Abstract
Overgrazing of China’s grasslands is increasingly causing biodiversity to decline. In degenerated grasslands of northwest China endophyte (Epichloё gansuensis) infected Achnatherum inebrians (drunken horse grass) is becoming widely distributed because of its toxicity to livestock. In this study, we investigated the ecological consequences of endophyte toxicity in this native grass, at three sites in northwest China, by comparing seed production of plant species and arthropod abundance in overgrazed grasslands with and without the presence of A. inebrians. Our findings demonstrate that the presence of endophyte infected A. inebrians reduces the loss of plant and arthropod biodiversity by providing a protected nursery free of animal grazing. Therefore, A. inebrians, typically regarded as an unwanted toxic invader by pastoralists, should be viewed as beneficial for grasslands as its presence maintains plant and arthropod biodiversity and provides a foundation stone in the reconstruction and restoration of these grassland ecosystems.
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Introduction
Overgrazing of grasslands worldwide is causing flora and fauna biodiversity to decline1,2,3. China has the second largest area of pastoral land in the world and these pastoral lands play a very important role in the global ecology4. Without exception, grasslands in northwest China face serious overgrazing from livestock, resulting in reduction of forage grasses, invasion of inedible plants and appearance of bare ground5,6,7. In contrast, a native perennial grass species Achnatherum inebrians, known as “drunken horse grass”, is now thriving in these grasslands due to its toxicity to grazing animals such as sheep, goats, cattle and horses8,9. This toxicity is caused by a seed-transmitted symptomless fungal endophyte, Epichloë gansuensis10. Epichloë endophytes can be viewed as fungi that grow and function in host grasses as if they are a host tissue, with the growth being fully synchronized and symptomless within host plant tissue11.
Achnatherum inebrians is now widely found in grasslands of northwest China, including Qinghai province, Tibet province, Gansu province, Xinjiang province and parts of Inner Mongolia9. The grasses distribution has expanded as pastures have degenerated through overgrazing in past decades. For example, in Xinjiang, A. inebrians occupied 400 000 ha in 1987 and had expanded to 533 000 ha by 19929. Due to its conspicuous appearance in pastures, that once had luxuriant forage grass and its toxicity, A. inebrians has become a target for control by livestock owners12,13,14. However, the role of this toxic grass in these systems is poorly understood.
Achnatherum inebrians can reach a height of 60–150 cm and each compact inflorescence can produce about 700 small easily-shed seeds9. Based on field observations, A. inebrians forms discrete tussocks within pastures. Due to its morphology and toxicity, A. inebrians could provide a refuge from grazing animals, enabling the survival of palatable plant species. This could also have flow on effects to the arthropod members of the grasslands ecosystem.
Burrowing animals also are a feature of these grassland ecosystems. These include zokor (Myospalax baileyi) that produces molehills and pika (Ochotona curesezoniae) that produce bare patches of ground within the grassland. Zokor are mainly located in eastern Asia15 while pika are widely distributed in Asia, Europe and North America16,17,18,19. These animals have been blamed for contributing to grassland degradation and are actively removed from grasslands6. Achnatherum inebrians appears to be a good colonizer of these bare patches and molehills whilst being rare in overgrazed areas that are still covered by vegetation.
The aim of this study was to determine if arthropod and plant biodiversity in areas with and without tussocks of A. inebrians differs and if bare ground produced by burrowing animals promotes A. inebrians establishment.
Results
Impact of A. inebrians on seed status of other plant species
Plant species present in grasslands of Xiahe, Guinan and Alxa generally, had a greater density of seeds per unit area when tussocks of A. inebrians (TA) were present, compared to areas without this toxic grass (NA). In Xiahe, an area dominated by Elymus nutans, there were 32 plant species that had mature seeds. Of these, 21 species had significantly higher inflorescence numbers or plant numbers in TA compared to NA and 11 of these 21 species only produced seeds in TA. Whilst A. inebrians was generally correlated with greater seed density in TA, five species showed the opposite trend and six species showed no significant difference. Total quantity of seeds of all species and all forage grasses were significantly more abundant in TA than NA (Table 1).
In Guinan, a wet area dominated by the sedge Kobresia capillifolia, there were 12 species that had mature seeds, nine of which were only found in TA and had increased inflorescence or plant numbers. Interestingly, two species were unique to NA, but they were in relatively low abundance. Only one species had a significantly higher number of plants with seed in NA. Overall, the total quantity of seeds of all species and all forage grasses were significantly more abundant in TA than NA (Table 1).
