The northern bald ibis Geronticus eremita: history, current status and future perspectives
C HRISTIANE B ÖHM,CHRISTOPHER G. R. BOWDEN,PHILIP J. SEDDON T ANER H ATIPOĞ LU,WIDADE O UBROU,MOHAMMED E L B EKKAY M IGUEL A. QUEVEDO,JOHANNES F RITZ,CAN Y ENIYURT,JOSE M ANUAL L OPEZ J ORGE F ERNANDEZ O RUETA,DIDONE F RIGERIO and M ARKUS U NSÖLD
Abstract The northern bald ibis Geronticus eremita was Keywords Conservation, demography, northern bald ibis, once widespread throughout the Middle East, northern population trends, reintroduction, threats, translocation, Africa, and southern and central Europe. Habitat destruc- waldrapp tion, persecution and the impacts of pesticides have led to Supplementary material for this article is available at its disappearance from most of its former range. It disap- doi.org/./S peared from central Europe . years ago, but has per- sisted as a relict and slowly growing breeding population in Morocco, where c. wild birds of all ages remain. In Algeria, the last confirmed breeding was in ;in Introduction Turkey the fully wild population disappeared in , but a population remains in semi-wild conditions. In Syria a he northern bald ibis Geronticus eremita is one of the small population was rediscovered in , only to subse- Trarest birds. Although recently recategorized on the quently decline to functional extinction. Restoration pro- IUCN’s Red List from Critically Endangered to Endan- grammes have been initiated independently in several gered, it has a precariously small wild population lim- locations, with over free-flying birds resulting from ited to a handful of breeding sites, and the main subpopu- reintroduction projects in Austria, Germany, Spain and lation has only recently recovered slightly (BirdLife, ). Turkey, to restore both sedentary and fully migratory popu- The northern bald ibis was probably once widespread lations. Maintaining current efforts in Morocco remains a across the Middle East, northern Africa, and southern and high conservation priority. central Europe, with wintering populations as far south as Mauritania and Senegal, and from the Arabian Peninsula and African Red Sea coast to Eritrea and Ethiopia. Habitat destruction, persecution and the impacts of agricultural CHRISTIANE BÖHM* Alpenzoo Innsbruck, Innsbruck, Austria pesticides led to its disappearance from most of its former CHRISTOPHER G. R. BOWDEN* (Corresponding author, orcid.org/0000-0001- range (Hirsch, , ; Collar & Stuart, ). It was ex- 8271-4311) Royal Society for the Protection of Birds, The Lodge, Sandy, . Bedfordshire, SG19 2DL, UK. E-mail [email protected] tirpated from central Europe years ago, but breeding populations persisted in Morocco, Algeria, Turkey and Syria PHILIP J. SEDDON* Department of Zoology, University of Otago, Dunedin, New Zealand into the th century. The only viable wild population is
TANER HATIPOĞLU Tarım ve Orman Bakanlığı, Ankara, Turkey now in Morocco, but there are significant captive zoo pop- ulations, release projects and semi-wild populations. Here WIDADE OUBROU and MOHAMMED EL BEKKAY Département des Eaux et Forêts, Parc National Souss-Massa, Inezgane, Morocco we review the species’ current status throughout its former
MIGUEL A. QUEVEDO Zoobotánico Ayto, Jerez, Cádiz, Spain range, and look at conservation prospects, ongoing reintro- ductions and natural recolonizations. The geographical dis- JOHANNES FRITZ† Waldrappteam, Mutters, Austria tribution of colonies, projects and sightings (up to and in- CAN YENIYURT Doğa Derneği, İzmir, Turkey cluding ), and consolidated figures for all wild, semi- JOSE MANUAL LOPEZ Consejería de Medio Ambiente Junta de Andalucía, Cádiz, Spain wild, released and captive populations, are summarized in Fig. and Table . JORGE FERNANDEZ ORUETA SEO/BirdLife, Madrid, Spain
DIDONE FRIGERIO† Konrad Lorenz Research Centre for Behaviour and Cognition, University of Vienna, Grünau im Almtal, Austria Indigenous range and population structure MARKUS UNSÖLD‡ Bavarian State Collection of Zoology, Munich, Germany *Joint first authors Based on minor morphological distinctions and preliminary †Also at: Department of Behavioral and Cognitive Biology, University of genetic work, two populations (eastern and western) have Vienna, Vienna, Austria ‡Also at: Waldrappteam, Mutters, Austria been identified, but the extent and timing of their separation Received June . Revision requested July . appears to be minor and recent (Pegoraro et al., ; Wirtz Accepted March . et al., , ). All fully captive populations in Europe,
This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted re-use, Downloadeddistribution, from https://www.cambridge.org/core and reproduction in any medium,. IP address: provided 170.106.33.19 the original work, onis 23 properly Sep 2021 cited. at 12:19:20, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/termsOryx, Page 1 of 13 © The Author(s),. https://doi.org/10.1017/S0030605320000198 2020. Published by Cambridge University Press on behalf of Fauna & Flora International doi:10.1017/S0030605320000198 2 C. Böhm et al.
