Changes in habitat selection patterns of the gray partridge Perdix perdix in relation to agricultural landscape dynamics over the past two decades

Abstract Changes in agricultural practices have reshaped agricultural landscapes and triggered a drastic decline in spatial and temporal heterogeneity leading to changes in habitat quality and food resources for birds. However, the precise relationships between landscape changes, spatial and temporal heterogeneity, and habitat preferences in response to those changes remain poorly known. We investigated patterns of habitat selection and causes for changes over the years 1997–2017 for the gray partridge Perdix perdix, an iconic farmland species which has experienced a severe decline since the 1950s. Using a long‐term (1997–2017) dataset collected over 435 km2, we modeled relationships between annual land‐cover maps and partridge sightings over 17 5‐year moving windows, assessing the effects of landscape metrics, the strength of the relationships, and the dynamics of habitat suitability. We detected a shift in gray partridge habitat preferences over time, toward more risky habitats. Avoidance of predator reservoirs (woodlands and buildings) has weakened, and selection of human infrastructure, such as roads and tracks, has increased. Since 1997, the mean size of suitable patches has also decreased by about 26%. We have interpreted these changes in habitat selection as being the result of decreasing habitat quality and the increasing prevalence of captive‐reared birds, currently released in their thousands in the study site. Synthesis and applications. The gray partridge has not adjusted well to changes in farming practices, and the low, still decreasing, population density suggests that it is not sustainable, despite local initiatives and the investment in captive‐bird releases. We emphasize that efforts must be redirected toward habitat improvement to restore the density of refuge cover, insects, and seeds in the landscape, hunting management to ensure self‐sustainable populations and massive releases of high‐quality birds. Only integrated local management, involving hunters, farmers, gamekeepers, and scientists can ensure the recovery of this species.


