Companion species mitigate nutrient constraints in high country grasslands in New Zealand伴生物种缓解新西兰高地草地的养分限制

Zhang Wei · Thomas M. R. Maxwell · Brett Robinson · Nicholas Dickinson

Received: 1 August 2022 / Accepted: 8 November 2022 / Published online: 17 November 2022 © The Author(s), under exclusive licence to Springer Nature Switzerland AG 2022

1Abstract摘要

Background Experimental work using pot trials and mesocosm studies has indicated that species combinations are more effective than single species mitigating the soil nutrient constraints that limit pasture productivity in New Zealand’s hill country, but there is little field evidence to support this.

背景 盆栽试验和中宇宙（mesocosm）研究表明，在缓解限制新西兰丘陵地区牧场生产力的土壤养分约束方面，物种组合比单一物种更为有效，但目前尚缺乏支持这一结论的田间证据。

Aim We question whether coexistence of species provides an opportunity to facilitate enhanced uptake and improved procurement of key soil nutrients in these mid-altitude grasslands.

目的 探讨在这些中海拔草地中，物种共存是否能够促进关键土壤养分的吸收并改善其获取。

Methods Native and exotic legumes and co-occurring plant species were sampled according to whether they were growing together in close proximity or in single species patches. Foliar concentrations of nutrients were compared.

方法 根据本土和外来豆科植物及与其共生的植物物种是紧邻共同生长还是生长于单一物种斑块中进行采样，并比较其叶片养分浓度。

Results Nutrient concentrations in a native broom, Carmichaelia petriei, were higher when it was growing in combination with native tussock grasses. Higher concentrations of eight nutrients were recorded in foliage of an exotic legume, Lotus pedunculatus, when it was growing with native grasses or within the acuminate foliage of Aciphylla aurea (golden spaniard). Foliar concentrations of only P and Mn were elevated in white clover (Trifolium repens) foliage when it was growing in combination with grasses.

结果 本土金雀花Carmichaelia petriei与本土丛生禾草共同生长时，其养分浓度较高。外来豆科植物Lotus pedunculatus与本土禾草共同生长或生长于Aciphylla aurea（金色刺芹，golden spaniard）的尖锐叶丛之中时，其叶片中8种养分的浓度较高。白三叶草（Trifolium repens）与禾草共同生长时，其叶片中仅P和Mn的浓度有所升高。

Conclusions These findings point to mutual facilitation of nutrient uptake by combinations of species growing together. Some species that are less desirable from an agricultural perspective improve acquisition of soil nutrients by the plant community. Novel native species assemblages represent a potential opportunity to refine pasture management, facilitating optimal exploitation of nutrients. This could reduce fertiliser requirements and enhance and protect native biodiversity in pastoral grasslands.

结论 上述结果表明，共同生长的物种组合在养分吸收方面存在相互促进作用。一些从农业角度看不太理想的物种可改善植物群落对土壤养分的获取。新型本土物种组合为优化牧场管理、促进养分的最佳利用提供了潜在机遇。这有望减少肥料需求，并增强和保护放牧草地中的本土生物多样性。

Keywords Mutualism · Biogeochemistry · Trace elements · Biodiversity · Pasture production

关键词 互利共生 · 生物地球化学 · 微量元素 · 生物多样性 · 牧草生产

2Introduction引言

Responsible Editor: Hans Lambers.

Z. Wei · T. M. R. Maxwell · N. Dickinson (*) Faculty of Agriculture and Life Sciences, Lincoln University, Lincoln 7647, Christchurch, New Zealand e-mail: Nicholas.Dickinson@lincoln.ac.nz

B. Robinson

Department of Chemistry, University of Canterbury, Christchurch 8140, New Zealand

坎特伯雷大学化学系，基督城 8140，新西兰

Steep hill country at altitudes of about 400—1000 m accounts for 37% of New Zealand’s land area, with approximately half of this being pastoral farmland (Thom 2016; Stats^NZ 2021). Future environmental and economic resilience of this landscape is considered to be critical, although this is a multi-faceted and complex management issue (Brower et al. 2020; Rissman et al. 2021; Tozer et al. 2021). Our thesis is that sustainable agricultural development requires more knowledge of nutrient dynamics in the context of biodiversity in both pastoral and conservation grasslands.

海拔约400—1000 m的陡峭丘陵地区占新西兰国土面积的37%，其中约一半为放牧农田（Thom 2016; Stats^NZ 2021）。尽管这是一个多层面且复杂的管理问题，但该景观未来的环境与经济韧性被认为至关重要（Brower et al. 2020; Rissman et al. 2021; Tozer et al. 2021）。我们的观点是，可持续农业发展需要在放牧草地和保护性草地中更深入地了解生物多样性背景下的养分动态。

Earlier forest clearance, historic overgrazing and associated soil erosion have provided scope for rebuilding hill country soils through improved pasture management. This has already been occurring for several decades through better land management, prevention of overgrazing and rabbit control (Parfitt et al. 2014; Schipper et al 2017). Potentially this could be enhanced further through restoration of native vegetation and incorporation of native species into existing naturalised exotic pasture (Trotter et al 2005). Native plant species are likely to be better adapted to the natural environment, but they are low yielding and of much lesser forage value. For this reason, agricultural management has focussed on conversion of native vegetation and replacement with more productive exotic species. However, pasture and stock production in the hill country are constrained by low soil pH and fertility, particularly in terms of phosphorus, sulphur and trace elements that include molybdenum and boron (Hendrie et al. 2021). These deficiencies restrict the successful establishment of clovers and other nitrogen (N) -fixing plants. Mt Grand Station, the location of the present study, provides a typical example of hill country conditions in these respects (Maxwell et al. 2010, 2016; Zhang et al. 2022a).

早期的森林砍伐、历史上的过度放牧以及随之而来的土壤侵蚀，为通过改进牧场管理重建丘陵地区土壤提供了空间。通过更好的土地管理、防止过度放牧和控制兔害，这一过程已持续了数十年（Parfitt et al. 2014; Schipper et al 2017）。通过恢复本土植被并将本土物种引入现有已归化的外来牧场，这一过程有望得到进一步加强（Trotter et al 2005）。本土植物物种可能更适应自然环境，但其产量低，饲用价值也低得多。因此，农业管理一直侧重于改造本土植被并以生产力更高的外来物种取而代之。然而，丘陵地区的牧草和牲畜生产受到土壤pH值低和肥力低的制约，尤其是磷、硫以及包括钼和硼在内的微量元素（Hendrie et al. 2021）。这些缺乏限制了三叶草和其他固氮（N）植物的成功定植。本研究所在地Mt Grand Station在上述方面是丘陵地区条件的典型代表（Maxwell et al. 2010, 2016; Zhang et al. 2022a）。

Top dressing with lime and fertilisers is largely impractical and too costly due to topography and the large area of land that will only support limited yields of herbage and stock in the prevailing climate and environment. During little more than 150 years since conversion of this landscape to sheep farming, oversowing with exotic species of grasses and legumes has substantially improved productivity (Bork et al. 2017). Hill country sheep and beef farming plays a highly important role in the nation’s economy (Scrimgeour 2016; Stats^NZ 2021). Nevertheless, both establishment and sustainability of improved pasture with a suitable component of annual and perennial legumes remains a challenge; seasonal resilience is difficult to achieve and there is also encroachment by less desirable invasive and exotic species of grasses and shrubs.