FIG. 1 Former and recent distribution, projects sites and zoo colonies of the northern bald ibis Geronticus eremita. Data from Collar & Stuart (), Welch & Welch () and Böhm et al. ().
Japan and North America, and those used in European re- The remaining global wild population now occupies a lease projects, derive from western origin birds (Böhm, , small coastal strip in southern Morocco in the region of ), whereas the Turkish semi-wild birds are of local, east- Agadir, where it breeds on sea cliffs in two main areas and ern origin. Thus, although more work is needed, the two is resident year-round. In the Moroccan authorities populations can be regarded as distinct management units. designated the Parc National de Souss-Massa, a , ha coastal protected area specifically delimited to protect the nesting and feeding areas of the northern bald ibis south Western subpopulations of Agadir. The other main breeding and feeding area is a coastal strip km north of Agadir in the region of ’ Morocco Tamri, a no-hunting area designated as a Site d Interêt Bio- logique et Ecologique, but with no formal protection status. Historically, breeding colonies occurred in the High and By a total population of c. birds was breeding in Middle Atlas Mountains and some Atlantic coastal areas three subcolonies within the Parc National de Souss- north of the present colonies. The number of populations Massa, and in one colony at Tamri (Bowden, ). There declined from sites in to in and only three is some movement between these sites, which are c. in , as a result of habitat modification, human distur- km apart (Bowden et al., ; El Bekkay et al., ). bance, hunting and pesticide use (Collar & Stuart, ). A project, started in as a collaboration between the Thevenot et al. () documented a higher number of Royal Society for the Protection of Birds and the Sociedad historical colonies because they treated some dispersed Española de Ornitología, and later Groupe de Recherche colonies as separate entities. Historical records suggest pour la Protection des Oiseaux au Maroc, working with that the now extinct inland populations were migratory, Parc National de Souss-Massa, aims to increase the nor- wintering further south in Morocco and as far away as thern bald ibis population in Souss-Massa. Local fishers Mauritania and Mali (Bowden, ). were hired and trained as wardens, and a range of local
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TABLE 1 Summary of the status of the estimated global adult northern bald ibis Geronticus eremita population in . Totals for captive populations include non-breeding birds, but totals for semi-captive and free-flying populations are recent counts of actively breeding adult birds only. Semi-captive means only seasonally free-flying and not self-sustaining.
Fully Relict Reintroduced Population/country captive Semi-captive free-flying free-flying Total Eastern population Syria 0 0 21 02 Turkey 0 263 0 0 263 Western population Algeria 0 0 0 0 0 Morocco 0 0 708 0 708 Spain 0 0 0 72 72 Germany (Burghausen) 0 0 0 15 15 Austria (Kuchl) 0 0 0 21 21 Austria (Grünau) 26 0 0 26 Austria (Rosegg) 36 0 0 36 European Endangered Species Programme for the 1,745 1,745 northern bald ibis (92 zoos) Extra-limital population North America 140 140 Japan 110 110 Non-studbook population (unknown parentage) Europe c. 800 c. 800 Total c. 2,350 263 710 108 c. 3,950
Syria figure is uncertain because of access and security issues.
rural development projects were implemented in the area increase. By , there was a total of individuals, with to develop grass-root interest in the species’ conservation. pairs raising fledglings. In , pairs bred and Managing and maintaining the local wardening at both there was a post-breeding total population of birds, in- Parc National de Souss-Massa and Tamri has been the cluding recently fledged juveniles. The total population at main intervention, and has been consolidated recently the end of the breeding season was . individuals, with Moroccan government support. with a breeding adult population of pairs (Oubrou & El By the population had declined to pairs following Bekkay, ; Table ). These trends appear to be linked to the unexplained death of birds in (Bowden, ; measures taken by Parc National de Souss-Massa to engage Touti et al., ), but by it had recovered to breed- local communities and develop wardening capacity. Intensive ing pairs (Oubrou & El Bekkay, ) and has continued to monitoring of breeding and feeding sites and the provision of
TABLE 2 Breeding productivity of the northern bald ibis in Souss-Massa and Tamri, Morocco. Pooled data from Bowden et al. (), El Bekkay et al. () and Oubrou & El Bekkay ().
