Plant Ecol (2011) 212:1349–1361 DOI 10.1007/s11258-011-9911-5
Grassland composition, structure, and diversity patterns along major environmental gradients in the Central Tien Shan John B. Taft • Loy R. Phillippe • Chris H. Dietrich • Kenneth R. Robertson
Received: 8 June 2010 / Accepted: 2 March 2011 / Published online: 19 March 2011 Ó Springer Science+Business Media B.V. 2011
Abstract What species and traits signal vegetation types along prominent environmental gradients in the Central Tien Shan and what are the corresponding diversity patterns? Vegetation was sampled at 41 sites throughout the Kyrgyz Republic using quadrats stratified throughout a 1,000-m2 sample area. Relationships among major environmental gradients, vegetation structure, and species composition were explored with nonmetric multidimensional scaling. Species distributions were examined to characterize phytogeographic patterns. Seven vegetation types ranging from desert grassland to meadow steppe were identified with cluster analysis, ordered primarily along elevation/mean annual temperature gradients. Four arid grassland types were distinguished, ranging mainly from 900 to 1,700 m elevation, and characterized by co-dominance of grasses and forbs with secondary dominance by shrubs. Annual and
biennial forbs equaled perennial forbs in total importance. Grasses include C3 and C4 species. Three montane grassland types were recognized and characterized by co-dominance of perennial C3 grasses and forbs. Transition to montane steppe occurred from 1,500 to 1,900 m and is correlated with absence of C4 grasses and dominance of Festuca valesiaca. Highest diversity was found at intermediate elevations, from 1,800 to 2,600 m, in meadow steppe habitats. Forty-six percent of 580 identified species are Middle Asian endemics and remaining species primarily have distributions including Eastern Europe, the Caucasus, and western Siberia. Although grassland degradation from overgrazing has been chronic throughout the region, grasslands are widespread throughout the Kyrgyz Republic and many, particularly mid-elevation meadow steppes, retain high levels of native species diversity.
Nomenclature: botanical nomenclature follows Czerepanov (1995).
Keywords Grazing Functional groups Kyrgyz Republic Middle Asia Nonmetric multidimensional scaling Species density Steppe
Electronic supplementary material The online version of this article (doi:10.1007/s11258-011-9911-5) contains supplementary material, which is available to authorized users. J. B. Taft (&) L. R. Phillippe C. H. Dietrich K. R. Robertson Illinois Natural History Survey, Institute of Natural Resource Sustainability, University of Illinois, 1816 S. Oak Street, Champaign, IL 61820, USA e-mail:
[email protected]
Introduction Grasslands throughout the world are among the most threatened ecosystems due to conversion for cropland, habitat degradation often from overgrazing, exotic species invasions, and woody encroachment
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(Samson and Knopf 1994; Gibson 2009). Intensive land uses in arid and semi-arid regions have lead in some cases to desertification (Grainger 1992; Babaev and Kharin 1999). Grasslands in arid and semi-arid regions also appear to be vulnerable to anthropogenic climatic change (Xiao et al. 1995; Zavaleta et al. 2003). Increasing woody encroachment of grasslands has been ongoing in some regions and may be an increasing factor in arid habitats (Zavaleta and Kettley 2006). Despite these threats, of the world’s major biomes temperate grasslands remain the least protected with less than 1% of the total area included in conservation reserves (Groombridge 1992; Gibson 2009). Among the most extensive temperate grasslands remaining are the steppes and semi-desert grasslands of Middle Asia, comprising 18% of the total grassland area of the world (McCloud 1974). Steppes are semi-arid grasslands characterized by relatively lowgrowing bunch grasses interspersed with forbs and shrubs (Gibson 2009). About 45% of the land area of the Kyrgyz Republic (Kyrgyzstan before 1991) retains grassland vegetation, broadly considered here as habitats dominated by herbaceous species with prominent graminoid cover, including habitats such as semi-desert and semi-savanna with scattered low shrubs (Nikol’skii 1994). Previous agricultural practices in Middle Asia resulted in extensive degradation of grasslands (Babaev 1982; Ponomarenko and Ponomarenko 1996) including overgrazing and degradation of the grasslands in Kyrgyzstan with up to 25% being severely overgrazed. Livestock numbers exceeded grazing capacity by 5–10 times (Ministry of Environmental Protection 1998). With one of the highest population growth rates in Middle Asia, as well as severe economic difficulties and high rates of poverty, agricultural and grazing pressures have been expected to increase again (Nikol’skii 1994; Ministry of Environmental Protection 1998) thus magnifying the urgency to document characteristics of the regional biodiversity. General descriptions of Middle Asian mountain floras include Berg (1950); Vykhodtsev (1976); and Korovin (1961); however, detailed descriptions are scarce (e.g., Wagner 2009) and the region remains insufficiently known (Agakhanjanz and Breckle 2002). Data specifically from Kyrgyz arid and montane grassland habitats are few (Heinicke 2003, 2004) or general (Kamelin 2002) despite their extent
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and ecological and economic importance. From 1998 to 2000, a series of expeditions throughout the Kyrgyz Republic conducted basic floristic and arthropod surveys in grassland habitats ranging from semidesert to high-elevation meadow steppe. Results from arthropod surveys partially have been reported (Novikov et al. 2006). Quantitative vegetation data were collected at selected sites as a representation of habitat characteristics. In this article, we examine patterns of plant species composition, structure, and diversity along major environmental gradients in the Central Tien Shan mountain complex. The 41 georeferenced vegetation samples used in this study (Online resource 1), collected from 15 of 17 floristic regions recognized in the Kyrgyz Republic (Kamelin 2002), provide a framework for further detailed comparative study of these diverse and little-known grasslands.
