Extensive sheep grazing is associated with trends in steppe birds in Spain: recommendations for the Common Agricultural Policy

Introduction

European natural and semi-natural open habitats, such as steppes, uplands and moorlands (natural steppes hereinafter), are generally the result of altitudinal/climatic and edaphic tree-limiting conditions, and regular low-intensity human disturbances such as low-yield agriculture, fire or livestock (Carboni et al., 2015). All these factors have shaped the characteristic open, treeless landscape of such habitats (Newton, 2004; Douglas et al., 2017), which harbors high biodiversity values (Carboni et al., 2015). In these economically disadvantaged areas, sheep systems have been decisive in maintaining rural livelihoods, but also providing several ecosystem services, such as protecting biodiversity and maintaining natural resources (Spiegel et al., 2019). However, sheep farm income in the European Union is supported by public subsidies, such as the Common Agricultural Policy (Bertolozzi, 2021) (CAP hereinafter), which makes the sector strongly dependent on changes in the policy framework (De Rancourt et al., 2006; Castillo et al., 2008; Reino et al., 2010).

Several works have suggested the existence of a complex system of multiple interactions where extensive sheep grazing affects plant structure spatial heterogeneity and plant species composition (Kurek et al., 2016; Adler, Raff & Lauenroth, 2001; Bugalho et al., 2011), as well as arthropod abundance both directly through its depositions and indirectly, by increasing habitat heterogeneity (Bugalho et al., 2011; Vickery et al., 2001; Dennis et al., 2008). Heavy levels of grazing have proven to be disadvantageous for a large number of farmland and steppe birds, due to overconsumption of plants and high fertilization (Fuller, 1996). However, light or moderate grazing may have positive effects since grazing decreases vegetation height (Vickery et al., 2001; Leal et al., 2019), and facilitates the occurrence of coprophagous species (De Rancourt et al., 2006; Jay-Robert et al., 2008; Perrin et al., 2019). Moreover, the foraging efficiency of steppe birds increases in more open habitats (Fuller, 1996; Haworth & Thompson, 1990; Buckingham & Peach, 2005; Zbyryt, Sparks & Tryjanowski, 2020) and greater visibility in sparser vegetation minimizes the risk of predation for ground-standing birds (Buckingham & Peach, 2005; Whittingham & Evans, 2004). All of these factors may favor the abundance and space use of insectivorous birds (Newton, 2004; Douglas et al., 2017; Gómez-Catasús et al., 2019; Smith et al., 2020). As a result, numerous threatened bird species have their strongholds in these extensively sheep-grazed natural steppes (Velado-Alonso et al., 2020). Of particular conservation concern are the Iberian natural steppes (shrub steppes, sensu (Traba, Sastre & Morales, 2013)), which, as with many Mediterranean calcareous grasslands, are the consequence of both anthropogenic and natural processes, with an important role played by extensive grazing by sheep in the spring and autumn (Suárez, 1994; Sainz Ollero, 2013). In Spain, sheep are traditionally reared in extensive or semi-extensive systems due to the hardiness of the autochthonous breeds and their good adaptation to adverse environmental conditions (Castillo et al., 2008).

Iberian natural steppes are among the European landscapes with the highest value for biodiversity conservation, since they harbor the main (or the entire) European population of several threatened steppe bird species, such as the Dupont’s lark (Chersophilus duponti), the Greater short-toed lark (Calandrella brachydactyla), the Stone curlew (Burhinus oedicnemus), the Little bustard (Tetrax tetrax), both the Black-bellied (Pterocles orientalis) and Pin-tailed sandgrouses (Pterocles alchata), and the Tawny pipit (Anthus campestris), among many others (Santos & Suárez, 2005). Steppe and farmland birds are the most threatened group of birds in Europe (European Environment Agency, 2015) and overall 83% of the steppe bird species show an unfavorable conservation status in Europe (Burfield, 2005). Agricultural intensification, together with habitat loss and land-use changes have partly caused the large declines detected over the past several decades for open-habitat bird populations (Carboni et al., 2015; Santos & Suárez, 2005; Fuller & Gough, 1999; Traba & Morales, 2019). In marginal regions such as those of Iberian natural steppes, where agricultural income has been traditionally low, agricultural intensification is also occurring at a field scale (Reverter et al., 2021). However, the negative trends for several steppe birds that only inhabit primary stages of vegetation succession are especially linked to shrub encroachment (Robinson & Sutherland, 2002; Herrando et al., 2014; Holmes, Maestas & Naugle, 2017). The spread of shrubs and dominant graminoids is one of the major consequences of grazing abandonment, altering local floristic and edaphic conditions (Carboni et al., 2015; Koch et al., 2015) and ultimately affecting to the entire animal community (Robinson & Sutherland, 2002).