由于地形原因，加之大面积土地在当前气候和环境条件下仅能支撑有限的牧草产量和载畜量，施用石灰和肥料进行表施在很大程度上不切实际且成本过高。自该景观转为养羊业以来的150余年间，补播外来禾草和豆科植物已大幅提高了生产力（Bork et al. 2017）。丘陵地区的羊和肉牛养殖在国民经济中发挥着极其重要的作用（Scrimgeour 2016; Stats^NZ 2021）。然而，建立并维持含有适当比例一年生和多年生豆科植物的改良牧场仍是一项挑战；季节韧性难以实现，且还存在不太理想的入侵性和外来禾草及灌木的侵占。

A better understanding of the coexistence of native vegetation with introduced grasses and legumes in the hill country environment may be of benefit to both agriculture and conservation. We have previously reported the results of experimental work of plant uptake of nutrients from hill country soils to investigate the compatibility of both exotic and native plants with contrasting root systems. Pot trials provided evidence of functional compatibility of mixed-species rhizospheres that facilitate and improve the procurement of limiting soil nutrients (Zhang et al. 2022b). We identified the existence of a mutualistic relationship between legumes and grasses that provided nutritional benefits not just to grasses, but also to legumes (Zhang et al. 2022c). However, in that study, a native tussock grass had lower N when growing with the exotic legumes that may reflect a lack of adaptation to coexistence. More recently published mesocosm studies used soil cores with component vegetation assemblages that were extracted from unfertilised grassland in the hill country, and then transferred to a controlled environment growth chamber (Zhang et al. 2022a). Once again, species co-existence was beneficial in terms of uptake of key soil nutrient; facilitation from grasses to clovers was evident.

更好地了解丘陵地区环境中本土植被与引入的禾草和豆科植物的共存，可能对农业和自然保护均有裨益。我们此前报道了植物从丘陵地区土壤中吸收养分的试验结果，以研究具有不同根系的外来植物和本土植物之间的相容性。盆栽试验提供的证据表明，混合物种根际具有功能相容性，可促进并改善对限制性土壤养分的获取（Zhang et al. 2022b）。我们发现豆科植物与禾草之间存在互利关系，这种关系不仅为禾草、也为豆科植物带来营养益处（Zhang et al. 2022c）。然而，在该研究中，一种本土丛生禾草与外来豆科植物共同生长时N含量较低，这可能反映出其缺乏对共存的适应。最近发表的中宇宙研究采用了从丘陵地区未施肥草地中采集的含有组成植被组合的土柱，并将其转移至可控环境生长室中（Zhang et al. 2022a）。结果再次表明，物种共存有利于关键土壤养分的吸收；禾草对三叶草的促进作用十分明显。

The aim of the research reported in the present paper was to investigate whether the same type of facilitation between species could be demonstrated in situ in a hill country grassland (Fig. 1). This sampling exercise was an attempt to validate earlier ex situ findings that legumes derive nutritional benefits from growing with grasses in terms of procurement of trace elements in limited supply in the hill country soils. Our hypothesis was simply that plants growing with companion species would have demonstrably different foliar concentrations of key nutrient elements compared to the same species growing alone.

本文所报道研究的目的是探讨能否在丘陵草地原位证实物种之间存在同样类型的促进作用（图1）。本次采样旨在验证早期异位研究的结果，即在丘陵地区土壤中供应有限的微量元素获取方面，豆科植物可从与禾草共同生长中获得营养益处。我们的假设很简单：与伴生物种共同生长的植物，其关键养分元素的叶片浓度与单独生长的同一物种相比存在明显差异。

3Site and methods研究地点与方法

This study was carried out at Mt Grand Station, a Lincoln University owned hill country pastoral farm situated in Hawea, Central Otago on South Island. The soils in the region have been created from the breakdown of schist, loess, and alluvial gravels (Molloy 1998; Duncan et al. 1997). The high country soils are light and prone to erosion by wind and water, especially after the loss of vegetation. Soils on Mt Grand are acidic and of low fertility (Table 1). Soil phosphorus (P) is essential grass-clover pastoral farming systems; its supply and availability is possibly the most significant constraint due to its promotion of the growth of clovers. Boron, Mo and nickel (Ni) were deficient in our analyses, although Sulphur (S) and a range of other micronutrients (cobalt, Co; copper, Cu; iron, Fe; manganese, Mn; Mo; zinc, Zn) are frequently in short supply for pasture plants and grazing livestock in New Zealand grasslands (Crush et al. 2018). The Mt Grand landscape provides a complex mosaic of microenvironments associated with altitude, aspect and vegetation cover (Duncan et al. 2001). Mt Grand Station (1607 ha) is mainly steep hill country (from 400 – 1445 m asl.); 60% is above 1000 m in 8 blocks, with 94% of land considered suitable for grazing. Summer soil moisture deficits constrain pasture production (annual rainfall is 690–800 mm).

本研究在Mt Grand Station进行，这是林肯大学所有的一处丘陵放牧农场，位于南岛中奥塔哥地区的Hawea。该地区土壤由片岩、黄土和冲积砾石风化形成（Molloy 1998; Duncan et al. 1997）。高地土壤质地轻，易受风蚀和水蚀，尤其是在植被丧失之后。Mt Grand的土壤呈酸性且肥力低（表1）。土壤磷（P）对禾草-三叶草放牧农业系统至关重要；由于其对三叶草生长的促进作用，磷的供应及有效性可能是最重要的限制因素。在我们的分析中，硼、Mo和镍（Ni）均缺乏，而在新西兰草地中，硫（S）以及一系列其他微量营养元素（钴，Co；铜，Cu；铁，Fe；锰，Mn；Mo；锌，Zn）对牧草植物和放牧牲畜而言也常常供应不足（Crush et al. 2018）。Mt Grand的景观由与海拔、坡向和植被覆盖相关的复杂微环境镶嵌而成（Duncan et al. 2001）。Mt Grand Station（1607 ha）主要为陡峭丘陵地（海拔400 – 1445 m）；其中60%位于1000 m以上，分为8个区块，94%的土地被认为适合放牧。夏季土壤水分亏缺制约着牧草生产（年降雨量为690–800 mm）。

tussocks, Festuca novae-zelandiae tussocks within exotic pasture grass vegetation in the middle distance, and more heavily grazed pasture in the background

丛草，中景为外来牧草植被中的Festuca novae-zelandiae丛草，背景为放牧强度较大的牧场

Analyses and units of measurement follow standard methodology from a commercial laboratory and also Lincoln University Analytical Services*. Analyses by the commercial laboratory are routinely carried out on defined volume rather than mass of soil. Analytical methods were: Olsen extraction ¹ followed by Molybdenum Blue colorimetry; HNO3 – HClO4 microwave digestion followed by ICP-OES determination ²; 1 M Neutral ammonium acetate extraction followed by ICP-OES determination ³; Mehlich 3 Extraction followed by ICP-OES ⁴ Significant deficiencies are emboldened

分析方法和计量单位遵循商业实验室及林肯大学分析服务中心*的标准方法。商业实验室的分析通常以土壤的一定体积而非质量为基础。分析方法为：Olsen浸提 ¹后采用钼蓝比色法；HNO3 – HClO4微波消解后采用ICP-OES测定 ²；1 M中性乙酸铵浸提后采用ICP-OES测定 ³；Mehlich 3浸提后采用ICP-OES测定 ⁴。显著缺乏的数值以粗体表示

Methodology in this study simply involved sampling and analysing foliage of a range of exotic and native legumes at different altitudes. Sampling locations were semi-randomly selected between altitudes of 700 – 1,000 m asl. in a walkover of the site on a single day by one individual (ZW) where species could be found both growing in close proximity and also in single species patches 0.5 – 3.0 m apart. Our assumption was that both above- and below-ground interactions between species would be markedly less when they were growing further apart. Visually comparable environments and similar soil were important selection criteria, and the reason why paired comparisons were always recorded within 3 m of each other. Above-ground non-woody plant biomass was sampled of legumes growing either in single species patches or in combination with exotic pasture grasses, a native tussock grass or a native acuminate umbellifer (Aciphylla aurea), all of which were widely established across the sampling site.

