Trade-offs in the adaptation strategy of two dominant rhizomatous grasses to sand burial in arid sand dunes

Abstract

Trade-offs have long been recognized as a crucial ecological strategy for plant species in response to environmental stresses and disturbances. However, it remains unclear whether trade-offs exist among different structures (or functions) of clonal plants in response to aeolian activities in sandy environments. We examined the growth (reproductive vs. vegetative), reproduction (sexual vs. asexual), and bud bank (tiller buds and rhizome buds, representing vertical and horizontal growth potential) characteristics of two dominant rhizomatous grasses (Psammochloa villosa and Phragmites australis) in the arid sand dunes of northwestern China. Our results showed that these two rhizomatous clonal species exhibited significant trade-offs in their adaptation strategies in response to changes in sand burial depth. Specifically, as sand burial depth increased, the clonal species tended to reduce their reproductive growth, sexual reproductive capacity, and horizontal growth potential, as evidenced by reductions in reproductive ramet number and proportion, panicles number, biomass, and their proportions, as well as rhizome bud number, biomass, and their proportions. Conversely, they increased vegetative growth, reproduction, and vertical growth potential, as evidenced by enhancements in vegetative ramet number and proportion, belowground bud number, biomass, and their proportions, and in tiller bud number, biomass, and their proportions. Our study underscores the importance of trade-offs in the adaptation strategies of rhizomatous clonal species in sandy environments where drought stress and aeolian disturbance coexist. Those trade-offs could ensure the population persistence and stability of pioneering psammophytes in sand dunes, which should be considered during sand-fixing and vegetation restoration efforts in arid sand dunes.

摘要

干旱沙区两种优势根茎型禾草对沙埋的适应性权衡策略

长期以来，权衡被认为是植物种响应环境胁迫与干扰的重要生态策略。然而，尚不清楚沙生环境中克隆植物响应风沙干扰不同结构(或功能)间是否存在潜在的权衡关系。为此，本研究以中国西北干旱沙区(乌兰布和沙漠)两种优势根茎型禾草[沙鞭(Psammochloa villosa)和芦苇(Phragmites australis)]为研究对象，调查其生长格局(生殖生长与营养生长)、繁殖策略(有性繁殖与无性繁殖)与芽库组成(分蘖芽与根茎芽，分别表征垂直和水平生长潜力)情况。结果表明，两种根茎型克隆植物在其对不同沙埋深度的适应策略中表现出显著的权衡关系。具体而言，随沙埋深度增加，克隆植物倾向于减少其生殖生长、有性繁殖和水平生长潜力，表现为生殖分株数量及其比例、穗数量、生物量及其比例以及根茎芽数量、生物量及其比例显著降低；相反，克隆植物增加其营养生长、营养繁殖和垂直生长潜力，表现为营养生长分株数量及其比例、地下芽数量、生物量及其比例以及分蘖芽数量、生物量及其比例显著增加。上述结果强调了权衡策略在根茎型克隆植物适应干旱胁迫与风沙干扰并存的沙生环境中的重要性。这些权衡策略确保了先锋沙生植物的种群持久性及其稳定性，在干旱沙区流沙固定与植被恢复中应予以足够重视。

Graphical Abstract

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INTRODUCTION

Competitor, stress-tolerator, ruderal (CSR) theory proposes that plant species tend to adjust their growth traits to adapt to environmental stresses and modify their reproduction patterns to respond to disturbances (Grime 1977; Pan and Price 2002; Stearns 1989). Trade-offs exist among different structures and/or functions in plant species, ensuring individual survival, fitness, and population persistence under environmental stress and disturbance (Bell and Koufopanou 1986). For example, in sand dune ecosystems, strong and frequent aeolian activities as well as environmental stresses (e.g. drought and nutrient-poor) seriously threaten individual growth and population regeneration (Zhang et al. 2002). To adapt to sandy environment, plant species need to optimize the allocation of limited resources, ensuring the maintenance and regeneration of their populations (Funk and Cornwell 2013). Although adaptation strategies of plants to sandy environment have been well documented, such as physiological process, morphological plasticity and population growth pattern (Gutterman 2000; Moles and Westoby 2006; Sun et al. 2023), the potential trade-offs in adaptation strategies of plant species to sandy environment have rarely been explored.

