# Effects of ecological restoration on beetle assemblages: results from a large-scale experiment in a Mediterranean steppe rangeland

Jean François Alignan, Jean-François Debras, Renaud Jaunatre, Thierry Dutoit

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## ► To cite this version:

Jean François Alignan, Jean-François Debras, Renaud Jaunatre, Thierry Dutoit. Effects of ecological restoration on beetle assemblages: results from a large-scale experiment in a Mediterranean steppe rangeland. Biodiversity and Conservation, 2018, 27 (9), pp.2155 - 2172. 10.1007/s10531-018-1528-8. hal-01936449

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# Effects of ecological restoration on beetle assemblages: results from a large-scale experiment in a Mediterranean steppe rangeland

Jean-François Alignan<fnref n="1" />,<fnref n="2" /> Ⓒ · Jean-François Debras<fnref n="2" /> · Renaud Jaunatre<fnref n="3" /> · Thierry Dutoit<fnref n="1" />

**Abstract** Given that biological conservation cannot prevent the full range of negative impacts on biodiversity, ecological restoration is nowadays commonly acknowledged as a necessary tool for conservation purposes. Here, we report on an ecological rehabilitation project in the La Crau area (south-eastern France), beginning in 2009 when a former industrial orchard (357 ha) was rehabilitated into a Mediterranean rangeland. We assessed the effect of ecological rehabilitation and different additional restoration treatments on beetle assemblages. Seven treatments were considered: the reference steppe, the rehabilitated treatment alone, three additional experimental restoration treatments (soil transfer; nurse species seeding and hay transfer), the control and the edge between the steppe and the former industrial orchard area. All beetle families were considered. Beetles were sampled with

Jean-François Alignan
jeanfrancois alignan@gmail.com

Jean-François Debras
jean-francois.debras@inra.fr

Renaud Jaunatre
renaud.jaunatre@irstea.fr

Thierry Dutoit
thierry.dutoit@univ-avignon.fr

<footnote n="1">¹ Institut Méditerranéen de Biodiversité et d'Ecologie (IMBE), UMR CNRS IRD Aix Marseille Université, IUT site Agroparc, Avignon Université, 337 Chemin des Meinajaries BP 61207, F-84911 Avignon Cedex 09, France</footnote>

<footnote n="2">² Institut National de la Recherche Agronomique (INRA), UR 1115 Avignon/INRA PSH, Site Agroparc, 84914 Avignon Cedex 9, France</footnote>

<footnote n="3">³ Université Grenoble Alpes, Iirstea, UR EMGR, 2 rue de la Papeterie-BP 76, 38402 St-Martin-d'Hères, France</footnote>
pitfall traps for 3 years (2011–2013). Our major finding was a positive effect of soil transfer and nurse species seeding treatments, which promote the characteristic beetle composition of the reference steppe. Nevertheless, strong differences remain between the steppe and the various assessed treatments in terms of composition. Long-term monitoring should therefore now focus on particular beetle indicator species that could reflect the response of the overall characteristic beetle assemblage of the reference steppe.

**Keywords** Coleoptera · Dry grassland · Hay transfer · Nurse species seeding · Rehabilitation · Soil transfer

Introduction

Agricultural intensification and the decline of traditional land management have led to deg-
radation, fragmentation and loss of habitats (Vitousek et al. 1997; Bakker and Berendse
1999). The importance of in situ conservation of natural habitats is commonly acknowl-
edged as is the postulate that nowadays biological conservation cannot prevent the full
range of negative impacts on biodiversity (Balmford and Cowling 2006). Ecological res-
toration appears to be more than ever necessary as an in situ conservation tool allowing
for instance to speed up the recovery of degraded ecosystems (Dobson et al. 1997) or to
prevent extinction. Wilson (1992) suggested that the twenty-first century would be the cen-
tury of restoration in ecology, and this is proving true: it has become a management tool in
conservation policies, and the Convention on Biological Diversity set the target of restor-
ing at least 15% of degraded ecosystems by 2020. Whereas restoration aims for a com-
plete return to the reference ecosystem state (i.e., its structure, composition and functions),
rehabilitation aims for an intermediate state, with recovery, for instance, of one function of
the ecosystem (Aronson et al. 1993). For the associated fauna, it is usually hypothesized
that it will naturally colonize the area under rehabilitation because suitable plant communi-
ties will develop (Watts et al. 2008). However, responses to restoration measures can dif-
fer from one taxonomic group to another and there may not be sufficient information for
a reliable evaluation of conservation and for the most thorough assessment of restoration
success. Using a multi-taxonomic approach (Woodcock et al. 2008, 2010a; Alignan et al.
2014; Görn and Fischer 2015) therefore appears desirable. A multi-taxonomic approach,
particularly at the population and community scales, would also shed light on species inter-
actions among several different taxonomic groups (plant–insect interactions for instance).
This is of major importance for conservation purposes (Meffe and Carroll 1994) and for
management of communities and ecosystems. Considering invertebrates for applied sci-
ence purposes in restoration ecology and biological conservation provides theoretical
knowledge of these focal taxa in fundamental biology and ecology. This is particularly true
of certain species, about which little is known. Applied research at species level can con-
tribute insights into ecological niche, abundance, phenology (e.g., Barber et al. 2017; Bird
et al. 2017); at population level, it can link population size to species migration and disper-
sion (e.g., Audino et al. 2017); and at assemblage level, it can reveal diversity and function
in the ecosystem (e.g., Watts and Mason 2015). Thus, such large-scale studies may con-
tribute to invertebrate species conservation status and definition. The need for improving
insect conservation has recently been put forward (Leandro et al. 2017) and can be linked
to protection of habitats and ecosystems.
The Mediterranean region poses particular problems for biological conservation and restoration ecology (Blondel et al. 2010). In this region, characterized by a mild climate, demographic and urban development put strong pressure on habitats that have been protected due to a particular biotope and/or a rare, patrimonial or endemic biocenosis evolving there. Grasslands and dry grasslands are among these threatened habitats. Throughout the world, grasslands have suffered degradation through intensification of agriculture, land abandonment, land conversion to other uses or destruction by civil engineering (Muller et al. 1998; Wallis de Vries et al. 2002). Due to their open and often flat land physiognomy, they have been over-exploited by humans until they have become some of the most degraded habitats (Huston 2005). Since these habitats are steadily vanishing in central Europe, they have received attention in restoration ecology, as the degradations they suffer are often beyond their resilience capacity (Muller et al. 1998).

