# Orthoptera prove good indicators of grassland rehabilitation success in the first French Natural Asset Reserve

Jean François Alignan, Jean-François Debras, Thierry Dutoit

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Jean François Alignan, Jean-François Debras, Thierry Dutoit. Orthoptera prove good indicators of grassland rehabilitation success in the first French Natural Asset Reserve. Journal for Nature Conservation, 2018, 44, pp.1-11. 10.1016/j.jnc.2018.04.002. hal-01936459

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# Orthoptera prove good indicators of grassland rehabilitation success in the first French Natural Asset Reserve

Jean-François Alignan<sup>a,b,*</sup>, Jean-François Debras<sup>b</sup>, Thierry Dutoit<sup>a</sup>

## ABSTRACT

**Keywords:**

Restoration

Mitigation banks

Offset

Ecological equivalence

Insects

In the last few years, legislation in more and more countries has stipulated compensation for impacts on biodiversity. France was one of the first countries to include compensation in its national law on nature preservation (1976), but habitat banking was only recently introduced into the mitigation regulatory framework. It was applied for the first time in 2008, when the first French Natural Asset Reserve was created in the plain of La Crau (Southeastern France), the last semi-arid steppe in Western Europe. This project was realized through mitigation banking and involved the ecological rehabilitation of an abandoned conventional orchard to a dry Mediterranean grassland habitat for the rare and protected steppe birds typical of this area. Here, to measure habitat rehabilitation success and validate the mitigation banking principle, we use Orthoptera as rapid and integrative indicators. Performing a six-year study (2008–2013), we assessed Orthoptera assemblages before rehabilitation (2008), when the conventional orchard was abandoned; during rehabilitation (2009); and for four years after rehabilitation (2010–2013). Three areas were considered: the area that was rehabilitated, the surrounding undisturbed steppe considered as reference ecosystem and the edge between them. The rapid recovery of typical Orthoptera assemblages measured in terms of species richness, abundance and composition confirms the successful rehabilitation of the habitat, allowing the return of steppe birds, the objective of the compensation project.

## 1. Introduction

Biodiversity offsets can be defined as measurable conservation outcomes resulting from actions designed to compensate for significant residual adverse biodiversity impacts arising from project development after appropriate prevention and mitigation measures have been taken (definition from Business and Biodiversity Offsets Program, 2012). The main goal of biodiversity offsets is to achieve no net loss or even a net gain of biodiversity with respect to species composition, habitat structure, ecosystem function and people's use and cultural values associated with biodiversity (BBOP, 2012). The principle of no net loss of biodiversity is based on the mitigation hierarchy 4-step procedure: avoiding; reducing; restoring; and, offsetting. First, care should be taken to ensure that infrastructure development does not impact biodiversity. Secondly, if impacts cannot be avoided, they should be minimized. Thirdly, if impacts cannot be avoided or minimized, rehabilitation and restoration should be conducted on the areas affected. Finally, if any residual impacts remain, offset measures should be implemented. To achieve no

net loss of biodiversity, the ecological equivalence principle needs to be applied by assessing biodiversity losses subsequent to infrastructure development and the biodiversity gains expected from offsets (McKenney & Kiesecker, 2010; Quétier & Lavorel, 2011; Robertson, 2004). Today, offsets are included in the regulations of several countries such as the United States, Canada, the European Union, Australia, New Zealand, Brazil (McKenney & Kiesecker, 2010; UICN France, 2011). In France, the mitigation hierarchy was included in the national Act on Nature Preservation of 1976. Nevertheless, the offsetting part of the mitigation hierarchy was ignored or injudiciously applied until 2007 (Calvet, Napoléone, & Salles, 2015; Quétier, Regnery, & Levrel, 2014). The European Union Directive 2004/35/CE on “environmental responsibility” contributed to the reinforcement of offsets in French law (UICN France, 2011; Quétier et al., 2014). In France, mitigation banks are one of the ecological compensation systems used. The first French mitigation bank project, also known as the “Cossure project”, was conducted in the plain of La Crau (Bouches-du-Rhône) in southeastern France in 2008, creating the first Natural Asset Reserve. A former

<footnote><sup>a</sup> UMR CNRS/IRD 7263 IMBE, Institut Méditerranéen de Biodiversité et Ecologie, Avignon Université et Aix-Marseille Université, IUT, Site Agroparc BP 61207, 84911 Avignon Cedex 09, France</footnote>

<footnote><sup>b</sup> INRA, UR 1115 Plantes et systèmes de cultures horticoles, Domaine St Paul, Site Agroparc, CS 40509, 84914 Avignon Cedex 9, France</footnote>

<footnote>* Corresponding author at: Institut Méditerranéen de Biodiversité et d'Ecologie (IMBE), Avignon Université, UMR CNRS IRD Aix Marseille Université, IUT site Agroparc, 337 Chemin des Meinajaries BP 61207, F-84911 Avignon Cedex 09, France.</footnote>

<footnote>E-mail addresses: jean-francois alignan@alumni.univ-avignon.fr (J.-F. Alignan), jean-francois.debras@inra.fr (J.-F. Debras), thierry.dutoit@univ-avignon.fr (T. Dutoit).</footnote>
<figure><img src="image_2.png" /><figcaption>**Fig. 1.** (A) La Crau area in southeastern France within the triangle formed by the cities of Arles, Salon and Fos; (B) An abandoned orchard rehabilitated as grassland in 2009. Three sampling areas were considered in this study (surrounding reference steppe, rehabilitated grassland and the edge between them).</figcaption></figure>

conventional orchard (357 ha) abandoned in 2006 was rehabilitated to a Mediterranean grassland habitat for the rare and protected steppe birds typical of this area.

**1.1. Cossure project: the first French Natural Asset Reserve for mitigation banking**

Preserving the La Crau area is vital as it is the last semi-arid steppe of Western Europe (Devaux, Archiloque, Borel, Bourrelly, & Louis-Palluel, 1983). Nevertheless, land-use changes (farming; military activities; industry) have contributed to the loss of 80% of its original surface, reducing it from 50,000 to 10,000 ha (Buisson & Dutoit, 2006). Between 1987 and 1992, the conventional Cossure orchard was cultivated on 357 ha in the steppe (Fig. 1) for the production of peaches and apricots. In 2006, the orchard was abandoned before being bought by the Caisse des Dépôts et Consignations Biodiversité bank in 2008. Inspired by the wetland mitigation banking measure of the United States (UICN (Union Internationale pour la Conservation de la Nature) France, 2011), CDC Biodiversité established a mitigation bank, also called in France a “Natural Asset Reserve”, of 357 ha acreage credits. Starting from 2010, these credits are being sold to developers to compensate for habitat conversion.

Mitigation banking is based on mitigation ratios. Most mitigation banks use a 1:1 ratio (ha compensated – ha converted) (Brown & Lant, 1999) and, to respect the ecological equivalence principle, compensation should involve the same ecosystem attributes (biodiversity, habitat, functions) in converted sites as those that are the object of the compensation (BBOP, 2012; Regnery, Couvet, & Kerbiriou, 2013). The aim of mitigation banking is the establishment or re-establishment of self-sustaining systems that replace systems expected to be adversely impacted (Brumbaugh & Reppert, 1994 in Brown & Lant, 1999). This was the principle behind the rehabilitation of the Cossure area. In 2008, the initial state was assessed, including biological studies on avifauna, flora, insects and soils (Dutoit et al., 2013). The study on birds pointed to the need for an ecological project to facilitate their return. For that purpose, in 2009, 22 years after the habitat loss due to the settlement of the conventional orchard, 200,000 peach trees and 100,000 poplars constituting the windbreak hedgerows were removed. The soil surface was leveled in 2010. Finally, the same year, the rehabilitation ended

with the reinstallation of the traditional sheep grazing system of the steppe through the return of two flocks of 800 heads arranged in two grazing units on the whole former orchard. No herbaceous plants were seeded or planted, the vegetation being expected to recover due to the soil seed banks or seed rains from the adjacent undisturbed steppe (Dutoit et al., 2013; Jaunatre, Buisson, & Dutoit, 2012; Jaunatre, Buisson, & Dutoit, 2014a). The main short-term objective of this project was therefore to rehabilitate one function of the ecosystem as an habitat for steppe birds and the long-term objective, through appropriate management by sheep grazing, to restore plant community succession, leading to the restoration sensu stricto (Aronson, Floret, Le Floc'h, Ovalle, & Pontanier, 1993) of the former steppe ecosystem that still exists all around the rehabilitated area (Fig. 1).

