Bryophyte Flora in Alpine Grasslands of the Qinghai–Tibet Plateau Based on Plot Sampling

Abstract

The species number of bryophytes is the second highest among land plants. Alpine grasslands on the Qinghai–Tibet Plateau (QTP) are the largest among global alpine biomes. However, bryophyte flora in alpine grasslands on the QTP remains poorly explored relative to its large geographic extent. A total of 347 plots were surveyed across the QTP, and 149 bryophyte taxa in 24 families and 49 genera were recorded in alpine grasslands. The largest family was Pottiaceae, followed by Bryaceae and Brachytheciaceae. The most species-rich genus was Bryum, followed by Didymodon and Brachythecium. The dominant species were Didymodon tectorus, Didymodon fallax, Bryum caespiticium, Didymodon constrictus, and Didymodon ditrichoides. The Jaccard similarity indexes of bryophyte compositions between alpine meadow and alpine steppe at the family, genus, and species levels were 0.375, 0.367, and 0.282, respectively. Turf was the most common life-form (75.2%), followed by weft (16.1%) and cushion (5.4%). Endemic species to China accounted for 8.05% of the total taxa. Bryophyte diversity in alpine grasslands on the QTP is exceptional and irreplaceable. The changes in species composition and life-forms between different grassland types reflect the adaptations of bryophytes to harsh environments.

1. Introduction

Bryophytes, including mosses, liverworts, and hornworts, are the earliest lineages among land plants and are widely distributed from the equator to polar regions. Due to the lack of vascular tissues, they usually have a small size and are thus ignored in biodiversity surveys. In fact, the species number of bryophytes is the second highest among land plants [1]. The unique morphological structure and physiological characteristics of bryophytes enable them to survive in extremely arid and cold environments [2,3,4]. In alpine ecosystems, bryophytes play important roles in soil water retention [5,6], sand fixation [7], and frozen soil protection [8].

The Qinghai–Tibet Plateau (QTP), with a total area of approximately 2.5 million km² and an average elevation of ca. 4000 m, is the largest and highest plateau in the world. Thus, it is well known as the roof of the world. Diverse biomes, such as forests, grasslands, deserts, and tundra, are distributed across the QTP. Of these, alpine grasslands, covering 60% of the total plateau, are the largest [9,10], even among global alpine biomes [11]. Alpine grasslands of the QTP are mainly distributed in the Xizang Autonomous Region (Tibet) and Qinghai Province of China, and they have vast ecological and socioeconomic value, such as nutrient cycling regulation, fresh water provisioning, biodiversity, and pastoral production [11]. In particular, the two primary grassland types on the QTP, i.e., alpine meadow (AM) and alpine steppe (AS) [11], have been identified as two ecoregions of global biodiversity conservation priority [12].

For a long time, poor traffic conditions, severe climate, and complex topography, as well as the paucity of bryologists, have hampered the investigation of bryophyte flora in alpine grasslands on the QTP. In recent years, an increasing amount of research has focused on the Tibet Plateau (TP). Song et al. [13] conducted a bryological survey across the TP and reported 22 Didymodon spp. (Pottiaceae), including a new record to China in the alpine grasslands of Tibet. Several new species from genera, including Bryoerythrophyllum [14], Didymodon [15,16,17], and Encalypta [18], are continuing to be described from TP grasslands. However, the bryophyte survey of the Qinghai Plateau has received little attention [19]. Therefore, bryophyte flora in alpine grasslands on the QTP remains poorly explored relative to its large geographic extent.

Biodiversity is multidimensional, including species richness, abundance, and evenness [20]. Plot sampling (PS) is one of the methods used to explore biodiversity and is especially common in community ecology and vegetation science. It is not only used to answer which and where species exist but also to quantify which species are dominant in plant communities of a certain area by a robust statistical analysis. Cheng et al. [21] carried out intensive fieldwork based on PS covering 11 vegetation types on the QTP to reveal the species richness of vascular plants. Unfortunately, to our knowledge, no studies thus far have attempted to estimate bryophyte biodiversity in the alpine ecosystem on a broad scale. The present study surveyed bryophytes in alpine grasslands across the QTP based on PS. The objectives were to elucidate species composition, life-forms, and endemism and to compare diversity between different grassland types. The results will improve our knowledge of bryophyte flora in alpine grasslands on the QTP and provide new insights into conservation strategies for bryophytes in alpine grasslands.