The La Crau area is a dry grassland ecosystem (steppe-like ecosystem) located in south-eastern France that, mainly due to human activities such as cultivation, industrial and military activities, suffered at the beginning of the twenty-first century from a drastic reduction in surface area (from originally about 60,000 to now 10,000 ha), threatening ecosystem persistence (Buisson and Dutoit 2006). Research aimed at preserving biodiversity through the conservation and restoration of this dry grassland habitat can provide keys to the conservation and restoration of grassland habitats in general. Such knowledge is particularly important for the other ecosystems in the Mediterranean Basin similar to La Crau area both in terms of herbaceous plant community structure and ecological processes (like Dehesa in Spain, Montado in Portugal or the semi-arid steppes of North Africa) (Buisson and Dutoit 2006; Dutoit et al. 2013a). Among the different grassland attributes and biodiversity groups needing to be preserved, grasslands are known to be a diverse habitat sheltering many arthropod species (Wallis de Vries et al. 2002).

Arthropods account for the largest part of global biodiversity (Kremen et al. 1993) and deserve greater consideration in conservation studies. Moreover, a decline of more than 75% in total flying insect biomass in protected areas over the last 27 years has recently been proved (Hallmann et al. 2017). Grasslands provide habitats for a wide range of insects including beetles (Fadda et al. 2007; Woodcock et al. 2008, 2012a), among the most widely examined insect groups in conservation studies. They can be sampled in a standardized way and quickly respond to environmental changes due to their life history traits (i.e., high reproductive rates and short generation times) (Lövei and Sunderland 1996; Perner and Malt 2003). Beetles represent 40% of the known world insect diversity (Hammond 1992). As a major component of world biodiversity, they provide a wide range of trophic roles (predators; phytophagous; saprophagous; coprophagous). They are thus involved in many ecological services, for instance pest predation, weed herbivory, decomposition and pollution (Grimbacher et al. 2007). In La Crau area, the importance of beetle assemblages has already been proved: beetles have the highest biomass of the Arthropods (Bigot et al. 1983) and consequently represent the main diet of some predators, notably the reptile *Timon lepidus* (Ocellated lizard) (Tatin et al. 2013). Moreover, studies of the effect of land-use changes on beetle assemblages revealed that characteristic species of the steppe were present in formerly cultivated areas, but in lower densities (Fadda et al. 2007). Nevertheless, even more than 20 years after the disturbance, persistent differences in habitat were found between the reference ecosystem and the disturbed areas, and colonization by these insects was shown to be very slow (Fadda et al. 2008a, b).

Beetles have been used as indicators in the assessment of anthropogenic disturbances and environmental changes (Sieren and Fischer 2002; Rainio and Niemelä 2003). The bioindicative potential of beetles has also been used in restoration ecology, especially to
assess the hypothetical success of ecological restoration projects or techniques (Mortimer et al. 1998; Borchard et al. 2014). In addition to the bioindicative approach, the effects of ecological restoration on beetles have been extensively studied, with a degree of positive response shown. For example, Watts and Gibbs (2002) found a positive effect of revegetation on the restoration of beetle assemblages in islands in New Zealand and Woodcock et al. (2012b) found a positive effect of seed addition on beetle assemblages in grasslands. As well as assessing the effects of vegetation restoration and, by extension, of habitat restoration on beetles, ground layer attributes have also been considered as a way of restoring beetle assemblages, for instance by modifying the ground stone cover (Blight et al. 2011). Finally, conservation and restoration can be tackled using translocation to restore animal species, which has already been tested for some beetle species (Knisley et al. 2005; Mawdsley 2005).