**1.2. Orthoptera as early integrative indicators of grassland rehabilitation success**

Indicators are used as a gauge for the condition of a particular habitat (i.e. alteration, fragmentation, or restoration), community or ecosystem (McGeoch, 1998; Meffe & Carroll, 1994). Plant communities or animal assemblages are generally considered as the most appropriate indicators for conservation at the ecosystem level (Kovacs et al., 1992 in Lee Foote & Rice Hornung, 2005). It is acknowledged that ecological indicators must fulfill important criteria such as being (i) sensitive to changes in the environment (natural or anthropogenic), (ii) widespread in the habitat considered, (iii) relevant to ecological phenomena, and (iv) easy and cost-effective to capture and measure (Noss, 1990).

Here therefore, we considered Orthoptera assemblages as efficient early indicators of grassland rehabilitation success in the mitigation bank experiment. Orthoptera have already been established as being: (i) able to characterize habitats and environmental changes or naturalness (Báldi & Kisbenedek, 1997; Bazelet & Samways, 2011); (ii) present in almost every grassland or rangeland; (iii) primary consumers of grassland vegetation (Joern, 1982a) or a source of prey for predators (Joern, 1986); (iv) easily captured with the sweep netting method, which can be standardized to obtain relative abundance (Gardiner, Hill, & Chesmore, 2005); and (v) economically important, especially when they act as herbivorous pests during outbreaks.

In the La Crau area, Orthoptera are a very important compartment
of steppe biodiversity (Léonide, 1983) because they constitute one of
the main average annual Arthropod biomasses (Bigot, Chemseddine, &
Delye, 1983; Tanet & Gicquiaux, 2013). They are a major source of prey
for birds (Foucart, 1997) and the second largest group (23%) in the diet
of the ocellated lizard (*Timon lepidus*), a reptile considered as vulnerable
in Europe (Tatin, Chapelin-Viscardi, Renet, Becker, & Ponel, 2013).
Being hypothetical herbivore pests during outbreaks (Báldi &
Kisbenedek, 1997), Orthoptera can have an economic impact, and
regular surveys of them need to be undertaken, as is the case for the
*Dociostaurus maroccanus* species (Léonide, 1983) in the plain of La Crau.

1.3. Aims of the study

The aim of the study was to assess Orthoptera assemblages in 2008 before the rehabilitation of the abandoned orchard, in 2009 during its rehabilitation and for the four years from 2010 to 2013 following re-habilitation. To do so, we considered species richness, abundance, diversity and composition of the Orthoptera assemblages in three different areas: the rehabilitated area, the steppe of La Crau considered as long-term reference ecosystem and the edge between these two areas, to assess whether there might be an edge effect or ecotone (Dutoit, Buisson, Gerbaud, Roche, & Tatoni, 2007). Orthoptera assemblages would then be used as an indicator of early grassland rehabilitation success for steppe birds.

We hypothesized that i) the recovery of Orthoptera would be rapid
after the abandonment of the orchard and the rehabilitation of a her-
baceous grassland layer; ii) there would rapidly be no significant dif-
ferences from the surrounding steppe reference ecosystem, because
Orthoptera are more sensitive to the structure of the herbaceous for-
mation than to its composition and plant species-richness. Thus,
Orthoptera assemblages could be used as early indicators of the re-
habilitation of a Mediterranean grassland ecosystem as a good habitat
for steppe birds.

## 2. Materials and methods

2.1. Study site

The plain of La Crau is located in south-eastern France, 50 km north-
west of Marseille (Fig. 1). Initially extending over 50,000 ha, the sur-
face of this steppe area has been strongly reduced because of increasing
human activities (Buisson & Dutoit, 2006). Now extending only over
10,000 ha, the steppe is characterized by the interaction of three fac-
tors: climate, topography and traditional sheep grazing. The climate is
Mediterranean, with long hot summers and mild winters. With a to-
pography that is extremely flat and stones covering an average 50% of
the soil surface, it is similar to Dehesas in Spain, to Montados in Por-
tugal and to the regos and hammadas of North Africa. The soil (40 cm
deep) covers an impermeable calcareous conglomerate which does not
allow plant roots access to groundwater (Colomb & Roux, 1978). For
3000 years there has been traditional sheep grazing on the steppe
(Badan, Brun, & Congès, 1995; Henry, Talon, & Dutoit, 2010). The
steppe is also a haven to the Crau Plain grasshopper (*Prionotropis rho-
danica*), endemic to the steppe, or the Crau jewel beetle (*Acmaeoderella
cyanipennis perroti*), endemic to southern Provence.

Among the different threatened steppe bird species in the La Crau
area, three emerge as emblematic of the steppe and of national im-
portance, both in terms of population size and because La Crau is the
northern limit of their natural range: the pin-tailed sandgrouse
(*Pterocles alchata*), the calandra lark (*Melanocorypha calandra*) and the
little bustard (*Tetrax tetrax*) (Vincent-Martin, Wolff, Paulus, & Tatin,
2013).

## 2.2. Experimental design and Orthoptera sampling

The study on Orthoptera was a six-year monitoring survey (2008-

2013). 2008 was the year when the initial state was assessed, just be-
fore the rehabilitation undertaken in 2009. The impact of rehabilitation
on Orthoptera assemblages was then assessed over the four following
years (2010–2013).

The study was conducted in three different areas: the surrounding steppe area used as reference ecosystem, the rehabilitated area and the edge area between them. We collected Orthoptera on three sampling plots for each area. Each plot was subdivided into seven transects of 40 m long and 2 m wide. In order to avoid proximity effects (Picaud & Petit, 2007), transects were arranged 10 m apart (Alignan, Debras, & Dutoit, 2014; Evans, 1984).

Because we needed to discriminate the effects of grassland re-
habilitation from those of orchard abandonment, an additional
Orthoptera sampling was performed during the same period in a nearby
orchard under exploitation. We selected a conventional orchard
(Domaine de Bayard) of 250 ha located Northwest of the abandoned
orchard (Fig. 1). Orthoptera were sampled for two years (2011–2012)
in two areas in the orchard: one in the center and one on the edge of the
orchard. The sampling design and protocol were identical to those
applied on the abandoned orchard and rehabilitated area.

Orthoptera were captured using a sweep net (Evans, 1984; Gardiner et al., 2005) which is acknowledged as an efficient sampling method for reliable estimations of relative abundance and species composition in short herbaceous vegetation. Along the 40 m transects, the standard capture procedure was applied: using a 38 cm diameter net, at a steady speed, the sampler gave more than 25 once-and-back sweeps in a 180° arc (Evans, 1984; Fuhlendorf, Engle, Arnold, & Bidwell, 2002; Gardiner et al., 2005). The sampling took place in July, when Orthoptera density is at a peak in the La Crau area (Foucart, 1997), on hot, windless days not preceding rainfall. Orthoptera were mainly captured at mid-day, during maximum sunshine (Guido & Gianelle, 2001). The day's catch of Orthoptera were taken to the laboratory, anaesthetized with CO2 (Dupuy, 2009) and identified according to Chopard (1951) and Bellmann and Luquet (1995). The following morning, captured individuals were returned to the exact spot where they had been collected, in order to minimize Orthoptera mortality due to the sampling procedure.

