The Origin of Out-Of-Range Pelicans in Europe: Wild Bird Dispersal Or Zoo

Home , Dalmatian pelican, Great white pelican

Ibis (2008), 150, 606Ð618

BlackwellThe Publishing Ltd origin of out-of-range pelicans in Europe: wild bird dispersal or zoo escapes?

F. JIGUET,* A. DOXA & A. ROBERT Centre de Recherches sur la Biologie des Populations d’Oiseaux, UMR 5173 MNHN-CNRS-UPMC, CP 51, Muséum National d’Histoire Naturelle, 55 rue Buffon, F-75005 Paris, France

We tested whether spatial and annual patterns of occurrence of out-of-range Great White Pelecanus onocrotalus, Dalmatian Pelecanus crispus and Pink-backed Pelicans Pelecanus rufescens recorded in Europe between 1980 and 2004 supported a natural vagrancy theory. Candidate variables tested were those likely to influence dispersal and escape probability (distance to the usual breeding/wintering range, national captive stock), and wild breeding population sizes and their movements (size of breeding colonies, climate conditions on wintering grounds or during dispersal). Spatial vagrancy patterns supported the hypothesis of wild birds dispersing from their normal range, with decreasing national totals with increasing distance to the usual range for the three species. Annual out-of-range numbers of Great White Pelican were predicted by breeding colony size and breeding success in Greece, with a further effect of Sahel rainfall during the previous year. Annual numbers of Dalmatian Pelican were related to the North Atlantic Oscillation index and to breeding success in Greece. Finally, annual numbers of Pink-backed Pelican were predicted by summer Sahel rainfall, which is known to drive dispersal of the species northwards into the sub-Sahelian steppes during wet summers there. Hence, annual vagrancy patterns in Europe were well predicted for all three species by population size indices, reproductive success and/or climatic components, which presumably influence survival and/or dispersal. We therefore consider that vagrancy patterns were driven by wild birds, whereas escapes – even if potentially numerous – do not create sufficient ‘noise’ to hide these patterns. Keywords: dispersal, North Atlantic Oscillation, Pelecanus, Sahel, vagrancy.

The origin of rare birds observed in Europe is of variables affecting wild populations, including climatic concern for authorities maintaining national lists of components suspected of affecting dispersal or sur- naturally occurring species (e.g. Dudley et al. 2006). vival on breeding and wintering grounds and along Whilst genuine vagrancy can be assumed for most migration ﬂyways (Dubois & Luczak 2004, McLaren Siberian or Nearctic passerines (Gilroy & Lees 2003, et al. 2006). McLaren et al. 2006), the case of waterbirds raises Three species of pelican occur annually and natu- more doubts, as large collections of such species breed rally in the Western Palaearctic (Del Hoyo et al. 1992): in captivity throughout Europe, either in zoos or in the Great White Pelican Pelecanus onocrotalus and smaller private collections. Anecdotal ringing recov- the Dalmatian Pelican Pelecanus crispus breed in eries have proven trans-Atlantic vagrancy for some Europe (the latter is rarer) with large numbers in duck species (e.g. Baroteaux et al. 2005), whereas Romania (Danube Delta), but colonies also exist progress in isotopic analyses has recently assessed the in other countries such as Greece, Albania, Bulgaria Siberian origin of a ﬁrst-winter Baikal Teal Anas for- or Ukraine. In Northern Africa, the Pink-backed Pelican mosa collected in Denmark in 2005 (Fox et al. 2007). Pelecanus rufescens is an annual spring and summer However, a more general approach is to examine the visitor to southern Egypt at Abu Simbel on Lake observed vagrancy pattern in relation to ecological Nasser, close to the Sudanese border, sometimes in large numbers (over 90 in 1990 and 1994), and it *Corresponding author. also breeds just outside the Western Palaearctic in Email: [email protected] Saudi Arabia (over 300 pairs; Newton & Symens 1996).