本研究的方法仅为在不同海拔采集并分析一系列外来和本土豆科植物的叶片。采样点在海拔700 – 1,000 m之间半随机选取，由一人（ZW）于同一天徒步踏查研究区完成，选取的地点须既有物种紧邻共同生长的情况，又有相距0.5 – 3.0 m的单一物种斑块。我们的假设是，物种间相距较远时，其地上和地下相互作用均会明显减弱。目测环境相近及土壤相似是重要的选择标准，这也是配对比较始终在相距3 m以内记录的原因。采集的是豆科植物地上非木质部分生物量，这些豆科植物或生长于单一物种斑块中，或与外来牧草、一种本土丛生禾草或一种本土尖叶伞形科植物（Aciphylla aurea）共同生长，上述植物在整个采样地均有广泛分布。

Vegetation across the sampling site varied with altitude and aspect, consisting of mixed communities of native tussock grassland species with oversown pasture grasses and legumes (Fig. 2), with scattered assemblages of woody shrubs (mostly Discaria toumatou, Kunzea robusta and Coprosma propinqua) (see DOC 2006; Duncan et al. 2001). Some invasive weeds are also well established, notably Hieracium spp. in inter-tussock spaces at higher parts of the altitude range, and an invasive shrub Rosa rubiginosa in some lower parts. Tall pasture grasses are prominent at lower altitudes of this range, particularly Anthoxanthum odoratum (sweet vernal grass), Agrostis capillaris (browntop) and Festuca rubra (red fescue), with a scattered dispersion of Trifolium (clovers) and Lotus spp. Samples of the three pasture grasses were amalgamated. Tussock grassland and the proportion of native species in plant communities tends to increase with altitude, with patches of tall acuminate rosettes of Aciphylla aurea (golden spaniard). Native tussock grasses included Chionochloa rigida (narrow-leaved snow tussock), Poa colensoi (blue tussock) and Festuca novae-zelandiae (hard tussock). A native broom (Carmichaelia petriei), one of a small number of threatened native species of broom found across the station and in the high country (nzpcn.org.nz; DOC 2006; Mark 2012), was scattered mostly as individual plants across the sampling site. Carmichaelia spp. are commonly referred to as New Zealand brooms (Tan 2014). Their role in soil development in chronosequences through a large build-up of soil N and facilitating forest species has been reported previously (Bellingham et al. 2001).

采样地植被随海拔和坡向而变化，由本土丛生草地物种与补播的牧草及豆科植物组成的混合群落构成（图2），并散布有木本灌木群落（主要为Discaria toumatou、Kunzea robusta和Coprosma propinqua）（见 DOC 2006; Duncan et al. 2001）。一些入侵杂草也已广泛定植，尤其是海拔较高处丛草间隙中的Hieracium spp.，以及部分低海拔处的入侵灌木Rosa rubiginosa。在该海拔范围的较低处，高大牧草占优势，特别是Anthoxanthum odoratum（黄花茅）、Agrostis capillaris（细弱剪股颖）和Festuca rubra（紫羊茅），并零星分布有Trifolium（三叶草）和Lotus spp.。3种牧草的样品进行了合并。丛生草地及本土物种在植物群落中所占比例往往随海拔升高而增加，并有高大尖叶莲座状的Aciphylla aurea（金色刺芹）斑块。本土丛生禾草包括Chionochloa rigida（窄叶雪丛草）、Poa colensoi（蓝丛草）和Festuca novae-zelandiae（硬丛草）。一种本土金雀花（Carmichaelia petriei）是在该农场及高地发现的少数受威胁本土金雀花物种之一（nzpcn.org.nz; DOC 2006; Mark 2012），主要以单株形式散布于采样地。Carmichaelia spp.通常被称为新西兰金雀花（Tan 2014）。此前已有报道指出其在土壤时间序列中通过大量积累土壤N和促进森林物种而在土壤发育中发挥作用（Bellingham et al. 2001）。

Carmichaelia and the four groups of companion grasses (pasture grasses and three species of native tussock grasses) were sampled. Two exotic legumes, Trifolium repens (white clover) and Lotus pedunculatus (bird’s-foot trefoil) and their companion native grass, Festuca novae-zelandiae (fescue tussock) and Chionochloa rigida amara (narrow-leaved snow tussock), were collected. Lotus was also sampled that was growing with or adjacent to Aciphylla aurea. Five replicates were sampled for each legume, each by excising five leaves across the canopy. Five replicates of each grass were sampled in the same way. All plant samples were collected at least 2 cm from the ground to avoid soil contamination of samples. All the plants were dried (48 h, 65 °C), finely ground in a mill, then microwave digested followed by elemental analysis using ICP-MS (7500cx, Agilent Technologies) using standard protocols. Total N was analysed using an Elementar Rapid Max N Elemental Analyser. Data that were not normally distributed were

对Carmichaelia及4组伴生禾草（牧草和3种本土丛生禾草）进行了采样。采集了两种外来豆科植物Trifolium repens（白三叶草）和Lotus pedunculatus（大百脉根），以及与其伴生的本土禾草Festuca novae-zelandiae（羊茅丛草）和Chionochloa rigida amara（窄叶雪丛草）。还采集了与Aciphylla aurea共同生长或相邻生长的Lotus。每种豆科植物采集5个重复，每个重复在冠层中剪取5片叶子。每种禾草以同样方式采集5个重复。所有植物样品均在离地面至少2 cm处采集，以避免样品受到土壤污染。所有植物样品经烘干（48 h，65 °C），用粉碎机磨细，然后进行微波消解，并按标准规程采用ICP-MS（7500cx，Agilent Technologies）进行元素分析。全氮采用Elementar Rapid Max N元素分析仪测定。不符合正态分布的数据

Fig. 2 Sampling locations at Mt Grand Station图2 Mt Grand Station的采样点

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log-transformed before analysis. Differences between means were determined using one-way ANOVA, with post-hoc Fisher LSD test. All analyses were conducted using Minitab 19.

在分析前进行对数转换。均值间差异采用单因素ANOVA测定，并进行Fisher LSD事后检验。所有分析均使用Minitab 19完成。

4Results结果

The native broom (Carmichaelia petriei) had significantly higher above-ground tissue concentrations of several elements when it was growing with companion species of grasses. Higher foliar concentrations of K, Ca, Mg and B were recorded when it was growing with pasture grasses and with P. collensoi at lower altitudes of the sampling range (Fig. 3A) and higher Mn, Zn and Ni when growing with F. novae-zelandiae at higher altitudes of the sampling range (Fig. 3B). Conversely, the two larger native tussock grasses tended to have lower foliar concentrations of nutrients when growing together with broom (Fig. 4). This was much less evident in the pasture grasses and the small blue tussock, P. colensoi. Of all chemical elements, only K and Mn were elevated in grasses growing with broom.

