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Spatial and Temporal Variations in Waterfowl Assemblage Structures in

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 diversity
Article
Spatial and Temporal Variations in Waterfowl Assemblage
Structures in Mongolian Lakes and the Changes Linked to the
Gradient of Lake Surface Areas
Zoljargal Purevdorj 1,2 , Namsrai Jargal 3 , Onolragchaa Ganbold 2 , Munkhbaatar Munkhbayar 2 ,
Erdenetushig Purevee 2 , Ariunbold Jargalsaikhan 2 , In-Hwan Paik 4 , Woon Kee Paek 5 and Joon Woo Lee 1, *
Citation: Purevdorj, Z.; Jargal, N.;
Ganbold, O.; Munkhbayar, M.;
Purevee, E.; Jargalsaikhan, A.;
Paik, I.-H.; Paek, W.K.; Lee, J.W.
Spatial and Temporal Variations in
Waterfowl Assemblage Structures in
Mongolian Lakes and the Changes
Linked to the Gradient of Lake
Surface Areas. Diversity 2023, 15, 334.
https://doi.org/10.3390/d15030334
Academic Editor: Vitor H. Paiva
Received: 21 November 2022
Revised: 20 February 2023
Accepted: 22 February 2023
Published: 27 February 2023
Copyright: © 2023 by the authors.
Licensee MDPI, Basel, Switzerland.
This article is an open access article
distributed under the terms and
conditions of the Creative Commons
Attribution (CC BY) license (https://
creativecommons.org/licenses/by/
4.0/).
Diversity 2023, 15, 334. https://doi.org/10.3390/d15030334
1 Department of Forest & Environmental Resources, Chungnam National University,
Daejeon 34134, Republic of Korea
2 Department of Biology, Mongolian National University of Education, Ulaanbaatar 210685, Mongolia
3 Department of Bioscience and Biotechnology, Chungnam National University,
Daejeon 34134, Republic of Korea
4 Biodiversity Information Institute of Korea, Daejeon 35312, Republic of Korea
5 Daegu National Science Museum of Korea, Daegu 43014, Republic of Korea
* Correspondence: jwlee@cnu.ac.kr
Abstract: Lakes and wetlands provide top-priority hotspots that play a key role in maintaining
and protecting threatened and migratory waterfowl. Identifying seasonal and spatial variations
in aquatic bird communities and their responses to environmental factors is vital conservation
efforts. However, there is a lack of information on waterfowl in Mongolian lakes and their associated
wetlands. The purpose of this study was to investigate the spatial–seasonal changes in waterfowl
assemblage structures in Mongolian lakes, as well as to determine how they respond to various
environmental factors (lake surface area, elevation, and geographical distribution). Statistical analyses
were performed using seasonal data (May, July, and September) for 28 waterfowl collected from
54 lakes across the country between 2016 and 2018. Seasonal heterogeneity in species richness
and abundance was observed in lakes in each geographical region (Eastern, Central, and Western
Mongolia). The composition of waterfowl in the lake was also relatively similar between May and
September compared to July. This was due to the overlapping migration seasons in spring and
autumn. Regionally, the number of waterfowl was much higher in the Eastern Mongolian lakes,
followed by Central Mongolian lakes and then Western Mongolian lakes. This is likely due to
differences in habitat availability and water levels between the regions. Eastern Mongolian lakes
tend to have more wetlands and shallow water habitats, while Central and Western Mongolian lakes
tend to have deeper open-water habitats. These differences in habitat types could contribute to the
observed differences in waterfowl abundance among the regions. Additionally, some small lakes
and the group of small lakes supported a greater abundance and diversity of waterfowl compared to
some medium-sized and large lakes, suggesting that they are important for conservation. Indices
of diversity (H’) and species dominance (D’) showed positive and negative correlations with lake
surface area, respectively. Perhaps the increased surface area of the lake decreases the habitat
overlap for designated waterfowl due to habitat heterogeneity. Accordingly, the indices (H’ and EH )
increased as the waterfowl species composition became relatively equivalent in large lakes. Overall,
spatial variations among the lakes were primarily attributable to the individual features of the lakes
(shallowness, small lake groupings, and surface area), and seasonal variation in the lakes depended
majorly on the compositional changes of the waterfowl due to migration.
Keywords: Mongolian lakes; flyways; anatidae; seasonal assemblages of waterfowl; lake size;
shallowness
https://www.mdpi.com/journal/diversity
Diversity 2023, 15, 334 2 of 14

1. Introduction
Lakes and their associated wetlands play a vital role in preserving aquatic ecosystems
and supporting ecological diversity [1]. A wide variety of waterbird species utilize the
habitats at different times during their annual life cycles for nesting, breeding, food, shelter,
migration stops, and wintering [2,3]. The presence and availability of wetlands and lakes
throughout the flyways is especially important in supporting the migration success of
long-distance migrants such as waterfowl, waders, and shorebirds [1,4]. Intense human
disturbances (such as land-use modification, water pollution, and heavy grazing) and
climate change, however, majorly affect their availabilities (natural presence, surface size,
and heterogeneity), leading to the high risk of waterbird decline worldwide [2,4,5]. It
is accordingly imperative to attend to and protect these habitats as they are vital to the
conservation of migratory waterbirds and other biodiversity.
There are a variety of environmental descriptors that influence the structure of water-
bird assemblages locally, regionally, and seasonally. Local characteristics of lakes such as
depth, surface area, sedimentation ratio, and trophic status are key factors in identifying
the composition, abundance, and richness of aquatic birds [2,5–7]. Shallow and highly
productive lakes with a high sedimentation ratio support a high abundance of waterbirds.
However, species richness increases with the size of lakes and their associated wetlands
due to habitat heterogeneity in large systems. The spatial and seasonal dynamics of wa-
terbird assemblages can also be found in systems due to differences in migration patterns,
such as period and corridor [2,8,9]. Accordingly, local environmental factors affecting
spatial–seasonal differences in aquatic bird communities are the basis for ecological studies
associated with conservation targets [10].
Mongolia is one of the top-priority countries for the research and conservation of
migratory birds due to its location at the junction of three major migratory flyways: East
Asia–Australia, Central Asia, and Eastern Africa–West Asia [11,12]. A number of pristine
natural habitats are also found in Mongolia such as the Altai-Sayan and Daguur ecoregions,
which are among the world’s most biologically outstanding regions and include sites
noted for their conservation value, Ramsar sites, and important bird areas (IBAs) [11–15].
Moreover, the IBAs with wetlands are considered important breeding and stopover sites
for migratory land and water birds [1,12,16,17]. Unfortunately, many lakes and wetlands
across Mongolia have been rapidly shrinking and drying up in recent decades due to the
continual decrease in river inputs and rapid water evaporation as a consequence of climate
change (increasing temperature and decreasing precipitation) [12,18–20]. The acceleration
of human activities is, moreover, a major cause for the loss of lake sizes in Mongolia and
their deterioration, which is due to overgrazing, intense mining, and expanding agricultural
practices [18–20]. Attending to their conservation is therefore valuable for supporting the
ecological requirements of aquatic birds, including nesting, breeding, food, shelter, and
migration stopovers, and has international significance. Despite the fact that several
monitoring programs have been actively implemented in a few lakes and rivers and their
associated wetlands in Mongolia, there is still a lack of information on waterfowl that is
connected with spatial–seasonal variations and the impacts of the local characteristics of
lakes and wetlands [12,15,18,19,21–26].
Based on biological data from 54 Mongolian lakes and their associated wetlands, the
present study has investigated spatial–seasonal variations in the assemblages of migratory
waterfowl along the different migration flyways. The influence of the size of lakes and the
grouping of small lakes was also addressed as descriptors for the changes in the waterfowl
community structures [4,27]. This is because of the lack of attention given by the govern-
ment to small lakes and wetlands in Mongolia compared to the larger lakes. Moreover,
several factors affecting waterfowl communities around the country were investigated,
including the gradients of geographical locations and longitudes.
Diversity 2023, 15, x FOR PEER REVIEW 3 of 14
Diversity 2023, 15, 334 3 of 14

