Limited inorganic N niche partitioning by nine alpine plant species after long-term nitrogen addition
Graphical abstract
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.
References (52)
- et al.
Are microorganisms more effective than plants at competing for nitrogen?
Trends Plant Sci.
(2000) - et al.
Dissolved organic nitrogen uptake by plants—an important N uptake pathway?
Soil Biol. Biochem.
(2005) - et al.
Evolutionary history resolves global organization of root functional traits
Nature
(2018) Plant coexistence and the niche
Trends Ecol. Evol.
(2004)- et al.
An extraction method for measuring soil microbial biomass C
Soil Biol. Biochem.
(1987) - et al.
Fate of organic and inorganic nitrogen in crusted and non-crusted Kobresia grasslands
Land Degrad. Dev.
(2017) - et al.
Preferences or plasticity in nitrogen acquisition by understorey palms in a tropical montane forest
J. Ecol.
(2013) - et al.
Plasticity in nitrogen uptake among plant species with contrasting nutrient acquisition strategies in a tropical forest
Ecology
(2017) - et al.
Niche complementarity due to plasticity in resource use: plant partitioning of chemical N forms
Ecology
(2010) - et al.
Pedogenesis, permafrost, and soil moisture as controlling factors for soil nitrogen and carbon contents across the Tibetan Plateau
Glob. Chang. Biol.
(2009)
Plant preference for ammonium versus nitrate: a neglected determinant of ecosystem functioning?
Am. Nat.
AIC model selection and multimodel inference in behavioral ecology: some background, observations, and comparisons
Behav. Ecol. Sociobiol.
The mineral nutrition of wild plants
Annu. Rev. Ecol. Syst.
Soil acidification exerts a greater control on soil respiration than soil nitrogen availability in grasslands subjected to long-term nitrogen enrichment
Funct. Ecol.
Mechanisms of maintenance of species diversity
Annu. Rev. Ecol. Syst.
Increased N affects P uptake of eight grassland species: the role of root surface phosphatase activity
Oikos
Chinese Soil Taxonomy: Theories, Methods and Applications
Competition for light causes plant biodiversity loss after eutrophication
Science
Stable isotope methods in biological and ecological studies of arthropods
Entomologia Experimentalis et Applicata
A climate-driven switch in plant nitrogen acquisition within tropical forest communities
Proc. Natl. Acad. Sci.
The paradox of the plankton
Am. Nat.
Competition between roots and microorganisms for nitrogen: mechanisms and ecological relevance
New Phytol.
Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed
Ecology
Community trait response to environment: disentangling species turnover vs intraspecific trait variability effects
Ecography
Aggravated phosphorus limitation on biomass production under increasing nitrogen loading: a meta-analysis
Glob. Chang. Biol.
Explaining maximum variation in productivity requires phylogenetic diversity and single functional traits
Ecology
Cited by (18)
Warming reconstructs the elevation distributions of aboveground net primary production, plant species and phylogenetic diversity in alpine grasslands
2021, Ecological IndicatorsCitation Excerpt :For example, warming increased the relative exclusive contribution of soil pH, temperature and water availability, but decreased the relative exclusive contribution of soil nutrition to changes of species richness and PD along the elevation gradient. The change in predominant/limited factor may result in the survival of species that are more adaptable to dominant/limited factors and subsequently alter plant community assembly toward niche partitioning related to dominant factor (Klanderud and Birks, 2003; Zhang et al., 2020). Fourth, plant dispersal can play very important roles in plant species survival and community assembly (Moser et al., 2011).
Competition for nitrogen between plants and microorganisms in grasslands: effect of nitrogen application rate and plant acquisition strategy
2024, Biology and Fertility of Soils