2.3. Habitat variables

In this study, vegetation height and cover of bare ground, stones and
vegetation were considered as habitat variables. To estimate percen-
tages of cover, three 2 × 2 m quadrats were surveyed at each of the
seven transects for each sampling plot and for each of the three areas.
Within the quadrats, average vegetation height was measured using a
graduated meter.

2.4. Statistical data analyses

All the statistical analyses were performed using the R 3.0.2 soft-
ware (R Development Core Team, 2013) with the additional packages
ade4 (Chessel, Dufour, & Thioulouse, 2004; Dray & Dufour, 2007), mass
(Venables & Ripley, 2002) and vegan (Oksanen et al., 2008). In each
sampling plot, the seven transects were pooled in order to ensure the
representativeness of Orthoptera sampling (Evans, 1984).

Orthoptera assemblages were measured using species richness,
abundance, Shannon index, Shannon evenness, Renkonen similarity
index, normalized Community Structure Integrity Index (CSIInorm) and
Higher Abundance Index (HAI). The CSIInorm and the HAI (Jaunatre
et al., 2013) are both based on proportions of species abundance. The
CSIInorm measures the proportion of species abundance in the re-
ference (steppe) Orthoptera assemblage in the assessed areas (edge and
rehabilitated). The index is bounded between 0 and 1, increasing when
the proportion of species abundance in the assessed areas is close to the
proportion of species abundance in the reference. The HAI measures the
proportion of species abundance in the assessed assemblages that is
higher than in the reference assemblages. The index is bounded between 0 and 1, increasing when non-target Orthoptera species abundance increases or when target Orthoptera species abundance increases above their abundance in the reference (Jaunatre et al., 2013).

The six-year survey period for the three areas considered was first analyzed for hypothetical interaction. Parametric conditions were not achieved, so we then tested the year effect and the area effect independently. Next, data were analyzed by comparing means: i) within one area over the six-year survey period and ii) among the three areas for the last year of the survey (2013). For these comparisons, when parametric conditions were reached, we used one-way ANOVA followed by Tukey's test allowing pairwise comparisons; otherwise, we used the Kruskal-Wallis non-parametric test followed by the Wilcoxon-Mann-Whitney test with p-adjustment according to the method of Benjamini-Hochberg (Benjamini & Hochberg, 1995) when a significant difference was detected. Box-Cox-transformation was applied on the ANOVA performed. Orthoptera composition characteristics were ordinated using Non-metric Multidimensional Scaling (NMDS) based on Orthoptera abundance. Ordination of habitat characteristics was performed using Principal Component Analysis (PCA).

## 3. Results

### 3.1. Assemblage characteristics

During the six-year survey, 23 Orthoptera species (17 *Acrididae* and 6 *Tettigoniidae*) and 2938 individuals were identified (Species list in Supplementary material). 2010 was the richest and most abundant year for Orthoptera. The richest area was the rehabilitated area, with 23 species identified, while 22 and 20 species were encountered in the steppe and edge areas respectively. The most abundant area was the steppe, with 1618 individuals identified, while only 760 and 560 were respectively identified in the edge and rehabilitated areas over the six years. The most common species identified was *Calliptamus wattenwylianus* and the scarcest species was *Aiolopus strepens* with only one individual identified.

In the last year of the survey (2013), there were no significant differences in any of the parameters (species richness, abundance, Shannon index, Shannon evenness, Renkonen index, CSIInorm and HAI) among the three areas considered in this study (steppe, edge, rehabilitated) (Table 1).

In the reference steppe and edge areas, species richness increased significantly between 2008 and 2010, decreased significantly between 2010 and 2011 and increased again significantly between 2011 and 2013, but only in the edge area (Fig. 2A). In the rehabilitated area, the only significant difference measured was between 2008 and 2013 (Fig. 2A).

In the edge area, abundance significantly increased between 2009 and 2010 and then significantly decreased between 2010 and 2011 (Fig. 2B). Finally, the abundance significantly increased between 2011 and 2013. In the rehabilitated area, abundance significantly increased between 2008 and 2013 (Fig. 2B). Abundance did not significantly differ between years in the steppe area.

In the steppe area, the Shannon index showed a significant increase between 2008 and 2010 and then significantly decreased between 2010 and 2011 (Table 2). The Shannon index showed no significant differences between sampling years for the edge and the rehabilitated area (Table 2).

In the edge area, the Shannon evenness showed no significant differences between 2008 and 2011 (Table 2). The Shannon evenness then significantly decreased between 2011 and 2012. In the steppe and rehabilitated areas, the Shannon evenness showed no significant differences between sampling years (Table 2).

Between the steppe and the edge areas, the Renkonen similarity index increased between 2008 and 2010, significantly decreased between 2010 and 2011 and then significantly increased between 2011 and 2013 (Table 2).

<caption>**Table 1**</caption>

Orthoptera assemblage characteristics for the three areas considered in this study (steppe, edge, rehabilitated) in 2013 (last year of survey). Values are mean ± standard errors, df (degree of freedom), F and p values of ANOVAs followed by Tukey post hoc test (ns when non-significant) performed for each Orthoptera assemblage characteristic in order to compare the three areas.

<table><thead><tr><th></th><th>ANOVA</th><th>Steppe</th><th>Edge</th><th>Rehabilitated</th></tr></thead><tbody><tr><td>Species richness</td><td>df = 2<br>F = 0.01<br>p = 0.99</td><td>11.67 ± 0.96ns</td><td>11.33 ± 1.17ns</td><td>11.67 ± 1.39ns</td></tr><tr><td>Abundance</td><td>df = 2<br>F = 1.49<br>P = 0.30</td><td>81 ± 3.84ns</td><td>61 ± 4.51 ns</td><td>72.67 ± 6.17ns</td></tr><tr><td>Shannon index</td><td>df = 2<br>F = 0.01<br>p = 0.99</td><td>2.58 ± 0.17ns</td><td>2.61 ± 0.10ns</td><td>2.64 ± 0.15ns</td></tr><tr><td>Evenness</td><td>df = 2<br>F = 0.07<br>p = 0.94</td><td>0.73 ± 0.05ns</td><td>0.76 ± 0.01ns</td><td>0.77 ± 0.05ns</td></tr><tr><td>Renkonen index</td><td>df = 1<br>F = 1.71<br>P = 0.21</td><td></td><td>0.47 ± 0.02ns</td><td>0.36 ± 0.02ns</td></tr><tr><td>CSIInorm</td><td>df = 2<br>F = 3.06<br>P = 0.12</td><td>1.00 ± 0.09ns</td><td>0.74 ± 0.03ns</td><td>0.59 ± 0.07ns</td></tr><tr><td>HAI</td><td>df = 2<br>F = 1.29<br>p = 0.34</td><td>0.33 ± 0.04ns</td><td>0.33 ± 0.04ns</td><td>0.54 ± 0.08ns</td></tr></tbody></table>

The HAI significantly decreased between 2008 and 2009 in the rehabilitated area (Table 2), and then significantly increased between 2009 and 2011. In the steppe and edge areas, no significant differences were measured between sampling years (Table 2).

The NMDS ordination, based on Orthoptera abundances in 2013, showed the three areas considered in this study (steppe, edge, rehabilitated) as close to each other (Fig. 3A). The trajectories of the barycenter of the rehabilitated and edge areas showed very strong dynamics between the sampling periods, especially for the edge area, whatever the sampling periods considered (before rehabilitation; during or after one to four years) (Fig. 3B). The trajectory of the barycenter of the steppe area showed a weaker dynamic compared to the two other areas, especially between 2012 and 2013. The ordination indicated that, despite the strong dynamics during the sampling periods, Orthoptera composition and abundance were close in the three areas, as the trajectories of the barycenter were similar (Fig. 3B).