2.
2. Materials
Materials and
and Methods
Methods
2.1. Background of Study Lakes
The lakes studied are distributed all over Mongolia, which is located in the transition
zone between the boreal forests of Siberia and the deserts of Central Asia (Figure 1). The
southern fringes of the
the Siberian
Siberian Great
Great Taiga
Taiga (boreal
(boreal forest)
forest) extend
extend into
into northern
northern Mongolia,
Mongolia,
whereas the vast Mongolian and Manchurian steppes spread into the country from the
The landscapes
east [12,13]. The landscapes of of southern
southern Mongolia
Mongolia are
are dominated
dominated by by the
the Gobi
Gobi Desert,
Desert,
while the high Altai Mountains dominate the west and northwest. From From north
north to to south,
south,
landscapechanges
the landscape changesfromfromforested
forestedmountains
mountains through
through grassy
grassy steppe
steppe to barren,
to barren, aridarid
de-
desert
sert plains
plains [12].
[12]. Meanwhile,
Meanwhile, the the topography
topography fromfrom the west
the west toeast
to the the changes
east changes
from from
a higha
high mountainous
mountainous terrain
terrain to boundless
to boundless plains.
plains. Each Each region
region has
has its its own
own specific
specific floralfloral and
and fau-
faunal characteristics. When combined, these characteristics comprise the unique
nal characteristics. When combined, these characteristics comprise the unique biological biological
richness of the country [12].

Figure
Figure 1.
1. Geographical
Geographical distribution
distribution of
of the
the lakes
lakes studied
studied throughout Mongolia.
throughout Mongolia.

There are
are three
threemain
mainwatersheds:
watersheds:the the Arctic
Arctic Ocean
Ocean Basin,
Basin, thethe Pacific
Pacific OceanOcean Basin,
Basin, and
and the Central
the Central AsianAsian
InternalInternal
DrainageDrainage BasinThe
Basin [28]. [28]. The majority
majority of lakesofinlakes in thisaddress
this study study
address
the thirdthe third
river river watershed
watershed and include
and include the western
the western and south–central
and south–central Mongolian
Mongolian lakes
lakes
such assuch as Buun
Uvs, Uvs, Buun
Tsagaan,Tsagaan,
and Kharand Khar
Lake.Lake.
EasternEastern Mongolian
Mongolian lakeslakes (Khukh,
(Khukh, Buir,Buir,
and
and Tashgai
Tashgai TavanTavan
Lakes,Lakes, etc.)
etc.) are are Pacific
in the in the Pacific OceanCentral–northern
Ocean Basin. Basin. Central–northern Mongolian Mongo-
lakes
lian lakes (Khuvsgul,
(Khuvsgul, TerkhiinUgii
Terkhiin Tsagaan, Tsagaan,
Lake, Ugii
etc.) Lake,
include etc.)
theinclude the Arctic
Arctic Ocean BasinOcean
[13]. Basin
Most
[13].
lakesMost
in thelakes in the
eastern eastern
region region
are fed are fed byhowever,
by rainwater; rainwater; however,
some lakes are some
alsolakes
fed byarerivers
also
and by
fed streams
rivers(e.g.,
and Khukh
streamsand Buir
(e.g., Lake,and
Khukh etc.)Buir
[12,15].
Lake,Theetc.)
small- and medium-sized
[12,15]. The small- andlakes me-
in the Gobi-desert
dium-sized lakes independ on rainfalldepend
the Gobi-desert levels. Most lakes levels.
on rainfall in the western
Most lakes andinnorth–central
the western
regions
and are fed by rivers
north–central regions and
arestreams
fed by[12,23]. The streams
rivers and surface area of the
[12,23]. Thestudy lakes
surface varied
area of thein
the range of 1.17 km 2 and 3350 km2 (<10 km 2 —twenty-six lakes, 10–20 km 2 —four lakes,
study lakes varied in the range of 1.17 km and 3350 km (<10 km —twenty-six lakes, 10–
2 2 2

20–50 2 —four lakes, 50–100 2km2 —8 lakes, 100–500 km 2 —seven lakes, 500–1000 km2 —
20 kmkm2—four lakes, 20–50 km —four lakes, 50–100 km2—8 lakes, 100–500 km2—seven
two lakes, and 1000 2
km <—three
lakes, 500–1000 km —two
2 lakes, andlakes) (Table
1000 km 2 1). Thelakes)
<—three average depth
(Table of the
1). The studydepth
average lakes
ranged
of from 0.9–137.9
the study lakes rangedm (<5 m—twenty-four
from 0.9–137.9 m (<5 lakes, 5–10 m—twelve
m—twenty-four lakes,
lakes, 10–20
5–10 m—four
m—twelve
lakes, 20–30
lakes, 10–20 m—three
m—four lakes,lakes, 20–30
and 100 m <—one
m—three lake)
lakes, (Table
and 100 1)m [28–30].
<—one lake) (Table 1) [28–
30].
Diversity 2023, 15, 334 4 of 14

Table 1. Summary data of waterfowl community metrics in the lakes, showing lake surface area
and depth.