Souss-Massa Tamri Morocco total Year Pairs Fledglings Fledglings/pair Pairs Fledglings Fledglings/ pair Pairs Fledglings Fledglings/ pair 2006 43 74 1.7 41 31 0.8 84 105 1.3 2007 50 81 1.6 55 61 1.1 105 142 1.4 2008 54 55 1.0 45 2 0.0 99 57 0.6 2009 62 90 1.5 49 38 0.8 111 128 1.2 2010 57 80 1.4 48 58 1.2 105 138 1.3 2011 56 79 1.4 49 59 1.2 105 138 1.3 2012 54 56 1.0 11 0 0.0 65 56 0.9 2013 53 77 1.5 60 71 1.2 113 148 1.3 2014 58 112 1.9 57 80 1.4 115 192 1.7 2015 60 111 1.9 56 94 1.7 116 205 1.8 2016 58 56 1.0 53 54 1.0 111 110 1.0 2017 67 69 1.0 55 83 1.5 122 152 1.2 2018 81 110 1.4 66 60 0.9 147 170 1.2
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supplementary fresh water has improved breeding productiv- TABLE 3 Breeding productivity of the northern bald ibis in Birecik, ity (Smith et al., ). The population is apparently depend- Turkey. ent on littoral steppe habitat and a traditional agriculture Year Pairs Fledglings Fledglings/pair system where large areas are left fallow and grazed by sheep 2006 15 26 1.7 for several years at a time. This supports high biomass and 2007 18 30 1.7 diversity of the invertebrates and reptiles that are the main 2008 12 21 1.8 prey for the ibis (Aghnaj et al., ). 2009 21 25 1.2 There is renewed hope that the birds may naturally re- 2010 21 30 1.4 colonize former breeding sites in Morocco (as predicted in 2011 20 27 1.4 Böhm & Bowden, , ). In breeding was confirmed 2012 24 37 1.5 for the first time in several decades in a small subcolony near 2013 32 49 1.5 2014 38 51 1.3 Immsouane (Aourir et al., ), km north of Tamri. 2015 41 59 1.4 2016 35 56 1.6 2017 47 64 1.4 Algeria 2018 59 113 1.9 In Algeria, most of the data on the historic distribution of the species are from the swhen colonies were known. station was established km north of the town of Birecik, Another colony was discovered in in the north-western and birds were caught during – and taken into El Bayadh region, persisting until the late s(Fellous,). semi-captivity. A similar number of birds were left in the Northern bald ibises in Algeria were migratory, arriving at wild. The captive birds were initially enclosed throughout breeding sites towards the end of winter in February and the year, but a decision was made to release them from early March, and departing after breeding in late summer. the aviaries each spring (in mid February, around the The Algerian colonies were historically estimated to be dates they would have arrived back from migration), and c. – birds, but signs of population decline were they were encouraged to breed on the rock ledges and in noted in the s (Collar & Stuart, ). Causes of decline nest boxes outside the aviaries, with supplementary food included hunting, habitat loss caused by overgrazing, and provided twice per day. This spring release practice con- droughts in the s and s, by which time , indi- tinues today, and the free-flying birds forage in the sur- viduals remained. The northern bald ibis became extinct in rounding area during the breeding season and until they Algeria during the late s or early s (Fellous, ). are recaptured each July. This prevents migration and is Questionnaires circulated by Algeria’s National Agency believed to improve survival rates, although a few birds for Nature Conservation showed that in autumn two (mainly juveniles) have disappeared before recapture, and birds were seen flying at Thiet Ould Moumen, km north of it is possible some of them have migrated south. Unfor- the last known breeding site for this species in Algeria; there tunately, the remaining fully wild population continued have not been any subsequent observations. to decline, and was declared extinct in (Akçakaya ; Yeniyurt et al., ). Eastern subpopulations The semi-wild population has increased despite a num- ber of sudden deaths of chicks and adult birds, notably – Turkey during , in part caused by contamination of supplementary food. By December there were The northern bald ibis was once present through large areas birds, of all ages, in seasonal captivity at Birecik (Table ). of south-eastern Turkey. By the first half of the s there Doğa Derneği (BirdLife Turkey) together with Doğa Koru- were five documented colonies, one with as many as , ma ve Milli Parklar Genel Müdürelüğü have monitored the birds (Akçakaya, ). This population underwent a dra- breeding population since (Yeniyurt et al., ), and are matic decline from the late s, principally resulting working to enhance veterinary conditions in the breeding sta- from the use of DDT to combat insect pests (Hirsch, , tion in Birecik, to increase the size of the semi-wild colony ; Hatipoğlu, ). Following deaths and reproductive and thereby re-establish the migratory population at Birecik. failure, the breeding population was reduced to pairs by From the release and tracking of juvenile birds from (Arihan, ). In Turkey’s General Directorate of the Birecik Breeding Centre confirmed that the Turkish nor- Nature Protection and National Parks (now Doğa Koruma thern bald ibis had not lost the ability to migrate (Hatipoğlu, ve Milli Parklar Genel Müdürlüğü) initiated a project in ). In juveniles moved south, following a similar collaboration with the Society for the Protection of Nature, trajectory to that of the Palmyra birds, and one bird re- Turkey (the former BirdLife Partner), to save the remaining turned to the colony in spring , although the overwinter wild northern bald ibis population in Birecik. A breeding location of this individual was not identified (Lindsell et al.,
