Limited inorganic N niche partitioning by nine alpine plant species after long-term nitrogen addition

https://doi.org/10.1016/j.scitotenv.2020.137270Get rights and content

Highlights

  • Nine species were selected for in-situ 15N labeling to quantify ammonium and nitrate uptake.

  • Plants absorbed more ammonium and nitrate with N addition.

  • Plants' N uptake was influenced by habitat qualities, instead of the amount of N added.

  • Species coexistence may be promoted by minimizing their fitness differences through preferring the most abundant soil inorganic N form, instead of inorganic N niche partitioning.

Abstract

  • 1.

    Nitrogen (N) is a major nutrient limiting plant growth in most terrestrial ecosystems. Both niche partitioning and fitness equalizing mechanisms related to N acquisition have been proposed to explain the maintenance of biodiversity and ecosystem functioning. However, their relative importance remains controversial and unclear, especially in worldwide terrestrial ecosystems increasingly threatened by N deposition.

  • 2.

    We added NH4NO3 at four levels over 7 years in an alpine meadow on Qinghai-Tibetan Plateau to simulate the effects of N deposition. Nine species that all occurred along an N addition gradient were selected for in-situ 15N labeling experiment to quantify their uptake of ammonium verse nitrate.

  • 3.

    Plants absorbed more ammonium and nitrate with increased N addition. We found limited inorganic N niche partitioning along the N addition gradient. Instead, species tended to prefer the most abundant form of inorganic N in soil, i.e. ammonium. Of all possible linear mixed effects models constructed to explain variation in either ammonium or nitrate uptake, the most parsimonious one included soil available N. That means plant' N uptake is influenced by habitat qualities, instead of the amount of added N itself.

  • 4.

    Our findings suggest that inorganic N niche partitioning may play limited role in the maintenance of high diversity in this alpine meadow. Instead, species coexistence might be promoted by minimizing their fitness differences through preferring the most abundant form of inorganic N in the soil. This provides important insights into species coexistence under future N addition in Tibetan alpine meadows.

Introduction

Nitrogen (N) is a major nutrient limiting plant growth in most terrestrial ecosystems (Vitousek and Howarth, 1991; LeBauer and Treseder, 2008), and shapes a plant community composition and ecosystem functions (McKane et al., 2002; Silvertown, 2004; Houlton et al., 2007; Andersen and Turner, 2013). Plants can absorb various forms of N directly from soil solution, e.g. inorganic ammonium (NH4+) and nitrate (NO3), and organic N with low molecular weight (e.g. free amino acids) to meet their N demands (Jones et al., 2005; Näsholm et al., 2009). Although plants can take up organic N, inorganic N has been considered to be a major N source for most plants (Chapin, 1980; Marschner, 2011). Alpine meadows are wildly distributed over the world with high altitudes, especially on the Qinghai-Tibetan Plateau. N limitation is common due to slow mineralization of soil organic matter (SOM) caused by low temperature and water deficiency, although the soil stores a large amount of N (Zhou, 2001; Baumann et al., 2009; Zhang et al., 2012). However, such alpine meadows are rich in plant species, often with >30 species coexisting within a 0.5 × 0.5 m area (Liu et al., 2017). The conflict between this high diversity and limited N supply has attracted ecologist's interests for decades (McKane et al., 2002; Silvertown, 2004; Xu et al., 2011a; Song et al., 2015).

Chemical niche partitioning mechanism has been frequently invoked to explain how plants meet their N demands when competing with a number of plant species (McKane et al., 2002; Xu et al., 2011b; Song et al., 2015). In a given community, species utilizing N resources in a similar way may likely compete more intensively and lead to competitive exclusion. Thus, coexisting species might specify their strategies in using different chemical forms of N to reduce niche overlap and promote stable coexistence (McKane et al., 2002). Usually, the most abundant N form is occupied by the dominant species, leaving the nondominant ones with less dominant N forms (McKane et al., 2002; Ashton et al., 2010). Besides of such stabilizing mechanisms, a coexistence mechanism can also function by minimizing average fitness differences between species according to the modern coexistence theory (Chesson, 2000). In fact, some studies reported that plants meet N demands through preferences for a specific form of N, which largely depend on the most available N forms in their rhizosphere (Houlton et al., 2007; Mayor et al., 2014; Andersen et al., 2017). The preference for the most abundant N form in the soil could result in reduced inequalities in N uptake and average fitness and thus contribute to coexistence. That particular physiological traits (i.e. preference) was ascribed to habitat selection effect, and the preference pattern would be flexible when species' native habitat qualities change accordingly (e.g. ammonium/nitrate ratios) (Wang and Macko, 2011; Andersen and Turner, 2013). However, the relative importance of niche partitioning (stabilizing) and fitness equalizing with respect to N acquisition for species coexistence remain controversial and unclear, and few studies have addressed this issue in face of global change.

