Topographical influences on foliar nitrogen concentration and stable isotope composition in a Mediterranean-climate catchment

https://doi.org/10.1016/j.ecoinf.2022.101569Get rights and content

Highlights

  • Foliar δ15N and [N] of Eucalyptus varied in a year as those of Acacia kept constant.

  • Foliar δ15N and [N] are positively correlated for both Eucalyptus and Acacia.

  • Eucalyptus foliar δ15N was higher at the downslope than the upslope locations.

  • Eucalyptus foliar [N] was independent of slope locations.

  • Drainage area explained 46% spatial variation of Eucalyptus dry-season foliar δ15N.

Abstract

Nitrogen (N) oligotrophication is increasing globally across terrestrial ecosystems and manifested in decreasing nitrogen concentration ([N]) and changes in the stable nitrogen isotope composition (δ15N) of foliage. Heterogeneity in plant nitrogen sources makes it challenging to detect the effects of N oligotrophication even at a small catchment scale with complex topography. Understanding the spatial and temporal variation of foliar δ15N and [N] at such a scale is required to develop useful ecological indicators and monitoring methods to support catchment management with a potential N oligotrophication problem. This study examined spatial and high-resolution temporal variation of foliar δ15N and [N] and their influencing factors in ten trees grouped by Eucalyptus and Acacia in a native forest vegetation catchment. Over 16 sampling campaigns within a 12-month period, foliar δ15N and [N] increased in Eucalyptus but were constant in the N2-fixing Acacia. The higher foliar [N] and δ15N in Acacia reflected its N2-fixation ability. Topographic flow accumulation area (NDVI) explained 46% (77%) of spatial variation in dry-season Eucalyptus foliar δ15N ([N]). For Eucalyptus, foliar δ15N was higher at the downslope than the upslope locations, but no hillslope location differences were observed for foliar [N]. These results suggest that in the non-N2-fixing Eucalyptus, seasonal water stress related nitrogen availability may be reflected in foliar δ15N rather than foliar [N]. As such, foliar δ15N of non-N2-fixing plants potentially is a more sensitive indicator of seasonal or topographical N availability than foliar [N].

Introduction

Nitrogen (N) oligotrophication of terrestrial ecosystems is increasing globally in the context of increasing atmospheric CO2 concentration (Craine et al., 2018; Feng et al., 2015; Gill et al., 2002; Smith et al., 2014). Consequently, foliar nitrogen concentrations ([N], in % by weight g/g) have decreased globally in grassland, cropland and forest ecosystems (Feng et al., 2015) by ~9% over the last 37 years (Craine et al., 2018). A similar trend was also confirmed by other studies. For example, a prolonged decline (−0.0086% per year) in foliar [N] was observed for mixed grasses and woody plants from 1926 to 2008 in central North American (McLauchlan et al., 2010). A historical record documented that foliar [N] decreased by ~14.5% for grasses, shrubs and trees from 1920 to 1990 in Spain (Peñuelas and Estiarte, 1997). The cause of oligotrophication is under debate. Two major possibilities are considered: (1) progressively increasing plant biomass which relatively dilutes N in ecosystem biomass production (McLauchlan et al., 2010; Smith et al., 2014) and (2) increased N demand due to a CO2 fertilization effect (Feng et al., 2015).

Whether foliar [N] or N availability in soil better reflects changing N supply in ecosystems remains an open question (Craine et al., 2009). Additional insight into soil N availability is gained from the combined changes in foliar [N] and its stable nitrogen isotope composition (δ15N) (Craine et al., 2009; Högberg, 1997). Due to the likelihood of 15N-enrichment processes (e.g. nitrification and denitrification) in ecosystems characterized by high N availability, the combination of low foliar [N] and low δ15N suggests low N availability (Craine et al., 2012; Högberg, 1997; McLauchlan et al., 2010). Globally, a foliar [N] decline of 9% was associated with a decline of 0.6–1.6‰ in foliar δ15N for terrestrial ecosystems between 1980 and 2017 (Craine et al., 2018). At a regional scale for grass and woody plants in central North American grasslands, δ15N and [N] are positively correlated (δ15N = 3.39 [N] - 5.28, R2 = 0.20, McLauchlan et al., 2010). Similar to this positive relationship, coniferous Picea trees at Glacier Bay, Alaska has a relationship of δ15N = 6.61 [N] - 13.79 (R2 = 0.73, Hobbie et al., 2000). Thus, the association between foliar δ15N and [N] seems to provide a useful indicator of nitrogen availability in an ecosystem.

