Journal of Asia-Pacific Biodiversity 16 (2023) 384e390

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Journal of Asia-Pacific Biodiversity

journal homepage: http://www.elsevier.com/locate/japb

Original Article

Predicting the current and future suitable habitats, species distribution,

and conservation assessment of Fritillaria dagana (Liliaceae)q
Zagarjav Tsegmed a, Shukherdorj Baasanmunkh b, Khurelpurev Oyundelger c, d,
Batlai Oyuntsetseg e, Uudus Bayarsaikhan e, Andrey Erst f, Hyeok Jae Choi b, *
a
Laboratory of Flora and Plant Systematics, Botanic Garden and Research Institute, Mongolian Academy of Sciences, Ulaanbaatar, Mongolia
b
Department of Biology & Chemistry, Changwon National University, Changwon, South Korea
c
Technical University Dresden, International Institute (IHI) Zittau, Chair of Biodiversity of Higher Plants, Zittau, Germany
d
Department of Botany, Senckenberg Museum of Natural History Görlitz, Görlitz, Germany
e
Department of Biology, School of Arts and Science, National University of Mongolia, Ulaanbaatar, Mongolia
f
Central Siberian Botanical Garden SB RAS, Novosibirsk, Russia

a r t i c l e i n f o a b s t r a c t

Article history: Fritillaria dagana Turcz. has a restricted global distribution, occurring only in southern Siberia and
Received 16 November 2022 northern Mongolia. Concerning its restricted distribution and endangered conservation status, we aimed
Received in revised form to forecast its current and future suitable habitats as well as distribution shifts for 2050 and 2080. The
5 January 2023
Maxent model with different scenarios (representative concentration pathway 4.5 and representative
Accepted 8 January 2023
Available online 16 January 2023
concentration pathway 8.5) was used to analyze 113 georeferenced records of F. dagana using 19
bioclimatic factors from the WorldClim database. As a result, the amount and variance of precipitation
and temperature, together with elevation, were shown to be the most significant factors affecting the
Keywords:
climate change
species’ distribution. In particular, precipitation during the plant growing season had the greatest impact
conservation status (55.2% variability) on the species distribution. Climate change was expected to cause a minor shift in the
forest steppe distribution of suitable habitats toward the north and an increase in habitat continuity, indicating that
Fritillaria the climate will become more favorable for the growth of species and in the future. The species’ highly
Maxent model suitable area will remain primarily concentrated in its current potential distribution area in central
Siberia (around Lake Baikal). The species’ conservation status was determined to be near threatened,
emphasizing the great relevance of facilitating proper conservation measures for F. dagana.
Ó 2023 National Science Museum of Korea (NSMK) and Korea National Arboretum (KNA), Publishing
Services by Elsevier. This is an open access article under the CC BY-NC-ND license (http://
creativecommons.org/licenses/by-nc-nd/4.0/).

Introduction occurrence data and environmental variables that are assumed to

Climate change as well as habitat fragmentation and loss are
major reasons for species extinction and biodiversity loss
(Secretariat of the Convention on Biological Diversity 2020). To
mitigate the impacts of climate change on ecosystems, biodiversity
conservation is a key objective that will require both quantifying
biodiversity and monitoring losses (Balmford and Bond 2005).
Species distribution models are commonly used to estimate the
geographical range of a species given its presence based on
q Given his role as Subject Editor, Hyeok Jae Choi had no involvement in the
peer-review of this article. Full responsibility for the editorial process for this article
was delegated to In-Su Choi.
* Corresponding author. ORCID.: 0000-0003-3644-6795
E-mail address: hjcoi1975@changwon.ac.kr (HJ Choi)
Peer review under responsibility of National Science Museum of Korea (NSMK) and
Korea National Arboretum (KNA).
influence their distribution (Peterson et al. 2011; Qin et al. 2017).
Various species distribution models, such as generalized additive
model, domain environmental envelope, genetic algorithm for
rule-set production, and maximum entropy model (Maxent), are
frequently used to predict the geographical distribution of plant
species. Among them, the Maxent model has been demonstrated to
be the most reliable and consistent (Elith et al. 2006, 2010; Wisz
et al. 2008; Kumar and Stohlgren 2009) with superior perfor-
mance (i.e. high robustness for variable collinearity) than that of
genetic algorithm for rule-set production and generalized additive
model (Padalia et al. 2014; Panda et al. 2018; Feng et al. 2019).
Numerous studies have frequently used the Maxent model to es-
timate and predict current and future suitable habitats for various
threatened and important medicinal plants (Wisz et al. 2008;
Kumar and Stohlgren 2009; Qin et al. 2017; Zhao et al. 2018; Purohit
and Rawat 2022).