本土金雀花（Carmichaelia petriei）与伴生禾草物种共同生长时，其地上组织中多种元素的浓度显著较高。在采样范围的较低海拔处，其与牧草及P. collensoi共同生长时，叶片K、Ca、Mg和B浓度较高（图3A）；在采样范围的较高海拔处，其与F. novae-zelandiae共同生长时，Mn、Zn和Ni浓度较高（图3B）。相反，两种较大的本土丛生禾草与金雀花共同生长时，其叶片养分浓度往往较低（图4）。这在牧草和小型蓝丛草P. colensoi中则远不明显。在所有化学元素中，仅K和Mn在与金雀花共同生长的禾草中有所升高。

Foliar concentrations of eight nutrients in Lotus foliage were higher when it was growing with either C. rigida or A. aurea, or with both (Fig. 5); Fe was the only element in lower concentrations. Snow tussock, C. rigida, foliage had significantly higher foliar concentrations of N, Zn, Cu and Mo when growing with Lotus (Fig. 6). In contrast, higher P and

Lotus与C. rigida或A. aurea之一或两者共同生长时，其叶片中8种养分的浓度较高（图5）；Fe是唯一浓度较低的元素。雪丛草C. rigida与Lotus共同生长时，其叶片N、Zn、Cu和Mo浓度显著较高（图6）。相比之下，较高的P和

significate differences were recorded. Histogram bars are means ± standard deviations. Data were log transformed prior to analysis. Different letters separately indicate significant differences (P < 0.05)

显著差异的元素。柱状图为平均值 ± 标准差。数据在分析前进行了对数转换。不同字母分别表示差异显著（P < 0.05）

(Carmichaelia petriei). Figure illustrates only elements when significate differences were recorded. Histogram bars are means ± standard deviations. Different letters separately indicate significant differences (P < 0.05)

（Carmichaelia petriei）。图中仅显示存在显著差异的元素。柱状图为平均值 ± 标准差。不同字母分别表示差异显著（P < 0.05）

Mn concentrations in the foliage of Trifolium were in when it was growing with Festuca novae-zelandiae were the only significant differences recorded in combinations of clover or grasses (Fig. 7). No data are available for foliar concentrations of nutrients in A. aurea.

Mn浓度出现在与Festuca novae-zelandiae共同生长的Trifolium叶片中，这是三叶草与禾草组合中记录到的仅有的显著差异（图7）。目前尚无A. aurea叶片养分浓度的数据。

only elements when significate differences were recorded. Histogram bars are means ± standard deviations. Different letters separately indicate significant differences (P < 0.05)

仅显示存在显著差异的元素。柱状图为平均值 ± 标准差。不同字母分别表示差异显著（P < 0.05）

5Discussion讨论

This study provides field validation that broadly supports the findings of earlier ex situ experimental work (Zhang et al 2022a, 2022c), supporting our hypothesis that plants growing with companion species would have demonstrably different foliar concentrations of key nutrient elements compared to the same species growing alone. These findings provide field evidence of significant benefits of grasses to legume nutrition, by facilitating the procurement of key nutrients. When growing with grasses, legume foliage frequently had higher concentrations of P, K, S and Mn. Improved uptake of six other elements (Ca, Mg, S, Zn, B, Ni) was recorded in more than a single study (Table 2). When growing with legumes, higher foliar concentrations of K, but lower Ca, Fe and Mn were recorded in grasses.

本研究提供的田间验证总体上支持了早期异位试验的结果（Zhang et al 2022a, 2022c），也支持了我们的假设，即与伴生物种共同生长的植物，其关键养分元素的叶片浓度与单独生长的同一物种相比存在明显差异。这些结果为禾草通过促进关键养分的获取而显著有益于豆科植物营养提供了田间证据。与禾草共同生长时，豆科植物叶片中P、K、S和Mn的浓度往往较高。在不止一项研究中记录到另外6种元素（Ca、Mg、S、Zn、B、Ni）的吸收得到改善（表2）。与豆科植物共同生长时，禾草叶片中K浓度较高，而Ca、Fe和Mn浓度较低。

There are natural differences in foliar trace element concentrations between different species of legumes. For example, in pot experiments in which the growth of twelve species of legumes (including nine species of Trifolium and Lotus pedunculatus) were grown in South Island high country soil, comparable to the site of the present study, Jordan (2011) found a wide range of shoot concentration of P (0.11 – 0.26%), Mo (0.23 – 2.3 mg kg ⁻¹) and B (6.4 – 17.7 mg kg ⁻¹). Among the species, T repens and L. pedunculatus were near the upper part of the range for P, with concentration similar to those in the present study. Mo was much higher than the present study, but the soil had been limed in the earlier study which would have provided a supply of this element. Boron was at the lower part of the range in both these species. Foliar concentrations of nutrients in legumes are also likely to differ within the same species, largely dependent on the type of soil and its fertility (Nguyen et al. 2020). Gounden et al. (2018) collected several species of Trifolium from different localities, and recorded large differences in Fe, Ca, and Mn. The process of symbiotic N fixation (Liu et al. 2018), requires the interplay of several variables involving rhizobial communities (Tan et al. 2015). These include the specificity and extent of rhizobial infection (Andrews and Andrews 2017), root nodule development (Schwember et al. 2019) and other factors such as mycorrhizal associations (Sprent and James 2007), all interacting with multiple nutrient availability in soil and uptake by legumes and grasses (e.g. Becana et al. 2018).

不同豆科植物物种之间的叶片微量元素浓度存在天然差异。例如，Jordan（2011）在盆栽试验中将12种豆科植物（包括9种Trifolium和Lotus pedunculatus）种植于与本研究地点相当的南岛高地土壤中，发现地上部P（0.11 – 0.26%）、Mo（0.23 – 2.3 mg kg ⁻¹）和B（6.4 – 17.7 mg kg ⁻¹）浓度范围很宽。在这些物种中，T repens和L. pedunculatus的P浓度接近该范围的上限，与本研究中的浓度相近。Mo浓度远高于本研究，但早期研究中的土壤曾施用石灰，这会提供该元素的供应。这两个物种的硼浓度均处于该范围的下限。豆科植物叶片养分浓度在同一物种内也可能存在差异，这在很大程度上取决于土壤类型及其肥力（Nguyen et al. 2020）。Gounden et al.（2018）从不同地点采集了多种Trifolium，并记录到Fe、Ca和Mn存在较大差异。共生固氮过程（Liu et al. 2018）需要涉及根瘤菌群落的多个变量相互作用（Tan et al. 2015）。这些变量包括根瘤菌侵染的特异性和程度（Andrews and Andrews 2017）、根瘤发育（Schwember et al. 2019）以及菌根共生等其他因素（Sprent and James 2007），它们均与土壤中多种养分的有效性以及豆科植物和禾草对养分的吸收相互作用（例如Becana et al. 2018）。

Undoubtedly, at the site of the present study there would be significant spatial variability in a range of soil nutrients associated with soil development, altitude, slope, aspect, erosion, vegetation cover and stock activity. However, this would be unlikely to explain differences in above-ground concentrations of nutrients recorded between legumes and grasses. Every species that was sampled when growing singly or in combination was within 3 m of each other. Furthermore, all replicates for each species pair were collected within a maximum land area of approximately 100 m ². The sampling procedure involved identifying

毫无疑问，在本研究地点，与土壤发育、海拔、坡度、坡向、侵蚀、植被覆盖和牲畜活动相关的多种土壤养分存在显著的空间变异。然而，这不太可能解释豆科植物与禾草之间所记录的地上部养分浓度差异。每一个单独生长或组合生长时采样的物种彼此相距均在3 m以内。此外，每个物种组合的所有重复均在最大约100 m ²的土地面积内采集。采样程序包括先确定

significate differences were recorded. Histogram bars are means ± standard deviations. Different letters separately indicate significant differences (P < 0.05)

显著差异的元素。柱状图为平均值 ± 标准差。不同字母分别表示差异显著（P < 0.05）

Vol:. (1234567890)Vol:. (1234567890)

centration in (A) legume spp. when growing with companion grasses, and (B) grass spp. when growing with companion legumes.