In the present study, we aimed to assess the effects of rehabilitation and three different restoration techniques (hay transfer; nurse species seeding; soil transfer) on beetle assemblages in a La Crau area ecological restoration project where the effects on soil and plants (Jaunatre et al. 2012, 2014) and Orthoptera (Alignan et al. 2014) have already been considered. Between 2011 and 2013, we considered seven treatments: the steppe (i.e., the reference ecosystem); the rehabilitated treatment; the three ecological restoration treatments; the control treatment; and the edge between the steppe and the area under restoration. The main assumption was that ecological restoration and rehabilitation treatments can accelerate beetle colonization. Dispersal limitation is known to affect beetle assemblages (Woodcock et al. 2010a, b), and differences in beetle assemblage composition and structure between the reference steppe and former cultivated plots have previously been measured in La Crau area (Fadda et al. 2007, 2008a, b). We also hypothesized that the beetle response to restoration would resemble the vegetation response, with soil transfer being the most efficient treatment at large scale (Jaunatre et al. 2014), creating a suitable habitat and dispersing beetles. Moreover, given the vicinity of the reference ecosystem to the area under restoration, we hypothesized that spontaneous beetle colonization at the edges of the site would be greater that in the inner site, even where the experimental restoration treatments were not applied, as beetles in restored areas have already been shown to recolonize habitats near remnant habitats (Grimbacher and Catterall 2007).

# Methods

## Study area (La Crau area) and study site (a former industrial orchard under rehabilitation)

The plain of La Crau is located in south-eastern France (lat 43°33′N, long 4°52′W), 50 km north-west of Marseille (Fig. 1). This vast area of dry grasslands is considered the sole xeric steppe of France (Devaux et al. 1983). Located on the paleo-delta of the Durance River, this steppe has been shaped by millennia of interactions between climate, soil and sheep grazing. The climate is Mediterranean and characterized by hot summers, mild winters and strong winds of above 50 km h⁻¹ over 110 days a year (Devaux et al. 1983). The steppe of La Crau has an extremely flat topography and a soil surface more than 50% of which is covered by siliceous stones. The soil, a thin layer 40 cm deep, lies on top of an impermeable calcareous conglomerate 1–5 m deep, which prevents plant root access to
<figure><img src="image_3.png" /><figcaption>**Fig. 1** Location of study site and experimental design. a La Crau area located in south-eastern France, b the abandoned orchard stretches over La Crau area, c the former orchard with the seven treatments considered in this study</figcaption></figure>

groundwater (Molliex et al. 2013). Traditional extensive sheep grazing has been practiced for 2000 years (Henry et al. 2010).

Among the different human activities practiced in La Crau area, there was intensive cultivation of a 357 ha peach orchard from 1987 to 2006 (Fig. 1). After its abandonment, biological surveys on birds, vegetation and insects (Coleoptera and Orthoptera) were conducted in 2008 to evaluate the former orchard's biodiversity attributes (Dutoit et al. 2013a, b). This revealed that 2 years after the orchard's abandonment, the steppe communities of the targeted taxa were absent. Thus, in 2009, a rehabilitation project was initiated to rehabilitate a herbaceous sheep-grazed rangeland especially for the nesting of characteristic steppe birds of La Crau area. It consisted in removing 200,000 peach trees, 100,000 poplar trees (planted as wind breakers) and 55 km of irrigation pipes (Dutoit et al. 2013a, b). The soil surface was subsequently leveled, and the rehabilitation period ended in March 2010 with the return of sheep grazing (two flocks of 800 heads). A control treatment was maintained, where the soil surface was not leveled but the peach trees were removed to avoid creating a source of disease (Sharka virus) and pests (*Scolytus rugulosus*, the Fruit bark beetle) for neighboring exploited orchards. Moreover, with a view to accelerating Mediterranean steppe plant community colonization, three additional experimental ecological restoration treatments were realized on a large scale in 2009: (i) hay transfer, (ii) nurse species seeding and (iii) soil transfer (Jaunatre et al. 2012, 2014). Hay transfer, implemented on 20 ha, consisted in vacuuming the seed bank in the reference ecosystem (the steppe
treatment) and spreading it over the rehabilitated treatment. Hay transfer is a very common
technique widely used in ecological restoration projects (Kiehl and Wagner 2006; Coif-
fait-Gombault et al. 2011). Nurse species seeding consisted in sowing on 60 ha three spe-
cies (*Festuca arundinacea*, Tall fescue; *Lolium perenne*, Perennial rye-grass; *Onobrychis
sativa*, Common sainfoin) able to rapidly cover the soil surface. The species were also cho-
sen for their high palatability, their low competitive abilities and their widespread presence
in the surrounding steppe of La Crau (Jaunatre et al. 2014). Here, the aim was to prevent
non-target species from densely covering the soil surface. Soil transfer consisted in gath-
ering the typical steppe soil and spreading it on 3 ha of the rehabilitated treatment. This
had two aims: to transfer seeds, propagules and associated organisms and to save a soil
resource scheduled to be destroyed by quarry enlargement. This treatment was therefore
more a rescue method than true restoration (Jaunatre et al. 2014; Bulot et al. 2017; Chenot
et al. 2017).

Beetle sampling and experimental design

Beetle sampling was carried out using polypropylene pitfall traps (50 mm diameter and 70 mm deep), half-filled with a non-attractive commercial anti-freeze (ethylene-glycol) preventing beetles from escaping and acting as a preservative fluid. A few drops of odorless detergent were added in each trap to reduce surface tension. This solution both kills and conserves captured beetles. Traps were sunk into the soil with the rim flush to ground surface level. Pitfall traps measure beetle activities rather than true abundances, but they are a standard method of measuring differences in species richness, abundance and composition between different areas (Topp et al. 2010). Using this sampling method ensured an uninterrupted period of capture (days and nights), whatever the climatic conditions.