Due to the adaptive advantages of physiological integration, lateral spread and foraging behaviors, clonal species often dominate stressful and frequently disturbed ecosystems (Gross et al. 2017; Yu et al. 2004; Zhang and Zhang 2007). Previous studies suggested that clonal species could adjust their growth allocation (vegetative vs. reproductive), reproduction (sexual vs. asexual), and clonal growth pattern (phalanx vs. guerilla) in response to environmental changes and disturbances (Brzyski et al. 2014). For instance, the biomass allocation for reproductive growth of Hedysarum laeve significantly increased with increasing soil moisture, but that for vegetative growth decreased (Zhang et al. 2002). A shift in reproduction mode occurred in Caragana stenophylla from sexual reproduction in semi-arid areas to asexual reproduction in extremely arid areas. With the inter-specific competition, Lolium perenne reduces resource inputs for leaf production to attenuate vertical growth but increases resource inputs for rhizome growth to enhance horizontal expansion (Cheplick and Gutierrez 2000; Perkins and Owens 2003; Wang et al. 2018). Accordingly, in sand dune ecosystems where water stress and aeolian disturbance coexist, clonal plants necessarily have evolved trade-offs to cope with the sandy environment (Harris and Davy 1986; Li et al. 2005; Moles and Westoby 2006).

In sand dune ecosystems, sand burial and wind erosion are the two main types of disturbances that affect individual growth, population maintenance and regeneration as well as community composition and dynamics (Maun and Lapierre 1986). Aeolian activities often change sand burial depth, and modify soil environment (Acosta-Martínez et al. 2015). Therefore, sand burial depth is an important environmental factor that affects plant growth and reproduction (Luo and Zhao 2015). Clonal plants often proceed vegetative and reproductive growth simultaneously, and the limited photosynthate needs to be optimally allocated between vegetative and reproductive growth, resulting in a trade-off between these two growth modes (Gross et al. 2017; Xu et al. 2013). Under long-term environmental stress of sand burial and wind erosion, plants tend to allocate more resources to reproductive growth and less to vegetative growth (Poorter et al. 2012). By this means, plants could produce more seeds, enabling offspring to escape from unfavorable habitats by long-distance seed dispersal (Harris and Davy 1986). In contrast, under relatively favorable conditions, plants tend to enhance their vegetative growth to gain local competitive advantages (Li et al. 2005; Liu et al. 2009; Poorter et al. 2012). For the shrub species Nitraria tangutorum in arid sand dunes, with the increase of precipitation, its vegetative growth (i.e. vegetative branch biomass) gradually increased while reproductive growth (i.e. reproductive branch biomass) decreased (He et al. 2016). While both vegetative and reproductive growth are enhanced in fertile habitats, plant species still tend to allocate more resources to vegetative growth to strengthen competitiveness (Li et al. 2012). Thus, clonal plants in arid sand dunes might trade off vegetative and reproductive growth to ensure their fitness in response to sandy environment. However, this potential trade-off has not been verified yet.

Clonal species generally adopt sexual (by seeds) and asexual (by buds) reproduction for population maintenance and regeneration, and these two reproductive modes have their specific strengths and weaknesses (Klimešová and Klimeš 2007). Sexual reproduction has been considered as the prerequisite for the adaptive evolution of plants since it could produce genetically variable offspring (Benson and Hartnett 2006). However, sexual reproduction is resource costly and requires relatively favourable conditions for seed germination and seedling establishment. Thus, the sexual reproduction of clonal species, often contribute little to population regeneration and vegetation restoration in sand dunes with harsh environmental conditions (Wang et al. 2018). In contrast, clonal species often dominate in sand dunes with harsh environments, largely relying on asexual reproduction via belowground bud bank. Furthermore, their offspring ramets could be supported by mother shoots by physiological integration, which ensures the survival of offsprings and population regeneration in response to water stress and aeolian disturbance (Ma et al. 2019; Wu et al. 2020, 2021). Nevertheless, clonal plants do not completely abandon sexual reproduction due to its evolutionary and adaptive advantages (Schulze et al. 2012; Wilk et al. 2009). Instead, most clonal species retain the two reproduction modes, and the relative importance and contribution of these two modes to population regeneration greatly depend on environmental conditions (Verhoeven and Biere 2013). Clonal plant species might trade-off their sexual and asexual reproduction in changing environments (Brzyski et al. 2014; Wilk et al. 2009). However, the potential trade-off between sexual and asexual reproduction in clonal plants in response to sandy environment has been rarely studied.