### 3.2. Habitat characteristics

The PCA ordination based on habitat characteristics for 2013 showed on the first axis (85.9%) that bare soil cover and stone cover were in opposition to vegetation cover and vegetation height (Fig. 4). The steppe area was more correlated with bare soil and stone cover, while the edge and rehabilitated areas were more correlated with vegetation cover and vegetation height.

### 3.3. Comparison of our results with an orchard still under exploitation

In 2011 and 2012, pairwise species richness and abundance comparisons were realized between the rehabilitated area and the orchard still under exploitation, at their centers and at the edges between them
<figure><img src="image_3.png" /><figcaption>Fig. 2. Means and standard errors of (A) species richness and (B) (abundance) over the six-year study: Before the rehabilitation (2008), During the rehabilitation (2009), 1 year to 4 years (2010–2013) After the rehabilitation. Three areas are considered: steppe (black), edge (gray) and rehabilitated (white). F and p values of ANOVAs or X² and p values of Kruskal-Wallis tests performed to compare the six years within each of the three areas are given above each area. Bars sharing a common letter have no significant differences according to Tukey post hoc or to Wilcoxon–Mann–Whitney test.</figcaption></figure>

and the surrounding reference steppe. Except for 2012's species-richness, the richness and the abundance of Orthoptera were significantly higher in the rehabilitated area than in the exploited orchard (Fig. 5). In 2011, although sampling was done just before pesticides were applied, no individuals were captured or observed in the center of the exploited orchard. No significant differences were measured between the edges of the two areas in 2011 or in 2012.

## 4. Discussion

In this study, we hypothesized that the recovery of Orthoptera assemblages would be rapid after abandonment of the orchard and grassland rehabilitation. Comparisons of Orthoptera species-richness and abundances between the center and edge of the rehabilitated area and the orchard still in use in 2011 and 2012 confirm that only a third
**Table 2**

Means and standard errors of Shannon index, Shannon evenness, Renkonen similarity index, CSIInorm and HAI over the six-year study: Before the rehabilitation (2008), During the rehabilitation (2009), 1 year to 4 years (2010–2013) After the rehabilitation for the three areas considered in this study: steppe, edge and rehabilitated. The given values are df (degree of freedom), F and p values of ANOVAs or X² and p values of Kruskal–Wallis tests performed to compare the six years within each of the three areas. Two boxes sharing a common letter have no significant differences according to Tukey post hoc or to Wilcoxon–Mann–Whitney test.

<table><thead><tr><th colspan="2">ANOVA Kruskal Wallis</th><th colspan="6">Steppe</th></tr><tr><th></th><th></th><th>2008</th><th>2009</th><th>2010</th><th>2011</th><th>2012</th><th>2013</th></tr></thead><tbody><tr><td>Shannon index</td><td>df = 5<br>F = 6.21<br>p &lt; 0.01</td><td>2.26 ± 0.13 a</td><td>2.67 ± 0.07 a</td><td>3.45 ± 0.05 b</td><td>2.20 ± 0.18 a</td><td>2.72 ± 0.07 ab</td><td>2.58 ± 0.17 a</td></tr><tr><td>Shannon evenness</td><td>df = 5<br>F = 1.21<br>p &gt; 0.05</td><td>0.75 ± 0.03 ns</td><td>0.75 ± 0.02 ns</td><td>0.87 ± 0.02 ns</td><td>0.87 ± 0.04 ns</td><td>0.78 ± 0.03 ns</td><td>0.73 ± 0.05 ns</td></tr><tr><td>CSIInorm</td><td>df = 5<br>F = 0.01<br>p &gt; 0.05</td><td>1.00 ± 0.23 ns</td><td>1.00 ± 0.16 ns</td><td>1.00 ± 0.14 ns</td><td>1.00 ± 0.29 ns</td><td>1.00 ± 0.12 ns</td><td>1.00 ± 0.09 ns</td></tr><tr><td>HAI</td><td>df = 5<br>F = 0.38<br>p &gt; 0.05</td><td>0.31 ± 0.06 ns</td><td>0.21 ± 0.06 ns</td><td>0.38 ± 0.06 ns</td><td>0.28 ± 0.08 ns</td><td>0.25 ± 0.07 ns</td><td>0.33 ± 0.04 ns</td></tr><tr><th colspan="2">ANOVA Kruskal–Wallis</th><th colspan="6">Edge</th></tr><tr><th></th><th></th><th>Before 2008</th><th>During 2009</th><th>After 1 Y 2010</th><th>After 2 Y 2011</th><th>After 3 Y 2012</th><th>After 4 Y 2013</th></tr><tr><td>Shannon index</td><td>df = 5<br>X² = 14.1<br>p &lt; 0.05</td><td>1.76 ± 0.03 ns</td><td>2.85 ± 0.01 ns</td><td>3.16 ± 0.06 ns</td><td>1.94 ± 0.30 ns</td><td>1.47 ± 0.04 ns</td><td>2.67 ± 0.10 ns</td></tr><tr><td>Shannon evenness</td><td>df = 5<br>F = 5.16<br>p &lt; 0.01</td><td>0.73 ± 0.06 ab</td><td>0.87 ± 0.02 ab</td><td>0.87 ± 0.01 ab</td><td>0.95 ± 0.01 a</td><td>0.62 ± 0.04 b</td><td>0.76 ± 0.01 ab</td></tr><tr><td>Renkonen index</td><td>df = 5<br>F = 11.4<br>p &lt; 0.001</td><td>0.47 ± 0.02 ac</td><td>0.54 ± 0.02 ac</td><td>0.62 ± 0.01 a</td><td>0.16 ± 0.02 b</td><td>0.33 ± 0.01 bc</td><td>0.47 ± 0.02 ac</td></tr><tr><td>CSIInorm</td><td>df = 5<br>F = 2.30<br>p &gt; 0.05</td><td>0.34 ± 0.11 ns</td><td>0.24 ± 0.05 ns</td><td>0.56 ± 0.05 ns</td><td>0.42 ± 0.09 ns</td><td>0.39 ± 0.01 ns</td><td>0.74 ± 0.03 ns</td></tr><tr><td>HAI</td><td>df = 5<br>F = 0.99<br>p &gt; 0.05</td><td>0.34 ± 0.09 ns</td><td>0.20 ± 0.11 ns</td><td>0.47 ± 0.05 ns</td><td>0.56 ± 0.03 ns</td><td>0.48 ± 0.09 ns</td><td>0.33 ± 0.04 ns</td></tr><tr><th colspan="2">ANOVA Kruskal–Wallis</th><th colspan="6">Rehabilitated</th></tr><tr><th></th><th></th><th>Before 2008</th><th>During 2009</th><th>After 1 Y 2010</th><th>After 2 Y 2011</th><th>After 3 Y 2012</th><th>After 4 Y 2013</th></tr><tr><td>Shannon index</td><td>df = 5<br>X² = 12.4<br>p &lt; 0.05</td><td>0.76 ± 0.44 ns</td><td>3.08 ± 0.14 ns</td><td>3.00 ± 0.02 ns</td><td>2.63 ± 0.02 ns</td><td>1.94 ± 0.12 ns</td><td>2.64 ± 0.15 ns</td></tr><tr><td>Shannon evenness</td><td>df = 5<br>X² = 14.1<br>p &lt; 0.05</td><td>0.25 ± 0.15 ns</td><td>0.92 ± 0.01 ns</td><td>0.93 ± 0.01 ns</td><td>0.94 ± 0.01 ns</td><td>0.69 ± 0.04 ns</td><td>0.77 ± 0.05 ns</td></tr><tr><td>Renkonen index</td><td>df = 5<br>X² = 22.0<br>p &lt; 0.001</td><td>0.16 ± 0.03 ade</td><td>0.54 ± 0.01 bc</td><td>0.38 ± 0.01 a</td><td>0.20 ± 0.01 d</td><td>0.42 ± 0.02 ace</td><td>0.36 ± 0.02 acde</td></tr><tr><td>CSIInorm</td><td>df = 5<br>F = 4.05<br>p &lt; 0.05</td><td>0.14 ± 0.07 a</td><td>0.25 ± 0.04 a</td><td>0.26 ± 0.03 a</td><td>0.36 ± 0.03 a</td><td>0.51 ± 0.01 a</td><td>0.59 ± 0.07 b</td></tr><tr><td>HAI</td><td>df = 5<br>F = 5.41<br>p &lt; 0.01</td><td>0.63 ± 0.10 a</td><td>0.16 ± 0.01 b</td><td>0.28 ± 0.05 ab</td><td>0.61 ± 0.04 a</td><td>0.39 ± 0.01 ab</td><td>0.54 ± 0.08 a</td></tr></tbody></table>