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). None of the other released birds have returned. The tagging and satellite-tracking of Syrian birds in con- release programme was suspended in when the Syrian firmed winter migration through Arabia to the Ethiopian civil war started, and satellite tags on three of the released highlands (Lindsell et al., ), c. km from Addis birds stopped transmitting in circumstances suggesting Ababa, where sightings of northern bald ibises had been hunting. Nevertheless, releases remain a high priority con- relatively common in the th century (Welch & Welch, servation action for the eastern flyway of the species. ; Wondafrash, ). Historical data (Welch & Welch, ) and satellite- Syria tracking, in combination with field surveys in , suggest young ibises disperse around the southern Red Sea basin to The northern bald ibis was previously relatively common in the Ethiopian highlands for – years before returning to the Al Badia landscapes of Syria (Serra et al., ). Little is their natal site in Syria, when close to sexual maturity. It is known of the species’ former distribution in Syria, or the unknown to what extent juveniles rely on adults to guide factors driving declines. The birds once migrated through them to optimum feeding sites, as is the case with the Jordan, Saudi Arabia, Yemen, Eritrea and Sudan, with stop- white stork Ciconia ciconia (Bildstein, ; Rotics et al., over sites during the autumn migration between breeding ), or whether the greater foraging time typical of ju- sites in Syria (and Turkey, see above) and the wintering veniles mean they could struggle to find sufficient food ground in the Ethiopian Highlands (Lindsell et al., ; (Brooks, ) and become too weak to migrate long dis- Bowden, ). Hunting along the migration route through tances (as for the white ibis Eudocimus albus; Del Hoyo the western areas of the Arabian Peninsula (Jordan and et al., ). In Arabia, where juveniles tended to winter Saudi Arabia) became unsustainable, and by the early (Lindsell et al., ; Serra, ), threats such as hunting s the Northern Bald Ibis was believed to be extinct and powerlines could be drivers of decline. On the adult in Syria (Aharoni, ; Safriel, ). This left the last wintering grounds in Ethiopia, disturbance and rainfall known colony of eastern northern bald ibis at Birecik, shortages are potential short-term threats, whereas pesticide Turkey, with , breeding pairs in the s (Bowden use and the conversion of pastures to crops could be signifi- et al., ). However, the first well-documented observa- cant in the longer term (Serra et al., ). tion in recent history was in , when an expedition of Following the Palmyra colony’s discovery, the site was the Ornithological Society of the Middle East recorded protected, but migration losses further reduced the tiny northern bald ibises in the Taiz wetlands in Yemen. Birds population (Serra, , ). During – at least were also sighted in western and south-western Arabia one adult failed to return from each migration, and of from (Brooks et al., ; Schulz & Schulz, ), giving juveniles leaving during – only seven returned rise to speculation that there was a hitherto undiscovered (Table ). Evidence suggests high mortality rates as a result colony in the region. of hunting in Syria and Saudi Arabia, in addition to electro- In a breeding colony of birds was discovered cution on power lines (Serra et al., ). Consequently, the in Syria’s Palmyra region (Serra et al., ). Subsequent Syrian population declined from seven birds in to five
TABLE 4 Population structure of the northern bald ibis colony at Palmyra, Syria, –. Data from Serra (, ), Serra et al. (), M. Abdallah, pers. comm. () and M. Wondafrash, pers. comm. ().
New Fledglings Birds that left Birds in wintering Year Adults breeders Subadults Nests Fledglings migrated Palmyra grounds 2002 7 0 3 3 3 10 2003 6 0 3 7 7 13 2004 5 1 2 4 4 10 2005 4 1 2 0 0 5 2006 3 1 3 2 6 6 13 4 2007 3 1 3 2 5 4 11 4 2008 4 2 2 0 0 6 4 2009 3 1 1 2 0 0 5 3 2010 3 1 1 1 1 1 4 2011 3 0 0 1 2 2 5 2 2012 2 0 0 0 2 20131 unknown 3 2014 1 1 2015 0
Reduced monitoring in because of security situation.
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in ; fledged young failed to reach the wintering site in colony recovered sufficiently to require exchanges only Ethiopia, reappearing in only very low numbers in subse- with another nearby sedentary semi-captive colony in quent years (Serra et al., ). Tierpark Rosegg. The latter was set up with birds in Unsustainably high annual mortality (c. %) of young – (Table ). During – a total of chicks birds outside the breeding grounds was the main reason from nine different zoos were donated to the release pro- for juveniles failing to return. Combined with breeding fail- ject Waldrappteam; have died while free flying and ures in and resulting from unknown causes, this returned to captivity because they were injured. Proyecto reduced the colony to one pair and an unpaired female Eremita in Spain received birds during the initial stage by . There was an attempted supplementation using (–), and in total birds from different zoos Turkish birds in , when two tagged juveniles were re- (including Jerez Zoo); had died by . leased, with both successfully migrating