| INTRODUC TI ON
For decades, evidence has accumulated that the main driver of the decline in farmland biodiversity lies in the rapid postwar changes in agricultural practices (Benton, Vickery, & Wilson, 2003;Krebs, Wilson, Bradbury, & Siriwardena, 1999;Robinson & Sutherland, 2002). Agricultural intensification and specialization have reshaped and simplified agricultural landscapes (Benton et al., 2003). The resulting loss of spatial and temporal heterogeneity has degraded habitat quality and food resources, resulting in severe declines in European farmland birds (Benton et al., 2003;Chamberlain, Fuller, Bunce, Duckworth, & Shrubb, 2000;Robinson & Sutherland, 2002).
Though agricultural landscapes cover about 40% of the earth's terrestrial biomes, and are highly dynamic, long-term changes in agricultural landscapes have seldom been quantified: only seven (3%) in a review of 244 studies assessing land-cover changes (Uuemaa, Mander, & Marja, 2013). The scarcity in such studies comes from the challenge of accessing land-cover data over the long term (Bertrand, Burel, & Baudry, 2016) as well as the complexity of analyzing interacting landscape features, each with their own spatio-temporal dynamics. For instance, in intensive agricultural landscapes, buildings, roads, hedgerows, and woodlands have broadly remained stable over the years, while crops change annually in a quasi-stochastic spatial pattern of crop rotation (Bretagnolle et al., 2018b). As a result, very few studies have investigated the temporal changes in habitat selection by farmland birds associated with the temporal changes in the agricultural landscape (but see Brambilla et al., 2010), despite the behavioral process of habitat selection being critical in determining population dynamics, survival, and productivity (Jones, 2001).
The gray partridge Perdix perdix L. used to be one of the most common farmland birds in Europe, but has been in a steep, widespread decline since the mid-20th century (Aebischer & Potts, 1994;Gée, Sarasa, & Pays, 2018;Sotherton, Aebischer, & Ewald, 2014). In many European countries, numbers are at <10% of their prewar level (Aebischer & Kavanagh, 1997). For example, the drop in abundance was estimated at 92% between 1970 and 2015 in the UK, and it is now a red-listed species in the UK Birds of Conservation Concern (Hayhow et al., 2017). Despite a decline of 23% in abundance from 1989 to 2015 (Vigie-Nature, 2018) and 20% in the distribution range from 1985 to 2013 (Comolet-Tirman et al., 2015), gray partridge is still considered as "Least Concern" in France. The decline was attributed to three main causes, all linked to the decrease in habitat quality resulting from agricultural intensification: the loss of breeding habitat, the decrease in availability of insects for chicks, and the concentration of partridges and predation pressure in remaining habitats (Aebischer & Ewald, 2012). Gray partridge habitat selection has been well studied: At a large scale, the species avoids woodlands, associated with high predation risk, as woodlands are predator reservoirs (Dudzinski, 1992), and also avoids the proximity of buildings with their predation risks from cats and mustelids (Reitz, Le Goff, & Fuzeau, 2002). At a more local scale, during the breeding season, gray partridges were found to be attracted by cereal cover, with a high nesting success rate, (Bro et al., 2013;Bro, Reitz, & Mayot, 1998), rape and grassy covers (Birkan, Serre, Skibnienski, & Pelard, 1992;Bro et al., 2013), crop diversity (Reitz et al., 2002), and linear features such as hedgerow fragments, roads, and tracks (Blank, Southwood, & Cross, 1967;Bro et al., 2013;Potts & Aebischer, 1991), even though these linear features are associated with lower nesting success (Bro et al., 1998). However, with a few exceptions (Reitz et al., 2002;Ronnenberg, Strauß, & Siebert, 2016), in most studies, the effects of landscape features have been studied independently from each other so that the relative contributions of different landscape features on gray partridge habitat selection remain unknown. Even less is known about potential changes in patterns of habitat selection over time in highly dynamic agricultural landscapes.
Here, we investigated long-term trends in gray partridge habitat preferences in a French farmland landscape, through a multistep approach using data collected annually in an area of 435 km 2 over 21 years (from 1997 to 2017). We first identified the key landscape features that explain the gray partridge occurrence over 1997-2017 studying the variable contributions to the probability of occurrence.
Contributions reflect the importance of variables to explain (or predict) the occurrence of a species and are commonly used to identify the key drivers of species distribution (e.g., Bellard, Leroy, Thuiller, Rysman, & Courchamp, 2016;Wilson, Sexton, Jobe, & Haddad, 2013). Secondly, to explore whether and how the habitat selection patterns have varied with changes in the landscape, we quantified changes in the relative contributions and effect of landscape features on gray partridge occurrence with time, over 17 5-year moving windows. Thirdly, we investigated whether overall habitat suitability for gray partridge has changed over time, using as reference the oldest habitat preferences of gray partridge available (i.e., models based on data from 1997 to 2001; see Pearman, Guisan, Broennimann, & Randin, 2008). In this study area, significant changes in land-cover, for example, a 20% increase in cereal cover since 1994 (Bretagnolle et al., 2018b) and a decrease in insect availability (Bretagnolle et al., 2011) have been recorded while observed partridge densities have strongly decreased (Figure 1b) despite huge annual releases of captive-reared birds to maintain local partridge populations (Bro & Crosnier, 2012). Given this observed decline in the study population associated with the relatively stable amount of captive-reared gray partridges annually released in France from 1995 to 2015 (around 2 million individuals in Bro, 2016), we therefore, assumed that the population in our study area has changed from mainly wild birds in  Year Number of gray partridge sightings per km² the nineties to mainly released captive-reared birds currently. We thus suggested the massive releases of captive-reared birds as a potential driver of changes in the pattern of habitat preferences.
Indeed, we might expect that naïve partridges would be less likely to avoid predator-rich habitats. If there has been a general decline in habitat quality, partridges may select the least altered or highest quality habitats. Although habitat selection is density dependent (Morris, 1989), over the same period the population of partridges has strongly declined, so that habitat preferences may have remained targeted to the highest quality habitats.