2. Materials and Methods

2.1. Study Area

The study area lies between 28°12′ and 38°47′ N and 79°27′ and 102°16′ E in Tibet and Qinghai Province of China on the QTP, with elevations ranging from 2185 to 5505 m (Figure 1). The QTP has an arid and semi-arid alpine climate. The uneven precipitation on the plateau forms the vegetation patterns of AM, AS, and alpine desert steppe (ADS) from east to west [22]. AM is characterized by a cold and wet climate, and the annual precipitation can reach up to 600 mm, and it is consequently dominated by Kobresia spp. [23,24,25]. Most AS is characterized by a cold and arid climate, and the annual precipitation varies from 600 mm in the east to below 60 mm in the west; therefore, it is dominated by Stipa spp. [23,25,26]. ADS is distributed in the west plateau and dominated by Ceratoides compacta, where it receives little precipitation (<50 mm yr⁻¹) and environmental conditions are extremely harsh with little or low vegetation coverage [23,25,26].

2.2. Plot Sampling

The PS of bryophyte flora in the alpine grasslands of the QTP was carried out from mid-July to late August 2019 and 2020. According to the Vegetation Map of China [22], plots were randomly selected at a scale of 0.5° × 0.5° grid cells. Based on the traffic accessibility, a total of 347 plots were selected, including 162 AS, 144 AM, and 41 ADS (Figure 1). A 20 m × 20 m plot was established, and its coordinates and elevation were recorded by a handheld GPS (Garmin, Beijing, China). A transparent plastic plate (20 cm × 20 cm) divided into 100 grids was used as the sampling quadrat. In each plot, 3–5 quadrats were randomly set. We collected all bryophytes and recorded the species cover in each quadrat. A total of 1454 quadrats were sampled. Since no bryophytes occurred in some harsh plots, 951 specimens were finally collected. They were taken back to the laboratory to identify the species level under a microscope and were stored in the Biological Herbarium of Chongqing Normal University (CTC). The nomenclature followed “Species 2000” (https://www.sp2000.org.cn/ (accessed on 1 May 2023).

2.3. Data Analysis

We used the importance value (IV), which was calculated as the average of the relative cover and relative frequency of a certain species in each plot, to identify the dominant species. Bryophyte life-forms followed those described by Bates [27] and Glime [28]. Since we unfortunately encountered any bryophytes in the sampling plots belonging to the ADS, we used the Jaccard similarity index (J) [29] to compare the floristic composition between AM and AS. It was calculated using the following formula: J = c/(a + b − c), where a and b are the total number of families, genera, or species in AM and AS, respectively, and c is the number of families, genera, or species common to both grassland types.

3. Results

3.1. Species Composition and Dominant Species in Alpine Grasslands

Among the 347 investigated sampling plots, bryophytes were found in 199 of them, whereas none were found in the other plots, including 11 AM, 96 AS, and 41 ADS. In total, 149 bryophyte taxa in 24 families and 49 genera were recorded in the alpine grasslands of the QTP based on PS (

Table 1. Bryophyte species, life-forms, cumulative importance value, and occurrence in grassland types in alpine grasslands of the Qinghai–Tibet Plateau. AM = alpine meadow; AS = alpine steppe.