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Outside their usual breeding grounds, migrating dispersal: breeding colony size (either because flyways or dispersal ranges, pelicans are regularly breeding birds cannot disperse while breeding, or reported in western and northern Europe. Such because larger population size implies a higher over- out-of-range birds are generally considered to be of all probability of some birds dispersing further doubtful wild origin, because all three species are (Veit 2000) or of detecting one bird dispersing further); kept in captivity, with some free-flying breeding breeding success (because larger breeding failure parties in a few zoos. As examples, in France for the might lead to more opportunity for failed breeders last 15 years there have been free-flying Dalmatian to disperse before normal migration); climatic con- Pelicans at Parc des Oiseaux of Villard-les-Dombes, ditions (temperature, precipitation) during the pre- Ain department, eastern France (c. 50 birds with up vious year or winter (which could affect individual to eight free-flying adults), and a free-flying colony survival and therefore the pool of birds available for of Pink-backed Pelican has been present at the dispersal) or during the current year (which could African Reserve of Sigean, Aude department, Medi- affect the dispersal amplitude). terranean coast (c. 30 pairs with, for example, 18 chicks fledged in 2004) since 1974. These birds are SPECIES-SPECIFIC PREDICTIONS known to wander a few tens of kilometres around their breeding sites. Therefore, casual pelicans observed In autumn, European populations of Great White in western and northern Europe, far away from the Pelican undergo long-distance movements across known ranges of wild populations, could have originated Turkey and the Middle East into Africa (Crivelli et al. from captive stocks, and obviously some do. Never- 1991a, Izhaki et al. 2002): pelicans arrive in the theless, pelicans are very good flyers (Weimerskirch Danube Delta late March–April and leave September et al. 2001) and are able to disperse over large areas to early November, whereas African breeders are (Izhaki et al. 2002), so the possibility of natural generally sedentary. Many Asian breeders winter in vagrancy far away from their usual quarters is entirely Pakistan (up to 25 000 individuals) and India (up to plausible. 10 000 individuals); 11–17 000 birds are found in For this study, we gathered official records of out- Senegal and Mauritania, and 75 000 in eastern Africa of-range pelicans from Europe and Israel between (Del Hoyo et al. 1992). European populations winter 1980 and 2004, to test predictions that could support in eastern Africa, possibly in Kenya and/or in Sudan a natural vagrancy instead of an escape theory. We (Izhaki et al. 2002). There are only two accepted first examined among-country variation in out-of-range records from Morocco (Thévenot et al. 2003), which total numbers during the whole period for each supports the theory that the resident African breeders species, and tested for the effects of population sizes are unlikely to be the source of out-of-range European officially kept in captivity in each country and of the records. Breeding population size in Europe could distance to the closest breeding colony (Great White drive the stock of individuals ‘available’ for European and Dalmatian Pelicans) or the only regular occur- vagrancy, as well as the water conditions during the rence site in the Western Palaearctic (Pink-backed previous winter in the winter quarters (eastern Pelican). If spatial patterns in out-of-range pelican Africa and India), which is possibly influenced by occurrences are mainly due to local escapes we annual precipitation during the previous year. Indeed, should find a positive effect of the size of national the amount of annual rainfall is known to influence captive stocks on national totals, and if they are the abundance of the species in some African wetlands driven by the dispersal of wild birds the number of (Guillet & Crowe 1987). We therefore considered out-of-range birds should decrease with increasing breeding population size and breeding success in distance to the usual range. Greece (the available data), the annual North Atlantic In a second approach, we made species-specific Oscillation (NAO) index in the current year, and predictions derived from the published descriptions annual standardized Sahel rainfall, Indian rainfall, of dispersal and migration strategy as found in the Monsoon index, annual rainfall in Sudan, all four Handbook of the Birds of the World (Del Hoyo et al. later climatic components in the previous year, as 1992; see below). The predictions were tested for potential predictors of out-of-range Great White each species on national annual numbers recorded in Pelican numbers in Europe. 18 countries. Candidate variables tested are those The Dalmatian Pelican is really only dispersive, most likely to influence wild population sizes, and rather than truly migratory, except in Asia; European therefore the pool of birds that are available for birds move short distances, staying mostly in the

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eastern Mediterranean zone (Crivelli et al. 1991b). we should also find a positive link between the Recoveries of birds ringed in former USSR suggest number of national records and the number of birds movement to the west or southwest, but recoveries kept in captivity in the country. If most of these of birds ringed in Greece suggest movement to the pelicans are of a wild origin, some of the species- southeast and also to the north (Bulgaria), with a few specific predictions should be validated, as long as recoveries in Israel, with pelicans arriving on breed- escapes do not create sufficient ‘noise’ to hide the ing grounds in February–March and leaving in August natural vagrancy pattern. In other words, temporal (Del Hoyo et al. 1992). Breeding population size in variation in out-of-range pelican numbers should be Europe could drive the stock of individuals available well explained by some of the proposed predictors, for long-distance vagrancy. As European birds are while it would not exclude that at least some indi- resident or dispersive, local winter climate conditions viduals had a captive origin. In this case, we should could influence local survival, and affect the pool of also find a negative link between national number of live birds that could potentially disperse the follow- records and the distance to the closest breeding ing year. Indeed, preliminary analyses of ringing data colony (or to southern Egypt for the Pink-backed indicated an effect of winter temperature and of the Pelican), suggesting a diffuse dispersal from the usual NAO index on survival rate in Greece (A. Doxa range. unpubl. data). We considered the breeding population size of six colonies in four countries (Greece, METHODS Albania, Bulgaria and Turkey) and breeding success in Greece (the available data), winter temperature at Pelican records two wintering sites in Greece, annual NAO index in the current year, and the Indian monsoon index and We gathered data on out-of-range pelicans from winter Indian rainfall (if Asian populations disperse official records with identification validated by national westwards) in the previous year or winter as potential rarities committees. Therefore the data relate to predictors of out-of-range Dalmatian Pelican numbers pelican records in countries where the species are in Europe and Israel. considered to be rare. We sent an e-mail asking for The Pink-backed Pelican breeds in sub-Sahelian national 1980–2004 accepted records to the mailing Africa, and makes regular movements north into list of the AERC (Association of European Records sub-Saharan steppes to coincide with the short sum- and Rarities Committees). Members of national rar- mer wet season there; local movements are possibly ities committees who provided information are cited related to water conditions or beginning of breeding; in the Acknowledgements. We also collected official the species can breed all year round, mostly starting records in annual reports of such committees, as late in the rainy season (Del Hoyo et al. 1992). Data published in ornithological journals, e.g. Ornithos on annual variation in breeding numbers are not (France), Limicola (Germany), Avocetta and Rivaria available for this species, but annual spring and Italiana Ornitologica (Italy), Dutch Birding (the summer rainfall in the Sahel could well influence Netherlands), Ardeola (Spain), British Birds (the UK). northward dispersal to Europe. Furthermore, rainfall Data were obtained for 17 countries in Europe plus conditions on breeding grounds could influence Israel: Austria, Belgium, Cyprus (not for Great White dispersal, so we considered spring (March–May) and Pelican), Denmark, Estonia and Finland (but no summer (June–August) rainfall in the Sahel, summer pelicans were identified to species in these two rainfall anomaly in Sudan, as well as annual rainfall countries), France, Germany, Hungary, Italy, Lux- in Kenya during the previous year, and the annual embourg, the Netherlands, Norway, Poland, Spain, NAO index as potential predictors of out-of-range Switzerland, and the UK. Data from Israel (Dalmatian Pink-backed Pelican numbers in Europe and Israel. and Pink-backed Pelicans only) were obtained from If out-of-range pelicans are mostly escapes, we Shirihai (1996) with the addition of two records of should not find any significant correlation between single Pink-backed Pelicans observed in 1997 and breeding numbers or climatic components and 2000 (Smith & the IRDC 2007). Individual birds temporal observation patterns, as long as the escape that have obviously escaped from captivity (e.g. birds probability of captive-bred pelicans in Europe does with evidence of wing-clipping, wearing zoo rings) not depend on the size of wild breeding colonies or are excluded from national counts by national rarities climatic conditions in Africa or Asia, which seems committees if reported to them. We therefore intuitive. If out-of-range pelicans are local escapes, considered all records accepted as category A (wild

