# Soil fertility and landscape surrounding former arable fields drive the ecological resilience of Mediterranean dry grassland plant communities

Renaud Jaunatre, Elise Buisson, Elsa Leborgne, Thierry Dutoit

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Renaud Jaunatre, Elise Buisson, Elsa Leborgne, Thierry Dutoit. Soil fertility and landscape surrounding former arable fields drive the ecological resilience of Mediterranean dry grassland plant communities. Frontiers in Ecology and Evolution, 2023, 11, pp.1_10. 10.3389/fevo.2023.1148226. hal-04108831

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EDITED BY
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Hungarian Academy of Sciences, Hungary

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José Antonio Molina,
Complutense University of Madrid, Spain
Panayiotis G. Dimitrakopoulos,
University of the Aegean, Greece
Florian Delerue,
Institut Polytechnique de Bordeaux, France

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Renaud Jaunatre

renaud.jaunatre@inrae.fr

RECEIVED 19 January 2023

ACCEPTED 08 May 2023

PUBLISHED 26 May 2023

CITATION

Jaunatre R, Buisson E, Leborgne E and Dutoit T (2023) Soil fertility and landscape surrounding former arable fields drive the ecological resilience of Mediterranean dry grassland plant communities.

Front. Ecol. Evol. 11:1148226.
doi: 10.3389/fevo.2023.1148226

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© 2023 Jaunatre, Buisson, Leborgne and Dutoit. This is an open-access article distributed under the terms of the [Creative Commons Attribution License (CC BY)](https://creativecommons.org/licenses/by/4.0/). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

# Soil fertility and landscape surrounding former arable fields drive the ecological resilience of Mediterranean dry grassland plant communities

Renaud Jaunatre¹*, Elise Buisson², Elsa Leborgne¹,² and Thierry Dutoit²

¹Université Grenoble Alpes, INRAE, LESSEM, Saint-Martin-d'Hères, France, ²IMBE, Avignon University, CNRS, IRD, Aix Marseille University, IUT, Avignon, France

**Introduction:** Semi-natural dry grasslands are among the species-richest and most diverse habitats in Europe especially in the Mediterranean Basin. They evolved with long-term severe environmental constraints, either biotic (e.g., grazing or mowing) or abiotic (e.g., dryness or oligotrophy). Their recovery after sever anthropogenic disturbance, such as cultivation is often very slow and incomplete. A deeper understanding of the processes driving the recovery would be of great benefit to better restore or conserve these grasslands. We used the filter model as a framework to assess the relative importance of dispersion, abiotic and biotic filters as drivers of this recovery.

**Methods:** We studied the medium-term dynamics of 37 Mediterranean dry grassland plant communities after an episode of cultivation in the plain of La Crau (Southern France) by two census: after 25 years of abandonment, and revisited 10 years later (35 years of abandonment). Our aims were to characterize the temporal medium-term dynamics of these communities, to measure their taxonomic resilience and to identify the drivers. We performed structural equation modeling to measure the importance of the various drivers, with cover of remnant dry grasslands surrounding each studied community as a proxy for the dispersion filter, soil pH and phosphorus content as proxies for the abiotic filter and cover of the most dominant species as a proxy for the biotic filter.

**Results and Discussion:** Our results show that former arable field vegetation do not recover after more than 40 years. The three filters drive the recovery of dry grassland vegetation: former arable fields that have lower phosphorus content (abiotic filter) have a lower cover of dominant species (biotic filter), a higher species richness and a higher similarity with remnant dry grassland plant communities, especially if the former arable fields are surrounded by remnant dry grasslands (dispersion filter).

KEYWORDS

old field, secondary succession, resilience, plant community, dry grassland

## 1. Introduction

Impacts of land-use changes, notably abandonment of intensive agriculture, are a major topic in conservation biology (Stoate et al., 2009). The conversion from intensive cultivation to extensive grasslands often raises the issue of ecosystem ability to recover their pre-cultivation state of semi-natural species-rich grasslands (Cramer and Hobbs, 2012). This is an important
topic as ecosystems recovering after cultivation will cover more than 4 billion ha in the next decades (including both grasslands and forests; Hurtt et al., 2011). Secondary succession is an essential concern in plant ecology (Cramer et al., 2008; Cramer and Hobbs, 2012), not only for theoretically-driven studies (Connell and Slatyer, 1977; Prach and Walker, 2011; Seabloom et al., 2020), but also for conservation and restoration perspectives (Luken, 1990; Walker et al., 2007; Suding, 2011; Rapson, 2023).