Methods Study area Vegetation samples in this study were collected within the Kyrgyz Republic, a Middle Asian country (199,900 km2) with continental climate located between China, Kazakhstan, Uzbekistan, and Tajikistan (Fig. 1). Physiographically, the region is dominated by the Tien-Shan and Pamir-Alai mountain systems. Elevation ranges from 132 to 7,439 m above sea level with about 25% of the land area above 3,500 m and dominated by snow, ice, and rock; land cover below 3,500 m includes predominantly grasslands with local non-grassland habitats such as shrubland, forest, sparsely vegetated (rocky) areas, and developed land (Ministry of Environmental Protection 1998). Grazing and haying remain common land use practices.
Vegetation sampling A total of 802 vegetation sampling quadrats [70.7 9 70.7 cm (0.5 m2)] were recorded along 41 transects at collection sites throughout the Kyrgyz Republic (Fig. 1; Online resource 1). Samples were recorded from elevations ranging from 675 to 3,530 m above sea level. Sample dates were
Plant Ecol (2011) 212:1349–1361 70 E 43 N
Kazakhstan
1351 73 E
76 E
79 E
Bishkek
Lake Issyk-Kul
Kyrgyz Republic
n Ti e
Uzbekistan
a n S h
ns t a i u n M o
40 N
China
Tajikistan Semi-Arid to Arid Grasslands
Pa m i r
M o u n t a i n s Montane Grasslands 0
General Collection Sites 50
100
150
200
250
300 Kilometers
Fig. 1 Quantitative and general sample locations for botanical (and entomological) collections in grassland habitats of the Kyrgyz Republic
throughout August 1998, June 1999, and July 2000. Some sites were sampled with multiple transects to account for local variation; in three instances, the additional transect was shortened (time limitations). No sample data were recorded in the southwestern Turkestan-Alay Province due to restricted access. Transects were located by tossing a ring into vegetation that was representative of sample areas. Transect orientation was determined randomly. Quadrat placement began every 5 m along 100-meter-long transects, with each quadrat randomly placed at distances up to 5 m from the transect line on alternating sides creating a stratified-random sample grid of typically 20 quadrats from a 1,000-m2 area (10 m2). Percent cover for each species rooted inside the quadrat frame and percent bare ground were estimated using modified Daubenmire cover classes (0 \ 1%, 1 \ 5%, 5 \ 25%, 25 \ 50%, 50 \ 75%, 75 \ 95%, and 95–100%). Plants senescent above ground were included if identifiable at least to family and from the current growing season. Voucher specimens were collected for most species and deposited in the herbarium of the Illinois Natural History Survey (ILLS). Data analysis Data analysis was conducted using PC-ORD Version 4.34 (McCune and Mefford 1999), CANOCO
Version 4.54 (ter Braak and Smilauer 2002), Primer Version 6.1 (Clarke and Gorley 2006), and Microsoft Excel 2002. Species abundance is based on importance values (IV) calculated as the sum of relative cover and relative frequency. Dominant species for each community type are the top-ranking taxa that sum to 50% of total IV. Dissimilarity among sites can be determined effectively with the Sørensen Index (Faith et al. 1987) and two transects identified in outlier analysis (PC-ORD) as moderate outliers (SD [ 2.3, \3) based on average distance among all transects were eliminated from further analysis. Cluster analysis, based on the clustering algorithm of Wishart (1969) and Post and Sheperd (1974) in PCORD, was used to produce a classification of sites from sample data. Flexible sorting with b set at 0.25 was used for its optimal grouping characteristics (Lance and Williams 1967) to construct a hierarchical dendrogram based on Sørensen distance measures. The dendrogram was pruned based on results from indicator species analysis (Dufrene and Legendre 1997) and recommendations by McCune and Grace (2002). Values from indicator species analysis also were used to identify taxa modal to particular community types with significance (P B 0.05) determined from Monte Carlo randomization tests (1,000 iterations). Qualitative similarity among sample groups was determined using Sørensen’s index (Mueller-Dombois and Ellenberg 1974). Within-group
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dispersion, based on Bray–Curtis similarity and tested with the PERMDISP procedure (Anderson 2004), was used to compare differences in Beta diversity between broad vegetation classes. Vegetation types follow Vykhodtsev (1976). Indirect gradient analysis using Nonmetric Multidimensional Scaling (Kruskal 1964) was used to examine variance in species composition among sites and we then searched for correlations between the ordination and selected environmental and structural variables. NMS was used for its independence from species response models and optimal graphical representation of community relationships (McCune and Grace 2002). Abiotic variables used in the analysis included elevation, longitude, latitude, mean annual temperature, and mean annual precipitation. Mean annual temperature and precipitation were taken from scalable isopleth thematic maps (World Trade Press 2007). These data were combined with vegetation structure parameters of percent cover, percent bare ground, alpha diversity [mean species density (richness/quadrat)], species diversity [Shannon–Wiener index (H0 )], and dominance (Simpson’s Index). All variables were log transformed to facilitate comparisons among variables with widely differing scales. Using the Sørensen distance measure and a random starting configuration, results from 400 random starts of NMS were examined in one to six dimensions. A Monte Carlo test was applied to the randomized runs to determine whether the ordination axes reduced more stress than expected by chance. The strength of the correlations between axes and environmental variables was determined with Pearson’s correlation coefficient (r). Phytogeographic distributions follow range information in Czerepanov (1995) and include Middle Asian endemics, and species with distributions ranging to eastern Europe, Caucasus, western Siberia, eastern Siberia, and the far East. Plant functional groups were distinguished based on a combinations of growth form (forb, grass, sedge, and shrub), life history (annual, biennial, and perennial), and ecophysiology (C3, C4, and nitrogen fixers) to further characterize habitat structure. Association of functional groupings and vegetation types were examined with Principal Components Analysis (CANOCO) after confirming that a linear response model was acceptable.
