Introduction
In a traditional, simplified view, migratory birds alternate short-distance non-directional movements, occurring in breeding and wintering areas, with long-distance directional movements, namely spring and autumn migrations (Newton Reference Newton2008). Recent advances in tracking technologies are revealing that this scenario is rather more complex (Klaassen et al. Reference Klaassen, Ens, Shamoun-Baranes, Exo and Bairlein2011), with species also performing pre-migratory movements, spending some weeks in staging areas away from breeding sites (Limiñana et al. Reference Limiñana, Soutullo, López-López and Urios2008, Strandberg et al. Reference Strandberg, Klaassen, Hake, Olofsson, Thorup and Alerstam2008, Catry et al. Reference Catry, Dias, Catry, Afanasyev, Fox, Franco and Sutherland2011), using stop-over areas for relatively long periods (Chevallier et al. Reference Chevallier, Le Maho, Brossault, Baillon and Massemin2010, Kochert et al. Reference Kochert, Fuller, Schueck, Bond, Bechard, Woodbridge, Holroyd, Martell and Banasch2011, Limiñana et al. Reference Limiñana, Romero, Mellone and Urios2012), or using staging areas different to breeding or wintering ranges before reaching sexual maturity (Mellone et al. Reference Mellone, Yáñez, Limiñana, Muñoz, Pavón, González, Urios and Ferrer2011a). To date, pre-breeding movements have been described only for some seabirds (Phillips et al. Reference Phillips, Catry, Silk, Bearhop, McGill, Afanasyev and Strange2007, Guilford et al. Reference Guilford, Meade, Willis, Phillips, Boyle, Roberts, Collett, Freeman and Perrins2009, Bogdanova et al. Reference Bogdanova, Daunt, Newell, Phillips, Harris and Wanless2011).
In this scenario, migratory species require conservation measures that are difficult to implement, since efforts carried out in one area can be jeopardised by threats occurring far away (Martin et al. Reference Martin, Chades, Arcese, Marra, Possingham and Ryan Norris2007, Angelov et al. Reference Angelov, Hashim and Oppel2012). Therefore, the identification of the different areas used throughout the year is of utmost importance from a conservation point of view.
Eleonora’s Falcon Falco eleonorae is a long-distance migratory raptor, which breeds colonially almost exclusively in islands of the Mediterranean Sea (Walter Reference Walter1979). The species is included in Annex I of the Directive 2009/147/EC on the conservation of wild birds and constitutes a priority species for conservation (BirdLife International 2004, 2010). The winter range of the species is concentrated in Madagascar (Walter Reference Walter1979, Mellone et al. Reference Mellone, López-López, Limiñana and Urios2012a) and migration routes have been recently mapped in detail (Gschweng et al. Reference Gschweng, Kalko, Querner, Fiedler and Berthold2008, López-López et al. Reference López-López, Limiñana and Urios2009, Reference López-López, Limiñana, Mellone and Urios2010, Mellone et al. Reference Mellone, López-López, Limiñana and Urios2011b, Kassara et al. Reference Kassara, Fric, Gschweng and Sfenthourakis2012).
This species presents a unique adaptation, since it delays reproduction to late summer (August-September) in order to take advantage of the passage of migratory passerines en route to Africa, which form its main prey during the breeding season (Walter Reference Walter1979). Nevertheless, timing of spring migration is similar to that of other Palearctic species, since Eleonora’s Falcons normally arrive in Europe in May (Bernis and Castroviejo Reference Bernis and Castroviejo1968, Walter Reference Walter1979). Therefore, for these birds there is a time lapse of two months between the end of the spring migration and the beginning of the breeding season. There are some data indicating that during this period Eleonora’s Falcons stay in inland areas far away from the breeding colonies (González et al. Reference González, González and Garzón1984, Ristow and Wink Reference Ristow and Wink1995, Cano Reference Cano2001, Belenguer et al. Reference Belenguer, Tena and Méndez2004, Gregory Reference Gregory2007), but satellite tracking data concerning this behaviour are practically absent and therefore it has been impossible to unravel the connectivity between those staging areas and the breeding colonies (but see Gregory Reference Gregory2007). Here we analyse the pre-breeding movements of Eleonora’s Falcons belonging to two different colonies in the western Mediterranean using Argos-based satellite telemetry.