浓度：（A）与伴生禾草共同生长的豆科植物，以及（B）与伴生豆科植物共同生长的禾草。

(A) Legumes（A）豆科植物

(B) Grasses（B）禾草

locations containing each species combination, then immediately sampling adjacent patches where each species was growing alone, providing direct comparisons between plants growing alone and with companion species. It is unlikely the measured differences could be accounted for by spatial variability, although this probably explains the high variability of data about the means. Nutrients can be patchy (e.g. Emeterio et al., 2021) and soils are impacted by random historic occurrences that include organic input from animals. However, in the present study, the important characteristic they have in common is deficiencies of the same range of nutrients. The significance of the recorded differences between plants growing alone and with companion species is associated with the replicated paired comparisons.

包含各物种组合的地点，然后立即对相邻的各物种单独生长的斑块进行采样，从而直接比较单独生长与伴生物种共同生长的植物。所测得的差异不太可能由空间变异来解释，尽管空间变异很可能是数据围绕均值高度变异的原因。养分分布可能呈斑块状（例如Emeterio et al., 2021），且土壤受到包括动物有机输入在内的随机历史事件的影响。然而，在本研究中，这些土壤的重要共同特征是缺乏同一系列养分。单独生长与伴生物种共同生长的植物之间所记录差异的显著性与重复配对比较相关。

Plant growth is influenced by multiple stressors; for example drought rather than soil nutrients would be the main limitation to plant growth during summer. Intraspecific competition in monospecific patches is likely to also play a significant role affecting nutrient uptake. Another consideration in this study is whether preferential grazing influenced the recorded differences between plants growing alone and those with companion species. The high country farm is fenced into large grazing blocks, each typically 100 + ha in size; the blocks that were sampled are all extensively grazed by sheep but also visited by several wild mammalian pests including rabbits and deer. Studies of compensatory growth in response to grazing (the compensatory continuum hypothesis) have provided some evidence that soil nutrient availability may affect compensatory growth by grazed plants (Wise and Abrahamson 2005; Venter et al. 2021). In studies of rotational grazing of fertile farmed grasslands, it is known that sustained defoliation of vegetation beyond its capacity to regrow subsequently degrades productivity. In the present study, preferential grazing of the legumes would undoubtedly deplete the available nutrient pool for the grasses, but the legume would then have more requirement for trace elements from the grasses. This certainly could be the start of the mechanistic explanation.

植物生长受多种胁迫因子的影响；例如，夏季限制植物生长的主要因素是干旱而非土壤养分。单一物种斑块中的种内竞争也可能在影响养分吸收方面发挥重要作用。本研究的另一个考虑因素是选择性采食是否影响了单独生长植物与伴生物种共同生长植物之间所记录的差异。该高地农场用围栏划分为大型放牧区块，每块面积通常在100 ha以上；所采样的区块均由羊进行粗放放牧，但也有包括兔和鹿在内的多种野生哺乳类有害动物出没。有关放牧补偿性生长的研究（补偿连续体假说）提供了一些证据，表明土壤养分有效性可能影响被采食植物的补偿性生长（Wise and Abrahamson 2005; Venter et al. 2021）。在肥沃农牧草地的轮牧研究中，已知持续超出植被再生能力的刈割会随后降低生产力。在本研究中，豆科植物被选择性采食无疑会耗竭禾草可利用的养分库，但豆科植物随后会对来自禾草的微量元素有更多需求。这很可能是机理解释的起点。

Native plants that fix N are largely lacking in New Zealand’s grassland flora; brooms are one of only a few exceptions, together with a small number of woody shrubs (e.g. Discaria toumatou, Rhamnaceae and Sophora spp., Fabaceae). The amount of N cycled was much less before vigorous N-fixing plants were introduced (Wardle 1991). In low fertility soils, it is well established that legume-grass assemblages are more productive than grassland without N-fixing plants (e.g. Berenji et al. 2017). Legumes have a higher demand than grasses for P, S and other trace elements essential for N2 fixation (Caradus 1980; Yuvaraj et al. 2020). However, many grass species have been shown to activate fixed phosphorus in the soil by releasing organic acid root exudates (Li et al. 2003, 2014). This obviously provides scope for neighbouring N-fixing plants and grasses to exchange mobilised soil nutrients. Unravelling the likely explanations for changes in patterns of nutrient uptake was discussed in an earlier paper (Zhang et al. 2022c).

新西兰草地植物区系中基本缺乏固氮本土植物；金雀花是少数例外之一，此外还有少数木本灌木（例如Discaria toumatou，鼠李科；以及Sophora spp.，豆科）。在引入强固氮植物之前，氮的循环量要少得多（Wardle 1991）。众所周知，在低肥力土壤中，豆科-禾草组合比没有固氮植物的草地生产力更高（例如Berenji et al. 2017）。豆科植物对P、S以及N2固定所必需的其他微量元素的需求高于禾草（Caradus 1980; Yuvaraj et al. 2020）。然而，已有研究表明许多禾草物种可通过分泌有机酸根系分泌物活化土壤中的固定态磷（Li et al. 2003, 2014）。这显然为相邻的固氮植物与禾草交换被活化的土壤养分提供了空间。关于养分吸收模式变化的可能解释，已在早期论文中进行了讨论（Zhang et al. 2022c）。

The present study showed benefits to Carmichaelia in terms of acquisition of a range of nutrients, corresponding with declining concentration of several elements in companion grasses that support the hypothesis of this study. The genus Carmichaelia contains about 30 species, all but one from New Zealand, although only a handful of species extend into the high country (Mark 2012). Rhizobial symbionts have been described for some species (Tan 2014; Tan et al. 2013) and there is evidence from chronosequences that native brooms provide N benefits to coexisting plant species and in soil and ecosystem development in (Bellingham et al. 2001; Lagerstrom et al. 2011). There is, however, far more research on an exotic Cytisus scoparius (Scotch broom), which is highly invasive and widespread in New Zealand, including montane shrubland and tussock grasslands (Bellingham and Coomes 2003), and of which more is known of its effect on soil N (Drake 2011; Broadbent et al. 2017). Little attention has been given to modification of soil biogeochemistry by native species. Legumes including brooms provide better nutrition than grasses by stock, but they are also preferentially grazed, suggesting this a possible example of how a threatened endemic species could provide a valuable component of pastoral grassland in the high country, even though grazing potentially threatens their resilience and conservation.

本研究表明，Carmichaelia在获取多种养分方面受益，同时伴生禾草中多种元素的浓度下降，这支持了本研究的假设。Carmichaelia属约有30个种，除一种外均产自新西兰，但仅有少数几个种分布至高地（Mark 2012）。已有研究描述了部分物种的根瘤菌共生体（Tan 2014; Tan et al. 2013），并有来自时间序列的证据表明，本土金雀花为共存植物物种提供氮素益处，并在土壤和生态系统发育中发挥作用（Bellingham et al. 2001; Lagerstrom et al. 2011）。然而，针对外来种Cytisus scoparius（苏格兰金雀花），的研究要多得多，该物种入侵性极强，在新西兰分布广泛，包括山地灌丛和丛生草地（Bellingham and Coomes 2003），人们对其对土壤N的影响了解得也更多（Drake 2011; Broadbent et al. 2017）。本土物种对土壤生物地球化学的改变则很少受到关注。包括金雀花在内的豆科植物为牲畜提供的营养优于禾草，但它们也会被选择性采食，这表明这可能是一个受威胁特有物种能够成为高地放牧草地有价值组分的例子，尽管放牧可能威胁其韧性和保护。

Lotus pedunculatus also received nutritional benefits from companion grasses. A marked effect of higher foliar nutrient concentrations of eight nutrient elements including N by Lotus when growing with its two companion species was evident. This legume develops a dense superficial underground system of roots and rhizomes, although above-ground recovery from defoliation is slow and it thrives only under light grazing pressure (Espie 1987). Old rhizomes breakdown in winter and spring but later propagate new discrete plants. This species thrives better than Trifolium repens on acid soils with low P (Stewart and Charlton 2006), but is generally considered to have a lesser effect than clovers on the growth of companion grasses (Nordmeyer and Davis 1977). The findings of the present study suggests that Lotus may provide a good example of a relationship between exotic legume and a native grass that is beneficial for grazing and stock production, and also to conservation of native species. Foliar concentrations of N and three key trace elements (Zn, Cu and Mo) were enhanced in snow tussocks at higher parts of the altitude range when growing together with Lotus.

