BioRisk 20: | 392 | 52 (2023) Apeer-reviewed open-access journal

doi: 10.3897/biorisk.20.97604 RESEARCH ARTICLE & B} lO R IS k

https://biorisk.pensoft.net

The use of boreal relict shrub habitats
of willow-leaf meadow sweet (Spiraea salicifolia)
and shrubby cinquefoil (Potentilla fruticosa)
in Western Rhodope Mts. by mammal species

Venislava Spasova', Daniela Simeonovska-Nikolova', Krastio Dimitrov’,
Gabriela Petrova', Kalina Pachedjieva', Rossen Tzonev'

I Sofia University, Faculty of Biology, Department of Ecology and Environmental Protection, Sofia, Bulgaria

Corresponding author: Venislava Spasova (v_spasova@biofac.uni-sofia.bg)

Academic editor: Kiril Vassilev | Received 15 November 2022 | Accepted 19 January 2023 | Published 15 May 2023

Citation: Spasova V, Simeonovska-Nikolova D, Dimitrov K, Petrova G, Pachedjieva K, Tzonev R (2023) The use of
boreal relict shrub habitats of willow-leaf meadow sweet (Spiraea salicifolia) and shrubby cinquefoil (Potentilla fruticosa)
in Western Rhodope Mts. by mammal species. In: Chankova S, Danova K, Beltcheva M, Radeva G, Petrova V, Vassilev
K (Eds) Actual problems of Ecology. BioRisk 20: 139-152. https://doi.org/10.3897/biorisk.20.97604

Abstract

Plant communities of two peat-shrub species — Spimea salicifolia and Potentilla fruticosa were studied in the
Rhodope Mts., with emphasis on their use as a resource for the mammals associated with them. These shrubs
are boreal relicts among the dominant coniferous forests. The field surveys were conducted in the spring-
autumn period of 2021-2022. In both study areas, the species composition of the mammals was studied by
camera traps for medium and large mammals, and by Sherman live traps for small mammals. ‘The species
registered were roe deer (Capreolus capreolus), red fox (Vulpes vulpes), wild boar (Sus scrofa), pine marten (Martes
martes), European hare (Lepus europaeus), red squirrel (Sciurus vulgaris), bank vole (Myodes glareolus) and
yellow-necked mouse (Apodemus flavicollis). Having in mind that small mammals are vital prey base for avian
and mammalian predators, it is not surprising that M. glareolus and A. flavicollis individuals were captured in
the habitats that they probably use as shelters. The pine marten inhabits the forests by which the community
of P fruticosa is surrounded, but probably feeds on the rodents in the shrub. In this way, it probably provides
it with an alternative to the forest food base and hunting ground. From the presented results, it seems that
the L. europaeus uses P fruticosa shrubs as food. ‘Therefore, the plant communities of the two relict peat-shrub
species studied probably provide shelter and food for the mammals. Their importance is established for at least
one species of mammal with conservation significance at national and European level — . martes. Therefore,

it is necessary to continue and expand the future monitoring on mammal diversity of these relict communities.

Keywords

camera traps, endangered species, live traps, mammals, relict shrub habitats

Copyright Venislava Spasova et al. This is an open access article distributed under the terms of the Creative Commons Attribution License (CC
BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

