Invasive weed disrupts facilitation of nutrient uptake in grass-clover assemblage

Highlights

● Nutrient constraints in low-fertility soil were modified by different species combinations.

● Grass-clover assemblages benefited both species in terms of nutrient procurement.

● Interplay of competition and facilitation is demonstrated.

● An invasive weed removed essential nutrients from the grazing cycle.

Abstract

To investigate the interplay of competition and facilitation between plants in low-fertility pasture grasslands of New Zealand, we compared nutrient uptake and acquisition of key nutrients of three species from different functional groups. Combinations of Pilosella officinarum (mouse-eared hawkweed, an invasive weed), Trifolium repens (white clover, a nitrogen fixer) and Dactylis glomerata (cocksfoot, a pasture grass) were planted into a soil with low-to-deficient concentrations of key nutrients. Highest yields were achieved by the grass growing alone but, when the clover and grass had grown together, there were complementary benefits in terms of procurement of a wide range of nutrients from soil despite lower root biomass. The invasive weed negated these benefits, and soil nutrients were exploited less efficiently when Pilosella had grown alone or in a mixture with the other species. Competition from the weed removed the benefits of grass-legume coexistence. These findings are interpreted to suggest that requirements for legumes to be the main source of nitrogen in pasture grasslands may be compromised unless competitive weeds are controlled to avoid disrupted procurement of key nutrients. It is likely these constraints to nutrient procurement would similarly impact conservation grasslands.

Graphical abstract

Keywords

soil fertility / facilitation / species coexistence / weed invasion / legumes

1 Introduction

Pastoral grasslands in New Zealand were developed for sheep farming only within the last two centuries, with exotic species of grasses and legumes introduced to improve productivity (Laidlaw, 2014; Bork et al., 2017). Excluding the intensively fertilised and irrigated lowlands, nearly a third of the land area is at higher altitudes that support most of the extensively managed grasslands where exotic and native species co-exist to varying extents (Wardle, 1991; StatsNZ, 2021; Yao et al., 2022). This presents a somewhat unique challenge of maintaining and improving productive pasture (Thom, 2016; Caradus et al., 2021), particularly by increasing the legume component of the pasture (Maxwell et al., 2016), while also protecting indigenous grasslands for conservation (Rissman et al., 2021; Tozer et al., 2021). Most of these soils naturally have low pH and low fertility, particularly in terms of phosphorus, sulfur, molybdenum and boron (Hendrie et al., 2021). An additional confounding factor is that these grasslands are frequently impacted by exotic pasture grasses and other weeds that are less desirable for forage. Invasive weeds also threaten native plant diversity (Duncan et al., 2001; Sage et al., 2009). Sustainability or improvement of plant assemblages in these grasslands undoubtedly requires a better understanding of the factors that influence the coexistence of species and susceptibility of this habitat to invasion by weeds (Sage et al., 2009). Elsewhere, for example in nutrient-poor meadows of Central Europe, the declining occurrence of plant species has been explained by a combination of elevated soil nutrients and invasive competitive species (Hockendorff et al., 2021). In the present paper, with a focus on New Zealand grasslands, we report the findings of a study of the ability of plants to procure limiting plant nutrients from soil constrained by nutrient deficiencies. Using a pot experiment, we investigate the apparently contrasting roles of competition and facilitation.

Competition between plants for resources is known to be an important driver of species diversity and processes of vegetation change in terms of complimentary resource use (Burrows, 1990; Yao et al., 2022), shaping both the structure and dynamics of plant communities (Klinerova and Dostal, 2020). Exotic plants become invasive through adaptations that are better suited to local or modified environmental conditions, in New Zealand’s grasslands as elsewhere (Buddenhagen et al., 2022). However, in broader terms, competition also allows coexistence when each species can dominate in at least one combination of abiotic and biotic variables at any particular location (Rebele, 2000). In low fertility grasslands, species abundance is regulated by competition for soil nutrients (Mamolos et al., 1995); it appears to be the case that differing competitive abilities between species should be viewed as being compatible in terms of allowing diversity to be maintained (Schippers et al., 1999). An example is seen in root system structures that vary according to both dispersion patterns of soil nutrients and the presence of competitive plants (Craine, 2006) which suggests some degree of complementarity between species.