Lotus pedunculatus同样从伴生禾草中获得了营养益处。Lotus与其两种伴生物种共同生长时，包括N在内的8种养分元素的叶片浓度明显升高。这种豆科植物形成致密的浅层地下根和根茎系统，但刈割后地上部分恢复缓慢，仅在轻度放牧压力下才能旺盛生长（Espie 1987）。老根茎在冬季和春季分解，但随后会繁殖出新的独立植株。该物种在低P酸性土壤上的生长优于Trifolium repens（Stewart and Charlton 2006），但一般认为其对伴生禾草生长的影响小于三叶草（Nordmeyer and Davis 1977）。本研究结果表明，Lotus可能是外来豆科植物与本土禾草之间关系的一个良好范例，这种关系既有利于放牧和牲畜生产，也有利于本土物种的保护。在海拔范围的较高处，雪丛草与Lotus共同生长时，其叶片中N和3种关键微量元素（Zn、Cu和Mo）的浓度均有所提高。

The present study did not provide similar evidence to show that Trifolium repens benefited from associations with any of the grasses, apart from improved concentrations of P and Mn when growing with Festuca novae-zelandiae. Supply of P is critical to P fixation (Liu et al. 2018). Manganese improves drought tolerance in legumes, being required for degradation of ureide, an acyl derivative of urea, which otherwise inhibits N fixation (Purcell et al. 2000). F. novae-zelandiae was the most widespread native grass in lower altitudes of the sampling area and is typical of dry and windy locations in South Island. An early study found that Poa colensoi has VA mycorrhizal association, but the other two tussocks do not (Crush 1973). The relationship between different species of grasses requires further field investigation to support the finding of earlier pot experiments (Zhang et al. 2022b, 2022c). In view of the long history of attempts to establish different species of annual and perennial clovers in the New Zealand hill county, this requires more research.

本研究未能提供类似证据表明Trifolium repens从与任何禾草的共生中受益，但与Festuca novae-zelandiae共同生长时P和Mn浓度有所提高。P的供应对P固定至关重要（Liu et al. 2018）。锰可提高豆科植物的耐旱性，因为它是降解脲类化合物（ureide，一种尿素的酰基衍生物）所必需的，否则脲类化合物会抑制固氮（Purcell et al. 2000）。F. novae-zelandiae是采样区较低海拔处分布最广的本土禾草，是南岛干燥多风地区的典型物种。早期一项研究发现，Poa colensoi具有VA菌根共生，而另外两种丛草则没有（Crush 1973）。不同禾草物种之间的关系需要进一步的田间研究，以支持早期盆栽试验的结果（Zhang et al. 2022b, 2022c）。鉴于在新西兰丘陵地区尝试建立不同种类一年生和多年生三叶草已有很长历史，这一问题需要更多研究。

In the two earlier ex situ studies (Zhang et al. 2022a, 2022c), elevated concentrations of nutrients in legumes often corresponded with lower concentrations of the same nutrients in grasses but, in the present study, there appeared to be less evidence this was the case. Without vegetation yield data from the sampling locations it is not possible to estimate the total mass of each nutrient extracted from the soil. However, mass balance calculations in the earlier studies showed that combinations of species enhanced overall exploitation of nutrients from defined volumes of soil, providing evidence of transgressive overyielding (Zhang et al. 2022a, 2022c). Undoubtedly, differences between studies can be attributed to differences between species in terms of requirements and rhizosphere biogeochemistry. Further study is required of the most significant species combinations that potentially could be managed to improve pasture productivity and to allow native species to be restored and sustained within this agricultural matrix.

在早期的两项异位研究中（Zhang et al. 2022a, 2022c），豆科植物中养分浓度的升高往往对应着禾草中同种养分浓度的降低，但在本研究中，这一现象的证据似乎较少。由于缺乏采样点的植被产量数据，无法估算从土壤中提取的各养分的总量。然而，早期研究中的质量平衡计算表明，物种组合提高了对一定体积土壤中养分的总体利用，为超产效应（transgressive overyielding）提供了证据（Zhang et al. 2022a, 2022c）。毫无疑问，不同研究之间的差异可归因于物种在养分需求和根际生物地球化学方面的差异。对于那些有可能通过管理来提高牧场生产力、并使本土物种得以在这一农业基质中恢复和维持的最重要物种组合，还需要进一步研究。

6Conclusion结论

The findings of the present work have shown that facilitation between species plays a role in nutrient procurement from soil in New Zealand’s hill country grasslands. This points to a requirement for more detailed studies into the combined influence of mixed plant species on multiple nutrient availability in soil, and for better mechanistic explanations. There are synergies between legumes, grasses and other coexisting plant species that optimise acquisition of deficient chemical elements from soil. This extends to a range of nutrients in addition to N. Clearly, there is variability between species and species combinations, but we have provided evidence of improved uptake of P, K, S and Mn, also extending to six other elements.

本研究结果表明，物种间的促进作用在新西兰丘陵草地从土壤获取养分的过程中发挥作用。这表明需要更深入地研究混合植物物种对土壤中多种养分有效性的综合影响，并提出更好的机理解释。豆科植物、禾草和其他共存植物物种之间存在协同作用，可优化对土壤中缺乏的化学元素的获取。这种作用不仅限于N，还涉及一系列其他养分。显然，物种之间以及物种组合之间存在差异，但我们已提供证据表明P、K、S和Mn的吸收得到改善，且这种改善还延伸至另外6种元素。

Earlier reported work on facilitation of nutrient uptake between plant species has largely focussed on agricultural intercropping systems (e.g. Li et al. 2014) making similar linkage between P acquisition with phytosiderophores and Fe, Zn and Mn. Mechanistic explanations for facilitation are also well known in Western Australia flora (Lambers 2014). The present study provides similar insights into low fertility high country grasslands in New Zealand. These grasslands originated from oversown, invasive and naturalised exotic species that have become established and maintained within large expanses of native vegetation, for the purpose of providing more productive fodder for stock. The novelty of the present findings is to introduce the concept of facilitation into these novel native ecosystems. These grasslands have high economic value for agriculture, but also exceptional conservation value as they contain the largest proportion of the endemic species of New Zealand.