Methods
Eighteen Eleonora’s Falcons were trapped in Balearic and Columbretes Islands (Spain) in autumn between 2007 and 2010 (Fig. 1; details in López-López et al. Reference López-López, Limiñana and Urios2009, Reference López-López, Limiñana, Mellone and Urios2010). Birds were sexed by molecular methods and equipped with Microwave Telemetry Inc. 9.5-g solar-powered satellite transmitters using Teflon ribbon. During the summer season, transmitters were programmed to collect data on a duty cycle of 12 h on/58 h off, apart from bird #92532 that partly transmitted with a cycle of 12 h on/18 h off. Here, we only used summer data from those individuals for which we recorded the complete summering event (since arriving in the Mediterranean basin until the onset of the following autumn migration). Overall, we used data from four summering events belonging to three individuals: two adult females captured in 2008 (#80399 from Dragonera, Mallorca and #80402 from Columbretes islands) and one immature (2nd calendar-year) male born in Columbretes Islands in 2010 (#92532). Bird #80402 was tracked for two consecutive summers. For the remaining tagged individuals, the transmitters did not work properly or birds died during migration (López-López et al. Reference López-López, Limiñana, Mellone and Urios2010, Mellone et al. Reference Mellone, Urios, Rguibi-Idrisi, Limiñana, Benhoussa and López-López2012a). Locations were collected using the Argos system. The locations are coded for accuracy and grouped into location classes (l.c. hereafter). In order of decreasing accuracy these classes are 3, 2, 1, 0, A, B and Z. Initially all data apart from those with a l.c. of were included. Data were then filtered to exclude locations obtained in the same hour (retaining the highest quality one) and locations resulting in unrealistic values of speed and direction (e.g. > 80 km/h during the day and > 5 km/h at night).
Locations outside the colonies of three Eleonora’s Falcons during four summering events occurring between 2009 and 2011. Bird #80399: n = 10 locations; bird #80402: n = 49 (2009) / n = 28 (2010); bird #92532: n = 153.
In order to identify the centroid of the areas used during summer outside the breeding colonies and to calculate its distance from colonies, we selected all the locations occurring on the mainland and calculated 50% fixed kernel density contours (Worton Reference Worton1989) for every summering event, using the Animal Movement Extension for ArcView 3.2 (Hooge and Eichenlaub Reference Hooge and Eichenlaub2000) and the least squares cross validation (LSCV) procedure (Silverman Reference Silverman1986).
In order to describe habitat composition, we followed a conservative approach, excluding data with l.c. A and B, and applying to the remaining data (l.c. 3, 2, 1 and 0; n = 86) a buffer whose radius was the nominal accuracy of each location (l.c.3: 250 m; l.c. 2: 500 m; l.c. 1: 1,500 m; Argos 1996). For data with l.c. 0, nominal accuracy is higher than 1,500 m, therefore we conservatively applied an arbitrary buffer of 5,000 m. In our experience, after filtering for direction and speed (see above), those data are reasonably accurate (Soutullo et al. 2007, López-López et al. Reference López-López, Limiñana, Mellone and Urios2010, Mellone et al. Reference Mellone, López-López, Limiñana and Urios2011b, Limiñana et al. Reference Limiñana, Romero, Mellone and Urios2012). Within each buffer, we calculated the area of the different habitat categories, using the GIS layers of Corine Land Cover (http://www.eea.europa.eu/publications/COR0-landcover). Since the buffer area differed according to the l.c. (e.g. a buffer whose centre was a l.c. 3 was smaller than a buffer with l.c. 2), we weighted the obtained surfaces according to the location class, in order to avoid a bias towards more inaccurate data. We compiled those percentages in Table 1.
Percentages of CORINE land cover classes included within the buffer areas of satellite fixes with l.c. 3–0 (see methods) for each summering event of Eleonora’s Falcons. “Others” includes: beaches, bare rocks, agro-forestry, sparsely vegetated and burnt areas, rice fields, inland and coastal water bodies.
Results
All individuals performed pre-breeding inland movements in areas hundreds of kilometres from the respective breeding colonies (Figure 1).