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Results Overall species diversity and composition Six hundred and sixty-one taxa were recorded in 802 quadrats along 41 transects throughout the Kyrgyz Republic; 583 of these taxa were identified to species accounting for 94% of the IV (200). Remaining taxa, mostly vegetative material, could not be determined to species; sterile individuals of Artemisia subgenus Serifidium account for nearly half the total unknown IV. Fifty-two plant families and 256 genera were recorded among the samples. The dominant plant families (with species numbers) were Asteraceae (100 species), Poaceae (93), Fabaceae (53), Lamiaceae (40), and Apiaceae (36) representing 49% of all species. The most species rich genera were Astragalus (16 species), Artemisia (14), Allium (14), Potentilla (13), and Carex (10). Fifty percent of all species occurred in a single transect and only 30% occurred in more than two transects. Mean alpha diversity per 0.5 m2 was 11.5 species and mean species richness per transect was 40.9 (Table 1); variables ranged widely with a maximum mean alpha diversity per transect of 22 and total richness per transect of 74 species. Mean vegetative cover and bare ground were 117.5 and 25.8%, respectively. Shannon diversity (H0 ) averaged 2.98, and dominance (Simpson’s index) averaged 0.086. Dominant species in descending rank order were: Festuca valesiaca, Carex turkestanica, Artemisia sp. [subgenus Seriphidium (vegetative)], Stipa capillata, Bothriochloa ischaemum, Poa bulbosa, Artemisia scoparia, Bromus oxydon, Artemisia persica, and Artemisia serotina. These ten dominants, six graminoids (one sedge and five grasses) and four subshrubs, account for 25.6% of importance among all species. Vegetation types Seven vegetation classes were identified in cluster analysis with 30% of information remaining. These classes form two main groups by pruning the dendrogram close to the base (Fig. 2). The first group includes three classes of montane grasslands [classification scheme approximates Vykhodtsev (1976) using combinations, as needed]: class 1—montane steppe, class 2—meadow steppe, and class 3—montane meadow. The second group includes four classes of
11.52 (4.56)
9.06 (2.72)
7.50 (1.80)
10.50 (2.60)
8.60 (3.70)
8.30 (1.60)
40.93 (13.5)
36.42 (9.48)
24.00 (1.70)
39.70 (6.20)
36.80 (11.80)
39.50 (9.10)
44.82 (15.37)
51.70 (12.20)
43.10 (17.20)
44.60 (14.80)
661
308
44
168
129
98
489
121
278
210
Gamma diversity
2.98 (0.42)
2.82 (0.31)
2.63 (0.11)
2.96 (0.27)
2.67 (0.36)
2.91 (0.33)
3.12 (0.46)
3.31 (0.15)
3.09 (0.54)
3.09 (0.43)
Shannon– Wiener
0.09 (0.04)
0.10 (0.03)
0.11 (0.02)
0.09 (0.03)
0.12 (0.04)
0.10 (0.04)
0.07 (0.041)
0.05 (0.003)
0.08 (0.053)
0.07 (0.031)
Simpson’s index
117.5 (49.8)
89.8 (38.4)
55.8 (12.1)
109.7 (45.2)
97.9 (25.0)
70.2 (33.7)
141.5 (46.5)
207.5 (18.5)
122.1 (38.2)
143.5 (43.0)
25.75 (18.16)
36.88 (16.05)
48.00 (4.35)
29.04 (17.56)
29.80 (4.28)
51.09 (16.48)
16.15 (14.10)
2.57 (1.66)
18.53 (13.96)
17.97 (15.02)
%Bare grd.