During the second half of the 20th century, land abandonment due to rural depopulation generated a reduction in extensive sheep farming in Spain, as well an increase in stocking rates (Soto et al., 2016; Martínez-Valderrama et al., 2021). However, changes in CAP subsidies during the 21st century have also led to important structural changes in the sector (De Rancourt et al., 2006). An example is the decoupling of CAP payments in 2003, which provoked a decrease in sheep numbers in less-favoured areas, while the persistence of CAP subsidies coupled to cattle and beef-cattle production has provoked a shift from sheep-based to cattle-based systems in permanent pastures (Ramos et al., 2021; Faria & Morales, 2020; Mújica et al., 2015), usually with an increase in stocking rate. All of these changes have had a great impact on land use (Soto et al., 2016; Riedel, Casasús & Bernués, 2007) and have led to an increase in shrub and tree cover in these areas (Martínez-Valderrama et al., 2021). While a number of studies have assessed the relationship between grazing pressure and bird abundance in farmlands and uplands in the United Kingdom (Newton, 2004; Douglas et al., 2017; Fuller & Gough, 1999), our current knowledge about the association between grazing and farmland and steppe birds in Mediterranean landscapes is still limited (see Leal et al., 2019; Riedel, Casasús & Bernués, 2007; Reino et al., 2010).

In this study, we aimed to assess the variation in steppe bird abundance in relation to changes in sheep abundance in Spain over the period from 1998–2018. We estimated the nation-wide relationship between trends in sheep abundance with an annual index in population trends estimated for 35 common farmland bird species (Farmland Bird Index, Table S1) and for 20 common bird species typical of Iberian natural shrub-steppes (Steppe Bird Index, Table S2) to evaluate the potential impact of changes in sheep numbers on abundance of open-habitat bird species. Additionally, we also tested the relationship between trends in sheep numbers and population trends of the Dupont’s lark (Chersophilus duponti). We selected this species because it is a threatened habitat-specialist whose European population is restricted to Iberian natural shrub-steppes (Gómez-Catasús et al., 2018), and for which accurate data have been collected during the last 15 years (Gómez-Catasús et al., 2018). Moreover, the promotion of extensive grazing has been traditionally described as one of the main conservation interventions to maintain optimal vegetation structure for the Dupont’s lark (reviewed by Pérez-Granados & López-Iborra (2021)). Based on the assumed positive impact that low-to-moderate grazing pressure has on steppe bird abundance (Vickery et al., 2001), we expected to find a close association between the decline in sheep numbers and the decline in the population indices estimated for the community of farmland and steppe birds, as well as for the Dupont’s lark. Our results might be useful in discussing the relationship between sheep numbers and farmland and steppe birds and to formulate recommendations for agri-environment schemes for these threatened groups of species.

Material and Methods

Results

Sheep numbers significantly declined in Spain during the period 1992–2020 (Fig. 1). In 2020, there were 37.3% fewer sheep than in 1992 (−9,175,782 sheep; linear regression, F-statistic = 128.2.10, df = 27, adjusted R² = 0.82; p < 0.001, see Table S3 for full statistics, Fig. 1). The Johansen test showed significant cointegration between bird indices and sheep trends, which indicates that our results are unlikely to be due to spurious relationships: Spanish farmland bird trend (FBI) vs. Sheep trends Johansen test = 26.82; p < 0.01; Spanish steppe bird trend (SBI) vs. Sheep trend: Johansen test = 27.31; p < 0.01; Dupont’s lark trend (FBI) vs. Sheep trend: Johansen test = 25.02; p < 0.01.

We found a strong, positive and significant relationship between the trend of Spanish farmland birds (FBI) during the period 1998–2018 and the sheep trend (linear regression, F-statistic = 39.85, df = 19, adjusted R² = 0.66, p < 0.001, Fig. 2A, Table S3). Similarly, a positive and significant association was found between the trend of natural steppe birds (SBI) and the sheep trend for the same period (linear regression, F-statistic = 27.4, df = 19, adjusted R² = 0.57, p < 0.001, Fig. 2B, Table S3). The linear relationship between Dupont’s lark trend and the sheep trend over the period 2004–2015 showed a positive relationship although it was not statistically significant (linear regression, F-statistic = 4.44, df = 9, adjusted R² = 0.26, p = 0.06, Fig. 3, Table S3).