No.	Family	Species	Life-Forms	Cumulative Importance Value	Grassland Types
1	Pottiaceae	Didymodon tectorus	Turf	25.255	AM, AS
2	Pottiaceae	Didymodon fallax	Turf	13.323	AM, AS
3	Bryaceae	Bryum caespiticium	Turf	11.866	AM, AS
4	Pottiaceae	Didymodon constrictus	Turf	10.044	AM, AS
5	Pottiaceae	Didymodon ditrichoides	Turf	10.019	AM, AS
6	Bryaceae	Bryum argenteum	Turf	6.873	AM, AS
7	Pottiaceae	Barbula gracilenta	Turf	6.110	AM, AS
8	Pottiaceae	Didymodon constrictus var. flexicuspis	Turf	5.567	AM, AS
9	Ditrichaceae	Distichium brevisetum	Turf	4.806	AM
10	Pottiaceae	Didymodon michiganensis	Turf	4.336	AM, AS
11	Bryaceae	Bryum lonchocaulon	Turf	4.029	AM, AS
12	Distichiaceae	Distichium capillaceum	Turf	3.031	AM, AS
13	Pottiaceae	Didymodon asperifolius	Turf	2.972	AM, AS
14	Pottiaceae	Vinealobryum vineale	Turf	2.958	AM, AS
15	Pottiaceae	Didymodon rivicola	Turf	2.813	AM, AS
16	Rhytidiaceae	Rhytidium rugosum	Weft	2.799	AM
17	Thuidiaceae	Abietinella abietina	Weft	2.761	AM
18	Thuidiaceae	Haplocladium angustifolium	Weft	2.735	AM
19	Bryaceae	Bryum algovicum	Turf	2.613	AM, AS
20	Entodontaceae	Entodon challengeri	Mat	2.260	AM
21	Pottiaceae	Didymodon tophaceus	Turf	2.256	AM, AS
22	Pottiaceae	Aloina rigida	Turf	2.242	AM, AS
23	Brachytheciaceae	Brachythecium moriense	Weft	2.217	AM
24	Brachytheciaceae	Brachythecium populeum	Weft	2.063	AM, AS
25	Pottiaceae	Didymodon nigrescens	Turf	2.003	AM, AS
26	Pottiaceae	Gymnostomum calcareum	Turf	1.961	AM, AS
27	Brachytheciaceae	Brachythecium pulchellum	Weft	1.873	AM, AS
28	Pottiaceae	Weissia longifolia	Turf	1.823	AM
29	Bryaceae	Bryum alpinum	Turf	1.732	AM, AS
30	Pottiaceae	Didymodon vinealis var. vinealis	Turf	1.731	AM, AS
31	Hypnaceae	Hypnum revolutum	Weft	1.676	AM
32	Brachytheciaceae	Brachythecium coreanum	Weft	1.498	AM
33	Pottiaceae	Barbula yunnanensis	Turf	1.476	AM, AS
34	Bryaceae	Bryum uliginosum	Turf	1.396	AM, AS
35	Pottiaceae	Barbula unguiculata	Turf	1.340	AM
36	Funariaceae	Funaria hygrometrica	Turf	1.327	AM, AS
37	Entodontaceae	Entodon concinnus	Mat	1.293	AM
38	Pottiaceae	Barbula indica	Turf	1.189	AM, AS
39	Pottiaceae	Tortella tortuosa	Turf	1.072	AM
40	Bryaceae	Bryum pallescens	Turf	1.017	AM, AS
41	Mniaceae	Pohlia elongata	Turf	1.017	AM
42	Pottiaceae	Bryoerythrophyllum gymnostomum	Turf	1.016	AM
43	Bryaceae	Bryum paradoxum	Turf	0.968	AM
44	Pottiaceae	Weissia controversa	Turf	0.904	AM
45	Pottiaceae	Trichostomum crispulum	Turf	0.851	AM, AS
46	Thuidiaceae	Thuidium delicatulum	Weft	0.794	AM
47	Pottiaceae	Gymnostomum laxirete	Turf	0.786	AM, AS
48	Bryaceae	Anomobryum auratum	Turf	0.775	AM, AS
49	Bryaceae	Bryum cellulare	Turf	0.768	AM, AS
50	Pottiaceae	Syntrichia sinensis	Turf	0.764	AM
51	Polytrichaceae	Pogonatum perichaetiale	Turf	0.734	AS
52	Bryaceae	Bryum sauteri	Turf	0.711	AM
53	Bryaceae	Bryum pseudotriquetrum	Turf	0.688	AM
54	Bryaceae	Bryum arcticum	Turf	0.671	AM, AS
55	Pottiaceae	Tortella fragilis	Turf	0.662	AM
56	Pottiaceae	Bryoerythrophyllum brachystegium	Turf	0.646	AM
57	Pottiaceae	Gymnostomum calcareum	Turf	0.639	AM, AS
58	Bryaceae	Bryum dichotomum	Turf	0.623	AM
59	Leucobryaceae	Campylopus umbellatus	Turf	0.605	AM
60	Ditrichaceae	Distichium inclinatum	Turf	0.589	AM
61	Pottiaceae	Hymenostylium recurvirostrum	Turf	0.585	AM
62	Hypnaceae	Hypnum cupressiforme	Weft	0.583	AM
63	Entodontaceae	Entodon cladorrhizans	Mat	0.573	AM
64	Bartramiaceae	Philonotis thwaitesii	Turf	0.547	AM
65	Hypnaceae	Hypnum plumaeforme	Weft	0.538	AM
66	Encalyptaceae	Encalypta rhaptocarpa	Turf	0.533	AM
67	Encalyptaceae	Encalypta spathulata	Turf	0.521	AM
68	Pottiaceae	Syntrichia ruralis	Turf	0.508	AM
69	Pottiaceae	Barbula pseudo-ehrenbergii	Turf	0.497	AM
70	Bartramiaceae	Philonotis turneriana	Turf	0.474	AM, AS
71	Pottiaceae	Hymenostylium recurvirostrum var. insigne	Turf	0.459	AM
72	Distichiaceae	Distichium bryoxiphioidium	Turf	0.450	AM
73	Funariaceae	Funaria discelioides	Turf	0.443	AM, AS
74	Pottiaceae	Weissia longifolia	Turf	0.442	AM, AS