Clonal plants could adjust their growth patterns to adapt to environmental changes and disturbances (Heggenstaller et al. 2009). In sand dunes, belowground bud bank is not only the basis of population regeneration, but its composition (different bud types) also determines clonal growth form (Dong et al. 2023; Maun et al. 1996; Wu et al. 2020). Different bud types represent different adaptation strategies and play diverse roles in clonal growth pattern, population regeneration and colonization (Fang et al. 2024; Liu et al. 2012; Ye et al. 2006). Specifically, tiller buds at shoot bases represent the vertical growth potential, whereas rhizome buds on rhizome systems reflect the lateral growth potential and population expansion ability (Klimešová et al. 2016). Clonal plants often adjust the relative proportion of tiller buds and rhizome buds in response to environment changes, which determines whether clonal growth pattern is phalanx or guerrilla (Ding et al. 2021; Ma et al. 2019; Wu et al. 2020). Clonal plants in suitable habitats often produce more tiller buds and proceed phalanx growth to consolidate their dominance in competitive environment (Chen et al. 2011; Oborny 1994). In contrast, clonal plants in resource-poor habitats often increase their rhizome buds and resort to guerrilla growth (Liu et al. 2014). By increasing the number of rhizome buds, plants increase their horizontal expansion potential to rapidly escape from unfavorable habitats and search for resources in a larger spatial area (Dong et al. 2023; Oborny 1994). It is essential to reveal the responses of belowground bud bank composition to sandy environment to test the potential trade-off between vertical and horizontal growth and predict clonal growth pattern in sand dunes.

Therefore, in this study we selected two dominant rhizomatous clonal species (Psammochloa villosa and Phragmites australis) in the arid sand dunes of northwestern China, and investigated the number and biomass of reproductive and vegetative ramets, buds (the potential of asexual reproduction) and panicles (the potential of sexual reproduction), rhizome buds (horizontal growth potential) and tiller buds (vertical growth potential) under different sand burial depths. We hypothesize that some key trade-offs exist in the adaptation strategy of clonal plants to sandy environment. Specifically, we hypothesize that: (i) With increasing sand burial depth, rhizomatous clonal plants proceed more vegetative growth than reproductive growth. (ii) Under severe sand burial, rhizomatous clonal plants rely more on vegetative reproduction by belowground bud bank for population regeneration, and increase the horizontal growth potential by increasing rhizome buds in their bud bank.

MATERIALS AND METHODS

Study site

This study was conducted at the Desert Ecosystem National Observation Research Station, Chinese Academy of Forestry, Dengkou, Inner Mongolia, China (40°09ʹ–40°57ʹ N, 106°9ʹ-107°10ʹ E). This region belongs to the temperate continental monsoon climate, with the mean annual temperature 7.4 °C, and the mean annual precipitation 114 mm, which mainly occurs from June to September. The mean annual potential evaporation is 2372.1 mm, about 20.8 times of the precipitation. This region belongs to the transition zone between desert and semi-desert in northwestern China. The geomorphology is mainly composed of mobile dunes, semi-mobile dunes and flat sandy land, and soil types mainly consist of aeolian sandy and gray-brown desert soils. The vegetation coverage is low, which is mainly dominated by psammophyte and xerophyte as well as planted sand-fixing forests (e.g. Haloxylon ammodendron), the dominant shrub and herb species are Psammochloa villosa, Phragmites australis, Artemisia ordosica, Nitraria tangutorum and Artemisia xerophytica. Specifically, Psammochloa villosa and Phragmites australis are perennial rhizomatous grasses, capable of both asexual reproduction through buds and sexual reproduction via seeds. In contrast, Artemisia ordosica and A. xerophytica belong to perennial forbs, primarily engaging in sexual reproduction through seeds but also capable of asexual reproduction via adventitious roots. Additionally, Nitraria tangutorum is a perennial shrub that exhibits versatility in reproduction, undergoing both sexual reproduction with seeds and asexual reproduction utilizing adventitious roots.