Species-rich grasslands are rarely resilient to severe anthropogenic disturbances (Helm et al., 2019; Nerlekar and Veldman, 2020; Buisson et al., 2022). They are composed with species that developed strategies to survive in moderately stressed and/or disturbed environment (i.e., xericity, grazing, mowing, combined or not) but not to recover after severe disturbance (Herben et al., 2018), such as intensive arable cultivation which involve soil disturbance as well as nutrient, herbicide and pesticide additions. In order to restore these degraded ecosystems it would be useful to better understand the drivers of recovery (i.e., their relative importance, their magnitude and directions). These drivers could then be used as levers that practitioners can modify.

Processes have been linked to theoretical models in order to summarize how communities assemble (Keddy, 1992; Lortie et al., 2004; Vellend, 2016). Most of these models are structured by filters that constrain community composition starting from a regional species pool. The first filter is dispersion: species have to be able to disperse and reach the community. This ability depends both on the landscape matrix and on the dispersability of species found in adjacent areas (Gibson and Brown, 1991; Pärtel and Zobel, 1999; Lindborg and Eriksson, 2004; Herault and Thoen, 2009). The second is the abiotic filter: species have to be able to germinate, grow and reproduce under given environmental conditions, and this ability depends on each species physiological capability (Kraft et al., 2015). The last one is the biotic filter: the occurrence and nature of biotic interactions alter the first two filters either by enhancing their mesh (sensu White and Jentsch, 2004), e.g., by increasing dispersion or by facilitating growth or establishment in limiting environmental conditions; or by reducing their mesh, e.g., by competitive exclusion (Bruno et al., 2003; Lortie et al., 2004). The aim of this paper is to disentangle the effect of dispersion, abiotic and biotic filters in driving the recovery of species-rich dry grassland plant communities after decades of intensive cultivation abandonment.

In this study, we measured diversity and composition recoveries in 35 and 45 year-old former arable fields in Mediterranean semi-natural species-rich dry grasslands and we have a hypothesis for each filter. The amount of remnant ecosystem in the surrounding of the former arable fields was used as a proxy of the dispersion filter as it provides a seed source for species occurring in the dry grassland. Our hypothesis was that its importance was rather low in driving plant communities. It is indeed widely recognized that most of the species from dry grasslands do not produce a permanent seed bank or seed that disperse on large distances (Graham and Hutchings, 1988; Buisson et al., 2006; Török et al., 2018; Arruda et al., 2021). Considering the size of the former arable fields (>100,000 m²) and the fact that most of the species do not colonize more than a few meters after decades (Buisson and Dutoit, 2004, 2006), these species are not expected to disperse to the whole area of each former arable fields, whatever the amount of remnant ecosystem in the surroundings. Two soil variables that were modified during former cultivation episode were used as proxies for the abiotic filter: one is related to fertility (phosphorus content) and the other is not directly

related to soil fertility (soil pH). Phosphorus is one of the most important abiotic drivers of grassland community assembly (Yang et al., 2022). It is also known to remain in soil decades after fertilized cultivation, contrary to potassium or nitrogen (Smits et al., 2008; Jaunatre et al., 2016; Saatkamp et al., 2021). Ploughing which scraped the underlying calcareous conglomerate (Römermann et al., 2005), changed soil chemistry, increasing CaO, CaCO3 and pH. We thus selected pH as a proxy of these changes, as they may prevent the plant community to recover the composition of remnant dry grasslands [e.g., pH contributes to explain plant species distribution (Dubuis et al., 2013)]. Our hypotheses were that soil pH would influence plant community composition as soil pH is also a soil physical-parameter integrative of others changes than chemical fertility (i.e., increase of Ca and CaCO3 contents) while phosphorus content would decrease diversity through an increase in competition (Janssens et al., 1998; Palpurina et al., 2019). The biotic filter may depend on the abiotic characteristics (Belyea, 2004). During former arable field recovery, plant species have to face dense cover of ruderals or opportunistic species (Baeten et al., 2009; Öster et al., 2009). Hence, we used the dominant species cover as an indicator of potential competition in former arable fields and thus as a proxy of the biotic filter. Our hypothesis was that phosphorus content would drive the dominant species cover which itself would drive the plant community diversity. We also hypothesized that high composition recovery would only occur when species richness has recovered. The composition of the community could indeed be different from that of the remnant dry grasslands if the number of species is lower.