75	Brachytheciaceae	Brachythecium garovaglioides	Weft	0.434	AM
76	Pottiaceae	Didymodon ferrugineus	Turf	0.429	AS
77	Pylaisiadelphaceae	Isopterygium albescens	Weft	0.415	AM
78	Pottiaceae	Trichostomum tenuirostre	Turf	0.404	AM
79	Brachytheciaceae	Brachythecium plumosum	Weft	0.399	AM
80	Dicranaceae	Dicranum fragilifolium	Turf	0.398	AM
81	Bryaceae	Bryum capillare	Turf	0.397	AM
82	Mniaceae	Rhizomnium gracile	Turf	0.395	AS
83	Bryaceae	Bryum blindii	Turf	0.386	AS
84	Brachytheciaceae	Brachythecium reflexum	Weft	0.378	AM
85	Dicranellaceae	Dicranella divaricatula	Turf	0.375	AM
86	Brachytheciaceae	Brachythecium buchananii	Weft	0.368	AM
87	Fissidentaceae	Fissidens curvatus	Turf	0.362	AM, AS
88	Pottiaceae	Syntrichia princeps	Turf	0.355	AM, AS
89	Grimmiaceae	Grimmia montana	Cushion	0.353	AM, AS
90	Thuidiaceae	Haplocladium microphyllum	Weft	0.339	AM
91	Bryaceae	Bryum turbinatum	Turf	0.318	AM, AS
92	Oncophoraceae	Oncophorus virens	Turf	0.311	AM
93	Dicranaceae	Dicranum scoparium	Turf	0.307	AM
94	Pottiaceae	Bryoerythrophyllum recurvirostrum	Turf	0.301	AM, AS
95	Funariaceae	Physcomitrium coorgense	Turf	0.300	AM
96	Brachytheciaceae	Cirriphyllum cirrosum	Weft	0.299	AM
97	Thuidiaceae	Thuidium pristocalyx	Weft	0.292	AM
98	Bartramiaceae	Philonotis calomicra	Turf	0.286	AM
99	Encalyptaceae	Encalypta ciliata	Turf	0.274	AM
100	Dicranaceae	Paraleucobryum schwarzii	Turf	0.257	AM
101	Mniaceae	Pohlia timmioides	Turf	0.254	AM
102	Pottiaceae	Timmiella anomala	Turf	0.253	AM
103	Bryaceae	Bryum radiculosum	Turf	0.252	AM
104	Pottiaceae	Bryoerythrophyllum yunnanense	Turf	0.250	AM
105	Pottiaceae	Tortula leucostoma	Turf	0.241	AM
106	Pottiaceae	Barbula subcomosa	Turf	0.217	AM
107	Pottiaceae	Didymodon perobtusus	Turf	0.216	AM
108	Orthotrichaceae	Orthotrichum anomalum	Cushion	0.201	AM
109	Pottiaceae	Didymodon rufidulus	Turf	0.201	AS
110	Grimmiaceae	Grimmia pilifera	Cushion	0.194	AM
111	Mniaceae	Plagiomnium arbusculum	Turf	0.189	AM
112	Fissidentaceae	Fissidens exilis	Turf	0.188	AM
113	Pottiaceae	Trichostomum brachydontium	Turf	0.188	AM
114	Brachytheciaceae	Brachythecium kuroishicum	Weft	0.183	AS
115	Mniaceae	Pohlia minor	Turf	0.174	AM
116	Bryaceae	Bryum pallens	Turf	0.173	AM
117	Entodontaceae	Entodon obtusatus	Mat	0.171	AM
118	Splachnaceae	Tayloria lingulata	Turf	0.154	AM
119	Grimmiaceae	Grimmia elatior	Cushion	0.146	AM
120	Mniaceae	Plagiomnium drummondii	Turf	0.146	AM
121	Mniaceae	Pohlia nutans	Turf	0.145	AM
122	Brachytheciaceae	Brachythecium salebrosum	Weft	0.141	AM
123	Pottiaceae	Bryoerythrophyllum inaequalifolium	Turf	0.131	AS
124	Bryaceae	Bryum blandum subsp. handelii	Turf	0.131	AM
125	Funariaceae	Physcomitrium sphaericum	Turf	0.126	AM
126	Bryaceae	Bryum purpurascens	Turf	0.115	AM
127	Pottiaceae	Bellibarbula recurva	Turf	0.113	AM
128	Brachytheciaceae	Brachythecium piligerum	Weft	0.108	AM
129	Pottiaceae	Tortula planifolia	Turf	0.101	AM
130	Bryaceae	Brachymenium sinense	Turf	0.100	AS
131	Pottiaceae	Tortula muralis	Turf	0.098	AM
132	Bryaceae	Bryum thomsonii	Turf	0.096	AM
133	Mniaceae	Pohlia crudoides	Turf	0.095	AM
134	Hypnaceae	Ptilium crista-castrensis	Weft	0.095	AM
135	Hylocomiaceae	Rhytidiadelphus squarrosus	Weft	0.095	AM
136	Funariaceae	Physcomitrium eurystomum	Turf	0.093	AM
137	Polytrichaceae	Polytrichastrum papillatum	Turf	0.092	AS
138	Grimmiaceae	Grimmia anodon	Cushion	0.092	AS
139	Grimmiaceae	Grimmia elongata	Cushion	0.089	AS
140	Splachnaceae	Tayloria subglabra	Turf	0.087	AM
141	Bryaceae	Brachymenium nepalense	Turf	0.085	AM
142	Bryaceae	Bryum salakense	Turf	0.073	AM
143	Pottiaceae	Syntrichia caninervis	Turf	0.064	AM
144	Leucobryaceae	Campylopus flexuosus	Turf	0.060	AM
145	Grimmiaceae	Schistidium subconfertum	Cushion	0.059	AM
146	Pottiaceae	Tortula yuennanensis	Turf	0.059	AM
147	Plagiotheciaceae	Plagiothecium piliferum	Mat	0.053	AM
148	Grimmiaceae	Grimmia pulvinata	Cushion	0.051	AM
149	Bryaceae	Bryum rutilans	Turf	0.040	AS