140 Venislava Spasova et al. / BioRisk 20: 139-152 (2023)

Introduction

Relict species have an important position in Earth’s biodiversity. Various studies are
known on the relict nature of many boreal plant species such as Parnassia palustris,
Salix lapponum, Potentilla fruticosa, etc. (Carni and Matevski 2015; Horsak et al. 2015;
Serafin et al. 2018). Due to their sedentary lifestyle and role in habitat foundation, rel-
ict plants have employed various strategies in adapting to their environment even under
dramatic climatic changes such as glaciations. Their populations preserve ecological and
evolutionary histories that can last thousands of years (Woolbright et al. 2014) but are
also threatened by climatic changes, which narrow their range of distribution (Hampe
and Jump 2011). Against this background, many studies have indicated climatic influ-
ences on mammal population dynamics, usually acting together with a complex set of
biotic factors (Humphries 2009). With the changes in global temperatures and conse-
quent changes to habitats, a clearer understanding of the relationship of mammals with
the environment has become imperative. Hence, it is of particular interest what mam-
mals inhabit the relict communities and how they use them. Determining habitat asso-
ciations of mammal species and the environmental characteristics important for site oc-
cupancy is central to understanding species biology and community organization. The
aim of the present study is to explore the use of two relict shrub habitats of willow-leaf
meadow sweet (Spiraea salicifolia) and of shrubby cinquefoil (Potentilla fruticosa) in the
region of Western Rhodope Mts as a resource for the mammals associated with them.
The two shrub habitats are assessed as critically endangered (Gussev and Vulchev
2015; Tzonev and Gussev 2015) at a national level. A particular feature of these shrub
communities is the combination of standing water or high soil and air humidity with
low temperatures characteristic of boreal and tundra biomes more broadly distributed
in the northern latitudes. This, together with the richness of northern and boreal floris-
tic elements and their complexity in terms of origin and evolution, significantly affects
their habitat value as a refuge of relict plant, invertebrate and vertebrate species. Due
to their glacial (boreal) relict origin, these habitats are threatened by climatic changes,
which narrow their range of distribution relative to all boreal and glacial relicts (Ham-
pe and Jump 2011). Many relict boreal plants, or even community types and animal
communities related to them, growing along the southern edge of their range and/or
at their altitudinal and climatic limits, are expected to be heralds of adverse climatic
changes (Freeman et al. 2018; Beniston 2000; Fescenco et al. 2020). Global warm-
ing in mountain plant communities is accompanied not only by extreme heat waves,
drought, and severe forest fires (Allen 1994), but also by invasion pressure from lower-
elevation plant communities and species (Lenoir et al. 2008). Surveys of relict boreal
plants or their communities growing near the extremes of their ecological tolerance
could help to estimate the pressure of climate change on the ecosystems and promote
better understanding and conservation of potential refuge areas for vulnerable to global
warming species. In European mountains various studies have investigated the impact
of recent climatic changes on mountain flora and vegetation (Dirnboock et al. 2011;
Pauli et al. 2012; Cannone and Pignatti 2014; Steinbauer et al. 2018) as some expected

‘The role of two boreal relict shrub habitats for mammals 141

and unexpected results were found, such as: elevation upshifting or downshifting for
different plant groups; increase of local species richness and decrease of rare or endemic
boreal plants. The significance of boreal mires and shrubs related to them as endan-
gered habitats for boreal relict plant and animal invertebrate species has already been
studied in Bulgaria (Hajek et al. 2009, 2010; Langourov et al. 2018). However, there
is still little information about their habitat use by mammals (Benedek et al. 2021).
Establishing what species of mammals inhabit these communities will help to initiate
effective monitoring programs in the context of climate change.

Materials and methods

Characteristics of Spiraea salicifolia and Potentilla fruticosa habitats

The investigated habitats are located and occupy areas in West Rhodope Mts., South-
west Bulgaria (Fig. 1). The communities in the studied sites are small and intra-zonal
phenomenon, being surrounded on all sides by the boreal coniferous forests that domi-
nate in Rhodope Mts. These forests are formed mainly by spruce (Picea abies), fir (Abies
alba) and scots pine (Pinus sylvestris) (Bondev 1991). Both habitats form close and
dense communities characterized by high soil moisture and represent parts of a huge
natural complex of boreal peatlands and bogs in the zone.

The main characteristics of the two communities were based on their floristic com-
position and ecological features and were determined as follows:

P fruticosa thickets are distributed in Beglika locality (41°50.11"N, 24°08.67"E),
near Batak town at 1510-1530 ma.s.l., covering an area of about 1.2 ha (Tzonev and
Gussev 2015) (Fig. 1). The soils are Humic Cambosols (Ninov 2002). The communities
occupy mountain slopes with low inclination, between 2 and 5 degrees. ‘They are dense
and closed with high coverage of the dominant species. The total vegetation cover is
90-100% (Fig. 2). The cool and humid climate and substrate predetermine the devel-
opment of mesophilic and cold-resistant plants. Almost 60 species and subspecies of
vascular plants (excluding bryophytes) are part of the composition of the P fruticosa
community with most species in the families Rosaceae, Poacea, Asteracea, Apiaceae and
Fabaceae, represented by 4—7 species each.