Over a period of 3 years (2011–2013), the pitfall traps were replaced in identical loca-
tions every 15 days throughout 3 months. April to June was chosen as it is the period when
beetle species richness is highest in La Crau (Fadda et al. 2008a), as in other ecosystems.
Every April, when traps were set for the first time, the pitfall traps were left closed for at
least a week to avoid digging effects (Leach et al. 2013) before becoming operational.

For each of the seven treatments considered in this study, beetles were sampled at three
sampling replicated points (Fig. 1). Within each sampling point, three sampling units were
set up (Fig. 2). A sampling unit consisted of three pitfall traps disposed at the vertex of a
1-m equilateral triangle. Sampling units were spaced 10 m apart to avoid interferences and
spatial autocorrelation (Fig. 2) (Fadda et al. 2008a, b) and at a distance > 10 m from the
boundaries of the different treatments considered, to avoid edge effects already measured in
this type of ecosystem (Fadda et al. 2008a, b). During the 3 years of sampling, traps were

<figure><img src="image_4.png" /><figcaption>**Fig. 2** Sampling design in each of the three sampling points for each of the seven treatments considered in this study</figcaption></figure>
replaced every 15 days for 3 months (six sampling dates) in seven treatments and arranged in three sampling units for each sampling point, with a total of 3402 pitfall traps set. Bees were counted, sorted out by morphospecies (Oliver and Beattie 1996) and identified to species level or the closest taxonomic level using a laboratory reference collection (Fadda et al. 2007, 2008a, b; Blight et al. 2011) and identification keys for some beetle families. The taxonomic nomenclature followed Fauna Europaea (2004).

## Statistical analysis

For each year, in order to exclude seasonal variations, data for all traps at one location throughout the three-month sampling were summed. We also pooled data across the three traps forming a sampling unit. The spatial arrangement of the treatments may influence the results as some treatments are often close to the reference steppe. However, we did not find any effect of distance between sampling points and the nearest surrounding steppe, whatever the treatment.

To assess the effect of ecological rehabilitation and restoration on beetle assemblage characteristics, we considered species richness, abundance, Shannon evenness, Bray-Curtis dissimilarity with the reference, normalized Community Structure Integrity Index (CSI-Inorm) and Higher Abundance Index (HAI). The CSIInorm is equivalent to a restoration percentage, as it measures the proportion of the species abundance in the reference steppe that is represented in the assessed treatments (Jaunatre et al. 2013). It is limited between 0 and 1 and increases when characteristic species abundance increases. The HAI measures the proportion of the species abundance in the assessed treatments that is higher than in the reference steppe (Jaunatre et al. 2013). It is limited between 0 and 1 and increases when non-target species abundance increases or when the abundance of characteristic species increases to above their abundance in the reference steppe. Beetle assemblage species richness was also assessed based on trophic groups (phytophagous, predator and saprophagous). We used either one-way ANOVA followed by Tukey's test when parametric conditions were reached, or the Kruskal-Wallis test followed by a pairwise Wilcoxon comparison, with a *p* value adjustment according to Benjamini-Hochberg's method if a significant difference was found, when parametric conditions were not met. Analyses were performed between treatments in the third and last year of the survey (n + 3) or within a single treatment between the 3 years of the survey (n + 1, n + 2, n + 3). Using the same methods, we focused on eight species representative of four different dynamic patterns of beetle responses to the restoration. Effect of ecological rehabilitation and restoration was ordinated by Non-Metric Multidimensional Scaling (NMDS) based on Bray-Curtis dissimilarity over the three years (n + 1, n + 2, n + 3). All analyses were conducted with R software (R Development Core Team 2013) with the additional packages "ade4" (Chessel et al. 2004) and "vegan" (Oksanen et al. 2008).

## Results

A total of 11,771 individuals belonging to 41 families and 228 beetle species were captured (supplementary materials; Tables S1, S2). The dominant species were *Protaetia morio* (Cetoniidae, 1537 individuals, 13% of total abundance), *Asida sericea* (Tenebrioidae, 993 individuals, 8.4%), *Acinopus picipes* (Carabidae, 940 individuals, 8%), *Harpalus distinguendus* (Carabidae, 939 individuals, 8%), *Protaetia oblonga* (Cetoniidae, 866
individuals, 7.3%) and *Poecilus sericeus* (Carabidae, 779 individuals, 6.6%). The other 222 species contributed to < 50% of total abundance, with 61 species represented by only one individual.