Bird #80399 first visited the breeding colony located in Dragonera (Mallorca, Balearic Islands), between 20 May 2009 and 13 June 2009. It then spent 16 days in southern Spain, in the Sierra de Segura mountain range (Sierras de Cazorla, Segura y Las Villas Natural Park), 444 km from its breeding colony. Afterwards, it came back to the colony, where it stayed until the beginning of the autumn migration.
Bird #80402 showed more complex movements during both summers that it was tracked. Its inland movements ranged from southern France to north-eastern Spain. During 2009 the first location within the Mediterranean basin was a low quality one in the Tyrrhenian Sea, close to central Italy (15 May). Then the falcon visited southern France (18 May), and before finally settling in the breeding colony (17 July) it alternated short visits to the colony (twice, of one and four days each) with inland movements to France (maximum period away from the colony of 31 days: 18 May to 17 June; 395 km away from the colony).
During 2010 it again first visited central Italy (16–18 May) and Corsica (20–24 May), then from 26 May, it stayed mainly in southern France, including a first short visit (15–17 June) to the breeding colony. It finally settled in the colony on 1 July, but between the 23 and 27 July stayed inland in Castellón province (eastern Spain), the closest mainland area to the colony. During this year two core areas were identified (Figure 1), completely overlapping with the core area of the previous year, and located 440 and 331 km respectively from the breeding colony in Columbretes Islands.
The immature bird (#92532) reached Spain on 24 June 2011, after having spent 10 days in northern Algeria, at the end of spring migration. Apart from two “trips” of four days each, one to northern Spain (central Pyrenees) and the other to southern Spain (Sierra Morena), it stayed in eastern Spain until 9 August, when it began to move northwards, stopping for 10 days in the eastern pre-Pyrenees and then for 12 days in a coastal areas of southern France. On 22 September, for the first time, it went back to its natal colony (Columbretes Islands), where it remained for roughly one month before beginning the autumn migration (25 October), including two short daily trips to inland areas (Castellón province). The centroid of its core area was located 173 km from the colony.
Concerning land cover, the main habitats were coniferous and broad-leaved forests, followed by areas covered by sclerophyllous vegetation, transitional woodland-shrub, and cultivated areas such as fruit plantations and vineyards (Table 1).
Discussion
Overall, during the summer pre-breeding season Eleonora’s Falcons visited a highly varying range of environments, spanning mountains (#80399) to lower hilly areas (#80402, #92532), to coastal areas (#92532), as well as the breeding colonies. The main habitats represented within the core areas were forests, shrubland, arable lands and vineyards (Table 1).
After performing these large-range movements, adult individuals settled in the breeding colonies in July, and after that they no longer visited inland areas, beginning the southward migration from the colonies in October. Apart from the last wave of spring migrant passerines that occurs in May, in late spring-early summer, small Mediterranean islands cannot offer enough food to support hundreds of falcons, and therefore birds are forced to look for areas where feeding opportunities are more favourable (Ristow and Wink Reference Ristow and Wink1995). It is remarkable that the peak of insect abundance, particularly beetles (Order Coleoptera) as well as dragonflies and damselflies (Odonata), occurs in the inland areas visited by Eleonora’s Falcons just during the pre-breeding period (Cano Reference Cano2001, Belenguer et al. Reference Belenguer, Tena and Méndez2004), providing an adequate food supply until the beginning of the autumn migration of passerines that form their main resource during breeding (Walter Reference Walter1979). It has been reported that Eleonora’s Falcons prey particularly upon the Common Cockchafer Melolontha melolontha (Cano Reference Cano2001, Belenguer et al. Reference Belenguer, Tena and Méndez2004), an abundant insect that shows demographic explosions in June in some years.
Inland observations of Eleonora’s Falcons occurring in August-September, during chick rearing, involve mainly immature, non-breeding individuals (Ristow and Wink Reference Ristow and Wink1995; authors’ unpubl. data). The pattern shown by our immature bird (#92532) fits well in this scenario, and its behaviour during the stay in the coastal area of southern France (movements over the open sea during early morning) might suggest that it was already chasing migrating passerines.