The communities of S. salicifolia occupy flattened river terraces along Dospatska
River, (41°45.45"N, 23°59.00"E), near Dospat town, at 1210-1250 m a.s.l., covering
an area of about 4.8 ha (Gussev and Vulchev 2015) (Fig. 1). The soils are Fluvisols with
a thick humus layer and acidic reaction (Ninov 2002). Spiraea salicifolia forms dense,
almost monodominant thickets along Dospatska River. The cover of the dominant
species S. salicifolia is higher than 80% (Fig. 3) with herbaceous plants of low abun-
dance. About 40 species and subspecies of vascular plants (excluding bryophytes) are
part of the composition of the S. salicifolia community. The plant families with highest
number of species are Rosaceae, Poaceae, Fabaceae which are also the biggest families in
the general Bulgarian flora (Assyov and Petrova 2012).

142 Venislava Spasova et al. / BioRisk 20: 139-152 (2023)

0.7 Kilometers

- Spiraea salicifolia habitat —— Rivers

Figure 2. Rhodope thickets of Potentilla fruticosa — individual plant (A) and habitat (B).

The climate in these regions is typical of the boreal coniferous forest belt where
both habitats are distributed. It is humid with mean annual temperature of 7.3 °C
(Batak) and 8.1 °C (Dospat), and annual precipitation of 912 mm and 966 mm re-
spectively (Fig. 4).

S. salicifolia and P fruticosa are listed in Annex 3 of the Bulgarian Biodiversity
Act. The territories occupied by their communities have been declared protected sites,
“Chibutsite” and “Hrastoviden ochibolets” respectively, and are included in the Natura
2000 network (Fig. 1).

The role of two boreal relict shrub habitats for mammals 143

ae

Figure 3. Rhodope thickets of Spiraea salicifolia — individual plants (A) and habitat (B).

Batak 1036 m Dospat 1360 m
60 120 70 2 140
50 7.3 °C 912 mm Ps 8.1°C 966 mm ia
100
50 100
40
80 ~ 80
30
Cc 60 mm °c 30 60 mm

40
10 10 20
0 20 0 )
Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec -20

-10 0 -10

A —<=t — precipitation B ——t —precipitation

Figure 4. Climate diagrams for the towns A Batak (P fruticosa habitat) and B Dospat (S. salicifolia
habitat). The model is based on weather data collected for the period 1991-2021 and has a resolution of
0.1-0.25 grade (data source Climate-Data.org).

Mammals’ data collection

The field surveys were conducted in the spring-autumn period of 2021 and 2022.
In both habitats over areas of about 0.5 to 1 ha, the species composition was studied
with camera traps (Moultrie M-40) for medium and large mammals, and by Sher-
man live traps (H. B. Sherman Traps, Inc., Tallahassee, Florida) for small mammals
(Fig. 5).

A total of four camera traps, two at the edge of each community, were installed on
trees at the height of about 50 cm. ‘The effort was the same at the two habitats — 167
trap-nights average per habitat (142 for 2021 and 192 for 2022).

A total of forty Sherman live traps baited with oat nuts were set per habitat. The
live traps were placed in lines at a distance of about 10 m from each other. To avoid
animal disturbance the trapping was carried out for one night in each shrub habitat.
All animals were released immediately after species determination at the place of cap-
ture. Relative abundance of small mammals was estimated on the base of the number
of individuals captured per trap-night. Additionally, the presence of mammals was also
registered by direct observation and traces of their activity.

144 Venislava Spasova et al. / BioRisk 20: 139-152 (2023)

Figure 5. Methods of mammal registration (A) camera trap (B) Sherman life trap.