| Study site and environmental layers
The Long-Term Socio-Ecological Research platform (LTSER) "Zone Atelier Plaine & Val de Sèvre" is located in Central Western France, Nouvelle-Aquitaine region ( Figure 1a, Bretagnolle et al., 2018b). This area is characterized by an intensive agricultural landscape for cereal production. Land-cover has been exhaustively surveyed annually from 1994 onward using more than 40 crop categories. Winter cereals largely dominate (41.5%, mean value calculated over the years 2009-2016), followed by sunflower (10.4%), maize (9.6%), rape (8.3%), and meadows (13.5%). Woodland fragments represent 2.9% of the study area (excluding the Chizé forest) and 9.8% of built-up areas (including isolated buildings). A preliminary analysis of landscape features showed that the density of hedgerows, buildings, and woodlands has varied little, whereas the areas of cereals, meadows, and rape, as well as crop diversity and the size of crop patches, have changed far more over the period (Figure 1c,d, Supporting Information Figure S1 and Table S1 for statistical details). In addition, crop locations change annually because of crop rotation.
The vector based GIS was first transformed into a grid of 200 × 200 m 2 cells (4 ha), using R (R Core  and QGIS (Quantum GIS Development Team, 2017), excluding all pixels that had less than half their area intersecting with the study area. The pixel size was chosen to have a meaningful fine scale resolution in relation to landscape dynamics that was close to the average field size (Bretagnolle et al., 2018b). Landscape features already identified in the literature as being selected by gray partridges were chosen for analyses as potential predictors of the gray partridge occurrence: cereals, rape, meadows, hedgerows, roads, and tracks (Birkan et al., 1992;Blank et al., 1967;Bro et al., 2013), and woodland and buildings, features that partridges avoid (Dudzinski, 1992;Reitz et al., 2002). The landscape metrics (i.e., layers assessing landscape  Table S2). Each of these seven metrics was calculated for each of the 21 years from 1997 to 2017 giving 147 map layers. Roads, tracks, and hedgerows have remained fairly stable over the period (Supporting Information Appendix S1, Figure S1) so one map layer was used for roads and tracks and three layers for hedgerows in 2006, 2011, and 2014 when aerial photographs were available. A total of 151 layers were, therefore, included.

| Partridge data
In total, there were 989 sightings of gray partridges in three distinct datasets covering 1997 to 2017 ( Figure 1e). The largest dataset (90% of total data) comprised opportunistic sightings either when ornithologists working in the LTSER were studying other bird species (Bretagnolle et al., 2018b) and saw partridges, or during the landcover surveys carried out twice a year systematically over the entire study site. Each year, opportunistic sightings were reported daily between late March and late July (see Figure 1f). In this dataset, the observation effort is not standardized and reporting is not systematic.
In the second dataset, with 5% of total sightings, observation pressure is standardized as this dataset collates the results from system-  Table S1 for statistical details

| Species distribution models
A multistep approach using species distribution modeling was carried out to (a) identify key landscape features and their effect on the gray partridge occurrence over the entire period 1997-2017; (b) explore trends in the contribution of key features and in their effect over 17 successive 5-year moving periods; (c) assess changes in habitat suitability for gray partridge over time.

| Modeling process
The following modeling process was first applied over the entire study period  to investigate the general pattern of habitat selection. Each landscape metric was pooled over the entire study period 1997-2017 (calculating an average value by pixel).
To perform the trend analysis assessing changes in habitat selection patterns, the modeling process was also applied using a 5-year mov-

| Assessing the contribution of each landscape metric
The

| Effect of landscape metrics on the gray partridge occurrence
The relationship between landscape metrics and the probability of the occurrence of gray partridge was assessed using the average response curves from GLMs calibrated on 100% of the data.