The role of complementarity or facilitation between species in grassland plant communities is best known in the context of legume-grass mixtures (Annicchiarico et al., 2015). Atmospheric nitrogen (N) fixed by rhizobial symbionts in the root nodules of legumes spills over in soil to facilitate improved growth of neighboring grasses (Lüscher et al., 2014). This beneficial effect may also result in transgressive overyielding in which the combined herbage yield exceeds that of the most productive of these species growing in monocultures (Sturludóttir et al., 2014). In intercropping systems, nutritional benefits within the rhizospheres of combinations of plant species extend beyond N to provide better access to phosphorus and improved uptake of a range of trace elements from the soil leading to increased productivity (Li et al., 2014). Our own earlier studies on low-fertility grassland pasture found that grasses provide reciprocal nutritional benefits to legumes by supplying key nutrients that are required for N fixation (Zhang et al., 2022a). Thus, when grasses and clovers grow together in unfertilized grassland, more nitrogen is procured by both species, and other limiting plant nutrients in the soil are better utilized (Zhang et al., 2022b). This type of complementarity between species effectively shares the differing abilities of each species to procure limiting nutrients from the soil (Zhang et al., 2022c).

The aim of the present study was to quantify nutrient acquisition by plants from soil, using three species with differing functional traits that are commonly found growing together in low fertility grasslands. We compared combinations of a pasture grass, an invasive weed and a clover grown in different combinations in a soil with defined elemental deficiencies. Our hypothesis was that appropriation of nutrients by the more competitive invasive weed might curtail the development of a beneficial relationship between the grass and clover.

The three species of plants used in this experimental work were all exotic species that have become naturalised in New Zealand. Species of Pilosella (hawkweeds) are prevalent invasive weeds, widely naturalised over more than 500 000 ha of the South Island, particularly in hill country tussock grasslands (Scott et al., 2001). Once established, Pilosella spreads rapidly and outcompetes other species (Rinella and Sheley, 2002; Williams and Holland, 2007). It is quite easy to see the repellent effect that Pilosella has on other species, sometimes with a visual halo of bare ground surrounding its dense mats. Dactylis glomerata (cocksfoot) is a common and widespread perennial species of pasture grass that was naturalised in New Zealand in the mid-19th century. In our earlier experimental studies, D. glomerata consistently provided evidence of the facilitation of nutrient procurement as a companion species to other plants. Trifolium repens (white clover) is the most common legume planted or oversown into grassland in New Zealand and worldwide (Annicchiarico et al., 2015). It has stolon and petiole traits that enhance its capacity to spread and forage (Annicchiarico et al., 2019), although a decline in the abundance and diversity of clovers has been associated with increasing N supplies (Tognetti et al., 2021).

2 Materials and methods

Pilosella officinarum (syn. Hieracium pilosella, mouse-ear hawkweed) was collected from a non-agricultural site at McLeans Island near Christchurch. This species is a small perennial rosette-forming herbaceous plant that often uses stolons and rhizomes to form interconnecting plants in dense clumps, growing particularly in grasslands, including tussock grasslands, with low to moderate fertility (see the website: New Zealand Plant Conservation Network). Both D. glomerata and T. repens were collected from paddocks on the Lincoln University campus.