Mammal identification

Species identification of mammals was made on the basis of external morphological fea-
tures, body size, and ecology according to Popov and Sedefchev (2003). In Bulgaria, the
wood mouse (Apodemus sylvaticus) and yellow-necked mouse (Apodemus flavicollis) do
not differ in external morphological features. Using cranial measurements in a study on
small mammal assemblages from North to South along the Bulgarian Black Sea coast,
Popov (2000) established that A. flavicollis was better represented in the southern area
where the forests were the prevailing vegetational type. In Central Western Bulgaria the
majority of adult wood mice also belong to A. flavicollis (Minkova and Popov 2002)
as well as in the Southwest part of the country (Popov 2015). This gives us reason to

consider that, in all probability, the captured Apodemus individuals are A. flavicollis.

Ethical notes

The investigation conformed to the international requirements for ethical attitude to-
wards the animals. All animals captured were released at the place of capture.

The role of two boreal relict shrub habitats for mammals 145

Results

In the S. salicifolia community, camera traps recorded the roe deer (Capreolus capreolus)
and red fox (Vulpes vulpes), both nocturnally and diurnally (Table 1, Fig. 6).

Among the rodents, the red squirrel Sciurus vulgaris and A. flavicollis were photo-
graphed. Around the community, tracks of C. capreolus, V. vulpes, hedgehog (Erinaceus
concolor), wild cat (Felis silvestris) and badger (Meles meles) were recorded as well. From
the small mammals in the live traps the bank vole M. glareolus and the yellow-necked
mouse A. flavicollis were captured (Fig. 7). Over the two years, the bank vole had a rela-
tive abundance 0.18—0.20 individuals per trap-night. The yellow-necked mouse was
captured only in 2022 with a relative abundance of 0.20 individuals per trap-night.

In the community of P fruticosa from the large and medium-sized mammals with
the camera traps the roe deer C. capreolus, the wild boar Sus scrofa, V. vulpes, and
the European hare (Lepus europaeus), as well as domestic horses (Equus caballus) were
recorded. Two different individuals of pine marten (artes martes) were recorded in
April and May of 2021 and 2022 with the camera traps as well. The martens were
registrated both during the night and the day (Fig. 8). From the small mammals, again
the bank vole M. glareolus and the yellow-necked mouse A. flavicollis were captured.
The bank vole was captured in both study years, while A. flavicollis was captured only
in 2021. The relative abundance of the bank vole was 0.25 individuals per trap-night,
and of the yellow-necked mouse 0.075 individuals per trap-night, respectively.

Table |. Camera trap recordings of mammals in S. salicifolia and P fruticosa habitats. Note: with * is
indicated the presence of both day and night registrations.

S. salicifolia habitat P. fruticosa habitat
Years 2021 2022 2021 2022
Recorded species Number of registrations
Capreolus capreolus 4 i el 14*
Sus scrofa - - - 2*
Vulpes vulpes 2 6* 3*
Martes martes - - os 10*
Lepus europaeus 1 — 4 12
Sciurus vulgaris - a - —
Apodemus flavicollis — 8 -
Equus callabus - - - 4
Discussion

The rodent species A. flavicollis and M. glareolus represented the small mammal com-
munity in our study. Their relative abundance is similar to those established by other
authors in mountain regions (Benedek et al. 2021). According to Benedek et al. (2021)
in most forests of Central and Eastern Europe M. glareolus and A. flavicollis are the
dominant rodent species, with one or the other being more numerous depending on
habitat conditions and geographic position. Our data are not sufficient to establish

146 Venislava Spasova et al. / BioRisk 20: 139-152 (2023)

I
C) 12°¢ #MOULTRIECAM 24 SEP 2022 04:50 pm

Figure 6. Camera trap registration of V. vulpes in S. salicifolia habitat.

whether there is microhabitat segregation of the two rodent species in the studied
habitats but, in other studies in mountanous areas, A. flavicollis seems to be more as-
sociated with the forest edge than M. glareolus, while the second species prefers areas
within the forest with high tree and shrub cover (Hille and Mortelliti 2010). In our
study M. glareolus was more numerous and captured in both habitats as well. Popov
(2007) also found that in Bulgaria the M. g/areolus is one of the rodent species with the
highest abundance in mountainous regions. Based on its highest abundance in moun-
tainous regions in Bulgaria we find that MZ. glareolus could be an indicator of climate
change here. Myodes glareolus has been identified also as a key species in genetic studies
for understanding the response of European fauna to climate change following the
Last Glacial Maximum, being an example of a woodland mammal surviving in cryptic
glacial refugia in Europe north of Mediterranean areas (Filipi et al. 2015).