Study species

Psammochloa villosa and Phragmites australis are perennial rhizomatous grasses that are dominant in arid sandy areas. As typical xerophytic and pioneering psammophyte, they have strong adaptability to sandy environment. Both species can reproduce sexually via seeds, which can be dispersed by wind over long distances. Meanwhile, their rhizomes can grow horizontally in sands, with the buds on shoot bases and rhizomes sprouting into offspring ramets under favourable conditions. These two rhizomatous grasses have been often used as target species for sand fixation and vegetation restoration because they have strong lateral colonization ability and can form multi-layered rhizome networks (Chen et al. 1996a, 1996b).

Field investigation and sampling

During the growing season (June-September) in 2022, six plots (20 m × 20 m) were randomly established in the mobile and semi-mobile sand dunes since the two target species Phragmites australis and Psammochloa villosa mainly dominate in mobile and semi-mobile sand dunes respectively in the study region. In each plot, the soil was carefully dissected with a spade to locate the apical bud of rhizomes, and then the rhizomes and ramets were dug from the apical buds along the rhizome until the rhizome was cut off where there were no ramets on the rhizome. Because rhizomatous grasses can be physiologically integrated through rhizomes, we measured sand burial depths at the anterior, middle and posterior ends of rhizomes and used their average values as the sand burial depths of the whole clonal fragment. At our study site, the sand burial depths of P. villosa and P. australis were in the range of 10 to 70 cm and 20 to 80 cm, respectively. Accordingly, we classified three degrees of sand burial: mild, moderate and severe sand burial (P. villosa: 10–30 cm, 30–50 cm, 50–70 cm; P. australis: 20-40 cm, 40–60 cm, 60–80 cm). For each sand burial depth, we dug out at least six clonal fragments with similar sizes. For each clonal fragment, we separated the reproductive ramets, vegetative ramets, rhizome buds, tiller buds and panicles, counted their numbers, and put them into marked envelopes. We put the envelopes into the drying oven at the 105 °C temperature for 30 min, and then at 65 °C for 48 h. Afterwards, we weighed the biomass of reproductive ramets, vegetative ramets, panicles, rhizome buds, and tiller buds.

Statistical analysis

Prior to data analysis, data were converted to the number and biomass of each organ (reproductive ramets, vegetative ramets, rhizome buds, tiller buds, and panicles) per unit of rhizome length (m). Data were first tested for normal distribution and homogeneity of variances, and the data met the prerequisites for ANOVA (normally distributed and passed the Chi-square test). One-way ANOVA was then used to compare the differences in the number, biomass and proportion of each organ at different sand burial depths. Tukey method was used for subsequent multiple comparisons. All statistical analyses of data were completed using SPSS 20.0 and plots were completed using Origin 2019.

RESULTS

Effect of sand burial on reproductive and vegetative growth

The growth pattern (reproductive vs. vegetative) of the two studied rhizomatous grasses in response to changing sand burial depth was similar. Specifically, for these two clonal grasses, the number of reproductive ramets significantly decreased (P < 0.05) while those of vegetative ramets remained unchanged. However, the biomass of both reproductive and vegetative ramets significantly increased with the increasing sand burial depth (P < 0.05, Table 1). More importantly, the proportions of reproductive- and vegetative ramets (both for the number and biomass of ramets) showed contrary responses to sand burial. For the two studied species, the number ratio (percentage) of reproductive ramets under mild sand burial was significantly higher than those under moderate and severe sand burial (P < 0.05), while the number ratio of vegetative ramets showed an opposite trend (Fig. 1a and b). As regard with the biomass ratio (percentage) of the two types of ramets, for Psammochloa villosa, the biomass ratio of reproductive ramets under mild (10–30 cm) and moderate (30–50 cm) sand burial were significantly lower than that under severe (50–70 cm) sand burial, while the biomass ratio of vegetative ramets under mild and moderate sand burial were significantly higher than that under severe sand burial (P < 0.05, Fig. 1c). Meanwhile, for Phragmites australis, the biomass ratio of reproductive ramets under mild (20–40 cm) sand burial was significantly lower those under moderate (40–60 cm) and severe (60–80 cm) sand burial, but the biomass ratio of vegetative ramets under mild sand burial was significantly higher than those under moderate and severe sand burial (P < 0.05, Fig. 1d).

