Pinching Off Syndrome In Free-ranging White-tailed Sea Eagles ( Haliaeetus Albicilla

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1 Pinching Off Syndrome In Free-ranging White-tailed Sea Eagles (Haliaeetus Albicilla) In Europe: Frequency And Geographic Distribution Of A Generalized Feather Abnormality Author(s): Kerstin MüllerDr Med Vet, Rainer AltenkampDipl Biol, Leo BrunnbergProf Med Vet, PhD, Lucia FašungováMVD, Hubert Freymann, Kai FrölichDr Med Vet, Dr Biol, PhD, Rainer KollmannProf Biol, PhD, Oliver KroneDr Med Vet, Ivan LiterákProf MVD, PhD, Tadeusz MizeraPhD, Paul Sömmer, and Elvira SchettlerDr Med Vet Source: Journal of Avian Medicine and Surgery, 21(2): Published By: Association of Avian Veterinarians DOI: URL: %5D2.0.CO%3B2 BioOne ( is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne s Terms of Use, available at Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder. BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research.

2 Journal of Avian Medicine and Surgery 21(2): , by the Association of Avian Veterinarians Original Studies Pinching Off Syndrome in Free-ranging White-tailed Sea Eagles (Haliaeetus albicilla) in Europe: Frequency and Geographic Distribution of a Generalized Feather Abnormality Kerstin Müller, Dr Med Vet, Rainer Altenkamp, Dipl Biol, Leo Brunnberg, Prof Med Vet, PhD, Lucia Fašungová, MVD, Hubert Freymann, Kai Frölich, Dr Med Vet, Dr Biol, PhD, Rainer Kollmann, Prof Biol, PhD, Oliver Krone, Dr Med Vet, Ivan Literák, Prof MVD, PhD, Tadeusz Mizera, PhD, Paul Sömmer, and Elvira Schettler, Dr Med Vet Abstract: Generalized feather abnormalities are rarely documented in free-living birds. Pinching off syndrome (POS) is a feather abnormality in which all remiges and retrices become malformed and are lost during the nestling stage, rendering the bird unable to fly. To determine the frequency of occurrence and geographic distribution of this syndrome in white-tailed sea eagles (Haliaeetus albicilla) in Europe, we sent questionnaires to ornithologists in 19 countries within the European range of this species. We also searched for reported cases of sea eagles with feather abnormalities that met the criteria of POS. Overall, 32 nestlings or fledglings with POS were identified between 1975 and The geographic distribution of cases was primarily restricted to 4 European countries: Germany (17 cases), Poland (11 cases), the Czech Republic (3 cases), and Great Britain (1 case). Eleven eagles from Germany and 2 eagles from the Czech Republic were examined clinically. In 15 birds in which sex was determined, 8 were female and 7 were male. From 2000 to 2005, the 5-year incidence of POS in white-tailed sea eagles in Germany was 3.5 cases per 1000 birds. Although the etiology of this syndrome in wild sea eagles is unknown, our results support a possible genetic cause. Key words: pinching off syndrome, feather loss, feather disease, feather dystrophy, avian, birds of prey, white-tailed sea eagle, Haliaeetus albicilla From the Small Animal Clinic, Free University of Berlin, Oertzenweg 19b, Berlin, Germany (Müller, Brunnberg), the Institute of Biology and Zoology (Section Evolutionary Biology), Free University of Berlin and Raptor Conservation Group Aquila e.v., Naturschutzstation Woblitz, Fürstenberg, Germany (Altenkamp), the Department of Biology and Wildlife Diseases, Faculty of Veterinary Hygiene and Ecology, University of Veterinary and Pharmaceutical Sciences, Palackého 1-3, Brno, Czech Republic (Fašungová, Literák), Welsower Str. Ausbau 2, Kerkow, Angermünde, Germany (Freymann), the Leibniz-Institute for Zoo and Wildlife Research, Alfred-Kowalke-Str. 17, Berlin, Germany (Frölich, Krone, Schettler), the Project Group for the Protection of the White-tailed Sea Eagle, Olshausenstraße 40, Kiel, Schleswig-Holstein, Germany (Kollmann), the Zoology Department, Agricultural University, Wojska Polskiego 71c, PL Poznan, Poland (Mizera), the Naturpark Uckermärkische Seen, Naturschutzstation Woblitz, Fürstenberg, Germany (Sömmer), and the Wildlife Park Eekholt, Großenaspe, Germany (Schettler). Introduction Generalized feather abnormalities are frequently documented in pet birds, especially in psittacine birds, 1 4 but are extremely rare in wild birds. 5 7 One of these abnormalities is the generalized pinching off syndrome (POS) in fledglings of the white-tailed sea eagle (Haliaeetus albicilla) This syndrome was first reported in a white-tailed sea eagle from Schleswig-Holstein, Germany, in In described cases of eagles with this syndrome, all remiges and retrices are malformed, 9,13 and contour feathers are sometimes malformed to varying degrees as well. Feather attachment of the primary and secondary feathers and retrices to the papillae is often weak. Therefore, many birds have already lost all flight feathers when found. Affected birds are unable to 103