Foliar δ15N values are influenced by the δ15N signatures of nitrogen sources, which are a function of environmental conditions (Hietz et al., 2011; Houlton et al., 2007), the limitation of N and the reliance on mycorrhizal N uptake (Högberg, 1997), forms of N taken up by the plant, and plant internal fractionation processes during assimilation (Evans, 2001; Robinson, 2001). The relationships between plant δ15N and climatic variables have been examined on regional and global scales. Foliar δ15N decreases with increasing mean annual rainfall (Ma et al., 2018; Schulze et al., 2014) and decreasing mean annual temperature globally (Amundson et al., 2003; Chen et al., 2017; Craine et al., 2009). Therefore, in a catchment where environmental conditions vary spatially, it is expected that N limitation, reflected in foliar δ15N and its relationship with [N], also varies spatially. Knowledge of this spatial variation would provide useful information for catchment management, which, however, is currently missing.

Environmental conditions, such as water, energy, and nutrients at a local scale are fundamentally shaped by hillslopes of different aspects (Fan et al., 2019). In a small catchment, the spatial variability of rainfall is likely small, but soil moisture can be very different resulting from topography-induced hydrological redistribution (Lanni et al., 2011; Quinn et al., 2010). In addition, radiation inputs can differ substantially between slopes causing potentially different evaporation and transpiration (Liu et al., 2022; Xu et al., 2017). It is also expected that local environmental conditions, including water and nutrient (including N) availability (Billings et al., 2016; Lehmann et al., 2003; Poorter, 1993) are directly controlled by the topography of a catchment (Daly et al., 2010; Turner et al., 1997). Knowledge of variations in foliar [N] and the factors driving its variation is useful for understanding the N oligotrophication problem and improving catchment management.

The differences in plant physiology driven by environmental conditions are often reflected in plant foliar δ13C (Cornwell et al., 2018; Diefendorf et al., 2010; Ehleringer et al., 1992; Farquhar and Sharkey, 1982; Xu et al., 2017). The relations between foliar δ13C and δ15N have been explored in a few studies. Zhao et al. (2010) reported negative correlations between foliar δ13C and δ15N for C3 plants except for legumes, but positive for C3 legumes and C4 plants in the Tengger Desert of China. Their work confirmed the linkage between foliar δ13C and δ15N. However, such a relationship was not found by Liu et al. (2007) based on leaf samples collected from 26 C3 shrubs and tree species in Ethiopia Rift Valley along an elevation gradient from 900 to over 4000 m above sea level. Similarly, Schulze et al. (2014) found no relationship between foliar δ13C and δ15N for the genera Eucalyptus and Acacia along a rainfall gradient across Western Australia. A possible reason for the difference between these two studies and Zhao et al. (2010) is that the studies by Liu et al. (2007) and Schulze et al. (2014) were focused on the rainy season when correlations between δ13C and δ15N were weak due to a lack of water stress. Thus, investigations covering both wet and dry seasons is required to obtain the whole picture of the relationships. Knowledge of which variables vary seasonally and which remain seasonally invariant would be useful for efficient and appropriate sampling designs. Such knowledge is relatively clear for δ13C (e.g., Xu et al., 2017), however, not for foliar δ15N and [N].

The differences in foliar δ13C, which is often used as an indicator of plant water stress for species of C3 photosynthetic pathway (e.g. Xu et al., 2017), originate from the cumulative stable isotope fractionation effects during photosynthesis (Farquhar et al., 1989). Carbon is fixed and accumulated throughout the whole lifetime of a leaf, while N could be transferred from an old leaf to a new one (Craine et al., 2015; Farquhar and Sharkey, 1982). The atmospheric CO2 is the single source for C in plants, while multiple sources, such as soil N, precipitation, and atmospheric N2 (for N2-fixing species only) provide N for plants (Craine et al., 2015). Nevertheless, the relationships between foliar δ13C and δ15N could still be valuable for investigating the cumulative water stress effect on plant nutrition and N limitation.