to southern Saudi Each year – new colonies are founded in European Arabia and surviving – weeks before dying (Bowden zoos. Besides the European Endangered Species Programme et al., ). In summer , during the Syrian civil war, there are two further studbooks, one in Japan and one in only one pair returned to the site but did not breed. Three North America, with fewer birds ( and , respectively). adults had been observed in – at their wintering There are an estimated additional non-studbook birds grounds in Ethiopia, and one in , but only one of these of unknown parentage in other collections. birds returned to the breeding grounds in ; no free-flying birds were seen by late February (Mahmud Abdallah & Yilma Dellelegn, pers. comm., ). The Syrian population European research and reintroduction projects now appears to be functionally extinct, although since The northern bald ibis was native in Europe until the Middle monitoring at the site has been extremely difficult because Ages (Kumerloeve, ; Pegoraro, ), but had become of security issues (Table ). extirpated by , possibly because of habitat loss, climate change and direct persecution (Schenker, ; Böhm & Pegoraro, ). It is likely the European population was mi- Captive populations gratory, an idea reinforced by Conrad Gessner () in his Vogelbuch description of northern bald ibis distribution, The northern bald ibis has been kept in zoos since the s. behaviour and fledging time. Centuries later, the northern The first few birds were imported from the eastern popula- bald ibis had become a mythical creature until it was re- tion, but none survived for longer than a few weeks, probably discovered by scientists at the end of the th century because of poor husbandry. The first surviving northern bald (Rothschild et al., ). ibises were juveniles imported from Morocco to Basel Zoo Three hundred years after the extinction of the northern in the early s. They became founders of the captive bald ibis in Europe, in the s, European zoos started to northern bald ibis population (Böhm, ), and now all keep the species, with the first captive breeding successes northern bald ibises in European zoos derive from the in the s at Basel Zoo (Mendelssohn, ). From the western population. late s improved husbandry resulted in the , birds Overall there were successful imports up to , and a now held in European zoo colonies (Böhm et al., ). further two during –. Approximately birds were imported in and to Zoo Rheine and Zoo Rabat. All captive birds can be separated into three bloodlines, termed Austria and Germany: developing reintroduction Basel stock, Rheine stock and Rabat stock. All three lines methodologies have been mixed in most collections, and currently most zoos keep descendants of at least two bloodlines (Böhm, In Alpenzoo Innsbruck started hand raising and releas- ). ing northern bald ibis chicks (Thaler et al., ). The The captive population increased over years from Konrad Lorenz Research Station (a core facility of the in to . , birds by , and , registered in the University of Vienna) in Grünau im Almtal established studbook by . This increase is a result of breeding suc- the first European free-flying sedentary (but not self- cess (c. – offspring per year), low mortality and the sustaining) northern bald ibis colony in (Kotrschal, longevity of the species. ). This population has maintained – breeding pairs Since juveniles have been donated from European over the last years (Table ) and was a starting point for Endangered Species Programme sources to three research the experimental northern bald ibis restoration projects in projects. The Konrad Lorenz Research Station, Austria, re- Europe. In hand rearing was stopped, and no summer ceived northern bald ibises from seven locations dur- supplementary food was provided while the birds remained ing – to establish a sedentary semi-captive colony free flying. During – the birds were enclosed in the (Table ), of which subsequently died. Since then, the aviary during the dispersal period (July–September). Since
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TABLE 5 Breeding productivity of the northern bald ibis in the two sedentary, semi-captive colonies Rosegg and Grünau, and the breeding sites in Austria and Germany in the context of the . IPaddress: LIFE+ reintroduction project.
Rosegg (Austria) Grünau (Austria) Burghausen (Germany) Kuchl (Austria)
170.106.33.19 Sedentary, semi-captive Sedentary, semi-captive Migratory, reintroduced Migratory, reintroduced Year Pairs Fledglings1 Fledglings/pair Pairs Fledglings Fledglings/pair Pairs Fledglings Fledglings/pair Pairs Fledglings Fledglings/pair 2001 4 2 0.5 , on 2002 12 7 0.6 23 Sep2021 at12:19:20 2003 5 1 0.2 2004 8 10 1.3 2005 5 7 (3) 2.0 10 12 1.2 2006 4 5 (4) 2.3 9 12 1.3 2007 5 5 (3) 1.6 11 12 1.1 2008 8 20 (0) 2.5 12 13 1.1 , subjectto theCambridgeCore termsofuse,available at 2009 10 11 (13) 2.3 11 15 1.4 2010 12 13 (14) 2.3 15 22 1.5 2011 13 14 (11) 1.9 13 18 1.4 1 3 3.0 2012 12 9 (0) 0.8 10 20 2.0 5 8 1.6 2013 10 8 (0) 0.8 10 25 2.5 7 6 0.9 1 0 0.0 2014 18 26 (16) 2.3 5 6 1.2 6 11 1.8 2 2 1.0 2015 19 15 (32) 2.5 5 7 1.4 4 10 2.5 2 7 3.5 2016 18 16 (32) 2.7 13 18 1.4 3 6 2.0 3 7 2.3 2017 4 10 2.5 5 8 1.6 2018 4 12 3.0 6 14 2.3 Numbers in parentheses are additional fledglings that were taken for hand-rearing by the LIFE+ Programme. otenbl bs7 ibis bald Northern 8 C. Böhm et al.
