sustainability
Article
Distribution Patterns and Driving Factors of the Phytoplankton
Community in the Middle Reaches of the Yarlung Zangbo River
Xiaodong Li 1,2 , Peng Zhang 2 , Qing Yang 1,2 , Huiqiu Liu 1,2 , Xin Chao 1,2 , Shengxian Yang 1,2 and Sang Ba 1,2, *
Citation: Li, X.; Zhang, P.; Yang, Q.;
Liu, H.; Chao, X.; Yang, S.; Ba, S.
Distribution Patterns and Driving
Factors of the Phytoplankton
Community in the Middle Reaches of
the Yarlung Zangbo River.
Sustainability 2023, 15, 7162. https://
doi.org/10.3390/su15097162
Academic Editor: Giulia Caneva
Received: 13 March 2023
Revised: 15 April 2023
Accepted: 23 April 2023
Published: 25 April 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/).
Sustainability 2023, 15, 7162. https://doi.org/10.3390/su15097162
1 Center for Carbon Neutrality in the Earth’s Third Pole, Tibet University, Lhasa 850000, China;
lixiaodong2021911@163.com (X.L.); yangqing970323@163.com (Q.Y.); liuhuiqiuer@163.com (H.L.);
15116198986@163.com (X.C.); 18285500432@163.com (S.Y.)
2 Laboratory of Wetland and Catchments Ecology in Tibetan Plateau, School of Ecology and Environment,
Tibet University, Lhasa 850000, China; pengzhang09@126.com
* Correspondence: hbasang2003@aliyun.com
Abstract: The middle reaches of the Yarlung Zangbo River are a hot zone of the Alpine Water System
and its ecological environment is diverse but vulnerable. We systematically examined and detailed
the phytoplankton community’s composition, spatial-temporal dynamics, and driving factors in
this area. A total of 224 samples from 28 sampling sites across wet and dry seasons were analyzed.
The results showed that: (1) the community structure of the main stream is more complex and
stable than that of the tributaries; (2) the number of species, average cell abundance, and average
biomass in the main stream were higher than those in the tributaries; (3) TN, TUR, WT, and pH
were the main influencing factors for the difference in the phytoplankton community’s structure
between the main stream and the tributaries; (4) the phytoplankton community had a closer structure,
higher connectivity, stronger resistance to environmental disturbance, and higher stability in the main
stream, while those in the tributaries had higher interspecific synergy; and (5) the phytoplankton
community’s assembly process in the main stream was mainly influenced by random processes and
was mainly driven by dispersal limitation in the middle reaches of the Yarlung Zangbo River.
Keywords: water environmental factors; phytoplankton; community composition; community
assembly; Yarlung Zangbo River
1. Introduction
Phytoplankton belong to eukaryotic micro-organisms in water bodies which are com-
posed of diatoms, cyanobacteria, green algae, naked algae, etc., and are important compo-
nents of rivers and lakes [1–4]. As an important primary producer, it plays an important
role in the material cycle and energy flow of the aquatic ecosystem. Its community charac-
teristics can respond quickly to changes in water environmental quality [5–7] and directly
to changes in nutrient level and are often used as indicator organisms and the basis for
water quality assessments [8,9]. Therefore, the study of phytoplankton provides useful
information for monitoring water quality [10,11] and important materials for exploring the
origin and evolution of micro-organisms.
As the “third pole of the Earth”, the Qinghai–Tibet Plateau has attracted extensive
attention from international scholars who study biological origins, evolution, flora, and
migration because of its unique geographical climate [12]. The wide area of the Yarlung
Zangbo River valley has a high average elevation, long sunshine time, and low temperature.
It is the highest area in the biodiversity of the Qinghai–Tibet plateau, with a vulnerable
ecological environment. The Yarlung Zangbo River has great significance in the study of
the plateau’s climate and the ecological environment of its special geographical location.
The study of phytoplankton distribution patterns in the middle reaches of the Yarlung
Zangbo River plays an important part in the management of the whole basin’s aquatic
ecosystem and the protection of its biodiversity. However, at present, studies on the
https://www.mdpi.com/journal/sustainability
Sustainability 2023, 15, 7162 2 of 14

phytoplankton community in the middle reaches of the Yarlung Zangbo River mainly focus
on the major tributaries [13–16], and there are no reports on the distribution patterns of the
phytoplankton community in the main stream and tributaries of the region.
In this study, we examined the phytoplankton species’ composition and community
features in the Yarlung Zangbo River’s middle reaches, analyzed the drivers of the phyto-
plankton community’s building process, and explored the phytoplankton species’ diversity
and ecology value. This study provides a scientific basis for the conservation of biodiversity
and ecological research on the Qinghai–Tibet Plateau and the optimal management of the
water ecosystem on the Qinghai–Tibet Plateau.

2. Materials and Methods

2.1. Survey of Study Area and Layout of Sampling Points
The Yarlung Zangbo River’s source is the Jama Yangzong Glacier at the northern foot
of the Himalayas, and its basin is located between the Gangdise and Nianqing Tanggula
Mountains and the Himalayan mountains [17]. It is the highest river in the world with the
largest elevation difference. The ecological and geographical environments of different
reaches are obviously different, and the total length of the river in China is 2057 km. The
basin ranges from 28◦ 000 to 31◦ 160 north latitude and 82◦ 000 to 97◦ 070 east longitude [18],
and the average altitude is over 3000 m.
The river is divided according to the topographic characteristics and climate types
of the basin: Lazi-pai Town is in the middle reaches of the basin, with a length of about
1293 km and a basin area of 165,000 km2 . The two banks of the river are dominated by
floodplains, and the annual average precipitation ranges from 300 mm to 600 mm, with a
plateau temperate semi-arid climate [19,20].
According to the layout principle of the surface water quality monitoring section and
the natural environment state of the middle reaches of the Yarlung Zangbo River, a total of
28 sampling points were set up in the middle reaches of the Yarlung Zangbo River (Figure 1,
Table 1, Supplementary Materials Figure S1, Table S1), including 11 sampling points of the
main stream and 17 sampling points of the tributaries. The longitude and latitude of each
sampling point were recorded by a GPS instrument. Phytoplankton samples were collected
in July 2021 (wet season) and October 2021 (dry season), and the physicochemical factors
of the water were measured.

