Action plan geographical scope and target audience - CIRCABC

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Action Plan for the

Conservation of the
European

Groun
d
Squirrel

Spermophilus

citellus

in the European Union


thir
d

draft

(
2
7
/
02
/20
1
3
)


















EUROPEAN COMMISSION,
201
3


THE

N2K

GROUP

European Economic Interest Group


EU Species Action Plan



Spermophil
us citellus



second draft

2


1.

Compiler
s:


Milan Janák

(Daphne/N2K Group,
Slovakia
)
,
Pavel Marhoul
(Daphne/N2K Group,
Czech Republic
)

&
Jan Matějů (Cz
ech Republic).



2.

List of contributors


Michal Adamec, State Nature Conservancy of the Slovak Republic, Slovakia

Michal Ambros, State Nature Conservancy of the Slovak Republic, Slovakia

Alexandru Iftime
,
Natural History Museum „Grigore Antipa”
, Romania

Barbara Herzig, Säugetiersammlung, Naturhistorisches Museum
Vienna
, Austria

Ilse Hoffmann
, University of Vienna, Austria

Andrzej Kepel,
Polish Society for Nature Conservation ”Salamandra”
, Poland

Yordan Koshev
,
Institute of Biodiversity and Ecosy
stem Research, B
ulgarian
A
cademy of
S
cience,
Bulgaria

Denisa L
ő
bbová,
Poznaj a chráň,
Slovakia

Mirna Mazija,
Oikon d.o.o.Institut za primijenjenu ekologiju,
Croatia

Olivér Váczi, Ministry of Rural Development, Department of Nature Conservation, Hungary

Jitka Větrovcová
,
Nature
Conservation Agency

of the Czech Republi
c
,
Czech Republic

Dionisios Youlatos, Aristotle University
o
f Thessaloniki, Greece



3.

Lifespan of plan/Reviews


2013
-

2023



4.

Recommended citation including ISBN


Janák M., Marhoul P.
,

Matějů

J.
2013. Action Plan for the Cons
ervation of the European Ground
Squirrel
Spermophilus citellus

in the European Union. European Commission.


©2013 European Communities

ISBN
978
-
92
-
79
-
08328
-
0


Reproduction is authorised provided the source is acknowledged


Cover photo:

Michal Ambros


Acknowledgements for help and support
:


Ervín Hapl (Slovakia), Rastislav Lasák (Slovak
ia), Peter Lindtner (Slovakia)


Polish Society for Nature Conservation “Salamandra”


for organizing
a

workshop
on

the
Action Plan

during the IV. European Ground Squirrel Meeting in Poland

2012
.



THE

N2K

GROUP

European Economic Interest Group


EU Species Action Plan



Spermophil
us citellus



second draft

3

CONTENTS


Preface/Introduction

................................
................................
................................
...............................

4

Summary

................................
................................
................................
................................
................

4

Species’ functions and values

................................
................................
................................
................

5

Action plan geographical scope and target audience

................................
................................
............

5

1.

Biological information and status review

................................
................................
...................

6

1.1 Description of the species

................................
................................
................................
............

6

1.2 Species life history, ecology and habitat requirements

................................
................................

7

1.3 Distribution, populations size and trends

................................
................................
...................

12

1. 4 Threats

................................
................................
................................
................................
......

19

2.

Species conservation and legal status across its geographic
range

................................
......

23

2.1 International status

................................
................................
................................
.....................

24

2.2 National status

................................
................................
................................
...........................

26

2.3
Existing conservation actions and identified priorities

................................
...............................

27

2.4 Gaps in knowledge

................................
................................
................................
.....................

30

3.

Framework for action

................................
................................
................................
...............

31

3.1 Goal

................................
................................
................................
................................
............

31

3.2 Objectives
................................
................................
................................
................................
...

31

3.3 Actions

................................
................................
................................
................................
........

33

3.4 Monitoring and review

................................
................................
................................
................

38

3.5 Other species that may benefit from the SAP

................................
................................
............

38

References:

................................
................................
................................
................................
..........

39

ANNEXES
................................
................................
................................
................................
.............

46


THE

N2K

GROUP

European Economic Interest Group


EU Species Action Plan



Spermophil
us citellus



second draft

4

Preface/Introduction


The European Ground Squirrel
,

Spermophilus citellus

is endemic to Europe
. Its
populations

bec
a
me
increasingly fragmented

and are facing serious declines across most of its range

throughout

last
decades
.
O
nly a coordinated conservation effort at the
European level may sustain the

species
viability.
With this respect this European Species Action

Plan has been prepared with the support of
the European Commission.



The aim of this
action plan

is to support the development of national or local action plans and

c
onse
rvation measures as appropriate
1
. The purposes of this
action plan

are as follows
:




To provide
up
-
to date
baseline information about species

ecology,

status

and threats



To provide scientifically
-
based recommendatio
ns to those who can promote and
support
species conservation




To establish priorities in species conservation



To provide a
common framework and f
ocus for a wide range of stakeholders


The information and
solu
tions presented
with
in this
action plan

have been

prepared
in consultation
with a group of

species
experts from
majority

of the
countries in the
European Ground Squirrel
’s

distribution range, as well as through a review of available literature.

The proposed action plan
therefore represents the best available up
-
to
-
date collective knowledge o
n

the species.


Within the frame of this
a
ction
p
lan,
an
expert
workshop has taken p
lace during the IV. European
Ground Squirrel Meeting in Poland 2012, where the a
naly
sis of information on the species, including
threats and possible conservation priorities were discussed with the experts in order
t
o define
a
conservation strategy and ide
ntify

the most important actions.


Summary


The
European Ground Squirrel,

Spermophilus citellus

is a ground dwelling rodent associated with
open non
-
forest steppe grassland habitats including the ‘cultural’ steppe of nowadays
-

the short
-
stalked grasslands

on field airports, golf courses, playgrounds etc.


The distribution range of
S. citellus

consists of two distinct parts divided by Carpathian Mountains.
The western part
extends from
southern
Poland,
through
Czech Republic
,

east of
Austria
,

through
Slovak
ia and Hungary into Pannonian part of Serbia and Croatia. The eastern part of the range
includes Transcarpathian region of Ukraine, Romania, part of Moldova
,

Bulgaria, south
-
east of
the
Former Y
u
goslav Republic of Macedonia
(
FYROM
)
, north
-
east of Greece an
d European part of
Turkey.


According to the 2008 IUCN Red List vers. 3.1, the species is considered Vulnerable, with a
decreasing population trend.
In 2007 reporting to the Habitats Directive
92/43/EC

the species has
been evaluated in unfavourable
-
bad st
atus for Alpine and Continental biogeographical regions and in
unfavourable
-
inadequate status for Mediterranean and Pannonic regions.
International group of
experts on research and
conser
vation of
S. citellus

declared in 2006 that
the species

i
s threatened

over most of its range, so coordinated conservation effort is needed for its survival
.
Dominant part of
distribution area of
S
.

citellus

belong
s

to the European Union
,

so concerned member states ha
ve

high
responsibility for the survival of the wor
l
d
’s

pop
ulation of
S. citellus
.



The most serious threats to the species reported incl
ude habitat loss and fragmentation especially in
connection with
land use
changes
which in synergy with adverse natural factors such as long winters,
floods etc. increase mortal
ity in the populations of this obligatory hibernant and in small isolated
populations quickly leed to extinction.


The overall goal of this action plan is to i
mprove conservation status of
Spermophilus citellus
to a
favourable level within the European Un
ion
. The objectives include

stopping the decline in
S. citellus




1

The EU Species Action Plans are not of a

binding nature; species action plans are drafted and implemented at the discretion
of Member States.