Average Surface
Elevation Total
Code Lake Name Province Depth Area Richness F.O H’ EH D’
(m) Abundance
(m) (km2 )
WL1 Tolbo lake Bayan-Ulgii 6.8 84 2083 22 17 7006 2.32 0.60 0.12
WL2 Khoton-Khurgana Lake Bayan-Ulgii 27 50 2072 8 12 836 1.73 0.47 0.26
WL3 Dayan Lake Bayan-Ulgii 2.3 67 2232 5 14 2325 2.17 0.62 0.14
WL4 Uvs Lake Uvs 11.9 3350 743 16 18 2787 2.06 0.44 0.22
WL5 Uvsiin Khar Us Lake Uvs 5.2 85.2 1792 10 15 2005 2.37 0.71 0.11
WL6 Uureg Lake Uvs 26.9 238 1425 12 16 1341 2.21 0.57 0.14
WL7 Uvsiin Baga-Bayan Lakes Uvs 8 30.6 931 11 21 2493 2.02 0.36 0.22
WL8 Airag lake Uvs 5.7 143 1030 15 16 987 1.98 0.45 0.19
WL9 Achit lake Uvs 2 296.8 1435 8 18 1756 2.31 0.56 0.13
WL10 Khar Us lake Khovd 2 1852 1157 8 16 3691 1.90 0.42 0.20
WL11 Khar Lake Khovd 4.2 578 1132 14 17 1591 1.90 0.39 0.20
WL12 Taigam Lake Govi-Altai 0.9 4.1 1730 14 18 4915 2.37 0.59 0.12
WL13 Ereen Lake Govi-Altai 2.1 4.31 1451 5 14 3733 1.94 0.50 0.19
WL14 Ulaagchiin Khar Lake Zavkhan 19.6 84.5 1647 4 14 2893 1.73 0.40 0.22
WL15 Telmen Lake Zavkhan 13.8 213.37 1544 11 9 328 1.82 0.69 0.20
WL16 Santmargatsiin Bayan Lake Zavkhan 21.7 64.2 1662 8 9 1109 0.65 0.21 0.74
WL17 Oigon Lake Zavkhan 3.4 75.57 1574 5 14 623 2.04 0.55 0.19
CL18 Olon Lakes Bulgan 1.5 5.6 980 14 18 4907 1.86 0.36 0.27
CL19 Terkhiin Tsagaan Lake Arkhangai 6 63.31 2060 24 15 5980 1.73 0.38 0.24
CL20 Selengiin Tsagaan Lake Selenge 1.3 5.8 680 8 11 1135 1.05 0.26 0.58
CL21 Targan Lake Khuvsgul 6 19.9 1536 12 7 561 1.09 0.43 0.48
CL22 Khuvsguliin Sangiin Dalai Khuvsgul 12.1 165 1889 21 17 7434 1.85 0.37 0.20
CL23 Khuvsgul Lake Khuvsgul 137.9 2760 1645 13 17 715 2.62 0.81 0.09
CL24 Erkhel Lake Khuvsgul 0.9 13.2 1544 4 15 1860 1.87 0.43 0.22
CL25 Dood Tsagaan Lake Khuvsgul 8 43.1 1538 10 8 963 1.42 0.52 0.29
CL26 Deed Tsagaan Lake Khuvsgul 5 2.7 1550 8 9 241 1.64 0.57 0.24
CL27 Ugii Lake Arkhangai 6.6 25.7 941 10 14 1485 1.98 0.51 0.17
CL28 Sharga Lake Bulgan 3.7 12.4 1335 5 13 1090 1.80 0.47 0.20
CL29 Ulziitiin Sangiin Dalai Uvurkhangai 1.5 2.4 1705 8 18 5712 1.03 0.16 0.61
CL30 Khargal Lake Bulgan 5 13.5 1071 6 2 82 0.26 0.65 0.86
CL31 Dashinchilengiin Bayan Lake Bulgan - 2.9 936 8 14 444 1.88 0.47 0.20
CL32 Airkhan Lake Bulgan 1.3 5 1030 6 15 2359 1.60 0.33 0.35
CL33 Taatsiin Tsagaan Lake Uvurkhangai 1 9.9 1234 5 10 669 1.89 0.66 0.19
CL34 Orog Lake Bayankhongor 3 121.37 1334 11 18 2462 2.29 0.55 0.13
CL35 Buun Tsagaan Lake Bayankhongor 9.3 252 1433 24 18 8705 1.74 0.32 0.29
EL36 Gun Tsengeleg Lake Dornod - 0.8 832 13 10 2524 1.54 0.47 0.35
EL37 Gurmen Lake Khentii 0.8 5.6 918 6 14 381 2.15 0.62 0.16
EL38 Ganga Lake Sukhbaatar 0.5 2.2 1294 4 10 2244 1.26 0.35 0.36
EL39 Turgen Tsagaan Lake Dornod 0.9 3.7 812 8 11 1553 2.07 0.72 0.14
EL40 Tashgain Lake Dornod - 1.1 718 9 17 5116 1.96 0.42 0.21
EL41 Shuut Lake Dornod - 1.1 715 8 12 1421 2.04 0.64 0.18
EL42 Shaazan Lake Dornod - 1.17 800 5 13 551 2.19 0.69 0.15
EL43 Khukh Lake Dornod 3.2 51.6 560 13 16 22,219 2.06 0.49 0.17
EL44 Khaichiin Tsagaan Lake Dornod 1.6 7.6 663 7 11 1484 1.98 0.66 0.17
EL45 Ikh Daila Lake Dornod - 2.2 601 9 7 459 1.65 0.74 0.22
EL46 Baga Dalai Lake Dornod - 2.8 715 6 6 609 1.49 0.74 0.27
EL47 Galuut Lake, Baga Dornod - 1 839 9 3 444 0.04 0.35 0.99
EL48 Galuut Lake Dornod 1.3 6.5 583 7 11 2943 1.61 0.45 0.32
EL49 Erveekhii Lake Dornod - 0.6 839 8 13 621 2.08 0.61 0.16
EL50 Duruu Lake Dornod 1.5 6.5 632 7 7 664 1.62 0.72 0.22
EL51 Chukh Lake Dornod 2.5 2.64 582 6 9 2517 1.09 0.33 0.51
EL52 Busiin Lake Dornod 1 2.9 628 6 3 1870 0.64 0.63 0.66
EL53 Buir lake Dornod 6.5 615 581 15 15 4342 1.79 0.40 0.27
EL54 Khurkheree Lake Khentii - 1.6 1020 6 6 456 1.17 0.54 0.40
Notes: F.O—frequency of observation, H’—Shannon diversity index, D’—dominance index, EH —Shannon
evenness index, WL—Western Lake, CL—Central Lake, EL—Eastern Lake.

2.2. Procedure of Field Observation

From 2016 to 2018, field surveys were conducted at all Mongolian important bird areas
in May, July, and September. Observation data on twenty-eight waterfowl in fifty-four lakes
were extracted from our collected data for this study. Observation sites were randomly
selected along the shoreline within each lake and their associated wetlands, with high points
being preferred. The waterfowl species were registered and counted from 525 sites using
the point counting method and research tools (the visible eye encounter, field binoculars
Diversity 2023, 15, 334 5 of 14

(Nikon Monarch HG, 10 × 42), and a spotting scope (CarlZeiss, 20—60 × 80)) [31]. The
number of observation sites varied from five to twenty-four, depending on the size of the
lakes and some difficult natural situations. The observations lasted approximately 10 min
to diminish the probability of bird recount [31], and the distance between observers along
the shores of the lakes varied from approximately 50 to 200 m.

2.3. Analytic Approach

Shannon–Weiner’s diversity (H’), evenness (EH ), and Simpson’s dominance (D’) were
applied to quantify the diversity of the waterfowl species because these indices provide
more information about community composition than species richness [32–34]. These
calculations were performed using PAST (version 4.3.0) [35]. Moreover, the following
formula was utilized to compute the species’ probability of observation: P(species 1,2 . . . ) = (nl
* nos )/(Nl * Nos ), where P is the species probability to observe, nl is the number of observed
lakes, nos is the number of observed sites, and Nl and Nos are the total numbers of study
lakes and counting point sites, respectively. The relative abundance (RA) of a bird species
was determined using the following expression: (number of individuals for species n/N
total number of individuals) × 100%.
To illustrate seasonal variations in waterfowl community attributes (i.e., species rich-
ness and abundance), we performed an analysis of variance (ANOVA) and a Tukey’s
post -hoc test using the function “aov” in R software (version 4.2.2) [36]. A non-metric
multidimensional scaling (NMDS) [37] was performed to examine spatial variations in the
waterfowl due to region and flyway differences across the country with the help of the func-
tion “metamds” in the R package vegan 2.6-2 [38]. Data on waterfowl abundance with total
species were Hellinger-transformed using the R package vegan function “decostand” [39],
which reduces the weights of abundant species but keeps the Bray–Curtis index between
lakes [39]. Additionally, a permutational multivariate analysis of variance (PERMANOVA,
using the “Adonis” function in R software [35]) was used to test for regional differences. A
principal component analysis (PCA) was used to analyze the relationship between envi-
ronmental variables and waterfowl community attributes, aided by the “FactoMiner” and
“factoextra” packages in R software [40].

3. Results
3.1. Waterfowl Diversity and Abundance in Lakes
During this study, 139,641 individual waterfowl were recorded, belonging to 28 wa-
terfowl species from the families Anatidae and Anseriiformes. The richness varied from
2 to 21 among the lakes, with a range of 0.04–2.62 for species diversity (H’) (Table 1).
The highest richness (21 species) was found in the group lake of Baga-Bayan in western
Mongolia. On the contrary, in the central region, Khargal Lake showed the lowest richness
(2 species). According to the evenness index (EH ), the evenness of waterfowl in the lakes
ranged between 0.16 and 0.81. The highest value was identified in Khuvsgul Lake and the
smallest value was found in the Ulziitiin Sangiin Dalai lake in central Mongolia. Regarding
the dominance index (D’), there was a high variation among lakes in the range of 0.09–0.99.
The total abundance of the 28 waterfowl varied greatly between lakes. The most abundant
lake (22219 individuals) was Khukh Lake in eastern Mongolia, and the lowest abundance
was observed in Khargal Lake, which had 82 individuals (Table 1).
According to each species’ abundance, the most numerous species were Tadorna
ferruginea (relative abundance: 19.35%, mean ± s.e.: 77.9 ± 10.2), Aythya ferina (10.14%,
80.9 ± 11.2), Anser indicus (8.87%, 129.0 ± 28.3), and Aythya fuligula (8.23%, 69.2 ± 8.6)
(Table 2). The first two species were observed in the majority of the lakes in our study,
which included 51 and 46 lakes, respectively. On the other hand, Anser indicus was mostly
found in lakes in western and central Mongolia (31/54), and Anser cygnoid was commonly
observed in the lakes of eastern and central Mongolia (35/54). Moreover, the least numerous
species were Oxyure leucocephala (0.02%, 6.6 ± 0.9), Cygnus columbianus (0.1%, 2.5 ± 0.8),
and Anas zonorhyncha (0.001%, 1.5 ± 0.5). Additionally, Tadorna ferruginea (62.42%), Cygnus
Diversity 2023, 15, 334 6 of 14

cygnus (46.05%), Aythya ferina (28.40%), and Aythya fuligula (26.35%) were evaluated as
having a higher possibility of observation than other species throughout Mongolia (Table 2).