Table 1. Information on sampling points in the middle reaches of the Yarlung Zangbo River.

Number Type Longitude Latitude Altitude (m) Depth of Water (cm) Velocity of Flow (m/s)
Y1 main stream 90◦ 470 26.8800 29◦ 160 35.7600 3537.0 58.0 0.1
Y2 main stream 91◦ 270 47.16” 29◦ 150 46.0800 3527.0 70.0 0.4
Y3 tributary 91◦ 510 42.4800 29◦ 30 25.5600 3714.0 69.0 0.7
Y4 tributary 91◦ 540 29.5200 28◦ 520 57.3600 4113.0 41.0 0.6
Y5 tributary 91◦ 530 37.6800 28◦ 490 14.1600 4505.0 55.0 1.1
Y6 tributary 91◦ 570 5.0400 28◦ 530 30.1200 4221.0 37.0 1.7
Y7 tributary 92◦ 00 12.9600 28◦ 500 33.3600 4740.0 39.0 0.4
Y8 main stream 91◦ 550 2100 29◦ 160 15.9600 3510.0 30.0 0.2
Y9 tributary 92◦ 10 25.6800 29◦ 110 38.0400 3571.0 45.0 0.6
Y10 tributary 92◦ 130 41.8800 29◦ 30 4.3200 3880.0 36.0 1.3
Y11 tributary 92◦ 10 13.800 29◦ 150 26.6400 3513.0 25.0 0.4
Y12 tributary 92◦ 20 37.3200 29◦ 200 11.0400 3752.0 34.0 0.7
Y13 main stream 92◦ 340 29.2800 29◦ 80 52.0800 3166.0 47.0 1.9
Y14 tributary 92◦ 400 0.8400 29◦ 100 2.6400 3369.0 60.0 1.9
Y15 tributary 92◦ 440 47.7600 29◦ 200 4.200 4137.0 70.0 0.5
Y16 main stream 92◦ 420 7.9200 29◦ 60 36.3600 3116.0 50.0 0.2
Y17 main stream 92◦ 530 52.4400 29◦ 30 57.2400 3076.0 70.0 0.6
Y18 tributary 93◦ 190 15.9600 28◦ 590 57.1200 3012.0 41.0 1.6
Y19 tributary 93◦ 240 3600 28◦ 520 33.2400 3479.0 37.0 1.0
Y20 main stream 93◦ 260 54.9600 29◦ 60 23.7600 2945.0 50.0 0.7
 Sustainability 2023, 15, 7162 3 of 14

Table 1. Cont.

Number Type Longitude Latitude Altitude (m) Depth of Water (cm) Velocity of Flow (m/s)
Y21 main stream 93◦ 350 40.9200 29◦ 100 5.1600 2934.0 50.0 0.1
Y22 tributary 93◦ 520 10.9200 29◦ 60 3.600 2956.0 40.0 1.0
Y23 tributary 93◦ 510 54.7200 28◦ 590 18.2400 3203.0 50.0 3.1
Y24 main stream 94◦ 260 4.5600 29◦ 240 33.4800 2896.0 50.0 0.1
Y25 tributary 94◦ 430 32.5200 29◦ 260 36.9600 2914.0 45.0 1.2
Y26
Sustainability 2023, 15,tributary 94◦ 440 2400
x FOR PEER REVIEW 29◦ 250 13.0800 2986.0 40.0 0.7 3 of 15
Y27 main stream 94◦ 440 41.2800 29◦ 270 19.800 2886.0 40.0 0.2
Y28 main stream 94◦ 520 53.7600 29◦ 310 32.8800 2874.0 43.0 0.1

Figure
Figure 1. The
1. The settingofofsampling
setting sampling points
points in
inthe
themiddle
middlereaches of the
reaches Yarlung
of the Zangbo
Yarlung River.River.
Zangbo
2.2. Sample Collection and Processing
Table 1. Information on sampling points in the middle reaches of the Yarlung Zangbo River.
Phytoplankton samples were collected and identified according to the methods speci-
Number Type fied in the Freshwater
Longitude PlanktonAltitude
Latitude Research(m)
Methods
Depth[21].ofFor the qualitative
Water characterization,
(cm) Velocity of Flow (m/s)
the samples were collected by plankton net with a pore size of 10 µm 0.5 m below the sur-
Y1 main stream 90°47′26.88″ 29°16′35.76″ 3537.0 58.0 0.1
face of the water body in a “∞” shape (8–10 min). The collected filtrate samples were stored
Y2 main stream 91°27′47.16″ 29°15′46.08″
in a 4% formaldehyde 3527.0
solution. The 70.0 in the room and sealed
samples were pretreated 0.4 into
Y3 tributary 91°51′42.48″
thin slices. An29°3′25.56″
OLYMPUS CKX533714.0 inverted fluorescence69.0microscope was used for0.7 species
Y4 tributary 91°54′29.52″
identification.28°52′57.36″ 4113.0
Phytoplankton identification was based41.0 0.6 For
on classical literature [22–24].
Y5 tributary the quantitative
91°53′37.68″ characterization,4505.0
28°49′14.16″ a 1 L mixed water sample
55.0 was collected from1.1 0–0.5 m
Y6 tributary below the
91°57′5.04″ surface of the
28°53′30.12″ water body and
4221.0 immediately fixed
37.0 with Luger’s reagent.
1.7 The
Y7 tributary 92°0′12.96″ 28°50′33.36″ 4740.0 39.0 0.4
Y8 main stream 91°55′21″ 29°16′15.96″ 3510.0 30.0 0.2
Y9 tributary 92°1′25.68″ 29°11′38.04″ 3571.0 45.0 0.6
Sustainability 2023, 15, 7162 4 of 14