, there have also been exchanges with another seden- tary semi-captive colony in Tierpark Rosegg. The primary aim of the Konrad Lorenz Research Station project was to investigate social behaviour and its relationships with physiology, ecological aspects of natural foraging, and the establishment of traditions through social learning (e.g. Puehringer-Sturmayr et al., ). It also aimed to improve management and release methodology, to be applicable for wider northern bald ibis reintroduction. Since the Konrad Lorenz Research Station aviary has been left open year-round. The population, which in comprised adult pairs (Table ), has remained sed- Torre de Castilnovo entary despite no longer being enclosed during the disper- sal period (Kotrschal, ). The birds use nearby foraging areas, spending the summer in the neighbouring valley, and returning to the aviary in autumn. The fledglings do not migrate, but up to % of them (in –) undergo juvenile dispersal, flying north/north-east and coming back to Grünau at the end of the summer. From Tierpark Rosegg in Carinthia has also managed a small sedentary, seasonally free-flying northern bald ibis colony, which in 1 comprised adult pairs (Table ). Numbers released and post-release survival during – are presented in Supplementary Tables and .
Austria and Germany: reintroduction of a migratory subpopulation
In the project Waldrappteam initiated a -year feasi- bility study (–) to develop methods for the estab- lishment of migratory northern bald ibis colonies using human-led migration techniques, involving training birds to follow human foster parents in ultra-light aircraft (Fritz et al., ). During –, a total of chicks from European zoos have been taken for hand rearing (Fritz et al., ). Before release, contact with the birds is limited to human foster parents to avoid habituation to other humans. Dur- ing the first weeks, hand rearing takes place at a zoo. Shortly before fledging, the birds are transferred to a field camp in the area where they will be released. Flight training takes months, starting immediately after fledging, with gradually increased flights up to km. The human-led migration starts mid August, when the young birds enter a state of migratory restlessness (Bairlein et al., ). The human-led migration routes cross the Alps to a wintering area in Southern Tuscany (Italy), with daily flight stages of up to km and hours (Fritz et al., ). In , the first juveniles hatched in the wild and fol-
lowed conspecifics from Burghausen to the wintering site Tajo de Barbate Barca de Vejer Sierra del Retin
in Tuscany (Fritz et al., ). Since then, an increasing pro- 6 Breeding productivity of the northern bald ibis in the four breeding sites in Andalusia, Spain. portion migrates independently. Spring migration starts ABLE Nest boxes in open aviary. Year2008 Pairs2009 12010 Fledglings 12011 1 Fledglings/pair2012 12013 Pairs 12014 02015 Fledglings2016 Fledglings/pair2017 1 2018 1 Pairs 0 Fledglings Fledglings/pair Pairs Fledglings Fledglings/pair 4 7 15 22 5 14 2 17 19 21 22 17 14 1.3 26 0.3 25 1.1 29 1.0 1.2 1.4 1.1 4 2.1 1 0.3 2 1 1 1 4 9 1 0 2 12 2.0 1.0 0.0 2.0 1.3 in late March, with the oldest birds departing first. Autumn T
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migration starts at the beginning of August, but birds regu- neighbouring release aviary for several months (October– larly remain north of the Alps up to mid September. In the January), then released to join the free-flying birds. This unusually mild winter of most of the birds delayed mi- technique facilitates the integration of additional birds gration to late December, resulting in significant mortality coming from collaborating zoos that are members of the (Fritz et al., ). In , juveniles followed conspecifics European Endangered Species Programme for the northern to the wintering site, and one group of seven juveniles and bald ibis. two adults reached the wintering area within days. On Annual releases of – birds during – one day the birds covered over km. (Table ) demonstrated the ability of captive bred northern In the feasibility study evolved into a -year rein- bald ibises to survive after release and to establish a wild col- troduction project involving eight partners from Germany, ony in the region of La Janda, Cádiz, south-west Spain. At Austria and Italy, with significant co-financing from the present post-release survival in the first year is c. %, with European Union under the LIFE+ programme. The aim the main causes of mortality being predation by eagle owls was to establish three migratory breeding colonies with a Bubo bubo and electrocution (Supplementary Table ; López total of at least birds (Fritz et al., ). A follow-up pro- & Quevedo, ). The first nesting of released birds was in ject has been proposed, aiming to achieve a viable popula- at Tajo Barbate, a coastal cliff km from the release tion by . site, where breeding occurred annually until .In By the end of , there were free-flying, migrating a new breeding site was established beside a busy road at northern bald ibises ( breeding pairs; Table ), belonging Barca de Vejer, km from the release site, and this has be- to two established breeding colonies at Burghausen, south- come the main colony (López & Quevedo, ). In a ern Germany, and Kuchl, Austria, with a third breeding new breeding site was established in Castilnovo, a coastal colony establishing from in Ueberlingen at Lake tower, km from the release site. By there were two Constance, southern Germany. A major challenge for the active breeding sites (Table ) within km of the release project are losses caused by illegal hunting during the au- site, with a total of birds in the wild, including breed- tumn migration (Fritz, ). During the feasibility study ing pairs (Supplementary Table ). The four breeding sites (–)upto% of the annual losses were attributable were naturally colonized by northern bald ibises; no boxes to illegal hunting in Italy (Fritz, ; Fritz et al., ). Since or ledges were provided. All birds are individually marked, , illegal hunting accounts for % of the annual losses, and some carry transmitters. From the hand-reared groups, with electrocution at medium voltage power poles caus- some juvenile dispersal, mainly southwards, has been re- ing % of the mortality (Supplementary Table ). Criminal corded, in contrast with the wild-hatched juveniles that and civil cases brought against an Italian northern bald have remained in the area with their parents and the rest ibis hunter raised awareness of the issues in Europe (Fritz of the group. In July the Environment Ministry of et al., , ). Since a total of juveniles fledged Spain formally approved the work as a northern bald ibis in the wild at the two breeding sites (Table ), a mean of reintroduction project. The project has two phases: () the . per nest. consolidation of the existing colonies, and () applying the Details of annual releases of – birds are presented in techniques refined by Proyecto Eremita to establish a second Supplementary Table . Overall annual post-release survival population of northern bald ibises in Cabo de Gata Natural in the first year is c. %. All released birds are individually Park, km away, also in Andalusia. To date, Proyecto marked and tracked (Fritz et al., ). Eremita has succeeded