Long-distance Migration of Eleonora's Falcon: Ecological Barriers and Migration Patterns -, Apuntes de Ecología

¡Descarga Long-distance Migration of Eleonora's Falcon: Ecological Barriers and Migration Patterns - y más Apuntes en PDF de Ecología solo en Docsity! RESEARCH ARTICLE From the Mediterranean Sea to Madagascar: Are there ecological barriers for the long-distance migrant Eleonora’s falcon? Pascual López-López • Rubén Limiñana • Ugo Mellone • Vicente Urios Received: 5 October 2009 / Accepted: 5 February 2010 / Published online: 21 February 2010
Springer Science+Business Media B.V. 2010 Abstract We examined the connection between landscape characteristics and behaviour of a long- distance migratory raptor. Our main goal was to test whether long-distance migratory birds adjust their migration programme according to the different characteristics of the habitats crossed during the journey with special emphasis in the so-called ‘‘ecological barriers’’, inhospitable environments such as deserts, ice fields, seas and mountain ranges, where the opportunities to fulfil energy requirements are low or absent and environmental factors could be extremely severe. To this end, 11 Eleonora’s falcons were tracked by satellite telemetry in their ca. 9000 km autumn migration route from colonies located in Western Mediterranean to their wintering grounds in Madagascar during 2007 and 2008. Our results show that Eleonora’s falcons migrated during day and night-time, adjusting migration speed and daily distance in relation to the crossed region. Unlike other migrant species, Eleonora’s falcons did not avoid ecological barriers by making unnecessary detours around them or converging on narrow corridors. Nocturnal migration and higher daily distances were observed when flying across the Sahara Desert and the Mozambique Channel. The circadian pattern of activity budget shows that Eleonora’s falcon relies on an internal navigation mechanism that works during both day and night. Finally, our results suggest that the Sahara is an ecological barrier not only for passerines but also for raptors migrating within the Palaearctic-African flyway. Keywords Falco eleonorae
Long-distance migration
Navigation
Orientation
Route convergence
Satellite tracking Introduction During their migratory movements between breeding and wintering ranges, birds face a variety of landscapes that can greatly affect their migration paths and schedules (Klaassen et al. 2008). Detailed understanding of the connection between landscape characteristics and behaviour of migrating birds is important in the light of current global changes. Moreover, this is particularly important in the case of long-distance migratory species for which changes in environmental conditions could affect timing of P. López-López (&) Cavanilles Institute of Biodiversity and Evolutionary Biology, Terrestrial Vertebrates Group, University of Valencia, Polı́gono de la Coma s/n, 46980 Paterna, Valencia, Spain e-mail: Pascual.Lopez@uv.es; lopez.pascual@gmail.com P. López-López
R. Limiñana
U. Mellone
V. Urios Grupo de Investigación Zoologı́a de Vertebrados, CIBIO, Universidad de Alicante, Apdo. 99, 03080 Alicante, Spain 123 Landscape Ecol (2010) 25:803–813 DOI 10.1007/s10980-010-9460-7 reproduction and migratory behaviour. In particular, ‘‘ecological barriers’’ have constrained the evolution of migration pathways. These are inhospitable envi- ronments such as deserts, ice fields, seas and mountain ranges, where the opportunities to fulfil energy requirements are low or absent and environ- mental factors could be extremely severe (e.g. extreme temperatures or adverse wind conditions; Newton 2008; Strandberg et al., in press). For example, there is a general agreement that the Sahara Desert is the major ecological barrier of the Palae- arctic-African migration system, especially for small birds such as passerines (Schmaljohann et al. 2007), as Himalaya and Karakorum mountain ranges are for migratory birds in Asia (Combreau et al. 2009). Recent studies have suggested that the equatorial rainforest could be an obstacle for migrating falcons (Strandberg et al. 2009a). On the other hand, vast open ocean could be a migration corridor for landbirds, since this environment provides a wind- assisted passage relatively free of pathogens and predators (Gill et al. 2009), challenging previous hypotheses and even the physiological limits of migratory birds. In order to overcome an ecological barrier, migrating birds can choose among different strate- gies. Birds can either (1) make a detour to avoid crossing the barrier; (2) concentrate along routes that involve a shorter crossing; (3) try to maximise the migration speed reducing