With up-to-date understanding of factors affecting foliar δ15N and [N], it has been applied as an effective ecological indicator for the trend of N oligotrophication regionally and globally. However, it is not known yet whether and how this indicator may work at a local scale to support catchment management. This study, conducted in a small native vegetated catchment on species with or without N2-fixation potential, aimed to (1) examine temporal and spatial variability of foliar [N] and foliar δ15N, and their possible explanatory factors; (2) reveal the relationship between foliar [N] and foliar δ15N. For a native vegetation catchment under the Mediterranean-climate part in Australia, objective (1) will contribute to predicting where in the landscape and under what condition N oligotrophication is likely to occur. Objective (2) will contribute to using foliar δ15N as an indicator for soil-plant nitrogen sources and conditions at the local scale.

Section snippets

Study area

The study site is located in a small catchment at the Mount Wilson (138.64°E, 35.21°S, 370 m above sea level) in the Mount Lofty Ranges of South Australia (Fig. 1). The catchment of 0.12 km2, surrounded by agricultural farms, is covered by remnant native vegetation. The vegetation is dominated by Eucalyptus species, with a small number of Acacia trees. The catchment is cool and humid in winter with a mean daily temperature of ~9.1 °C in July while hot and dry in summer with a mean daily

Foliar [N], C/N and δ15N

Generally, both foliar [N] and δ15N were slowly increasing over time for Eucalyptus trees but were quite constant for Acacia trees (Fig. 2). Foliar [N] of four Eucalyptus trees gradually increased (by 0.5%) in the 12-month sampling period (p < 0.05) while that of Eucalyptus upE2 and two Acacia trees were relatively constant (p-values were very close to 1). Similarly, foliar δ15N of the same four Eucalyptus trees gradually increased (by 0.5‰) (p < 0.05) while those of the Eucalyptus upE2 and two

Localized foliar [N] and δ15N

The range of foliar [N] in this study was 0.5–2.2% for Eucalyptus trees and 1.4–2.5% for Acacia trees at the Mount Wilson study site. This range of values is similar to that reported for the same genera by Schulze et al. (2014), where foliar [N] had an average value of 1.2% for Eucalyptus trees and 1.9% for Acacia across Western Australia. In northeastern Kansas, USA, the mean foliar [N] was about 2.5% for non-N2-fixing species and around 3.6% for the N2-fixing species (Craine et al., 2012). At

Conclusions

This study, based on high frequency leaf sampling over one year in a small native-vegetation catchment, foliar δ15N and [N] were gradually increasing over 12 months for the examined Eucalyptus trees. They remained constant for the examined Acacia trees with N2-fixing abilities. The examined N2-fixing Acacia trees appear to have higher foliar [N] and δ15N, indicating that N2-fixing does occur in the root zone of the Acacia trees. Both tree groups show a positive correlation between foliar [N]

Funding information

National Natural Science Foundation of China, Grant/Award Number: 41807148;

The Open Foundation of MOE Key Laboratory of Western China's Environmental System, Lanzhou University and the Fundamental Research Funds for the Central Universities, Grant/Award Number: lzujbky-2019-kb01;

National Centre for Groundwater Research and Training, Australian Research Council, Grant/Award Number: SR08000001;

Australian Research Council, Grant/Award Number: FT110100352.

Declaration of Competing Interest

We declare we have no competing interests.

Acknowledgments

Data analysis of this study was funded by the National Natural Science Foundation of China (41807148), the Open Foundation of MOE Key Laboratory of Western China's Environmental System, Lanzhou University and the Fundamental Research Funds for the Central Universities (lzujbky-2019-kb01). The field experiments were funded by National Centre for Groundwater Research and Training (Australia SR08000001), China Scholarship Council, and a Future Fellowship from the Australian Research Council

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