). All of them were mosses. The largest family (i.e., species number > 10) was Pottiaceae (14 genera, 50 taxa), followed by Bryaceae (3, 26) and Brachytheciaceae (2, 12), accounting for 59.1% of the total number of taxa (Figure 2a). The most species-rich genus was Bryum (23 taxa), followed by Didymodon (14) and Brachythecium (11, Figure 2b). Details on the bryophyte families and genera are presented in Figure 2.

The top 10 dominant species in alpine grasslands were Didymodon tectorus, Didymodon fallax, Bryum caespiticium, Didymodon constrictus, Didymodon ditrichoides, Bryum argenteum, Barbula gracilenta, Didymodon constrictus var. flexicuspis, Distichium brevisetum, and Didymodon michiganensis. The rank of all bryophyte species based on IV is presented in Table 1.

3.2. Comparing Species Composition between AM and AS

A total of 137 bryophyte taxa in 23 families and 46 genera were recorded in AM, while 54 taxa in 10 families and 21 genera were recorded in AS. Pottiaceae and Bryaceae were the most species-rich families in both AM and AS, cumulatively accounting for 51.1% and 74.0%, respectively (Figure 3a,c). Bryum and Didymodon were the most species-rich genera in both AM and AS. In particular, the proportions of Didymodon increased from 8.8% in AM to 24.1% in AS (Figure 3b,d).

The Jaccard similarity indexes of bryophyte compositions between AM and AS at the family, genus, and species levels were 0.375, 0.367, and 0.282, respectively. AM and AS shared 42 taxa. A total of 95 taxa, including Rhytidium rugosum, Abietinella abietina, Haplocladium angustifolium, Entodon challengeri, Brachythecium moriense, Brachythecium populeum, and Hypnum revolutum, were only found in AM, while 12 taxa, including Didymodon ferrugineus, Rhizomnium gracile, Bryum blindii, and Bryoerythrophyllum inaequalifolium, only occurred in AS.