the travelling time when flying over the barrier; and even (4) the combination of the second and third scenarios. In the first scenario, a clear significant change in migration direction when approaching the barrier would be expected, whereas, in the second scenario, converging routes rather than scattered ones would be expected. In the third case, the expected behaviour would be the achievement of higher travelling speed during the barrier crossing (eventually increasing flight speed and reducing the number of stops, e.g. flying during night; Alerstam 2009), counterbalanced by more stops when flying across more suitable regions. To test these hypotheses, we used satellite-based telemetry to investigate the case of an extreme long- distance migratory raptor, the Eleonora’s falcon (Falco eleonorae), in the 9000 km migration between breeding colonies in western Mediterranean Sea and wintering areas in Madagascar. Eleonora’s falcon is one of the smallest bird species that is possible to track with satellite transmitters without exceeding 3% of bird’s body mass (Kenward 2001), and for this reason, while there are several studies on migration of large raptors, those dealing with medium and small-sized species have been absent until recently. In addition, Eleonora’s falcon crosses a huge variety of different environments such as large water bodies, deserts and dense forests that presumably could be acting as ecological barriers, and thus this species may provide interesting insights into the behavioural response of migratory birds to landscape characteristics. Materials and methods Study species The Eleonora’s falcon is a cliff-nesting raptor that usually breeds on isolated small islands and feeds mainly on small birds and insects (Ferguson-Lees and Christie 2001). A unique characteristic of the species is that it adjusts its breeding season to coincide with the post-breeding autumn migration of its small passerine prey, usually in late August and early September, making it one of the latest raptor breeding seasons in the Northern Hemisphere (Walter 1979). The global population has been recently estimated between 13,000 and 14,000 breeding pairs (Dimal- exis et al. 2008) after a strong decrease in population numbers in past decades, mainly due to poisoning in foraging areas, decrease of food abundance and human disturbance at colonies (Walter 1979; Dimal- exis et al. 2008). Unlike bigger raptors, such as eagles and vultures that migrate by exploring thermal convection using soaring flight, the Eleonora’s falcon is characterised by higher wing aspect ratio and therefore is more adapted to flapping flight (Spaar 1997). This allows Eleonora’s falcons to migrate irrespective of large water bodies (Kerlinger 1989; Meyer et al. 2000) and therefore it is a good model to study landscape effects on avian migration patterns. Animal tagging, PTT programming and study area The 11 Eleonora’s falcons tracked in this study were captured in the Balearic Islands in autumn 2007 and 2008, and in the Columbretes Islands in autumn 2008 (Table 1), both in Spain. Birds were trapped using 804 Landscape Ecol (2010) 25:803–813 123 Fig. 1 Autumn migration routes of six Eleonora’s falcons (Falco eleonorae) tracked by satellite telemetry from their breeding colonies in the Western Mediterranean to Madagascar during 2007 and 2008. Route of adult birds shown with solid line and the juvenile with dashed line. Desert and equatorial rainforest regions are highlighted in two shades of grey (adapted from Olson et al. 2001). The main geographic regions used for analyses are shown (see text for details) Landscape Ecol (2010) 25:803–813 807 123 each interval assigned to an hour according to local time at the end of the segment. Local time was calculated by correcting GMT times according to each time zone. Nocturnal segments were those for which at least half the time length occurred after sunset or before sunrise. The exact time of sunrise and sunset for every location was obtained from the website http://aa.usno.navy.mil. Segments were con- sidered either ‘‘travelling’’ or ‘‘stationary’’ according to the same criteria mentioned before (stationary if migration speed was \5 km/h) (Strandberg et al. 2009b). Differences in travel rates among regions were tested by means of contingency tables. Results After trapping and marking 11 Eleonora’s falcons, we obtained six complete autumn migration routes from the Western Mediterranean breeding colonies to wintering areas in Madagascar, corresponding to four adults, one subadult (second calendar year) and one juvenile (Fig. 1). Detailed migration parameters, bird histories and signal transmission data are shown in Table 1. The comparison of