Field observations confirm the importance of the areas identified in this study, suggesting that our findings may apply to a larger proportion of individuals. For example, within the mountain range of Sierra de Segura (southern Spain) a maximum of 11 Eleonora’s Falcons were observed together in early July 2009, and six were recorded in the same period the previous year (C. Ruiz pers. comm. 2011). In addition, the species is regularly observed in southern France and Corsica (Carp and Cheylan Reference Carp and Cheylan1979, Mayol Reference Mayol, Muntaner and Mayol1996). Finally, bird #80402 briefly visited Tolfa hills (central Italy) in 2010 (and probably also in 2009, but not enough data were obtained). This area is the most important one in inland Italy concerning the number of Eleonora’s Falcons regularly observed, with up to 18 individuals observed hunting insects together (Celletti and Meschini Reference Celletti and Meschini1992). In inland areas of Mallorca (Spain), close to the colony of bird #80399, up to 49 individuals have been observed hunting insects in the Albufera wetland in May (Ristow and Wink Reference Ristow and Wink1995), and the species is usually observed year after year in particular areas of the Serra de Tramuntana (Mayol Reference Mayol1977, Reference Mayol, Muntaner and Mayol1996). Unfortunately no satellite locations have been obtained from our tracked individuals that could confirm movements to this area.
Other areas where Eleonora’s Falcons are regularly observed far away from the colonies occur elsewhere within its breeding range and in a wide range of habitats and altitudes (reviewed by Ristow and Wink Reference Ristow and Wink1995, see also Premuda and Mellone Reference Premuda and Mellone2007, Díaz-Portero et al. 2009). Not surprisingly, the highest numbers have been reported in mainland Greece and Crete (up to 120 individuals hunting insects together, Ristow and Wink Reference Ristow and Wink1995), the region where the breeding density is the highest worldwide (Dimalexis et al. 2007). The use of cultivated areas by Eleonora’s Falcons could be a cause for concern, given the widespread use of pesticides in Spain and France (Geiger et al. Reference Geiger, Bengtsson, Berendse, Weisser, Emmerson, Morales, Ceryngier, Liira, Tscharntke, Winqvist, Eggers, Bommarco, Part, Bretagnolle, Plantegenest, Clement, Dennis, Palmer, Onate, Guerrero, Hawro, Aavik, Thies, Flohre, Hanke, Fischer, Goedhart and Inchausti2010). Ristow (Reference Ristow2001) showed that poison ingested by Eleonora’s Falcons through drinking at polluted pools inland in Crete caused several deaths and a strong decline in a close-by breeding colony. It has been also shown that insect availability prior to egg-laying, even near the colonies, can affect clutch size (Xirouchakis et al. Reference Xirouchakis, Fric, Kassara, Portolou, Dimalexis, Karris, Barboutis, Latsoudis, Bourdakis, Kakalis and Sfenthourakis2012). Therefore, events occurring in the pre-breeding staging areas could have serious consequences at the population level and it is thus of paramount importance to identify and protect at least the areas where the highest concentrations of Eleonora’s Falcons occur. Our results highlight that conservation schemes for migratory species should be focused not only at breeding and wintering grounds, but should also take into account temporary staging areas. Similar processes have been described for non-migratory species, when juveniles disperse and settle in temporary staging areas (see Penteriani et al. Reference Penteriani, Otalora, Sergio and Ferrer2005, Soutullo et al. Reference Soutullo, López-López and Urios2008, Cadahía et al. Reference Cadahía, López-López, Urios and Negro2010, Caro et al. Reference Caro, Ontiveros, Pizarro and Pleguezuelos2011). However, it is very difficult to obtain these data and only recently, transmitters lasting more time than just one or two years, are allowing gain new insights into hitherto unknown processes such as the pre-breeding movements, as shown here.
Acknowledgements
The Terra Natura Foundation and the “Servicio de Biodiversidad” (Generalitat Valenciana) funded this project. Special thanks are due to all the people who helped in bird trapping. We thank Phil Atkinson for his useful comments on an earlier draft of the manuscript. We also thank C. Ruiz for providing unpublished data. U. Mellone is supported by an FPU grant of the Spanish Ministry of Education (reference AP2008-0947). R. Limiñana has a postdoctoral grant (reference 10/12-C) co-funded by “Consejería de Educación y Ciencia” (JCCM) and the European Social Fund. P. López-López is supported by a “Juan de la Cierva” postdoctoral grant of the Spanish Ministry of Economy and Competitiveness (reference JCI–2011–09588). This paper is part of the Ph.D. dissertation of U. Mellone at the University of Alicante. This study complies with the current laws in Spain.