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origin) or category D (wild origin possible but not average monthly temperature in January (n = 18 certain), but available data could not include relevant countries, r = 0.82) or in July (r = 0.85). We then comprehensive information on known escapes looked for potential effects of national captive stocks (category E of national lists), which were therefore (as the number of birds officially kept in zoos in each not considered, except for the Pink-backed Pelican country, obtained from the web portal of the ISIS – for which we considered all documented records http://www.isis.org/CMSHOME/) and of the distance even if not published by rarities committees (with from a country barycenter to the usual range, as breeding the exception of those obtained at close proximity to colonies (either in the Danube Delta 45.2°N, 29.2°E the French free-flying colony, which are not consid- or in Greece 40.8°N, 21.1°E) for the Great White ered by the French rarities committee). For the Great and Dalmatian Pelicans, or as the regular occurrence White Pelican in Italy, we gathered records from site within the Western Palaearctic for the Pink- different sources with the help of Nicola Baccetti, a backed Pelican (i.e. Abu Simbel on Lake Nasser in member of the Italian RC, as the species is not southern Egypt; 22.34°N, 31.72°E). For the latter considered by this committee. Finally, different species, we also considered the distance to the large rarities committees have different stances on what free-flying colony in southern France (c. 80 birds at they consider acceptable for a potential wild origin. the African Reserve of Sigean) as a fifth control So the datasets we used certainly include escapes, variable, as birds originating from this breeding pop- but the most obvious ones have been excluded. ulation could well be responsible for some European However, as we are interested in temporal variation records. These analyses were conducted using log- in out-of-range numbers, our results should not depend linear models, first adjusted for the effects of the four on such cases, as long as their annual distribution is or five control variables, then for the effects of the close to random. two predictors adjusted to each other (type III error). In total, records included 216 Great White, 40 We did not consider hierarchical partitioning analyses Dalmatian and 92 Pink-backed Pelicans. Pelican as our data had first to be adjusted for the effects of numbers kept in European zoos have been found on the number of documented years, total area, wetland the web portal of the International Species Informa- area and latitude. The number of captive birds (+1) tion System ISIS (http://www.isis.org/CMSHOME/): and distances (originally in kilometers, obtained there were 636 Great White, 367 Dalmatian and 167 from GoogleEarth at www.earth.google.fr) were log- Pink-backed Pelicans officially reported in captivity transformed before analyses. throughout Europe in 2006. In these analyses, we used all information available: 18 countries for Dalmatian and Pink-backed Pelicans, but without Estonia, Cyprus and Israel for the Great Variation among countries White Pelican. We examined variation in national totals among countries for the whole period and for each species. Breeding numbers and success Raw data used were total number of out-of-range individuals recorded in each country for the period. Breeding colony sizes for the Great White Pelican in As the information on presence or absence of records Greece (Lake Mikri Prespa) were obtained for the was not available for each country in each year period 1983–98 from Crivelli et al. (2000). The between 1980 and 2004, we first controlled for an same reference was also used to obtain breeding effect of the number of years with available data (so numbers of Dalmatian Pelican at six colonies: Greece including years with information that there was no (two colonies), Albania (one colony), Bulgaria (one record in that year). We also controlled for potential colony) and Turkey (two colonies) for the period effects of country size (as the total area covered by 1980–98. Additional data for the period 1999–2004 the country: larger countries could receive more were also available for the two Greek colonies of pelicans just because they are large), total area covered Dalmatian Pelican (D. Hatzilacou, G. Catsadorakis by wetlands in the country (as the amount of available & H. Nikolaou unpubl. data). As breeding numbers suitable habitat where out-of-range pelicans could were not reported for each colony each year for the stop), and mean latitude of the country (as a proxy Dalmatian Pelican, we further estimated an annual for climate, related to the latitudinal gradient of abundance index of breeding pairs. The abundance temperatures across Europe). Latitude is strongly index was obtained from a log-linear model that correlated with other climatic variables, such as accounts for missing data performed on the annual