| Trends in the relation between partridge occurrence and landscape metrics
To test whether time (explanatory variable) had a significant effect on the contribution (response variable) of landscape metrics, we used a generalized least squares (GLS) model using the nlme package. To handle autocorrelation in our time series, we run an autocorrelation function on each dependent variable to identify the time lag after which the non-autocorrelation assumption was confirmed at 95% confidence level (Shumway & Stoffer, 2011). Then, GLSs were implemented with an autoregressive moving average (ARMA) term in which the moving average (MA) errors were accounted for using the maximum time lag determined in the previous step. The lack of sequential autocorrelation in the residuals was checked using the acf function. The 5-year moving average windows allow a smoothing effect in the shape of the relationship between time and variable contribution. Finally, we included a quadratic time term in the GLS models and used backward stepwise selection procedure (Faraway, 2005).
The curves for each of four contiguous windows (1997-2001, 2002-2006, 2007-2011, and 2012-2016) were also drawn for each landscape metric that both made a large contribution and changed significantly with time.

| Habitat suitability maps and trends in habitat quality
We

| RE SULTS
First, we investigated the key landscape metrics explaining the gray partridge occurrence over the study period , and their effect on gray partridge occurrence. Of the nine candidate explanatory variables, cereal density, distance to woodlands, and distance to the nearest building were the metrics with the highest contributions when fitting to the aggregated dataset for 1997-2017 (contributions >0.1, Figure 2; Supporting Information Table S3). Most response curves were quadratic: Moderate values of cereal density (25%-65%) and distance to woodlands (300-1,310 m) were preferred by partridges while extreme values were avoided (Figure 3). Partridges also preferred being more than 125 m from a building (Figure 3).  Information Table S4). For example, the contribution of cereal density was variable in the first few years and then increased in the last 15 years. This increase in contribution was associated with a decrease of sightings in areas with low cereal density unselected Contributions of landscape metrics to models calibrated on the whole 21-year period (black) and cumulative contributions to models calibrated on the four contiguous 5-year periods (1997-2001, 2002-2006, 2007-2011, 2012-2016 Table   S6). Recently, partridges appeared to avoid woodlands and to buildings less, as the contributions of these metrics decreased (Figure 4, Supporting Information Table S4). Currently, partridges prefer areas closer to woodlands (distance to woodlands is 19.5% shorter) than at the start of the study period ( Table S6). In 1997-2001, 13% of sightings were collected at a distance lower than 160 m to buildings, against 21% in 2012-2016 (Supporting Information Table S5). The contribution of the size of crop patches decreased while that of hedgerow density increased, but both contributions were small (Supporting Information Figure S2, Table S4).
Finally, we assessed the trends in habitat suitability with time.
Habitat suitability maps calibrated on the first period (1997)(1998)(1999)(2000)(2001) and  Table S7). Even though the quality of our models remained relatively low (TSS = 0.42 ± 0.03 for the seventeen 5-year periods, Supporting Information Table S3), it was high enough to be considered useful being above the recognized threshold of 0.4 (Engler et al., 2011;Zhang et al., 2015).

| D ISCUSS I ON
Despite many releases of captive-reared birds in the study area, the population of gray partridges has suffered a drastic decline over the last 21 years. While we observed a general decrease in the size and suitability index of suitable patches, our study showed that occurrence of partridges has changed with landscape features.
Considering the overall 21-year period , the density of cereals, the distance to woodlands, and the distance to the nearest building were identified as the main contributors or key drivers of F I G U R E 3 Probability of occurrence of gray partridge as a function of the landscape metrics that contributed most. Dashed lines represent the mean probability of occurrence below the cutoff, dotted lines represent 95% confidence intervals, and solid lines represent the range of values selected by gray partridge (above the cutoff, see Methods) Road density (m/ha) Distance to buildings (m) Cereal density D istance to woodland (m) Values of landscape metrics Probability of occurrence gray partridge occurrence (Bellard et al., 2016;Wilson et al., 2013).
Cereals is well known as the main breeding cover selected by gray partridges (69% of nests in Bro et al., 2013), associated with high nesting success (Bro et al., 1998). However, the response curve shows saturation, indicating a need for complementary habitats, for example, rape for food (Birkan et al., 1992). High contributions F I G U R E 4 Top: contributions (black dots) of landscape metrics in the 5-year moving window. Solid lines show the trends from the GLS model with autoregressive moving average (see Table S4 for statistical details). The dashed line represents the threshold used to distinguish the landscape metrics that contributed most to the models (Capinha & Anastácio, 2010;Leroy et al., 2013). Error bars correspond to the standard deviation of the contributions. Bottom: Probability of occurrence of gray partridge as a function of the landscape metrics for the four contiguous 5-year periods (1997-2001, 2002-2006, 2007-2011, 2012-2016). Dashed lines represent the mean probability of occurrence below the cutoff, dotted lines represent 95% confidence intervals, and solid lines represent the range of values selected by gray partridge (above the cutoff, see Methods)