We monitored vegetation on 37 former arable field plots and 10 remnant dry grassland plots (in 2009 and in 2019), respectively 35 and 45 years after cultivation abandonment. We also characterized soil physico-chemical parameters on each plot and the landscape in the surroundings of each plot. In order to link the different drivers of plant community assembly we performed a structural equation modeling for each date were filter proxies were explanatory variables and vegetation diversity and composition were response variables.

# 2. Materials and methods

## 2.1. Site description

The La Crau area is a large dry grassland in southeastern France (ca. 10,000 ha; c. 43°33' N, 4°52' E; Figure 1) that has been shaped by (i) a Mediterranean climate with mean annual temperature of 15°C, a variable annual sum of precipitation between 400 and 600 mm concentrated in autumn, 4 months of summer drought, and more than 110 days with a >50 km.h-1 wind; (ii) 40 cm deep soil composed with about 50% of siliceous stones overlaying a calcareous conglomerate layer, making the alluvial water table unreachable by the roots of plants and (iii) itinerant sheep that have grazed the area over the past several 1000 years (Devaux et al., 1983; Buisson and Dutoit, 2006). This has led to a unique and species-rich plant community composed mainly by a high number of annuals yet dominated in biomass by perennials, such as *Brachypodium retusum* Pers. and *Thymus vulgaris* L. Most of the species occurring in La Crau area are species adapted to extensive grazing, xeric and oligotrophic conditions. This community characterizes the remnant ecosystem in this study (i.e., that has been grazed for millennia but that has not undergone any disturbance due to cultivation) and will henceforth be referred to as dry grasslands. The
<figure><img src="image_3.png" /><figcaption>FIGURE 1</figcaption></figure>

Map of the La Crau area in 2023. Remnant dry grasslands habitats are shown in grey. Colored large circles are remnant dry grasslands plots whereas colored small squares are former arable field plots. The different geographical areas are discriminated by different colors that are used in the ordination plot (Figure 4).

60,000 ha of original dry grasslands was characterized by relatively homogeneous vegetation composed only of different micro-patterns due to particular soil conditions and difference in sheep grazing regimes (Martin et al., 2022), before being fragmented by various severe anthropogenic disturbances, in particular, cultivation (Devaux et al., 1983; Buisson and Dutoit, 2006). Melon cultivation occurred in the La Crau area between 1971 and 1988. This cultivation implied soil disturbance, plant mortality and fertilizers application. Most of the fields

have been subsequently abandoned; they now contain various plant communities dominated by *Anisantha* species (Römermann et al., 2005).

## 2.2. Site selection

Mapping based on aerial photographs enabled us to identify more than 220 areas that (i) appear as dry grasslands on the earliest
photographs available (1947); (ii) show evidence of cultivation in
later photographs (1955–1971–1975–1978–1979–1984–1988); and
(iii) were abandoned between 1978 and 1988. After abandonment, all
these areas were grazed again with the same intensity as the remnant
dry grasslands. To avoid the introduction of an additional source of
variability, we focused only on former open-field melon cultivation
and not on large plastic tunnel fields that left less-disturbed trackways
between the tunnels (Römermann et al., 2005). Thirty-seven of these
Former Arable Fields, hereafter called FAF, were chosen and are
spatially randomly distributed. The distance between any two sampled
sites varies between 100 m and 20.9 km (Figure 1).

## 2.3. Vegetation sampling

Vegetation sampling was carried out at the center of each of the 37 FAF and of 10 dry grassland areas from all geographical zones of the La Crau area (Figure 1) in 2009 and in 2019, by the same team of botanists. On each FAF and remnant dry grassland areas, we monitored the vegetation in three 4 m² quadrats at the tips of an 11 m side triangle. A Braun-Blanquet coefficient (Braun-Blanquet et al., 1952) was given to all plant species recorded and then transformed into percentage according to Guinochet (1973; 5: 87.5%, 4: 62.5%, 3: 37.5%, 2: 17.5%, 1: 5% and +: 0.1%). To avoid biases in abundance attributions, we transformed these percentages into relative percentage to the total vegetation cover. By doing so, we keep abundance hierarchy but we lever the potential overlap between species cover by constraining the sum of abundances into the total vegetation cover. We used species richness (alpha diversity) and similarity to the remnant dry grassland communities (composition) as response variables. The similarity to the remnant dry grassland communities was calculated as 1 – the minimum Bray-Curtis distance (Bray and Curtis, 1957) with the remnant dry grassland plot communities. We used the minimum Bray-Curtis distance instead of the average value in order to reduce the effect of the heterogeneity of remnant dry grassland vegetation. This similarity index with remnant dry grassland communities was thereafter referred as composition.