3.3. Bryophyte Life-Forms

Four types of bryophyte life-forms were observed in the alpine grasslands of the QTP (Figure 4). Turf was the most common (112 taxa, 75.2%), followed by weft (24, 16.1%) and cushion (8, 5.4%). The rank of life-forms was similar between AM and AS. Compared to AM, turfs increased by 13.7% in AS, while wefts sharply decreased (16.8% vs. 5.6%) and mats disappeared. Cushions (3, 5.6%) increased to as many as the wefts in AS.

3.4. Endemism

Twelve species, namely Barbula yunnanensis, Dicranella divaricatula, Distichium brevisetum, Didymodon constrictus var. flexicuspis, Didymodon rivicola, Didymodon rufidulus, Distichium bryoxiphioidium, Funaria discelioides, Gymnostomum laxirete, Pohlia timmioides, Tortula planifolia, and Tortula yuennanensis, were endemic to China, accounting for 8.05% of the total taxa. Of which, five species occurred in both AM and AS; six and one species were only in AM and AS, respectively (Table 1).

4. Discussion

4.1. Sampling Methods for Estimating Biodiversity

Different sampling methods influence the detection of biodiversity [30,31,32]. Chen et al. [33] obtained the higher species richness of epiphytic bryophytes by using the PS method than by using the floristic habitat sampling (FHS) method. In contrast, Newmaster et al. [32] found that the FHS method was more efficient than the PS method in estimating bryophyte species in forest stands. Additionally, the diversity of forest floor bryophytes explored by microcoenose sampling was higher than that explored by random sampling [34]. Song et al. [13] collected some Didymodon species from the arid regions of southwestern Tibet, where no bryophytes occurred in our sampling plots. Moreover, we have not sampled any liverworts. This incomplete species pool is possibly due to the random sampling of the plots and quadrats, the unoptimized species–area relationship [35], and the uncovering of entire microhabitats [32]. Although PS may underestimate species diversity, we believe that the intensive sampling effort on a broad scale contributed the baseline information of bryophyte diversity to the QTP flora, even global alpine flora. More investigations incorporating the floristic sampling method are still needed to elucidate the overall bryophyte diversity in alpine grasslands on the QTP. In particular, the absence of bryophytes in sampling sites located in the ADS needs to be further tested to determine whether it results from sampling bias or growth limits in harsh environments.

4.2. Bryophyte Composition of Alpine Grasslands on the QTP

Pottiaceae and Bryaceae were dominant in both alpine grassland types, which are important components of the biological soil crusts in the dryland or desert [36,37,38]. The reasons for this predominance in the alpine grasslands of the QTP were not only because these two families were cosmopolitan and had abundant species but also because they possessed some morphological traits to resist drought stress. For instance, the laminal cells with papillae in most Pottiaceae species in Table 1 formed capillary spaces [39] and thus channeled water movement across the lamina [40,41]. The large proportions of hyaline basal laminal cells in such species as Syntrichia and Bryoerythrophyllum are associated with a higher speed of water conduction [40]. The leaf hair points of Syntrichia spp. and Tortula spp. aid in collecting water from the air [42] and therefore delay and reduce evaporation rates [43]. Overall, Barbula, Bryoerythrophyllum, Didymodon, Syntrichia, Tortula, and Tortella belonging to Pottiaceae and Bryum belonging to Bryaceae, which were identified in our inventory (Table 1), have been documented as desiccation-tolerant [44]. In particular, Syntrichia spp. [42,45,46] and Bryum argenteum [47,48] are emerging as important model organisms for desiccation tolerance in plants.

Although Bryum had the most abundant species in alpine grasslands on the QTP, 6 of the 10 dominant species belonged to the genus Didymodon, corroborating a previous study focused on arid and semi-arid areas of Tibet [13]. Furthermore, we noticed that the proportions of Didymodon increased nearly twofold from AM (8.8%, Figure 3b) to AS (24.1%, Figure 3d), providing additional evidence that Didymodon can be an indicator of climate change on the QTP [49].