in establishing a sedentary popula- tion without supplementary feeding or other intensive in- terventions. The population is not yet self-sustaining, so Spain: reintroduction of a sedentary population supplementation with additional birds is continuing, improv- ing genetic variability and aiming for a minimum of birds In a joint project between Zoobotánico Jerez and the and breeding pairs by . Andalusian government established Proyecto Eremita, to develop techniques for the release of captive-bred northern bald ibises (López & Quevedo, ), with the aim to estab- Conservation progress lish a sedentary, free-flying colony in southern Spain. The release area in south-western Cádiz province has coastal Management of the remaining population in coastal and inland cliffs, and extensive foraging areas, allowing Morocco has generated the first sustained increase in the the birds to feed all year round. Birds are hand-reared by natural wild population in historical times. Although the human foster parents wearing black shirts and ibis-shaped northern bald ibis was categorized as Critically Endangered cycle-helmets (Quevedo et al., ; Quevedo, ). Once a in the IUCN Red List up to , the positive trend in free-flying hand-reared group of ibises was established in Morocco since justified recategorization from Critically the area, groups of parent-reared juveniles were kept in a Endangered to Endangered (BirdLife, ). Management by
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the Moroccan National Parks authority has been key to this small western population in Morocco, and in developing success, along with regulation of development pressures and the methodology and prospects for establishing a sedentary increasing tourism. Maintaining the traditional agricultural population in southern Spain and possibly also a migratory areas and preventing disturbance around the breeding sites population in central Europe. will be ongoing challenges to support this largely resident northern bald ibis population. Future perspectives By the last wild migratory breeding northern bald ibis pair had disappeared from the Middle East, although There is a need to evaluate the suitability of potential and they survive in semi-wild conditions and retain the ability former breeding sites and associated feeding areas for to migrate, and thus could serve as a source of founders both the western (Morocco, Algeria) and eastern (Syria, for the re-establishment of a migratory eastern population. Turkey, Yemen, Iraq) populations. This is especially needed The lessons learned from the European reintroduction pro- in Morocco where the in situ population increase means jects provide cause for optimism that sedentary populations there is potential for natural recolonization beyond the cur- (Spain) and even migratory populations (Austria) can be re- rently occupied sites. In addition, there is evidence that birds established, and could inform the reintroduction of species from the Spanish project can cross to Morocco, with sight- with similarly migratory and sedentary phenotypes. ings of lone birds in both and , and multiple In the International Advisory Group for the observations in and (Muñoz & Ramírez, ; Northern Bald Ibis was founded. Its principal aims are to Bowden et al., ). facilitate good communication and information exchange Every year some birds at the Birecik Breeding Station, amongst all parties working with the northern bald ibis. Turkey, disappear before enclosure; they may not be dead The group distributes new and accumulated knowledge but, rather, migrating south. Release trials of satellite- about the species by organizing periodic meetings, publish- tracked birds have shown promising results for potential re- ing newsletters and the meeting proceedings, and maintain- establishment of a fully wild Turkish population, although ing its own website with a download section for reports. The because birds inevitably pass through Syria where civil con- group’s activities have been recognized by the Agreement flict means personal firearms are ubiquitous, this may be- on the Conservation of African-Eurasian Migratory Water- come viable only after the region has stabilized politically. birds (AEWA) that initiated and sponsored the first Species The captive population of western origin is managed Action Plan for the northern bald ibis in . A revision of through studbooks and continues to increase slowly, al- this action plan was produced from the st Meeting of the though individual captive colonies need careful breeding man- AEWA Northern Bald Ibis International Working Group agement as some bloodlines are already over-represented in in Saudi Arabia, and finalized in (Bowden, and aviary space is becoming limited. However, the age struc- ). It states that because of significant progress in meth- ture and sex ratio indicate that the captive population is still odology over the past decade, conservation translocation viable and . % of the birds are of optimal breeding age. has become a viable approach to improve the status of the This means sufficient genetically appropriate birds can be species in the wild (Bowden, ). The two European re- made available for reintroduction projects, but cooperation lease projects (LIFE+ project and Proyecto Eremita) have between holders is essential to control inbreeding and main- so far developed largely independently of the AEWA pro- tain genetic variability. cess, but have demonstrated the potential to develop re- Finally, our understanding of methodology for the re- introduction projects within the more recent former range introduction of this species, for both sedentary and migra- in Algeria, Turkey and Syria. The first steps for this were tory populations, has advanced significantly since . The outlined in the updated implementation plan for Algeria positive trend for the remaining wild Moroccan popula- (AEWA, ). The AEWA Northern Bald Ibis Working tion is a result of the measures taken by the Moroccan gov- Group is composed of one nominated senior government ernment together with partner NGOs. The recent signs of representative plus a national expert from each of the recolonization of former areas, if maintained, will be an range states, with a regional coordinator for the eastern important consolidation and a positive step in the recovery and western populations, and an overall coordinator. Ex- of the species. Meanwhile, pressures on current feeding and perts, usually from the International Advisory Group for breeding habitats are increasing. Interventions such as war- the Northern Bald Ibis, are invited to periodic meetings in dening, water provisioning and law enforcement to pre- line with the main issues on the agenda for the implemen- vent illegal construction activities thus remain a top priority tation of the action plan. The Moroccan government hosted and may need further reinforcement. Availability of viable the most recent meeting in November , at which -year management options such as reintroduction offers signifi- implementation plans were developed and agreed for each cant opportunities for the species and provides hope that country (AEWA, ). Significant progress has thus been the re-establishment of further self-sustaining populations made both in maintaining and steadily increasing the is possible.