## 2.4. Explanatory variables

### 2.4.1. Remnant dry grassland cover

We used remnant dry grassland percent cover within a 900 m radius circle around the centre of each field as a proxy of dispersion potential. Map of remnant dry grassland areas was provided by the national reserve environmental managers (Réserve Nationale des Coussouls de Crau, Wolff et al., 2015). The 900 m radius was chosen based on preliminary analyses showing a tradeoff between (i) a smaller radius that would have caused the landscape factors to be especially influenced by the area of each field, and (ii) a larger radius that would have made the landscape factors of two fields close together almost identical. Cover were calculated using Geographical Information System software: Quantum GIS 2.18 "Las Palmas" (QGIS Development Team, 2016).

### 2.4.2. Soil analyses

We used soil analyses as a proxy of abiotic filter. For soil analyses,
in 2009 and in 2019, a subsample of 70 g of soil was gathered in each

of the three vegetation quadrats in the topsoil layer (0-10 cm) before
being pooled to obtain one 210 g soil sample for each FAF. Samples
were then sieved with a 2 mm mesh sieve. Analyses were carried out
by the INRAE (Institut National de Recherche pour l'Agriculture
l'Alimentation et l'Environnement). Phosphorus content (P2O5; Olsen
et al., 1954) and water pH were measured according to the standard
methods described in Baize (2018).

### 2.4.3. Dominance

We used the dominance as a proxy of the biotic filter. Dominance
was calculated as the sum of abundances of the four most abundant
species in each quadrat, which represented in average 45% of the sum
of all species abundances (Appendix 1).

## 2.5. Statistical analyses

All the analyses were conducted using R 4.2.2 (R Core
Team, 2022).

The alpha diversity of remnant dry grasslands and FAF were
compared using a generalized linear mixed model performed with
LME4 package (Bates et al., 2015). The kind of plant community
(remnant dry grasslands or FAF) and monitoring years were included
as fixed factors and the monitoring years and plot interaction as
random factor to take into account the repeated nature of data.

In order to describe the vegetation of dry grasslands and FAF
together, a Non-metric Multidimensional Scaling (NMDS) ordination
was performed on the vegetation matrix to ordinate quadrats
according to their plant community characteristics (Borcard et al.,
2011) with VEGAN package (Oksanen et al., 2022). We performed a
permutational analysis of variance using Bray-Curtis distance matrices
(McArdle and Anderson, 2001), with the VEGAN::ADONIS2
function. This analysis measures the difference in the position of the
centroid by groups, but may confound location and dispersion effects
(Warton et al., 2012), we therefore also performed a test of
homogeneity of group dispersion (Anderson, 2006) with the
VEGAN::BETADISPER function.

In order to understand how the variation of landscape context,
soil parameters and cover of dominant species influence the diversity
and composition (i.e., similarity to remnant dry grassland areas) of
FAF, we built a structural equation model (SEM) with PIECEWISESEM
package (Lefcheck, 2016) for each monitoring year (2009 and 2019).
This analysis, based on pathway dependence between variables, makes
it possible to identify hypothesized relationships between selected
variables (Lefcheck, 2016). We included dominance, alpha diversity
and composition as response variables and remnant dry grassland
cover, phosphorus content, pH and dominance as predictor variables
for each plot (Figure 2). We fitted the SEMs with mixed models using
the predictor variables as fixed factors and plots as random factor. For
dominance, we used a linear model, with LMERTEST package
(Kuznetsova et al., 2017), after square root transformation in order to
fulfill parametric conditions. For alpha diversity we used a generalized
linear model, with LME4 package (Bates et al., 2015), with poisson
family and log link function. For composition, we used linear model,
with LMERTEST package (Kuznetsova et al., 2017). Once fitted,
we added missing pathways if they had been highlighted by Fisher
d-separation tests (Shipley, 2013). We chose the best SEM model as
the one with no significant missing pathways and with the lowest
<figure><img src="image_4.png" /><figcaption>FIGURE 2</figcaption></figure>

Pathway diagram representing the hypotheses tested in the structural equation modelling. Each arrow represents an expected effect, positive in green and negative in red.