sample was brought back to the laboratory for precipitation for 48 h and concentrated
to 50 mL. The 0.1 mL concentrated solution was then transferred to a 0.1 mL counting
plate and the entire slide was counted at 10 × 40 magnification, with each sample counted
2–3 times. The phytoplankton abundance was converted into biomass (fresh weight) using
an appropriate volume formula, and its specific gravity was assumed to be 1.0, that is,
the biomass is the phytoplankton abundance multiplied by the average wet weight of the
respective volume [25–27].
A HI98195 high-precision portable multi-parameter comprehensive water quality
tester (HANNA, Woonsocket, Italy) was used for the determination of water pH (pH),
conductivity (EC), salinity (Salt), water temperature (WT), and water velocity (V) using
an FP-111 direct reading type current meter (Global Water, Phoenix, AZ, USA). The dis-
solved oxygen (DO) was measured by a HI98193 microcomputer dissolved oxygen tester
(HANNA, Woonsocket, Italy), the ammonia nitrogen (NH3 -N) was measured by salicylic
acid spectrophotometry, and the turbidity (TUR) was measured by a HI98703 microcom-
puter multi-range turbidity tester (HANNA, Woonsocket, Italy); three parallel tests were
carried out, respectively. Water samples were collected, stored, and transported in strict
accordance with GB3838-2002 Quality Standards for Surface Water Environment, and sent
to the qualified testing company for the determination of total phosphorus (TP), total
nitrogen (TN), nitrate nitrogen (NO3 -N), and dichromate index (COD).

2.3. Data Processing and Analysis

The main diversity indices were the Margalef richness index (d) [28], the Simpson
dominance index (DS ) [29], the Shannon–Wiener diversity index (H0 ) [30], and the Pielou
Evenness index (J) [31]. These four indices were used to calculate phytoplankton biodi-
versity in the middle reaches of the Yarlung Zangbo River. The calculation formula is
as follows:
S−1
d= (1)
ln N
S
Ds = 1 − ∑ ( Pi )2 (2)
i =1

S
H 0 = − ∑ Pi × ln Pi (3)
i =1

J = H 0 /InS (4)
where S is the number of species at the sampling point; N is the cell abundance of all
phytoplankton at the sampling site; and Pi is the proportion of individuals of type i.
The differences between the 12 water environmental factors in the main stream and
tributaries of the middle reaches of the Yarlung Zangbo River were analyzed. Besides pH,
the data were normalized to the logarithm and used for the t-test. The Wilcoxon rank-sum
test was performed after calculating the α diversity index of phytoplankton communities in
different reaches of the middle reaches of the Yarlung Zangbo River. Spearman’s correlation
analysis was performed on the phytoplankton’s α diversity index and water environmental
factors in the middle reaches of the Yarlung Zangbo River. A Mantel test analysis was
conducted on the phytoplankton species (S), cell abundance (A), and biomass (B) in the
middle reaches of the Yarlung Zangbo River with significant differences compared to water
environmental factors. The neutral community model was used to predict the relationship
between the occurrence frequency of the phytoplankton community and its cell abundance.
The ArcMap 10.8 software was used to draw maps, the Excel 2016 software was
used to calculate phytoplankton species, cell abundance, and biomass, and the OriginPro
2019 software was used to map the community structure. The ggplot2 package in R
software (version 3.4.2) was used to draw boxplots of water environmental factors. The
α diversity index was calculated using R software. Principal Coordinate analysis (PCoA)
 Sustainability 2023, 15, 7162 5 of 14

and Similarity analysis (ANOSIM) were used to calculate the Bray–Curtis distance and
draw the ranking map by using the package of R and ggplot2. The heatmap package of
R software was used to draw the correlation heatmap. The Spearman correlation among
phytoplankton was calculated by the Hmisc package of R software to construct the co-
occurrence network, which was visualized in Gephi (version 0.9.2). The neutral community
model was visualized using the minpack.lm package in R software.

3. Results
3.1. Difference Analysis of Water Environmental Factors in Different River Reaches
As shown in Figure 2, the pH of the main stream (8.31) was significantly higher than
that of the tributaries (7.61). WT of the main stream (17.47 ◦ C) was significantly higher
than that of the tributary (10.25 ◦ C). The NO3 -N of the main stream (0.36 mg·L−1 ) was
significantly higher than that of the tributary stream (0.18 mg·L−1 ). The TUR of the main
stream (126.09 NTU) was significantly higher than that of the tributary (32.86 NTU). V of
the main stream (0.41 m·s−1 ) was significantly lower than that of the tributary (0.86 m·s−1 ).
TN in the main stream (0.65 mg·L−1 ) was significantly higher than that in the tributary
Sustainability 2023, 15, x FOR PEER REVIEW 6 of 15
stream (0.42 mg·L−1 ). Other water environmental factors, including EC, Salt, COD, DO,
NH3 -N, and TP, were not different in the main and tributary streams.

Figure
Figure 2. Difference
2. Difference analysisofofwater
analysis water environmental
environmental factors
factorsin in
different reaches
different of the
reaches of Yarlung
the Yarlung
Zangbo
Zangbo River (* p(* <p 0.05;
River < 0.05;****p p<<0.01; *** pp << 0.001,
0.01;*** 0.001, t-test).
t-test).(M)
(M)main
main stream. (T)(T)
stream. tributary.
tributary.
3.2. Spatio-Temporal Distribution Patterns of Phytoplankton Communities
3.2. Spatio-Temporal Distribution Patterns of Phytoplankton Communities
From the perspective of the two hydrological periods, the overlap degree of phyto-
From the
plankton perspective
community of the
clusters in two hydrological
the wet season and periods, the overlap
the dry season was highdegree
at theof
95%phyto-
plankton community
confidence clusters
interval (Figure inindicating
3a), the wet season
the highand the dry
similarity season was high
of phytoplankton at the 95%
communi-
confidence interval
ties between (Figure
the wet and dry 3a), indicating
seasons. From the high similarity
the different of phytoplankton
river reaches, commu-
the phytoplankton
communities in the tributaries and the main stream could be clearly separated,
nities between the wet and dry seasons. From the different river reaches, the phytoplank- and there
tonwas only a smallin
communities overlap area of phytoplankton
the tributaries and the main community clustersbe
stream could in clearly
the 95% separated,
confidence and
interval
there (Figure
was only 3b). The
a small resultsarea
overlap of ANOSIM showed that
of phytoplankton the phytoplankton
community clusterscommunities
in the 95% con-
in the main stream and the tributaries were significantly different.
fidence interval (Figure 3b). The results of ANOSIM showed that the phytoplankton com-
munities in the main stream and the tributaries were significantly different.