the observed routes with randomly simulated ones did not show significant differences that would suggest convergence towards goal areas or travelling along narrow corridors (Fig. 2). Similar results were obtained when exclud- ing the juvenile from analyses and when dividing the journey in two or three intervals (all tests non- significant, Table 2). Daily distances differed among regions (Kruskal– Wallis test: H4,30 = 16.18, P = 0.003), with the highest value observed in the Mozambique Channel and the lowest in the Sahel (Fig. 3). The comparison of observed speeds with expected speeds among different regions showed a high variation within individuals, with results being significant in 11 cases (Table 3). Observed speeds were lower than expected in the Sahel (four cases) and in the equatorial region (two cases), while higher speeds were observed in the Sahara and in the Mozambique Channel, respectively. The average number of daily travelling hours was 11.3 ± 4.6 h (range: 5–24), with higher values in the Mozambique Channel (24 h) and the Sahara (12.7 ± 6.6 h), and the lowest in the Sahel region (9.2 ± 3.2 h). Birds migrated during both day and night and within all regions (Fig. 4), although during night-time there were differences in the number of travelling segments among regions (Fig. 5; v2 = 29.67, d.f. = 3, P \ 0.001). The nocturnal travel rate was higher in Sahara than in the Sahel (v2 = 24.1, d.f. = 1, P \ 0.001). However, no differences occurred among the equato- rial region and SE Africa plains (v2 = 2.01, d.f. = 1, n.s.). During day-time, no differences occurred among the four regions (v2 = 3.4, d.f. = 3, n.s.) but interest- ingly, of the six Saharan segments, none was a stationary one. Discussion Our results show that Eleonora’s falcons tracked from Western Mediterranean islands migrate during day and night-time, travelling through inland Africa until reaching the wintering areas in Madagascar. Similar inland routes have been reported for Eleonora’s falcons tracked from other Mediterranean colonies Fig. 2 Comparison between a mean longitude and b scatter of longitudes (measured as standard deviation), for the six observed routes of Eleonora’s falcons (connected by a solid line with triangles) and 1,000 simulated random tracks (dashed line with circles). Values were calculated at 5 latitude intervals 808 Landscape Ecol (2010) 25:803–813 123 either in Sardinia (Gschweng et al. 2008) or Greece (http://www.ornithologiki.gr/life/falcoel/en/program/ satellite_map.php; unpubl. data). The Eleonora’s falcons tracked in this study migrated through the Sahara Desert, the Sahelian region and the equatorial rainforest without making any detour to avoid those regions, until finally converging in SE Africa (Tanzania and Mozambique) just before crossing the Mozambique Channel. Despite individual variation, our analysis did not discover the existence of narrow migration corridors through ecological barriers (e.g. the Sahara Desert or the equatorial rainforest; Bert- hold 2001; Strandberg et al. 2009a). In fact, the only apparent convergence occurred in the final part of the route, which leads to the shortest route between mainland Africa and Madagascar. Our results are different than those obtained by Strandberg et al. (2009a) for the Eurasian hobby (Falco subbuteo) using the same random tracks simulation analysis, despite the close taxonomic relationship between the two species and their similar food habits (Ferguson-Lees and Christie 2001). In their migration from Northern Europe to Southern Africa, Eurasian hobbies converged in a narrow corridor after crossing the equatorial rainforest, suggesting that the rainforest acts as an ecological barrier for migratory birds, perhaps related to reduced feeding opportunities at this habitat (Strandberg et al. 2009a). Commenting on the results of satellite tracking of Eleonora’s falcons breeding in Sardinia, the same authors hypothesized that this could also happen for Eleonora’s falcons because the adults partially avoided the rainforest, migrating along the eastern border, and juveniles changed their direction abruptly after beginning the crossing of the rainforest (Gschweng et al. 2008). However, in our study, four of six adults crossed the equatorial rainforest, and Table 2 Comparison between observed migration parameters (mean longitude and scatter in longitude measured as standard deviation) and a set of 1,000 simulated random tracks per animal Latitudinal range Individuals Mean longitude observed Mean longitude simulated Mean s.d. longitude observed Mean s.d. longitude simulated Number of random simulations P-value longitude P-value s.d. longitude 1 interval 35N 15S All 21.049 24.896 12.445 12.285 