THE

N2K

GROUP

European Economic Interest Group


EU Species Action Plan



Spermophil
us citellus



second draft

5

populations by ensuring necessary management
of
habitat
s

at existing localities
, restoring

metapopulations
by adding new/restored habitats, creating corridors and stepping stones, supporting
p
opulations by repatriation of animals. It is also necessary to fill in the
identified gaps in knowledge

and to support
the species
conservation by public awareness activities.


In order to achieve these objectives, a list of recommended actions has been pr
epared taking

into
account the speci
fic

situation and threats in each country. The actions are divided into six

categories:
habitat management

and land use
,
species

recovery,
mapping and monitoring,
scientific research,
coordination
and funding o
f

the A
cti
on
P
lan implementation
,

and public awareness, education and
information.



Species’ functions and values


European Ground
S
quirrel
,

Spermophilus citellus

is endemic to Europe.
It is undoubtedly an important

natural element of the steppic grassland
ecosystem
.
I
n the short grass steppe habitat
S. citellus

represent
s one of the main prey
for
several
top predato
rs
lis
t
ed in Annex I of the Birds Directive,

such
as the
Imperial Eagle
Aquila heliaca
, Lesser Spotted

Eagle
Aquila pomarina
, Saker Falcon
Falco
cherrug

etc. and also other species of community importance such as the
Steppe Polecat
Mustela
eversmanii

or Marbled Polecat
Vormela peregusna
. Some rare invertebrates are specialized to co
-
existence with
S. citel
lus
, such as the coprofagous beetles
Ontophagus vitulus
,
Aphodius citellorum

feeding on excrements of

S. citellus
.

Old burrows of
S. citellus
are used by other
protected
species,
such as Green Toad
Bufo viridis

or
smooth snake

Coronella austriaca
.
In some
habitats it might be
also an important consumer of primary production able to limit spreading of some plant species,
including invasive plants, such as the
Silver
-
leaved Nightshade
Solanum elaeagnifolium
.

In line with
these, keystone species function is pr
obable
though
still not prove
n

in the case of
S. citellus.

However, at least

in some countries

S. citellus

can serve as a
n umbrella species
for

extensively used

grassland

habitats

and associated

species.

Its

usefulness

as an

umbrella

species

is
supported b
y

the
fact that

i
t is a species which can be brought to the attention of people through its at
t
ractive
appearance
and social diurnal activities above

the

ground
.




Action plan geographical scope and target audience


Within the EU this plan is intended for implementation in: Austria,
Bulgaria
,
Czech Republic,
Greece,
Hungary, Poland, Romania

and
Slovakia
.


Outside of the EU this plan is recomme
nded for implementation in:

Croatia
,

F.Y.R.

of Macedonia,
Moldova,
Serbia,

Turkey, Ukraine.


Information has
also
been compiled for

Germany.



THE

N2K

GROUP

European Economic Interest Group


EU Species Action Plan



Spermophil
us citellus



second draft

6

1.


Biological information and status review


1.1
Description of the species


Taxonomy


The European Ground Squirrel
Spermophilus citellus

has been first described as a species by Linné
as
Mus citellus

in 1766 (
L
INNAEUS
, 1766). The
valid

genus name
Spermophilus

was introduced by
C
UVIER
,
F. in
1825.



The name
Citellus
Oken, 1816 was in routine use for the genus throughout the world until
H
ERSHKOVITZ

(1949) argued that Oken’s work was invalid, and that
Spermophilus
Cuvier, 1825 was
the oldest available name for the genus.

The opinion was supported by

the International Commission
on Zoological Nomenclature (1956; Opinion 417), and has been generally adopted by American
authors.

However, some European, and especially Russian authors, continued to use
Citellus
until as
recently as 1995, although others a
dopted
Spermophilus
(
H
ARRISON

et al. 2003).


Altogether n
ine subspecies

of European Ground Squirrel
were
recognized
within its distribution area
(
overview according to
M
ATĚJŮ

et al. 2010)
:

The nominotypical subspecies
Spermophilus citellus citellus
(
L
INNAE
US
, 1766) is distributed in the
Czech Republic, Austria, Slovakia and Hungary (
R
UŽIĆ

1978).

The occurrence of
S. c. gradojevici
(
M
ARTINO

&
M
ARTINO
, 1929) is limited to lowlands in the
surroundings of Vardar River and Dojran Lake in Macedonia (
K
RYŠTUFEK

199
3).

The subspecies
S. c. karamani
(
M
ARTINO

&
M
ARTINO
, 1940) is also found only in Macedonia, namely
in the area of Karadžica Mountains, at altitudes of approximately 2,000 m, on meadows and pastures
in the Patiška River basin (
K
RYŠTUFEK

1993, 1996).

The su
bspecies
S. c. istricus
(
C
ALINESCU
, 1934
) from Romania has been described, distributed in the
Muntenia area on the left bank of Danube River (
R
UŽIĆ

1978).

Another subspecies,
S. c. laskarevi
(M
ARTINO

&
M
ARTINO
, 1940) has been described in Serbia,
specifica
lly in the southeast part of the Pannonian Lowlands, in the Banat and Syrmien areas (
R
UŽIĆ

1978).
P
EŠEV

(1955) also classifies some Bulgarian populations as belonging to this subspecies.
Compared to
S. c. citellus
,
S. c. laskarevi

differs in its smaller si
ze and shorter tail.

The validity of the following two subspecies,
S. c. martinoi
(
P
EŠEV
, 1955) and
S. c. balcanicus
(
M
ARKOV
, 1957) described in the Bulgarian Mountains has been called into question.
O
NDRIAS

(1966)
synonymizes both these subspecies with th
e subspecies
S. c. karamani
.
R
UŽIĆ

(1978) considers
S. c.
balcanicus
and
S. c. martinoi
as a single subspecies.

Based on different physical size and length of the lower jawbone, the subspecies
S. c. thracius
(
M
URSALOGLU
, 1964)

has been described in the easternmost part of its area, the

European part of
Turkey.

The subspecies
S. c. macedonicus
(
F
RAGUEDAKIS
-
T
SOLIS

et
O
NDRIAS
,

1985) has been recognized
based on immunological research into

ground squirrel populations found in the Pontokomi area, in
Greek

Macedonia (
F
RAGUEDAKIS
-
T
SOLIS

1977).

A subsequent detailed study

led to the discovery of
morphological differences and to the description

of this subspecies (
F
RAGUEDAKIS
-
T
SOLIS

&
O
NDRIAS

1985).



Nowadays

only 4 subspecies

are considered to be valid
:
S. c. citellus
,

S. c. gradojevici, S. c.
istricus
and
S. c. martinoi

(
W
ILSON
&

R
EEDER
2005
;
H
ELGEN

et al. 2009)
. However
existence of subspecies
needs

fu
r
t
her

revision according to published
information

on the genetic diversity of the species
(K
RYŠTUFEK

et al. 2009)
. For instance K
RYŠTUFEK

et al.

(2009)
described

only
three separate
S.citellus

phylogeographical lineages (south, north and Jakupica)
and suggest
treating

them
as
independent
conservation units.

K
RYŠTUFEK

(1996) found no diagnostic differences in skull
characters, ratios and colouratio
n to support formal division of
S. citellus
into subspecies
.


H
ybridization with other species
h
as not
been studie
d

yet
in

S. citellus
.


THE

N2K

GROUP

European Economic Interest Group


EU Species Action Plan



Spermophil
us citellus



second draft

7

Description


As its name
suggests
the European Ground Squirrel
Spermophilus citellus

is a ground dwelling
(living
in b
urrows)
rodent
resembling the squirrel
but with the tail far shorter and thinner and the
body
colour
of mottled ochre
-
yellow. The
body length
of
full grown

wild
animal
is

about
18
-

24 cm
(
G
RULICH

1960
,

R
UŽIĆ

1978
)

and the weight

of

adults
is

highly
variable
,
being

lowest after the hibernation

and
highest

in the late summer prior to onset of hibernation



145

to 520g (M
AT
ĚJŮ

2008
), 150 to
>
400g (M
ILLES
I

et al. 1999).
Males are significantly

heavier than fe
males (
M
ILLES
I

et al. 1999,
M
ATĚJŮ

2008
).