Small mammals are also vital prey base for avian and mammalian predators. There-
fore, it is not surprising that many small vertebrates prefer to forage under plant cover
where it is more difficult for predators to detect them, avoiding areas with sparse cover
or greater distances between shelters (Loggins et al. 2019). It is considered that the
shrub cover is likely to have a strong influence on the species and communities of
small mammals that rely on it for safety (Stephens and Anderson 2014). In this sense,
the communities studied are very valuable for the small mammals found here, due to
their location between open space and forest. Both habitats probably also serve as a
shelter for roe deer, red fox and hare. These species were recorded both during the day
and at night. From a camera trap video it seems that the hare is pulling and chewing
a twig of the P fruticosa. For herbivores, shrubs can be important food sources, but

The role of two boreal relict shrub habitats for mammals 147

~~

Figure 7. Bank vole M. g/areolus captured in S. salicifolia habitat.

are relatively sustainable to the grazing due to their deep root system, multiple stems,
and height (Wikeem and Wikeem 2005). Besides, it is established that species such as
birch-leaved spirea (Spiraea lucida; syn. S. betulifolia) are negligible in the diet of wild
herbivores (Quinton 1984). However, the horses present in the area could be a threat
to the shrubs due to trampling. Therefore, measures should be taken to monitor and
control the number of domestic animals around the communities.

148 Venislava Spasova et al. / BioRisk 20: 139-152 (2023)

? . " * —_ 4 =
“3 3 J . Pp >, ;

#MOULTRIECA APR 2022 08:07 am

#MOULTRIECAM 01 SEP 2022 06:28 am

Figure 8. Camera trap registration of M. martes (A) and L. europaeus (B) in the P fruticosa habitat.

In the community of P fruticosa two pine marten were recorded. Martes martes is
considered a habitat specialist mainly associated with forests (Clevenger 1994; Caryl et
al. 2012; Lombardini et al. 2015). We assume that the pine marten inhabits the spruce
forests surrounding the P fruticosa community, but probably feeds on the rodents in
the shrub community. In this way, it provides pine martens with an alternative to the
forest food base and hunting ground. The M. martes is included in the Red Data Book
of Bulgaria vol. II in the category of “Endangered” species (Spassov and Spiridonov
2015) and in the Biological Diversity Law — Appendix II and III. It is also included
in the IUCN Red List, “Least Concern” category. The pine marten is a species that is

The role of two boreal relict shrub habitats for mammals 149

monitored within the National Biodiversity Monitoring System. ‘The studies carried
out in the two shrub communities provided data on its distribution at the national
level and could be useful in clarifying its habitat specialization. However, more studies
are needed to better understand the use of these boreal relict shrub habitats by mam-
mals in the region. Like other authors such as Humphries (2009) we also think that it
is necessary to continue and expand the examples of long-term monitoring of mammal
diversity with more taxa and regions before it is too late.

Conclusion

The studied relict peat-shrub plant communities dominated by S. salicifolia and
P. fruticosa in the Rhodope Mts. probably provide shelter and food for the mam-
mals. Their importance is established for at least one species of mammal with con-
servation significance at national and European level — M. martes. The limited dis-
tribution of these communities makes it necessary to initiate a long-term program
to monitor the impact of climate change on them and on their connection with the
associated mammals.

