 species, 28.57%) or endemic (13 species, 26.53%). A higher fraction of the endemic species belongs to the Allolobophora and Dendrobaena genera. With the 13 endemic and some Balkanic-Alpine (4), Alpine-Dinaric (2), Illyric (Western Balkans) (2) species, it is proven that 42.85% of the total lumbricidae fauna shows an autochthonous character. These results represent another confirmation of particularity of this fauna and prove the need for further research in this area.
... For example, the lowest species richness of testate amoeba assemblages in the northernmost location (northern forest tundra) might be related not only to the unfavorable environmental conditions but also to relatively recent (thousands of years) deglaciation of the area. It has been previously shown that the plains previously covered with glaciers are now inhabited by a few species of earthworms, many of which are cosmopolitan (Perel 1979;Kvavadze 1985;Pop et al. 2010). ...
Article
Full-text available
The relationship between species diversity and spatial scale is a central topic in spatial community ecology. Latitudinal gradient is among the core mechanisms driving biodiversity distribution on most scales. Patterns of β-diversity along latitudinal gradient have been well studied for aboveground terrestrial and marine communities, whereas soil organisms remain poorly investigated in this regard. The West Siberian Plain is a good model to address diversity scale-dependence since the latitudinal gradient does not overlap with other possible factors such as elevational or maritime. Here, we collected 111 samples following hierarchical sampling (sub-zones, ecosystem types, microhabitat and replicate samples) and performed multi-scale partitioning of β-diversity of testate amoeba assemblages as a model of study. We found that among-ecosystem β-diversity is a leading scale in testate amoeba assemblages variation. Rare species determine β-diversity at all scale levels especially in the northern regions, where rare taxa almost exclusively accounted for the diversity at the ecosystem level. β-Diversity is generally dominated by the turnover component at all scales in lower latitudes, whereas nestedness prevailed at among-ecosystem scale in higher latitudes. These findings indicate that microbial assemblages in northern latitudes are spatially homogeneous and constrained by historical drivers at larger scales, whereas in southern regions, it is dominated by the turnover component both at the microhabitat and ecosystem scales and therefore determined by recent vegetation and environmental heterogeneity. Overall, we have provided the evidence for the existence of negative latitudinal gradient for among-ecosystem β-diversity but not for among-microhabitat and among-sample β-diversity for terrestrial testate amoeba communities.
... We have tried to summarise the zoogeographical patterns of earthworms from the study area. According to the distribution types given by several authors (Omodeo 1952, Omodeo & Rota 1991, 1999, Mršić 1991, Csuzdi & Zicsi 2003, Pop et al. 2010, Csuzdi et al. 2011, the present review showed the occurrence of several zoogeographic categories. These categories are: peregrine, Central-European (inhabiting the central part of Europe), Trans-Aegean (distributed from the European Alps to the Ural Mts., including Anatolia, the Levant and Mesopotamia), Circum-Mediterranean, Atlanto-Mediterranean, Illyrian endemics (widespread in the Western Balkans), Balkanic-Alpine and Balkan endemics of wider distribution (widespread in Balkan Peninsula) and endemics of narrow distribution in a limited area of the Balkan Peninsula. ...
Article
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We have summarised the current knowledge on earthworm diversity in Kosovo and Metohia. The complete list of earthworm taxa includes 40 species and subspecies belonging to 11 genera of the family Lum-bricidae. Among them, Aporrectodea handlirschi (Rosa, 1897), Cernosvitovia paratuleskovi (Šapkarev, 1975), Cernosvitovia strumicae (Šapkarev, 1973), Cernosvitovia treskavicensis (Mršić, 1991), Dendro-baena vejdovskyi (Černosvitov, 1935) and Lumbricus meliboeus (Rosa, 1884) were registered for the first time in the study area. With respect to the zoogeographical characteristics, most of the earthworm species belong to peregrine (14 species, 35%) and endemic groups (11 species, 27.5%). The group of the endemic species belongs to the genera Dendrobaena and Cernosvitovia.
... Because the narrow road to Bigăr passes through forests and it is wet even in the summer, the earthworms can cross it and are direct victims of the road traffic. Although earthworms are not protected by law in Romania (O.U.G. 57/2007), in the Carpathian Mountains there are numerous endemic earthworm species (e.g., Pop et al., 2010;Csuzdi et al., 2011), thus they have high biogeographic importance. ...
... sylvatica, Picea abies) and spruce (P. abies) forests [97]. Additionally, we also extended our sampling to some localities in the Eastern Carpathians (T , inutul Sării, Baraolt and Liban). ...