Sustainability 2023, 15, 7162
plankton community clusters in the wet season and the dry season was high at the 95%
confidence interval (Figure 3a), indicating the high similarity of phytoplankton commu-
nities between the wet and dry seasons. From the different river reaches, the phytoplank-
ton communities in the tributaries and the main stream could be clearly separated, and
there was only a small overlap area of phytoplankton community clusters in the 95% con-
fidence interval (Figure 3b). The results of ANOSIM showed that the phytoplankton6com-
of 14
munities in the main stream and the tributaries were significantly different.

Figure3.
Figure 3. Similarity
Similarity analysis
analysis of
of the
the phytoplankton
phytoplankton community
community in in the
the middle
middle reaches
reaches of
of the
theYarlung
Yarlung
ZangboRiver.
Zangbo River.(a)
(a)Similarity
Similarity
ofof phytoplankton
phytoplankton communities
communities in different
in different hydrological
hydrological periods.
periods. (b)
(b) Sim-
Similarity of phytoplankton communities in different river reaches. (M) main stream. (T)
ilarity of phytoplankton communities in different river reaches. (M) main stream. (T) tributary. tributary.

3.3.
3.3. Differences
Differences inin Alpha
Alpha Diversity
Diversity ofof Phytoplankton
Phytoplankton Communities
Communities
As
As shown
shown in in Figure
Figure 4,4, the
theSimpson
Simpson dominance
dominance index
index ofof the
the main
main stream
stream (0.94)
(0.94) was
was
higher than that of the tributary stream (0.92), and there was no significant
higher than that of the tributary stream (0.92), and there was no significant difference.
Sustainability 2023, 15, x FOR PEER REVIEW difference. The
7 ofThe
15
Shannon–Wiener
Shannon–Wiener diversitydiversity index
index inin the
the main
main stream
stream (3.89)
(3.89) was
was significantly
significantly higher
higher than
than
that
that in
in the
the tributary
tributary stream
stream (3.46).
(3.46). The
The Margalef
Margalef richness
richness index
index of thethe main
main stream
stream (8.16)
(8.16)
was
was significantly
significantly higher
higher than
than that
that of
of the
the branch
branch stream
stream(4.99).
(4.99). The
The Pielou
Pielou evenness
evenness index
index
of the
of the main
main stream
stream (0.83)
(0.83) was
was smaller
smaller than
than that
that of
of the
the tributaries
tributaries (0.87),
(0.87), and there was
and there was nono
significant difference.
significant difference.

Figure 4. Diversity
Diversity index
index of
of the
the phytoplankton
phytoplankton community
community in different
different reaches of the middle reaches
of the
of the Yarlung
Yarlung Zangbo
ZangboRiver
River(**(**pp<<0.01;
0.01;******
p <p 0.001, Wilcoxon
< 0.001, rank-sum
Wilcoxon rank-sumtest). (M)(M)
test). main stream.
main (T)
stream.
tributary.
(T) tributary.

3.4. Characteristics of the Phytoplankton Community’s Structure Structure

A total of
of 140
140genera
generaof ofphytoplankton
phytoplanktonwere wereidentified,
identified,belonging
belonging toto
7 phyla,
7 phyla,1111
classes,
clas-
24 orders, and 47 families, and the overall community characteristics were
ses, 24 orders, and 47 families, and the overall community characteristics were Bacillari- Bacillariophyta,
Chlorophyta, and Cyanophyta
ophyta, Chlorophyta, (Figure (Figure
and Cyanophyta 5a). A total
5a). Aoftotal
99 genera of phytoplankton
of 99 genera were
of phytoplankton
identified in theinmain
were identified stream,
the main belonging
stream, to 6 phyla,
belonging 8 classes,
to 6 phyla, 20 orders,
8 classes, andand
20 orders, 38 families.
38 fam-
Bacillariophyta accounted
ilies. Bacillariophyta for 70.67%,
accounted Chlorophyta
for 70.67%, 14.32%,
Chlorophyta Cyanophyta
14.32%, 11.09%,
Cyanophyta and other
11.09%, and
phyla 3.92%.3.92%.
other phyla A total of 123
A total of genera of phytoplankton
123 genera of phytoplankton were identified
were in the
identified tributaries,
in the tributar-
belonging to 7 to
ies, belonging phyla, 10 classes,
7 phyla, 23 orders,
10 classes, andand
23 orders, 46 families. Bacillariophyta
46 families. accounted
Bacillariophyta accountedfor
54.24%, Chlorophyta for 23.94%, Cyanophyta for 16.10%, and other
for 54.24%, Chlorophyta for 23.94%, Cyanophyta for 16.10%, and other phyla for 5.72%.phyla for 5.72%. The
average
The averagecell cell
abundance
abundance in the main
in the mainstream
streamof of
thethemiddle
middleofofthe
theYarlung
YarlungZangbo
Zangbo River
River
was 7.83 × 10 5 cells·L−1 and was 1.62 × 105 cells·L−1 in the tributaries. Bacillariophyta
was 7.83 × 105 cells·L−1 and was 1.62 × 105 cells·L−1 in the tributaries. Bacillariophyta was
was dominant
dominant in theincell
theabundance
cell abundance
in bothinmain
bothstream
main stream and tributaries,
and tributaries, followedfollowed
by Chloro- by
Chlorophyta and Cyanophyta, and the percentage of other species was
phyta and Cyanophyta, and the percentage of other species was small. The average bio- small. The average
mass of the main stream in the middle reaches of the Yarlung Zangbo River was 0.897
mg·L−1, and the average biomass of the tributaries was 0.372 mg·L−1. The biomass of dia-
toms was higher than that of other species in both the main stream and tributaries. The
Wilcoxon rank-sum test was performed for phytoplankton community parameters in the
 Sustainability 2023, 15, 7162 7 of 14

biomass of the main stream in the middle reaches of the Yarlung Zangbo River was
0.897 mg·L−1 , and the average biomass of the tributaries was 0.372 mg·L−1 . The biomass
of diatoms was higher than that of other species in both the main stream and tributaries.
Sustainability 2023, 15, x FOR PEER REVIEW Wilcoxon rank-sum test was performed for phytoplankton community parameters8 of 15
The
in the main stream and tributaries (Figure 5b), and there were significant differences in
species number, cell abundance, and biomass.