Acknowledgements

This work has been carried out in the framework of the National Science Program “En-
vironmental Protection and Reduction of Risks of Adverse Events and Natural Disas-
ters’, approved by the Resolution of the Council of Ministers No 577/17.08.2018 and
supported by the Ministry of Education and Science (MES) of Bulgaria (Agreement
No A01-279/03.12.2021)

References

Allen L (1994) Fire management in the sky islands. In: DeBano LH, Ffolliott PH, Ortega-
Rubio A, Gottfried GJ, Hamre RH, Edminster CB (Eds) Biodiversity and the Manage-
ment of the Madrean Archipelago: the Sky Islands of Southwestern United States and
Northwestern Mexico, 386-388. https://doi.org/10.2737/RM-GTR-264

Assyov B, Petrova A [Eds] (2012) Conspectus of the vascular plants in Bulgaria. Bulgarian
Biodiversity Foundation, Sofia, 1-489. [In Bulgarian]

Benedek AM, Sirbu I, Lazar A (2021) Responses of small mammals to habitat characteristics
in Southern Carpathian forests. Scientific Reports 11(1): 1-13. https://doi.org/10.1038/
s41598-021-91488-6

Beniston M (2000) Environmental Change in Mountains and Uplands. Arnold Publishers,
London and Oxford University Press, New York, 172 pp.

Bondev I (1991) The Vegetation of Bulgaria. Map 1:600000 with explanatory text. St. Kliment
Ohridski University Press, Sofia. [in Bulgarian]

150 Venislava Spasova et al. / BioRisk 20: 139-152 (2023)

Cannone N, Pignatti S (2014) Ecological responses of plant species and communities to climate
warming: Upward shift or range filling processes? Climatic Change 123(2): 201-214.
https://doi.org/10.1007/s10584-014-1065-8

Carni A, Matevski V (2015) Impact of climate change on mountain flora and vegetation in the
Republic of Macedonia (central part of the Balkan peninsula) In: Oztiirk M et al. (Eds)
Climate change impacts on high-altitude ecosystems. Springer, 189-213. https://doi.
org/10.1007/978-3-319-12859-7_7

Caryl FM, Quine CP, Park KJ (2012) Martens in the matrix: The importance of nonforested
habitats for forest carnivores in fragmented landscapes. Journal of Mammalogy 93(2):
464-474, https://doi.org/10.1644/11-MAMM-A-149.1

Clevenger AP (1994) Habitat characteristics of Eurasian pine martens Martes martes in
an insular Mediterranean environment. Ecography 17(3): 257-263. https://doi.
org/10.1111/j.1600-0587.1994.tb00101.x

Dirnboock T, Essl F, Rabitsch W (2011) Disproportional risk for habitat loss of high-alti-
tude endemic species under climate change. Global Change Biology 17(2): 990-996.
https://doi.org/10.1111/j.1365-2486.2010.02266.x

Fescenco A, Downer J, Fescenco I (2020) Persistence of remnant boreal plants in the Chir-
icahua Mountains, southern Arizona. Global Ecology and Conservation 23: e01131.
https://doi.org/10.1016/j.gecco.2020.e01131

Filipi K, Markova S, Searle J, Kotlik P (2015) Mitogenomic phylogenetics of the bank vole
Clethrionomys glareolus, a model system for studying end-glacial colonization of Eu-
rope. Molecular Phylogenetics and Evolution 82: 245-257. https://doi.org/10.1016/j.
ympev.2014.10.016

Freeman B, Lee-Yaw J, Sunday J, Hargreaves A (2018) Expanding, shifting and shrinking:
The impact of global warming on species’ elevational distributions. Global Ecology and
Biogeography 27(11): 1268-1276. https://doi.org/10.1111/geb.12774

Gussev Ch, Vulchev V (2015) 15F2 Rhodope thickets of Shrubby cinquefoil (Potentilla
fruticosa). In: Bisserkov et al. (Eds) Red Data Book of Bulgaria. Vol. 3. Natural habitats,
MOEW-BAS, Sofia, 237-238. http://e-ecodb.bas.bg/rdb/en/vol3/15f2.html

Hajek M, Hajkova P, Apostolova I, Horsak M, Plasek V, Shaw B, Lazarova M (2009) Disjunct
occurrences of plant species in the refugial mires of Bulgaria. Folia Geobotanica 44(4):
365-386. https://doi.org/10.1007/s12224-009-9050-0