Effect of sand burial on sexual and asexual reproduction potential

For the two rhizomatous grasses, the sexual and asexual reproduction potential, which were represented by the number and biomass of panicles and buds respectively, showed opposite trends in response to the increasing sand burial depth. Specifically, in P. villosa, the number and biomass of buds increased significantly while those of panicles decreased significantly with the increasing sand burial depth (P < 0.05). In P. australis, the bud number under mild sand burial was significantly lower than that under severe sand burial while the panicle number under mild sand burial was significantly higher than those under moderate and severe sand burial (P < 0.05). Meanwhile, the biomass of buds significantly increased but that of panicles decreased from mild to moderate and then to severe sand burial (P < 0.05, Table 2). Besides, results further showed for the two rhizomatous species the number ratio and biomass ratio of buds significantly increased while those of panicles significantly decreased from mild to severe sand burial (P < 0.05, Fig. 2).

Effect of sand burial depth on belowground bud bank composition

As regard with the belowground bud bank composition, the number and biomass of tiller buds increased significantly with the increasing sand burial depth in two rhizomatous species (P < 0.05). But they showed different response of rhizome buds to sand burial. In P. villosa, the number and biomass of rhizome buds were significantly lower under mild sand burial than under moderate and sever sand burial (P < 0.05), while in P. australis, both the number and biomass of rhizome buds were not significantly changed with sand burial depth (Table 3). It is notable that both number ratio and biomass ratio of rhizome buds and tiller buds showed contrasting responses to sand burial. For P. villosa, the number ratio and biomass ratios of rhizome buds under mild sand burial were significantly higher than those under severe sand burial, while those of tiller buds were significantly lower under mild sand burial than severe sand burial (P < 0.05, Fig. 3a, c). Similarly for P. australis, both the number ratio and biomass ratio of rhizome buds significantly decreased while those of tiller buds significantly increased with the increasing sand burial depth (P < 0.05, Fig. 3b, d).

DISCUSSION

Trade-off between reproductive and vegetative growth

Rhizomatous grasses could regulate their growth patterns and adjust the resource allocation towards organs that are most conductive to plant survival and reproduction to adapt to sandy environment (Creagar et al. 2023; Gross et al. 2017). In this study, we found that while the number of vegetative ramets remained unchanged with increasing sand burial depth, the number of reproductive ramets gradually decreased. Furthermore, the biomass of both reproductive and vegetative ramets increased with sand burial depth. Rhizomatous grasses tend to produce more and smaller ramets under mild sand burial but produce fewer and larger ramets under severe sand burial, which to some extent verifies the trade-off between ramet size and number in rhizomatous grasses in sand dunes (Ba et al. 2024).

We found contrasting responses of reproductive and vegetative growth (especially for the number of reproductive and vegetative ramets and their proportions) in response to sand burial. Rhizomatous grasses tend to adopt reproductive growth under mild sand burial but vegetative growth under severe sand burial. This might be attributed to changes in environmental factors with sand burial depth that affect plant growth and reproduction. In arid sand dunes, soil moisture generally increased with sand burial depth (Yao and Zhao 2021). Under mild sand burial, plant species face severe water stress and the risk of uprooting by wind erosion, and thus tend to allocate more resources to reproductive growth to enhance seed production and help offspring escape from unfavorable habitats with long-distance seed dispersal (Creagar et al. 2023; Silvertown 2008). Under severe sand burial, biomass of both reproductive and vegetative ramets increased, which was perhaps owing to higher soil moisture. Meanwhile, as sand burial depth increases, the resource cost for reproductive growth increases because deep sand burial forms physical barriers that prevent plants from growing up to soil surface, flowering and producing seeds (Gilbert et al. 2008; Luo and Zhao 2015). Under the circumstances, it is advantageous for plant species to shift their growth patterns towards vegetative growth.