https://doi.org/10.1016/j.japb.2023.01.004
pISSN2287-884X eISSN2287-9544/Ó 2023 National Science Museum of Korea (NSMK) and Korea National Arboretum (KNA), Publishing Services by Elsevier. This is an open
access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
 Z Tsegmed et al. / Journal of Asia-Pacific Biodiversity 16 (2023) 384e390
Fritillaria L. (Liliaceae), a genus of bulbous plants with approxi-
mately 150 species, is primarily distributed in the Northern
Hemisphere (Rix et al. 2001). Furthermore, it has medicinal and
horticultural value (Day et al. 2014). About 20 species’ conservation
status has been evaluated globally according to the International
Union for Conservation of Nature (IUCN) (IUCN 2022), predomi-
nantly from the Mediterranean region. Additionally, several studies
have assessed the conservation status of Fritillaria at the national
level, such as Iran, Turkey, and Mongolia (Tekşen and Aytaç 2011;
Kiani et al. 2017; Oyuntsetseg et al. 2018).
Fritillaria dagana Turcz. was first described in Russia and has been
recorded in several administrative areas, including Buryatiya, Chita,
Irkutsk, and Krasnoyarsk (Malyschev and Peschkova 2001). This
species is listed as rare in the Red Data Book of the Russian Federation
(Bardunov and Novikov 2008). In Mongolia, F. dagana was found from
the Khentei mountain range in north-western Mongolia (Ganbold
2010; Sandanov 2013; Baasanmunkh et al. 2022a, 2022b) and is
categorized as endangered in the country (Oyuntsetseg et al. 2018).
Recently, some studies have been conducted on species conservation
such as in situ conservation (Erst et al. 2014) and evaluation of genetic
fidelity in Russia (Muraseva et al. 2018).
In the present study, we aimed to (i) assess the species’ “global”
conservation status based on all occurrence records; (ii) project
current and future species’ suitable habitats and distribution; (iii)
provide species’ distribution maps and detailed photo illustrations
based on recently collected materials.
Material and methods
Study area
Fritillaria dagana is a bulbous perennial plant growing in
meadow and forest-steppe habitats on grassy slopes of the hill-
Figure 1. Photo illustration of Fritillaria dagana from Mongolia: A, general habitat; B, habit; C, cauline leaves; D, pistil; E, Filaments; F, Perianth; G, bulb.
385
forest belt between 400 and 3000 m (Figure 1) (Baasanmunkh
et al. 2019). Furthermore, it is distributed in northern Mongolia
and eastern Russia between 84.38
Ee113.33
E and 46.57
Ne
58.66
N (Figure 2A). A point distribution map was created using
ArcGIS version 10.4.1 (ESRI 2012). Typical habitats of F. dagana were
photographed in the northern part of Mongolia (Figure 1). A brief
description of the morphology and taxonomy of the species is
provided based on newly collected samples from Mongolia.
Data collection of species occurrence
Point data were obtained from several sources: (i) field obser-
vations in Mongolia in 2017 and 2018; (ii) literature sources; (iii)
herbarium specimens from herbaria LE, NS, NSK, MW, and UBU
(Thiers 2019), and the Global Biodiversity Information Facility (GBIF
2021). Distribution records without specified geographic co-
ordinates were retrieved from Google Earth (http://www.google.
com/earth). A total of 133 occurrences were collected and 20 oc-
currences were removed owing to lack of collection information
(Appendix A).
Conservation assessment
Global assessment was based on IUCN criterion B (including
sub-criteria B1: the extent of occurrencedEOO, and B2: the area of
occupancydAOO), which uses the geographic range size of a spe-
cies and evidence of declining or fragmented populations (IUCN