Discussion

Our results show a strong decline in sheep numbers in Spain during the last three decades, which is in agreement with the decreasing number of sheep livestock in many European countries: 15% for the period 2002–2018 (Eurostat, 2020; Pollock et al., 2013; Varga & Molnár, 2014; Vargaa et al., 2016; De Arriba & Barac, 2018). Nonetheless, the sheep decline detected in Spain has been especially steep since 2007, firstly, and even more so since 2009, when the number of sheep drastically declined (Fig. 1). This decrease in sheep numbers may be related to changes in CAP subsidies and largely explained by the uncoupling of sheep subsidies that started in 2006 and become permanent in 2010 (Mújica et al., 2015). After controlling for spurious correlations, we found a very strong and positive relationship between the reduction in sheep numbers and the decline in farmland and shrub-steppe birds at the national scale. The relationship between sheep numbers and the population trend of the Dupont’s Lark, a strong habitat specialist of Mediterranean natural steppes (Suárez, 2010), was just close to significant (p = 0.06). This result was obtained using an independent dataset (Gómez-Catasús et al., 2018) and at a shorter temporal scale (11 vs. 20 years) than FBI and SBI analyses. The lack of a significant relationship for the Dupont’s Lark case might be partly related to the more restricted distribution range of the species, which may make it difficult to detect nation-wide changes. Likewise, the decline in the Dupont’s Lark has been associated with other land-use changes due to human activity, such as habitat loss due to ploughing (Tella et al., 2005) and the development of wind farms (Gómez-Catasús, Garza & Traba, 2018), which may have muddled our results.

We are aware that the decline in farmland and shrub-steppe birds in Spain is not exclusively explained by the decline in sheep numbers, but our results and previous studies strongly suggest that the significant relationships found are not simple correlations. It is well known that the negative trends in farmland and steppe birds in Europe are mainly related to agricultural intensification and land use changes, such as the decline in fallow lands (Traba & Morales, 2019; McMahon et al., 2010), which traditionally were an important grazing source (Ramos, Robles & González-Rebollar, 2010), as well as the increase in the use of pesticides and herbicides (Boatman et al., 2004; Chiron et al., 2014), higher mechanization (Santangeli, Di Minin & Arroyo, 2014), or the increase in trellis vineyards and irrigated woody crops, which are largely unsuitable habitats for the considered groups of birds (De Frutos, Olea & Mateo-Tomás, 2015; Casas et al., 2020), to cite a few. Velado-Alonso et al. (2020) recently found strong geographical associations between steppe bird richness and local sheep breed richness, which may be interpreted as an indicator of the intensity of extensive sheep grazing. Though these relationships are probably mediated by other environmental gradients, sheep grazing could have effects on increasing habitat heterogeneity, which could help to promote steppe bird richness and abundance (Velado-Alonso et al., 2020).

The associations found between the decline in both sheep numbers and farmland and shrub-steppe birds in Spain are in agreement with the well-recognized positive impact that extensive grazing has on the distribution and abundance of farmland and steppe birds (Douglas et al., 2017; Fuller, 1996; Haworth & Thompson, 1990; Traba, Sastre & Morales, 2013; Santangeli et al., 2019) (see Fuller, 1996; Evans et al., 2006) for a negative effect of both heavy or very low levels of grazing in steppe birds). For example, steppe birds are adapted to open habitats, which are partly maintained by light or moderate grazing (Fuller, 1996). Grazing plays an important role by decreasing vegetation height and increasing spatial heterogeneity (Bugalho et al., 2011; Leal et al., 2019; Evans et al., 2006), which may increase the foraging efficiency of steppe birds by facilitating foraging in more open habitats (Fuller, 1996; Leal et al., 2019; Zbyryt, Sparks & Tryjanowski, 2020; Murray et al., 2016) and minimizing their predation risk while foraging on the ground (Buckingham & Peach, 2005; Whittingham & Evans, 2004). Sheep grazing has been described as a main driver of these habitats, as it may favor open, creeping plant phenotypes, which disperse their seeds through the livestock dung (Malo & Suárez, 1995; González-Rebollar & Ruiz-Mirazo, 2013). The amount of plants consumed by sheep in Mediterranean shrub steppes under extensive grazing has been estimated at around 1,500 kg/ha/year (dry weight), while dung production is around 600 kg/ha/year (Le Hourèou, 1991). Moreover, sheep dung is twice as attractive to Mediterranean dung beetles as cattle dung, three times more than red deer pellets, and four times more than horse dung (Dormont et al., 2007). Thus, extensive sheep grazing will reduce plant structure and density (Adler, Raff & Lauenroth, 2001) and facilitate the occurrence of dung-processing arthropods (Prather & Kaspari, 2019), an important food source for some farmland and steppe birds (Vickery et al., 2001; Dennis et al., 2008; Jay-Robert et al., 2008). Finally, these areas might be preferred by birds feeding on insects and especially on dung beetles and other coprophagous arthropods (Leal et al., 2019; Jay-Robert et al., 2008; Gómez-Catasús et al., 2019; Smith et al., 2020).