## Effect of ecological restoration on beetle assemblage characteristics

In 2013, the last year of survey (n + 3), species richness was significantly higher in the edge, rehabilitated and control treatments than in the steppe (Table 1). The mean species richness in the nurse species seeding treatment was very close to that of the steppe. The highest value was measured for the edge. For the trophic groups (phytophagous, predator and saprophagous), we measured significantly higher predator species richness in the edge, soil transfer, hay transfer, rehabilitated and control treatments than in the steppe (Table 2). For the saprophagous species, all treatments except nurse species seeding, soil transfer and

<table><caption>**Table 1** Short-term effect (after 3 years of survey, n + 3) of the different treatments on beetle assemblages: steppe, edge, soil transfer (Soil T.), nurse species seeding (NSS), hay transfer (Hay T.), rehabilitated (Rehab.) and control</caption><thead><tr><th>ANOVA</th><th>Steppe</th><th>Edge</th><th>Soil T.</th><th>NSS</th><th>Hay T.</th><th>Rehab.</th><th>Control</th></tr></thead><tbody><tr><td>Kruskal-Wallis</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>Species richness</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>df = 6</td><td>13.8 ± 0.37</td><td>25.3 ± 0.65</td><td>20.4 ± 0.53</td><td>13 ± 0.41</td><td>18.1 ± 0.35</td><td>21 ± 0.79</td><td>22 ± 0.35</td></tr><tr><td>F = 8.02</td><td>cd</td><td>a</td><td>abc</td><td>d</td><td>bcd</td><td>ab</td><td>ab</td></tr><tr><td>p < 0.001</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>Abundance</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>df = 6</td><td>80.3 ± 1.92</td><td>70.8 ± 4.79</td><td>53.5 ± 1.45</td><td>30.1 ± 1.09</td><td>51.8 ± 1.58</td><td>75.6 ± 4.09</td><td>78.7 ± 4.13</td></tr><tr><td>X<sup>2</sup> = 23.24</td><td>a</td><td>ab</td><td>b</td><td>c</td><td>b</td><td>ab</td><td>ab</td></tr><tr><td>p < 0.001</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>Evenness</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>df = 6</td><td>0.55 ± 0.01</td><td>0.85 ± 0.01</td><td>0.86 ± 0.01</td><td>0.88 ± 0.01</td><td>0.83 ± 0.01</td><td>0.82 ± 0.01</td><td>0.80 ± 0.01</td></tr><tr><td>X<sup>2</sup> = 30.95</td><td>a</td><td>bcd</td><td>cd</td><td>d</td><td>b</td><td>b</td><td>bc</td></tr><tr><td>p < 0.001</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>Bray-Curtis Index</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>df = 6</td><td>0.33 ± 0.01</td><td>0.74 ± 0.02</td><td>0.78 ± 0.01</td><td>0.88 ± 0.01</td><td>0.87 ± 0.01</td><td>0.86 ± 0.01</td><td>0.85 ± 0.01</td></tr><tr><td>X<sup>2</sup> = 38.06</td><td>a</td><td>b</td><td>b</td><td>d</td><td>d</td><td>cd</td><td>bc</td></tr><tr><td>p < 0.001</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>CSIInorm</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>df = 6</td><td>1 ± 0.01</td><td>0.38 ± 0.03</td><td>0.25 ± 0.01</td><td>0.12 ± 0.01</td><td>0.14 ± 0.01</td><td>0.18 ± 0.01</td><td>0.21 ± 0.01</td></tr><tr><td>X<sup>2</sup> = 37.73</td><td>a</td><td>b</td><td>b</td><td>c</td><td>c</td><td>bc</td><td>b</td></tr><tr><td>p < 0.001</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>HAI</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>df = 6</td><td>0.23 ± 0.01</td><td>0.68 ± 0.01</td><td>0.71 ± 0.01</td><td>0.74 ± 0.01</td><td>0.82 ± 0.01</td><td>0.83 ± 0.01</td><td>0.80 ± 0.01</td></tr><tr><td>X<sup>2</sup> = 35.37</td><td>a</td><td>b</td><td>bcd</td><td>bc</td><td>cd</td><td>d</td><td>bcd</td></tr><tr><td>p < 0.001</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr></tbody></table>

For each characteristic, the values given are mean ± SE, *df*, F and *p* values resulting from the ANOVAs or Chi square and *p* values of Kruskal-Wallis tests performed to test the effect of each treatment for each characteristic. Within a characteristic, treatments sharing common letters do not have significant differences according to Tukey post hoc test or Mann-Whitney-Wilcoxon test
<table><caption>**Table 2** Short-term effect (after 3 years of survey, n + 3) of the different treatments (steppe, edge, soil transfer (Soil T.), nurse species seeding (NSS), hay transfer (Hay T.), rehabilitated (Rehab.) and control) on beetle species richness for three trophic groups</caption><thead><tr><th>ANOVA</th><th>Steppe</th><th>Edge</th><th>Soil T.</th><th>NSS</th><th>Hay T.</th><th>Rehab.</th><th>Control</th></tr></thead><tbody><tr><td><strong>Kruskal-Wallis</strong></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>Phytophagous</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>df = 6</td><td>6.44 ± 0.22</td><td>6.22 ± 0.28</td><td>6.44 ± 0.24</td><td>3 ± 0.19</td><td>4.67 ± 0.26</td><td>6.56 ± 0.39</td><td>8.89 ± 0.19</td></tr><tr><td>F = 5.23</td><td>bc</td><td>abc</td><td>bc</td><td>a</td><td>ab</td><td>bc</td><td>c</td></tr><tr><td>p < 0.001</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td><strong>Predator</strong></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>df = 6</td><td>3.44 ± 0.18</td><td>9.33 ± 0.27</td><td>8.44 ± 0.23</td><td>6.11 ± 0.28</td><td>7.55 ± 0.21</td><td>7.67 ± 0.24</td><td>7.11 ± 0.26</td></tr><tr><td>F = 6.73</td><td>a</td><td>c</td><td>bc</td><td>ab</td><td>bc</td><td>bc</td><td>bc</td></tr><tr><td>p < 0.001</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td><strong>Saprophagous</strong></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>df = 6</td><td>3.33 ± 0.11</td><td>9.33 ± 0.26</td><td>5.33 ± 0.20</td><td>3.89 ± 0.21</td><td>5.56 ± 0.19</td><td>6.33 ± 0.29</td><td>5.44 ± 0.25</td></tr><tr><td>X<sup>2</sup> = 26.62</td><td>a</td><td>c</td><td>ab</td><td>ab</td><td>b</td><td>bc</td><td>ab</td></tr><tr><td>p < 0.001</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr></tbody></table>