3 104 JOURNAL OF AVIAN MEDICINE AND SURGERY Table 1. European countries included in the survey, contacted persons, and the number of reported cases of whitetailed sea eagles with pinching off syndrome. Country Cases Contact person(s) Austria 0 R. Probst Croatia 0 M. Schneider-Jacoby Czech Republic 3 I. Literák, L. Fašungová Denmark 0 B. Génsbøl Estonia 0 T. Randla Finland 0 J. Koivusaari, P. Saurola, T. Stjernberg Germany 17 P. Hauff, R. Kollmann, C. Scharnweber, P. Sömmer Great Britain (Scotland) 1 J. Grant, R. Broad, R. Dennis, R. J. Evans Greenland (Denmark) 0 F. Wille Hungary No response Iceland 0 K. H. Skarphedinsson Latvia No response Lithuania 0 D. Dementavicius Norway 0 T. Nygard Poland 11 T. Mizera, Z. Pielowski Russia (1 a ) S. Ganusevich, V. Ptschelinzev Slovakia 0 J. Chavko, M. Adamec, J. Lengyel Sweden 0 B. Helander, J.-E. Wallin Ukraine 0 M. Gavrilyuk a Excluded from further analysis; see text. fly because of malformed or missing flight feathers. In reports of birds with POS that were kept in temporary captivity, feather development deteriorated and new flight feathers were malformed and became progressively shorter with every new feather generation. 9,13 Investigations thus far into the cause of this syndrome have failed to determine an etiologic agent. 14 The purpose of this study was to determine the distribution and frequency of POS within the range of white-tailed sea eagles in Europe. Materials and Methods A questionnaire with a detailed description of POS including photos of affected birds was designed and sent to all known researchers of white-tailed sea eagles in the 19 European countries (including Greenland) where this species occurs (Table 1). We asked for information concerning eagles with feather abnormalities and for detailed descriptions and photographs. When a suspected case of POS was reported, information was confirmed by personal contact. Additionally, we searched for published information about affected eagles. In most cases, these cases were reported without a complete description. 8,11,12 Therefore, we contacted the involved researchers for more detailed information. Eagles that were reported or brought to private individuals, zoos, or raptor rehabilitation centers without veterinary examination were included in this study only if the typical symptoms of POS were documented with a detailed description and/or photograph. When possible, live birds were brought in for clinical examination. For classification as POS, feather alterations in white-tailed sea eagles had to meet 6 or more of the following criteria: 1) loss of all or most flight and tail feathers and eventually covert feathers during the nestling or fledgling period (Fig 1); 2) longitudinal splitting or deformation of the rachis of the primary or secondary feathers and retrices (Fig 2b); 3) excessive keratin deposition on the ventral side of the rachis (Fig 2c); 4) extremely shortened primary and secondary feathers and retrices, including the calamus (Fig 3); 5) curved appearance of the primary and secondary feathers and retrices; 6) replacement of lost abnormal flight and tail feathers by new abnormal feathers; 7) new feathers easily removable; and 8) constriction of the distal part of the calamus. Where possible, sex of affected birds was determined by polymerase chain reaction testing, by endoscopy, or at necropsy. Results Replies to the questionnaire were received from 17 European countries within the range of whitetailed sea eagles (Table 1). Eagles with feather abnormalities from Germany were reported by

4 MÜLLER ET AL PINCHING OFF SYNDROME IN WHITE-TAILED SEA EAGLES 105 Figure 1. (a) Fledgling white-tailed sea eagle with pinching off syndrome standing on the nest. All flight feathers and most retrices are lost. Mecklenburg-Western Pomerania, Germany, August 2005 (photograph courtesy of R. Nestmann). (b) Fledgling white-tailed sea eagle with pinching off syndrome (sedated). All primaries and secondaries are malformed or lost. All but 1 malformed retrices are lost as well. Brandenburg, Germany, July 2005 (photograph courtesy of G. Fritsch). (c) Wing of a healthy white-tailed sea eagle (photograph courtesy of K. Müller). Figure 2. Ventral surface of a tail feather of a healthy white-tailed sea eagle. (b) Primary of a white-tailed sea eagle with pinching off syndrome. Note open rachis on the ventral side of the feather. (c) White-tailed sea eagle with pinching off syndrome showing excessive keratin deposition on the rachis. (Photographs courtesy of U. Leinen.)

