Shift in nurse effect from facilitation to competition with increasing size of Salix cupularis canopy in a desertified alpine meadow on the Tibetan Plateau
Introduction
The Tibetan Plateau is regarded as one of the most ecologically important and sensitive regions worldwide (Qiu, 2008). In recent years, however, as a consequence of climate change and human activities, the degradation of alpine meadows in this region has become a widespread problem (Sun et al., 2019, Sun et al., 2018a, Sun and Wang, 2016). The Zoige basin, which is located on the eastern edge of the Tibetan Plateau, covers the largest area of peat marshes in China and is the largest area of alpine swamp worldwide (Shuang et al., 2009). Nevertheless, this region has been experiencing severe desertification in recent decades, and its grassland area has shrunk by more than 30%, which has altered ecosystem functioning and processes (Sun et al., 2018b, Wang et al., 2019a). In response to this increasing desertification, the Chinese government has adopted a number of remedial measures on the Tibetan Plateau, including the planting Salix cupularis as wind-breaks and to promote the stabilization of sand, with the aim of eventually restoring the degraded grassland. During such restoration processes, so-called ‘nurse plants’ can be used to promote vegetation succession. Consistent with the stress-gradient hypothesis, the use of nurse plants as a recovery measure is currently attracting wide attention, although simultaneously provoking heated debate (Sun et al., 2013, Wang et al., 2019b, Wu et al., 2009).
According to the interspecific relationship theory, the stress-gradient hypothesis (Bertness and Callaway, 1994) describes the outcome of interactions between different plant species along environmental gradients (Maestre et al., 2003, Stachowicz, 2001). It proposes that interspecific competition is particularly prevalent in fertile environments, notably when there are facilitative changes during periods of increasing environmental stress and disturbance, such as when there are reductions in nutrient or water availability (Brooker and Callaghan, 1998, He et al., 2013). In general, when plants enhance the establishment, growth, and survival of other plants, their interactions with the other plants can be beneficial (Bonanomi et al., 2011). The stress-gradient hypothesis maintains that plant community dynamics and ecosystem processes are widely regulated via the effects of nurse plants (Armas et al., 2004, Bruno et al., 2003, Goldberg and Barton, 1992). These plants are species that provide benefits to other plants or plant communities (Brooker et al., 2007, Filazzola and Lortie, 2014, Padilla and Pugnaire, 2006) and are typically found among perennial species such as shrubs, trees, and cushion plants (Cavieres et al., 2005, Ren et al., 2008). Nurse plants facilitate the growth of target plant species beneath their canopy and offer a favourable microhabitat (e.g. temperature buffering, protection against herbivores, and seed and particle traps) (Bruno et al., 2003, Cavieres et al., 2006, Padilla and Pugnaire, 2006; Fig. 1a). The findings of numerous studies have indicated that nurse plants indirectly affect the fitness or productivity of plants under their canopy through intermediary species (Barbosa et al., 2009, Michalet et al., 2014b). Additionally, some studies have demonstrated that the net interactions between nurse and target plants are dependent on the modification and amelioration of abiotic factors at different functional levels in different regions (Bertness and Callaway, 1994, He et al., 2013, Smit et al., 2006). At the population level, herbaceous plants generally have negative effects on their neighbours, whereas shrubs have positive effects (Gómez-Aparicio, 2009). At the community level, nurse plants can facilitate the development of a community structure, alter the spatial dynamics of plant communities, and increase local diversity in response to complex stresses (Raffaele and Veblen, 1998, Soliveres et al., 2012). At the ecosystem level, nurse plants play a vital role in restoring the structure and functions of primary ecosystems and act a driving force in certain environments, particularly under extremely degraded conditions (Gomezaparicio et al., 2004, Liu et al., 2013, Ren et al., 2008).
Interestingly, some studies have identified a shift from competitive to facilitative interactions when comparing the centre and edge of nurse plant distributions, indicating that canopy dominant species can perform better in the presence of neighbours than when standing alone in edge microhabitats (Alnamazi et al., 2017, Michalet et al., 2014a). In addition, numerous studies focussing on seedling emergence (Dominguez et al., 2015, Foronda et al., 2019) have examined the utility of nurse plants in restoring desertified grasslands by monitoring the survival of target plants and changes in microenvironmental conditions (Gonzalez and Ghermandi, 2019). Nevertheless, the mechanisms whereby the interspecific relationships between shrubs and undergrowth vegetation change in response an increase in the canopy area of Salix cupularis remain unclear, although it is assumed that the resulting processes might affect traits of the target plants, soil properties, and microbial communities (Ren et al., 2008). As a plant native to the Tibetan Plateau, S. cupularis plays a vital role in the restoration of grasslands through artificial planting. In this regard, we hypothesized that concomitant with the growth of S. cupularis, particularly when the canopy area reaches a certain size, facilitative interactions will shift to competitive interactions. Accordingly, having developed a large canopy, S. cupularis may not be suitable for alpine meadow restoration (Fig. 1b). To test this hypothesis, we conducted experiments to investigate the various characteristics of grassland communities growing under nurse plants of different canopy sizes, as well as to examine the effects canopy size on soil physicochemical properties and microbial communities. We believe the findings of this study could provide theoretical guidance for the restoration of degraded grasslands.
Section snippets
Study site
The study site, which is dominated by alpine meadow, is located in the Zoige region (33°07′35″N, 102°37′40″E, 3500 m a.s.l.) (Fig. 2a) of Hongyuan County, in the eastern part of the Tibetan Plateau. The mean annual temperature of this region is 1.1 °C, and the coldest temperature reaches −36.2 °C. The mean annual precipitation is 747 mm, which falls primarily between the months of May to September. The climate type of the study area is a continental plateau cold temperate monsoon climate, with
Response of target plants to a canopy area gradient
We found that the importance value of Carex, Poa annua, and Artemisia nanschanica initially increased and then decreased, with maximal values of 0.31, 0.22, and 0.33 under NS2 canopies, respectively (Table 1). The aboveground biomass in NS1 plots was significantly lower than that recorded for vegetation under canopies of the other three size categories, among which, a maximum value of 20.3 g m−2 was recorded under the NS2 canopy (Fig. 3a). In contrast, we found that the belowground biomass
Discussion
Generally, it is a whole process for S. cupularis to have effects on the grassland ecosystem from the aboveground to the belowground. This can be illustrated by relationship between S. cupularis and the target plants Carex, Poa annua, and Artemisia nanschanica, which showed a shift from facilitation to competition under canopy areas of 3.8–5.5 m2. This shift was intimately linked with soil properties such as temperature, SOC, TN, and SCA, and we also found that bacterial community diversity
Conclusions
In the context of severe grassland desertification in the Tibetan Plateau, it is vitally important to examine the nurse effect of plants used for the restoration of grassland ecosystems. Our findings indicate that, with continued growth, the effects of nurse plants shift from facilitative to competitive, and that these latter effects play a dominant role at later stages in the restoration process, particularly when the area of the nurse plant canopy reaches a certain size. A notable observation
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgments
This research was supported by The State Key Research Development Program of China (Grant No. 2016YFC0501802 and 2016YFC0501803), the Second Tibetan Plateau Scientific Expedition and Research (Grant No.2019QZKK0405), and the National Natural Science Foundation of China (No. 41871040).
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This author contributed equally to this work.