Cereal density
Distance to woodland (m) Road density (m/ha) Distance to buildings ( of distances to woodlands and buildings were expected because of avoidance of carnivore reservoirs (Dudzinski, 1992;Reitz et al., 2002;Reitz & Mayot, 1999), and woodlands have already been identified as the main driver of gray partridge distribution at local district scale (Ronnenberg et al., 2016). For the four 5-year contiguous periods, the distance to buildings was less important while road density was more important. Partridges avoided low road densities, as nesting sites are frequently close to roads (25% of nests located in cereals, Bro et al., 2013), but they also avoided high road densities, either because of predation risk (Reitz & Mayot, 1999) or disturbance by traffic (Fahrig & Rytwinski, 2009). Although the population was mainly captive bred, this suggests that the partridges showed patterns of habitat selection that were driven by well-known ecological requirements.
An unexpected result is that there was a strong increase in the contribution of cereals to explain the gray partridge occurrence over the past 15 years. As the cereal density has increased by about 20% of the preexisting density observed in 1997 (Bretagnolle et al., 2018b), this cover has become more widespread, and a subsequent decrease in the contribution of cereals might be expected. The selection and high nesting success of cereals (Bro et al., 2013(Bro et al., , 1998 associated with the depletion of gray partridge densities may explain this result. The depletion would have been higher in the low and unselected densities, as supported by the decreasing number of sightings in areas providing low cereal densities. The other main result is the decreasing contributions of distances to woodlands, buildings, on the partridge occurrence, associated with increasing proportions of partridge sightings close to these predator-rich features. While these landscape features have remained fairly stable over time, this suggest that partridges became less likely to avoid woodlands and buildings (predator reservoirs), and roads (high exposure to predation; Reitz & Mayot, 1999), though they were expected to select the best quality habitats. Nonetheless, lower avoidance of roads could also be partly explained by the decreasing partridge density associated with the opportunistic nature of sightings, usually collected from roads.
Such shifts in gray partridge habitat preferences toward more risky habitats associated with lower survival expectancy have already been described and explained by captive rearing of partridge and other galliformes, lacking antipredator behavior (Rantanen, Buner, Riordan, Sotherton, & Macdonald, 2010a,2010bSokos, Birtsas, & Tsachalidis, 2008). Furthermore, captive-reared birds could also suffer from natal habitat preference induction (Stamps & Swaisgood, 2007), encouraging them to select anthropogenic features similar to those where they were reared. However, as habitat selection impairing fitness has also been documented in wild gray partridges (Bro, Mayot, Corda, & Reitz, 2004) and other farmland birds (e.g., the yellow wagtail Motacilla flava in Gilroy, Anderson, Vickery, Grice, & Sutherland, 2011), there may be another explanation. This shift in habitat selection pattern could be linked to a behavioral adjustment to the decreasing habitat quality and food availability. For instance, over the last 30 years, seed availability has dropped faster in field cores than at field edges (Fried, Petit, Dessaint, & Reboud, 2009).
Partridges could therefore avoid roads less, as roadside habitats may provide more insect and seed food (Hopwood, 2008;von der Lippe, Bullock, Kowarik, Knopp, & Wichmann, 2013), and higher seed abundance has already been linked to higher densities of farmland birds, including gray partridge (Moorcroft, Whittingham, Bradbury, & Wilson, 2002 6,560,000 6,570,000 6,580,000 6,560,000 6,570,000 6,580,000 6,560,000 6,570,000 6,580,000 6,560,000 6,570,000 6,580,000 in the contribution of cereal density as the decrease in landscape diversity would encourage partridges to prefer this cover which is associated with a high nesting success rate (Bro et al., 2013(Bro et al., ,1998. The continuous drop in habitat quality caused by agricultural intensification could have increased the concentration of prey and the predation pressure on the remaining suitable patches (Aebischer & Ewald, 2012). This raises concern about low-density populations, which may be particularly damaged as a result of a behaviorally mediated Allee effect: There is no competition for space and individuals are free to select their preferred, though possibly associated with lower survival, habitats (Kokko & Sutherland, 2001).