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Acknowledgements We thank the numerous funders and suppor- BÖHM,C.() European Endangered Species Program: nd Northern ters of the enormous body of work this paper encompasses although Bald Ibis Studbook. Alpenzoo Innsbruck-Tirol, Innsbruck, Austria. these are too many to mention individually. Two anonymous referees BÖHM,C.() European Endangered Species Program: rd Northern helped develop earlier drafts of this paper, and Amina Fellous com- Bald Ibis Studbook. Alpenzoo Innsbruck-Tirol, Innsbruck, Austria. mented on the Algeria text. We are unable to mention all the field BÖHM,C.&BOWDEN, C.G.R. () Northern Bald Ibis Conservation workers that have contributed to gathering the information presented, and Reintroduction Workshop. Proceedings of rd Meeting of the but due to the harsh conditions and the difficulties on the ground, we International Advisory Group for Northern Bald Ibis (IAGNBI), would particularly like to acknowledge the full team of wardens in November , Palmyra, Syria. Morocco who have dedicated their lives to protecting and monitoring BÖHM,C.&BOWDEN, C.G.R. () Northern Bald Ibis Conservation the birds. The team continues to do this, often in very tough field and Translocation Workshop. Report of th Meeting of the conditions, and Mohammed El Gadrouri and Abdallah Essamar de- International Advisory Group for the Northern Bald Ibis (IAGNBI), serve special mention having both been fully involved for 25 years. August , Seekirchen, Austria. Likewise, in Syria, the wardens and rangers there have served often BÖHM,C.&PEGORARO,K.() Der Waldrapp Geronticus eremita: through extraordinarily difficult times, well beyond the call of duty, Ein Glatzkopf in Turbulenzen. Neue Brehm Bücherei, Bd. . and although many more have been involved, we would like to pay VerlagsKG Wolf, Magdeburg, Germany. special tribute to Mahmud S. Abdullah and Ahmed Khaber Abdallah. BÖHM, C., SCHAD, K., FIENIEG,E.&VOORHAM,M.() Long-term Management Plan for the Northern Bald Ibis (Geronticus eremita) Author contributions Lead on compiling the information and writ- European Endangered Species Programme (EEP). Alpenzoo ing: CB, CGRB, PJS; contribution of updated information from the re- Innsbruck-Tirol, Innsbruck, Austria, and EAZA Executive Office, spective range states and projects, and revisions: TH, WO, MEB, MAQ, Amsterdam, The Netherlands. JF, CY, JML, JFO, DF, MU; overall coordination: CGRB. BOWDEN, C.G.R. () Last chance for the northern bald ibis. World Birdwatch, , –. Conflicts of interest None. BOWDEN, C.G.R. (ed.) () International Single Species Action Plan for the Conservation of the Northern Bald Ibis (Geronticus eremita). Ethical standards This work abided by the Oryx guidelines on eth- AEWA Technical Series, , Bonn, Germany. ical standards. BOWDEN, C.G.R., AGHNAJ, A., SMITH, K.W. & RIBI,M.() The status and recent breeding performance of the Critically Endangered northern bald ibis Geronticus eremita population on the Atlantic References coast of Morocco. Ibis, , –. BOWDEN, C.G.R., HAMOUD, A., JBOUR, S., FRITZ, J., PESKE, L., AEWA (AGREEMENT ON THE CONSERVATION OF AFRICAN- RIEDLER, B. et al. () Attempted supplementation of the relict EURASIAN MIGRATORY WATERBIRDS)() Report of the nd wild eastern population of northern bald ibis in Syria with Turkish Meeting of the AEWA Northern Bald Ibis International Working semi-wild juveniles. IUCN Reintroduction Specialists Group Case Group, – September , Agadir, Morocco. AEWA, Bonn, Studies, Part III, –. Germany. 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