For each trophic group, the species richness values given are mean ± SE, *df*, *F* and *p* values resulting from the ANOVAs or Chi square and *p* values of Kruskal-Wallis tests performed to test the effect of each treatment. Within a trophic group, treatments sharing common letters do not have significant differences according to Tukey post hoc test or Mann-Whitney-Wilcoxon test

control showed significantly higher species richness compared with the steppe (Table 2). For the phytophagous group, the nurse species seeding and hay transfer treatments showed significantly lower species richness compared with the steppe and the other treatments (Table 2). The abundance measured in the steppe was significantly higher than the abundance measured for the three experimental restoration treatments (Table 1). The nurse species seeding abundance was also significantly lower compared with that of the soil transfer and the hay transfer treatments. In terms of Shannon evenness, Bray-Curtis index and HAI, we measured a significant difference between the steppe and the other six treatments (including the control), the steppe values always being significantly lower (Table 1). The CSIInorm within the steppe was significantly higher than the CSIInorm measured in the other six treatments (Table 1).

## Effect of ecological restoration on beetle assemblage composition

The NMDS ordination showed an opposition in the beetle assemblage composition between the steppe and the six other treatments (Fig. 3). Nevertheless, there was a gradient of differences between the six other treatments and the steppe. The composition of the edge and soil transfer treatments was closest to that of the steppe, nurse species seeding and control treatments showed high variability, whereas the beetle composition in the rehabilitated and hay transfer treatments differed most from that of the steppe. Moreover, the steppe was distinguished by characteristic beetle species such as *A. sericea*, *Coniocleonus nigrosuturatus* (Curculionidae), *Rhizotrogus cicatricosus* (Melolonthidae) or *Cicindela maroccana* (Carabidae). In contrast, the restoration or rehabilitation treatments and the control were characterized by species such as *H. distinguendus*, *Calathus fuscipes* (Carabidae), *Tachyporus nitidulus* (Staphylinidae), *Hirticomus quadriguttatus* (Anthicidae) and *Drasterius bimaculatus* (Elateridae). The control showed variability between sampling points and was
<figure><img src="image_5.png" /><figcaption>**Fig. 3** NMDS ordination based on 189 samples and the 132 beetle species present in at least three samples. For clarity, only the 63 most correlated species are shown. Steppe (dark gray); edge (gray); soil transfer, nurse species seeding, hay transfer, rehabilitated (gray); and control (white) are the treatments considered</figcaption></figure>

also characterized by the high abundance, or almost exclusive presence, of some species such as *Stenosis sardoa* (Tenebrionidae, 17 of the 19 total individuals), *Otiorhynchus vitellus* (Curculionidae, 27 of the 31) and *Sphenoptera gemmata* (Buprestidae, 11 of the 19). An edge effect was measured in terms of composition, with characteristic species of the steppe and species characterizing the restoration treatments both being found in the edge treatment: *P. sericeus*, *Anthicus tristis* (Anthicidae), *Endomia tenuicollis* (Anthicidae) and *Brachinus sclopeta* (Carabidae).

Assessments of the different populations yielded a range of results. First, some beetle species characterized the reference steppe: *A. sericea* and *Amphimallon ruficorne* (Melolonthidae) (Fig. 4a, b). Secondly, some non-target species were only found in the control, rehabilitation and restoration treatments; for instance *H. distinguendus* and *C. fuscipes* (Fig. 4c, d). The third finding, illustrated with *A. picipes* and *P. morio*, was that some beetle species were present in high abundance both in the steppe and in all the other treatments including the control (Fig. 4e, f). The fourth finding from measuring the edge effect was that some characteristic beetle species of the steppe like *Bioplanes meridionalis* (Tenebrionidae) and *Scaurus atratus* (Tenebrionidae) were colonizing the edges and the
<figure><img src="image_6.png" /></figure>

<figure><img src="image_7.png" /></figure>

<figure><img src="image_8.png" /></figure>

<figure><img src="image_9.png" /></figure>

<figure><img src="image_10.png" /></figure>

<figure><img src="image_11.png" /></figure>

<figure><img src="image_12.png" /></figure>

<figure><img src="image_13.png" /><figcaption>**Fig. 4** Effects of the different treatments on the abundance in 2013 (n + 3) of *a* *Asida sericea*, *b* *Amphi-* *mallon ruficorne*, *c* *Harpalus distinguendus*, *d* *Calathus fuscipes*, *e* *Acinopus picipes*, *f* *Protaetia morio*, *g* *Bioplanes meridionalis* and *h* *Scaurus atratus*</figcaption></figure>
rehabilitated treatments (Fig. 4g, h). Finally, we measured the positive effect of the soil transfer and the nurse species seeding treatments for some species such as *A. sericea* and *B. meridionalis* (Fig. 4a, g).