Table 2. The assemblage patterns of 28 waterfowl in lakes throughout the country.

Lake O.F Probability to Total Average Std.

Scientific Name English Name Max Min R.A
Observed (54) (525) Observe (%) Abundance Abundance Error
Anas acuta Northern Pintail 38 105 14.07 3793 36.1 7.1 485 1 2.72
Anas crecca Common Teal 31 58 6.34 1685 29.1 4.7 158 2 1.21
Anas platyrhynchos Mallard 40 156 22.01 4445 28.5 3.6 424 1 3.18
Anas zonorhyncha Eastern Spot-billed Duck 2 2 0.01 3 1.5 0.5 2 1 0.00
Anser anser Graylag Goose 22 126 9.78 5440 43.2 6.2 574 1 3.90
Anser cygnoid Swan Goose 35 96 11.85 12,386 129.0 28.3 1425 1 8.87
Anser fabalis Bean-Goose 6 11 0.23 2185 198.6 117.9 1300 2 1.56
Anser indicus Bar-headed Goose 31 134 14.65 11,391 85.0 33.5 4300 1 8.16
Aythya ferina Common Pochard 46 175 28.40 14,154 80.9 11.2 1112 1 10.14
Aythya fuligula Tufted Duck 45 166 26.35 11,486 69.2 8.6 803 1 8.23
Aythya marila Greater Scaup 4 6 0.08 47 7.8 1.2 12 3 0.03
Aythya nyroca Ferruginous Duck 13 18 0.83 256 14.2 3.9 62 2 0.18
Bucephala clangula Common Goldeneye 41 146 21.11 10,378 71.1 9.8 745 1 7.43
Cygnus columbianus Tundra Swan 3 6 0.06 15 2.5 0.8 6 1 0.01
Cygnus cygnus Whooper Swan 48 272 46.05 5248 19.3 3.2 544 1 3.76
Cygnus olor Mute Swan 7 10 0.25 34 3.4 1.2 14 1 0.02
Mareca falcata Falcated Duck 5 6 0.11 72 12.0 3.1 24 3 0.05
Mareca penelope Eurasian Wigeon 38 101 13.54 4407 43.6 7.5 414 1 3.16
Mareca strepera Gadwall 41 165 23.86 9856 59.7 11.3 1160 1 7.06
Melanitta fusca Velvet Scoter 22 50 3.88 1460 29.2 14.6 730 1 1.05
Mergus merganser Goosander 12 32 1.35 1596 49.9 37.4 1200 1 1.14
Mergus serrator Red-breasted Merganser 4 12 0.17 54 4.5 0.9 11 1 0.04
Netta rufina Red-crested Pochard 14 46 2.27 2260 49.1 14.3 550 1 1.62
Oxyura leucocephala White-headed Duck 3 5 0.05 33 6.6 0.9 9 4 0.02
Spatula clypeata Northern Shoveler 33 82 9.54 2102 25.6 4.4 244 1 1.51
Spatula querquedula Garganey 19 28 1.88 339 12.1 2.1 48 1 0.24
Tadorna ferruginea
Diversity Ruddy
2023, 15, x FOR Shelduck
PEER REVIEW 51 347 62.42 27,014 77.9 10.2 1917 1 7 19.35
of 14
Tadorna tadorna Common Shelduck 37 125 16.31 7502 60.0 12.8 1285 1 5.37
Notes: RA—relative abundance; O.F—observation frequency.

Amongthe
Among theobserved
observedmonths,
months,a astatistical
statistical difference
difference in species
in species diversity
diversity andand even-
evenness
ness (H’ and E H) was found during the study years (ANOVA, df = 122.2, F = 14.34 and
(H’ and EH ) was found during the study years (ANOVA, df = 122.2, F = 14.34 and 14.86,
p14.86, p < respectively).
< 0.001, 0.001, respectively). The indexes
The indexes and species
and species richnessrichness wereinhigher
were higher the Mayin the May
surveys
surveys than in the July and September surveys (Figure 2A, Table
than in the July and September surveys (Figure 2A, Table 3). Waterfowl abundance and 3). Waterfowl abun-
dance
the and the
species speciesofdiversity
diversity regionalof regional
levels showedlevels showed
similar similarpatterns
seasonal seasonal(Table
patterns (Table
3), with a
3), with
lower a lower abundance
abundance of birds in of birds
May, in May,byfollowed
followed a tendencyby atotendency
peak in Julyto peak
and in July and
September.
September.
The seasonalThe seasonal
variation in variation
waterfowlinabundance
waterfowl wasabundance was significantly
significantly different
different in the in
eastern
the eastern
region region (May–July–September;
(May–July–September; one-way ANOVA, one-way
df =ANOVA,
98.78, F = df
1.6,= p98.78,
= 0.1),Fcentral
= 1.6, pRegion
= 0.1),
central Region
(ANOVA, (ANOVA,
df = 89.9, F = 7.6,dfp=<89.9,
0.01)Fand
= 7.6,
thep western
< 0.01) and the (ANOVA,
region western region (ANOVA,
df = 101.2, df
F = 6.3,
= 101.2, F = 6.3,
p < 0.01) (Table 3).p < 0.01) (Table 3).

Figure 2.
Figure 2. Seasonal
Seasonal and
and regional
regional differences
differences in
in waterfowl
waterfowl diversity (H’) and abundance in the lakes.
lakes. Different small letters indicate significant differences
Different small letters indicate significant differences between
between seasons
seasons at p <at p < analyzed
0.05 0.05 analyzed
by the
by the Tukey
Tukey test. test.

Table 3. The seasonal patterns in waterfowl assemblage structures are described by the regions and
overall.

Eastern (19 Lake) Central (18 Lakes) Western (17 Lakes) Total (54 Lakes)
May July September May July September May July September May July September
Diversity 2023, 15, 334 7 of 14

Table 3. The seasonal patterns in waterfowl assemblage structures are described by the regions and
overall.

Eastern (19 Lake) Central (18 Lakes) Western (17 Lakes) Total (54 Lakes)
May July September May July September May July September May July September
F.O 40 59 53 71 68 58 59 50 67 152 197 176
Richness 21 13 17 24 27 21 24 21 22 28 27 27
H’ 2.44 a 1.59 b 2.33 a 2.57 a 2.12 b 2.20 b 2.49 a 2.46 a 2.63 b 2.65 a 2.39 b 2.56 a
EH 0.54 a 0.37 b 0.60 a 0.54 a 0.31 b 0.37 b 0.50 a 0.55 a 0.63 b 0.50 a 0.40 b 0.48 a
Abundance 10,038 a 18,820 a 23,560 a 6523 a 23,374 b 16,915 b 8774 a 16,205 b 15,432 b 25,335 a 58,399 b 55,907 b
Mean 250.9 318.9 444.5 91.8 343.7 291.6 148.7 324.1 230.2 149.2 329.9 314.4
Std.Error 59.8 83.3 87.9 17.6 86.4 69.2 21.7 50.6 26.9 17.9 44.9 36.4
Max 1972 4038 2581 867 4388 3234 722 1527 1068 1972 4388 3234
Min 8 2 5 2 1 1 2 4 12 2 1 1
Notes: Abundance and diversity metrics with different letters (a, b) in the same row indicate significant differences
(p < 0.05); F.O—frequency of observing; H’—waterfowl diversity index (using Shannon index); and EH —waterfowl
evenness index.

A Tukey test (all pairwise multiple comparisons) determined that there were differ-
ences in species diversity and the evenness of waterfowl surveys from May to September,
whereas the diversity and evenness of surveys from July were statistically different from
others and clearly lower than that of other months (Figure 2A and Table 3). By contrast, the
abundance of twenty-eight waterfowl was higher in July than in other months (ANOVA,
df = 302.8, F = 13.07, p < 0.001) (Figure 2B). Additionally, Tukey tests evaluated that the
abundance recorded by the surveys in July and September was no different, although
both of them differed statistically from the May survey with respect to the abundance of
waterfowl.