S. citellus

form
s

colonies

of various
sizes
.
It is a mammal with diurnal activity and an obligatory

(true)

hibernant.


1.2
Species life history, ecology and habitat requirements


Habitat requirements


S. citellus

is originally associated with open non
-
forest steppe
grassland
habitats, though it is less
adapted to typical steppe conditions than the more East
-
distributed
S. suslicus
.
S. citellus

nowadays
inhabits different types of grassland habitats,
both semi
-
natur
al and artificial,
though with strong
preference to
grasslands with permanent
short
-
stalk
vegetation
(
10
-
20

cm)

developed on different soil
types
,

from l
ight,
fine
-
grained soils

(such as
those developed
on sand)

to heavy soils and both on
deep as on shallo
w soils with presence of
soil
skeleton, but usually with good water retention and
medium aeration (
J
ANDERKOVÁ

et al. 2011)
.
Vegetation height around 20 cm
provides cover while not
obstructing sight
(
S
TRASCHIL

1972, cf.
H
OFFMANN

et al. 2008).


Current local
ities represent mainly different types of mown grassland and pastures, artificial habitats
include lawns,
playgrounds,
golf courses, river embankments (d
y
kes)
, etc.

For nowadays, grassy
airports are important refuge areas of the species (
V
ÁCZI

&
A
LTBÄCKER

1999
,
M
ATĚJŮ

et al.

2008
).
In
periods of population gradation it pervades also to sub
-
optimal habitats such as
mesoph
i
l
e
,

humid
or
temporarily flooded
grasslands, grasslands with scrubs etc. In the past it often occupied grassy
stripes along roads, railway

ramparts,
field balks and also perennial fodder crops


clovers, lucerne

(
G
RULICH

1960;
R
UŽIĆ

1978;
H
ULOVÁ

2001)
.
Apart
from

grasslands
S. citellus

usually avoids
intensively
cultivated l
and
, although it occurs also in
vineyards
, orchards and gardens
in s
ome parts
of its
range
(
S
PITZENBERGER

2001
;

E
NZINGER

et al. 2006,
H
ERZIG
-
S
TRASCHIL

2007;
H
OFFMANN

et al.
2008,
M
ATĚJŮ

et al.
2008,
20
1
0
;

Y
OULATOS

in litt.
)
.


The
analysis of the Natura 2000 database (end 2011 version) does not show a representative result
in terms of habitat classes cover on
427
S. citellus

sites

(
sites
where
S. citellus

is listed among
conservation targets or
among non
-
target
species)





in total 21.57% of the overall area is covered by
broad
-
leaved deciduous woodland
. This is obviously b
ecause of the character of Sites of Community
Importance listed in the database, which are often multi
-
purpose, with many conservation targets and
thus covering a variety of different habitat types. In any case some approximation
can be derived for
these s
ites


19.07% of the
total

area of all sites is formed by dry grasslands and steppes, other
arable land covers 8.85%,
salt marshes, salt pastures and salt steppes cover 6,43%, both humid
grasslands and mesophile grasslands and improved grasslands cover 5,4
% of the total area of SCIs
with
S. citellus
.


The
relation of
S. citellus

to Habitats Directive Annex I habitat types as estimated by local experts is
summarized below

(S


significant,
I
S


in
significant, UN


unknown/uncertain)
:


Habitat type

Country

AT

BG

CZ

EL

HU

PL

RO

SK

1340 * Inland salt meadows









1530 * Pannonic salt steppes and salt marshes

IS




S




2330 Inland dunes with open
Corynephorus

and
Agrostis

grasslands



IS






2340 * Pannonic inland dunes

UN




UN



I
S

4060 Alpine and
Boreal heaths


S







THE

N2K

GROUP

European Economic Interest Group


EU Species Action Plan



Spermophil
us citellus



second draft

8

Habitat type

Country

AT

BG

CZ

EL

HU

PL

RO

SK

4070 * Bushes with
Pinus mugo

and
Rhododendron
hirsutum

(
Mugo
-
Rhododendretum hirsuti
)


S







40A0 * Subcontinental peri
-
Pannonic scrub


IS



I
S




5210 Arborescent matorral with
Juniperus

spp.


UN







5420
Sarcopoterium spino
sum

phryganas




I
S





6110 * Rupicolous calcareous or basophilic
grasslands of the
Alysso
-
Sedion albi








S

6120 *
Xeric sand calcareous grasslands






UN



6170

Alpine and subalpine calcareous grasslands


I
S







6210 Semi
-
natural dry grasslan
ds and scrubland
facies on calcareous substrates (
Festuco
-
Brometalia
) (* important orchid sites)

S

S

UN


S

S


S

6220 * Pseudo
-
steppe with grasses and annuals
of
the
Thero
-
Brachypodietea


S







6230

* Species
-
rich
Nardus

grasslands, on silicious
substra
tes in mountain areas (and submountain
areas in Continental Europe)


UN




UN
(Ex)


S

6240
* Sub
-
Pannonic steppic grasslands

S

S

UN


S


S

I
S

6250 * Pannonic loess steppic grasslands

S

S



S


S

S

6260 * Pannonic sand steppes

S




S



S

62A0

Eastern sub
-
Mediterranean dry grasslands
(
Scorzoneratalia villosae
)


UN







62C0

* Ponto
-
Sarmatic steppes







S


62D0

Oro
-
Moesian acidophilous grasslands


S







6410
Molinia meadows on calcareous, peaty or
clayey
-
silt
-
laden soils (
Molinion caeruleae
)






UN



6510 Lowland hay meadows (
Alopecurus pratensis,
Sanguisorba officinalis
)

S

S



S

S


S

6520 Mountain hay meadows


S



I
S



I
S

91I0 * Euro
-
Siberian steppic woods with
Quercus

spp.





UN




91N0
* Pannonic inland sand dune thicket
(
Junipero
-
Populetum a
lbae
)





I
S





Ground squirrels are often described as relying on open grassland habitats. Yet, they appear to be
capable of adapting to variations in the structure of the habitat
(
R
UŽIĆ

1978)
and are likely to thrive as
long as minimal habitat requirements are fulfilled.
Apart basic requirements concerning climate
,
water
table, soil depth and plant cover

(
S
PITZENBERGER

2001)
,
particular conditions are required to sustain a
viable pop
ulation, such as minimal
habitat
size

and

adequate

resource availab
ility
(
H
OFFMANN

et al.
2008).
Studies conducted so far suggest that
short
-
stalk vegetation cover

is more important for
presence of
S. citellus

than specific vegetation types of plant specie
s at their localities

(
K
IS

et al.
1998;
G
EDEON

et al. 2011
)
.
According to
M
ATĚJŮ

et al. 201
1

t
he
vegetation of
S
.

citellus

localities in
Czech Republic
can be
is
classified in three main types characterized
by presence of
(i)
Lolium
perenne
, (ii)
Festuca rupicola

and
Poa angustifolia

and (iii)
Festuca rubra

agg.

K
OÓSZ

(unpublish
ed
data) found that
Trifolium
spp. are also important components of the vegetation of
S. citellus

habitat.
The localities in mountain environment usually represent
pastures w
ith

dominant

Nardus
stricta

(
R
UŽIĆ

1978).