<figure><img src="image_5.png" /><figcaption>FIGURE 3</figcaption></figure>

Means and standard errors of species-richness (4 m²) for 2009 and 2019 in remnant dry grasslands and former arable field plots (GLMM; z=-2.49, *p*=0.013). “NS” indicated that the effect was not significant and “*” that it was with a *p* value between 0.05 and 0.01 according to a generalized linear mixed model.

difference of dispersion (F1 = 88.98; *p* < 0.001). Some FAFs are indeed embedded within remnant dry grassland vegetation and characterized by species, such as *Brachypodium retusum* P. Beauv., *Thymus vulgaris* L., *Medicago* spp. and *Trifolium* spp. while others are still discriminated from the remnant dry grasslands and are characterized by the dominance of more ruderal type species for the Crau area, such as *Lobularia maritima* (L.) Desv., *Anisantha madritensis* (L.) Nevski or *Clinopodium nepeta* (L.) Kuntze.

According to the best fitted SEM, 2 out of 6 hypothesized relationships were confirmed for 2009 and 2019: the negative relationship between dominance and alpha diversity and the positive relationship between alpha diversity and composition (Figures 5, 6). The hypothesized negative relationship between pH and composition was confirmed in none of the models. Other relationships depended on the monitoring year. Phosphorus content was positively correlated (although non significantly) with dominance in 2009 and negatively correlated with alpha diversity in 2019. The remnant dry grassland cover had a positive relationship with composition in 2019 only. Surprisingly, a negative relationship that was not included in our a priori hypotheses was identified as missing pathways by Fisher d-separation tests (Shipley, 2013) between remnant dry grassland cover and dominance in 2009 (Figure 5).

# 4. Discussion

As reported in many studies that have focused on plant community resilience (Tomanek et al., 1955; Bonet and Pausas, 2004; Jaunatre et al., 2016; Helm et al., 2019; Isbell et al., 2019), even more than 30 years after disturbance, the species richness of the plant communities that colonized the disturbed sites are still lower than, and the composition is still considerably different from, those from the remnant dry grasslands. When we disentangle the different drivers of vegetation, we first notice that in 2009 phosphorus content and remnant dry grassland cover in the surroundings increase the abundance of the most dominant species in the FAF (e.g., *Anisantha* spp.). This dominance appears to reduce alpha diversity which itself drives the composition (i.e., a lower species richness leads to a lower similarity to the remnant dry grasslands). We then note that in 2019 while alpha diversity is reduced by dominance, it is also reduced by phosphorus content. Finally, we measured that while composition is driven by alpha diversity, it is also driven by the cover of dry grasslands in the surroundings (i.e., a higher cover of remnant dry grasslands in the surrounding leads to a higher similarity with these dry grasslands). It is therefore interesting to stress that the three filters play an

Akaike information criterion by at least 2 units (AIC; Akaike, 1974; Burnham and Anderson, 2004; Appendix 1).

# 3. Results

In total, 172 plant species were recorded: 156 in 222 FAF quadrats (37×3×2 quadrats) and 127 in 60 remnant dry grassland quadrats (10×3×2 quadrats). Despite the high number of species in common between remnant dry grasslands and FAF plots, mean species richness was significantly higher in remnant dry grassland areas than in FAFs (38.6±0.9 vs. 31.1±0.5; *z* = -2.49, *p*=0.013; *Figure 3*). There was however neither an effect of monitoring year (*z*=0.292; *p*=0.771) nor an effect of interaction between year and location (*z* = -0.011; 0.992).

There were no clear tendencies for the composition trajectories between 2009 and 2019 (Figure 4), although there is a significant year effect on the position of the centroid (F1 = 15.06; *p* < 0.001) with no difference of dispersion (F1 = 0.16; *p*=0.686). On the contrary, remnant dry grasslands and FAF have a significantly different position of centroids (F1 = 24.25; *p* < 0.001) associated with a significant
<figure><img src="image_6.png" /><figcaption>FIGURE 4</figcaption></figure>

Remnant dry grasslands (filled circles, 10 sites × 3 plots × 2 years) and FAF (filled squares, n = 37 FAF × 3 plots × 2 years) ordination based on NMDS of plant community composition, final stress=0.28. For clarity purpose, only the 30 most correlated species are shown (out of 172). Arrows link 2009 plots to 2019 plots. Points with the same colors are located within the same geographical zones (Figure 1).