of the total 24 species (i.e. *Calliptamus barbarus*; *C. wattenwylianus*; *C. brunneus*; *Dociostaurus jagoi*; *Euchorthippus chopardi*; *Euchorthippus elegantulus*; *Oedaleus decorus*; *Oedipoda caerulescens*) are able to survive, in low abundance, in a conventional orchard which experienced regular use of insecticides. This points to the positive role of orchard abandonment as a preliminary to rehabilitation. The positive impact of orchard abandonment on insects found here confirms results already obtained for other arthropod assemblages (i.e earwigs; spiders) (Malagnoux, Marliac, Simon, Rault, & Capowiez, 2015; Mazzia et al., 2015). In the light of these results, it is clear that abandoning exploitation of the orchard and ceasing to apply insecticides in 2006 had already allowed Orthoptera recolonization, even before the

rehabilitation of the grassland.

Furthermore, our results show that in 2013, seven years after the orchard's exploitation was abandoned and four years after its rehabilitation into grassland in 2009, there were no significant differences in species richness, abundance, diversity or composition of the Orthoptera assemblages compared with the surrounding reference ecosystem. This highlights the high recovery potential of Orthoptera assemblages. The significant increase measured in the rehabilitated area between 2008 and 2013 for Orthoptera species richness, abundance and CSIInorm proves that the grassland habitat rehabilitation was successful for Orthoptera assemblages.

For species richness and abundance, it highlights not only the strong
<figure><img src="image_4.png" /><figcaption>**Fig. 3.** NMDS ordination: the (A) plot shows only the 2013 sampling for the three areas: steppe (black); edge (gray) and rehabilitated area (white). The (B) plot shows the succession of Orthoptera assemblages for each of the three areas, according to the position of their barycenter: **bold dashed arrows** represent the succession from before rehabilitation (2008) to during rehabilitation (2009); **solid arrows** represent the succession from during rehabilitation (2009) to the 1st year after rehabilitation (2010); **dashed arrows** represent the succession from the 1st year after rehabilitation (2010) to the 2nd year after rehabilitation (2011); **dashed point arrows** represent the succession from the 2nd year (2011) to the 3rd year (2012); **solid bold arrows** represent the succession from the 3rd year after rehabilitation (2012) to the 4th year after rehabilitation (2013).</figcaption></figure>
<figure><img src="image_5.png" /><figcaption>Fig. 4. PCA realized on habitat characteristics in 2013 from each area: steppe (black), edge (gray) and rehabilitated (white). Habitat characteristics considered here are bare soil cover, stone cover, vegetation cover and vegetation height.</figcaption></figure>

<figure><img src="image_6.png" /><figcaption>Fig. 5. Means and standard errors of species richness (A) and abundance (B) of each area: edge and rehabilitated areas (white), edge and conventional orchard (black) in 2011 and 2012. The p-values of the t.test or wilcox.test when (non-parametric data) are indicated by: *: p < 0.05; **: p < 0.01; ***: p < 0.001.</figcaption></figure>

capacity of Orthoptera for recolonization but also the speed with which the former orchard area has been restored as a suitable habitat for these insects. Alate Orthoptera are known to have outstanding flying abilities, although this varies from species to species (Picaud & Petit, 2007). It has been proved that vegetation height can be correlated either positively or negatively with Orthoptera (Báldi & Kisbenedek, 1997; Batáry et al., 2007; Gardiner, Pye, Field, & Hill, 2002). Vegetation cover and vegetation structure also influences Orthoptera assemblages (Clark, 1948; Gardiner et al., 2002; Hochkirch, Witzenberger, Teerling, & Niemeyer, 2007) and especially by affecting the microclimate (Joern, 1982b). Fluctuation of both species richness and abundance between 2010 and 2011 was measured with the same dynamic (values dropped between 2010 to 2011) for the three treatments considered in the study. Thus, it cannot challenge the comparison of Orthoptera assemblage for the six years study between the different treatments and subsequently

the recovery of the species. On the other hand, it may have slowed down the recovery. The most valuable explanation must lie in the climatic variables. We assessed climatic variables for the two years by considering temperature, relative humidity and atmospheric pressure (data gathered thanks to one of the "Institut National de la Recherche Agronomique – EMMAH Unit" weather station located in La Crau - results not shown). Nevertheless, no significant differences between the two years were measured for temperature and relative humidity. Significant difference was only measured for atmospheric pressure. As it is acknowledged that this ecological factor can affect daily activity of insects (Tatin, Dutoit, & Feh, 2000), we can hypothesize that this may explain the lower abundances measured in 2011.

Considering the CSIInorm, it significantly and continuously increased between 2008 and 2013. This indicates that the Orthoptera assemblage structure in the rehabilitated area is becoming more and
more similar to that of the surrounding reference steppe. Moreover, the result of the NMDS based on abundance proves that the composition in the three different areas is already very similar. The NMDS analysis of the trajectories of the barycenter also proves that the Orthoptera assemblage dynamics in the edge and the rehabilitated area have been tending towards that of the steppe since 2009, when grassland rehabilitation started. For the Shannon index, Shannon evenness, Renkonen similarity index and HAI, either no significant differences were observed or, despite significant inter-annual variations, the values remain not significantly different between 2008 and 2013. Furthermore, no edge effect occurs between the two zones, even in 2008 when there was a poplar hedgerow between the abandoned orchard and the surrounding steppe. This result shows that Orthoptera were able to cross from the reference steppe to the former orchard before, during and after its rehabilitation.

In the study site, significant differences in composition, species-richness and diversity of the vegetation were measured, especially between the rehabilitated grassland and the surrounding reference steppe (Jaunatre et al., 2014a). Here in our study, we measured that the edge and rehabilitated areas are characterized by tall vegetation and dense vegetation cover, while the reference steppe ecosystem is mainly characterized by bare soil and stone cover. Vegetation structure and composition are known to influence Orthoptera species distribution, composition of assemblages and abundances (Evans, 1984; Guido & Gianelle, 2001; Joern, 1982a, 1982b; Kemp, Harvey, & O'Neill, 1990; Marini, Fontana, Scotton, & Klimek, 2008; Tatin et al., 2000). Dense vegetation cover with tall vegetation provides abundant food resources (Gardiner et al., 2002). However, vegetation with bare soil areas can provide suitable environmental conditions for Orthoptera activity and egg development (Clark, 1948). Orthoptera with broad niches can therefore be encountered both in areas with dense herbaceous vegetation and in areas with sparse herbaceous vegetation (Gardiner et al., 2002) like for instance *C. wattenwylianus* and *Pezotettix giornae*. *C. wattenwylianus* is a species notably frequenting dry grasslands, dunes, fallows and field crops in Mediterranean phytoclimate (Defaut & Morichon, 2015) and *P. giornae* is a species that can be found in xeric or mesohumid areas and in grasslands with short or tall and dense vegetation (Defaut & Morichon, 2015). This may explain why, despite the differing habitats offered by the rehabilitated area, the edge or the surrounding reference steppe in our study, no significant differences were measured for Orthoptera assemblages.