1,922.5 (783.1)
1,303.7 (494.9)
1,683.3 (14.4)
1,205.6 (704.5)
1,521.4 (158.5)
918.8 (12.6)
2,456.9 (559.2)
2,293.3 (46.2)
2,843.8 (421.8)
1,986.1 (428.1)
Elevation (m)
Environmental
4.42 (4.9)
8.49 (2.67)
5.83 (0.00)
9.01 (3.37)
8.17 (2.20)
10.00 (1.60)
0.91 (3.42)
-1.57 (1.60)
-0.73 (2.57)
4.10 (2.54)
Temp. (MA C)
417.7 (132.9)
388.2 (155.3)
125.0 (0.0)
375.0 (0.0)
575.0 (111.8)
375.0 (0.0)
443.2 (107.2)
416.7 (72.2)
386.4 (87.6)
531.3 (88.4)
Precip. (MA mm)
Veg vegetation, Trans transect, Grd ground, Temp temperature, Precip precipitation, MA mean annual, Sd standard deviation. Vegetation classes 1–3 are the Montane grassland group; classes 4–7 are the arid grasslands group. Values between [] are totals, not averages
41
3
7
Total
7
6
[19]
5
5
Avg.
4
4
13.64 (4.81)
15.90 (6.00)
[22]
3
Avg.
3
13.90 (4.90)
2
12.40 (4.50)
8
11
1
Spp. richness
%Cover
Alpha diversity Mean (SD)
Veg. class
No. trans.
Vegetation structure
Species diversity
Table 1 Summary variables for species diversity, vegetation structure, and select environmental variables from vegetation sample data recorded throughout the Kyrgyz Republic in Middle Asia
Plant Ecol (2011) 212:1349–1361 1353
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Plant Ecol (2011) 212:1349–1361
25
Information Remaining (%)
0
1354
1
2
3
4
5
6
7
Fig. 2 Dendrogram of results from cluster analysis. Two broad groups were identified. The first group includes three classes of montane grasslands: class 1 montane steppe, class 2 meadow steppe, and class 3 montane meadow. The second group includes four classes of arid to semi-arid community
types: class 4 sub-shrub semi-desert/montane semi-savanna, class 5 semi-savanna/montane steppe, class 6 sub-shrub semidesert/montane semi-savanna/montane steppe, and class 7 temperate desert
arid to semi-arid grasslands: class 4—sub-shrub semi-desert/montane semi-savanna; class 5—montane semi-savanna/montane steppe; class 6—subshrub semi-desert/semi-savanna (with elements of montane steppe); and class 7—desert grassland. Dominant and significant indicator species for each vegetation class are shown in Online resource 2. Montane grasslands (classes 1–3) were distinguished from the more arid grasslands by dominance of Festuca valesiaca (Online resource 2). Dominant species identified as significant indicators for class 1 were Carex turkestanica and Eremurus fuscus. Other significant indicators include Veronica arvensis, Phlomoides speciosa, Ferula kuhistanica, and Linaria transiliensis. Dominant indicators for class 2 were Festuca valesiaca, Euphrasia regelii, Potentilla nervosa, Helictotrichon tianschanicum, and H. hookeri. Other significant indicators include Geranium saxatile and Ligularia thomsonii. Dominant species identified as significant indicators for class 3 were Iris rutanica, Geranium collinum, Achillea millefolium, Bromopsis inermis, Galium turkestanicum, Trifolium repens, Plantago major, and Agrostis gigantea. Other significant indicators include Delphinium iliense and Vicia tenuifolia. Several other indicator species with minor abundances were identified (Online resource 2). Arid grasslands (classes 4–7) were distinguished from montane grasslands by dominance of Bothriochloa ischaemum, Artemisia scoparia, A. serotina, and Kochia prostrata and the near absence of Festuca valesiaca. Dominant species identified as indicator species at class 4 sites were Artemisia sp. (Subgen.
Serifidium), Setaria viridis, Lappula microcarpa, and Artemisia serotina. Other indicator species include Diarthron vesciculosum, Althaea nudiflora, and Vinca erecta. Pistacia vera was a common associate although it was infrequently recorded in sample plots. Dominant indicators in class 5 sites included Artemisia persica and Centaurea squarrosa. Other indicators include Verbascum songoricum, Leptorhobdos parviflora, Helianthemum songoricum, and Phlomis sewarsowii. Dominant indicator species in class 6 sites were Hordeum bulbosum, Aegilops cylindrica, Taeniatherum crinitum, and Miniocus linifolius. Other indicators include Trigonella grandiflora, Gelium tenuissimum, Camalina sylvestris, Ferula pennivervis, and Galagania fragrantissima. Dominant indicators in class 7 sites were Caragana kirgisorum, Ephedra intermedia, and Artemisia borotalensis. Other indicators were numerous and included Acantholimon alatavicum, Eurotia ceratoides, Neotorularia korolkowii, Seseli valentinae, and Orostachys thyrisiflora. Several other indicator species with minor abundance were identified for each vegetation class (Online resource 2). Sørensen’s index of similarity (IS) between the arid and montane grasslands was 34%; only four species were dominants in both broad vegetation groups: Artemisia sp. (Subgen. Serifidium), Carex turkestanica, Stipa capillata, and Poa bulbosa. These species were found primarily in semi-savanna to montane steppe; they were of lesser importance or absent in semi-desert, meadow steppe, or mountain meadow habitats.