<figure><img src="image_7.png" /><figcaption>FIGURE 5</figcaption></figure>

2009 survey pathway diagram of the best fitted SEM illustrating how dominance, alpha diversity and composition are influenced by remnant dry grasslands cover, phosphorus content, pH and dominance. Boxes represent responses and predictor variables. Only included links in this model are drawn with arrows (green if the relationship is positive and red if negative). Dotted arrows represent links that were not included in our a priori hypotheses but were added after looking for missing pathways by Fisher d-separation tests (Shipley, 2013). Numbers on arrows are the slope estimates, accompanied or not with stars (*p<0.05; **p<0.01; ***p<0.001).

important role in driving the vegetation recovery, but not with the
same processes.

Surprisingly, the dispersion proxy (remnant dry grassland
cover) switched from being negatively correlated with dominance
in 2009 to being positively correlated with composition in 2019.
A possible explanation of this result, is that when remnant dry
grassland cover is low, cultivated area or former arable field
covers are high. Differential dispersal limitation can cause wide
species-specific deviations in the probability of finding a species
from the landscape species pool in the community (Grace, 2001).
Fields surrounded by cultivated areas or former arable fields may
therefore exhibit a higher abundance of anemochorous ruderal
species like Anisantha spp. that are known to exhibit higher
dispersion abilities (Gaba et al., 2017). Ten years later, the
presence of remnant dry grasslands in the vicinity promotes a
composition more similar to the dry grassland. It is well known

that presence of remnant patches in the vicinity promotes the
dispersal of remnant dry grassland species to the community
(Tansley and Adamson, 1925) and that this effect increases with
time (Cook et al., 2005). We had not hypothesized a high
importance of remnant patches as most of the species from dry
grasslands do not disperse on large distances due to the low
quantity of seeds from remnant communities in the seed bank
and the seed rain (Graham and Hutchings, 1988; Buisson and
Dutoit, 2004; Török et al., 2018; Arruda et al., 2021). Nevertheless,
on the long term (over 30 years), long distance dispersion events
(i.e., hundreds of meters) with low probability (i.e., which was
not detected by sampling design) can occur (Higgins and
Richardson, 1999) and may be favored by the presence of remnant
patches in the vicinity. This is supported by the fact that FAF tend
to differ from each other in patterns similar to those of the dry
grasslands. Such patterns are also observed on secondary
<figure><img src="image_8.png" /><figcaption>FIGURE 6</figcaption></figure>

2019 survey pathway diagram of the best fitted SEM illustrating how dominance, alpha diversity and composition are influenced by remnant dry grasslands cover, phosphorus content, pH, and dominance. Boxes represent responses and predictor variables. Only included links in this model are drawn with arrows (green if the relationship is positive and red if negative). Numbers on arrows are the slope estimates, accompanied or not with stars (*p<0.05; **p<0.01; ***p<0.001).

succession in abandoned mining sites in Central Europe (Jírová et al., 2012). However, the design of our study does not allow us to differentiate whether this pattern is a result of the dispersion or the abiotic filters. A more in depth spatial characterization of the remnant dry grasslands would be required to disentangle the effect of the species-pool it provides and the abiotic spatial organization. In order to thoroughly tackle the dispersion filter, numerous census of occurring species would be required as well as the correspondence with dispersal traits of these species (Lewis et al., 2016).