5 106 JOURNAL OF AVIAN MEDICINE AND SURGERY Figure 3. Normal secondary (left) of a healthy whitetailed sea eagle compared with extremely short flight feathers of a white-tailed sea eagle with pinching off syndrome, Brandenburg, Germany, July 2005 (photograph courtesy of U. Leinen). Rüger, 12 Oehme and Manowsky, 11 and Robitzky. 8 All of these cases were confirmed as POS and therefore included in this study. Eleven eagles from Germany and 2 eagles from the Czech Republic were evaluated clinically. From the results of questionnaires, clinical reports, and clinical evaluations, a total of 32 free-living sea eagles with POS were identified between 1975 and With 1 exception (see below), the geographic distribution of eagles with this syndrome was restricted to the white-tailed sea eagle population south of the Baltic coast (Fig 4a). Most POS cases were found in Germany (17 cases) and Poland (11 cases) (Fig 4a and b). Three eagles with POS were identified in the Czech Republic, 2 in 2001 and 1 in One case in Scotland was geographically isolated. One case was reported from the Kola peninsula (Russia), but because information was not confirmed for this case, it was omitted from Figure 4 and from further analysis. Sex was determined in 15 birds (8 females, 7 males), comprising 13 birds from Germany and from 2 birds from the Czech Republic. Sex was determined in the 2 birds from the Czech Republic by polymerase chain reaction testing and in the 13 birds from Germany by endoscopy or at necropsy. Information about brood size and siblings of eagles with POS was obtained from 20 birds. Twelve nestlings with POS were single nestlings, 4 had 1 healthy sibling each, and 1 nestling had 2 healthy siblings. In 1 nest, both nestlings were affected (Czech Republic, 2001), and 1 affected nestling had a sibling of unknown health status. In Germany, nestlings with POS occurred at the same nest site 2 (3 nests) and 3 (1 nest) times at Figure 4. (a) European range of white-tailed sea eagles (hatched area) and distribution of white-tailed sea eagles with pinching off syndrome (POS) in Europe, (white circles) (n 5 32). Four circles represent 2 and 1 circle represents 3 cases of POS each (see Fig. 4b, Table 2). Note the isolated case of POS in Great Britain. Range of white-tailed sea eagle based on Helander and Mizera, 15 Evans et al, 16 Gavrilyuk and Grishchenko, 17 Hauff, 18 Helander, 19 Lipsbergs and Bergmanis, 20 Mecionis and Dementavicius, 21 Mizera, 22 Procházka, 23 Ptschelinzev, 24 Saurola et al, 25 Schneider- Jacoby et al, 26 Tofft, 27 and Volke and Randla. 28 (b) Distribution of white-tailed sea eagles with POS in Germany, Poland, and the Czech Republic (n 5 31) within 3 time periods. Numbered spots indicate nests from which nestlings with POS hatched in 2 (numbers 123) or 3 (number 4) different years. Two nestlings with POS from the Czech Republic in 2001 came from the same nest and are marked with one point. varying time intervals (Table 2). In Poland, a bird with POS fledged from the same nest site in 2 consecutive years (1982 and 1983). Of the 32 cases, 27 affected sea eagles were found near their nests between June and Septem-

6 MÜLLER ET AL PINCHING OFF SYNDROME IN WHITE-TAILED SEA EAGLES 107 Table 2. Nest sites from Germany where white-tailed sea eagle nestlings with pinching off syndrome hatched in different years Nest number Years with affected nestlings , , , , 2005, 2006 ber. One bird from an unknown nesting site was found in November. The date or season of identification was not available for 4 birds. In Germany, 1 white-tailed sea eagle with POS was detected per year from 2000 to 2004, and 3 were identified in 2005 (Fig 5). Between 2000 and 2005, approximately 2300 white-tailed sea eagles fledged in Germany (P. Hauff, oral communication, October 2005). Therefore, the 5-year incidence of POS in white-tailed sea eagles in Germany for the years 2000 to 2005 was 3.5 cases per 1000 birds. However, because not all affected eagles are identified, the true incidence may be higher. Discussion Between 1975 and 2006, 