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Middle Asian endemism and phytogeography
Vegetation–environment relations
Forty-six percent of species identified in vegetation samples are Middle Asian endemics (Fig. 3a), averaging 36–39% of all species in arid and montane grassland groups, respectively. Among Middle Asian endemics, similarity between grassland groups is lower (IS = 27.8%) compared to overall betweengroup similarity (IS = 34%). From 32 to 38% of all species have distributions that include each of Eastern Europe, the Caucasus, and Western Siberia; species distributed from Middle Asia to the far East and eastern Siberia were 18–24%, respectively (Fig. 3a). Species distributed in western Siberia had the greatest overall importance (Fig. 3b), particularly among montane grasslands species, and arid grassland species had greater importance among Middle Asian endemics; all other species distribution types were similar between montane and arid grasslands. Seventeen of the approximately 200 vascular plant species endemic to the Kyrgyz Republic were recorded, occurring mostly in meadow steppe or secondarily in transitional semi-savanna/montane steppe habitats.
Mean values for vegetation and environmental parameters for each vegetation class are shown in Table 1 and summarized for the broader arid and montane grassland groups. Results from NMS indicate that a three-dimension solution provided the best configuration (stress value 14.6, P \ 0.05, Monte Carlo randomization test) explaining 69% of the variation in the species data. Correlations between biotic and abiotic environmental factors and ordination axes are shown in Table 2. Axis 1 (37% of overall site variability) is most highly correlated with mean annual temperature (r = -0.89) and elevation (r = 0.88) and separates the montane and arid grassland groups (Fig. 4). Axis 2 (12% of site variability) is most highly correlated with mean annual rainfall, percent cover, and percent bare ground. These factors separate class 5 sites (semisavanna/montane steppe), with relatively greater percent cover and rainfall, from other arid grasslands. Axis 3 (20% of site variability) is most highly correlated with percent bare ground and alpha diversity and separates mountain meadow sites (class 3) from other montane grasslands (Fig. 4). Axis 3 also separates arid grasslands belonging to classes 4 and 7 (sub-shrub semi-desert/semi-savanna and desert grassland, respectively), with lower percent cover and diversity and greater percent bare ground, from class 6 (sub-shrub semi-desert/semi-savanna/montane steppe).
25
50 45
% of Spp
40
Proportion of IV
20
35
15
30 25
10
20 15
Proportion of IV
% of Species
a
5
10 5
0
0 E. Europe Caucasus W. Siberia E. Siberia Far East
% of IV
b
Middle Asian Endemics
Table 2 Pearson correlation coefficients are shown for comparisons with biotic and abiotic site factors and nonmetric multidimensional scaling axis scores Ordination axes (% variance)
1 (37%)
2 (12%)
3 (20%)
Elevation
0.882
-0.009
-0.065
Alpha diversity (spp. density)
0.483
-0.155
0.482
Longitude
0.442
-0.368
0.069
50 45 40 35 30
Montane Grasslands Arid Grasslands
25 20 15 10 5 0 E. Europe Caucasus W. Siberia E. Siberia Far East Middle Asian Endemics
Fig. 3 a Percent of species and proportion of IV for each species distribution type. b Percent of importance value between the arid and montane grasslands for each species distribution type
% Cover
0.405
-0.446
0.392
Shannon diversity (H0 )
0.252
-0.065
0.459
Mean annual rainfall Latitude
0.104 -0.086
-0.614 0.020
-0.016 0.061
Dominance
-0.390
0.077
-0.413
% Bare ground
-0.447
0.412
-0.492
Mean annual temperature
-0.886
-0.061
-0.143
Percent of variance is shown for each axis. Significant correlations (P \ 0.05) are shown in bold
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Plant Ecol (2011) 212:1349–1361 14.0
3,500
LEGEND Class 1 Class 2 Class 3 Class 4 Class 5 Class 6 Class 7
Axis 3
1.0
H' Spp Density % Cover
0.0 Temp.
Elev.
Elevation
3,000
Elevation (m)
a
Mean Annual Temperature
2,500
12.0 10.0 8.0 6.0
2,000
4.0 1,500
2.0
1,000
0.0 -2.0
Dominance
500
% BG
-4.0
Mean Annual Temperature (C)
1356
-6.0
0 Class 4 Class 6 Class 5 Class 7 Class 1 Class 3 Class 2
-1.0 -1.5
-0.5
0.5
1.5
Axis 1
----------Arid Grasslands----------
---Montane Grasslands---
Fig. 5 Mean elevation (m) and mean annual temperature (°C) for vegetation classes identified in cluster analysis. Error bars are standard deviation
b 0.5
Axis 2
% BG
Longitude
Temp.