We also observed that as sand burial depth increased, the number and biomass ratio of reproductive ramets of rhizomatous grasses gradually decreased whereas the response of vegetative ramets exhibited an opposite trend. Previous studies have confirmed that in suitable habitats, plant species tend to reduce their resource allocation to reproductive growth to produce seeds for escaping the habitat, but invest more resources to vegetative growth to enhance their local competition advantages (Luo and Zhao 2015; Wang et al. 2018). Our results showed that rhizomatous grasses tend to rely more on reproductive growth under mild sand burial but turn to vegetative growth under severe sand burial conditions, providing the compelling evidence of trade-off between reproductive and vegetative growth in response to sand burial depth.

Trade-off between sexual and asexual reproduction potential

Environmental changes could alter the relationship between sexual and asexual reproduction and their relative importance/contributions regarding population maintenance and regeneration in clonal plants (Mitchell et al. 2014; Yang and Kim 2016). In this study, we employed the number and biomass of panicles and buds to represent sexual and asexual reproduction potential, respectively. We found that with increasing sand burial depth, the studied indices (number, biomass, and ratios) of panicles significantly decreased while those of buds increased. It means that rhizomatous grasses tend to more rely on sexual reproduction under mild sand burial while more rely on asexual reproduction under severe sand burial for population maintenance and regeneration, showing a trade-off between these two reproduction modes.

Sexual reproduction by seeds and asexual reproduction by buds have their specific strengths and weaknesses (Klimešová and Klimeš 2007; Ott et al. 2019). The choice of these two reproduction modes for clonal species greatly depends on environmental conditions (Yang and Kim 2016). Under mild sand burial, seeds are often buried in the shallow sand profile, which is beneficial for seed germination and seedling emergence (Tao et al. 2022). Yet the stronger water stress and wind erosion under mild sand burial conditions might result in low seed availability and failed seedling survival and establishment (Kolář et al. 2017; Zhu et al. 2014), thus plant species tend to allocate more to sexual reproduction processes (increased number and biomass of panicles) to produce more seeds which can be dispersed afar to favourable habitats. In contrast, severe sand burial often make seeds being deeply buried and form persistent soil seed bank, making seeds in deep sand profile difficult for them to germinate (Liu et al. 2014; Wang et al. 2017; Zhu et al. 2009), which only contribute to population regeneration when they are brought to the shallow sand layer by wind erosion (Qian et al. 2016). Just for this reason, clonal species tend to reduce their sexual reproduction potential but turn to asexual reproduction by virtue of belowground bud bank under severe sand burial. The importance of vegetative reproduction by means of rhizome system and the role of belowground bud bank in response to environmental stress and disturbance in sand dunes have been well documented (Ma et al. 2019; Wu et al. 2021). Under severe sand burial, rhizomatous grasses expand horizontally by means of their extensive rhizome systems, and the buds bearing on shoot bases and rhizomes will sprout into ramets and contribute to population regeneration when they are buried at proper depths and environmental conditions are favourable (Liu et al. 2014). We also observed the three-dimensional reticular structure of rhizome system (especially for Phragmites australis) that rhizomes are buried at various depths, meticulously probing for optimal burial depth for bud sprouting. This further highlight the importance of asexual reproduction of rhizomatous grasses under severe sand burial. Therefore, our study demonstrates the shift between sexual and asexual reproduction with sand burial depth and the trade-off between these two reproduction modes. However, one should be aware of that there might exist a threshold in sand burial depth for the shift between two reproduction modes and the threshold might species-specific, which all need to be further studied.