All the species encountered during the study and forming the Orthoptera assemblages are common species to very common species in France and/or in the Bouches-du-Rhône department (Sardet, Roesti, & Braud, 2015) and are not classified as threatened species in France (Sardet & Defaut, 2004). The positive results highlighted in this study must be qualified in terms of biological conservation and in terms of typical assemblage of species characterizing La Crau area as only the common species were encountered. Indeed, La Crau area is well-known in France and in the world as a locality of rare or protected Orthoptera species, namely the Crau Plain Grasshopper (*Prionotropis rhodanica*) and the Predatory Bush Cricket (*Saga pedo*). The Crau Plain Grasshopper is listed as Critically Endangered on both French Red List (Sardet & Defaut, 2004) and IUCN Red List of threatened species (Hochkirch & Tatin, 2016). Its distribution is highly localized and no hypothetical presence in the vicinity of the site under rehabilitation is known. *S. pedo* is protected in France and the species has been identified once in a restoration treatment on the former orchard: the topsoil removal, a restoration treatment developed on 0.1 ha (Jaunatre, Buisson, & Dutoit, 2014b) and which was not considered for assessment of ecological restoration effects on insects (Alignan et al., 2014) as the size of the treatment was too small.

### 4.1. Orthoptera as early indicators of grassland rehabilitation success in a Natural Asset Reserve

Their rapid response to changes in land use, their strong capacity for colonization, their key role in the foodweb and their relative ease of sampling mean that Orthoptera can be considered really good early indicators to measure grassland habitat rehabilitation success. In years to come, Orthoptera can be used as a shortcut to assess progress on rehabilitation of the grassland in the abandoned orchard, replacing the time-consuming repeated annual vegetation survey (Dutoit et al., 2015; Jaunatre et al., 2014a). A long-term and adaptive monitoring (Lindenmayer & Likens, 2009) could then be considered by still focusing on assessing the progress on rehabilitation.

One of the main goals of the creation of the first Natural Asset Reserve in France was the return of the steppe birds typical of the La Crau area. The tall vegetation in the abandoned orchard must have been unfavorable for birds, particularly for predation. Studies on predation by birds show that insects are more accessible in low herbaceous layers (Belovsky & Slade, 1993; Joern, 1986; Tatin et al., 2000). Nevertheless, during the first years after rehabilitation of a grassland, steppe birds were encountered on the site (Dutoit et al., 2015; Wolff, 2010). Given the established importance of Orthoptera as prey for birds and lizard species in the steppe of La Crau (Foucart, 1997; Tatin et al., 2013), the Orthoptera recolonization on the Cossure area must have played a key role in the combined return of the typical steppe bird species. The hypothetical positive role of Orthoptera's return on steppe birds' return has not yet been quantified in this project making it difficult to judge. In the years to come, such an assessment would be wothwhile. It would also be necessary to test for no net loss of biodiversity in this compensation project given the importance, stakes and difficulties of offset assessment and achievement. The calculation should be based on calculating loss from development projects and gain from offsets through the rehabilitation project. Several solutions that could be considered have recently been suggested: a calculator to identify development scenarii in which no net loss is feasible using biodiversity offsetting (Gibbons et al., 2016) or a model describing all biodiversity elements with balance between losses at an impact site and gains at an offset site (Maseyk et al., 2016).

In La Crau area, the compensation is between the rehabilitation of a former intensive orchard on one hand and the construction of logistic platforms that is left in perpetuity on the other hand. True compensation would aim to renaturate an equivalent artificial area to that of developed, requiring subsequently much more time and effort than enhancing a degraded area (Moreno-Mateos, Maris, Béchet, & Curran, 2015).

The purchase of the 357 ha former Cossure orchard by CDC *Biodiversité* has had positive effects by: i) allowing the rehabilitation of a typical Mediterranean rangeland and ii) partially favoring the return of the typical steppe biodiversity (Alignan, Debras, & Dutoit, 2013; Dutoit et al., 2015; Jaunatre et al., 2014a; Wolff, 2010). Furthermore, in this enclave surrounded by the natural reserve of La Crau, the replacement of the conventional orchard by a rangeland will certainly have improved ecological continuum for typical species, thereby improving functional connectivity.

## 5. Conclusion

This study shows that Orthoptera can be used as indicators in an ecological restoration context, more precisely to assess the restoration of grassland vegetation for steppe birds. Orthoptera assemblages have been widely used as indicators. For instance, they have been used to indicate grassland naturalness (Báldi & Kisbenedek, 1997) or habitat quality (Bazelet & Samways, 2011). Our study further proves their usefulness as indicators and suggests that they could be a way to rapidly and easily assess the evolution of habitat restoration in post-restoration monitoring programs according to the time, scientific expertise and
funding available. The success of compensatory measures needs to be assessed both medium and long term in mitigation projects such as that in La Crau. Our findings suggest that Orthoptera could reliably be used to measure medium term grassland rehabilitation success in this first French Natural Asset Reserve.

## Acknowledgements

We are grateful to Marjorie Sweetko for the English language revision. We are also grateful to Caisse des Dépôts et Consignation Biodiversité, Région Provence-Alpes-Côte d'Azur, the Réserve Naturelle des Coussou de Crau and Domaine Bayard for supporting this study. We thank the UMR 1114 Environnement Méditerranéen et Modélisation des Agro-Hydrosystèmes research unit (INRA Avignon) for climatic data. We are also grateful to two anonymous reviewers for their comments that greatly improved earlier versions of this article.

## References

Alignan, J. F., Debras, J. F., & Dutoit, T. (2013). Quelles places pour les Coléoptères et les Orthoptères dans la restauration écologique de la plaine de Crau (Bouches-du-Rhône, France)? *Symbioses*, **31**, 9–15.

Alignan, J. F., Debras, J. F., & Dutoit, T. (2014). Effects of ecological restoration on Orthoptera assemblages in a Mediterranean steppe rangeland. *Journal of Insect Conservation*, **18**, 1073-1085. http://dx.doi.org/10.1007/s10841-014-9717-6.

Aronson, J., Floret, C., Le Floc'h, E., Ovale, C., & Pontanier, R. (1993). Restoration and rehabilitation of degraded ecosystems in arid and semi-arid lands. II. Case studies in Southern Tunisia, Central Chile and Northern Cameroon. *Restoration Ecology*, **1**, 168-187. http://dx.doi.org/10.1111/j.1526-100X.1993.tb00023.x.

Badan, O., Brun, J. P., & Congès, G. (1995). Les bergeries romaines de la Crau d'Arles. Les origines de la transhumance en Provence. *Gallia*, **52**, 263-310. http://dx.doi.org/10.3406/galia.1995.3152.

Báldí, A., & Kisbenedek, T. (1997). Orthopteran assemblages as indicators of grassland naturalness in Hungary. *Agriculture, Ecosystems and Environment*, **66**, 121-129. http://dx.doi.org/10.1016/S0167-8809(97)00068-6.

Batáry, P., Orci, K. M., Báldí, A., Kleijn, D., Kisbenedek, T., & Erdős, S. (2007). Effects of local and landscape scale and cattle grazing intensity on Orthoptera assemblages of the Hungarian Great Plain. *Basic and Applied Ecology*, **8**, 280-290. http://dx.doi.org/10.1016/j.baae.2006.03.012.

Bazelet, C. S., & Samways, M. J. (2011). Identifying grasshopper bioindicators for habitat quality assessment of ecological networks. *Ecological Indicators*, **11**, 1259-1269. http://dx.doi.org/10.1016/j.ecolind.2011.01.005.

BBOP (Business and Biodiversity Offsets Program) (2012). Biodiversity offset design handbook-updated. Washington, D.C: BBOP.