Hajek M, Hajkova P, Apostolova I, Horsak M, Rozbrojova Z, Sopotlieva D, Velev N (2010)
The insecure future of Bulgarian refugial mires: Economic progress versus Natura 2000.
Oryx 44(4): 539-546. https://doi.org/10.1017/S00306053 10000530

Hampe A, Jump A (2011) Climate relicts: Past, present, future. Annual Review of Ecology,
Evolution, and Systematics 42(1): 313-333. https://doi.org/10.1146/annurev-ecol-
sys-102710-145015

Hille SM, Mortelliti A (2010) Microhabitat partitioning of Apodemus flavicollis and Myodes
glareolus in the sub-montane Alps: A preliminary assessment. Hystrix the Italian Journal of
Mammalogy 21(2): 157-163. https://doi.org/10.4404/hystrix-21.2-4458

Horsak M, Chytry M, Hajkova P, Hajek M, Danihelka J, Horsdkova V, Ermakov N, Ger-
man DA, Koci M, Lustyk P, Nekola JC, Preislerova Z, Valachovi¢é M (2015) European

The role of two boreal relict shrub habitats for mammals 151

glacial relict snails and plants: Environmental context of their modern refugial occurrence
in southern Siberia. Boreas 44(4): 38-657. https://doi.org/10.1111/bor.12133

Humphries MM (2009) Mammal ecology as an indicator of climate change. In: Letcher TM
(Ed.) Climate change: observed impacts on planet Earth. Elsevier, 197-214. https://doi.
org/10.1016/B978-0-444-53301-2.00010-5

Langourov M, Simov N, Bekchiev R, Chobanov D, Antonova V, Dedov I (2018) Inventory of
selected groups of invertebrates in sedge and reedbeds not associated with open waters in
Bulgaria. Acta Zoologica Bulgarica 70(4): 487-500. https://www.acta-zoologica-bulgarica.
eu/downloads/acta-zoologica-bulgarica/2018/70-4-487-500.pdf

Lenoir J, Gegout J, Marquet P, de Ruffray PB, Brisse H (2008) A significant upward shift in
plant species optimum elevation during the 20" century. Science 320(5884): 1768-1771.
https://doi.org/10.1126/science. 1156831

Loggins AA, Shrader AM, Monadjem A, McCleery RA (2019) Shrub cover homogenizes small
mammals’ activity and perceived predation risk. Scientific Reports 9(1): 1-11. https://doi.
org/10.1038/s41598-019-53071-y

Lombardini M, Cinerari CE, Murru M, Rosin AV, Mazzoleni L, Meriggi A (2015) Habitat
requirements of Eurasian pine marten Martes martes in a Mediterranean environment.
Mammal Research 60(2): 97-105. https://doi.org/10.1007/s13364-014-0211-z

Minkova TV, Popov VV (2002) Spatial Patterns of Terrestrial Small Mammal Communities in
Central Western Bulgaria (Mammalia: Insectivora, Rodentia). Acta Zoologica Bulgarica
54(3): 55-74.

Ninoy N (2002) Soils. In: Kopralev I (Ed.) Geography of Bulgaria. ForKom, Sofia, 277-315.
[in Bulgarian]

Pauli H, Gottfried M, Dullinger S, Abdaladze O, Akhalkatsi M, Alonso J, Coldea G, Dick J,
Erschbamer B, Calzado R, Ghosn D, Holten J, Kanka R, Kazakis G, Kollar J, Larsson P,
Moiseev P, Moiseev D, Molau U, Mesa J, Nagy L, Pelino G, Puscas M, Rossi G, Stanisci A,
Syverhuset A, Theurillat J-P, Tomaselli M, Unterluggauer P, Villar L, Vittoz P, Grabherr G
(2012) Recent plant diversity changes on Europe’s mountain summits. Science 336(6079):
353-355. https://doi.org/10.1126/science. 1219033

Popov VV (2000) Epigeobiont animal assemblages from two landscapes of the Bulgarian Black
Sea coast: Relationship to environmental gradients, assemblage structure and biodiversity.
HI. Small Mammals (Mammalia: Insectivora, Rodentia). Acta Zoologica Bulgarica 52(3):
79-96.