3.2. Spatial–Seasonal Variations of Waterfowl Diversity and Abundance and with Species
Similarity among Lakes
The lakes of eastern Mongolia observed a higher abundance of waterfowl than western
and central Mongolian lakes, but not significantly (Table 1 and Figure 2C). In contrast, the
species richness of the western and central Mongolian lakes was slightly higher than that
of the eastern Mongolian lakes (Tables 1 and 3). The ANOVA determined that the species
richness in the three regions differed statistically (ANOVA, df = 33.6, F = 7.73, p < 0.05).
The NMDS analysis specified 28 species of waterfowl that were affected by regional
variables (Figure 3). Tadorna tadorna and Anser cygnoid were highly abundant in the eastern
lakes with low altitudes and small sizes. In contrast, Anser fabalis, Anser indicus, Anas acuta,
Aythya marila, and Mergus merganser were found in western and central lakes with high
altitudes and large lakes. Furthermore, an NMDS (stress = 0.22) analysis of waterfowl
abundance based on Bray–Curtis revealed a distinct similar grouping in all three regions.
There was no dramatic separation of waterfowl species according to the regional level
(PERMANOVA: R2 = 0.15, F2,53 = 1.45, p = 0.1).

3.3. Species Diversity Metric-Lake Size Relationship Pattern

In order to confirm the diversity relationship results, we show the PCA of the diversity
metric for the three regions together with the lake surface area, altitude, and longitude
(Figure 4). As a general trend, the lakes of the same region are grouped together indepen-
dently with respect to the environmental factor. For example, the dispersion of the lakes in
central and western Mongolia are on the right side and the eastern lakes are on the left side.
The dominance index (D’) was negatively correlated with the lake surface area (R = 0.33,
p < 0.05) and positively explained the variations in the indices of waterfowl diversity (H’)
(R = 0.29, p < 0.05). By contrast, the richness of waterfowl was significantly and positively
correlated with the elevation (R = 0.38, p < 0.05). The longitude did not show a significant
correlation with the diversity metric and total abundance (p > 0.05) (Figure 4).

Diversity 2023, 15, 334
Diversity 2023, 15, x FOR PEER REVIEWFigure3.3.Non-metric
ern lakes with low altitudes and small sizes. In contrast, Anser fabalis, Anser indicus, Anas
acuta, Aythya marila, and Mergus merganser were found in western and central lakes with
high altitudes and large lakes. Furthermore, an NMDS (stress = 0.22) analysis of waterfowl
abundance based on Bray–Curtis revealed a distinct similar grouping in all three regions.
There was no dramatic separation of waterfowl species according to the regional 8 of level
14
(PERMANOVA: R2 = 0.15, F2,53 = 1.45, p = 0.1).
Figure
Non-metricmultidimensional scaling (NMDS)
multidimensional scaling (NMDS)ordination
ordinationofofthe
the waterfowl
waterfowl community
9 of 14
community
structure
structureunder
underthe
thedifferent
different regions.
regions.
3.3. Species Diversity Metric-Lake Size Relationship Pattern
In order to confirm the diversity relationship results, we show the PCA of the diver-
sity metric for the three regions together with the lake surface area, altitude, and longitude
(Figure 4). As a general trend, the lakes of the same region are grouped together inde-
pendently with respect to the environmental factor. For example, the dispersion of the
lakes in central and western Mongolia are on the right side and the eastern lakes are on
the left side. The dominance index (D’) was negatively correlated with the lake surface
area (R = 0.33, p < 0.05) and positively explained the variations in the indices of waterfowl
diversity (H’) (R = 0.29, p < 0.05). By contrast, the richness of waterfowl was significantly
and positively correlated with the elevation (R = 0.38, p < 0.05). The longitude did not show
a significant correlation with the diversity metric and total abundance (p > 0.05) (Figure
4).
Figure
Figure4.4.Principal
Principalcomponent
component analysis (PCA)correlation
analysis (PCA) correlationbiplot
biplotofofthe
the environment
environment and
and biological
biological
variables in the survey lakes.
variables in the survey lakes.
4.4.Discussion
Discussionand
andConclusions
Conclusions
Spatial–seasonalvariations
Spatial–seasonal variations and
and local
local environmental
environmentalfactors
factorsofofthe individual
the water-
individual water-
bodies are responsible for structuring aquatic bird assemblages [1,2,6,41]. Based on data
bodies are responsible for structuring aquatic bird assemblages [1,2,6,41]. Based on data
collected from 54 Mongolian lakes between 2016 and 2018, this study identified several
collected from 54 Mongolian lakes between 2016 and 2018, this study identified several
changes in the waterfowl community that were related to spatial–seasonal features and
changes in the waterfowl community that were related to spatial–seasonal features and
lake size (their associated wetlands). A high probability existed of observing Aythya fulig-
ula, Aythya ferina, Cygnus Cygnus, and T. ferruginea throughout the lakes. Also, Tadorna
ferruginea, Aythya ferina, Anser indicus, and Anser cygnoid were recorded more abundantly
than other species during the study period. The first two species (T. ferruginea and A.
Diversity 2023, 15, 334 9 of 14

lake size (their associated wetlands). A high probability existed of observing Aythya fuligula,
Aythya ferina, Cygnus Cygnus, and T. ferruginea throughout the lakes. Also, Tadorna ferrug-
inea, Aythya ferina, Anser indicus, and Anser cygnoid were recorded more abundantly than
other species during the study period. The first two species (T. ferruginea and A. ferina)
were observed commonly throughout the country; however, the composition of waterfowl
communities changed spatially with major contributions from A. indicus and A. cygnoid.
A. indicus was abundantly observed in the lakes of western and central Mongolia and is
mainly attributed to breeds in central Asia, from Kazakhstan and Kyrgyzstan in the extreme
east, across southern Russia to western Mongolia and the Qinghai–Tibetan Plateau, south
to Ladakh in India, and migrating along the Central Asian flyway [42,43]. By contrast,
A. cygnoid were copiously observed in the lakes of eastern Mongolia and some central Mon-
golian lakes. Studies in the past have indicated a high prevalence of A. cygnoid in eastern
Mongolia. In northeastern Mongolia, for instance, the small lakes of Mongol Daguur and
Buir Lake support the largest population of A. cygnoid by serving as stopover sites and
breeding habitats. Ganga Lake does the same in southeastern Mongolia [15,26,44–46]. The
global population trend reports announced A. ferina, A. cygnoid, and A. indicus are in a
downward trend, the trends of T. ferruginea and C. cygnus are unknown, and the other
two species are experiencing an upward trend [22,47–50]. Accordingly, considering only
the common and abundant species, the lakes and their associated wetlands in Mongolia
can show a high importance value in waterfowl conservation, particularly for the species
whose populations are globally and regionally decreased [15,22,25].
A large number of birds generally arrive in Mongolia by the East Asia—Australia
flyway to breed and forage [12,15]. Similarly, according to our study, there appeared
to be a higher abundance of waterfowl in Eastern Mongolia than in the western and
central Mongolian lakes. This is likely due to differences in habitat availability and water
levels between the regions. The PCA showed two main clusters of lake similarity, which
comprised the most central Mongolian lakes and all western Mongolian lakes (right side),
and some central Mongolian lakes and all Eastern Mongolian lakes (left side). Eastern
Mongolian lakes tend to have more wetland and shallow water habitats, while central and
western Mongolian lakes tend to have deeper open-water habitats [28]. For this study, these
differences in habitat types could contribute more to the observed differences in waterfowl
abundance among the regions than different flyways. Non-metric multidimensional scaling
(NMDS) was used to demonstrate the geographic dissimilarity of waterfowl species. We
did not find any differences in waterfowl community patterns between different lake sizes
of lakes and regions in different latitudes. These findings show no significant difference
between the species of waterfowl birds distributed in Mongolia; differences were observed
only within seasonal and same regions.
The seasonal analysis of waterfowl data showed that the species diversity and evenness
indices were higher in May and September than in July. There was no difference in
species diversity and the evenness of waterfowl in the surveys from May–September, while
the diversity and evenness in July were statistically different from others. A significant
difference was, however, not found in the species richness among the study months
(27 species in July and September and 28 species in May) for the chosen twenty-eight
waterfowl. Another way to put it is that the composition of the selected species was more
similar in May and September than in July. This can be explained in part by the seasonal
movement of waterfowl during migratory periods. Several studies have found that the
temporal variation in species diversity and the evenness of water birds is mainly driven by
migration and movement in the northern hemisphere during spring and fall [2,9,51].
A number of studies have indicated that habitat heterogeneity with the increasing size
of lakes and their associated wetlands is an influencing factor in the deviation of aquatic
bird diversity [2,3,6,7,15,41,51–53]. Our study shows that the richness and abundance of
waterfowl were not clearly related to the surface area of the lake. Regarding abundance,
some small lakes supported a greater number of waterfowl than large ones during the
migration terms. This might be attributable to the weak relationship between the lake size
Diversity 2023, 15, 334 10 of 14