早期有关植物物种间养分吸收促进作用的研究主要集中于农业间作系统（例如Li et al. 2014），并建立了P获取与植物铁载体以及Fe、Zn和Mn之间的类似联系。促进作用的机理解释在西澳大利亚植物区系中也广为人知（Lambers 2014）。本研究为新西兰低肥力高地草地提供了类似的认识。这些草地起源于补播、入侵及已归化的外来物种，这些物种在大面积本土植被中定植并得以维持，目的是为牲畜提供生产力更高的饲草。本研究结果的新颖之处在于将促进作用的概念引入这些新型本土生态系统。这些草地具有很高的农业经济价值，同时也具有特殊的保护价值，因为其中包含了新西兰比例最大的特有物种。

Novel native plant community assemblages in this agroecological mosaic represent a potential opportunity to refine pasture management by exploiting combinations of plant species that facilitate optimal exploitation of nutrients, with less reliance on fertilisers. Furthermore, informing ecological knowledge of the role of nutrient acquisition in the origin and maintenance of biodiversity in grassland is an additional outcome of this research. Incorporating more native species into this mid-altitude pastoral landscape would provide undoubted benefits to protection of biodiversity through land sharing. Generally, however, native plants have little resilience to or protection against ruminants, whether or not they are preferentially grazed. Prior to relatively recent human arrival in New Zealand, the endemic flora evolved and existed largely without fertile soils and in the absence of mammals. Native brooms provide one of only a small number of legumes that provide an obvious nutrition contribution to grazers through fixing N. Otherwise, native species persist in contemporary pastoral grassland occasionally through their physical defences, as in golden spaniard, or though being a secondary choice for grazing, as in snow tussocks. Nonetheless, grasses and other species that are less desirable from an agricultural perspective clearly play a facilitation role in nutrient procurement by species that are more desirable for agriculture or conservation. Combinations of plants enhance the acquisition of key soil nutrients. These findings justify more attention to enhancement rather than restriction of plant species diversity in the vegetation matrix of the New Zealand hill country.

在这一农业生态镶嵌体中，新型本土植物群落组合为优化牧场管理提供了潜在机遇，即利用能促进养分最佳利用的植物物种组合，减少对肥料的依赖。此外，增进对养分获取在草地生物多样性起源和维持中所起作用的生态学认识，也是本研究的另一成果。在这一中海拔放牧景观中引入更多本土物种，将通过土地共享为生物多样性保护带来毋庸置疑的益处。然而，一般而言，无论是否被选择性采食，本土植物对反刍动物几乎没有抵御力或保护机制。在人类相对较晚抵达新西兰之前，特有植物区系在很大程度上是在缺乏肥沃土壤且没有哺乳动物的条件下演化和生存的。本土金雀花是少数几种通过固氮为食草动物提供明显营养贡献的豆科植物之一。除此之外，本土物种在当代放牧草地中得以存续，有时是依靠物理防御（如金色刺芹），有时则是因为其作为放牧的次要选择（如雪丛草）。尽管如此，从农业角度看不太理想的禾草和其他物种，在对农业或保护更有价值的物种获取养分方面显然发挥着促进作用。植物组合可增强对关键土壤养分的获取。这些结果表明，应更加重视在新西兰丘陵地区植被基质中增加而非限制植物物种多样性。

Becana M, Wienkoop S, Matamoros MA (2018) Sulfur Transport and Metabolism in Legume Root Nodules. Front Plant Sci 9:1434

Becana M, Wienkoop S, Matamoros MA (2018) Sulfur Transport and Metabolism in Legume Root Nodules. Front Plant Sci 9:1434

Bellingham PJ, Coomes DA (2003) Grazing and community structure as determinants of invasion success by Scotch broom in a New Zealand montane shrubland. Divers Distrib 9:19–28

Bellingham PJ, Coomes DA (2003) Grazing and community structure as determinants of invasion success by Scotch broom in a New Zealand montane shrubland. Divers Distrib 9:19–28

Bellingham PJ, Walker LR, Wardle DA (2001) Differential facilitation by a nitrogen-fixing shrub during primary succession influences relative performance of canopy tree species. J Ecol 89:861–875

Bellingham PJ, Walker LR, Wardle DA (2001) Differential facilitation by a nitrogen-fixing shrub during primary succession influences relative performance of canopy tree species. J Ecol 89:861–875

Berenji S, Moot DJ, Moir JL, Ridgway H, Rafat A (2017) Dry matter yield, root traits, and nodule occupancy of lucerne and Caucasian clover when grown in acidic soil with high aluminium concentrations. Plant Soil 416:227–241

Berenji S, Moot DJ, Moir JL, Ridgway H, Rafat A (2017) Dry matter yield, root traits, and nodule occupancy of lucerne and Caucasian clover when grown in acidic soil with high aluminium concentrations. Plant Soil 416:227–241

Bork EW, Gabruck DT, McLeod EM, Hall LM (2017) Five- Year Forage Dynamics Arising from Four Legume-Grass Seed Mixes. Agronomy 109:2789–2799

Bork EW, Gabruck DT, McLeod EM, Hall LM (2017) Five- Year Forage Dynamics Arising from Four Legume-Grass Seed Mixes. Agronomy 109:2789–2799

Broadbent AAD, Orwin KH, Peltzer DA, Dickie IA, Mason NWH, Ostle NJ, Stevens CJ (2017) Invasive N-fixer Impacts on litter decomposition driven by changes to soil properties not litter quality. Ecosystems 20:1151–1163

Broadbent AAD, Orwin KH, Peltzer DA, Dickie IA, Mason NWH, Ostle NJ, Stevens CJ (2017) Invasive N-fixer Impacts on litter decomposition driven by changes to soil properties not litter quality. Ecosystems 20:1151–1163

Brower AL, Harding MAC, Head NJ, Walker S (2020) South Island high country: let’s get it right this time. N Z J Ecol 44:3405

Brower AL, Harding MAC, Head NJ, Walker S (2020) South Island high country: let’s get it right this time. N Z J Ecol 44:3405

Caradus JR (1980) Distinguishing between grass and legume species for phosphorus use. N Z J Agric Res 23:75–81

Caradus JR (1980) Distinguishing between grass and legume species for phosphorus use. N Z J Agric Res 23:75–81

Crush JR (1973) Significance of endomycorrhizae in tussock grassland in Otago, New Zealand. NZ J Bot 11:645–660

Crush JR (1973) Significance of endomycorrhizae in tussock grassland in Otago, New Zealand. NZ J Bot 11:645–660

Crush JR, Lee JM, Cosgrove GP, Rossi L, Chapman DF, Ste-

Crush JR, Lee JM, Cosgrove GP, Rossi L, Chapman DF, Ste-

Acknowledgements The research team are grateful to the Miss E.L. Hellaby Indigenous Grasslands Research Trust for grant funding to support Zhang Wei for his PhD stipend and operational funds. Special thanks also to Dasom Jeon, Shyam Provost and Emily Huang for practical support.

致谢 研究团队感谢Miss E.L. Hellaby Indigenous Grasslands Research Trust提供资助，用于支持Zhang Wei的博士生津贴及研究经费。同时特别感谢Dasom Jeon、Shyam Provost和Emily Huang提供的实际帮助。

Authors’ contribution All authors contributed to the planning and execution of the project, and to manuscript preparation. Zhang Wei carried out the practical work and data analysis as part of his PhD programme supervised by Nicholas Dickinson, Thomas Maxwell and Brett Robinson. Nicholas Dickinson is responsible for the final manuscript draft.

作者贡献 所有作者均参与了项目的规划与实施以及论文的撰写。Zhang Wei在Nicholas Dickinson、Thomas Maxwell和Brett Robinson指导下，作为其博士研究的一部分完成了实验工作和数据分析。Nicholas Dickinson负责论文终稿。

Funding This study was supported by Lincoln University and the Miss E.L. Hellaby Indigenous Grasslands Research Trust.

基金资助 本研究由林肯大学和Miss E.L. Hellaby Indigenous Grasslands Research Trust资助。

Data availability Lincoln University Data Repository.

数据可用性 林肯大学数据存储库。

Code availability Not applicable.

代码可用性 不适用。

Declarations声明

Conflict of interest There are no conflicts of interest.