Figure
Figure 5. 5. Phytoplankton
Phytoplankton communitystructure
community structure in
in different
different reaches
reaches of
of the
themiddle
middlereaches
reachesofofthe
the Yar-
Yarlung
lung Zangbo Zangbo
River.River. (a) Species
(a) Species composition,
composition, cell cell abundance,
abundance, andand percentage
percentage ofofbiomass
biomassofofphyto-
phytoplankton
plankton in different
in different river reaches.
river reaches. (b) Differences
(b) Differences in phytoplankton
in phytoplankton species
species composition, cell
composition, cell abun-
abundance,
dance, and biomass
and biomass in different
in different river
river segments(**
segments (** pp <<0.01,
0.01,Wilcoxon
Wilcoxon rank-sum test).test).
rank-sum (M) main
(M) main
stream.
stream. (T)(T) tributary.(All)
tributary. (All) the whole
wholebasin
basinofofthe river.
the river.
3.5. Co-Occurrence Network of the Phytoplankton Community
3.5. Co-Occurrence Network of the Phytoplankton Community
Phytoplankton species with an annual occurrence frequency greater than 0.1 were
Phytoplankton
screened species
to analyze the with an network
co-occurrence annual of occurrence frequency
the phytoplankton greater (Figure
community than 0.1
6). were
screened to analyze
The topological the co-occurrence
parameters network of
of the co-occurrence the phytoplankton
network were shown in community
Table 2. The(Figure
6).average
The topological parameters
degree of the main streamof (19.375)
the co-occurrence
> tributariesnetwork were
(9.512) > All shown
(5.722); the in Tableof2. The
density
the main
average stream
degree of(0.060)
the main> tributaries (0.029) >>All
stream (19.375) (0.017). The
tributaries modularity
(9.512) coefficient
> All (5.722); theofdensity
the of
network of the main stream (1.145) > tributaries (0.661) > All (0.493). The average
the main stream (0.060) > tributaries (0.029) > All (0.017). The modularity coefficient of the clustering
coefficient
network of the
of the main
main stream
stream (0.377)><tributaries
(1.145) tributary (0.5527)
(0.661)<>AllAll(0.658).
(0.493).TheTheaverage
averagepath
cluster-
length of the main stream (2.588) < tributary (3.869) < full reach (4.648).
ing coefficient of the main stream (0.377) < tributary (0.5527) < All (0.658). The average
path length of the main stream (2.588) < tributary (3.869) < full reach (4.648).
Sustainability 2023, 15, x FOR PEER REVIEW 9 of 15
Sustainability 2023, 15, 7162 8 of 14

Figure 6. 6.Species
Figure Speciesco-occurrence networkofofthe
co-occurrence network thephytoplankton
phytoplankton community
community in different
in different reaches
reaches of of
thethe
middle
middle reaches
reachesofofthe
theYarlung ZangboRiver
Yarlung Zangbo River(the
(the node
node represents
represents species
species andsize
and the therepresents
size represents
annual occurrence
annual occurrencefrequency). (M) main
frequency). (M) mainstream.
stream.(T)(T) tributary.
tributary. (All)
(All) the whole
the whole basinbasin
of theof the river.
river.

Table 2. Topological characteristics of the phytoplankton community’s co-occurrence network.

Table 2. Topological characteristics of the phytoplankton community’s co-occurrence network.
Parameter Main Stream Tributary All
Parameter Main Stream Tributary All
Number of nodes 323 324 345
Number
The number of nodes
of connections 3129 323 1541 324 987 345
The number of connections
Average degree 19.375 3129 9.512 1541 5.722 987
Average weighting
Average degree
degree 6.548 19.375 8.204 9.512 6.383 5.722
Proportion of positive correlation
Average weighting degree 69.93 6.548 97.66 8.204 99.7 6.383
(%)
Proportion of positive
Proportion correlation (%)30.07
of negative 69.93 2.34
97.66 0.30
99.7
correlation (%)
Proportion of negative correlation (%) 30.07 2.34 0.30
The density of figure 0.06 0.029 0.017
The density of figure
Coefficient of modularity 1.145 0.06 0.661 0.029 0.493 0.017
Coefficient
Average of coefficient
clustering modularity 0.377 1.145 0.527 0.661 0.658 0.493
Average path length 2.588 3.869 4.648
Average clustering coefficient 0.377 0.527 0.658
Average path length 2.588 3.869 4.648
3.6. Environmental Factors Drive Diversity and Composition of the Phytoplankton Community
As shown in Figure 7, there was no significant correlation between the α diversity
3.6. Environmental Factors Drive Diversity and Composition of the Phytoplankton Community
index and water environmental factors in the main stream. The Tributary Simpson dom-
As shown
inance in Figure
index was 7, there
negatively was no
correlated significant
with TUR, while correlation
the Pielou between
evenness the
index α and
diversity
index
the Shannon–Wiener diversity index were positively correlated with WT. From the wholedomi-
and water environmental factors in the main stream. The Tributary Simpson
nance index
reach, was negatively
the Margalef richness correlated with TUR, while
index was significantly the correlated
positively Pielou evenness
with NOindex and the
3 -N, TN,
TUR, WT, and pH, and negatively correlated with V. The Simpson dominance
Shannon–Wiener diversity index were positively correlated with WT. From the whole index and
the Shannon–Wiener
reach, diversity
the Margalef richness index
index waswere positivelypositively
significantly correlatedcorrelated
with pH. The
with Simpson
NO3-N, TN,
dominance index was positively correlated with WT.
TUR, WT, and pH, and negatively correlated with V. The Simpson dominance index and
As shown in Figure 8, from the perspective of the main flow, the cell abundance was
the Shannon–Wiener diversity index were positively correlated with pH. The Simpson
correlated with WT, TUR, and NO3 -N, and the biomass was correlated with TUR. From the
dominance
tributaries,index was
NO3 -N waspositively
negativelycorrelated withpH
correlated with WT.and V and positively correlated with
TUR. There was no significant correlation between species number, cell abundance, biomass,
and physicochemical indexes. In general, the number of species was significantly correlated
with WT and NO3 -N, and pH and TN. Cell abundance was significantly correlated with
WT and NO3 -N, and pH, TUR, V, and TN. Biomass was correlated with WT.