Individual plants of P. officinarum, tillers of D. glomerata and plantlets of T. repens were transplanted into low nutritional potting mix in 3.5 L plastic pots (diameter 15 cm, height 20 cm), either alone or in combination with individuals of one or both of the other species. The basic potting medium contained no peat or other sources of organic matter. One plant of each species was used. The nutrient content of the soil was routinely analyzed at a commercial laboratory. Each of the seven treatments (Pilosella alone; Trifolium alone; Dactylis alone; Pilosella and Trifolium; Pilosella and Dactylis; Trifolium and Dactylis; Pilosella and Dactylis and Trifolium) had five replicates. Pots were randomly arranged in a single-block design on a bench in unheated glasshouse with ambient sunlight and were watered sparingly to maintain adequate soil moisture for growth. Soil moisture kept approximately the same in the different treatments. The experiment was set up in December 2021 (early summer) and plants were harvested after two months. Aboveground biomass was harvested, sorted into separate species, oven-dried (65°C, 48 h) then weighed. Roots were carefully separated from the soil, washed, and dried in the same way. All plant samples were then finely ground and microwave-digested in 5 M HNO₃ before nutrient analysis. Nitrogen was analyzed using an Elementar Rapid Max N Elemental Analyzer and other nutrients were analyzed by ICP-OES following the standard method. Data not normally distributed were log-transformed before analysis. Differences between means were determined using one-way ANOVA, with a post-hoc Fisher LSD test. All analyses were conducted using Minitab 19.

3 Results

The growth medium was low to deficient in several key elements (Tab.1) including available concentrations of N, P and key trace elements. Species growing alone produced more biomass, as would be expected (Fig.1), which was a particularly large difference for the grass. The presence of Pilosella was detrimental to growth of Dactylis and Trifolium in both 2- and 3-species combinations. Pilosella and Trifolium produced the same total yield per pot whether they had grown singly or together (Fig.2), although the total biomass produced in pots was higher when Pilosella had grown in mixtures with Dactylis rather than when it had grown alone. There were no significant differences in above-ground pot yields in the presence of Dactylis, whether it was growing alone or in any combination with other species, although root biomass was lower when this species grew with Trifolium.

Tab.1 Significant determinants of fertility in the soil used in the pot experiment, with typical ranges in agricultural soils in New Zealand.

Analysis	Units	Concentration	Typical range*
pH [1]	pH Units	6	5.2−6.5
Electrical Conductivity (EC) [2]	mS cm−1	0.3	0.5−1.8
Nitrate-N [3]	mg L−1	5	20−80
Ammonium-N [4]	mg L−1	2	1−20
Phosphorus [5]	mg L−1	6	5−20
Sulphur [5]	mg L−1	10	10−20
Potassium [5]	mg L−1	35	20−80
Calcium [5]	mg L−1	13	30−70
Magnesium [5]	mg L−1	12	7−25
Sodium [5]	mg L−1	14	5−40
Iron [6]	mg L−1	27.6	20−50
Manganese [6]	mg L−1	15.6	1−15
Zinc [6]	mg L−1	1.88	0.3−10.0
Copper [6]	mg L−1	0.48	0.4−10.0
Boron [6]	mg L−1	0.11	0.1−0.65

*Typical range for agricultural soils in New Zealand. Method: [1] 1:1.5 (v/v) Water extraction followed by potentiometric pH determination. In-house. [2] 1:1.5 (v/v) Water extraction followed by potentiometric conductivity determination (25°C). In-house. [3] 1:1.5 (v/v) Water extraction followed by Salicylate colorimetry. In house. [4] 1:1.5 (v/v) Water extraction followed by Berthelot colorimetry. In house. [5] 1:1.5 (v/v) Water extraction followed by ICP-OES. In-house. [6] 2 mM DTPA extraction (Australian Standard 3743-1989) followed by ICP-OES. In-house.

Fig.1 Individual plant species yields when each species was growing alone or in a mixture with other species. Symbols are means ± s.d. Letters indicate significant differences (p<0.05) within each block.

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Fig.2 Total pot biomass (aboveground and underground, n = 5). Histogram bars are means + standard deviations. Values are means ± s.d. Letters showing significant differences (p < 0.05) refer to shoots and roots separately.