Article
Full-text available
Cortinarius s.l. is a globally distributed agaricoid genus that has been well studied in Europe with over 1000 described species. However, the information about their taxonomy and diversity in eastern Central Europe is still limited. Only 124 species have been reported so far from Romania, based solely on morphological observations. The aim of this study was to re-examine the diversity of the genus Cortinarius s.l. in the Romanian Carpathian area, employing molecular phylogenetic and morphological methods. During intensive field work in the period 2017–2020, a total of 234 Cortinarius s.l. specimens were collected and studied with integrative taxonomic methods. For all the samples, we amplified and sequenced the nrDNA ITS region, which is the widely used official barcode marker of fungi. These sequences were compared to the data found in public databases (GenBank, UNITE, BOLD). Based on phylogenetic analyses, we identified 109 Cortinarius s.l. species, which represent 40 sections and 3 clades. Out of these species, 43 have previously been documented from Romania based on morphological identification methods, while 66 species are reported as new to the country.
... Species richness was represented by the number of species on the forests, and total abundance by the total number of individuals of each species on the forests. The categorization of earthworm taxa was based on their zoogeographic distribution, as proposed by Csuzdi and Zicsi (2003), Pop et al. (2010) and Csuzdi et al. (2011). In addition, earthworm fauna was classified into five ecological categories (epigeic, anecic and endogeic, coprophagic and hydrophilic), based on their ecological behaviors (Bouché 1972;Lee 1985;Paoletti et al. 2013). ...
Conference Paper
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The aim of the present study was to investigate the diversity and presence of ecological categories of earthworm fauna in oak and spruce forests. We sampled a total of 96 samples (48 in oak and 48 in spruce forests) during two years of fieldwork. In total, 13 earthworm species belonging to six genera were found in the studied forests. The earthworm abundance and species richness were higher in oak forests (113 individuals/9 species) than spruce forests (82 individuals/5 species). The differences in ecological categories between the studied forests were clearly evident and expected. Namely, in spruce forests our results indicate a complete absence of anecic and endo-geic species, whereas epigeic species were the most dominant. However, it seems that these patterns depend primarily on the soil type. A combination of alpha diversity index (Shannon-Weaver, Evenness, and Berger-Parker) and beta diversity (Jaccard's coefficient of similarity) were used for determining the impact of the studied forests on the earth-worm community structure. Shannon's diversity and Shannon's evenness indices were higher for oak forests, while the Berger-Parker index of dominance was lower in oak forests than spruce forests. As expected, Jaccard's index of similarity showed that the earthworm community structure was clearly separated between oak and spruce forests. Overall, our results based on these indices indicate that vegetation cover and altitude strongly influence the differences in earthworm community structure in the studied forests.
Article
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The results of our study provide new data about a Lumbricus meliboeus (Rosa 1884) distribution. It is for the first time registered for the territory of Kosovo and Metohija. The new finding place Dubrava represents the southeasternmost point of the species' natural areal. Summarizing all the data reported so far, it can be concluded that this species possesses a wider distribution than was previously thought.
Article
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This paper presents the first list of earthworm fauna of the Kopaonik National Park, a total of 16 taxa, belonging to eight genera of the family Lumbricidae. The genera with the largest number of the registered taxa are Dendrobaena and Lumbricus, while the genera Aporrectodea, Bimastos, Eisenia, Eiseniella, Octodrilus and Octolasion are represented by one species each. Also, the review of zoogeographical types and ecological categories of registered species are presented. Half of the species are peregrine, while the rest are autochthonous. Regarding ecological categories, anecic (2) and endogeic (4) species are more sensitive to high mountain environmental conditions than epigeic (12) species, which are more adapted to such conditions. Overall, our results highlight how little was previously known about the earthworm fauna in this area and emphasize the need for further collecting to better understand the hidden earthworm diversity in Kopaonik NP.
Article
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Allolobophora (sensu lato) is one of the most controversial genera in the taxonomy of Lumbricidae. Due to its poor definition, this genus is plagued by extensive taxonomic confusion, and its generic composition and internal relationships have remained uncertain, especially in species of the Balkan Peninsula. In this study, we have combined the study of morphological data and molecular phylogenetics based on five genetic markers, regions of the nuclear 28S rRNA and mitochondrial 16S rRNA, 12S rRNA, NADH dehydrogenase (ND1) and cytochrome oxidase C subunit 1 (COI), to delimit the taxonomic status of five controversial Balkanic endemic species, Allolobophora (s.l.) dofleini, Allolobophora (s.l.) serbica, Allolobophora (s.l.) strumicae, Allolobophora (s.l.) paratuleskovi and Allolobophora (s.l.) treskavicensis, sampled in the Kopaonik Mountain. Phylogenetic analyses based on our sampling of these five species recovered a well-supported clade containing the species Allolobophora (s.l.) robusta, Allolobophora (s.l.) mehadiensis mehadiensis, Allolobophora (s.l.) sturanyi dacica, Cernosvitovia rebeli and Cernosvitovia dudichi. Based on these results and previous evidence, the aforementioned Balkanic species are transferred to a redefined Cernosvitovia. We further present a revised list of all species currently included in Cernosvitovia., which includes now 21 species and subspecies taxa, 13 of them newly combined here. Serbiona Mršić & Šapkarev, 1988 is considered a junior synonym of Cernosvitovia Omodeo, 1956.