2019). The EOO and AOO parameters were estimated using the R-
package ConR (Dauby et al. 2017) in R 4.0.3 (R Core Team 2020). The
minimum AOO was estimated based on a user-defined grid cell of
2 km2 according to IUCN (IUCN 2019).
386 Z Tsegmed et al. / Journal of Asia-Pacific Biodiversity 16 (2023) 384e390
Figure 2. The suitable distribution of Fritillaria dagana under current and future scenarios: A, current distribution; B, 2050s (RCP 4.5); C, 2050 (RCP 8.5); D, 2080s (RCP 4.5); E, 2080s
(RCP 8.5).
Environmental variables
The environmental variables of present and future global
climate conditions were derived from the WorldClim database
(https://www.worldclim.org/). The current climate data were ob-
tained from the WorldClim Database 2.0 with an accuracy of
w1 km2 (30 arc seconds). Based on the global climate model GFDL-
CM3 for climate change forecasting, 19 biological climate variables
for 2050 and 2080 years for two representative concentration
pathways (RCP) 4.5 and 8.5 were downloaded from Climate
Change, Agriculture and Food Security data portal (CCAFS; http://
ccafs-climate.org/data/) (Griffies et al. 2011; Van Vuuren et al.
2011; Chaturvedi et al. 2012; Navarro-Racines et al. 2020). These
two RCP scenarios have been recently used in the most recent
projection in the fifth report of the Intergovernmental Panel on
Climate Change (IPCC5) (Moss et al. 2010; Remya et al. 2015). We
redesigned all data layers to uniform size (w1  1 km) and con-
verted them to the American standard code for information
interchange (Hijmans et al. 2005).
Species distribution modeling
The predicted distribution of F. dagana was modeled using
Maxent model v. 3.4.1 with the default standard parametrization
was used for model training (Phillips et al. 2017). The training and
test data were set at a ratio of 75:25, and the background dataset
points were set at 10,000 with 20 replicates (Phillips 2008). To
assess the suitability of the distribution model, Maxent gives a
value from 0 to 1, with a value of <0.5 indicating unsuitable and a
value of >0.5 indicating a suitable habitat. We considered the value
of the area under the Receiver Operating Characteristic curve curve
(AUC) from 0 to 0.2 as not suitable, 0.21 to 0.4 as less suitable, 0.41
to 0.6 as moderate, and value of >0.6 as highly suitable area.
Results and discussion
Taxonomic description
Fritillaria dagana Turcz., Flora 17 (1, Beibl.): 25 (1834).
Imperialis dagana Turcz., Bull. Soc. Imp. Naturalistes Moscou 10(1):
62 (1837).
Description. Herbs, perennial, 20e35 cm tall, glabrous
(Figures 1AeB). Leaves 3e5 in upper part (Figure 1C), cauline leave
oblong-lanceolate to ovate with 4e10 cm (Figure 1B). Flowers sol-
itary, nutant (Figures 1AeB). Perianth 2e4 cm, brown violet
outside, yellowish inside (Figure 1F). Capsule 1.5 cm long, oblong
narrow wings. Bulbs a few small scales (Figure 1G).
Distribution. Mongolia (Khentei and Khuvsgul region) and Russia
(Buryatiya, Chita, Irkutsk and Krasnoyarsk) (Malyschev and
Peschkova 2001).
Chromosome number. 2n ¼ 24 (Rice et al. 2015).
Flowering and fruiting time. early June to July (Malyschev and
Peschkova 2001; Baasanmunkh et al. 2019).
Taxonomic notes. Fritillaria dagana resembles to F. maximowiczii
Freyn, and F. sonnikovae Shaulo & Erst in morphology. However, this
species differs from F. maximowiczii by its perianth oblong-
elliptical, acuminate, and filament slightly thickened toward base
(Malyschev and Peschkova 2001), and distinguished from
F. sonnikovae by its oblong ovate-lanceolate rather than linear-
 Z Tsegmed et al. / Journal of Asia-Pacific Biodiversity 16 (2023) 384e390 387