Bryophyte diversity at the family, genus, and species levels in AM was much higher than that in AS, which was similar to the species richness pattern of vascular plants [21,50,51] along the decreased precipitation gradient from southeast to northwest on the QTP [52]. Moreover, mosses were rare in the AS of the QTP based on the PS performed by Miehe et al. [26], although they were not specific to bryophyte sampling. On the other hand, the similarities in bryophyte composition at different taxonomic levels between AM and AS were all very low, indicating the sensitivity of bryophytes to different environments. We speculated that one of the climatic drivers of the large differences may be attributed to precipitation. In addition, the simulations of Wen et al. [53] suggested that temperature seasonality and precipitation of the coldest quarter were the key climatic variables for bryophyte distribution on the QTP. Considering the limitations of the current analysis, the roles of various climatic variables in bryophyte composition need to be further examined.

4.3. Bryophyte Life-Forms and Indications for Climate Change

Bryophyte life-forms refer to the arrangements of the whole colony and interact with habitat conditions in terms of moisture availability and light intensity [27,28]. Turfs were predominant (72.5%) across alpine grasslands on the QTP, as previously described in natural grasslands [54], rupestrian grasslands [55], and the summits of Alps between the upper tree line and the nival belt [56]. Compared to AM, the 2/3 decreased proportion of wefts, the absence of mats, and the slightly increased cushions in AS occurred where bryophytes were subjected to stronger drought stress. These results support the general notion that turfs and cushions are common in arid and exposed habitats, whereas mats and wefts mostly occur in shady and humid habitats [27,28].

Turfs and cushions have advantages over wefts and mats to survive in harsh environments of alpine grasslands on the QTP, with strong solar radiation and drought stress. Their colonies are erect and compact, which are effective in retaining water within the capillary spaces between individuals, and thus protect against desiccation [39,57,58]. The dense colonies of turfs and cushions are also beneficial for receiving less light due to self-shading than those widely spaced, such as wefts and mats, and for providing photoprotection [27,59]. Therefore, the types of bryophyte life-forms in AM and AS reflect the adaptive strategies of species to severe environments.

Alpine grasslands on the QTP are among the most sensitive and fragile ecosystems to climate change [60]. The QTP is getting warmer and wetter. Its warming rate has been about twice the global mean in the last three decades [61], and precipitation has slightly increased [62]. In the context of climate change, AM is sharply decreasing, whereas AS is expanding [63]. Warming had different effects on plant productivity and composition in AM and AS [64]. Based on the observed changes in bryophyte life-forms between AM and AS, we suggest that bryophyte life-forms can be used to monitor vegetation dynamics in alpine grasslands of the QTP. Furthermore, they are easily and directly obtained in the field and have already been used to indicate land-use changes in tropical forests [65], in forest successions in Latvia [66], and among different land cover types in an alpine area of northern Italy [54].

4.4. Endemism

Species endemism is one of the most important metrics for evaluating biodiversity [67]. Our results showed that the proportion of endemic bryophytes to China in alpine grasslands on the QTP was 8.05%, which was lower than that of forests (21.8%) in the southeastern QTP [68]. The possible reasons for these are largely attributed to the differences in climate and habitat heterogeneity between the two vegetation types [69]. Mild climates with relatively higher temperatures and precipitation are undoubtedly favorable for supporting more bryophytes in the southeastern forests than in alpine grasslands on the QTP. Moreover, various substrates, such as soil, living trunk, rocks, and fallen logs, increase habitat heterogeneity in forests for bryophytes. In contrast, habitats in alpine grasslands are usually homogeneous. The differential climate of the two grassland types could also explain why more endemic bryophytes occurred in AM (11 species) than in AS (six species). Likewise, the decline of endemism from the southeastern (forests) to the northwestern (grassland) QTP has also been found in seed plants [69,70,71]. Additionally, compared with 38.2% endemic seed plants on the QTP [71], the lower level of bryophyte endemism is usually explained by the strong long-distance dispersal capacities and low diversification rates of bryophytes [72].

5. Conclusions

Our study is the first systematic description of bryophyte flora in alpine grasslands to an outstanding geographic extent based on PS. The bryophyte composition, richness, life-forms, and their changes in different alpine grassland types reflect the adaptations of bryophytes to harsh environments. Considering the conservation priority of AM and AS on the QTP for global biodiversity, bryophyte diversity in alpine grasslands on the QTP is exceptional and irreplaceable regardless of species richness, especially when these species are experiencing unusual ecological and evolutionary processes on a unique tectonic unit of the Earth. Therefore, the exploration of bryophyte flora and conservation should be strengthened in the future.