The pH does not appear to exert an effect on composition, which was not expected by our hypotheses. We expected higher changes due to the calcareous conglomerate that was broken during the cultivation phase (Buisson and Dutoit, 2004) and therefore lower composition recovery of plant community compared to remnant dry grasslands that contains some acidophilous species (Devaux et al., 1983). The range of variation of pH was however rather low: 6.9 and 7.2 being, respectively, the first and third quartiles. If relationship between pH and composition should occur, a higher range of variation would be require to detect it. Phosphorus content has first a positive relationship with dominance and then with species richness. Higher fertility leads to higher biomass of annual grasses (higher dominance) that should have increased competition (Michalet et al., 2023). Nutrient enrichment does not prevent remnant dry grassland species development in itself but enhances competition of more generalist species due to their dense cover (Huenneke et al., 1990; Buisson et al., 2015). Sowing typical remnant dry grassland species in FAF abiotic conditions or in remnant dry grassland abiotic conditions does not influence their establishment (Coiffait-Gombault et al., 2012). Our results show that species richness is limited both by biotic (dominance) and abiotic (phosphorus content) filters that interact together. This is in accordance with previous studies that show that dominance by more competitive and ruderal species on soil with higher nutrient contents can lead to a decline of remnant community species (Yurkonis and Meiners, 2004; Seabloom et al., 2020). Apart from the important feedback with the abiotic filter, the biotic filter is complicated to take into account. In our study, we only focused on the dominance of the above ground vegetation. The competition between plants may also be tackled by measurement of functional trait patterns, but inferring competition processes from these patterns may sometimes be misleading (Münkemüller et al., 2020). Besides intra guild competition, there

is also below ground interactions (Kiær et al., 2013), facilitative interactions (Brooker et al., 2007), soil microfauna (Sun et al., 2023), microbial communities (Kaisermann et al., 2017), etc. We are currently able to measure the importance of these trophic network in the driving of ecosystem functioning (Martinez-Almoyna et al., 2022), but it is still very difficult to disentangle all the direct and indirect interactions that could lead to the favoring or (dis)favoring of specific set of species.

We studied the recovery on the vegetation composition having as reference, remnant patches of remnant dry grassland vegetation (i.e., extensively grazed vegetation). Considering the vegetation dynamics that we measured after several decades of recovery, it is unlikely that these plant communities will converge toward remnant dry grassland vegetation on the medium term. As was shown in previous studies, dozens of decades after abandonment, the composition is still different from the remnant ecosystems (Jaunatre et al., 2016, for species-rich dry grassland; Nerlekar and Veldman, 2020 for various grasslands). For such non-resilient species-rich grasslands, reconstructive restoration (i.e., ending degradation, active remediation of substrate condition and reintroduction of major proportion of target biota sensu Atkinson and Bonser, 2020) would be needed to ensure a potential complete recovery of plant communities. Our result confirm the fact that the restoration of abiotic conditions prior to forcing the dispersion of target species would be a key for successful restoration.

Our results show that FAF vegetation did not recover after more than 30 years. The three filters drive the recovery of remnant dry grassland vegetation: FAF that have lower phosphorus content (abiotic filter) have a lower cover of dominant species (biotic filter), a higher species richness and a higher similarity with remnant dry grassland plant communities, especially if the FAF are surrounded by remnant dry grasslands (dispersion filter). Based on these results we therefore recommend that the restoration of species-rich semi-natural remnant dry grasslands is primarily focused on the recovery of suitable abiotic conditions [i.e., by decreasing fertility, for instance with expensive topsoil removal (Hölzel and Otte, 2003; Jaunatre et al., 2014), repeated carbon addition (Corbin and D'Antonio, 2004; Ossanna and Gornish, 2023) or long-term phosphorus mining (Schelfhout et al., 2015)] and on increasing propagule pressure of the typical remnant dry grassland species in a second phase. In order to be able to use SEM, we only used a few variables that we attributed to the three filters. These variables were chosen regarding the specific characteristics of the degradation and of the remnant ecosystem. Our study is a piece into the
comprehension of the relative importance of each filters that would benefit from both similar analyses in other ecosystems but also more in depth measure of how the propagule pressure and the abiotic characteristics drive interaction between species and therefore plant community recovery.

## Data availability statement

The original contributions presented in the study are included in the article/Supplementary material, further inquiries can be directed to the corresponding author. Code and data are also publicly available at https://forgemia.inra.fr/renaud.jaunatre/friches_frontiers.

## Author contributions

RJ, EB, and TD conceived the design of this study. RJ performed the data analysis and wrote the first draft of the manuscript. All authors contributed to floristic surveys and approved the final version.

## Funding

This study was supported by the CDC Biodiversité, CEN PACA, the Réserve Naturelle des Coussouls de Crau, the Conseil Régional de Provence Alpes Côtes d'Azur, and CNRS RTP Ingecotech funding.

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## Acknowledgments

The authors would like to thank Jennifer Matwyschuk and Daniel Pavon (IMBE) for help with fieldwork.

## Conflict of interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

## Publisher's note

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.

## Supplementary material

The Supplementary material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fevo.2023.1148226/full#supplementary-material

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