lanceolate or linear leaves, broadly campanulate, not closed peri- Table 1. Prediction distribution size of the species distribution using the model of
anth, brown-purple rather than light greenish-yellow outside, RCP4.5 and RCP8.5.

orange-purple with light fine checkerboard pattern than bright Period (Climate scenario) Habitat suitability Area (km2) Proportion (%)
yellow with purple flecks inside coloring (Shaulo and Erst 2010). Current High 50708.51 13.82
Moderate 73457.41 20.02
Low 242764.90 66.16
Conservation assessment 2050 (RCP4.5) High 59044.45 17.44
Moderate 78278.81 23.12
Low 201265.56 59.44
According to the Con R package, the EOO was estimated to be 2050 (RCP8.5) High 54419.02 12.10
300,000 km2, which was considered as Least Concern. The AOO, on Moderate 92519.92 20.58
the other hand, was estimated to be 364 km2, and was evaluated as Low 302654.00 67.32
near threatened. The gap between EOO and AOO appeared to be 2080 (RCP4.5) High 53574.13 13.06
Moderate 88506.94 21.57
significant because of the extensive dispersal range of the species. In Low 268196.59 65.37
addition, the majority of the Russian populations were not in pro- 2080 (RCP8.5) High 49992.08 13.81
tected areas, unlike to the completely protected, but sparsely Moderate 77641.92 21.45
distributed, populations of Mongolia (Figure 2A). This suggests that Low 234338.97 64.74
Russia should consider protecting this rare species. Our assessment of
projected changes in species distribution in the future supports
Russia’s need for conservation management. The species would Predicted distribution for the years of 2050 and 2080
continue shifting further north, where larger area would be suited for
it. Therefore, the establishment of border protected areas between According to the results of modeling for the coming 30 and 50
Russia and Mongolia (Tuva Republic, Altai Republic, and Irkutsk) years (2050 and 2080), the distribution area of the species will shift
would be a remarkable conservation management to cover the spe- further northwards depending on the main climatic factors
cies’ current and future territory. (Figures 2BeE). In particular, the following climatic factors were
found to be the primary drivers, contributing to the highest vari-
ability: precipitation of the wettest month (Bio13), maximum tem-
Modern potential distribution areas perature of the warmest month (Bio5), precipitation of the wettest
quarter (Bio16), precipitation of the warmest quarter (Bio18), iso-
For the years 2020, 2050, and 2080, the Maxent model based on thermality (Bio3 ¼ bio2/bio7*100), and elevation with 55.2%, 11.8%,
113 georeferenced data of F. dagana produced AUC values of 0.947, 6.7%, 4.5%, 3.1%, and 2.4% contribution, respectively (Table 2;
0.969, and 0.946, respectively (Figure 3). An AUC value higher than Figure 4). The cumulative contribution of these six factors was 83.7%.
0.5 indicates that the model displays a better performance than According to RCP 4.5, in which the emission peaked around
random prediction (Phillips and Elith 2010). 2040 and then declined, the total distribution of the species will
The current potential distribution of F. dagana was found to be decline by 8% in 2050 and rice by 22% in 2080 compared to the
366,931 km2 (Figure 2A). Among these, 288,589 km2 (79%) belongs current distribution. Moreover, it was predicted that a similar
to Russia (Irkutsk, Tuva, Krasnoyarsk and Gorno-Altay) and tendency will be observed in the areas of both high and moderate
78,342 km2 (21%) belongs to northern Mongolia (Khuvsgul, Bulgan suitability habitats. Overall, the less suitable area of the distribution
and Selenge provinces). Currently, highly suitable areas for F. dagana will decrease slightly in 2050 and 2080 (Table 2). Based on RCP 8.5,
cover approximately 50,709 km2 (14%), medium suitable areas where the emission rose continuously throughout the 21st century,
73,457 km2 (20%) and low suitable areas 242,765 km2 (66%) (Table 1). the expected total distribution of species will increase by 12% in

Figure 3. AUC result of Maxent modelling for Fritillaria dagana.

388 Z Tsegmed et al. / Journal of Asia-Pacific Biodiversity 16 (2023) 384e390

Table 2. Environmental variables related to the distribution of Fritillaria dagana.