In Alxa, an arid area dominated by the C4 grass Pennisetum centrasiaticum, five species, three of which only had seeds in TA, produced more abundant mature seeds, in TA compared to NA (Table 1).
Impact of A. inebrians on arthropods
Most of the arthropod families identified from soil samples were found with significantly greater numbers in TA compared to NA. In Xiahe, of the 15 families of arthropods 12 were significantly greater in TA when compared with NA. Distribution of three arthropod families did not significantly differ between in the two treatments. Total quantity of individuals of all families was significantly more abundant in TA than NA (Table 2).
In Guinan, there were 11 families of arthropods that were unique to TA. No arthropods were identified in the NA pastures in this study. Nine of the 11 families had significantly greater number in TA than NA (Table 2).
In Alxa, there were 12 families of arthropods identified, seven of which were only found in TA, with 5 families being present in both treatments, only one of which was significantly increased in the TA sample. Total quantity of all arthropods was significantly greater in TA than NA (Table 2).
Contribution of zokor and pika to the spread of A. inebrians
The establishment rate from seeds of A. inebrians on molehills of zokor was significantly greater than in NA in Xiahe (Fig. 1a). The average density of one-year old A. inebrians plants in bare patches was significantly greater than in NA in Guinan (Fig. 1b).
The spread of Achnatherum inebrians.
(a) Comparison on the establishment rate of A. inebrians seeds in molehills and in overgrazed area without A. inebrians (NA) in Xiahe. (b) Comparison on number of one-year old A. inebrians plant in bare patches and overgrazed area without A. inebrians (NA) in Guinan. Mean values were presented in the text ± 1 SE.
Discussion
Achnatherum inebrians is likely to play a positive role in the protection and regeneration of overgrazed grassland ecosystems in northwest China since it was shown in this study to be able to colonise bare ground. The growth habit of A. inebrians is such that large tussock plants develop interspaced with other palatable pasture species which can become established due to the production by A. inebrians of endophyte toxins that deter livestock grazing. This sheltered environment becomes a nursery area where the protected plants can flourish and again produce seed. Therefore, rather than being an undesirable invader12,13,14, this study has revealed that A. inebrians provides a means by which the seed resources of edible plant species can be saved in the face of over-grazing.
Without bare soil A. inebrians has a poor ability to establish from seed. The bare land in which A. inebrians can establish and which is now a widespread feature of degenerated grasslands, is frequently the result of the feeding activity of burrowing animals18. A common viewpoint is that the bare patches caused by pika and the molehills of bare earth caused by zokor are a major cause of grasslands degeneration6. Zokor and pika are widely distributed in grasslands and have a high density in the Qinghai-Tibetan Plateau (QTP)20,21. Bare patches caused by pika accounted for 62.6% of the total area of degraded grassland in Qinghai Province, while 25% of the total area was degraded in the QTP18. However, it is likely that continual overgrazing by livestock is primarily responsible for the conspicuous damage that these rodents are now causing. As suggested by Harris22, the presence of abundant rodents may be an indicator rather than a cause of grasslands degradation. Maybe overgrazing weakens the plant cover, even leading to the eradication of some plants and making the land more prone to bare patch formation. With a reduction in the concentration of suitable plants for food23, it seems that these small animals have increased their intensity of burrowing24 and also the area of burrowing activity in order to obtain sufficient food. These activities of the small animals facilitated the spread of A. inebrians, which can reach a height of 60–150 cm that is close to the height of livestock and produce about 700 small easily-shed seeds from each compact inflorescence9. The seed also has long awns that can adhere to livestock which may aid dispersal.
Achnatherum inebrians plants alone will not provide a stable ecosystem and this study has shown that within and between these large plants, members of the grasslands plant community also become established and have mature seeds. For a period of time after the onset of overgrazing there will remain a viable seed-bank in the soil and this may be the source of many of the new plants. However, continuous overgrazing will reduce the density and richness of forage seeds in soil25,26,27. Plants within and between the protective A. inebrians tussocks were shown in this study to produce more abundant seed compared with overgrazed areas. Some of the seeds may fall on the ground and so enrich the local seed-bank. In addition, some seed may move with the wind while other seed may be consumed by birds and thus get long distance dissemination28. These seeds will regenerate the broad-species seed-bank essential for maintaining a long-term stable ecosystem.
