Introduction
For resident bird populations at higher latitudes, winter conditions represent an important mortality factor (Graber and Graber Reference Graber and Graber1979, Cawthorne and Marchant Reference Cawthorne and Marchant1980). The availability of food can particularly influence the likelihood of birds dealing successfully with the often harsh environmental conditions during the winter months. The importance of an adequate food supply in winter has been demonstrated both empirically (Houston and Francis Reference Houston and Francis1995) and experimentally through artificial food supplementation (Lahti et al. Reference Lahti, Orell, Rytkönen and Koivula1998).
In human-dominated landscapes crops such as winter oilseed rape can contribute a significant proportion of food used by birds during the winter months. For example, in Britain the introduction of oilseed rape Brassica napus provided an abundant winter food for the Common Woodpigeon Columba palumbus which as a consequence recovered from a population decline in the late 1960s (Inglis et al. Reference Inglis, Isaacson, Smith, Haynes and Thearle1997). Oilseed rape fields are also an important foraging habitat in winter for Dark-bellied Brent Geese Branta bernicla bernicla (McKay et al. Reference McKay, Langton, Milsom and Feare1996) and attract many other birds (Eyre et al. Reference Eyre, Hughes and Leifert2012).
Winter food supply for farmland birds such as game birds and insectivorous or granivorous passerines can be enhanced by cultivating seed-rich ‘winter bird crops’ (Henderson et al. Reference Henderson, Vickery and Carter2004) and fodder brassica crops, by maintaining stubbles (Hancock and Wilson Reference Hancock and Wilson2003) or by setting aside areas of arable farmland (Buckingham et al. Reference Buckingham, Evans, Morris, Orsman and Yaxley1999). These management actions are of particular importance since 58% of farmland and grassland bird species declined during 1990–2000 (BirdLife International 2004).
Great Bustards are mainly herbivorous, especially in the mid-winter period (December to March). During that time of year, faeces of Great Bustards in north-west Spain consisted almost entirely of green plant material and contained only a very small quantity of invertebrates and seeds (Lane et al. Reference Lane, Alonso, Alonso and Naveso1999). The importance of oilseed rape as food for Great Bustards has already been emphasised (Sterbetz Reference Sterbetz1980, Litzbarski et al. Reference Litzbarski, Litzbarski and Petrick1987, Kalmár and Faragó Reference Kalmár and Faragó2008) and its cultivation within traditional wintering areas has even been recommended as a conservation measure to decrease winter mortality (Nagy Reference Nagy2009). To optimise the value of rape fields as conservation tool for improving food availability for Great Bustards during winter, we studied how field parameters such as rape field size, isolation of fields from other rape cultivations and human disturbance affect their suitability as feeding habitat for West Pannonian Great Bustards. We expected that larger rape fields are preferred by Great Bustards. They do not just provide a larger amount of high-quality food but also may allow Great Bustards to escape human disturbance by movements within the rape field without the necessity of changing to another disturbance-free area by energy consuming flights. Consequently, minimising the need for movements between different rape fields by using large fields may decrease the importance of the distance between rape fields as predictor for rape field use. Human disturbance can also play an important role in habitat choice of Great Bustards (López-Jamar et al. Reference López-Jamar, Casas, Díaz and Morales2011, Alonso et al. Reference Alonso, Álvarez-Martínez and Palacín2012, Burnside et al. Reference Burnside, Végvari, James, Konyhás, Kovács and Székely2014). Reducing escape flights induced by human disturbance may be particularly important during winter when energy loss has to be minimised. Therefore, we expect that a decreasing distance of rape fields to paved roads, used as proxy for human disturbance, will negatively affect the occurrence of Great Bustards.
Methods
Study areas
The study was conducted in a total of three areas which have been regularly used as winter habitat by the West Pannonian population of Great Bustards for at least 15 years. One was situated in the Westliches Weinviertel Special Protection Area (SPA) (WW; 1,560 ha) in Eastern Austria, the second one in the three SPAs - Parndorfer Platte – Heideboden, Sysl’ovské polia and Mosoni-sík (PH; 3,880 ha) on the Austrian–Slovakian–Hungarian border and the third one in the southern part of the Mosoni-sík SPA (MS; 3,004 ha) on the Moson Plain in Hungary (Figure 1).