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number of breeding pairs in each colony and calcu- average December–January temperatures for each lated using the software TRIM (TRends and Indices year over the period 1980–2004, as the mean of the for Monitoring data; Pannekoek & van Strien 2001). two sites. TRIM is designed to analyse time-series of counts with missing observations using Poisson regression Statistical analyses on annual patterns (log-linear models). Missing counts from particular colonies were estimated (‘imputed’) from changes in We used pelican data of annual national totals per all other colonies. This abundance index was highly species for all countries, when data was available correlated with the (log-transformed) breeding (true absence of national records in a given year numbers at Prespa in Greece (Pearson’s correlation, being reported as zero). For each species, we tested n = 24, r = 0.94). Breeding successes of Great White our predictions by performing a stepwise log-linear (1984–98) and Dalmatian (1984–2003) Pelicans at model (Poisson distribution and log-link function) Greek colonies were also considered as the average on national number of out-of-range pelicans observed number of fledged young per pair (Catsadorakis each year, with an additive effect of country. Effects et al. 1996, M. Malakou & H. Nikolaou unpubl. of predictors were tested while being adjusted to data). Breeding success and (log-transformed) colony each other (type III errors). The annual colony size size were highly negatively correlated for the Great of Great White Pelicans was log-transformed before White (r = −0.584, n = 15, P < 0.01) and positively the analysis. All tested predictors were included in a correlated for the Dalmatian Pelican (data from first model and we then performed a stepwise selec- Prespa in Greece; r = 0.636, n = 20, P < 0.001). tion of the best model explaining the variance most parsimoniously, i.e. with the smallest set of predictors using the Akaike Information Criterion (Akaike Large scale climate indices 1973). Some links to large-scale climatic variables were There is a distinction between finding the best found on the Climate Diagnostics Centre website model to describe the data and drawing inferences (http://www.cdc.noaa.gov/ClimateIndices/). The about the likely causality of variables, and dealing selected variables were the annual NAO index with multicollinearity is difficult in single-model (http://www.cgd.ucar.edu/cas/jhurrell/indices.data. approaches. A possible solution is hierarchical parti- html#naostatann), the monthly standardized Sahel tioning, which uses all models in a regression hierarchy rainfall (http://jisao.washington.edu/data/sahel/), the to distinguish those variables that have high inde- monthly Indian rainfall as well as the annual Indian pendent correlations with the dependent variable Monsoon index (http://www.cdc.noaa.gov/Correla- (Chevan & Sutherland 1991). We therefore also tion/indiamon.data). Data were initially obtained on analysed our data with hierarchical partitioning a monthly basis, but were also computed on an (MacNally 2002). For each species, we first performed annual (sum of monthly data from January to a regression on out-of-range numbers by considering December) or seasonal (December–February, March– a country effect alone, and stored the residuals to May, June–August and September–November) basis perform the hierarchical partitioning on them. We when judged necessary. Annual rainfall at Nairobi, obtained the independent (I) and joint (J) contribu- Kenya, was obtained from http://envstudies.brown.edu/ tions of the predictors; Z-scores were obtained using thesis/2005/timothy_downing/Rainfall.htm. Spring 500 repeated randomizations (Walsh & MacNally 2003). (March–May) and summer (July–September) rainfall We performed these analyses using the hier.part in Sudan were obtained from the Climate Explorer package of the R statistical software (R DCTeam 2004). of the Royal Netherlands Meteorological Institute We are aware that performing regression or hierar- KNMI (http://climexp.knmi.nl/start.cgi?someone chical analyses on residuals obtained from a prelim- @somewhere). Rainfall in Sudan was considered inary regression model can be sensitive (Freckleton because the Sahel rainfall index does not cover 2002), but we thought that this hierarchical parti- Eastern Africa, although it covers a wide area and is tioning could be an interesting complementary probably more representative of African rainfall analysis to the stepwise regression models we per- than data from Sudan. Winter temperatures used for formed, though their results are to be considered with the Dalmatian Pelican analyses were those from some precaution. We did not consider hierarchical Amvrakikos Gulf and Lake Kerkini, two wintering partitioning approaches for studying spatial patterns sites for the species in Greece; we considered the in out-of-range records, as the dependant variable

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Table 1. Results of log-linear models performed on national totals of out-of-range pelicans (period 1980Ð2004) for countries with available data. Models were first adjusted for effects of the number of years with documentation, total country area, wetlands area per country, and latitude. After controlling for these variables, two predictors were tested: number of birds kept in captivity in each country and shortest distance to the usual range. For the Pink-backed Pelican, we also (b) replaced the distance to the usual range by the distance to the French free-flying colony, and (c) then tested the effect of distance to the usual range in a model initially also controlling for the effect of distance to the free-flying colony. Significant P-values are in bold.

Species Predictor Estimate ± sd t-value P

P. onocrotalus Captive stock 0.83 ± 0.20 4.10 0.003 (df = 8) Distance to closest breeding site −2.72 ± 0.30 −8.99 2.10−5 P. crispus Captive stock −0.86 ± 0.29 −1.97 0.07 (df = 11) Distance to closest breeding site −4.04 ± 0.81 −4.97 0.001 P. rufescens (a) Captive stock −0.12 ± 0.15 0.86 0.41 (df = 11) Distance to Lake Nasser −1.27 ± 0.13 −1.87 0.088 (b) Captive stock −0.11 ± 0.13 −0.83 0.42 (df = 11) Distance to French ‘colony’ −1.56 ± 0.39 −3.97 0.002 (c) Captive stock −0.14 ± 0.14 −1.01 0.34 (df = 10) Distance to Lake Nasser −2.46 ± 0.71 −3.44 0.006