32 free-living whitetailed sea eagles with POS were identified in Germany, Poland, the Czech Republic, and Great Britain. However, the likelihood of identifying young eagles with POS strongly depends on monitoring activities for white-tailed sea eagles and therefore varies by locality. No birds were identified in Sweden, Denmark, Finland, and Austria. Monitoring activities for white-tailed sea eagles are intensive in these countries, similar to Great Britain, Germany, Poland, and the Czech Republic. Affected birds would likely have been found there if present. Furthermore, young sea eagles with POS have survived weeks or even months on the ground, and some birds walked far distances from their nest. The maximum distance to the next known nest site from the area that a young eagle with POS was found was approximately 6 km (2000, Poland). Therefore, a fledged eagle with POS would most probably live until found by members of the public, and affected birds, if present, would likely have been detected in those countries in which none were reported (Table 1). Hence, the distribution and incidence of POS in white-tailed sea eagles reported in questionnaires are likely accurate. Few cases of feather loss and feather abnormalities have been reported in free-living birds of Figure 5. Number and origin of white-tailed sea eagles with pinching off syndrome in Europe from 1975 to 2006 (n 5 32). prey. Pinching off, which usually describes the loss of 1 or a few abnormal premature primary or tail feathers, was first mentioned by Mavrogordato 29 without specifying the involved species. Typical characteristics of the affected feathers are a constricted calamus and a pinched appearance A new normal feather will develop after a brief interval, and the syndrome does not appear to severely impact flying or hunting abilities of the affected birds. 29,30 Pinched-off feathers have been described in different raptor species, such as the northern goshawk (Accipiter gentilis), the lizard buzzard (Kaupifalco monogrammicus), 31 and the common buzzard (Buteo buteo). 35 Without human intervention, generalized feather abnormalities in free-living raptors that involve almost all flight feathers lead to death because the birds are not able to fly. In Europe, apart from white-tailed sea eagles, generalized feather abnormalities are described only from fledglings of the northern goshawk. Four affected goshawks (2 males, 2 females) with feather abnormalities were found in the Netherlands in 1994, , , 33 and As in sea eagles, POS in the goshawks was not related to sex. Two birds, a male (1994) and a female (1996), came from the same nest, each of which had 3 unaffected siblings. The parents were not identified. 33 Very similar to the condition in white-tailed sea eagles, the goshawk fledglings with POS had malformed retrices, coverts, and primary and secondary feathers and were not able to fly. The birds lost a part of the retrices, and the secondary feathers had many stress marks. A free-living goshawk fledgling showing POS was held in captivity in the Netherlands for 2 years. 37 All new growing feathers were abnormal, the coverts had stress

7 108 JOURNAL OF AVIAN MEDICINE AND SURGERY marks, and the primary feathers and retrices were abnormally short. The alula and the primary feather 10 (counted from proximal to distal) on 1 wing were normally developed. This fact, together with the generalized appearance, excludes mechanical irritation. 37 In contrast to POS in whitetailed sea eagles, no cases of POS in goshawks were reported in the following years (R. G. Bijlsma, written communication, November 2005). Feather loss and feather abnormalities are well known in companion avian medicine. Possible causes of skin and feather changes are viral, bacterial, or fungal infections; parasites; trauma; chemical or toxic substances; inadequate nutrition; congenital, neoplastic, or immune-mediated diseases; allergy; irradiation; and neurologic disorders. 38 Also, hormonal imbalances, such as hypothyroidism, may play a role. 39 Investigations into viral, bacterial, fungal, and hormonal causes of POS thus far have failed to reveal an underlying cause. 