According to her
,

“lowland”
S. citellus
localities
from the territory of former Yugoslavia

could b
e

characterized by presence of:

(i)
Poa bulbosa
,
Euphorbia seguieriana
,
Botriochloa
ischaemum
,
Cynodon dactylon
,
Medicago ninima
,
M. lupulina

or

(ii)
Festuca rupicola
,
Chrysopogon
gryllus
,
Stipa cap
illata
,
Paeonia tenuifolia
.



Food consumption analysis based on faeces epidermal remains shows that
Trifolium campestre, T.
arvense, T. repens, T. media, T. pratense, Medicago minima, Coronilla varia, Ononis spinosa,
Plantago lanceolata, P. media, Pimpine
lla saxifrage, Festuca
spp.,

Dactylis glomerata
and

Agropyron
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repens

re
present

important nutrit
ion

of
S. citellus

in lowland areas
(K
OÓSZ

2002;
K
OÓSZ

unpublished
data).
Also other studies
(
G
RULICH
1960,

D
ANILA
1984,

L
EŠŠOVÁ
2010
)

described
a wide variety o
f
plant

species and their parts

consumed by the
S. citellus
, ranging from leaves and seed of grasses
(Poaceae), through radix of

dandelion (
Taraxacum
sp.), plantain (
Plantago
sp.) seeds, yarrow
(
Achillea millefolium
agg.). D
ifferent species of cereals or e
ven potatoes or fallen apricots,
are

known
to be consumed by
S.

citellus

(
M
ATĚJŮ

et al. 2011)
.

H
ERZIG
-
S
TRASCHIL

(1976) recorded in colonies

of
S. citellus

in Burgenland (Austria) more than 40

foodplants


by direct observations.

As nest material of
S
. cit
ellus

in lowland
localities
nearly exclusively the leaves of fescue
(Festuca
pseudovina)

were

found
(
G
EDEON

et al. 2010).


T
hough the presence of permanent short
-
stalk grass cover

or a vegetation cover at the height, which
allows
good
on
-
site
view
for the
animal seem

to be a principal
factor
for
S. citellus

occurence,
it was
also recorded on some localities where grass cover regularly reaches height of 30 cm (
M
RLÍKOVÁ

1999). On such localities instead of trod up path
s

the

tunnels made in higher grass connec
ting single
burrows were observed (
A
MBROS

in
litt
.).

In the case of newly introduced populations extremely short
vegetation can
affect
negative
ly

on the survival of the individuals (
G
EDEON

et al 201
1
).


Yearly precipitation and temperature has been also re
ported as factors determining the suitable
habitats for
S. citellus
.
Almost all localities of
S. citellus

in the Czech

Republic and Slovakia fall in

the
zone
with boundary set
by the July isotherm of 17 °C
, in Poland (historical range)
-

of 1
8

°C
. Sites
wi
th high population density
do

not
exceed to
areas cooler than
18.5 °C
July
isotherm (
G
RULICH

1960).
G
RULICH

(l. c.) furthermore found a relation between the
S. cite
l
lus

distribution and yearly
precipitation of 500 mm. Only on some sites, the
occurrence

was

limited by yearly precipitation
of 800
mm. However, according to
H
ULOVÁ

(2001), these limits are not completely accurate.

According to
K
OSHEV

et
K
OCHEVA

(2007) the yearly precipitation on
S. citellus

localities in Bulgaria varies between
500
-
700 mm.

Data
from
the Czech Republic

and

Slovakia

(
G
RULICH

1960
) confirm this range, locally
culminating to
1000 mm

per year

(
locality Kráľova hoľa

in

Nízké Tatry Mts
.
,
S
LÁDEK

1963)
.

In Austria
data collected in 1968 to 1971 showed a distribution of
S. citellus

bordere
d by the 18 °C July isotherm
but the greater density of colonies was within the area bordered by the 20°C July isotherm. The yearly
precipitation in the area was 600 to 800 mm (
S
TRASCHIL

1972).
I
n Poland, on
the
northern edge of the
species range
,
t
he year
ly precipitation
varies
between 550 and 650 mm (historical locations)
.

According to
W
ERT

(
1932)

the overall distribution of
Spermophilus
spp
. in Europe is limited by July
isotherm 19°C

(species prefer hot and dry continental summer) and

January isotherm

C (species
prefer cold and dry continental winter).


Altitude of the
S. citellus

colonies differs across countries. For example in Bulgaria it inhabits localities
from the sea level to an altitude of 2300


2
6
00 m a.s.l. (the highest located colony

on 2592

m a.sl

is
near Belmeken peak in Rila Mts.)

(
K
OSHEV



pers. comm.
)
. In Slovakia the highest known locality of
S. citellus

was
located on the South
-
East mountainside of Kráľova skala in 1250 m a.s.l., nowadays
the highest located locality is near Telgárt village in 9
6
0 m a.s.l. (
A
MBROS

1998
).


Although
S.

citellus

lives in colonies, it is not truly a social animal. While home ran
ges are overlapping
(
T
URRINI

et al. 2008), each individual inhabits its own burrow system, apart from maternal care.

In
principle there are two types of burrows which
S. citellus

uses

during its
l
ife cycle


permanent or
nesting burrows and temporary or s
helter burrows. The temporary burrows used for a short
-
time
shelter in case of danger have usually only one exit, it is 30


40 cm long and 5
-
7 cm in diameter; it is
without branches and only widened at the terminal part to allow the animal to turn around
(
G
RULICH
,
1960,
R
UŽIĆ

1978). A permanent burrow is created by expansion of a shelter burrow and it consists of
a horizontal corridor 30
-
50 cm below the ground, which may branch to various directions and can
continue also deeper underground

(see
B
RINKMANN

1
951,
G
RULICH
, 1960, K
RATOCHVÍL

1964,
R
UŽIĆ

1978,
H
UT

and
S
CHARFF

1998 for examples).

In suitable places
S. citellus

digs a nesting burrow which
consists of several cavities 17
-
30 cm in diameter, filled with bedding

(e.g. from fescue grass
Festuca

sp.
,
G
EDE
ON

et al. 2010
)
. When preparing
for

hibernation
S. citellus

creates a new vertical corridor
with dead end just below the surface. The material dug out of this new corridor is used to plug the
entrance to the burrow and thus insulating the nesting chamber.
When
emerg
ing from the hibernation
S. citellus

penetrates the new corridor to the ground and thus opens a new entrance to the nesting
burrow

(
G
RULICH
1960
)
.


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second draft

10

After the mating period, when females moved to breeding burrows and adapted them for parturition,
individual males were observed digging at the female's burrow. In most of the cases the male was
identified as the female's previous mate, in the others the potential father was unknown. Paternal
behavior was more frequent in males with lower reproductive
success (1
-
2 mates). Parental behavior
had costs for males in terms of lower foraging time and, correspondingly, delayed body
-
mass
increase after the stressful mating period.
These data give a new insight to the variation and flexibility
of a so
-
called aso
cial species

(
H
UBER

et al.

2002
)
.


Life history


The active period of
S. citellus

starts in early March


April

(
depending on the altitude

and longitude
)
when temperature in the nesting chamber reaches 6
-
8 °C (
G
RULICH
, 1960)
.
M
ales emerge firs
t
followed by

females and young
from
previous

year

(
M
ILLESI

and
H
OFFMANN

et al. 2008,
M
ILLESI

et al.
1999a).



Fig 1. Typical annual activity cycle of
S. citellus

(
V
ÁCZI

2005).