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In each of the three species there were some significant differences in foliar nutrient concentrations when they had grown together with other species (Tab.2). Pilosella had higher concentrations of Ca and Mg when it had grown with Trifolium but lower foliar concentrations of N, P and B when it had grown with Dactylis. Trifolium had higher Zn but lower Ca when growing with Dactylis than when growing alone, and higher K but less Ca when growing with Pilosella. Dactylis had more N, and Cu when growing with Trifolium.

Tab.2 Foliar nutrient concentrations (mg kg−1) in Pilosella (A), Trifolium (B) and Dactylis (C) when each of these species had grown as single species or together with the other species (n = 5).

Species/combinations	N (%)	P	K	Ca	Mg	S	Fe	Mn	Zn	Cu	B	Mo	Ni
(A)
Pilosella	2.06ab	4040a	32800ab	7300b	2840b	3560ab	307a	80.8a	46.7a	5.29a	71.1a	0.90ab	0.95a
With Trifolium	2.40a	4150a	37200a	8650a	3340a	4170a	290a	102a	52.8a	4.62a	70.5a	1.22a	0.78a
With Dactylis	1.60c	3150b	29700b	7230b	2790b	3020b	349a	74.1a	51.5a	5.47a	54.6ab	0.64b	0.81a
With 2 spp.	1.84bc	2950b	34900ab	7070b	2800b	3450ab	304a	90.2a	48.3a	4.92a	48.5b	0.76b	0.79a
(B)
Trifolium	3.38ab	2770a	28600b	12800a	3720a	3490b	415a	60.3a	25.5b	4.84ab	27.7a	2.66a	0.85a
With Dactylis	3.88a	4280a	37700b	13100a	3670a	4650a	150a	43.6a	32.9a	4.96a	28.2a	3.58a	0.43b
With Pilosella	3.05ab	3910a	48300a	9450b	3660a	5020a	142a	43.8a	30.1ab	3.61b	28.1a	4.84a	0.49ab
With 2 spp.	2.59b	4000a	38400ab	12100a	3350a	5170a	191a	62.3a	29.3ab	4.58ab	28.7a	2.98a	0.66ab
(C)
Dactylis	0.88b	1660ab	25700ab	2380a	1530ab	3260ab	95.3a	78.5a	22.9ab	3.13b	4.17a	0.89b	0.81a
With Trifolium	1.30a	2010a	31300a	2350a	1850ab	4760a	99.9a	90.1a	30.9a	4.68a	4.41a	2.40a	0.87a
With Pilosella	1.01ab	1910ab	28800ab	2630a	1910a	4430ab	83.9a	77.5a	27.5ab	4.04ab	4.96a	1.77ab	1.14a
With 2 spp.	0.97ab	1390b	21100b	2050a	1360b	3010b	77.8a	65.5a	19.7b	2.83b	10.0a	1.20b	1.17a

Different letters and bold font alphanumeric indicate significant differences (p < 0.05).

In terms of mass balance (yield ×nutrient concentration), Dactylis and Trifolium mixtures procured a larger amount of eight soil nutrients from the soil than when either species was growing alone or with Pilosella (Tab.3), but this was not significantly different when all three species had grown together.

Tab.3 Total pot nutrient uptake (units shown below) into foliage of Trifolium, Dactylis and Pilosella when they were growing either alone or in mixtures with other species (n = 5).