Figure 1. Map indicating the three study areas where Great Bustard surveys were conducted: MS – Mosoni-sík (Western Hungary); WW – Westliches Weinviertel (Eastern Austria); PH – Parndorfer Platte–Heideboden (Eastern Austria), Sysl’ovské polia (Western Slovakia) and Mosoni-sík (Western Hungary).
The study areas are located in a mainly flat or gently undulating open landscape and are largely free of vertical structures such as trees or hedges, a landscape structure preferred by Great Bustards (Collar Reference Collar, del Hoyo, Elliott and Sargatal1996, Osborne et al. Reference Osborne, Alonso and Bryant2001). All three study areas lack any natural grassland and mainly consist of arable land and are cultivated for the most part with winter and spring cereals, maize and various root crops. There is intensive cultivation, although agri-environmental schemes are initiated to support the requirements of Great Bustards. Associated non-obligatory measures available to farmers due to the EAFRD (European Agriculture Fund for Rural Development) ensured that cultures of winter oilseed rape, lucerne and set-aside land cover a relatively large area of the study region. Winter rape covered on average (± SD) 351.86 (± 209.02) ha per winter at MS, 185.11 (± 39.57) ha at PH and 137.80 (± 35.51) ha at WW. The data on habitat cover were gathered through ground surveys on the basis of digital cadastre maps (1:1,000).
Great Bustard counts
Field work was conducted in the winters 2005/2006, 2006/2007, 2007/2008 and 2008/2009. During the four winters, all study areas were surveyed for Great Bustards from mid-November until mid-March. MS was visited on a total of 68 days (20, 16, 19 and 13 days in the winters 2005/2006, 2006/2007, 2007/2008 and 2008/2009, respectively), PH on 55 days (18, 13, 10 and 14 days) and WW on 35 days (13, 7, 8 and 7 days). Survey duration was approximately 3.5, 5.5 and 3 hours per visit at MS, PH and WW, respectively, reflecting size differences of the study areas. During each visit the total study area was surveyed for birds. Locations of all encountered single individuals and flocks were immediately marked in the field on topographical (1:12,500) maps and, when observed in a rape field, assigned to an identified rape field. If more than one survey round was conducted per day, only the one with the higher total number of recorded Great Bustards was considered. When birds were observed changing their location during a survey round, only the first observation was considered for further analyses. Also if size and composition (e.g. sex and/or age ratio of individuals) of a flock was similar to a flock observed earlier that day and the latter flock could not be rediscovered again at its former location, the second observation was rated as a double count and was not considered in further analyses.
Winter rape fields and paved roads
The two winter rape field parameters, size and isolation from other rape fields, were measured by ArcMap 9.1 (ESRI) for all four winters. Field isolation was quantified as the median distance to the four nearest rape fields. Distances between fields were measured as the minimum distances between field margins. As a substitute for human disturbance, we measured the minimum distance between the field margin and the nearest paved road with ArcMap 9.1.
Data analysis
To assess effects of field size (log x transformed), field isolation (√x transformed) and distance from the field margin to the nearest paved road (√x transformed) on the occurrence (incidence data: presence/absence) of Great Bustards in rape fields, Generalized Linear Mixed Models (GLMMs) with binomial error distribution and logit-link function were calculated. Winter was fitted as random factor. Due to differences in Great Bustard numbers in the three study areas, GLMMs were calculated separately for all three areas. GLMMs with winter fitted as random factor were also used to detect effects of field size, field isolation, and distance to nearest roads on the maximum number of Great Bustards counted in rape fields during individual winters. These GLMMs were calculated with a Poisson error structure and a log-link function, which is recommended for count data (e.g. Bolker et al. Reference Bolker, Brooks, Clark, Geange, Poulsen, Stevens and White2009). All GLMMs were calculated using standardised variables. All statistical analyses were conducted using STATISTICA version 7.1 (StatSoft Inc. 2005).
Results
GLMMs (with winter as random effect) including the variables field size, field isolation and distance to nearest paved road indicate a significant effect of field size on Great Bustard occurrence for all three study areas (Table 1). The probability of Great Bustard occurrence predicted by the GLMMs increased with rape field size in all three study areas (Figure 2). The rape field variables ‘isolation’ and ‘distance to the next paved road’ only affected the occurrence of Great Bustards in rape fields at the WW study area. However, both variables only weakly influenced the occurrence of Great Bustards as indicated by the small coefficients (Table 1).