3.7. The Dispersal Limitation Effect on the Phytoplankton Community’s Assembly Processes
As shown in Figure 9, the occurrence frequency of the species was mostly within
the 95% confidence interval of the neutral community model. The neutral community
model successfully estimated most of the relationships between the occurrence frequency
of phytoplankton species and changes in their cell abundance. There was a high inter-
 Proportion of positive correlation (%) 69.93 97.66 99.7
Proportion of negative correlation (%) 30.07 2.34 0.30
Sustainability 2023, 15, x FOR PEER REVIEW The density of figure 0.06 0.029 0.017
10 of 15
Coefficient of modularity 1.145 0.661 0.493
Sustainability 2023, 15, 7162
Average clustering coefficient 0.377 0.527 0.658 9 of 14
Average path
Figure 7. Correlation length
analysis 2.588 community’s
between the phytoplankton 3.869
diversity index4.648
and water
environmental factors in the middle reaches of the Yarlung Zangbo River (* p < 0.05; ** p < 0.01,
pretation rate 2 ) in the main stream, tributaries, and the whole reach, indicating that
3.6.
Spearman). (M) (R
Environmental
main Factors
stream.Drive Diversity(All)
(T) tributary. andtheComposition
whole basin ofof
thethe
Phytoplankton
river. Community
the stochastic process had a strong driving effect on the phytoplankton
As shown in Figure 7, there was no significant correlation between the α diversity community’s as-
sembly in different habitats, and the interpretation rate of the main stream (0.843) > the
indexAs shown
and waterinenvironmental
Figure 8, fromfactorsthe perspective
in the main of the mainThe
stream. flow, the cell abundance
Tributary Simpson domi-was
whole reach (0.795)
correlated >TUR,
the tributaries (0.756). Nm,biomass
the product of metacommunity size (N)
nance indexwith
wasWT,
negatively and NO3-N,
correlated andTUR,
with the while thewas correlated
Pielou evenness with TUR.
index From
and the
and mobility (m), quantifies
the tributaries, NOdiversity an
3-N was negatively
estimate of dispersal between communities, determining
Shannon–Wiener index werecorrelated
positively with pH and with
correlated V andWT.positively
From thecorrelated
whole
the correlation
with TUR. Therebetween
was no occurrence
significant frequency
correlation and regional
between relative
species abundance.
number, cell The Nm
abundance,
reach, the Margalef richness index was significantly positively correlated with NO3-N, TN,
value of the phytoplankton
biomass, community ingeneral,
the main stream (Nm of = 148) >was
the significantly
whole reach
TUR, WT,and
andphysicochemical
pH, and negatively indexes. In
correlated with the number
V. The Simpson species
dominance index and
(Nm = 65)
correlated > tributaries
with WT and (Nm = 46),
NO3-N,index indicating
and pH that
andpositively the driving
TN. Cell abundance force of diffusion
was significantly restric-
corre-
the Shannon–Wiener diversity were correlated with pH. The Simpson
tion
lated on phytoplankton
with WT and NO community
-N, and pH, construction
TUR, V, and was
TN. higher
Biomass in
wasthe main stream
correlated with than
WT. in
dominance index was positively correlated with WT.
3
the tributaries.

Sustainability 2023, 15, x FOR PEER REVIEW 10 of 15

Figure 7. Correlation analysis between the phytoplankton community’s diversity index and water
environmental factors in the middle reaches of the Yarlung Zangbo River (* p < 0.05; ** p < 0.01,
Spearman). (M) main stream. (T) tributary. (All) the whole basin of the river.

As shown in Figure 8, from the perspective of the main flow, the cell abundance was
correlated with WT, TUR, and NO3-N, and the biomass was correlated with TUR. From
the tributaries, NO3-N was negatively correlated with pH and V and positively correlated
with
FigureTUR. Theretest
8. Mantel was no significant
analysis between correlation between
the phytoplankton species number,
community’s cell abundance,
characteristics and water
biomass, and physicochemical
environmental indexes.
factors in the middle reachesInofgeneral, the number
the Yarlung of species
Zangbo River was significantly
(* p < 0.05; ** p < 0.01; ***
Figure 7. Correlation analysis between the phytoplankton community’s diversity index and water
p < 0.001, Spearman).
correlated with WT (M)
andmain
NO3stream.
-N, and(T)
pHtributary.
and TN. (All)
Cellthe whole basinwas
abundance of the river.
significantly corre-
environmental factors in the middle reaches of the Yarlung Zangbo River (* p < 0.05; ** p < 0.01,
lated with WT and NO3-N, and pH, TUR, V, and TN. Biomass was correlated with WT.
Spearman). (M) main stream. (T) tributary. (All) the whole basin of the river.
3.7. The Dispersal Limitation Effect on the Phytoplankton Community’s Assembly Processes
As shown in Figure 9, the occurrence frequency of the species was mostly within the
95% confidence interval of the neutral community model. The neutral community model
successfully estimated most of the relationships between the occurrence frequency of phy-
toplankton species and changes in their cell abundance. There was a high interpretation
rate (R2) in the main stream, tributaries, and the whole reach, indicating that the stochastic
process had a strong driving effect on the phytoplankton community’s assembly in differ-
ent habitats, and the interpretation rate of the main stream (0.843) > the whole reach (0.795)
> the tributaries (0.756). Nm, the product of metacommunity size (N) and mobility (m),
quantifies an estimate of dispersal between communities, determining the correlation be-
tween occurrence frequency and regional relative abundance. The Nm value of the phy-
toplankton
Figure community in the main stream (Nm = 148) > the wholecharacteristics
8. Mantel reach (Nm = 65) >water trib-
Mantel test analysis between the phytoplankton community’s
community’s characteristics and and water
utaries (Nm =factors
environmental 46), indicating that the driving force of diffusion restriction on **
phytoplank-
environmental factorsin inthe
themiddle
middlereaches
reachesofofthe
theYarlung
YarlungZangbo
ZangboRiver (* (*
River p <p0.05;
< 0.05; p**< p0.01; ***
< 0.01;
pton community
< 0.001, construction
Spearman). was higher
(M) main stream. in the main
(T) tributary. stream
(All) the than
whole inofthe
basin thetributaries.
river.
*** p < 0.001, Spearman). (M) main stream. (T) tributary. (All) the whole basin of the river.