Worldwide terrestrial ecosystems are increasingly threatened by N enrichment through anthropogenic activities. Anthropogenic N addition (hereafter, N addition) through N deposition, and/or fertilization, can alleviate N limitation and thus lead to concomitant consequences for biodiversity and ecosystem functions (Chen et al., 2016; Niu et al., 2016; Midolo et al., 2018). It has been reported that N addition would stimulate plant N uptake (Lu et al., 2011; Niu et al., 2016), and show plasticity in N preference in response to the addition of different forms of N (Song et al., 2015). However, it remains unclear how N addition affects the N acquisition patterns in terrestrial ecosystems mediated by habitat qualities (e.g. available N in soil, microorganisms, and pH) (Niu et al., 2016). Apart from soil N enrichment introduced by N addition, plant-microbial interaction and indirect environmental qualities including pH and Al3+, would also affect plant N uptake from different forms (Niu et al., 2016). Firstly, two processes are mainly responsible for the production of the available N in soil across N addition gradients. At low levels of N addition, plants allocate more carbon and energy to belowground for microorganisms, and activate rhizospheric microorganisms to produce more available N. At high levels, plants would allocate more carbon to aboveground parts and decrease their reliance on microorganisms (Kuzyakov and Xu, 2013; Sun et al., 2014). Thus, microbial biomass would influence soil available N, and then plant N uptake. Secondly, soil acidification can decrease microbial activities. At the same time, soil acidification potentially mobilizes phytotoxic metal ions, such as Al3+, Mn2+ (Q. Tian et al., 2016; D. Tian et al., 2016), which suppress a plant's N uptake through affecting its root physiology. At least three processes can affect soil acidification caused by NH4NO3 addition: (i) deposition of H+ with NO3 from the oxidation of NH4+, (ii) H+ release when plants or microorganisms absorb NH4+, and (iii) leaching of buffering base cations (Chen et al., 2016). However, it remains unclear how habitat qualities caused by N addition affects plant N uptake pattern through mediation by soil N enrichment, soil acidification etc.

To clarify how the N uptake strategy (chemical N partitioning verses preference) of species changes with N addition, we determined the uptake of ammonium and nitrate of 9 plant species that all appeared along the N addition gradient (0, 5, 10, and 15 g N m−2 year−1) with 15N labeling in a 7-year NH4NO3 addition alpine meadow on the Qinghai-Tibetan Plateau. Specially, we investigated: (i) Whether chemical N partitioning (species specialize in utilizing different forms of N resources) or fitness equalizing mechanism (species prefer the most common form of N) dominated community assembly under conventional land use (i.e., winter grazing) along the N addition gradient; and (ii) How do changes in habitat qualities resulted from N addition would affect plant N uptake.

Section snippets

Study site

Our experiment was conducted in an alpine meadow in the eastern part of the Qinghai-Tibetan Plateau (35°58′ N, 101°53″E), i.e. in Maqu, Gansu, China. The elevation is approximately 3500 m. The mean annual temperature is 1.2 °C, ranging from −10.7 °C in January to 11.7 °C in July. The mean annual precipitation is 620 mm, which mainly falls in summer. This typical alpine meadow is about 54 species, and is dominated by annual and perennial herbaceous species, e.g. Aster diplostephioides,

Plant N content, δ15N and aboveground biomass

N content (%) varied among the 9 plant species. Without N addition (i.e., 0 g m−2 year−1), plant N content ranged from 1.09% (L. virgaurea) to 1.81% (Anemone trullifolia) (Table 1). Under N addition, Anemone trullifolia had the highest N content (2.01%, 4.08%, and 4.75% under N addition of 5, 10, 15 g m−2 year−1, respectively, whereas C. aridula had the lowest (1.05%, 1.45%, and 1.5%, respectively). The 9 species also varied in δ15N (‰) except under N addition of 5 g m−2 year−1. Of all the 9

Discussion

As N is one major nutrient limiting plant growth in most terrestrial ecosystems, N uptake strategy may play a critical role in species coexistence (McKane et al., 2002; Silvertown, 2004; Houlton et al., 2007; Andersen and Turner, 2013). Here we examined whether species N uptake strategy changes after 7 year's N (NH4NO3) addition using the 15N labeling approach in an alpine meadow. We found that instead of specialized on different inorganic N forms, diverse species could track changes in N cycle

Conclusions

In summary, we conclude that there is an apparent community-wide trend of tracking the most abundant form of inorganic N in the soil after N addition in the alpine meadow. Our findings suggest that the fitness equalizing associated to N resource, rather than niche partitioning mechanism, might contribute to the community assembly in the alpine meadow. However, investigations with considerable sampling of species and on systems without anthropogenic disturbance are needed to assess the

Declaration of competing interest

All authors have no conflict of interest to declare.

Acknowledgements

This work was supported by the National Natural Science Foundation of China (31830009, 31770518 and 41877089). The work was done in the Research Station of Alpine Meadow and Wetland Ecosystems of Lanzhou University. We thank Dexin Sun, Shengman Lyu for helping us perform the experiment.

Authors' contribution

SZ designed the experiment. LZ, TBZ conducted experiments, and collected data. LZ, XLX, MN and SZ developed the hypothesis. LZ and XL analyzed the data. LZ, XLX, and SZ wrote the manuscript. All authors approved the final manuscript.

Data accessibility

All data supporting the manuscript are presented, and additional information related is available from the corresponding author if reasonable request.

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