Table 1. Results of GLMMs (with the variable winter as random effect) testing for effects of field size, field isolation and distance from field margin to the next paved road on the occurrence of Great Bustards in winter rape fields for each of the three study areas. Significant effects are indicated in bold.
Figure 2. The relationship between probability of Great Bustard occurrence in winter rape fields and field size predicted by GLMMs including the variables field size, field isolation and distance of fields to the next paved road. Visualized are resulting linear regression curves for all three study areas: MS – Mosoni-sík; WW – Westliches Weinviertel; PH – Parndorfer Platte–Heideboden, Sysl’ovské polia and Mosoni-sík.
Subsequently calculated univariate logistic regressions testing for effects of winter rape field size on the occurrence of Great Bustards also indicate a strongly increasing likelihood of occurrence with increasing field size for the study areas MS (χ 2 = 13.20, P < 0.001) and PH (χ 2 = 10.48, P = 0.001; Figure 3). For WW only a weak positive effect of field size on the occurrence of Great Bustards was found (χ 2 = 3.94, P = 0.047), perhaps because average size of rape fields was smaller at WW than at MS and PH in all winters (Figure S1 in the online supplementary material). Both the logistic regression curves for MS and PH indicate a 50% likelihood of Great Bustard occurrence in winter rape fields for a field size of c.15 ha (Figure 3).
Figure 3. Likelihood of Great Bustard occurrence in winter rape fields in relation to field size, described by logistic regressions calculated separately for the two study areas MS (solid line) and PH (dotted line). The arrow indicates the field size at which the likelihood of Great Bustard occurrence is 50%.
GLMMs testing for effects of all three rape field variables on the maximum number of Great Bustards counted per winter in individual rape fields again indicate a significant effect of field size in the three study areas. Although field isolation at MS and WW and distance to the nearest paved road at all three study areas also proved to significantly influence Great Bustard numbers in rape fields, their comparably small coefficients provide evidence that they were only of minor importance for predicting numbers (Table 2). An increase in isolation of rape fields and distance to paved roads both appeared to positively affect the number of Great Bustards at MS and WW. In contradiction, the distance to the nearest paved road was negatively related to Great Bustard numbers at PH.
Table 2. Results of GLMMs (with the variable winter as random effect) testing for effects of field size, field isolation and distance from field margin to the next paved road on the maximum number of Great Bustards in winter rape fields recorded per year, separately calculated for the three study areas. Significant effects are indicated in bold.
Discussion
Farming activities can be the major determinant of food abundance and availability for wintering birds (Tucker Reference Tucker1992, Gill et al. Reference Gill, Watkinson and Sutherland1996). As a consequence, farming can affect habitat use of birds and even contribute to an increase in bird populations (Inglis et al. Reference Inglis, Isaacson, Smith, Haynes and Thearle1997, Guzmán et al. Reference Guzmán, García, Amado and del Viejo1999, Gauthier et al. Reference Gauthier, Giroux, Reed, Béchet and Bélanger2005, López-Jamar et al. Reference López-Jamar, Casas, Díaz and Morales2011, Martín et al. Reference Martín, Martínez, Bautista and Martín2012). Especially for Great Bustards, areas dominated by agriculture provide very important feeding habitats. Perhaps the nutritional value of the rape leaves and the fact that rape is less often covered by snow than other food sources like winter cereal sowings (Inglis et al. Reference Inglis, Isaacson, Smith, Haynes and Thearle1997) makes rape a profitable food resource for Great Bustards during the winter months.
In our study region, the size of winter rape fields appeared to have a significant effect on their importance as feeding habitat for Great Bustards. Both Great Bustard numbers and the likelihood of occurrence increased with increasing field size. In Pink-footed Geese Anser brachyrhynchus field size was also shown to be an important predictor variable for field use and even seemed to have a greater effect than the biomass available on particular fields (Gill et al. Reference Gill, Watkinson and Sutherland1996). Furthermore, fields under 6 ha in size and close to roads were often completely avoided by the geese (Gill et al. Reference Gill, Watkinson and Sutherland1996). The size of rape fields which attracted Great Bustards with a likelihood of 50% was remarkably similar at MS and PH. At both study sites the value was approximately 15 ha. This may explain the weak explanatory power of field size for Great Bustard occurrence in individual rape fields at WW, where all rape fields were below a size of 9 ha.