had first to be adjusted to four/five control variables, Great White Pelican only a positive effect of the and performing hierarchical partitioning on residuals national number of birds kept in captivity. without accounting for error estimation for these For the Pink-backed Pelican, we also ran a similar control variables would produce questionable results. model but replaced the distance to Abu Simbel by the distance to the free-flying colony in southern France (43.03°N, 2.98°E). In this model, 79.6% of RESULTS variance was captured, and we found no significant effect of the national captive stock but a significant Comparing zoo and out-of-range pelican effect of the distance to the free-flying colony numbers (Table 1). We ran a final model for this species, first A chi-squared test revealed that numbers of captive controlling for effects of the four previous control vs. out-of-range birds have different proportions variables in addition to distance to the free-flying χ2 = < across the three species (2 65.6, P 0.001), with colony, and further looked at adjusted effects of the highest number of birds observed in the wild, captive stock and distance to the usual range. In this compared to the captive stock, for the Pink-backed model (Table 1), 86.7% of variance was captured, Pelican (the species with the highest number of free- and we found a significant effect of distance from the flying birds), and the lowest for the Dalmatian Pelican usual range (Table 1; t = −3.44, df = 10, P = 0.002). (the most sedentary species). Inter-annual occurrence variation Variation among countries Great White Pelican Results of log-linear models investigating among We used data on out-of-range Great White Pelicans country variation in national totals are presented in in Europe from 1983 to 1998, including records Table 1. Proportion of variance captured by models from Austria (three birds), Belgium (two), France (with four control variables and two predictors) was (30), Germany (four), Hungary (24), Italy (10), the 96.4% for the Great White Pelican, 72.5% for the Netherlands (two), Poland (45), Spain (13), Swit- Dalmatian Pelican and 74.7% for the Pink-backed zerland (one) and the UK (one). The initial model Pelican. The four control variables alone captured included colony size at Mikri-Prespa (Greece), NAO 52.6%, 39.6% and 71.8% of total variance for the index in the current year, standardized Sahel rainfall, Great White, Dalmatian and Pink-backed Pelicans, Indian Monsoon index, annual Indian rainfall, annual respectively. For the first two species, we found a sig- Kenyan rainfall and annual Sudanese rainfall, all in nificant negative effect of the distance to the closest the previous year. The final log-linear model included natural occurrence site (see Table 1), and for the two predictors: colony size (t = −6.70, df = 151,

df = 124, P < 0.001; Fig. 2) and the breeding success (t = −2.71, df = 124, P < 0.001); 32.3% of the total variance was captured.

Pink-backed Pelican We used data on out-of-range Pink-backed Pelicans in Europe and Israel from 1980 to 2004, including records from Austria (one bird), Belgium (four), France (28), Germany (nine), Hungary (nine), Israel (three), Italy (24), Luxembourg (one), the Nether- lands (one), Norway (two), Poland (one), Spain (14), Switzerland (one) and the United Kingdom (three). The initial stepwise log-linear model first included the annual NAO index, annual, spring (March–May) Figure 1. Correlation between annual number of out-of-range Great White Pelicans Pelecanus onocrotalus observed in Europe and summer (June–August) Sahel rainfall anomalies, and breeding colony size in Greece. Each dot represents 1 year spring and summer rainfall in Sudan, as well as annual between 1983 and 1998. Variables are log-transformed. rainfall in Kenya during the previous and current year. The final model included three predictors: standardized Sahel rainfall in spring (t = 1.64, df = 183, P < 0.001; Fig. 1) and standardized annual Sahel P = 0.10) and summer (t = 3.46, df = 183, P < 0.001), rainfall during the previous year (t = 2.42, df = 151, and annual rainfall in Kenya during the current year P = 0.017), which captured 55.5% of the total (t = 2.37, df = 183, P = 0.019), which captured 50.8% variance. of the total variance. We ran this model again after We further ran the same stepwise model after replacing the standardized spring and summer Sahel excluding records from Hungary and Poland, where rainfalls with a single combined standardized spring– the species is considered to be of wild origin and summer Sahel rainfall (as the sum of spring and where records are most numerous (69, so more than summer values, so from March to August). In this half of the total). The final model included the same case, the final model included this Sahel rainfall two predictors: colony size (t = −5.42, df = 121; variable, which was highly significant (t = 4.81, P < 0.001) and standardized Sahel annual rainfall df = 184, P < 0.001; Fig. 3), and annual rainfall in during the previous year (t = 3.52, df = 121, P < 0.001), Kenya (t = 2.23, df = 184, P = 0.027); 47.5% of the with 54.8% of total variance captured. total variance was captured. These results were If also considering the reproductive success in the robust to the exclusion of a potential outlying year initial model, the final model for all countries included (2001), as the Sahel received exceptional rainfall three predictors: colony size (t = −6.18, df = 142, during spring and summer in that year, while 12 P < 0.001), breeding success (t = −1.90, df = 142, Pink-backed Pelicans were recorded in southern P = 0.059) and standardized annual Sahel rainfall Europe (see Fig. 3): spring–summer Sahel rainfall during the previous year (t = 2.98, df = 142, P = 0.003), (t = 3.69, df = 171, P < 0.001; annual rainfall in for which 55.9% of the total variance was captured. Kenya, t = 3.13, df = 171, P = 0.002); 43.0% of total variance was captured. Dalmatian Pelican We used data on out-of-range Dalmatian Pelicans in Hierarchical partitioning Europe and Israel from 1980 to 2003, including Results of the hierarchical partitioning are presented records from Cyprus (three birds), France (one), in Table 2, where independent and total (independent Hungary (14), Israel (five), Italy (one), Spain (10) and joint) contributions of predictors are given, as and Poland (three). The initial stepwise log-linear well as the Z-scores (for the generated distribution of model first included annual estimates of breeding randomized independent contributions of variables pair numbers, breeding success in Greece, NAO Is) and their corresponding statistical significance. index, Indian monsoon index in the previous year, For the Great White Pelican, we found a significant winter rainfall in India (December–February) and independent effect of the breeding colony size but winter temperature in Greece. The final model not of the breeding success. The hierarchical partition- included two variables: the NAO index (t = 3.41, ing for the Dalmatian Pelican identified independent

Table 2. Results of hierarchical partitioning of variance investigating the temporal patterns in out-of-range records of three species of pelicans in Europe. The hierarchical partitioning is performed on residuals from a first regression model accounting for a country effect. Independent (I) and total (independent and joint) contributions of predictors are given, as well as the corresponding Z-scores (obtained using 500 repeated randomizations) and their statistical significance. Significant P-values are in bold.