Arthropod diversity and abundance are also enhanced by the presence of A. inebrians. Part of the reason for the increased presence of arthropods is likely to be due to the open soil structure with high plant residues and organic matter content within A. inebrians protected pasture. In contrast, soil is generally very compacted in degraded pasture. In addition, the abundance of leaves will provide a food source for herbivorous arthropods29. Further, the high numbers of inflorescences provides pollen that is also a food source for some arthropods30 and so further increases arthropod biodiversity. The abundant arthropods and seeds will also become a food source of birds28,31.
The grasslands sites studied in the research ranged from a very dry area (Alxa) dominated by a C4 grass, to a wet area (Guinan) dominated by a sedge species. Achnatherum inebrians had become naturally established in this diverse range of habitats. This ability to colonise under such varied conditions makes this grass an effective agent for the regeneration of diverse degraded grasslands.
A further example of ecological impacts from another toxin-producing Epichloë species (E. coenophialia) that infects tall fescue (Lolium arundinaceum)32 has shown different effects on biodiversity. When endophyte-infected tall fescue was introduced to a pasture ecosystem by densely planting, the density and diversity of other plant species was reduced compared with tall fescue that is endophyte-free33. Endophyte-infected tall fescue also significantly reduced diversity of arthropods compared with endophyte-free plants34,35. However, one study suggested that there was no difference on effect on biodiversity between endophyte-infected and endophyte-free of tall fescue, but environmental condition played more important role36. Further research has also shown that compared with endophyte-free, endophyte-infected Achnatherum robustum and Festuca arizonica can increase biodiversity37,38,39 and endophyte-infected L. multiflorum strengthened interactions of resource-consumers40.
All of above studies compared different ecological roles between endophyte-infected and endophyte-free grass, but ignored the relationship between grass-endophyte symbiosis and livestock. A common practice to recover degenerated grassland is to use wire fences to prevent grazing livestock from exacerbating grassland degradation. However, wire fences also hindered the migration of wild animals41,42. In contrast, our research has demonstrated that A. inebrians can function as a natural fence which allows free movement of animals whilst naturally deterring grazing from damaging livestock. As such A. inebrians can be very helpful in the recovery of grassland.
In conclusion, A. inebrians can play a positive role in the stabilization and restoration of degenerated grasslands in northwest China. In addition, the effects of burrowing animals, implicated by many as a causal factor for grasslands degradation6, may in fact be beneficial in the restoration of pastures by providing suitable bare land for A. inebrians to establish.
Methods
Site descriptions
We conducted this study at three grasslands in northwest China that have been overgrazed by livestock in recent decades and where Achnatherum inebrians plants have become increasingly more abundant. Xiahe county of Gansu province (35°07′ N, 102° 26′ E), Guinan county of Qinghai province (35° 28′ N, 101° 16′E) and Alxa Left Banner county, Inner Mongolia (38° 39′ N, 105° 46′E). In Xiahe, the dominant grass is Elymus nutans; Guinan, a wetland dominated by Kobresia capillifolia; Alxa, an arid grassland where Pennisetum centrasiaticum, a C4 grass, is the dominant species. Details of the three sites, including temperature and precipitation data, were presented in Supplementary Table S 1.
Experimental designs
The entire study was performed in 2013, with the field assessments carried out between August 22nd and September 21st. Achnatherum inebrians plants in all locations were assessed and determined to be endophyte infected using the method of Bacon et al.32.
Impact of A. inebrians on seed status of other plant species
In order to determine the effects of A. inebrians on other plant species in the three sites, we employed two treatments in overgrazed grassland of each site: one area with tussocks of A. inebrians in the quadrats (5 m ×5 m), termed tussock area (hereafter TA) and the other one without A. inebrians, termed non-A. inebrians area (hereafter NA) that was still covered by short vegetation and each treatment had four replications. The seed status of plants in each quadrat was recorded. We only investigated plants that had mature seeds. The inflorescence number for Poaceae and Cyperaceae species, because of relatively uniform inflorescences and the plant number of plant species in other families with seeds were counted by visual observation in every quadrat in situ. Difference of vegetation between TA and NA can be seen in Fig. 2a.