Elev. Spp Density % Cover
-0.5 Rainfall
-1.5 -1.5
-0.5
0.5
1.5
Axis 1
Fig. 4 Nonmetric multidimensional scaling ordination diagrams showing a axes 1 (R2 = 0.369) and 3 (R2 = 0.206) and b axes 1 and 2 (R2 = 0.118). Montane grasslands (squares) are: class 1 montane steppe, class 2 meadow steppe, class 3 montane meadow. Arid grasslands (triangles) are class 4 subshrub semi-desert/semi-savanna, class 5 semi-savanna/montane steppe, class 6 sub-shrub semi-desert/semi-savanna/montane steppe, and class 7 desert grassland. %BG percent bare ground, Elev mean annual elevation, H0 Shannon diversity, Spp Density species density/quadrat, Temp mean annual temperature
In general, the arid grasslands correlate with increasing mean annual temperature, percent bare ground, dominance, and decreasing elevation. Meadow steppe and montane meadow sites are correlated with increasing elevation, percent cover, and species density. Montane steppe sites are intermediate between arid grasslands and meadow steppes (Fig. 4). Mean annual precipitation was greater in montane grasslands (443 mm) compared to arid habitats (388 mm), but the differences were not significant. Transitions from arid communities to montane steppe generally occurred from about 1,500 to 1,900 m elevation and where mean annual temperatures are less than 6°C (Fig. 5), though there are exceptions. One of the two southern-most sites was classified in the arid group at 2,530 m elevation but
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has lower mean annual precipitation than other sites in this elevation range (i.e., 37.5 cm/year compared to 62.5 cm/year). One northern site classified as montane steppe occurring at 1,100 m elevation had mean annual temperature of 8.6°C. Transitions from montane steppe to meadow steppe occurred at 2,200–2,400 m and 0–2°C mean annual temperature (Fig. 5); however, one site classified as meadow steppe occurring at 2,260 m elevation had mean annual temperature of 5.8°C. Species diversity patterns among vegetation types Montane grasslands, with 489 recorded taxa in 22 transects, had greater gamma diversity compared with arid grasslands with 308 taxa recorded in 19 transects (Table 1). As a test of Beta diversity, mean homogeneity of multivariate dispersion, based on Bray–Curtis similarity scores, is greater among arid grasslands (61.9) versus montane grasslands (58.8) and the difference, tested with permutational multivariate analysis of dispersion (PERMDISP), was significant (P = 0.03). Alpha diversity, species richness, and percent cover were greatest in the mountain meadow vegetation type (class 3) followed by meadow steppe and montane steppe (Table 1). However, diversity ranged widely across the elevation gradient and only a weakly unimodal, humped pattern was observed (R2 = 0.0997), fit best by a 3rd order polynomial trend line (R2 = 0.205; see Online resource 3 for details of Bayesian normal cubic regression). Mean alpha diversity and total species richness among montane steppe and meadow steppe sites ranged widely from 6.2 to 22 (alpha diversity)
1357 LEGEND Class 1 Class 2 Class 3 Class 4 Class 5 Class 6 Class 7
C3 p-grass
p-sedge
p-monoforb hemipar C3 a-grass tree a-legume a-forb bi forb
Axis 2
and 11 to 74 (species richness); the highest mean alpha diversity samples were from mid-elevation sites (1,800–2,600 m). The range of variation for diversity among arid grasslands was far less compared to montane grasslands with no single vegetation class greatly different from the others (Table 1). Overall for the study, alpha diversity is correlated positively with increasing percent vegetation cover and a polynomial trend line only explains slightly greater variance in the data (R2 = 0.428, P \ 0.00001) compared to a linear trend (R2 = 0.415).
1.0
Plant Ecol (2011) 212:1349–1361
leg. shrub
leg. p-forb
shrub C4 a-grass
C4 p-grass leg. biforb
p-forb
-1.0
Vegetation structure–functional groups Forbs account for about 44% of the total IV among species and graminoids (grasses and sedges) account for 41%, with 38 and 46% of the IV in arid and montane grasslands, respectively (Fig. 6). Woody plants, mostly Artemisia subshrub species, account for 13.9% of the total IV. In more detailed groupings based on life history, physiognomy, and ecophysiognomy, perennial forbs were the most dominant with 26.4% of the IV, and the most species rich with 45.6% of all species. Perennial C3 grasses rank second in dominance with 24% of the IV and 10% of species. Only three C4 grass species were recorded (arid grasslands), accounting for 3.3% of total IV. While montane grasslands had greater species diversity, functional-group diversity was greater among the arid grasslands with montane steppe intermediate between the arid grassland groups and meadow 100 90 80 70
-1.0
1.0
Axis 1
Fig. 7 Scatterplot of a principal components analysis of plant functional groups and vegetation types from sample data in the Central Tien Shan mountain complex. Scaling is focused on inter-species (functional group) correlations. Cumulative explained species data in four ordination axes was 88.1%. Classes 1–3 are montane grasslands (squares) and classes 4–7 are arid grasslands (triangles). a annual, bi biennial, p perennial, leg legume, hemipar hemiparasite
steppe (Fig. 7). Short-lived species (annuals/biennials), C4 grasses, and shrubs were predominately associated with the arid grassland group (Fig. 7) where they comprise about 59% of the total IV versus 15% among the montane grasslands (Fig. 6). Sum IV of these groups is correlated inversely with elevation (R2 = -0.70) and positively with mean annual temperature (R2 = 0.69). Perennials including forbs, C3 grasses, sedges, and legumes predominately were associated with the montane grasslands (Fig. 7), accounting for 83% of the total IV compared to 39% in arid grasslands (Fig. 6).