Code Environmental variables Unit Current

Percent contribution Permutation importance

Bio1 Annual mean temperature C


Bio2 Mean diurnal range (mean of monthly (max temp  min temp)) C
Bio3 Isothermality (bio2/bio7) (*100) e 3.1 0.5
Bio4 Temperature seasonality (standard deviation*100 C of V


Bio5 Max temperature of warmest month C 11.8 42.3


Bio6 Min temperature of coldest month C


Bio7 Temperature annual range (bio5-bio6) C


Bio8 Mean temperature of wettest quarter C


Bio9 Mean temperature of driest quarter C


Bio10 Mean temperature of warmest quarter C


Bio11 Mean temperature of coldest quarter C
Bio12 Annual precipitation mm
Bio13 Precipitation of wettest month mm 55.2 15.8
Bio14 Precipitation of driest month mm
Bio15 Precipitation seasonality (coefficient of variation)
Bio16 Precipitation of wettest quarter mm 6.7 0.1
Bio17 Precipitation of driest quarter mm
Bio18 Precipitation of warmest quarter mm 4.5 0.4
Bio19 Precipitation of coldest quarter mm
Elevation Altitude M 2.4 2.9

2050 and decrease by 3% in 2080 compared to the current total area
of distribution. Under each climatic scenario, the highly suitable
area of the species will continue to be mainly concentrated in the
current potential distribution area (around Lake Baikal), and the
total area of suitable habitat will not change significantly (Table 2).
Notably, there will be significant habitat loss in the eastern and
western parts of the species distribution in 2080, according to both
emission scenarios (RCP 4.5 and 8.5; Figure 2).
There is a slight latitudinal shift, habitat continuity, and even
habitat loss in the distribution of the species, most likely as a result
of climate change. The main climatic variables that affect the ex-
pected distribution of a species are displayed in Figure 5, where the
most important environmental predictors are linked to precipita-
tion patterns and temperature during the summer months. In
particular, the optimal climatic conditions for a suitable habitat are
at 200e250 mm precipitation in the wettest month and 15
C

Figure 4. Result of Jackknife test for evaluating the relative importance of environmental variables for Maxent model on habitat suitability.
 Z Tsegmed et al. / Journal of Asia-Pacific Biodiversity 16 (2023) 384e390 389

Figure 5. Response curves the relationship of predicted probability of Fritillaria dagana occurrence to high six environmental variables: Bio3, Isothermality (bio2/bio7*100); Bio5,
Max temperature of warmest month; Bio13, Precipitation of wettest month; Bio16, Precipitation of wettest quarter; Bio18, Precipitation of warmest quarter.

maximum temperature in the warmest month (Figure 5). While
there will be no significant altitudinal shift, the optimum distri-
bution of the species will be between 1500 and 2200 m. The
findings showed that if the climate continues to warm, the pro-
spective distribution areas of F. dagana would migrate slightly
northwards, where wet and mild habitats exist, but with no sub-
stantial change in the total distribution area.
for the growth. However, segregated populations could become
extinct distant from the distribution’s center, most likely as a result
of isolation. The highly suitable area for the species will continue to
be mainly concentrated in the current potential distribution area in
central Siberia (around Lake Baikal). Furthermore, appropriate
protection measures for F. dagana should be facilitated.

Conclusion Declaration of competing interest

Occurrence data sets for F. dagana, a rare and near threatened
species, were obtained from Russia and Mongolia and used to
project the presence of suitable habitat in both present and future
scenarios. Many endangered plant species require urgent conser-
vation measures, which can be taken if the effects of climate change
are properly assessed. According to our modeling, the predicted
current potential range of the species is broader than its current
distribution range. Precipitation and temperature during the
summer months are the most important factor affecting the
regional distribution of F. dagana. Climate change was anticipated
to result in a minor shift in the distribution of suitable habitats
toward the north and an increase in habitat continuity, indicating
that the climate in the future may become increasingly favorable
The authors declare that they have no known competing
financial interests or personal relationships that could have
appeared to influence the work reported in this paper.
Acknowledgments
This study was supported by a research project (A study on the
distribution of vascular plants in Mongolia; Grant KNA1-2-38, 20-5)
of the Korea National Arboretum, Republic of Korea, partially sup-
ported by the National University of Mongolia, Mongolia (Grant
P2021-4186) and State Assignment of the CSBG SB RAS (project No.
AAAA-A21-121011290024-5).
390 Z Tsegmed et al. / Journal of Asia-Pacific Biodiversity 16 (2023) 384e390
Appendix A. Supplementary data
Supplementary data related to this article can be found at
https://doi.org/10.1016/j.japb.2023.01.004.
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