The protection on other plant species from Achnatherum inebrians and its spread.
(a) Compared with those plant species that almost had no seeds and grew with low height in overgrazed grassland area, forage grasses and other plant species are abundant and have many inflorescences with mature seeds within tussocks of A. inebrians in Xiahe. (b) Achnatherum inebrians could easily establish in molehills that produced by zokor and widely distributed in overgrazed grassland in Xiahe. (c) Small A. inebrians plant established in a bare patch nearby a pika hole in overgrazed grassland in Guinan. (d) Many one-year old A. inebrians plants that had established in bare patches produced by pika in Guinan.
Impact of A. inebrians on arthropods
In each overgrazed grassland in Xiahe, Guinan and Alxa, 30 soil blocks (0.4 m in diameter and 0.2 m in depth, 15 each for the TA and NA quadrats) were randomly dug out and crumbled. All arthropods except for ants in one block were put in one collection bottle. The arthropod collections were brought to the laboratory and then the specimens were identified to the family level and counted.
Contribution of zokor and pika to the spread of A. inebrians
A seed establishment experiment was conducted in grassland in Xiahe. Seeds of A. inebrians collected from Xiahe grassland in September 2012 were used in this study. Fifteen blocks were randomized in the overgrazed grassland, with each block having two small circular plots approximately 15 cm in diameter. One plot was on a zokor molehill and the other one was in adjacent overgrazed area (NA) that was still covered by short vegetation. These small plots were away from each other by at least 1 m. The sowing time was in April 2013 and in each plot 100 seeds were sown. The establishment rate of A. inebrians in each of the small plots was assessed in September 2013. Given the presence of A. inebrians in previously bare area produced by pikas, the ability of A. inebrians naturally colonising in these bare patches was investigated. This study was conducted in the grassland trial site of Guinan county. Only those A. inebrians plants that had established within the past year (less than one-year old plants), were investigated in this study to calculate the increase of plant number of A. inebrians in one year. Some areas covered by A. inebrians were randomly selected to compare the establishment ability of A. inebrians in bare patches and overgrazed grassland areas (NA) that were still covered by short vegetation. Those areas containing A. inebrians were not only close to bare patches but also close to NA areas. For each treatment, four quadrats (10 m ×10 m) were randomly selected in the overgrazed grassland. Calculation of the mean number of one-year old A. inebrians plants per m2 was carried out in every quadrat. The establishment ability of A. inebrians was compared by the mean number per m2 in the two treatments. The difference in establishment between bare land (molehill and patch) and NA can be seen in Fig. 2b–d.
Data analysis
Data analysis was performed with SPSS 17.0 for Windows (USA). A nonparametric, Mann-Whitney U test was used to test: 1) the impact of A. inebrians on seed status of different plants species in two treatments; 2) the impact of A. inebrians on number of different arthropods in two treatments. Independent samples T-test was used to test: 3) the establishment rates of A. inebrians in molehill produced by zokor and NA; 4) the number of one-year old A. inebrians per m2 in bare patch produced by pika and NA.
Additional Information
How to cite this article: Yao, X. et al. A toxic endophyte-infected grass helps reverse degradation and loss of biodiversity of over-grazed grasslands in northwest China. Sci. Rep. 5, 18527; doi: 10.1038/srep18527 (2015).
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Acknowledgements
We thank professors W. G. Zhang and S. Q. Shang for identification of plants and arthropods; K. Takahashi, Richard Johnson, B. Skipp, D. Hume, S. Card, A. Popay and A Stewart for valuable comments for the preparation of this manuscript; M. L. Song, J. X. Cao and C. H. Guo for help. This work was supported by the National Basic Research Program of China (2014CB138702) and Program for Changjiang Scholars and Innovative Research Team in University (IRT13019).
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X.Y., C.J.L. and Z.B.N. designed the experiments. X.Y., G.S.B. and X.Z.L. performed the experiment. X.Y., M.J.C. and C.P.Z. analysed the data and wrote the paper.
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Yao, X., Christensen, M., Bao, G. et al. A toxic endophyte-infected grass helps reverse degradation and loss of biodiversity of over-grazed grasslands in northwest China. Sci Rep 5, 18527 (2015). https://doi.org/10.1038/srep18527
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DOI: https://doi.org/10.1038/srep18527
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