Reproduction starts right after emerging from the hibernation. Mating lasts 20
-
25 days
(2
8

days
according to
Millesi et al. 1999b) and gestation lasts 25
-
30 days
, on average 29 days (
A
SCHAUER

et
al. 2006;
M
ILLESI

et al. 1999b)
. The freshly born young
S. citellus

are around 50 mm long with weight
of 4.7 to 6.6 g (Ružić, 1978). The number of you
ng in utero is 2
-
9 (Ružić 1978), per litter usually 3
-
7.
Litter sizes
at emergence from the natal burrow vary from 2
-
5 (
A
SCHAUER

et al. 2006), 4
-
7 (
S
TRAUSS

et al. 2007
), 3
-
10 (
H
UBER

et al. 2001), 2
-
6 (
M
ILLESI

et al. 1999b)
, and 2
-
9 (
K
RYŠTUFEK

and
V
OHRALÍK

(2005
). D
uration

of
lactation
varies among

females
, ranging from 22
-
52 days (
A
SCHAUER

et al. 2006;
M
ILLESI

et al. 1999b) and 45
-
61 days (
H
UBER

et al. 2001;
Ö
ZKURT

et al. 2005).

When young reach an
age of 17
-
21 days (when the incisors start to cut through)
the female leaves the nesting burrow and
returns only to feed the young. When they reach an age of 25
-
28 days the young leave the burrow for
the first time and start to feed on vegetation. When they reach 140
-
150 mm of body length,
at nine
weeks of age
, re
spectively (
H
OFFMANN

et al. 2004),

j
uveniles start to depart from their birth sites

aiming at digging their own burrow (or occupy an abandoned one) at a distance of 200
-
500 m from
the maternal burrow.


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second draft

11

When preparing for hibernation the animals increase t
heir body fat reserves. Pre
-
hibernation fattening
starts first in males


right after reproduction


while in females and young it starts after weaning
(
M
ATĚJŮ

et al.
20
1
0)
.
The weight of their subcutaneous

fat often
increases to
1/3 of the
ir

body weight
(
G
RULICH

1960).

Hibernation of
S.

citellus

starts between August and October.
Immergence dates
seem to vary throughout the species range: In Austria, n
on
-
reproducing females terminate surface
activity as early as at the end of July, followed by reproducing females during August. Males
immerge

into hibernation during September up to early October, while young animals start to hibernate last
(
M
ILLESI

et al. 1
999a). Similar results were reported also from the Czech Republic (
M
ATĚJŮ

20
08).
In
Hungary the adult males with highest body mass start
immergence

in the first part of August,
depending on food availability in the respective year. Non
-
reproducing females, reproducing females
and finally the young of the actual year
immer
ge

till the end of October (
V
ÁCZI

2005).
The duration of
hibernation

is highly variable and ranges from 180 to

240 days (
M
ATĚJŮ

2004).

Similar median lengths
(days) were

reported by
M
ILLESI

et al.
(
1999a
),

w
ith

females hibernat
ing

longer (228) than males
(
185), yearling males (178) and juveniles (191).
Body temperature of the animal decreases
to 19.8

22
°C at the beginning of hibernation and

continues decreasing down to 3.1

4.5 °C during deep
torpor

(
R
UŽIĆ

1978)
. Similar to other obligate hibernators,
S. ci
tellus

exhibits a typical torpor
-
arousal rhythm
during the hibernation phase (
S
TRIJKSTRA
1999,

N
ÉMETH

2010). Under non
-
natural circumstances
hibernation may be interrupted by long
-
term increase in temperature of the environment. When
temperature drops agai
n
S. citellus

falls back into lethargy. Awaking from hibernation and warming
up, respectively, is highly energy
-
demanding and exhausts the body fat of the hibernating animal.
In
average they cause 86% of energy costs during the hibernation season

(
S
TRIJKST
RA

1999)
.
If
repeated too frequently it may cause its death.


According to
G
RULICH

(l. c.) and
R
UŽIĆ

(1978), the maximum
life span

of the
S. citellus

is 3 to 5 years.
Life span in the field was
four years for males and six years for females (
H
OFFMANN

et a
l. 2003)
, and
may be more than nine years under laboratory conditions (
A
NDJUS

et al
.

2000,

Ž
IVADINOVIĆ

and
A
NDJUS

1996
). While most females

ar
e

sexually mature after
their
first hibernation
,
timing of puberty in
males is facultative (
M
ILLESI

et al. 1998),
becoming sexually active either as yearlings or as 2
-
year
olds (
M
ILLESI

et al. 1999a)
.



Plants represent at least 80% of the diet of
S. citellus

and it includes leafs, shoots, flowers, fruits and
stems of various grasses and herbs
(see also above)
. The an
imal food includes insects, especially
suborders
Caelifera
,
Ensifera
,
Lepidoptera
,

Coleoptera

and
Hymenoptera
. In the food of pregnant
females,

the animal component may represent 1/3 to 2/3 of the total food volume,

while in males it
reaches a maximum of 1
/5 (
G
RULICH

1960).

Remains of
Saltatoria

and
Formicidae

were also identified
in gut contents and droppings (
H
ERZIG
-
S
TRASCHIL

1976).
Vertebrates are found occassionally in the
diet

of
S. citellus
. They are represented especially by the rodents
Microtus arva
lis
,
Mus
spicileg
us
, the
insectivores
Talpa europaea
,
Sorex araneus
,

young of the hedgehog
Erinaceus concolor
,

eggs of
ground
-
nesting

birds (
D
ANILA

1989
,
H
ERZIG
-
S
TRASCHIL

1976,
V
ÁCZI

2005
)

as well as reptiles
Lacerta

sp.
(
P
ASPALEV

et
P
ESHEV

1957,
S
TRAKA

19
61),
Anguis fragilis
,
Coronella austriaca

(
W
OJTASZYN

et al.
2012).


Home ranges may exceed 1 ha in adult males throughout the year (
H
OFFMANN

in litt.), but usually
extend between >0.1 and <0.4 ha area, depending on reproductive state, sex, age, population

density
and habitat attributes (
H
UBER

1996,

T
URRINI

et al. 2008). Correspondingly, h
ome
-
range span
s range
from 39 to 338 m (
T
URRINI

et al. 2008).


According to
S
UTHERLAND

et al.
(
2000
),

a
llometric

relationships between body

mass

and

dispersal

distance
re
sult in
<1 km

f
or

S.
-
citellus
.
However, dispersal is possible
when

the population is growing
and environments are suitable (
H
ULOVÁ

and
S
EDLÁČEK

2008
)
.

Natal

dispers
al

occurs
when
juveniles
start to
explore their surroundings a
t nine weeks of age, depart
ing

up to approximately 350 metres
from the maternal burrow
, which may result in establishing a new home range (
H
OFFMANN

et al.
2004)
.
In
a nearly natural habitat in Austria
, minimum home
-
range span was 71 m in juveniles and 39
m in nonjuveniles,

and maximum
home
-
range span was 338 m in juveniles and 203 m in
nonjuveniles. In
a strongly altered

alfalfa meadow, home
-
range span ranged between 40 m and 136
m in juveniles and between

45 m and 93 m in nonjuveniles

(
T
URRINI

et al. 2008)
.

D
ispersal
of young
males
up
to 1

2 km cannot be excluded

either
(
R
UZIĆ

1978;

M
ATĚJŮ

unpubl.).

Scarce

evidence
suggests that also juvenile females and yearling males may cover distances between 350 and 750 m
(
H
OFFMANN

et al. 2004,
T
URRINI

et al. 2008).
In Bulgaria p
robably the habitat
s around rivers
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us citellus



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represented dispersal corridors for the species. The average distance
between

active
S. citellus

colonies
is

3.25±1.4 km and 5.95±2.37 km of

inactive ones (
K
OSHEV

2009).


Species
is a
carrier
for

number of zoonoses such as plague (
Yersinia
pestis
) (
P
ESHEV

1955).
G
ENOV

(1984) reported 9 species of parasitic helminths, two of which
found
only
in
the region of town Pirdop.
S
TEFANOV

et al
. (2001) examined 67 individuals in the period 1998
-
2001 from seven locations in
Bulgaria

for endoparasites a
nd found
4 helminth species and a new parasite f
or

S. citellus



Ctenotaenia

marmotae



present in

mountain populations of the species (
S
TEFANOV

et al. 2001).