Although it was stated earlier that fully grown Great Bustards have hardly any natural predators (Glutz von Blotzheim et al. Reference Glutz von Blotzheim, Bauer and Bezzel1994), a more recent study on mortality causes of juvenile and immature birds in Spain classified red foxes Vulpes vulpes and feral dogs as potentially frequent predators (Martín et al. Reference Martín, Alonso, Alonso, Palacín, Magaña and Martín2007). However, so far feral dogs have not been recorded as predators of juvenile or adult Great Bustards in our study region. Eagles represent not only an important source of disturbance (Eisenberg et al. Reference Eisenberg, Ryslavy, Putze and Langgemach2002, Sastre et al. Reference Sastre, Ponce, Palacín, Martín and Alonso2009, pers. obs.) they can even kill Great Bustards. For example, in Germany 50 birds (but predominantly chicks and juveniles) were killed by White-tailed Eagles Haliaaetus albicilla since 2000 (T. Langgemach pers. comm.). Great Bustards are particularly sensitive to human disturbance (Sastre et al. Reference Sastre, Ponce, Palacín, Martín and Alonso2009, pers. obs.) and respond to humans with an escape flight already at distances of several hundred metres (pers. obs.). Therefore, they may prefer larger fields because these should provide more potential refuge areas (i.e. parts of the field opposite to a source of disturbance) which can be reached by walking, thereby preventing large-scale flight movements to reach other (perhaps less profitable) feeding habitats. A higher frequency of flight movements can have a severe negative impact on the birds’ energy budget, especially in mid- or late winter when hours of daylight are limited, food resources have already been noticeably depleted and regrowth of plants is very low (Riddington et al. Reference Riddington, Hassall, Lane, Turner and Walters1996). Great Bustards weigh up to 18 kg (Collar Reference Collar, del Hoyo, Elliott and Sargatal1996) and feed during the winter months mainly on nutrient-poor green plant material (Lane et al. Reference Lane, Alonso, Alonso and Naveso1999, Rocha et al. Reference Rocha, Marques and Moreira2005), which is difficult to digest (Begon et al. Reference Begon, Harper and Townsend1990). In such birds flight movements can represent particularly high energy expenditure. In addition, wintering Great Bustards mostly forage in flocks and smaller fields may not be attractive enough for a large number of birds. Indeed our data also indicate that the size of Great Bustard flocks feeding in winter rape fields increases with field size.
Sources of disturbance associated with roads or paths like cars, walkers, motorcyclists or cyclists are identified as “high-risk threatening factors” by Great Bustards and usually cause a flight response (Sastre et al. Reference Sastre, Ponce, Palacín, Martín and Alonso2009). This may explain the weak positive effect of the minimal distance between field margins and paved roads on Great Bustard occurrence (at WW) and recorded maximum numbers (at MS and WW). Surprisingly, a very weak negative effect of the distance between field margin and the nearest paved road and the maximum number of counted Great Bustards was indicated by the GLMM calculated for PH. Weak positive effects of field isolation on occurrence and maximum counts of Great Bustards were found at WW and MS and WW, respectively. Perhaps, more isolated fields attract Great Bustards passing accidentally, independent of field size.
Providing a sufficient supply of winter oilseed rape during winter months should be a priority in habitat management of the West Pannonian Great Bustard population. Unfortunately, in the Austrian part of our study region winter rape fields are less profitable than cultivation of other annual crops. Therefore, the cultivation of winter rape in the near future can just be maintained by providing financial support to the farmers for special winter rape fields in the Great Bustard areas. Supporting winter grazing areas for Great Bustards by means of the Austrian Rural Development Program has already been realised within a LIFE-Nature project (LIFE05 NAT/A/000077; http://www.grosstrappe.at) addressing the conservation of the West Pannonian Great Bustard population, and two further projects financed by the local government of Lower Austria and the European Commission (RD project RU5-S-428/001-2005; http://www.grosstrappe.at) and the local government of Burgenland (LPF project 5-N-A1025/148-2009; http://www.grosstrappe.at). Furthermore, access to these winter grazing areas should be ensured during the whole winter. Removal of snow, which may become deep and crusty, is an important action to undertake (Nagy Reference Nagy2009), since a snow cover of only 5 cm covers all potential food plants of Great Bustards, which they then have to pull out of the snow using only their bills (Streich et al. Reference Streich, Litzbarski, Ludwig and Ludwig2006).