14 These results strongly support a genetic cause of POS. To our knowledge, POS in white-tailed sea eagles is the first description of a lethal, generalized feather malformation in a free-ranging population of birds of prey. It has occurred in wild birds over at least several decades. The first cases were described in Schleswig-Holstein, Germany, in 1975 and in 1981, when the white-tailed sea eagle population in Germany had decreased to approximately 120 breeding pairs, 40 with 4 to 5 breeding pairs inhabiting Schleswig-Holstein. 41 Moreover, reproduction was extremely low because of contamination with DDT. 40,42 Furthermore, the first affected birds were found within Germany near the western limit of the species. Even now, the incidence of POS near the southwestern limit of the species range in Europe is striking. Therefore, extremely low genetic drift, possible inbreeding, and the longevity of whitetailed sea eagles may have contributed to the persistence of this disorder. The isolated case in Scotland supports a possible association of POS with low genetic drift. The Scottish population of white-tailed sea eagles is the result of a release program. All eagles released in Scotland came from one county in Norway. Furthermore, reproduction of sea eagles in Scotland was restricted to a small number of successful pairs. Between 1985 and 2000, 68% of all young eagles were offspring from only 4 territories. 16 In the future, all researchers who study whitetailed sea eagles and raptors in general should document cases of feather abnormalities in wild birds and collect samples if possible. A centralized archive for such data on a national or at least state-wide scale is urgently required. Acknowledgments: We thank all the European researchers studying white-tailed sea eagles who helped us in detecting eagles with pinching off syndrome, especially T. Broehl, O. Büxler, C. Fentzloff, E. Franke, J. Grant, D. Haas, P. Hauff, F. Jabs, J. Krasselt, V. Latendorf, K. Linke, H. G. Nehls, R. Nestmann, C. Scharnweber, and A. Valentin. We also thank T. Frey and N. Kenntner for their help in preparing the map for Figure 4. L. Fašungová andi. Literák were funded by grant MSM from the Ministry of Education, Youth and Sports of the Czech Republic. References 1. Perry RA. A psittacine combined beak and feather disease syndrome. Proc Conf Post Graduate Comm Vet Sci, Cage and Aviary Birds. 1981: Ritchie BW, Niagro FD, Lukert PD, et al. A review of psittacine beak and feather disease. Characteristics of the PBFD virus. J Assoc Avian Vet. 1989;3: Oglesbee BL, Oglesbee MJ. Feather dystrophy in a cockatiel (Nymphicus hollandicus). J Assoc Avian Vet. 1994;8: Greenacre CB, Latimer KS, Niagro FD, et al. Psittacine beak and feather disease in a scarlet macaw (Ara macao). J Assoc Avian Vet. 1992;6: McOrist S, Black DG, Pass DA, et al. Beak and feather dystrophy in wild sulphur-crested cockatoos (Cacatua galerita). J Wildl Dis. 1984;20: Raidal SR, Riddoch PA. A feather disease in senegal doves (Streptopelia senegalensis) morphologically similar to psittacine beak and feather disease. Avian Pathol. 1997;26: Pass DA, Plant SL, Sexton N. Natural infection of wild doves (Streptopelia senegalensis) with the virus of psittacine beak and feather disease. Aust Vet J. 1994;71: Robitzky U. Artenhilfsprogramm für den Seeadler Haliaeetus albicilla in Schleswig-Holstein. In: Meyburg B-U, Chancellor RD, eds. Eagle Studies. Berlin: WWGBP; 1996: Schettler E, Müller K, Krone O, et al. Severe feather loss and abnormalities ( pinching off ) in a juvenile free-living white-tailed eagle (Haliaeetus albicilla) from northern Germany. Proc Annu Conf Europ Assoc Zoo Wildl Vet / Europ Wildl Dis Assoc. 2002: Mizera T. Bielik. Swiebodzin: Wydawnictwo Lubuskiego Klubu Przyrodników; Oehme G, Manowsky O. Entwicklung und Reproduktion des Seeadlerbestandes im ehemaligen Bezirk Frankfurt/O. unter besonderer Berücksich-

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