The most frequent ectoparasites of the
S. citellus

are fleas (Siphonaptera), especially the foll
owing
species:
Citellophilus simplex, C. martinoi, Ctenophthalmus orientalis, Neopsylla sctosa
and
occasionally
Ctenophthalmus assimilis

(see
e.g.

C
YPRICH

1986
)
. Some mites also parasitize
S.
citellus
such as
Hirstionyssus criceti
and
Haemogamassus citelli
. Of ticks, only the species
Ixodes
laguri
has been found in Czech and Slovak
S. citellus

populations (
G
RULICH

1960). Data in the
literature on endoparasites are sporadic.
G
RULICH

(l. c.) mentions the intestinal parasites
Hymenolepis
fraterna
and
Monilifor
mis moniliformis
found in large numbers in infertile females.


G
OLEMANSKY
,
K
OSHEV

(
2007, 2009) examined
faecal samples collected from 109
individuals of
S.
citellus

from 10 different localities in Bulgaria

for
a presence of
Eucoccidians:
Eimeria citelli

K
artchner
& Becker, 1930,
E. callospermophilli

Henry, 1932,
E. cynomysis

Andrews, 1928 and
Klossia

sp.

The
results
showed that 96 samples were positive for presence of coccidian oocysts, an infestation
percentage of 88.05%.


1.3
Distribution, population si
ze and trends


Species range


Spermophilus citellus

is
distributed

throughout

central and south
-
eastern Europe, where it occurs
approximately south of 50
°

northern
la
titude
.
The species range reached its histor
ical maximum
probably in the warmer period of last glacial period würm (interstadial würm 1
-
2) when it extended
from the Baltic Sea and the territories of
current

Britain in the north to Italy and Bulgaria in the south. It
is assumed
that
the current centr
al
-
European distribution is a result of expansion conditioned by
human activities in historical times. The
current
species
range is divided in two by
the
Carpathian
M
ountains. The north
-
western p
a
rt extends through
Poland,
the Czech Republic, Slovakia,
Aus
tria,
Hungary, northern Serbia and western Romania, whilst the south
-
eastern p
art

extends from
eas
tern
Serbia,
Macedonia and
northern
Greece
through Bulgaria
,

southern
and western
Romania to
European
Turk
ey
, Moldova and Ukraine
.

The distribution of
S. cite
llus

in most of its range is however
disjunctive

(
K
RYŠTUFEK

1999).

In
the
20
th

century the species has become extinct
in peripheral parts
of its range in Germany
(
F
EILER

1988
,

H
AUER
et al.

2009
) and Poland (
at the turn of 1970s and 1980s
)
although the spec
ies has recently been reintroduced

here.


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second draft

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Map
1


Spermophilu
s
citellus

range. (Data source:
IUCN

20
08
2
)



EU member
state
s with current occur
r
ence


Austria

The recent distribution of European ground squirrels in Aus
tria is confined to about 13,000 km²

gross
of the continental area (Pannonian zone) in the country’s easternmost states (Burgenland, Lower
Austria, Vienna), which is equi
valent to the south
-
western pe
riphery of the species’ geo
graphic range.
The area of occurrence is limited by the Bohemi
an Massif in the northwest (crystalline and
metamorphic rocks like granite, gneiss, slate etc.), and the easternmost foothills of the Alps in the
southwest and south (limestone and crystalline, respectively).


The first semiquantitative information on the
distribution of
S. citellus

in Austria derives from the time
between 1968 till 1972 (
S
TRASCHIL
1972). During following years further colonies were discovered
while others disappeared especially around 1970 in Burgenland when areas of large colonies were
tu
rned into intensive agriculture or building areas. The information was stored in a data bank at the
Mammal Collection at the Museum of Natural History in Vienna
. In 2001
,

S
PITZENBERGER

pu
b
lished a
map containing this

information. In 2006 (
E
NZINGER

et al. 2
006) reported in detail on distribution,
habitats and status of
S. citellus

in Lower Austria,
H
ERZIG
-
S
TRASCHIL
did the same for the Burgenland
in 2007. Since then a volunteer monitoring was established in Lower Austria and a scientific
monitoring is going
on in Burgenland. The Viennese colonies
of
S. citellus

were
last
mapped
once
in



2

IUCN (International Union for Conservation of Nature) 2008. Spermophilus citellus. In: IUCN 2011. IUCN Red List of
Threatened Species. Version 2012.1 (
http://maps.iucnredlist.org/map.html?id=20472
)


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the South

(
H
OFFMANN

2002
) and once in the North (
H
OFFMANN

200
5
).
Since 2011, a few hectares of
the distribution range

in the Viennese North have been monitored (
H
OFFMANN

2011,

H
OFFMANN

et al.

2012
).


In
the
frame of her research projekt

(
www.fwf.ac.at/en/abstracts/
,
www.fwf.ac.at/
en/finals/
), I.E.
H
OFFMANN
launched a home page (
www.univie.ac.at/ziesel
) where sightings and other occur
r
ences of
S. citellus

can be reported, and
established a data set based on these reports. Up to

now, the data
base contains over 300 notifications
, which were used for model
ing the potential distribution of
S.
citellus

in Europe
(
H
EITHER

et

B
LOMENKAMP

2012).


At present times there are altogether more than 280 known sites of
S. citellus

with about 1
5.000


30.000 individuals.

Most of the Austrian ground
-
squirrel sites are in agricultural areas, some on artificial surfaces like golf
courses and parks, and an evanescent minority in (semi
-
)natural areas. Virtually the whole area of
occurrence is fragmen
ted, which is not surprising as Austria has the second highest density of roads
per km² in Europe. Recent findings suggest that complex, patchy cultivation patterns

represent a
considerable part of available ground
-
squirrel habitat in Austria (
H
OFFMANN

in
litt
.). Conservation
measures should be aimed at promoting and preserving agricultural mosaics, and connecting such
heterogeneous habitat clusters with dispersal corridors.


Bulgaria

There
is no comprehensive overview of the overall past and current
S. cit
ellus

distribution in the
country available. The data are available only from different parts of the country, collected in different
periods

and
by
using different methods
, therefore only

a

comparison of some regional populations
'

status
is possible.
K
OSHE
V

(2008) established that the percent
age

of extinct colonies was highest in
the
Sofia field (58%) and
in m
ountain region
(
32%
)
. There are
also
extinct
S. citellus

colonies around
south
-
western corner of Bulgaria.

The
study
of
S
TEFANOV

et

M
ARKOVA

(
2009) est
ablished that after
1985 the species
ha
s
been
found
only on
15
localiti
es in Sofia valley (38.5% of the total number of
territories confirmed for the region).
K
OSHEV

(
2009) carried out
assessment of distribution of the
species in Trakia valley and he found

out
that 18% of
all known
colonies p
e
r
ish
ed.


K
OSHEV

(2008) established that the
distribution of the species in Bulgaria in the period
1990
-
2008
include
d

275 sites covering 212 UTM squares (10x10km
2
) or 16.9% of
the
country
's territory, but
these
are prob
ably underestimated (
K
OSHEV

unpubl.).



Czech Republic

A
n

integrated image of the distribution of
S. citellus

within
Czech Republic

was provided by
G
RULICH

(1960).

Based on a questionnaire project in 1948 and 1949, field investigations

and verifying of
the

questionnaire data from 1948 to 1953, th
e overall distribution of the species in former
Czechoslovakia

was established
. At that time

S. citellus

was widely

distributed almost all over the Bohemian basin
with the exception of

the South Bohemian basins, the

Brdy Mts
.

area and part of the

Českomoravská
vysočina Highlands.
It

was not

found in border mountain regions except for part of the Krušné hory

M
ts
. In Moravia,
S. citellus

was found especially

in the south and central parts, while
it
was missing
completely in the

Ostrava Region. During

1947

1952, the population reached its peak

in
Czech lands

and the ground squirrel was even considered to be a

significant field pest (
G
RULICH

1960).