Species Predictor I I + J Z-score P

P. onocrotalus Colony size 0.0717 0.0939 7.88 <10–10 Breeding success 0.0055 0.0223 −0.17 − NAO 0.0005 0.0007 −0.68 − Sudanese rainfall 0.0123 0.0324 0.74 0.23 Sahel rainfall 0.0045 0.0123 −0.23 − Indian rainfall 0.0011 0.0004 −0.66 − Monsoon index 0.0009 0.0005 −0.69 − P. crispus Colony size 0.0051 0.0093 −0.29 − Breeding success 0.0314 0.0206 1.42 0.078 NAO 0.0461 0.0361 3.33 4.10–4 Winter temperature 0.0034 0.0061 −0.50 − Indian rainfall 0.0023 0.0004 −0.85 − Monsoon index 0.0019 <0.0001 −0.86 − P. rufescens NAO 0.0045 0.0025 −0.11 − Sahel rainfall (spring) 0.0090 0.0243 0.39 0.348 Sahel rainfall (summer) 0.0131 0.0145 1.23 0.109 Sahel rainfall (spring + summer) 0.0182 0.0320 2.52 0.006 Sudanese rainfall 0.0170 0.0127 0.89 0.187 Kenyan rainfall 0.0312 0.0158 1.68 0.046

contributions of NAO index and breeding success an adult Great White Pelican coming back from its (though the latter just short of statistical significance; African wintering grounds faces an alternative, either Table 2), and spring/summer Sahel rainfall and breeding or dispersing. Such a decision could depend Kenyan rainfall were significant independent contri- on local spring conditions or previous wintering butions for the Pink-backed Pelican (Table 2). conditions, which could determine the opportunity for such long-lived birds to invest in reproduction in a given year (Stearns 1992). Moreover, we found a DISCUSSION negative effect of breeding success on out-of-range numbers, revealing that for a given colony size Great White Pelican (because effects of predictors were adjusted to each National totals of out-of-range numbers during the other in regression models, which means that the whole period were significantly positively correlated effect of breeding success was measured on residuals with the number of birds kept in captivity; we that were independent of colony size), vagrancy is conclude that some of the out-of-range Great White more likely when more breeders failed in their Pelicans observed in Europe were in fact escapes, breeding attempt. This suggests that more failed even if they were not obvious ones (obvious escapes breeders might disperse during the summer. In such being excluded from national reports by rarities a scenario, we should expect out-of-range birds to committees). However, we also found a significant, be mainly potential breeders, hence mature adults, strong negative correlation with the distance to the and to occur in late spring and summer. Indeed, closest breeding colony, suggesting that out-of-range most out-of-range Great White Pelicans observed in records could also include birds dispersing from western and northern Europe have been reported European breeding sites. as adults (see Fig. 4a, 4b). The records for 1980–2004 When testing species-specific predictions (inter- concerned 37 adults, two subadults and 17 imma- annual occurrence variation), we found a highly tures in Poland; 15 adults, five subadults and five significant negative relationship between breeding immatures in Hungary; and 22 adults and four numbers in Greece and out-of-range numbers in immatures in France. For these three countries, two Europe, suggesting that, for a given pool of live birds, abundance peaks were obvious in April–May, and to

a lesser extent in August–September, which probably from breeding colonies, and probably were not mirror the dispersion of adult-type non-breeders in mainly local zoo escapes (we found no significant spring and of failed breeders in summer. Ageing effect of national captive stocks). Great White Pelicans is difficult in the field, espe- When testing species-specific predictions on inter- cially outside the breeding season, because 2- or annual occurrence variation, we found, as for the 3-year-old immatures can look adult-like, although previous species, a negative relationship between the ages of birds reported here are as reported by out-of-range records and breeding success in Greece. national rarities committees. This suggests that failed breeders might be prone to Furthermore, wintering conditions seem to influ- disperse, which is in accordance with the abundance ence the potential for migrants to disperse into peak of European records in late spring (Fig. 4c). western or northern Europe, as we found an effect of More interesting was the positive relationship found Sahel rainfall during the previous year on out-of-range with the annual North Atlantic Oscillation index, numbers, although this effect was not confirmed by suggesting that general atmospheric conditions in the hierarchical partitioning analysis. Such rainfall Europe (a large NAO is generally linked to larger air could affect the water conditions on the wintering mass movements over the continent; Stenseth et al. grounds, and then the ability of European individu- 2002) might influence the survival or the dispersal of als to survive the winter in Africa and to come back the species in Europe. Interestingly, this pattern to Europe the next spring. We obtained similar results approaches the one found for the Great White when excluding data from Hungary and Poland, two Pelican: a negative effect of breeding numbers and/or countries with numerous records of vagrant Great breeding success in the current year and a positive White Pelicans and where they are considered to be effect of a climatic variable potentially enhancing of a wild origin. wintering conditions during the previous winter. The breeding population used here to estimate The observed phenology of out-of-range Dalmatian breeding numbers is relatively small (between 54 Pelicans in Europe and Israel revealed two peaks and 139 pairs) compared with the larger populations (Fig. 4c), in May (after breeding onset, probably due breeding, for example, in the Danube Delta (460– to the dispersal of early-failed breeders) and in 2000 pairs; Schogolev et al. 2005), but it is not October following autumn dispersal. inconceivable that factors affecting breeding numbers in Greece could also affect those in Romania, and Pink-backed Pelican the very strong relationship found here between European vagrant and Greek breeding numbers Models for this species produced the most surprising suggests that many Great White Pelicans observed in results, as it initially seemed fair to consider European western and northern Europe are genuine vagrants, records as involving only zoo escapes. But as for the and indeed come from such European populations. other two species, national totals of out-of-range Greater confidence in this pattern would be sup- numbers during the whole period were significantly ported by the use of breeding numbers in Greece negatively correlated with the distance to the closest and in the Danube Delta, too, but annual surveys of regular occurrence site in the Western Palaearctic the species in the Danube Delta are not regular and (Lake Nasser in southern Egypt). However, these only started in 1996. Available censuses gave 1800 national totals were also well predicted by the dis- breeding pairs in 1996, 2000 in 1997, 460 in 1999 tance to the large colony of free-flying birds located and 1700 in 2001 (Schogolev et al. 2005); only 2 of in southern France, so Pink-backed Pelicans observed these years were included in our analyses (available in the wild around Europe certainly include captive- censuses of breeding colony size in Greece from reared birds. When controlling for this effect in an 1983 to 1998). adjusted model, the number of national records still increased with decreasing distance to Abu Simbel, though the high totals from France and Spain strongly Dalmatian Pelican suggest that most of these birds are escapes from the National totals of out-of-range numbers during the French free-flying colony. However, beyond the whole period were significantly negatively correlated effects of variables controlled for, the correlations we with the distance to the closest breeding colony, found seem to support the controversial hypothesis suggesting that out-of-range Dalmatian Pelicans of natural dispersal to Europe of a few African wild observed in Europe could involve birds dispersing Pink-backed Pelicans.