3.7. The Dispersal Limitation Effect on the Phytoplankton Community’s Assembly Processes
As shown in Figure 9, the occurrence frequency of the species was mostly within the
95% confidence interval of the neutral community model. The neutral community model
successfully estimated most of the relationships between the occurrence frequency of phy-
toplankton species and changes in their cell abundance. There was a high interpretation
rate (R2) in the main stream, tributaries, and the whole reach, indicating that the stochastic
process had a strong driving effect on the phytoplankton community’s assembly in differ-
ent habitats, and the interpretation rate of the main stream (0.843) > the whole reach (0.795)
> the tributaries (0.756). Nm, the product of metacommunity size (N) and mobility (m),
quantifies an estimate of dispersal between communities, determining the correlation be-
tween occurrence frequency and regional relative abundance. The Nm value of the phy-
Figure 9. Neutral
Neutral phytoplankton
phytoplankton community model in different reaches of the middle reaches of the
toplankton
Yarlung Zangbo
community
Zangbo River.
inmain
River. (M)
the main
(M) main
stream
stream. (T)
(Nm = (All)
(T) tributary.
148)the
tributary. (All)
> the whole reach
whole basin
basin of
(Nm
of the
= 65) > trib-
the river.
river.
Yarlung stream. the whole
utaries (Nm = 46), indicating that the driving force of diffusion restriction on phytoplank-
ton community construction was higher in the main stream than in the tributaries.
Sustainability 2023, 15, 7162 10 of 14

4. Discussion
4.1. Phytoplankton Community Diversity and Its Driving Factors
In the middle reaches of the Yarlung Zangbo River, the Simpson dominance index,
the Shannon–Wiener diversity index, and the Margalef richness index of the main stream
were higher than those of the tributaries. The Shannon–Wiener diversity index and the
Margalef richness index were statistically significantly different for the main stream and the
tributaries, indicating that the phytoplankton community’s structure in the main stream
was more complex and stable than that in the tributaries [32,33], which was consistent with
the research results of Yangling Qiu et al. [34]. This may be due to the low flow rate of the
main stream, which can provide a relatively stable living space for phytoplankton, and
the species can fully optimize the resources. Compared with the main stream, the tribu-
taries provide fewer resources and space for phytoplankton due to their high flow velocity
and low runoff. The population size is affected by the intensification of interspecific and
intraspecific competition, which causes the main stream to be relatively rich in species com-
position. The Spearman correlation coefficient results showed that the Margalef richness
index was significantly positively correlated with NO3 -N, TN, and WT, and significantly
negatively correlated with V, indicating that the Margalef richness index was affected by
multiple water environmental factors. When combined with the Mantel correlation analysis
(Figure 8), these water environmental factors were significantly correlated with species
number and cell abundance, which may be because nutrients such as NO3 -N and TN can
provide nitrogen for the metabolism of phytoplankton, and the increase in concentrations
of NO3 -N and TN in water can provide sufficient nutrients for phytoplankton. A higher WT
enhances the absorption rate of nutrients by phytoplankton and promotes the propagation
of the phytoplankton population. The Shannon–Wiener diversity index was significantly
positively correlated with pH. Diatoms have strong adaptability in alkaline water environ-
ments, and the diatom species are the most abundant in this basin. The increase in pH in
water may lead to the mass multiplication of diatoms, resulting in an increase in community
diversity. The Simpson dominance index was extremely significantly positively correlated
with WT. When combined with the Mantel correlation analysis, the water temperature
was significantly correlated with species number and cell abundance, indicating that water
temperature was the main water environmental factor indirectly affecting the dominant
taxa in water.

4.2. The Characteristics and Driving Factors of the Phytoplankton Community’s Structure
The species composition, cell abundance, and biomass of the phytoplankton com-
munity in the middle reaches of the Yarlung Zangbo River were statistically analyzed.
The diatom phyla were dominant. The Yarlung Zangbo River is a plateau river with an
average altitude above 3000 m. The altitude gradient is negatively correlated with the
water temperature of the river. The water temperature of the Yarlung Zangbo River is
lower than that of the altitude region. WT was an important driving force of phytoplankton
metabolism, including photosynthesis, nutrient absorption, cell division, and prolifera-
tion [35,36]. The average water temperature in the study area was low (13.08 ◦ C). The
results of the Mantel correlation analysis showed that the number of phytoplankton species,
cell abundance, and biomass were significantly correlated with WT. Diatoms have strong
adaptability to the environment of low water temperatures and alkaline environments,
have a wide ecological range, and are more restricted to water environmental factors than
other algae [37,38]. The previous study of the Lhasa River suggested that Bacillariophyta
are closely related to the cell density and pH of the dominant species. As well as the Lhasa
River [39], diatoms exhibit a greater percentage of cell abundance and biomass in the main
stream of the Yarlung Zangbo River middle reaches. At the same time, the mean pH of the
main stream (8.31) was significantly higher than that of the tributaries (7.61). The Mantel
correlation analysis showed that the number of phytoplankton species and the average cell
abundance were significantly correlated with pH, indicating that pH was also an important
Sustainability 2023, 15, 7162 11 of 14

driving factor affecting the distribution of diatoms in the middle reaches of the Yarlung
Zangbo River.
The average abundance of phytoplankton cells in the main stream was significantly
higher than that in the tributaries. Studies have found that the flow velocity and size of the
river discharge will affect the phytoplankton community’s structure [40]. The flow velocity
of the main stream of the middle reaches of the Yarlung Zangbo River is lower than that of
the tributaries, and the difference is significant. The main stream can provide a relatively
stable living space for phytoplankton. Compared with the main stream, the tributaries
provide fewer resources and space for phytoplankton due to their high flow velocity and
low runoff. Therefore, the interspecific and intraspecific competition is intensified, and
the cell abundance of species is affected accordingly. The phytoplankton community’s
composition and species distribution are greatly affected by pH, which can directly affect
the physiological and biochemical activities of phytoplankton itself, and can also act on
algae together with other physical and chemical factors in water [41,42]. In this study, the
mean pH of the main stream is greater than that of the tributaries. Cell abundance was
significantly correlated with pH, indicating that pH was one of the influencing factors for
the difference in phytoplankton cell abundance in the middle reaches of the Yarlung Zangbo
River. Altitude can indirectly affect the river ecosystem by influencing environmental
factors such as temperature, illumination, and precipitation in a region [43]. In the study
area, the average altitude of the tributary (3650 m) is higher than that of the main stream
(3133 m), and the river has a longer freezing period, so the water temperature is also lower
than that of the main stream. In this study, the average phytoplankton biomass was higher
than tributaries. The Mantel correlation analysis showed that phytoplankton biomass was
significantly correlated with WT. These results indicated that altitude indirectly affected
phytoplankton biomass in the middle reaches of the Yarlung Zangbo River by influencing
water temperature, velocity, and nutrients. In general, the phytoplankton structure in the
middle reaches of the Yarlung Zangbo River is affected by water temperature, velocity, pH,
and other factors. The differences in geographical factors and water environment directly
or indirectly drive the survival and reproduction of the phytoplankton community, forming
the unique community structure characteristics of the main and tributaries of the middle
reaches of the Yarlung Zangbo River.