Discussion

The aim of the study was to assess, at a large scale, the short-term effect of ecological reha-
bilitation and restoration in situ experiments on beetle assemblages.

Our study reveals strong differences between the reference steppe and the different reha-
bilitation and restoration treatments. In the latter treatments, the characteristic beetle target
steppe species are replaced by non-target opportunist species that typically inhabit agri-
cultural habitats. The higher species richness measured inside the rehabilitated or restored
treatments is explained by the high frequencies of very common species in post-cultural
fallows such as *H. distinguendus* (predominant granivorous species), *C. fuscipes* (predomi-
nant predator species) and saprophagous species such as *E. tenuicollis* or *H. quadrigutta-
tus*. This is because there are more food resources (attractive weeds, seeds, phytophagous
insects and litter) for beetles, as already demonstrated for former cultivated fields in the La
Crau area (Fadda et al. 2007). In the short term, the beetle assemblage in these different
treatments showed a significantly greater evenness than in the reference steppe. The vari-
ous treatments were found to contain similar high abundances of many species, whereas in
the steppe, the assemblage was dominated by a few abundant species and numerous other
species with a few individuals each. La Crau area provides a habitat with harsh ecological
conditions (hydric stress, poor resources), which creates an imbalance among plant and
beetle assemblages (Buisson and Dutoit 2006; Fadda et al. 2008a). A few species, the spe-
cialist species of such habitats, are dominant and only some generalist species are pro-
moted. In contrast, most species found in the different treatments are generalist species
adapted to a wide range of environmental conditions.

Our assessment of the effect of the experimental ecological restoration highlights the
relative success of some treatments. Soil transfer was the most efficient restoration treat-
ment for beetle assemblages, promoting the colonization of characteristic beetle species.
Several characteristic steppe beetle species were already established in the soil transfer
treatment (A. *sericea*, *B. meridionalis* and *S. atratus*) and the NMDS showed this treat-
ment to be the one most similar to the reference steppe in terms of beetle composition. Two
previous studies measured the effect of soil transfer on beetle assemblages. Soil transfer did
not promote beetle assemblage in the Mortimer et al. (2002) study, whereas soil transfer
rapidly promoted beetle species composition after 2 years in the Watts et al. (2008) study.
Furthermore, beetle restoration success has been shown to be positively correlated with
plant restoration success (Woodcock et al. 2010b). Given that at a large scale, soil trans-
fer previously provided better results for plant communities than other ecological restora-
tion treatments realized at the same scale (Jaunatre et al. 2014), the best result for beetle
assemblages was therefore expected to be obtained with soil transfer. This hypothesis was
strengthened by the fact that active fauna restoration often consists in translocating species
per se or perhaps translocating their habitats (Grimbacher and Catterall 2007). In our case,
when the soil was transferred, beetles (larvae, nymphs or adults) may have been transferred
too.

Nurse species seeding met with relative success. Results from the NMDS highlight the
high variability from one sampling unit to another. The nurse species seeding treatment
was the one whose vegetation structure was most similar to the steppe, having short vegeta-
tion and high bare soil cover. However, it showed the highest dissimilarity with the steppe
in plant composition and plant species-richness (Jaunatre et al. 2014). For beetles, the
significantly lower species richness and abundance showed that this treatment prevented
numerous opportunist species from colonizing the area in high abundances. Moreover this
treatment eased the colonization of characteristic species, as previously shown in studies
where areas with bare soil promoted several flightless steppe beetle species in early suc-
cessional stages (Cizek et al. 2012). This is confirmed by the characteristic beetle species
found in this treatment, such as *A. sericea*, *B. meridionalis* and *C. maroccana*.

The rehabilitated and hay transfer treatments were the two treatments showing the high-
est beetle composition dissimilarity with the steppe. Hay transfer did not promote charac-
teristic beetle assemblages. Unlike soil transfer, hay transfer may not have shifted larvae,
nymphs or adults of many species, as several characteristic beetle species of the steppe
live on the ground, under stones. The effect of hay transfer on beetles has already been
measured (Mortimer et al. 2002; Woodcock et al. 2008, 2010a, b, 2012b), showing rapid
success (Woodcock et al. 2012b) or moderate success (Mortimer et al. 2002). Our results
on vegetation for the hay transfer treatment showed strong differences in composition even
after 3 years (Jaunatre et al. 2014). Adding seed to overcome plant dispersal limitations did
not promote the establishment of characteristic plant communities, and the result on bee-
tles followed the trend shown with vegetation. Explanations for the low plant community
restoration success of hay transfer include the possibility that high residual soil fertility led
to over-strong competition, preventing target plant species from establishing (Jaunatre et al.
2014).