and the average abundance, which some papers reported [2,54]. The waterfowl diversity
index was positively related to the surface area of the lake, whereas the species dominance
index showed a negatively correlation. It might be due to the fact that the increased surface
area of the lake decreases the habitat overlap for the designated waterfowl due to habitat
heterogeneity [2,6,55]. In other words, there is more chance to select suitable habitats for the
waterfowl seeking to breed, rest, and refuel. Accordingly, the composition of the waterfowl
species might become relatively equivalent in large lakes, and these indices may increase.
The richness in our study was restricted to a certain species of waterfowl; thus, it may not
appropriately elucidate the relationship with the size of a lake.
Furthermore, shallow lakes with a large surface area had a tendency to support larger
waterfowl assemblages during the migration seasons. The shallowness is also one of the
main physical factors influencing the community structure of the water birds (richness and
abundance) because the depth prerequisites of various feeding groups overlap [2,6,7,54,56].
Rich food availability also makes the waterfowl more flexible in foraging, and many
duck species may have high diet overlap in such a type of “super-abundant” foraging
habitat [57]. Generally, waterfowl utilize large amounts of protein during migration, nesting,
and molting, and they fulfill this requirement by consuming aquatic invertebrates [58].
As lakes become shallower, they are more likely to be highly diverse in aquatic plants,
which support a high number of aquatic invertebrates [54,59,60]. Therefore, the nutritional
requirements of waterfowl have been met in shallow lakes and wetlands where diverse
aquatic plant growth is abundant [60]. Additionally, the trophic state is a major factor
that influences the abundance and richness of species on lakes with shallowness and a
high primary productivity [5,6]. On one hand, some small lakes and the groups of small
lakes also support the same number and more waterfowl species when compared with
some medium-sized and large lakes. For instance, Erveekhii lake and Gun Tsengeleg lake,
which was one of the smallest lakes in our study, demonstrated a higher richness than
the Khoton, Dayan, Dood Tsagaan, and Telmen lakes, which were medium-sized and
large-sized lakes. The four groups of small lakes, which were the Tsengeleg Lakes, Tashgain
Tavan Lakes, Teshigiin Olon Lakes, and Uvsiin Baga-Bayan Lakes, had a greater abundance
of waterfowl with the same richness compared to larger lakes with an equivalent area.
Several studies suggested that a group of small lakes provides nearby alternative feeding
sites and a suitably undisturbed breeding habitat for waterfowl and contain high habitat
heterogeneity in the wetlands among small lakes [2,7].
Regardless of their size, all lakes and wetlands through certain flyways play a role
during waterfowl migration as a stopover site (staging post). These sites are crucial to
the success of the birds’ long migratory route, while water birds fly over and lack a direct
way around large expanses of land that lack acceptable wetlands and lakes for resting and
refueling, such as the Tibetan and Mongolian Plateau [2]. Therefore, the loss of any lakes
and wetlands through flyways can have a harmful impact on migratory birds [1,16,61].
The lakes studied are internationally designed as wetlands of great conservation value for
threatened species and migratory waterfowl, including the IBAs and the Ramsar sites in
Mongolia. These can include, for instance, the lakes of Mongol Daguur, the Valley of Lakes,
and Khar–Us Nuur National Park, located along the East Asia–Australia, Central Asian,
and Eastern Africa–West Asian flyways [12,13].
Unfortunately, some valuable lakes and wetlands in Mongolia have rapidly shrunk
and dried up due to intensive anthropogenic activities around the lakes (e.g., livestock over-
grazing, mining, etc.) and climate changes, which have decreased precipitation, increased
water evaporation, and increased the air temperature [12,18–23]. A rapid drying-out of
lakes was reported around Mongolia from 1996 to 2011 in accordance with the study of [62].
Furthermore, Kang and Hong (2016) [18], who analyzed the surface area of 73 lakes in
four different regions of Mongolia, identified that the lake area decreased by −9.3% at an
annual rate of −53.7 km2 yr−1 from 2001 to 2011 for the lakes studied. The study also
indicated slight-to-moderate decreases of lake surface area in semi-arid regions (desert
steppe) and rapid reductions of lake surface area in arid regions (Gobi Desert). According
Diversity 2023, 15, 334 11 of 14

to their study at Ugii lake, Sumiya et al. (2020) [20] revealed a significant decline in the total
precipitation and inflow river discharge and an increase in the total annual evaporation
and annual average temperature, as well as an abrupt diminishing of the lake surface
area (which reduced by 13.8% over 32 years). However, there is a lack of information on
the relationship between the lake surface area reduction and the water birds’ dynamics
in Mongolian lakes, in addition to the physical and chemical variations associated with
environmental conditions.
In summary, the presence of numerous migratory waterfowl recorded in our study
shows that Mongolian lakes are a hotspot habitat for waterfowl birds and are used as
breeding and stopover sites. We suggest that land-use changes and anthropogenic threats
in Mongolia can have a significant impact on heterogeneity in waterfowl communities
among lakes which may be greater than the impact of seasonal movements and migration
patterns. Anthropogenic threats, such as overgrazing, mining, and expanding land use,
have caused the degradation of wetland habitats, including the loss of vegetation and the
degradation of water quality [18,19,21]. This can reduce the availability of food resources
and nesting sites for waterfowl, as well as increase their vulnerability to predators and other
threats [1,58,63]. There was little indication that changing wetlands and lakes resulted
in a waterfowl habitat loss in Mongolia. A further monitoring program and frequent
research on lakes and their associated wetlands are crucial for developing fundamental
scientific resources for the conservation and management of waterbirds, with a priority
on anthropogenically induced impacts on lakes and their surroundings. For instance, the
factors should consider the degradation of land, water quality losses, and intense human
activities near shorelines.

Author Contributions: This paper received individual contributions from each author as specified:
Conceptualization: Z.P., N.J. and O.G.; data curation: Z.P., N.J. and O.G.; formal analysis: Z.P. and
N.J.; funding acquisition: W.K.P. and J.W.L.; investigation: Z.P., N.J., O.G., M.M., E.P., A.J. and I.-H.P.;
methodology: Z.P., N.J. and O.G.; software: Z.P. and N.J.; supervision: W.K.P. and J.W.L.; validation:
Z.P., O.G., M.M., E.P., A.J., I.-H.P., W.K.P. and J.W.L.; visualization: Z.P. and N.J.; writing—original
draft: Z.P. and N.J., writing—review & editing: Z.P., O.G. and J.W.L. All authors have read and agreed
to the published version of the manuscript.
Funding: This research was funded by the research fund of the R&D Program for Forest Science
Technology (Project No. 2021366B10-2223-BD 0131482092640102) provided by the Korea Forest
Service (Korea Forestry Promotion Institute).
Institutional Review Board Statement: Not applicable.
Data Availability Statement: Not applicable.
Acknowledgments: The authors appreciate the researchers and students of the Mongolian National
University of Education who participated in carrying out the field work. We would also like to
thank our research colleagues from the Mongolian National University of Education (MNUE), the
National Science Museum of Korea, and the Cultural Heritage Administration of the Republic of
Korea. This research was also sponsored by the National Research Foundation of Korea (NRF) and
funded by the Korean government (Ministry of Science and ICT) (Grant No. 2022M3H9A1097213).
The authors would also like to thank the Bio & Medical Technology Development Program of
the National Research Foundation (NRF), funded by the Korean government (MSIT) (No.NRF-
2017M3A9A5070202), for its support regarding the fieldwork.
Conflicts of Interest: The authors declare no conflict of interest.