Goat abundance was around six times lower than sheep abundance in Spain in 2018, and especially linked to specific regions. Thus, in this work we only considered trends in sheep numbers. Nonetheless, the negative relationship between Iberian steppe birds and sheep numbers was maintained when the trends in goat numbers in Spain were included, which was around −10% during the period 2002–2018 according to official data (MAPA, 2020). Besides sheep number decline, during the last decades there has also been a great change in livestock husbandry towards higher intensification (Riedel, Casasús & Bernués, 2007; Bernhard, 2008) that may alter the role that sheep play in natural steppes and other plant communities. For example, in recent times sheep are more often kept indoors than free-ranging (Martínez-Valderrama et al., 2021) and the proportion of pregnant and lactating ewes, which are usually kept indoors, has increased (Martínez-Valderrama et al., 2021; Riedel, Casasús & Bernués, 2007; Naylor et al., 2005). These changes in sheep husbandry imply a substantial reduction in the workload and may maximize farmers’ income, but reduce the intensity and duration of outdoor grazing (Soto et al., 2016; Mújica et al., 2015).

Under these circumstances, extensive sheep grazing in Spain has practically disappeared (Martínez-Valderrama et al., 2021), and the role of sheep as an ecosystem engineer species has disappeared (Naylor et al., 2005) or has even become negative due to pollution or overgrazing and soil degradation around intensive farms (O’Brien et al., 2016; Pulido et al., 2018). In Spain, shrub- and tree-encroachment has steeply increased in areas considered as transitional from former extensive grazing to current land abandonment (Martínez-Valderrama et al., 2021), and the consequences of this functional change are yet to be fully determined.

Our results suggest that the alarming decline in Iberian farmland and shrub-steppe birds might be, at least partly, associated with the sharp decline in sheep livestock occurring in Iberia. Further research is needed to understand the role of sheep grazing in steppe and farmland bird declines. In the meantime, there is a need to reverse the negative effect that this trend in sheep numbers may have on habitat heterogeneity and quality (i.e. food resources) for steppe birds. Our findings suggest that extensive grazing should be considered as a key factor in future Common Agricultural Policy reforms and conservation programs to stabilize, and even better increase, the traditional sheep farming system. Such changes in CAP policies to promote sheep farming may partially tackle other concerns in the EU, such as the preservation of biodiversity, reduction of risks due to wildfire, valorization of environmentally friendly agricultural practices and prevention of desertification (Mújica et al., 2015). Besides, changes from sheep to cattle, which could be seen as an opportunity for farmers due to lower production and maintenance costs, has to be deeply evaluated, as may provoke relevant changes in ecosystem structure and functionality (Ramos et al., 2021; Faria & Morales, 2020; Mújica et al., 2015). As the same grazing pressure may be favorable for some species of conservation concern but detrimental to others (Leal et al., 2019; Reino et al., 2010), we encourage researchers to estimate the adequate grazing intensity for protecting most farmland and steppe birds, as well as to perform species-specific studies for proposing a concrete grazing intensity to protect the most threatened species. These studies would provide scientific evidence to managers and therefore increase the implementation of extensive grazing as a conservation intervention (Gibbons, Wilson & Green, 2011). Extensive sheep grazing should be promoted as a multirole and low impact practice, which may contribute to increasing habitat heterogeneity, reversing shrub encroachment and improving the situation for birds while avoiding the need to apply other resource-consuming, and potentially hazardous practices such as mowing, manual shrub-clearing and/or controlled burning (Carboni et al., 2015). In a climate change scenario, natural steppe habitats may need habitat management actions aimed at improving habitat quality for open-habitat bird species (Leal et al., 2019; Gibbons, Wilson & Green, 2011; Menz, Brotons & Arlettaz, 2009; Pérez-Granados, Serrano-Davies & Noguerales, 2018; Hellicar & Kirschel, 2020).

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