6000 0.818 0.560 35N 15S Adults 22.551 25.896 11.931 12.046 4000 0.786 0.649 2 intervals 35N 10N All 11.313 9.856 2.618 2.580 6000 0.360 0.717 10N 15S All 29.497 28.356 10.745 11.250 6000 0.362 0.667 35N 10N Adults 13.173 11.523 2.982 2.793 4000 0.333 0.542 10N 15S Adults 30.718 29.631 10.041 10.734 4000 0.457 0.551 3 intervals 35N 15N All 10.911 8.618 2.712 1.747 6000 0.279 0.557 15N 0 All 18.691 19.548 8.073 7.505 6000 0.609 0.333 0 15S All 35.337 35.847 6.523 6.503 6000 0.557 0.500 35N 15N Adults 12.751 10.423 3.127 2.086 4000 0.256 0.415 15N 0 Adults 20.776 21.636 8.017 7.384 4000 0.705 0.250 0 15S Adults 36.126 37.108 6.068 5.921 4000 0.750 0.333 To analyze for convergence in the migratory route, comparisons were made between the migration route as one single interval, and by dividing into two and three latitudinal intervals. Comparisons were also made including all individuals together (juvenile, subadults and adults) or only adults Fig. 3 Daily distance covered across the five main regions during autumn migration of six Eleonora’s falcons tracked by satellite telemetry. Median, 25 and 75% percentiles and maximum and minimum data are shown Landscape Ecol (2010) 25:803–813 809 123 the crossing of desert landscapes, the lower travel rates observed in the Sahel region just after having crossed the Sahara desert may reflect a strategy to replenish their energy reserves in a more productive environment. Our study also shows that long-distance migratory birds adjust their migration activity accord- ing to the different landscapes crossed during the journey, but that the response differs among individ- uals. In the light of the rapid shift of world biomes due to global change (Williams et al. 2007), detailed understanding of the connection between landscape characteristics and behaviour of long-distance migra- tory birds is of utmost importance. This is especially important in the case of long-migrant species crossing such a great variety of environments as Eleonora’s falcon do, for which small changes in environmental conditions could have unexpected consequences that could jeopardize timing of reproduction and even the survival of maladjusted birds (carry-over effects), given the mismatch between migration schedules and food availability (Both et al. 2006). Forecasting how global changes will shape the future behaviour of migratory birds constitutes the next challenge. Acknowledgements The Terra Natura Foundation and the ‘‘Conselleria de Medi Ambient, Aigua, Urbanisme i Habitatge’’ of the Generalitat Valenciana financed this project. Special thanks are due to J. Jiménez and J.V. Escobar of the ‘‘Servicio de Biodiversidad’’ of the regional government. We would like to thank J. De la Puente, A. Bermejo, E. Escudero (SEO-Monticola), J.L. Martı́nez (GOB), M. Suárez (GOB) and T. Muñoz (GOB) who helped in trapping some Eleonora’s falcons in Balearic Islands and V. Ferrı́s, E. Sánchez, B. Sarzo, M.A. Bartolomé and C. Garcı́a who helped us in Columbretes Islands. The ‘‘Conselleria de Medi Ambient’’ of the ‘‘Govern Balear’’ kindly gave permission to trap falcons in Balearic Islands, and special thanks are due to J. Mayol and J. Muntaner. J. Garcı́a, sexed the falcons, and blood samples were provided by Ll. Parpal of the ‘‘Centre de Recuperació de Fauna de Balears’’. L.M. Carrascal, T. Alerstam and R. Strandberg kindly gave us statistical advice and helped us revise a previous draft of the manuscript. We also thank two anonymous referees and E. Gustafson for valuable comments on earlier versions of this manuscript. P. López-López and U. Mellone are supported by FPU grants of the Spanish Ministry of Science and Innovation (references AP2005-0874 and AP2008-0947). This paper is part of the Ph.D. of U. Mellone and complies with the current laws in Spain. References Alerstam T (2009) Flight by night or day? Optimal daily timing of bird migration. J Theor Biol 258:530–536. doi: 10.1016/j.jtbi.2009.01.020 Argos (1996) User’s manual. CLS/Service Argos, Toulouse Berthold P (2001) Bird migration. A general survey. Oxford University Press, New York Both C, Bouwhuis S, Lessells CM, Visser ME (2006) Climate change and population declines in a long-distance migratory bird. Nature 44:81–83 Bub H (1991) Bird trapping and bird banding. Cornell Uni- versity Press, Ithaca Combreau O, Judas J, Lawrence M (2009) Importance of satellite tracking in Houbara Bustard conservation program in Asia. In: Proceedings of the 2009 bird fish tracking conference. Microwave Telemetry Inc., Elicott City Coyne MS, Godley BJ (2005) Satellite tracking and analysis tool (STAT): an integrated system for archiving, analyz- ing and mapping animal tracking data. Mar Ecol Prog Ser 