Popov V (2007) Terrestrial Mammals of Bulgaria: Zoogeographical and Ecological Patterns
of Distribution. In: Fet V, Popov A (Eds) Biogeography and Ecology of Bulgaria. Mon-
ographiae Biologicae 82. Springer, Dordrecht, 9-37. https://doi.org/10.1007/978-1-
4020-5781-6_2

Popov V (2015) Presence-only habitat suitability modelling using unclassified landsat
ETM+Imagery: Fine-resolution maps for common small mammal species in Bulgaria. Acta
Zoologica Bulgarica 67(1): 51-66. https://www.acta-zoologica-bulgarica.eu/downloads/
acta-zoologica-bulgarica/2015/67-1-51-66.pdf

Popov V, Sedefchev A (2003) The mammals in Bulgaria — handbook. Geosoft, Sofia, 144-145.
[In Bulgarian]

152 Venislava Spasova et al. / BioRisk 20: 139-152 (2023)

Quinton DA (1984) Cattle diets on seeded clearcut areas in central interior British Columbia.
Journal of Range Management 37(4): 349-352. https://doi.org/10.2307/3898709

Serafin A, Urban D, Bronowicka-Mielniczuk U, Szczurowska A (2018) To what degree can the
specifics of occurrence of glacial relic Betula humilis Schrank be an indicator of habitat
conditions of moderate climate peatlands? Water 10(8): 1062. https://doi.org/10.3390/
w10081062

Spassov N, Spiridonov G (2015) Pine Marten Martes martes (Linnaeus, 1758). In: Golemanki
V et al. (Eds) Red Data Book of the Republic of Bulgaria. Vol. 2. Animals, MOEW-BAS,
Sofia, 154 pp. http://e-ecodb.bas.bg/rdb/en/vol2/Mamartes.html

Steinbauer M, Grytnes J-A, Jurasinski G, Kulonen A, Lenoir J, Pauli H, Rixen C, Winkler
M, Bardy-Durchhalter M, Barni E, Bjorkman A, Breiner FT, Burg S, Czortek P, Dawes
MA, Delimat A, Dullinger S, Erschbamer B, Felde VA, Fernandez-Arberas O, Fossheim
KE, Gémez-Garcia D, Georges D, Grindrud ET, Haider S, Haugum SV, Henriksen H,
Herreros MJ, Jaroszewicz B, Jaroszynska KF, Kanka R, Kapfer J, Klanderud K, Kiihn I, Lam-
precht A, Matteodo M, di Cella UM, Normand S, Odland A, Olsen SL, Palacio S, Petey
M, Piscova V, Sedlakova B, Steinbauer K, Stéckli V, Svenning J-C, Teppa G, Theurillat
J-P, Vittoz P, Woodin SJ, Zimmermann NE, Wipf S (2018) Accelerated increase in plant
species richness on mountain summits is linked to warming. Nature 556(7700): 231-234.
https://doi.org/10.1038/s41586-018-0005-6

Stephens RB, Anderson EM (2014) Habitat associations and assemblages of small mammals
in natural plant communities of Wisconsin. Journal of Mammalogy 95(2): 404-420.
https://doi.org/10.1644/13-MAMM-A-025

Tzonev R, Gussev Ch (2015) 32F9 Rhodope thickets of Willow-leaf meadow sweet (Spiraea
salicifolia). In: Bisserkov et al. (Eds) Red Data Book of Bulgaria. Vol. 3. Natural habitats,
MOEW-BAS, Sofia, 272-273. http://e-ecodb.bas.bg/rdb/en/vol3/32F9.html

Wikeem B, Wikeem S (2005) Impacts of Browsing on Key Wildlife Shrubs in British Colum-
bia and Recommendations for their Use. B.C. Ministry of Environment, Lands and Parks,
Victoria, BC. Wildlife Working Report No WR 114, 1-76.

Woolbright S$, Whitham Th, Gehring C, Allan G, Bailey J (2014) Climate relicts and their
associated communities as natural ecology and evolution laboratories. Trends in Ecology &

Evolution 29(7): 406-416. https://doi.org/10.1016/j.tree.2014.05.003