Species/combinations	N (g)	P (mg)	K (mg)	Ca (mg)	Mg (mg)	S (mg)	Fe (µg)	Mn (µg)	Zn (µg)	Cu (µg)	B (µg)	Mo (µg)	Ni (µg)
Pilosella	0.07b	13.0ab	108abc	24.2bc	9.38a	11.8bc	1000a	266bc	152ab	17.3a	242a	3.02b	3.15bc
Trifolium	0.11ab	8.41b	90.0c	43.7ab	12.8a	11.1c	1790a	203c	83.2b	16.1a	90.1bc	9.33ab	3.19bc
Dactylis	0.06b	11.7ab	180ab	16.1c	10.7a	23.3abc	601a	529a	156ab	22.1a	28.7c	6.53b	5.55ab
Pilosella & Trifolium	0.06b	10.1ab	106bc	24.2bc	9.33a	11.0c	892a	195c	137ab	15.0a	144b	5.49b	2.20c
Pilosella & Dactylis	0.07b	13.6ab	165abc	25.1bc	12.8a	22.0abc	1080a	443ab	207a	25.9a	136b	7.49ab	5.92a
Trifolium & Dactylis	0.15a	16.3a	195a	49.1a	16.4a	25.0a	684a	371abc	182a	27.3a	102b	15.6a	3.20bc
All 3 spp.	0.10ab	15.0ab	181ab	36.3abc	14.4a	24.0ab	1010a	473ab	196a	25.9a	138b	9.31ab	5.85a

Different letters and bold font alphanumeric indicate significant differences (p < 0.05).

4 Discussion

Previous field-based studies in nutrient-poor grasslands have shown that biomass production is enhanced in species-rich swards (Lüscher et al., 2014). Coexistence of grasses and legumes has generally been explained in terms of differing functional traits that provided for better exploitation of light, nutrients and other resources, leading to higher yields than can be achieved by monocultures (Gaëtan et al., 2018). This was not the case in the present study in which interspecific competition was evident; all three species produced higher above ground biomass when growing alone within the confines of the pots. The highest biomass yield was achieved by the grass and in combinations of species that included the grass. However, the results demonstrate the competition for nutrients and the complementary benefits of growing clover and grass together (Fig.3). Foliar concentrations of various elements were elevated in each of the species when they were growing in combination. It is presumed that the grass acquired N from fixation by the legume (clover root nodulation was observed), but the grass also competed well against Pilosella for N, P and B. Pilosella clearly had the upper hand in acquiring Ca. The presence of the grass supplied Zn to the legume, as we have demonstrated previously (Zhang et al., 2022b). In terms of mass balance, a larger amount of N and nine other elements were transferred from soil to foliage, and this was often achieved through a smaller root biomass than when clover or grass grew alone.

Fig.3 Facilitation and competition in acquisiton of soil nutrients by the three species, based on changes in foliar nutrient concentration when the species grown either alone or combination with the other species (see Table 2).

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Mutual facilitation of nutrient procurement between the same species of grass and clover occurs through increased uptake and sharing of trace elements by the grass allows increased nitrogen fixation by the clover (Zhang et al., 2022c). Nyfeler et al. (2011) similarly found stimulatory effects from an accompanying grass on the symbiotic N fixation activity of clover, with acquisition of symbiotic N by the mixture stimulated by the grasses. This is likely to be valuable to legumes which have higher demands than grasses for P and S and other trace elements essential for N fixation, thus already creating considerable metabolic demand (Zhang et al., 2022b). Variable herbage concentrations of Ca, Mg and Na associated with graminoid and forb ground cover and different species composition has been recorded in other recent studies reported in this journal (Kajzrová et al., 2022; Kang et al., 2022). Likely mechanistic explanations in grass and clover are discussed in an earlier paper (Zhang et al., 2022a). It is possible that increased Ca (and Mg) recorded in Pilosella foliage when it had grown with clover may be due to small changes of pH in the rhizosphere altering mobility of these elements.

There was increased total foliar uptake from the fixed mass of soil of eight nutrients when Trifolium and Dactylis had grown together (Tab.3). This is likely to be a substantial practical significance. Since the 1960s in New Zealand, the role of legumes in agricultural pastures has been displaced by fertilizers, and there has been a continuing decline in the abundance and diversity of forage legumes (Laidlaw, 2014), with an 8-fold increase in N use on dairy farms from 1988 to 1994 (Harris et al., 1996) and a further 3.65-fold increase in N fertiliser sold from 1994 to 2019 (StatsNZ, 2021). In a likely reversal of this trend, it is now widely recognized that a return to increased incorporation of clovers and other legumes into grassland species mixtures will be a critical component of future sustainable agricultural pasture management, with less reliance on urea and ammonia fertilizer (Rubiales et al., 2021). However, the process of nitrogen fixation requires a supply of other key elements, as described above, and mobilising these elements in the rhizosphere appears be the role of companion grasses through facilitation.