Bellmann, H., & Luquet, G. (1995). Guide des sauterelles, grillons et criquets d'Europe occidentale. Lausanne: Delachaux et Niestlé.

Belovsky, G. E., & Slade, J. B. (1993). The role of vertebrate and invertebrate predators in a grasshopper community. *Oikos*, **68**, 193-201.

Benjamini, Y., & Hochberg, Y. (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing. *Journal of the Royal Statistical Society Series B: Methodological*, **57**, 289-300.

Bigot, L., Chemseddine, M., & Delye, G. (1983). Contribution à la connaissance de la structure et de la dynamique de la communauté d'Arthropodes terrestres de la plaine désertifiée (ou coussou) de la Crau (Bouches-du-Rhône). *Biologie Ecologique Méditerranéenne*, **10**, 119-144.

Brown, P. H., & Lant, C. L. (1999). The effect of wetland mitigation banking on the achievement of no-net-loss. *Environmental Management*, **23**, 333-345.

Brumbaugh, R., & Reppert, R. (1994). National wetland mitigation banking study: First phase reportAlexandria, Virginia: Institute for Water Resources, Water Resources Support Center, US Army Corps of Engineers.

Buisson, E., & Dutoit, T. (2006). Creation of the natural reserve of La Crau: Implications for the creation and management of protected areas. *Journal of Environmental Management*, **80**, 318-326. http://dx.doi.org/10.1016/j.jenvman.2005.09.013.

Calvet, C., Napoléone, C., & Salles, J. M. (2015). The biodiversity offsetting dilemma: Between economic rationales and ecological dynamics. *Sustainability*, **7**, 7357-7378. http://dx.doi.org/10.3390/su7067357.

Chessel, D., Dufour, A. B., & Thioulouse, J. (2004). The ade4 package-I: one-table methods. *R News*, **4**, 5-10.

Chopard, L. (1951). *Faune de France. 56: Orthopteroïdes*, Vol. 56. Paris: Faune de France.

Clark, E. J. (1948). Studies in the ecology of British grasshoppers. *Transactions of the Royal Entomological Society of London*, **99**, 173-222. http://dx.doi.org/10.1111/j.1365-2311.1948.tb01235.x.

Colomb, E., & Roux, E. (1978). La Crau, données nouvelles et interprétations. *Géologie Méditerranéenne*, **5**, 303-324.

Defaut, B., & Morichon, D. (2015). *Faune de France. 97: Criquets de France (Orthoptera, Caelifera)*, Vol. 1. Paris: fascicule a. Faune de France.

Devaux, J. P., Archolope, A., Borel, L., Bourrelly, M., & Louis-Palluel, J. (1983). Notice de la carte phytoécologique de La Crau (Bouches-du-Rhône). *Biologie Ecologique Méditerranéenne*, **10**, 5-54.

Dray, S., & Dufour, A. B. (2007). The ade4 package: Implementing the duality diagram for ecologists. *Journal of Statistical Software*, **22**, 1-20.

Dupuy, F. (2009). *La perception des mouvements d'air par le système cercal chez le grillon des bois, Nemobius sylvestris* Tours: François Rabelais University Ph.D. Thesis.

Dutoit, T., Buisson, E., Gerbaud, E., Roche, P., & Tatoni, T. (2007). The status of transition zones between cultivated fields and their boundaries: Ecotones, ecoclines or edge effects? *Acta Oecologica*, **31**, 127-136. http://dx.doi.org/10.1016/j.actao.2006.03.010.

Dutoit, T., Buisson, E., Fadda, S., Henry, F., Coiffait-Gombault, C., Jaunatre, R., et al. (2013). *The pseudo-steppe of La Crau (South-Eastern France): Origin, management and restoration of a Mediterranean rangeland. Steppe ecosystems: Biological diversity, management and restoration*. USA: Nova Publishers287-301.

Dutoit, T., Calvet, C., Jaunatre, R., Alignan, J. F., Wolff, A., Sauguet, F., et al. (2015). Première expérimentation de compensation par l'offre: bilan et perspective. *Sciences, Eaux et Territoires*, **16**, 64-69.

Evans, E. W. (1984). Fire as a natural disturbance to grasshopper assemblages of tallgrass prairie. *Oikos*, **43**, 9-16.

Foucart, A. (1997). Inventaire et dynamique annuelle du peuplement acridien de la plaine de la Crau sèche (Bouches-du-Rhône, France) (Orthoptera, Arcloidea). *Bulletin de la Société Entomologique de France*, **102**, 87-87.

Fuhlendorf, S. D., Engle, D. M., Arnold, D. C., & Bidwell, T. G. (2002). Influence of herbicide application on forb and arthropod communities of North American tallgrass prairies. *Agriculture, Ecosystems & Environment*, **92**, 251-259. http://dx.doi.org/10.1016/S0167-8809(01)00291-2.

Gardiner, T., Pye, M., Field, R., & Hill, J. (2002). The influence of sward height and vegetation composition in determining the habitat preferences of three *Chorthippus* species (Orthoptera: Acrididae) in Chelmsford, Essex, UK. *Journal of Orthoptera Research*, **11**, 207-213.

Gardiner, T., Hill, J., & Chesmore, D. (2005). Review of the methods frequently used to estimate the abundance of Orthoptera in grassland ecosystems. *Journal of Insect Conservation*, **9**, 151-173. http://dx.doi.org/10.1007/s10841-005-2854-1.

Gibbons, P., Evans, M. C., Maron, M., Gordon, A., Le Roux, D., von Hase, A., et al. (2016). A loss-gain calculator for biodiversity offsets and the circumstances in which no net loss is feasible. *Conservation Letters*, **9**, 252-259.

Guido, M., & Gianelle, D. (2001). Distribution patterns of four Orthoptera species in relation to microhabitat heterogeneity in an ecotonal area. *Acta Oecologica*, **22**, 175-185. http://dx.doi.org/10.1016/S1146-609X(01)01109-2.

Henry, F., Talon, B., & Dutoit, T. (2010). The age and history of the French Mediterranean steppe revisited by soil wood charcoal analysis. *The Holocene*, **20**, 25-34. http://dx.doi.org/10.1177/0959683609348841.

Hochkirch, A., & Tatin, L. (2016). *Prionotropis rhodanica*. The IUCN Red List of Threatened Species 2016: e.T15038481A47713628. Downloaded on 13 June 2017 https://doi.org/10.2305/IUCN.UK.2016-3.RLTS.T15038481A47713628.en.

Hochkirch, A., Witzenberger, K. A., Teerling, A., & Niemeyer, F. (2007). Translocation of an endangered insect species, the field cricket (*Gryllus campestris* Linnaeus, 1758) in northern Germany. *Biodiversity and Conservation*, **7**, 355-365. http://dx.doi.org/10.1007/978-1-4020-6865-2-25.

Jaunatre, R., Buisson, E., & Dutoit, T. (2012). First-year results of a multi-treatment steppe restoration experiment in La Crau (Provence, France). *Plant, Ecology and Evolution*, **145**, 13-23. http://dx.doi.org/10.5091/plecevo.2012.690.

Jaunatre, R., Buisson, E., Muller, I., Morlon, H., Mesléard, F., & Dutoit, T. (2013). New synthetic indicators to assess community resilience and restoration success. *Ecological Indicators*, **29**, 468-477. http://dx.doi.org/10.1016/j.ecolind.2013.01.023.

Jaunatre, R., Buisson, E., & Dutoit, T. (2014a). Can ecological engineering restore Mediterranean rangeland after intensive cultivation? A large-scale experiment in southern France. *Ecological engineering*, **64**, 202-212. http://dx.doi.org/10.1016/j.ecoleng.2013.12.022.