301:1–7 De Candido R, Bierregaard RO, Martell MS Jr, Bildstein KL (2006) Evidence of nocturnal migration by Osprey (Pandion haliaetus) in North America and Western Eur- ope. J Raptor Res 40:156–158 Dimalexis A, Xirouchakis S, Portolou D, Latsoudis P, Karris G, Fric J, Georgiakakis P, Barboutis C, Bourdakis S, Iv- ovič M, Kominos T, Kakalis E (2008) The status of Ele- onora’s falcon (Falco eleonorae) in Greece. J Ornithol 149:23–30. doi:10.1007/s10336-007-0207-4 Ferguson-Lees J, Christie DA (2001) Raptors: birds of prey of the world. A & C Black Publishers, Ltd., London Garcı́a-Ripollés C, López-López P, Urios V (in press) First description of migration and wintering of adult Egyptian vultures Neophron percnopterus tracked by GPS satellite telemetry. Bird Study Gill RE, Tibbitts TL, Douglas DC, Handel CM, Mulcahy DM, Gottschalck JC, Warnock N, McCaffery BJ, Battley PF, Piersma T (2009) Extreme endurance flights by landbirds crossing the Pacific Ocean: ecological corridor rather than barrier? Proc R Soc B 276:447–457 Gschweng M, Kalko EKV, Querner U, Fiedler W, Berthold P (2008) All across Africa: highly individual migration routes of Eleonora’s falcon. Proc R Soc B 275:2887– 2896. doi:10.1098/rspb.2008.0575 Hake M, Kjellén N, Alerstam T (2003) Age-dependent migration strategy in honey buzzards Pernis apivorus tracked by satellite. Oikos 103:385–396 Kenward R (ed) (2001) A manual for wildlife radio tagging. Academic Press, London Kerlinger P (1989) Flight strategies of migrating hawks. Uni- versity of Chicago Press, Chicago Kjellén N, Hake M, Alerstam T (2001) Timing and speed of migration in male, female and juvenile Ospreys Pandion hal- iaetus between Sweden and Africa as revealed by field obser- vations, radar and satellite tracking. J Avian Biol 32:57–67 Klaassen RHG, Strandberg R, Hake M, Alerstam T (2008) Flexibility in daily travel routines causes regional varia- tion in bird migration speed. Behav Ecol Sociobiol 62:1427–1432 Limiñana R, Soutullo A, Urios V (2007) Autumn migration of Montagu’s harriers Circus pygargus tracked by satellite telemetry. J Ornithol 148:517–523 Limiñana R, Soutullo A, López-López P, Urios V (2008) Pre- migratory movements of adult Montagu’s Harriers Circus pygargus. Ardea 96:81–96 812 Landscape Ecol (2010) 25:803–813 123 López-López P, Limiñana R, Urios V (2009) Autumn migra- tion of Eleonora’s falcon Falco eleonorae tracked by satellite telemetry. Zool Stud 48:485–491 Meyer SK, Spaar R, Bruderer B (2000) To cross the sea or to follow the coast? Flight directions and behaviour of migrating raptors approaching the Mediterranean Sea in autumn. Behaviour 137:379–399. doi:10.1163/156853900 502132 Newton I (2008) The migration ecology of birds. Academic Press, London, pp 699–727 Olson DM, Dinerstein E, Wikramanayake ED, Burgess ND, Powell GVN, Underwood EC, D’Amico JA, Itoua I, Strand HE, Morrison JC, Loucks CJ, Allnutt TF, Ricketts TH, Kura Y, Lamoreux JF, Wettengel WW, Hedao P, Kassem KR (2001) Terrestrial ecoregions of the world: a new map of life on earth. Bioscience 51:933–938. doi: 10.1641/0006-3568(2001)051[0933:TEOTWA]2.0.CO;2 Rubinstein RY, Kroese DP (2007) Simulation and the Monte Carlo method, 2nd edn. Wiley, New York Schmaljohann H, Liechti F, Bruderer B (2007) Songbird migration across the Sahara: the non-stop hypothesis rejected!. Proc R Soc B 274:735–739 Spaar R (1997) Flight strategies of migrating raptors; a com- parative study of interspecific variation in flight charac- teristics. Ibis 139:523–535 Spaar R, Stark H, Liechti F (1998) Migratory flight strategies of Levant sparrowhawks: time or energy minimization? Anim Behav 56:1185–1197 Stark H, Liechti F (1993) Do Levant sparrowhawks Accipiter brevipes also migrate at night? Ibis 135:233–236 Strandberg R, Klaassen RH, Hake M, Olofsson P, Alerstam T (2009a) Converging migration routes of Eurasian hobbies Falco subbuteo crossing the African equatorial rain forest. Proc R Soc B 276:727–733. doi:10.1098/rspb.2008.1202 Strandberg R, Klaassen RHG, Olofsson P, Alerstam T (2009b) Daily travel schedules of adult Eurasian Hobbies Falco subbuteo—variability in flight hours and migration speed along the route. Ardea 97:287–295 Strandberg R, Klaassen RHG, Hake M, Alerstam T (in press) How hazardous is the Sahara Desert crossing for migra- tory birds? Indications from satellite tracking of raptors. Biol Lett. doi: 10.1098/rsbl.2009.0785 Walter H (ed) (1979) Eleonora’s falcon. Adaptations to prey and habitat in a social raptor. The University of Chicago Press, Chicago Williams JW, Jackson ST, Kutzbach JE (2007) Projected dis- tributions of novel and disappearing climates by 2100 AD. Proc Natl Acad Sci USA 104:5738–5742 Landscape Ecol (2010) 25:803–813 813 123