利益冲突 不存在利益冲突。

7References参考文献

Andrews M, Andrews ME (2017) Specificity in Legume- Rhizobia Symbioses. Int J Mol Sci 18:705

vens DR (2018) Foliar micronutrient concentrations of eight perennial ryegrass (Lolium perenne L.) cultivars grown in four regions in New Zealand. N Z J Agric Res 61:301–311

DOC (2006) Conservation Resources Report on Tenure Review of Mount Grand Pastoral Lease. (Department of Conservation, PAL 14–04–349d), Land Information New Zealand, Wellington

Drake DC (2011) Invasive legumes fix N2 at high rates in riparian areas of an N-saturated, agricultural catchment. J Ecol 99:515–523

Duncan R, Lucas R, Palmer C (1997) Mt Grand Station: Baseline Survey of the Vegetation and Soils. Lincoln University, New Zealand, Department of Plant Sciences

Duncan RP, Webster RJ, Jensen CA (2001) Declining plant species richness in the tussock grasslands of Canterbury and Otago, South Island, New Zealand. N Z J Ecol 25:35–47

Emeterio S, Duran M, Canals RM (2021) Relating the spatial distribution of a tall-grass to fertility islands in a temperate mountain grassland. Soil Biol Biochem 163:108455

Espie PR (1987) Edaphic ecology of Festuca novae-zelandiae,

Lotus pedunculatus and Trifolium repens on Craigieburn high country yellow-brown earth & related soils. PhD thesis, Lincoln College, New Zealand

Gounden T, Moodley R, Jonnalagadda SB (2018) Elemental analysis and nutritional value of edible Trifolium (clover) species. J Environ Sci Health B 53:487–492

Hendrie DL, Moir JL, Boitt G, Simpson ZP, Condron LM (2021) Investigating the relationships between soil

acidity and phosphorus fractions in high country farmland of New Zealand’s South Island. Soil Research 59:463–471

Jordan PR (2011) Response of 12 Pasture legumes to phosphorus and lime additions when grown in a high country soil under glasshouse conditions. Bachelor of Agricultural Science, Honours thesis, Lincoln University, New Zealand

Lagerstrom A, Bellingham PJ, Bonner KI, Wardle DA (2011) The effect of simulated herbivory on growth and nutrient status of focal and neighbouring early successional woody plant species. Oikos 120:1380–1392

Li L, Tang C, Rengel Z, Zhang F (2003) Chickpea facilitates phosphorus uptake by intercropped wheat from an organic phosphorus source. Plant Soil 248:297–303

Li L, Tilman D, Lambers H, Zhang FS (2014) Plant diversity and overyielding: insights from belowground facilitation of intercropping in agriculture. New Phytol 203:63–69

Liu AL, Contador CA, Fan KJ, Lam HM (2018) Interaction and Regulation of Carbon, Nitrogen, and Phosphorus Metabolisms in Root Nodules of Legumes. Front Plant Sci 9:1860 Mark AF (2012) Above the Treeline: A Nature Guide to Alpine New Zealand. Craig Poton Publishing, Nelson

Maxwell TMR, Moir JL, Edwards GR (2016) Grazing and Soil Fertility Effect on Naturalized Annual Clover Species in New Zealand High Country. Rangel Ecol Manage 69:444–448

Maxwell TMR, Moir JL, Edwards G (2010) Influence of environmental factors on the abundance of naturalised annual clovers in the South Island hill and high country. New Zealand Grassland Association 72:165–169

Molloy L (1998) Soils in the New Zealand Landscape: the Living Mantle. Soil Science Society, New Zealand

Nguyen TD, Andrews M, Ley TWS, Dash D, Petterson M, Weir BS, Morton JD, Black AD, Lucas RJ (2020) Caucasian clover (Trifolium ambiguum) specific rhizobia persist in low and high fertility soils in the South Island of New Zealand. N Z J Agric Res 63:332–340

Nordmeyer AH, Davis MR (1977) Proc. N.Z. New Zealand Grassland Association 38:119–125

Parfitt RL, Stevenson BA, Ross C, Fraser S (2014) Changes in pH, bicarbonate-extractable-P, carbon and nitrogen in soils under pasture over 7 to 27 years. N Z J Agric Res 57:216–227

Purcell LC, King CA, Ball RA (2000) Soybean cultivar differences in ureides and the relationship to drought tolerant nitrogen fixation and manganese nutrition. Crop Sci 40:1062–1070

Rissman AR, Daniels MC, Tait P, Xing X, Brower AL (2021) Conservation and privatization decisions in land reform of New Zealand’s high country. Environ Conserv 48:165–173

Schipper LA, Mudge PL, Kirschbaum UF, Hedley CB, Golubiewski NE, Smail SJ, Kelliher FM (2017) A review of soil carbon change in New Zealand’s grazed grasslands. N Z J Agric Res 60:93–118

Schwember AR, Schulze J, del Pozo A, Cabeza RA (2019) Regulation of Symbiotic Nitrogen Fixation in Legume Root Nodules. Plants-Basel 8:333

Scrimgeour FG (2016) Pathways ahead for New Zealand hill country farming. Journal of New Zealand Grasslands 78:73–82

Sprent JI, James EK (2007) Legume Evolution: where do nodules and mycorrhizas fit in? Plant Physiol 144:575–581

Stats^NZ (2021) Agricultural and horticultural land use. Retrieved 24 Jan, 2022, from https:// www. stats. govt. nz/ indic ators/ agric ultur al- and- horti cultu ral- land- use.

Stewart AV, Charlton JFL (2006) Pasture and forage plants of New Zealand, 3rd edn. New Zealand Grassland Association, New Zealand Grassland Trust

Tan HW (2014) Characterisation of Rhizobia Associated with New Zealand Native Legumes (Fabaceae) and a Study of Nitrogen Assimilation in Sophora microphylla. PhD thesis, Lincoln University, New Zealand.

Tan HW, Heenan P, Ridgway H, Andrews M (2013) The New Zealand alpine endemic Montigena novae-zelandiae (Fabaceae) shares rhizobial symbionts with Carmichaelia and Clianthus. NZ J Bot 51:297–307

Thom ER (2016) Proceedings of the Hill Country Symposium. New Zealand Grassland Association, Dunedin.

Tozer K, Douglas G, Dodd M, Muller K (2021) Vegetation options for increasing resilience in pastoral hill country. Frontiers in Sustainable Food Systems 5:550334

Trotter C, Tate K, Scott N, Townsend J, Wilde H, Lambie S, Marden M, Pinkney T (2005) Afforestation/reforestation of New Zealand marginal pasture lands by indigenous shrublands: the potential for Kyoto forest sinks. Ann for Sci 62:865–871

Venter ZS, Hawkins HJ, Cramer MD (2021) Does defoliation frequency and severity influence plant productivity? The role of grazing management and soil nutrients. African Journal of Range and Forage Science 38:141–156

Wardle P (1991) Vegetation of New Zealand. Cambridge University Press

Wise MJ, Abrahamson WG (2005) Beyond the compensatory continuum: environmental resource levels and plant tolerance of herbivory. Oikos 109:417–428

Yuvaraj M, Pandiyan M, Gayathri P (2020) Role of legumes in improving soil fertility status. In: Hasanuzzaman M (ed) Legume crops-prospects, production and uses. Intechopen, pp 17–25

Zhang W, Maxwell T, Robinson B, Dickinson N (2022a) Grasses procure key soil nutrients for clovers. Nature Plants 8:923–929

Zhang W, Maxwell T, Robinson B, Dickinson N (2022b) Plant Species Complementarity in Low-Fertility Degraded Soil. Plants 11:1370

Zhang W, Maxwell T, Robinson B, Dickinson N (2022c) Legume nutrition is improved by neighbouring grasses. Plant Soil 475:443–455

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