Trade-off between vertical and horizontal growth potential

Rhizomatous grasses need to adjust their growth patterns to adapt to environmental stress and aeolian disturbance in sand dunes (Liu et al. 2012). As the basis of clonal growth and reproduction, the responses of belowground bud bank composition to sand burial largely determine the clonal growth pattern of rhizomatous grasses. A previous study showed that soil moisture rather than soil nutrient determines the belowground bud bank size and composition of rhizomatous grasses in arid sand dunes (Dong et al. 2023). Rhizomatous grasses possess two types of buds: tiller buds at shoot bases and rhizome buds on belowground rhizomes, representing the potential of vertical and horizontal growth, respectively. We found that the number and biomass of tiller buds are significantly higher under severe sand burial, but those of rhizome buds increased under mild sand burial. It implies that rhizomatous grasses tend to produce more tiller buds for potential vertical growth to adapt to severe sand burial. In mild sand burial habitats, rhizomatous grasses produce more rhizome buds for lateral expansion to forage more resources in larger spatial scales due to the strong water stress in shallow sand profiles. In other words, more rhizome buds under mild sand burial guarantee the formation and maintenance of extensive rhizome systems, which perform the physiological integration function of distributing resources between ramets, and enhancing the survival and persistence of rhizomatous grasses in harsh sandy environment. Therefore, our study provides concrete evidence for the trade-off between vertical and horizontal growth potential in rhizomatous grasses in response to sand burial.

Many studies have documented the changes in belowground bud bank composition in responses to sandy environment. In semi-arid sand dunes of Horqin sandy land, plants tend to produce more tiller buds in severe sand burial habitats (i.e. the leeward slope of sand dunes), while rhizome buds are more sensitive to water stress since they were significantly positive correlated with soil water content in sand dunes (Ma et al. 2019), which is consistent with our findings that tiller buds significantly increased under severe sand burial and rhizome buds increased under mild sand burial. The resource cost of vegetative growth/reproduction might also help explain the contrasting trends of tiller buds and rhizome buds with sand burial, i.e. under severe sand burial, rhizome buds engaged in horizontal colonization need to overcome soil compaction and consume large amount of energy, while the cost of vertically growing tiller buds is relatively small (Gilbert et al. 2008; Luo and Zhao 2015). Thus, the clonal growth direction of the two rhizomatous grasses shifts from horizontal growth to vertical growth under severe sand burial conditions. A previous study also found a trade-off between the vertical and horizontal growth of P. australis in semi-arid sand dunes. This rhizomatous grass tends to produce more vertical ramets under severe sand burial while produce more rhizome-originated ramets under mild sand burial (Liu et al. 2014), and a key threshold sand burial depth (40 cm depth) exists for the alternation between the two growth directions. Although our findings fall short of comprehensively elucidating the ultimate outcome of vegetative reproduction among rhizomatous grasses in sandy habitats, owing to its intricate interplay during bud sprouting and ramet development, our research still demonstrates a pivotal trade-off between the potential for vertical and horizontal growth strategies.

CONCLUSIONS

Our study indicates that as sand burial depth increased, these rhizomatous clonal species tended to augment their vegetative growth, adopt asexual reproduction via belowground bud banks, and enhance vertical growth potential. This study contributes to our understanding of clonal species’ adaptation strategies to harsh sandy environments and provides a crucial foundation for vegetation restoration in sand dunes. For effective implementation of vegetation restoration measures in severely sand-buried habitats, rhizomatous clonal grasses with robust vegetative growth ability, powerful asexual reproduction, and enhanced vertical growth potential should be selected.

Funding

This research was supported by the National Natural Science Foundation of China (41877542) and the Key Scientific and Technological Project of Henan Province (232102320245).

Acknowledgements

We thank Chaoqun Ba and Shanshan Zhai for their assistance during the field investigation and sampling. We are very grateful for the field assistance of colleagues at the Inner Mongolia Dengkou Desert Ecosystem National Observation Research Station. We are also very grateful for the valuable comments from the editor and two anonymous reviewers, which help us to improve our manuscript greatly.

Conflict of interest statement. The authors declare that they have no conflict of interest.

REFERENCES

Author notes