In the control, we found several steppe beetle species only represented by one to three
isolated individuals: *A. sericea*, *B. meridionalis*, *S. atratus*, and *C. maroccana*. Moreover,
some species were only found in this control treatment: *Acinopus megacephalus* (Carabi-
dae), *Coniocleonus excoriatus* (Curculionidae), *Pachycerus segnis* (Curculionidae), all
three of high biological value in Mediterranean ecosystems, as well as common species
like *S. sardoa*, *O. vitellus*, *S. gemmata*, *Chlorophorus varius* (Cerambycidae) and *Cer-
tallum ebulinum* (Cerambycidae). However, the initial state assessed both in 2008 in the
abandoned orchard before its rehabilitation in 2009 (Dutoit et al. 2009) and through moni-
toring in an orchard still active in 2013 (unpublished data) showed that the characteristic
steppe beetle species were not present. These results, combined with the promoting effect
of soil transfer and nurse species seeding treatments, prove that active restoration is needed
to improve restoration success. On the other hand, the control treatment results here indi-
cate that it might be worthwhile maintaining part of the area under a non-interventionist
approach when restoring a habitat. This could lead to a new habitat with new species of
high biological value.

The assessment of the different treatments in our study revealed that some species were
present in high abundances whatever the treatment considered. For instance, *A. picipes* and
*P. morio*, were found in high abundances in all treatments. The former is a granivorous
species which must have found the food resources needed in the assessed treatments, while
the latter has no particular ecological niche, being a generalist species. *P. sericeus* was
also found in all the assessed treatments, with the highest mean abundances in the reha-
bilitated treatment. *A. sericea* and *P. sericeus* are the most dominant species of the steppe.
*P. sericeus* is a common species in France and in most of Europe, living under stones and
in different habitats such as mountains, hills or cultivated areas (Thérond 1975). Given the
particularly high abundance of the species in the reference steppe, finding such abundances
in the restored treatments could therefore be an early indicator of restoration success.
Finally, considering the edge allowed us to measure an edge effect between the reference steppe and the assessed treatments. The fact that species richness was highest in the edge, together with the result from NMDS on beetle composition, are indicators of this classic effect in ecology (Odum 1971; Magura 2002; Dutoit et al. 2007). This edge effect proves that beetle colonization from the steppe can occur on the different assessed treatments.

Woodcock et al. (2010a) showed that restoration success increases over time, indicating that the establishment and thus the persistence of beetle species depends on the colonization abilities of the species. The vicinity of the steppe promoted spontaneous colonization, as shown for several beetle species such as *B. meridionalis* or *S. atratus*, and can thus be considered a major factor. Moreover, the relative restoration success of soil transfer and nurse species seeding may promote colonization, as restored treatments can provide suitable habitat components (Jellinek et al. 2013). Nonetheless, colonization will be somewhat limited because of the barriers to the south (expressway) (Melis et al. 2010) and to the east (industrial orchard) and will take time, given the size of the area (357 ha). When considering beetles in ecological restoration, it is important to determine whether it is habitat quality or dispersal limitation that most impedes colonization (Martay et al. 2014). In our case, habitat quality is not fully restored and is therefore likely the major factor preventing beetles from colonizing. The conservation and protection of the original steppe habitat surrounding the area under restoration should be given the highest priority (Bulot et al. 2014). Nevertheless, it has been highlighted that both protection of habitats and restoration of habitats are essential components of biological conservation (Possingham et al. 2015) and thus, that ecological restoration can help biological conservation achieve its aims (Wiens and Hobbs 2015).

Four years after the restoration, beetle assemblages were dominated by opportunists and non-target species. Long-term analysis will be required to assess the succession of the different beetle assemblage composition. Restoration of the overall steppe ecosystem, with its characteristic vegetation and insects, is a very time-consuming process. However, it is accepted that most restoration monitoring does not last more than 5 years (Ruiz-Jaen and Aide 2005), and the protocol set up for beetle assessment in our study was onerous. It would therefore be useful to identify indicator species reflecting the response of the overall characteristic beetle assemblage to the restored area. In conclusion, despite the limited success of the restoration treatments, conservation of this dry grassland constitutes a major goal for the preservation of the overall characteristic biodiversity of the steppe.

In conclusion, soil transfer was the most efficient treatment for the restoration of the characteristic beetle assemblages of a pre-existing Mediterranean steppe destroyed by an industrial orchard. Nurse species seeding promoted colonization by several characteristic beetle species of the reference steppe, with vegetation structure close to that of the reference, but not plant species composition.

**Acknowledgements** We are grateful to *Caisse des Dépôts et Consignation Biodiversité, Région Provence-Alpes-Côte d'Azur*, the *Réserve Naturelle des Coussous de Crau* and *Domaine Bayard* for supporting this study. We are also grateful to Pierre Alignan, Romain Angeleri, Sylvain Bernard, Adeline Bizart, Elise Buisson, Adeline Bulot, Diane Cattenoz, Clémentine Coiffait-Gombault, Capucine Fournier, Pablo Gazon, Marie-Charlotte Gicquiaux, Benjamin Gutjahr, Laurent Hardion, Claire Lafon, Julien Larivière, Laure Malagnoux, Solène Masson, Christophe Mazzia, Isabelle Muller, Myriam Siegwart and Julie Tanet for help with field or laboratory work. We also thank Sylvain Fadda and Philippe Ponel for help with beetle identifications and Marjorie Sweetko for English language revision. Comments from anonymous reviewers and editorial staff substantially improved the manuscript.
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