When testing species-specific predictions (inter- annual occurrence variation), we first did not expect to predict variation in European annual records with a climatic variable known to drive the northwards dispersal of this species into the Sahel. However, we found a strong positive effect of summer Sahel rainfall and Kenyan annual rainfall on the number of Pink-backed Pelicans reaching Europe and Israel. This pattern was not driven by vagrancy to Israel, which lies closer to breeding sites in eastern Africa and Saudi Arabia, as only three of the 80 records came from this country. This result is in accordance with the observed phenology of the species in Europe and Israel, with more reports in August and September (Fig. 4d), though this could also partly imply a post- Figure 2. Correlation between annual number of out-of-range Dalmatian Pelicans Pelecanus crispus observed in Europe and breeding dispersal of European full-winged zoo Israel (first adjusted to breeding success in Greece, e.g. residual birds. The absence of records from the Middle East not explained by this predictor) and the North Atlantic Oscillation (outside Israel) and south-eastern Europe (Turkey, index. Each dot represents 1 year between 1984 and 2003. Greece) could well reflect a lack of detection of the Numbers of out-of-range pelicans have been log-transformed. species, due to a low observation effort or little inter- est in verifying the specific identity of any observed pelican. The phenology of records during the year, with at least three to four birds recorded each month (Fig. 4d), is probably a nice illustration of the potential ‘noise’ created by escapes. Genuine European vagrants could find their origin in eastern or western Africa (e.g. the record from the Canary Islands), and as natural movements are known to occur in Africa with northward dispersal into the Sahel during the short wet summer of this region, our results are consistent with a wild origin of some Pink-backed Pelicans in Europe in some years, driven by rainfall amplitude in the Sahel from June to August. As examples, some of the records obtained in 1990, 1994 and 2001 could well be attributed to natural vagrancy from Africa; in these years unprec- Figure 3. Correlation between annual number (log-transformed) edented large numbers of Pink-backed Pelicans were of out-of-range Pink-backed Pelicans Pelecanus rufescens recorded in Europe and Israel and standardized springÐsummer noted in southern Egypt on Lake Nasser (more than (MarchÐAugust) Sahel rainfall. Each dot represents 1 year 90 individuals in 1990 and 1994, and at least 30 in between 1980 and 2004. The dashed line represents the linear April 2001). Spring and summer rainfall in the Sahel trend obtained when excluding data from 2001, which could have was exceptional in 2001 and in that year 10 birds been an outlier. were seen in Italy (including a group of five juveniles during September), one individual was reported In Saudi Arabia, four major nesting colonies of from Corsica (France), and one individual was sighted Pink-backed Pelicans with 310 active nests were in Andalucia (Cadiz province of Spain). Although discovered in 1995; the breeding season appears to Europe could be regarded as having received unusual span October–February; the Saudi Arabian population numbers of Pink-backed Pelican in 2001, this year holds c. 1200 birds and a further 300–500 probably falls well within the modelled pattern obtained if occur along the Yemen Red Sea coast (Newton & 2001 is excluded from the analysis (see Fig. 2), and Symens 1996). Given the breeding phenology of thus it is likely that some Pink-backed Pelicans this population, the last chicks fledge just before the observed in Europe were of wild origin and not just beginning of the wet season in the Sahel and the escapes. northward migration of Great White Pelicans through

Figure 4. Phenology of out-of-range records of pelicans, on a monthly basis. (a) Great White Pelican Pelecanus onocrotalus (for a total of 215 birds observed between 1980 and 2004); (b) Great White Pelican, for all countries except Poland and Hungary; (c) Dalmatian Pelican Pelecanus crispus (for the 40 birds reported in this study between 1980 and 2003); (d) Pink-backed Pelicans Pelecanus rufescens (for a total of 91 birds observed between 1980 and 2004). Only the ﬁrst date of observation is considered for birds that remained at one site for a long time or for individual birds that were recorded switching between sites. Results are also presented according to the age of the birds if reported (adult-type versus immatures).