The effects of plants on abiotic (and also biotic) soil components that in turn influence plant performance, is referred to as plant–soil feedback (PSF). Klinerova and Dostal (2020) found PSF reduced differences in competitive ability among 46 plant species. Dostál (2021) showed that nutrient addition attenuated negative PSF. If invasive weeds disrupt the acquisition of nutrients by legumes, as in the present study, there is little possibility of increasing pastoral productivity without the use of fertilisers. The additional presence of Pilosella did not alter total uptake (Fig.3) but this invasive perennial weed is likely to have captured nutrients that otherwise would circulate within the grazing system; prostrate rosettes of Pilosella multiply though stolons and can rapidly produce extensive and dense ground cover. This equated to capture of 12% to 51% of the nutrients by Pilosella (Tab.4). In the case of Zn and B, this is substantially above the 22% accounted for by biomass; these are key elements limiting N fixation and productivity in low fertility grasslands (Zhang et al., 2022b).

Tab.4 The proportion accounted for by each nutrient of total foliar uptake from the soil that was captured by Pilosella in pots containing all three species. Pilosella accounted for 22% of biomass yield.

N	P	K	Ca	Mg	S	Fe	Mn	Zn	Cu	B	Mo	Ni
25%	28%	26%	29%	29%	20%	45%	27%	41%	29%	51%	12%	18%

In a review of 39 studies of pairs of coexisting plant species, Adler et al. (2018) found that 96% of the studies featured both intraspecific competition and interspecific facilitation. They concluded these are processes that promote stable coexistence. This is likely to be applicable to low-fertility grasslands that are managed for conservation in New Zealand, particularly in the high country. However, the impact of interspecific competition from a recently introduced invasive weed, such as Pilosella in the present study, requires further consideration, particularly if its successful establishment is a consequence of environmental change. Grazing mammals were absent from New Zealand until two centuries ago, and their introduction and management has undoubtedly altered soil fertility. It is known that nutrient accumulation in soil due to grazing management can reduce the interspecific competitive ability of native plants and favor the invasion of exotic species (Ba and Facelli, 2022). This has consequences for protection of native species; increasing soil nutrients in combination with invasive competitive species has explained the declining occurrence of plants species in grasslands (Hockendorff et al., 2021).

5 Conclusions

An improved understanding of the impact of coexisting plant species on procurement and management of soil nutrients is clearly required. This represents an opportunity to refine pasture management and also to protect biodiversity in conservation grasslands. Exploiting combinations of plant species that facilitate nitrogen fixation and optimal exploitation of nutrients could reduce fertiliser requirements and enhance and protect biodiversity in pastoral grasslands. In the present study, increased foliar uptake of nutrients when Trifolium and Dactylis grew together was disrupted in the presence of Pilosella. Invasive competitive weeds may disrupt this procurement of key nutrients achieved by facilitation through complementary plant species assemblages. The impact of other biotic and abiotic environmental variables in these processes and of increased soil fertility in nutrient-poor grasslands remains poorly understood.

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Acknowledgments

The authors thank to the Miss E.L. Hellaby Indigenous Grasslands Research Trust for grant funding to support ZW for his PhD stipend and operational funds, and AGLS at Lincoln University for a Summer Scholarship for RM. Open Access funding enabled and organized by CAUL and its Member Institutions.

Conflicts of interest

The authors declare that there is no conflict of interest that could be perceived as prejudicing the impartiality of the research reported.

Data availability statement

Raw data supporting the findings of this study are available through the website Data@Lincoln. Source data are provided with this paper.

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