A
pproximately
s
ince the beginning of the 1960s a gradual decline o
f
this species’ numbers ha
s

been
record
ed, similarly as it occurred in surrounding countries


Germany, Poland and Slovakia
.

In 1972,
the presence of
S. citellus

was confirmed in 330 map squares

(
A
NDĚRA

et
H
ANZAL

1995) while in 2007
it has been recorded only in 27 map squares
representing in total
34 more or less isolated localities,
distributed irregularly

throughout the entire territory of the Czech Republic except East

Bohemia and
North Moravia

(AOPK ČR,
M
ATĚJŮ

et al. 2010).


C
urrent (2011) population size

represents
33 localities/colonies

with
3700


3900 individuals

estimated in total, but only at
11 localities
the
population
is
estimate
d

at

100 individuals or more

(
M
ATĚJŮ

et

S
CHNITZEROVÁ

201
1
).


THE

N2K

GROUP

European Economic Interest Group


EU Species Action Plan



Spermophil
us citellus



second draft

15

Greece

Historically, the species was ranging continuously and according to available

habitats from western
Macedonia to Thrace, with the southernmost range

reaching the prefecture of Pieria in central

Macedonia. Currently, the species

occurs in three

different and possibly disjoint areas in Greece: (a)
western

Macedonia (prefecture of Kozani), (b) central Macedonia (prefectures of

Imathia, Pella
,
Pieria, Thessaloniki, Kilkis)

and (c) Thrace (prefectures of

Rodopi, Evros). There might be isolated
popul
ation enclaves in the adjacent

areas between the confirmed ones, but this remains to be proven
in the field.


Total population size is difficult to estimate as densities vary depending on

habitats and areas, and
therefore extrapolating could be very errone
ous. Thus

far, no survey to this end has been ever
performed in Greece. A very

approximate estimate of covered area by the current population would
be

around 4319.1 km²

(
Y
OULATOS

in litt)
.


Hungary

No country
-
wide data on historical range
are available,
bu
t indirect indications show that there was a
drastic population collapse around the middle of the last century. National monitoring data
,

which
are
available since 2000
,

show relative stability
of the population
with high asynchronous local fluctuation
and

threatening local extinctions.
There is an on
-
going work on
updating
of map of the c
urrent
distribution.

Population size
indicated in the Habitats Directive
Art
icle

17 reporting
in 2007
is 156
-
434
(min
-
max number of) localities.
P
opulations are highly iso
lated from each other

(
V
ÁCZI

in litt)
.


Poland

In
Poland, the
species became extinct in
late

1970
s

or beginning of 1980s

(
M
ECZYNSKI

1985
)
,
but
the
historical range extended approximately in the Odra
R
iver valley in

south
-
western part of the country.
In las
t few years
a

s
uccessful

repatriat
ion was
implemented to several localities
near
Kamień Śląski
,
Głębowice and Jakubowo Lubińskie. The national wild population according to the monitoring in 2012
is estimated at 850

900 individuals (
K
OŃCZAK

et al.
2012
).

For historical distribution see
J
ACOBI

(1902) and
W
ERTH

(1932).


Romania

Historica
l range includes all plain and low hill areas, except for the intra
-
Carpathian basin: eastern
and southern Moldova, entire Dobroudja, eastern and southern Wallachia, the western plain of Banat
and Crişana (along the western border of Romania with Serbia an
d Hungary).

The current
distribution
is on a large
extent

identical with the
historical
range

but it is more fragmented and also some major
gaps occurred as a consequence of local extinction (
I
FTIME

in litt.).


According to distribution surveys completed

mainly in
2006
-
2009, in the Pannonian part of the country
S. citellus

was recorded in 79 UTM grids of 10x10 km. The localities and thus the colonies are
mostly
isolated, which represents a serious threat for
S. citellus

populations. Extinction has been pro
ven in
few cases and suspected for many more. The Balkan population of
S. citellus

(Oltenia, Muntenia,
Moldavia and Dobrudja regions) has been surveyed in 2009
-
2010 and the species was present in 379
UTM grids, with relatively large populations in Dobrudja

and some parts of Moldavia
,

but with

considerable gaps in the southern part of the country (
H
EGYELI

et al. 2012).


Slovakia

Current knowledge on the distribution of
S. citellus

in Slovakia
is based on
mapping of the species
since 1996

(
A
MBROS

2008)
.
Also
literature data as well as unpublished information from other
scientific projects (for example epidemiological)
were used to create a distribution

map and detect the
present state of the population. Between 1996 and 2008
altogether
120 localities
were reco
rded
in the
country. Visits of localities
of
S
. citellus

listed in older literature showed that majority
(87%)
of the
se

had been altered and the species did not occur there anymore.
Some
localities where
S. citellus

was
still
register
ed

were in different s
uccession stages as a consequence of change
d

farming practices or
land use and extinction of these local populations
may

happen

within 3 or 4 years.


On the basis of literature data
the
distribution of
S
. citellus

in Slovakia

till 1970 and from 1971
-
1995

was reconstructed
.
When c
omparing the data
from field mapping
with the
literature data
it can be
concluded that the species’ range in Slovakia has lost its continuous pattern since 1950 and has
THE

N2K

GROUP

European Economic Interest Group


EU Species Action Plan



Spermophil
us citellus



second draft

16

become fragmented into several more or less separated segments
. Continuous mapping with the
application of monitoring elements
providing
further observation of
S
. citellus

population shows
progressing isolation of the existing colonies with continuing
fragmentation

of the species’ range in
Slovakia. The situation gra
dually gets into a state when immediate action is needed to preserve the
S
.
citellus

in the country

(
A
MBROS
et

A
DAMEC

in litt)
.


EU member states with extinct populations


Germany


According to T
HALLWITZ

(1898) and
J
ACOBI

(1902)

at the end of 19th century
S.
citellus

occurred all
over Silesia up to the border of Brandenburg in the North (Silesia west of the River Nei
sse now
belongs to Germany, e.g.

the area of Oberlausitz)
.

I
n Saxony
S. citellus
occurred in
east E
rzgebirge
Mts. next to border with Bohemia in

a limited area ca. 10 km
2

(H
AUER

et al. 2009). T
HALLWITZ

(1898)
and
J
ACOBI

(1902) named localities

Olsen, Oelsengrund,

Breitenau, Liebenau, Lauenstein and
Hellendorf
respectively Markersbach and Lauenstein
.

Werth (1932) add to this list also localities

rstenwalde
,

Fürstenau
, Hartmannsbach

and Zuschendorf by Pirna
.
Distribution of
S. citellus
in
Silesia in 1920s was described by Wert (1932), who provide detailed description of localities and map
of distribution.


Until 1933,
S. citellus

had disappeared f
rom Reichenbach, Zittau and Bischofswerda (Saxonian
Oberlausitz), and until 1944 from Görlitz, Rothenburg and Hoyerswerda (Silesian Oberlausitz;
B
RINKMANN

1951).

Decline of
S.
citellus

population in Saxony was first recorded in 1930s and the last
populatio
n by Geising persisted for sure until the 1968, possibly until the 1980s
(
F
E
I
LE
R

1988
,
H
AUER

et al. 2009).



Non
-
EU states with recent populations


F
.
Y
.
R
. of
Macedonia

The Jakupica phylogeographic lineage
(also referred to as
S. citellus karamani
)
of centr
al Macedonia
is the smallest of the three major evolutionary lines of
S. citellus
. This lineage is an important reservoir
of within
-
species diversity and should be regarded as an independent unit for conservation
management purposes. It is endemic to Mt
.