References
1. Kirby, J.S.; Stattersfield, A.J.; Butchart, S.H.; Evans, M.I.; Grimmett, R.F.; Jones, V.R.; O’Sullivan, J.; Tucker, G.M.; Newton, I. Key
conservation issues for migratory land-and waterbird species on the world’s major flyways. Bird Conserv. Int. 2008, 18, S49–S73.
[CrossRef]
2. Ma, Z.; Cai, Y.; Li, B.; Chen, J. Managing wetland habitats for waterbirds: An international perspective. Wetlands 2010, 30, 15–27.
[CrossRef]
3. Nudds, T.D. Niche dynamics and organization of waterfowl guilds in variable environments. Ecology 1983, 64, 319–330. [CrossRef]
Diversity 2023, 15, 334 12 of 14

4. Roach, J.; Griffith, B. Climate-induced lake drying causes heterogeneous reductions in waterfowl species richness. Landsc. Ecol.
2015, 30, 1005–1022. [CrossRef]
5. Crozier, G.E.; Gawlik, D.E. Avian response to nutrient enrichment in an oligotrophic wetland, the Florida Everglades. Condor
2002, 104, 631–642. [CrossRef]
6. Hoyer, M.V.; Canfield, D.E. Bird abundance and species richness on Florida lakes: Influence of trophic status, lake morphology,
and aquatic macrophytes. In Aquatic Birds in the Trophic Web of Lakes; Springer: Dordrecht, The Netherlands, 1994; pp. 107–119.
[CrossRef]
7. Sebastián-González, E.; Green, A.J. Habitat use by waterbirds in relation to pond size, water depth, and isolation: Lessons from a
restoration in southern Spain. Restor. Ecol. 2014, 22, 311–318. [CrossRef]
8. Josens, M.L.; Haydee, E.A.; Favero, M. Seasonal variability of waterbird assemblages in relationship to habitat characteristics in a
Pampas wetland. Waterbirds 2009, 32, 523–530. [CrossRef]
9. Liao, J.T.; Ye, H.; Huang, T.F.; Peng, G.H. Seasonal waterbird population changes in Lashihai Lake in northwest Yunnan, China.
J. Mt. Sci. 2017, 14, 1852–1862. [CrossRef]
10. Pöysä, H.; Rintala, J.; Johnson, D.H.; Kauppinen, J.; Lammi, E.; Nudds, T.D.; Väänänen, V.M. Environmental variability and
population dynamics: Do European and North American ducks play by the same rules? Ecol. Evol. 2016, 6, 7004–7014. [CrossRef]
11. Gombobaatar, S.; Monks, E.M.; Seidler, R.; Sumiya, D.; Tseveenmyadag, N.; Bayarkhuu, S.; Baillie, J.; Boldbaatar, S.; Uuganbayar,
C. Regional Red List; Series Birds; Zoological Society of London, National University of Mongolia and Mongolian Ornithological
Society: London, UK, 2011; Volume 7.
12. Nyambayar, B.; Tseveenmyadag, N. (Eds.) Directory of Important Bird Areas in Mongolia: Key Sites for Conservation; Wildlife Science
and Conservation Center, Institute of Biology and BirdLife International: Ulaanbaatar, Mongolia, 2009.
13. Batnasan, N. Freshwater issues in Mongolia. In Proceedings of the National Seminar on IRBM in Mongolia, Ulaanbaatar,
Mongolia, 24–25 September 2003; p. 24.
14. Batbayar, N.; Purev-Ochir, G. Biodiversity and Artisanal and Small-Scale Mining in Mongolia; Scoping High Biodiversity Values in
Soums with Active Artisanal and Small-Scale Mining (ASM)within ESEC II Project Sites; Wildlife Science and Conservation of
Mongolia: Ulaanbaatar, Mongolia, 2004. [CrossRef]
15. Ganbold, O.; Bing, G.C.; Paik, I.H.; Purevee, E.; Munkhbayar, M.; Jargalsaikhan, A.; Paek, W.K. Avifauna of Mongol Daguur
important bird area in Eastern Mongolia. Korean J. Ornithol. 2017, 24, 13–23. [CrossRef]
16. BirdLife International. 2010. The Flyways Concept Can Help Coordinate Global Efforts to Conserve Migratory Birds. Available
online: http://www.birdlife.org (accessed on 13 July 2020).
17. Liu, H. Conservation of wetlands especially as waterfowl habitat in northeast China. Chin. Geogr. Sci. 1998, 8, 281–288. [CrossRef]
18. Kang, S.; Hong, S.Y. Assessing seasonal and inter-annual variations of lake surface areas in Mongolia during 2000-2011 using
minimum composite MODIS NDVI. PLoS ONE 2016, 11, e0151395. [CrossRef] [PubMed]
19. Tao, S.; Fang, J.; Zhao, X.; Zhao, S.; Shen, H.; Hu, H.; Tang, Z.; Wang, Z.; Guo, Q. Rapid loss of lakes on the Mongolian Plateau.
Proc. Natl. Acad. Sci. USA 2015, 112, 2281–2286. [CrossRef] [PubMed]
20. Sumiya, E.; Dorjsuren, B.; Yan, D.; Dorligjav, S.; Wang, H.; Enkhbold, A.; Weng, B.; Qin, T.; Wang, K.; Gerelmaa, T.; et al. Changes
in Water Surface Area of the Lake in the Steppe Region of Mongolia: A Case Study of Ugii Nuur Lake, Central Mongolia. Water
2020, 12, 1470. [CrossRef]
21. Bayarjargal, Y.; Adyasuren, T.; Munkhtuya, S. Drought and vegetation monitoring in the arid and semi-arid regions of the
Mongolia using remote sensing and ground data. In Proceedings of the 21st Asian Conference on Remote Sensing, Taipei, Taiwan,
4–8 December 2000; Volume 1, pp. 372–377.
22. Ganbold, O.; Bing, G.C.; Lee, J.H.; Munkhbayar, M.; Paik, I.H.; Jargalsaikhan, A.; Purevee, E.; Purevdorj, Z.; Paek, W.K. An
avifaunal survey of middle Mongolian wetlands: Important Bird Areas and threatened species. J. Asia-Pac. Biodivers. 2018, 11,
340–345. [CrossRef]
23. Kang, S.; Lee, G.; Togtokh, C.; Jang, K. Characterizing regional precipitation-driven lake area change in Mongolia. J. Arid. Land
2014, 7, 146–158. [CrossRef]
24. Nyambayar, B.; Tuvshinjargal, E.; David, W.; Otgonbayar, T.; Tseveenmyadag, N. For the migration survey of Mongolian birds.
J. Toodog 2016, 2, 10–16. (In Mongolian)
25. Purevdorj, Z.; Paek, W.K.; Munkhbayar, M.; Ganbold, O.; Bing, G.C.; Jargalsaikhan, A.; Purevee, E.; Paik, I.H.; Choi, W.S.; Jargal,
N.; et al. The avifaunal survey at Important Bird Areas in western Mongolia. Korean J. Ornitol. 2019, 26, 7–15. [CrossRef]
26. Tuvshintugs, S.; Gankhuyag, P.; Bolormunkh, E.; Tseveenmyadag, N. The avifauna and their conservation in Dariganga Nature
Park, Mongolia. J. Toodog 2016, 2, 1–9. (In Mongolian)
27. Tian, S.; Xu, X.L.; Liu, S.T.; Zhang, S.P. The influence of Dalai Lake area change on waterbird community. Sichuan J. Zool. 2016, 35,
201–209. [CrossRef]
28. Limnological Gatalog of Mongolian Lakes 2015. Available online: http://oslo.geodata.es/mongolian_lakes/map/mongolia-map.
php?lang=en (accessed on 15 May 2020).
29. Mitamura, O.; Khadbaatar, D.; Ishida, N. Comparative investigation of chemical and biological characteristics in waters and
trophic state of Mongolian lakes. Limnology 2010, 11, 17–30. [CrossRef]
30. Tserensodnom, J. Catalog of Mongolian Lakes; The Institute of Geography, Mongolian Academy of Science: Ulaanbaatar, Mongolia,
2000; pp. 26–58.
Diversity 2023, 15, 334 13 of 14