| Implications for management
The gray partridge study population, with a current density of around 1 male (or pair) per 400 ha, may not be sustainable. Additionally, the observed changes in habitat selection toward more risky habitats could impair the situation and may be exacerbated by releases of captive-reared birds, documented to suffer deficiencies in antipredator behavior, poor survival, and breeding success (Parish & Sotherton, 2007;Rantanen, Buner, Riordan, Sotherton, & Macdonald, 2010b). Therefore, initiatives releasing captive-reared birds (about 250 birds per 1700 ha, the mean area of a local community) may actually precipitate, rather than mitigate, the fate of local populations, since these naïve birds outnumber wild individuals (Reitz, 2003;Sokos et al., 2008). Furthermore, these costly release programs, about €55k to €60k each year in the LTSER (36 hunting associations × 250 birds × €6.5), have so far failed to help the population recover, as numbers are still declining in the LTSER and the surrounding countryside. Extrapolating to other gamebird species (€55-€60k per year for red-legged partridges and €45-€50k for ringnecked pheasants), the costs of supplementing the local populations of gamebirds can be estimated at €155-€170k per year in our study area, with no perceivable improvement in population sustainability.
This does not imply that reinforcement is an invalid strategy, since several conservation programs would have sustainably increased partridge densities (Bro, 2016;Browne, Buner, & Aebischer, 2009;Buner & Aebischer, 2008). These programs, however, included supplementary feeding, reestablishment of refuge covers and insectrich habitats for chicks (set-asides, grassy strips along field edges, field divisions, game covers), and nest protection or predation control when needed to accelerate population recovery (Aebischer, 2009;Aebischer & Ewald, 2012;Bro, 2016). In our study area, money saved by reducing by half the amount of captive-reared bird released (i.e., by €80k) might be reallocated to create, for example, 270 ha of setasides or wildlife covers, or a maintenance of 40 km 2 (i.e., 1/5 of the cereal area) of stubble fields until the end of the chick-rearing period.
In addition, the origin of the released birds was identified as a critical factor in success whether the aim was game management or conservation (Fischer & Lindenmayer, 2000;Griffith, Scott, Carpenter, & Reed, 1989). For instance, Sokos et al. (2008) reported a failure to re-establish a pheasant population in a release program involving 3,000 captive-reared birds, while the release of 1,000 wild-caught individuals succeeded.
In the case of the gray partridge, we believe that we need to change from releasing captive-reared gamebirds for "put and take" shooting (Sokos et al., 2008), to conservation programs aiming to restore self-sustaining populations. Efforts should be redirected toward habitat improvement through selected agricultural practices, to greatly increase refuge covers, insects, and seeds in the landscape, with hunting restrictions to ensuring that the bird populations are self-sustaining, coupled with releases of wildcaught or predator-trained birds (Sokos et al., 2008). Creating synergy between all stakeholders, hunters, farmers, and scientists is, however, critical to achieve such integrated, local biodiversity management.

ACK N OWLED G M ENTS
This study was possible thanks to the financial support of the Fédération Nationale des Chasseurs (FNC-PSN-PR15-2014). We thank all fieldworkers who contributed to data collection, and particularly Maxime Saillard for his dedicated work in digitalizing the partridge sightings. We also thank Nicholas Aebischer, Elisabeth Bro, and Jérome Moreau for their helpful comments, and Karen Fournier for her graceful English corrections.