J
akupica, where it lives in mountain pastures at 1,500

2,250 m altitude. The total area occupied by
S. citellus

(884 ha) is fragmented and 94% of individuals
occur in four colonies. Densities (0.8

5.5 adults ha

1
) are lower than those reported elsewhere for

the
species, with the total population probably <2,000 adults. One large colony, reportedly of
app
. 1,000
animal
s, was decimated in 2007 by a catastrophic fire and had still not recovered by 2010

(
K
RYŠTUFEK

et al. 2012)
.


Lowlands of the River Vardar and
the Dojran region of south
-
eastern Macedonia are inhabited by
different subspecies


Spermophilus citellus gradojevici
. In 2010 the population was surveyed by
H
ABERL

et al. (2012). Altogether 70 settlements in 15 colonies were mapped, all patchily distribu
ted
and imbedded between fields and vi
neyards. These could be attributed to four distinct populations,
more or less isolated by topographic barriers

(
H
ABERL

et al. 2012)
.


Serbia

In Serbia, the species is distributed in Vojvodina region what represents the

southernmost part of its
distribution in the Pannonian lowland.
S. citellus

populations in Vojvodina are highly fragmented, but
their genetic variation is still higher than in peripheral populations in Central Europe

(
Ć
OSIĆ

et al
.

2013).

I
n the period
2004

2008
Ć
IROVIĆ

et al.
(2008) had
monitor
ed

the population of
S. citellus

in
Serbia
at the localities: Neradin, Krušedol and Banatska Palanka.
A
bundance and density of
the local
populations were determined by census meth
od on experimental 50×50 m sample plots. The
determined abundance per plot was then recalculated for the total surface area of each habitat,
resulting in the total abundance of the

population. Population density
o
f
S. citellus

showed
pronounced fluctuation
s, from only 4 to 88 individuals/ha. The mean value of density at all three
localities was 41.6 individuals/ha. In spite of
these
fluctuations at the study sites,
authors consider
these populations viable,
though pointing that
future survival of th
e

specie
s in Serbia is exclusively
determined by conservation of
i
t
s

natural habitats.


THE

N2K

GROUP

European Economic Interest Group


EU Species Action Plan



Spermophil
us citellus



second draft

17


Non
-
EU states with extinct populations

or unclear status


Croatia

In the past,
S. citellus

in
habited

the
eastern
most

part of

Croatia

where occurred in high
population

den
s
itie
s
.

It

inhabited pastures,

stepp
e

grasslands
, high sloped river banks,

house backyards etc.
Since the beginning of the 1980s,
degradation
,

fragmentation
,

isolation and succession of stepp
e

habitats,
similar
as in the rest of Europe,
led to a significant dec
line of
the species
population size. It

persi
s
ted

only
o
n individual, isolated l
ocalities in the Baranja region

and around Osijek, Vukovar and
Ilok
,

until the beginning of the Homeland War

in

the
1990s
.

During the war,
th
o
se areas were
abandoned by the loc
al
population

and the grasslands and pastures
were
left to
overgrow
.
It seems
that this period lead the species to extinction. During 2010 and 2011,
intensive efforts
were

made to
reveal live individuals or any other signs of their possible presence. Resea
rch involved interviews with
local
inhabita
n
ts
, especially shepherds, detailed research of localities known to be inhabited by
S.
citellus

in the past

and preliminary habitat analyses.
On s
ome sites
the
steppe vegetation
had
recovered
as they are now frequ
ently used as pastures or are traditionally burned once a year (mostly
at the end of summer or the beginning of autumn), but not a single individual of
S. citellus

was found.
The closest populations are in Vojvodina area (Serbia) but they are divided by th
e D
anube

River
which
represents

an insuperable natural barrier for

eventual spreading
of the species
to Croatia. In
the future, actions will be focused on detailed habitat research o
n

possible sites where this species
could be re
establish
ed

(
M
AZIJA

in litt
.)
.


Ukraine

In Ukraine, distribution of
S. citellus

was restricted to
southwestern part of
Transcarpathian region,
where it re
ache
d
the easternmost limit of its distribution
.
Earlier it occur
r
ed also in northwestern part
of the region, but as back as 1950
ies the species disappeared from most localities except the area on
the confluence of the Latorica and Tisa rivers. Also in this area it became missing for 50 years while in
2006 a small colony in Uzhorod area was discovered. Having considered the fact tha
t grazing on this
last
remaining
locality has ceased
in recent years exti
n
ction of the species in the country is highly
probable (
B
ASHTA

&
P
OTISH
, 2007).



Bosnia and Herzegovina

Data not available


Moldova

Southern limit of the species distribution passe
s over Moldova.
In the Red book of Moldova from 2002
the species has been considered as critically endangered (
C
OROIU

et al. 2008). Population d
ata
are
not available
.


Turkey (European part)

Distribution of the species is restricted to European part of Tur
key, where it reaches the southern limit
of its distribution.
D
etailed d
ata
on the population size are lacking

W
OJTASZYN

et al. 2012).



Table 1
.


Country

Biogeo
g
.
region

Population size

Date of
estimation

Data
quality
1

Trend**

Period for
estimation
of po
p.
trend

Data quality

on
population
trend

Source

EU countries

Austria

Alpine and

Continental

15.000
-
30.000

2001
-
2006

G

-

2001
-
2006

G

Artic.17
report

Bulgaria

Continental



Alpine


About 200
-

300
localities


About 50
-
100
colonies

2005
-
2012

M

=/
-

2005
-
2012

M

Koshev,
Kocheva
2007;
Koshev
2008;

THE

N2K

GROUP

European Economic Interest Group


EU Species Action Plan



Spermophil
us citellus



second draft

18

Black sea
region



About 50
-
100
colonies

Koshev 2009

Stefanov &
Markova
2009

Stefanov in
press


Czech
Republic

Continental
and

Pannonic

3600
-
3950
individuals

(31
-
35 localities)

2008
-
2011

G

=

2008
-
2011

G

Větrovcová
in litt. ex
Matějů et al.
2008, 2010;
Matějů and
Schnitzerová
2011

Germany

Continental

Extinct

last observ
.

19
68
(1980???)







Greece

Mediterranean

4319.1 km
2

2002
-
2006

M

= /
-

2002
-
2012

G

Youlatos in
litt. ex Art.17
report

Hungary

Pannon
ic

156
-
434

localities

2001
-
2006

M

=

2000
-
2006

M

Váczi in litt.
ex Art.17
report

Poland

Continental

Extinct

last observ:
at the
turn of the 70s and
80
;
Reintroduced

population
:
850
-
900

in 3 localities,
program ongoing

07/2012

G

+

2005
-
2012

G

Wojtaszyn et
al. 2012,
K
OŃCZAK

et
al.
2012

Romania

Steppic

Ca. 86 localities

1950
-
present

B

-

1950
-
present

(but
decreasing all
along, i.e.
also
decreasing
during 2000
-
present)

M

Iftime in litt.

Continental

Ca.
155

localities

1950
-
present

B

-

1950
-
present

(but
decreasing all
along, i.e.
also
decreasing
during 2000
-
present)

M

Iftime in litt.
ex Art.17
report

Pannonic

Ca.
5
8 localities

1950
-
present

B

-

1950
-
present

(but
decreasing all
along, i.e.
also
decreasing
during 2000
-
present)

M

Iftime in litt.
ex Art.17
report

Slovakia


Pannonic

77 sites

1996
-

2008

G

-

1970
-
1995

M
/
B

Ambros
2008

Alpine

94 sites

1996
-

2008

G

-

19
96
-
2008

M
/
B

Ambros
2008

Non
-
EU countries

Croatia

Continental

Probably extinct






Mazija in litt.

FYRo
Macedonia



S. citellus