4.3. Co-Occurrence Patterns and Driving Factors in Phytoplankton Communities

There are interactions among various organisms in the community, such as symbio-
sis, cooperation, competition, and predation, which determine the mode of biological
coexistence [44]. The Microbial symbiosis model is an important tool to evaluate the
function of microbial communities. It can reveal the potential interactions between micro-
organisms [45] and is widely used to study the coexistence between micro-organisms
in natural environments [46]. The results of community co-occurrence network analysis
showed that the degree of association among phytoplankton in tributaries was greater than
that in the main stream and much greater than that in the whole watershed, indicating that
the community’s complexity of phytoplankton in tributaries was lower, and the interaction
between phytoplankton was simpler or the niche overlap was lower. In this study, the
tributaries had low nitrogen, phosphorus, and organic matter contents, resulting in a low
nutrient concentration environment, which may be the main factor causing the simple
phytoplankton community in the tributaries, while the main stream was relatively rich
in nutrients, which may lead to more complex interactions, high niche overlap, and tight
network structure. The network with higher connectivity responds more quickly to envi-
ronmental disturbances [47–49]. The connectivity of the phytoplankton community in the
main stream is higher than that of tributaries (Figure 6), indicating that the phytoplankton
community in the main stream is more stable, and responds more quickly to environmen-
tal disturbances. In the co-occurrence network, the positive and negative correlations of
edges between two nodes represent the reciprocal and competitive relationship between
connected species, respectively. The positive correlations between network nodes (Figure 6)
Sustainability 2023, 15, 7162 12 of 14

suggest a synergistic relationship between species, and organisms from the same group
often have antagonistic effects due to the competition for resources [50,51]. The positive
correlation ratio of tributaries was higher than that in the main stream, suggesting a higher
synergistic effect of the phytoplankton community in the tributaries, which dominated the
phytoplankton community. It may be due to the high altitude, high velocity, and low water
temperature of the tributaries, and the synergistic effect among species was stronger than
the competition effect in the more extreme habitats.
According to the analysis of the neutral community model, there was a high R2 matter
in the main stream, tributaries, or the whole river reach. R2 represents the reproducibility
of fit in the neutral community model. The value of R2 in the neutral model indicated
the stochastic (more) or deterministic (less) process affected community construction [52].
The results (Figure 9) showed that the stochastic processes played important roles in the
formation of phytoplankton community assembly in the main stream of the middle reaches
of the Yarlung Zangbo River, especially in the main stream. Nm is used for estimating
the dispersal between communities and determining the correlation between occurrence
frequency and regional relative abundance [53]. The Nm value was highest in the main
stream, followed by that in the whole reach, and lowest in tributaries, indicating that the
construction of the phytoplankton community in the main stream was mainly driven by dif-
fusion restriction. There were more co-occurrence relationships among species in the main
stream phytoplankton community, indicating that the balance between species selection
and dispersal mediated the coexistence of species in the phytoplankton community.

5. Conclusions
This study investigated the biogeographic dynamics of the phytoplankton community
in the middle reaches of the Yarlung Zangbo River. The results show that the Shannon–
Wiener diversity index and the Margalef richness index of the main stream were higher than
those of the tributaries. The community structure of the main stream was more complex and
stable than that of the tributaries. Total nitrogen, turbidity, water temperature, and pH were
the main environmental factors affecting the diversity of the phytoplankton community.
The average cell abundance and biomass of phytoplankton in the main stream were higher
than those in the tributaries. Water temperature, pH, turbidity, and velocity were the main
influencing factors for the difference in phytoplankton community structure between the
main stream and tributaries. The phytoplankton community in the main stream had a close
structure, high connectivity, more rapid response to environmental disturbance, and higher
stability. The interspecific synergism of the phytoplankton community in the tributaries
was higher than that in the main stream. The random process played a greater role in
the phytoplankton community’s construction in the main stream than in the tributaries,
and the phytoplankton community’s construction process in the main stream was mainly
driven by diffusion restriction.

Supplementary Materials: The following supporting information can be downloaded at: https://
www.mdpi.com/article/10.3390/su15097162/s1, Figure S1: Habitat information from 28 sampling
sites in the middle reaches of Yarlung Zangbo River; Table S1: Habitat information of sampling sites
in the middle reaches of the Yarlung Zangbo River; Table S2: Characteristics of water environmental
factors in the middle reaches of Yarlung Zangbo River; Table S3: List of phytoplankton in the middle
Yarlung Zangbo River.
Author Contributions: Conceptualization, Q.Y. and S.Y.; methodology, S.B.; software, S.B.; validation,
P.Z., Q.Y. and H.L.; formal analysis, X.C.; investigation, X.L.; resources, S.B.; data curation, X.L.;
writing—original draft preparation, X.L.; writing—review and editing, S.B.; visualization, H.L.;
supervision, X.L.; project administration, S.B.; funding acquisition, S.B. All authors have read and
agreed to the published version of the manuscript.
Funding: This work was supported by the National Natural Science Foundation of China (32070418)
and the 2021 Special Funds for the Basic Research and Development Program in the Central Nonprofit
Research Institutes of China (Tibetan Finance, Science and Education Guidance [2021] No. 1).
Sustainability 2023, 15, 7162 13 of 14

Institutional Review Board Statement: Not applicable.

Informed Consent Statement: Not applicable.
Data Availability Statement: Not applicable.
Conflicts of Interest: The authors declare no conflict of interest.

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