Subshrubs
% IV
60
Pforbs
50
ABForbs
40
Graminoids - C4
Discussion
Graminoids - C3
30
Structure, composition, and phytogeography
20 10 0
Montane Grasslands
Arid Grasslands
Fig. 6 Relative importance (% IV) of plant functional groups comparing montane and arid grasslands from sample data in the Central Tien Shan mountain complex. P perennial, AB annuals/biennials, IV importance value (200)
Vegetation types sampled in this study form a continuum from semi-desert to meadow steppe within somewhat discrete temperature and elevation belts, stressing the dominant role of temperature as the major driver of species changes along elevation gradients (Walter 1985). Dominant and indicator species and the assemblage of plant functional groups
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signal particular vegetation types along the elevation gradient. These grasslands, ranging from 39° to 43°N latitude and from 675 to 3,530 m above sea level, correspond somewhat to structure and dominant species composition of steppes arranged along latitudinal gradients primarily above 48°N latitude. The arid grasslands correspond to semi-desert and desert grasslands in the southernmost region described by Lavrenko and Karamysheva (1993) and Titlyanova et al. (1999) and montane steppes correspond most closely to the true and meadow steppes further north. The arid communities range primarily from subshrub semi-desert grasslands to semi-savannas. The much greater proportion of short-lived species (annuals and biennials) in the arid vegetation types is to be expected given greater available niche space for regeneration and the adaptive strategy of seed-bank storage in arid habitats. Grazing in semi-arid steppe habitats also can increase the proportion of shortlived species (Zhang 1998). Transitions from arid to montane grassland vegetation types occurred over a relatively broad elevation range compared to transitions from montane steppe to meadow steppe. Gradual transitions have been reported for other arid mountain floras in Middle Asia (Agakhanjanz and Breckle 2002). Species that could be expected in this broad ecotone include the four taxa found as dominants in both vegetation groups: Artemisia sp. (subgenus Serifidium), Carex turkestanica, Poa bulbosa, and Stipa capillata. In general, transitions from more arid grasslands to montane steppe communities have a predictable pattern in vegetation structure and are associated with scarcity or absence of C4 grasses and short-lived taxa, increasing importance of perennial forbs and perennial C3 grasses, and emergence of Festuca valesiaca as a dominant species. The relatively abrupt transition from montane steppe to meadow steppe occurring at about 1°C mean annual temperature suggests an ecophysiological threshold. The strong dominance of perennial forbs and C3 grasses in montane steppe and meadow steppe vegetation types has similarities and some noteworthy differences with other temperate grasslands. Perennial forbs also dominate eastern tallgrass prairies in North America in terms of species richness and total percent cover. However, in the North American grasslands, with hot summer temperatures and periodic droughts, C4 grasses are characteristic and among the dominant species although often
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intermixed with subdominant C3 graminoids (Anderson 2007). The occurrence of C4 grasses in arid grasslands and their absence in the montane grasslands of the Central Tien Shan is associated with an altitudinal gradient despite the largely semi-arid climate. Similar distributions of C4 and C3 grasses along altitudinal gradients have been observed for other mountain grassland ecosystems (e.g., Cabido et al. 1997) reinforcing the primary role of temperature in governing the transition from C4 to C3 dominance (Terri and Stowe 1976). Increases in C4 species (e.g., Bothriochloa ischaemum) or establishment into higher elevation zones of the Central Tien Shan may provide an indicator for climate change. Similarities among dominant species in the montane grassland group of this study to dominant or diagnostic species from the northwestern (NW) Tien Shan (Wagner 2009) include the widespread Festuca valesiaca, Iris sogdiana, Koeleria cristata, Poa angustifolia, and Bromopsis inermis. However, there are notable differences. Six Stipa and two Helictotrichon species, grasses among the dominant and/or indicator species in this study, are scarce or absent from meadow steppe and montane meadows in the NW Tien Shan (Wagner 2009), including the wideranging S. capillata. This needlegrass, present but scarce in the NW Tien Shan, is among the dominant species in montane steppe grasslands in this study and elsewhere in Kazahkstan (Lavrenko and Karamysheva 1993; Cheng and Nakamura 2007). The proportion of Middle Asian endemics among all recorded species in this study (46%) is similar to reports from the NW Tien Shan (Wagner 2009). The 39% of Middle Asian endemics in montane grasslands reported here is notably greater than reports for the total mountain region of the western Tien Shan where 17% of species were reported to be endemic (Pavlov 1974). The lower similarity between montane and arid grasslands among Middle Asian endemics, contrasted with similarity in these groups among all species, suggests that widespread species tend to have broader ecological amplitude compared with regional species. Species with distributions ranging to Siberia and Eastern Europe also are prominent, contributing up to 38% of taxa and up to 44% (among montane grasslands) of species importance in this study. This extends the relatively high prominence of Euruosiberian elements further south than previously