Jaunatre, R., Buisson, E., & Dutoit, T. (2014b). Topsoil removal improves various restoration treatments of a Mediterranean steppe (La Crau, southeast France). *Applied Vegetation Science*, **17**, 236-245.

Joern, A. (1982a). Distributions, densities, and relative abundances of grasshoppers (Orthoptera: Acrididae) in a Nebraska sandhills prairie. *The Prairie Naturalist*, **14**, 37-45.

Joern, A. (1982b). Vegetation structure and microhabitat selection in grasshoppers (Orthoptera, Acrididae). *The Southwestern Naturalist*, **27**, 197-209.

Joern, A. (1986). Experimental study of avian predation on coexisting grasshopper populations (Orthoptera: Acrididae) in a sandhills grassland. *Oikos*, **46**, 243-249.

Kemp, W. P., Harvey, S. J., & O'Neill, K. M. (1990). Patterns of svegetation and grasshopper community composition. *Oecologia*, **83**, 299-308. http://dx.doi.org/10.1007/BF00317552.

Kovacs, M., Podani, J., Tuba, Z., Turcsanyi, G., Csintalan, Z., & Meenks, J. L. D. (1992). *Biological indicators in environmental protection*. London, U.K: Ellis Horwood.

Lee Foote, A., & Rice Hornung, C. L. (2005). Odonates as biological indicators of grazing effects on Canadian prairie wetlands. *Ecological Entomology*, **30**, 273-283. http://dx.doi.org/10.1111/j.0307-6946.2005.00701.x.

Léonide, J. C. (1983). Richesse et intérêt du foyer acridien grégarigène et du foyer parasitogène acridophage de la Crau. *Biologie Ecologique Méditerranéenne*, **10**, 145-154.

Lindenmayer, D. B., & Likens, G. E. (2009). Adaptive monitoring: A new paradigm for long-term research and monitoring. *Trends in Ecology and Evolution*, **24**, 482-486. http://dx.doi.org/10.1016/j.tree.2009.03.005.
Malagnoux, L., Marliac, G., Simon, S., Rault, M., & Capowiez, Y. (2015). Management strategies in apple orchards influence earwig community. *Chemosphere*, *124*, 156–162. http://dx.doi.org/10.1016/j.chemosphere.2014.12.024.

Marini, L., Fontana, P., Scotton, M., & Klimek, S. (2008). Vascular plant and Orthoptera diversity in relation to grassland management and landscape composition in the European Alps. *Journal of Applied Ecology*, *45*, 361–370. http://dx.doi.org/10.1111/j.1365-2664.2007.01402.x.

Maseyk, F. J. F., Barea, L. P., Stephens, R. T. T., Possingham, H. P., Dutson, G., & Maron, M. (2016). A disaggregated biodiversity offset accounting model to improve estimation of ecological equivalency and no net loss. *Biological Conservation*, *204*, 322–332. http://dx.doi.org/10.1016/j.biocon.2016.10.016.

Mazzia, C., Pasquet, A., Caro, G., Thénard, J., Cornic, J. F., Hedde, M., et al. (2015). The impact of management strategies in apple orchards on the structural and functional diversity of epigeal spiders. *Ecotoxicology*, *24*, 616–625. http://dx.doi.org/10.1007/s10646-014-1409-1.

McGeoch, M. A. (1998). The selection, testing and application of terrestrial insects as bioindicators. *Biological Reviews*, *73*, 181–201. http://dx.doi.org/10.1111/j.1469-185X.1997.tb00029.x.

McKenney, B. A., & Kiesecker, J. M. (2010). Policy development for biodiversity offsets: A review of offset frameworks. *Environmental Management*, *45*, 165–176. http://dx.doi.org/10.1007/s00267-009-9396-3.

Meffe, G. K., & Carroll, C. R. (1994). *Principles of conservation biology*. Sunderland, Massachusetts: Sinauer Associates, Inc.

Moreno-Mateos, D., Maris, V., Béchet, A., & Curran, M. (2015). The true loss caused by biodiversity offsets. *Biological Conservation*, *192*, 552–559. http://dx.doi.org/10.1016/j.biocon.2015.08.016.

Noss, R. F. (1990). Indicators for monitoring biodiversity: A hierarchical approach. *Conservation Biology*, *4*, 355–364. http://dx.doi.org/10.1111/j.1523-1739.1990.tb00309.x.

Oksanen, J., Kindt, R., Legendre, P., O'Hara, B., Simpson, G. L., Henry, M., et al. (2008). *Vegan: Community ecology package*. R package version 1.13-1.

Picaud, F., & Petit, D. P. (2007). Primary succession of acrididae (Orthoptera): Differences in displacement capacities in early and late colonizers of new habitats. *Acta Oecologica*, *32*, 59–66. http://dx.doi.org/10.1016/j.actao.2007.03.005.

Quétier, F., & Lavorel, S. (2011). Assessing ecological equivalence in biodiversity offset schemes: Key issues and solutions. *Biological Conservation*, *144*, 2991–2999. http://dx.doi.org/10.1016/j.biocon.2011.09.002.

Quétier, F., Regnery, B., & Levrel, H. (2014). No net loss of biodiversity or paper offsets? A critical review of the French no net loss policy. *Environmental Science & Policy*, *38*, 120–131. http://dx.doi.org/10.1016/j.envsci.2013.11.009.

R Development Core Team (2013). *R: A language and environment for statistical computing*. Vienna, Austria: R Foundation for Statistical Computing.

Regnery, B., Couvet, D., & Kerbiriou, C. (2013). Offsets and conservation of the species of the EU habitats and birds directives. *Conservation Biology*, *27*, 1335–1343. http://dx.doi.org/10.1111/cobi.12123.

Robertson, M. M. (2004). The neoliberalization of ecosystem services: Wetland mitigation banking and problems in environmental governance. *Geoforum*, *35*, 361–373. http://dx.doi.org/10.1016/j.geoforum.2003.06.002.

Sardet, E., & Defaut, B. (2004). Les Orthoptères menacés en France. Liste rouge nationale et listes rouges par domaines biogégraphiques. *Matériaux Orthoptériques et Entomocénotiques*, *9*, 125–137.

Sardet, E., Roesti, C., & Braud, Y. (2015). *Cahier d'identification des Orthoptères de France, Belgique, Luxembourg et Suisse*. Mèze: Biotope (collection Cahier d'identification), 304p.

Tanet, J., & Gicquiaux, M. C. (2013). *Contribution à la connaissance de la biomasse des Arthropodes en plaine de Crau*. Marseille: University of Aix-Marseille M. Sc. Thesis.

Tatin, L., Dutoit, T., & Feh, C. (2000). Impact du pâturage par les chevaux de Przewalski (Equus przewalskii) sur les populations d'Orthoptères du Causse Méjean (Lozère, France). *Revue d'Ecologie (Terre et Vie)*, *55*, 241–261.

Tatin, L., Chapelin-Viscardi, J. D., Renet, J., Becker, E., & Ponel, P. (2013). Patron et variations du régime alimentaire du lézard ocellé *Timon lepidus* en milieu steppique méditerranéen semi-aride (plaine de Crau, France). *La Terre et la Vie* (Revue d'Ecologie), *68*, 47–58.

UICN (Union Internationale pour la Conservation de la Nature) France (2011). *La compensation écologique: Etat des lieux et recommandations*. Paris, France: UICN.

Venables, W. N., & Ripley, B. D. (2002). *Modern applied statistics with S* (fourth edition). New-York: Springer.

Vincent-Martin, N., Wolff, A., Paulus, G., & Tatin, L. (2013). *Les oiseaux steppiques. Ecologie et conservation d'une steppe méditerranéenne: La plaine de Crau*. France: Editions Quae130–140.

Wolff, A. (2010). *Rapport d'activité 2010 de la Réserve Naturelle des Coussouls de Crau*. Saint-Martin-de-Crau: RNCC – CEN PACA.