31. Bibby, C.J.; Burgess, N.D.; Hill, D.A. Bird Census Techniques; Academic Press: London, UK, 1992.
32. Shannon, C.E.; Weaver, W. The Mathematical Theory of Communication; University of Illinois Press: Champaign, IL, USA, 1963.
33. Pielou, E.C. The measurement of diversity in different types of biological collections. J. Theor. Biol. 1966, 13, 131–144. [CrossRef]
34. Simpson, E. Measurement of Diversity. Nature 1949, 163, 688. [CrossRef]
35. Davis, J.C. Statistics and Data Analysis in Geology; John Wiley & Sons: New York, NY, USA, 1986.
36. R Core Team. R: A Language and Environment for Statistical Computing; R Foundation for Statistical Computing: Vienna, Austria,
2015. Available online: https://www.R-project.org/ (accessed on 22 January 2023).
37. Anderson, M.J. A new method for non-parametric multivariate analysis of variance. Austral. Ecol. 2001, 26, 32–46.
38. Oksanen, J.; Simpson, G.L.; Blanchet, F.G.; Kindt, R.; Legendre, P.; Minchin, P.R.; O’Hara, R.B.; Solymos, P.; Stevens, M.H.H.;
Szoecs, E.; et al. Vegan: Community Ecology Package. 2019. Available online: https://cran.r-project.org/package=vegan
(accessed on 5 January 2022).
39. Legendre, P.; Gallagher, E.D. Ecologically meaningful transformations for ordination of species data. Oecologia 2001, 129, 271–280.
[CrossRef] [PubMed]
40. Francois, H.; Sebastien Le, S.; Pagès, J. Exploratory Multivariate Analysis by Example Using R, 2nd ed.; Chapman Hall/CRC: Boca
Raton, FL, USA, 2017. Available online: http://factominer.free.fr/bookV2/index.html (accessed on 10 January 2023).
41. Paracuellos, M.; Tellería, J.L. Factors affecting the distribution of a waterbird community: The role of habitat configuration and
bird abundance. Waterbirds 2004, 27, 446–453. [CrossRef]
42. Batbayar, N.; Takekawa, J.Y.; Natsagdorj, T.; Spragens, K.A.; Xiao, X. Site selection and nest survival of the Bar-headed Goose
(Anser indicus) on the Mongolian Plateau. Waterbirds 2014, 37, 381–393. [CrossRef]
43. Liu, D.; Zhang, G.; Li, F.; Ma, T.; Lu, J.; Qian, F. A revised species population estimate for the bar-headed goose (Anser indicus).
Avian Res. 2017, 8, 7. [CrossRef]
44. Batbayar, N.; Takekawa, J.Y.; Newman, S.H.; Prosser, D.J.; Natsagdorj, T.; Xiao, X. Migration strategies of Swan Geese Anser
cygnoides from northeast Mongolia. Wildfowl 2011, 61, 90–109.
45. Goroshko, O.A. Extremely unfavourable year (2003) for Swan Geese in Dauria trans-boundary region (Russia and Mongolia). In
Proceedings of the International Anatidae Symposium in East Asia & Siberia Region, Seosan, Korea, 31 October–3 November
2003; pp. 83–92.
46. Goroshko, O.A. Data for waterbirds at Buyr-Nuur (Eastern Mongolia). Mong. J. Biol. Sci. 2004, 2, 67–68. [CrossRef]
47. BirdLife International. Tadorna ferruginea. The IUCN Red List of Threatened Species 2016:e.T22680003A86011049. 2016. Available
online: https://dx.doi.org/10.2305/IUCN.UK.2016-3.RLTS.T22680003A86011049.en (accessed on 19 August 2021).
48. BirdLife International. Anser cygnoid. The IUCN Red List of Threatened Species 2016: E.T22679869A92832782. 2016. Available
online: https://dx.doi.org/10.2305/IUCN.UK.2016-3.RLTS.T22679869A92832782.en (accessed on 19 August 2021).
49. BirdLife International. Cygnus cygnus. The IUCN Red List of Threatened Species 2016: E. T22679856A85965262. 2016. Available
online: https://dx.doi.org/10.2305/IUCN.UK.2016-3.RLTS.T22679856A85965262.en (accessed on 19 August 2021).
50. BirdLife International. Anser indicus. The IUCN Red List of Threatened Species 2018: E.T22679893A131908564. 2018. Available
online: https://dx.doi.org/10.2305/IUCN.UK.2018-2.RLTS.T22679893A131908564.en (accessed on 19 August 2021).
51. Hattori, A.; Mae, S. Habitat use and diversity of waterbirds in a coastal lagoon around Lake Biwa, Japan. Ecol. Res. 2001, 16,
543–553. [CrossRef]
52. Colwell, M.A.; Taft, O.W. Waterbird communities in managed wetlands of varying water depth. Waterbirds 2000, 23, 45–55.
53. Guadagnin, D.L.; Maltchik, L. Habitat and landscape factors associated with neotropical waterbird occurrence and richness in
wetland fragments. Biodivers. Conserv. 2007, 16, 1231–1244. [CrossRef]
54. Scheffer, M.; Van Geest, G.J.; Zimmer, K.; Jeppesen, E.; Søndergaard, M.; Butler, M.G.; Hanson, M.A.; Declerck, S.; De Meester, L.
Small habitat size and isolation can promote species richness: Second-order effects on biodiversity in shallow lakes and ponds.
Oikos 2006, 112, 227–231. [CrossRef]
55. Elmberg, J.; Nummi, P.; Poysa, H.; Sjoberg, K. Relationships between species number, lake size and resource diversity in
assemblages of breeding waterfowl. J. Biogeogr. 1994, 21, 75–84. [CrossRef]
56. Tavares, D.C.; Guadagnin, D.L.; de Moura, J.F.; Siciliano, S.; Merico, A. Environmental and anthropogenic factors structuring
waterbird habitats of tropical coastal lagoons: Implications for management. Biol. Conserv. 2015, 186, 12–21. [CrossRef]
57. Nummi, P.; Väänänen, V.M. High overlap in diets of sympatric dabbling ducks—An effect of food abundance? In Annales
Zoologici Fennici; Finnish Zoological and Botanical Publishing Board: Helsinki, Finland, 2001; pp. 123–130. Available online:
https://www.jstor.org/stable/23735758 (accessed on 31 May 2020).
58. Fredrickson, L.H.; Reid, F.A. Nutritional Values of Waterfowl Foods. In Waterfowl Management Handbook; U.S. Fish and Wildlife
Service: Fort Collins, CO, USA, 1988.
59. Gregg, W.W.; Rose, F.L. Influences of aquatic macrophytes on invertebrate community structure, guild structure, and microdistri-
bution in streams. Hydrobiologia 1985, 128, 45–56. [CrossRef]
60. Wersal, R.M.; Getsinger, K.D. Chapter 3: Impacts of invasive aquatic plants on waterfowl. In Biology and Control of Aquatic
Plants: A Best Management Practices Handbook; Aquatic Ecosystem Restoration Foundation: Marietta, GA, USA, 2009; Volume 210,
pp. 19–24.
61. Hutto, R.L. On the importance of stopover sites to migrating birds. Auk 1998, 115, 823–825. [CrossRef]
Diversity 2023, 15, 334 14 of 14

62. Ministry of Environment and Green Development. Mongolian Second Assessment Report on Climate Change; Ministry of Environment
and Tourism: Ulaanbaatar, Mongolia, 2014; pp. 109–126.
63. Fredrickson, L.H.; Drobney, R.D. Habitat utilization by post breeding waterfowl. In Waterfowl and Wetlands: An Integrated Review;
Midwest Fish & Wildlife Conference: Overland Park, KS, USA, 1979; pp. 119–127.

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