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described (Wagner 2009). Eurosiberian species recorded from montane grasslands in the Central Tien Shan that were dominant or diagnostic species from meadow steppe and montane meadows in NW Tien Shan (Wagner 2009) include Achillea millefolium, Alopecurus pratensis, Bromopsis inermis, Phleum phleoides, Poa angustifolia, and Polygala comosa. Some of the common forage species may be introductions; however, the widespread occurrence of these northern elements may represent pre-Pleistocene relicts or post-Pleistocene migrations (Korovin 1961; Wagner 2009). Species diversity Kyrgyz grasslands appear as species rich or in some cases more so than other temperate Asian grasslands. Results from Mongolian steppe recorded in 64 1 m2 quadrats (Zhang 1998) yielded a total richness of 60 species. Four sites in this study exceeded this level in 20 0.5 m2 quadrats. Data from steppe vegetation in eastern Kazakhstan (Cheng and Nakamura 2007) yielded 8.4–20 species per stand, but stand size among samples ranged from 1–4 m2 and precise estimates of mean species density can not be determined. Mean alpha diversity in 4 m2 plots in meadow steppe and montane meadow habitats in the NW Tien Shan ranged from 18 to 31 species and total richness in 94 plots was 193 species (Wagner 2009). Mean alpha diversity of montane grasslands in this study ranged from 12.4 to 15.9 species in 0.5 m2 plots and total richness in 22 montane grassland transects was 489 species. The individual sites combining highest dominance and lowest diversity were level, high elevation (2,967 and 3,530 m, respectively) meadow steppes with strong dominance of Festuca valesiaca and no recent grazing. Species richness recorded from these sites is consistent with a pattern of floristic drainage (species attrition) in higher elevations (Agakhanjanz and Breckle 2002; Dickore and Miehe 2002), though such findings are not universal (Shimono et al. 2010). Intermediate elevations in this study (1,800–2,600 m) included the highest diversity sites as well as sites with below-mean levels of alpha diversity. The most diverse sites were meadow steppes while the lower diversity sites included examples of montane steppe and arid grassland types. The weakly humped pattern of diversity along the elevation gradient observed
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from the Central Tien Shan indicates the relationship can be complex with much variation at each elevation belt. The highest transect-level means for Shannon diversity, alpha diversity, and species richness were recorded from two grazed montane meadow habitats within a spruce zone (Picea schrenkiana), the only samples from within a humid montane forest belt in this study. The maximum individual species density recorded (31 species/0.5 m2) was from a sloping high elevation (3,000 m) meadow steppe that also was grazed. While grazing intensity at these sites appeared relatively heavy at the time of sampling, duration is unknown. It was not possible in this study to assess site land-use histories in detail. In general, moderate grazing appears to maintain species diversity in Middle Asian steppe vegetation (Berg 1950; Walter 1985; Zhang 1998; Zhou et al. 2002). However, in Mongolian steppes as grazing intensity increases there have been demonstrated effects including increases among ruderal and unpalatable species, including some Artemisia species. These changes were associated with nutrient gradients facilitated by livestock (Fernandez-Gimenez and Allen-Diaz 2001). In another study, intensive grazing shifted communities to domination by Artemisia frigida with declines in the formerly dominant Cleistogenes squarrosa (one of the few C4 grasses recorded in the present study), leading to a stable state of shrub domination that did not recover with grazing cessation (Gao et al. 2005). Dominance of Festuca valesiaca has been considered in some regions to be representative of initial stages of true steppe degradation from overgrazing, replacing former dominance by Helitotrichon desertorum (Titlyanova et al. 1999). However, Helitotrichon species in the Central Tien Shan were limited to the meadow steppe community type where there was no clear relationship to the abundance of F. valesiaca. Montane grasslands in the Central Tien Shan were grazed mostly by sheep and horses while cattle grazed more frequently in arid grasslands. Past regional policies have promoted exploitation of rangeland leading to grassland degradation in both Kyrgyzstan (Ministry of Environmental Protection 1998) and Mongolia (Sneath 1998). The reduction in livestock numbers experienced in Kyrgyz grasslands since independence in 1991 [though not forests (Schickhoff et al. 2008)], if prolonged, may result
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in gradual recovery from excessively grazed conditions and a shift toward greater dominance of perennials in arid regions. These geo-referenced data provide a framework for examining future vegetation changes. Acknowledgments Our sincere gratitude to the following systematists who assisted with selected species identification: Georgy Lazkov, Anton Reznicek (Cyperaceae), Mary Barkworth (Poaceae), Lyuba Kapustina, and Jason Koontz (Delphinium). Special thanks to expedition coordinator Dmitry Milko and for field assistance to Natalia Novikova and Emily Warren. Thanks also to Janet Jarvis for assistance with location map and to Associate Editor Peter Minchin and anonymous reviewers for constructive comments. This study was supported by a grant from the National Science Foundation (NSF Grant # DEB 9870187).
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