Ethiopia, Sudan and the Middle East; hence it seems escaped pelicans wandering around Europe, either conceivable that some Pink-backed Pelicans prone to wearing zoo rings or not. Indeed, our results on disperse may join migrating Great White Pelicans in variation among countries revealed that the data we sub-Sahelian or Sahelian Africa and Saudi Arabia used should include escapes for the Great White Pel- and further disperse into Europe during the summer. ican (the larger the national captive stock, the more records in a country) and for the Pink-backed Pelican (with more records in countries closer to the French CONCLUSION free-ﬂying zoo colony). However, as national num- By regulation, captive birds of non-domestic species bers of out-of-range birds decreased with increasing should wear special rings to indicate their origin, distance to usual ranges, and as annual variations in although this is often not the case. In France, ﬂedged out-of-range numbers have been well predicted by Pink-backed Pelicans from the African Reserve of meaningful ecological and climatic variables, our Sigean have been ringed annually since 2002, but results give strong support to a genuine occurrence were not marked before this time. There are certainly of all three pelican species in northern and western

Europe. However, determining the true origin of any Crivelli, A.J., Leshem, Y., Mitchev, T. & Jerrentrup, H. 1991a. particular individual will never be an easy task, unless Where do Palaearctic Great White Pelicans (Pelecanus it had been ringed in a wild population, and would onocrotalus) presently overwinter? Rev. Ecol. Terre Vie 46: 145Ð171. be mainly probabilistic, based on the analysis of Crivelli, A.J., Mitchev, T., Catsadorakis, G. & Pomakov, V. global pattern and climatic conditions whenever 1991b. Preliminary results on the wintering of the Dalmatian relevant. Finally, such analyses could also be con- Pelican, Pelecanus crispus, in Turkey. Zool. Middle East 5: ducted to assess the potential genuine occurrence in 11Ð20. Europe of other African/Asian waterbirds. For example, Crivelli, A.J., Catsadorakis, G., Hatzilacou, D., Hulea, D., Malakou, M., Marinov, M., Michev, T., Nazirides, T., Peja, N., the Pygmy Cormorant Phalacrocorax pygmeus occurs Sarigul, G. & Siki, M. 2000. Status and population develop- annually in western and central Europe outside its usual ment of Great White Pelican Pelecanus onocrotalus and range, while it shares a large range with Eurasian Dalmatian Pelican P. crispus breeding in the Palearctic. In pelicans. Among African species suspected to reach Yésou, P. & Sultana, J. (eds) Monitoring and Conservation of Europe naturally, similar analyses could be developed Birds, Mammals and Sea Turtles of the Mediterranean and Black Seas: 38Ð46. Malta: Ministry of Environment. for Ruddy Shelduck Tadorna ferruginea, Fulvous Del Hoyo, J., Elliott, A. & Sargatal, J. (eds) 1992. Handbook of Whistling Duck Dendrocygna bicolor, Lesser Flamingo the Birds of the World, Vol. 1. Barcelona: Lynx Edicions. Phoenicopterus minor, African Spoonbill Platalea alba, Dubois, P.J. & Luczak, C. 2004. Les limicoles néarctiques en Yellow-billed Mycteria ibis and Marabou Stork France: synthèse des données pour la période 1965Ð2000. Leptoptilos crumeniferus and Allen’s Gallinule Porphyrio Ornithos 11: 214Ð229. Dudley, S.P., Gee, M., Kehoe, C., Melling, T.M. & the British alleni. Ornithologists’ Union Records Committee (BOURC) 2006. The British List: a Checklist of the Birds of Britain (7th edition). Alain Crivelli provided invaluable help in gathering original Ibis 148: 526Ð563. data and commenting on early analyses. D. Hatzilacou, Fox, T., Christensen, T.K., Bearhop, S. & Newton, J. 2007. G. Sarigul, M. Malakou, M. Siki, P. Simeonov and H. Using stable isotope analysis of multiple feather tracts to Nikolaou provided unpublished data on pelican censuses. identify moulting provenance of vagrant birds: a case study of We wish to thank all authorities who provided access to Baikal Teal Anas formosa in Denmark. Ibis 149: 622Ð625. national records: Jean-Yves Frémont and Georges Olioso Freckleton, R.P. 2002. On the misuse of residuals in ecology: (France), Nicola Baccetti, Daniele Occhiato, Luciano Rug- regression of residuals vs. multiple regression. J. Anim. Ecol. gieri and Marco Zenatello (Italy), José Ignacio Dies (Spain), 71: 542Ð545. Colin Richardson (Cyprus), Bernard Volet (Switzerland), Gilroy, J.G. & Lees, A.C. 2003. Vagrancy theories: are autumn Patric Lorgé (Luxembourg), Johannes Laber (Austria), vagrants really reverse migrants? Br. Birds 96: 427Ð438. Tamás Zalai (Hungary), Tadeusz Stawarczyk (Poland), Guillet, A. & Crowe, T.M. 1987. Monthly and seasonal changes Vegard Bunes (Norway), Antero Lindholm (Finland), Uku in the aquatic avifauna at Rondevlei Bird Sanctuary (Cape Province, South Africa). Avocetta 11: 1Ð16. Paal (Estonia) and Laurent Raty (Belgium). Pierre-Yves Izhaki, I., Shmueli, M., Arad, Z., Steinberg, Y. & Crivelli, A. Henry provided an easy access to climatic databases, while 2002. Satellite tracking of migratory and ranging behavior of Julien Gonin and Pierre Crouzier helped with clarifying immature Great White Pelicans. Waterbirds 25: 295Ð304. the current status of captive but free-ﬂying breeding peli- MacNally, R. 2002. Multiple regression and inference in ecology cans in France. Pierre Camberlin provided data on rainfall and conservation biology: further comments on identifying in Sudan from the Royal Netherlands Meteorological important predictor variables. Biodiv. Conserv. 11: 1397Ð1401. Institute. Stuart Newson helped with improving the McLaren, I.A., Lees, A.C., Field, C. & Collins, K.J. 2006. English and three anonymous referees provided helpful Origins and characteristics of Nearctic landbirds in Britain comments on a ﬁrst draft of the manuscript. and Ireland in autumn: a statistical analysis. Ibis 148: 707Ð 726. Newton, S.F. & Symens, P. 1996. 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