Our data indicate a clear preference for larger winter rape fields (> 15 ha) by Great Bustards. This observation has important implications for habitat management. The establishment of larger rape fields in traditional winter grazing areas can potentially attract Great Bustards to a predictable number of focal areas. Here, potential sources of disturbance can be more effectively controlled or reduced during the sensitive winter months, when food is generally limited. Also, rape fields should be established as far as possible from paved roads with high disturbance levels causing frequent escape flights, which increase energy expenditure and could additionally increase the risk of collision with man-made structures such as power lines (e.g. Alonso et al. Reference Alonso, Martín, Palacín, Martín and Magaña2005, Pinto et al. Reference Pinto, Rocha and Moreira2005). Such collisions can represent the main non-natural cause of mortality for adult Great Bustards (Martín et al. Reference Martín, Alonso, Alonso, Palacín, Magaña and Martín2007, Raab et al. Reference Raab, Schütz, Spakovszky, Julius and Schulze2012), although they are able to adapt their flight behaviour (Raab et al. Reference Raab, Spakovszky, Julius, Schütz and Schulze2011). This risk should be reduced by establishing rape fields far from existing power lines to reduce the risk of collision (Nagy Reference Nagy2009). Our recommendations for improving the habitat management in the species’ West Pannonian distribution range are relevant for the region’s entire breeding population, which winters exclusively in these three areas (as indicated by the monthly winter counts; Raab et al. unpubl. data).
Winter food of West Pannonian Great Bustards certainly comprises a large fraction of oilseed rape. However, the composition of the diet of Great Bustards (Lane et al. Reference Lane, Alonso, Alonso and Naveso1999, Rocha et al. Reference Rocha, Marques and Moreira2005) and their selection of foraging habitats underlies seasonal changes (Moreira et al. Reference Moreira, Morgado and Arthur2004) and varies geographically (Morales et al. Reference Morales, Suárez and García de la Morena2006). At the same time wintering and breeding areas can spatially overlap to a large extent, as in the West Pannonian Great Bustard population. Therefore, supporting special winter grazing areas for Great Bustards during winter months should not be at the cost of other habitats that are important at other times of the year, like set-aside land during the breeding season (Rocha et al. Reference Rocha, Morales and Moreira2013). So maintaining a mosaic of different habitat types is essential for satisfying the requirements of Great Bustards in agricultural landscapes throughout the whole year. Furthermore, the behavioural context has to be considered. Different land uses provide more choices for birds not only for feeding but also displaying, resting, preening etc. Therefore, we not only recommend maintaining large winter rape field cover but also other habitats such as fallows, a management measure also important for other farmland birds (Tucker Reference Tucker1992).
Supplementary Material
The supplementary materials for this article can be found at journals.cambridge.org/bci
Acknowledgements
We would like to give our special thanks to more than 450 farmers for providing part of their fields to support suitable winter grazing areas for Great Bustards by means of the Austrian Rural Development Program within the LIFE project LIFE05 NAT/A/000077, the RD project RU5-S-428/001-2005 and the LPF project 5-N-A1025/148-2009. For the most part field work took place within the two LIFE Projects “Crossborder Protection of the Great Bustard in Austria” (LIFE05 NAT/A/000077, www.grosstrappe.at) and “Conservation of Otis tarda in Hungary” (LIFE04 NAT/HU/000109, www.tuzok.hu). Most of the analyses were completed within the LIFE+ Project “Crossborder Protection of the Great Bustard in Austria – continuation” (LIFE09 NAT/AT/000225, www.grosstrappe.at). All three LIFE Projects are supported by the EU, many project partners and co- funders. Without this support the time-consuming work for the conservation of the entire West Pannonian Great Bustard population during recent years would not have been possible. Finally, we are grateful to Luc Lens, Dan Chamberlain, Kate Ashbrook, Al Dawes, Allan Goddard, Andrew Taylor, Tracé Williams and two anonymous reviewers for providing helpful comments, which significantly improved the manuscript.
