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Home , African spoonbill, Australian white ibis, Cattle egret, Heron, Ibis, Marsh tern

The Sacred in : ecology and management Pierre Yésou, Philippe Clergeau, Suzanne Bastian, Sébastien Reeber and Jean-François Maillard

Abstract The Sacred Ibis aethiopicus is common and widespread in its native range. The ’ adaptability means that it thrives in landscapes modified by human activity. In recent decades, non-native populations have become established in several areas of Europe as a result of escapes or deliberate releases from collections. Such populations have the potential to become established and increase quickly, and thus to have a significant impact on native species. This paper summarises the current situation in Europe, with particular reference to . The largest non-native populations in Europe became established in France between about 1990 and 2005, prompting a costly eradication programme, the progress and results of which are described.

The Sacred Ibis in its native range The Sacred Ibis is a social breeder, in The Sacred Ibis Threskiornis aethiopicus is colonies from a few tens up to c. 2,000 pairs. common and widespread throughout much Nests are built on a variety of supports, of sub-Saharan , and a small, isolated mostly in trees and bushes but sometimes on and decreasing population persists in the ground or among rocks (Urban 1974; southern Iraq (Bonn 2005). The world popu- Brown et al. 1982; Hancock et al. 1992). lation, estimated at some 200,000–450,000 Around Cape Town, breed in reedbeds, individuals, is thought to be stable or on the ground, in trees and bushes and even declining ( International wpe. on artificial breeding platforms. In all cases, wetlands.org; BirdLife www.birdlife.org), and breeding sites are completely surrounded by it is treated as a species of Least Concern water or on an offshore island, and the under IUCN criteria (iucnredlist.org). species will breed almost anywhere provided In , where most studies have that the ‘island’ criterion is met (Doug Hare- been carried out, the Sacred Ibis bred only on bottle in litt.). coastal islets near Cape Town at the begin- Ibises are similarly social when feeding, ning of the twentieth century, moving to mostly foraging in groups, often with other inland marshes in winter. Subsequently, it long-legged species such as Yellow-billed benefited from irrigation, agriculture intensi- ibis, African fication, and conservation measures, and Platalea alba and Little garzetta progressively established colonies as far (Hancock et al. 1992). In Africa as a whole, inland as Zimbabwe (Harrison et al. 1997; the main foraging habitats are farmland, wet- Kopij 1999). Although it is nominally resi- lands, and rubbish dumps (Brown et al. dent, over 50% of ring-recoveries are more 1982), while in South Africa over 80% of than 100 km from the ringing site (Hockey et records are from grassland habitats, the al. 2005), while post-breeding movements of remainder mainly from freshwater wetlands up to 1,000 km occur, and some consider the and estuaries (Harrison et al. 1997). The Sacred Ibis to be more accurately described species will also use a wide variety of man- as nomadic (Clark & Clark 1979; Harrison et modified and artificial habitats (Clark & al. 1997; Underhill et al. 1999). Clark 1979).

© British 110 • April 2017 • 197–212 197 Yésou et al. Sébastien Reeber 94. Sacred Ibises Threskiornis aethiopicus, Lac de Grand-Lieu, France, May 2011.

The Sacred Ibis feeds mainly on locusts, reports from Egypt (Egyptian Ornithological , and aquatic beetles; it will also Rarities Committee http://chn-france.org/ take a variety of other aquatic and terrestrial eorc), and none has reached Morocco , in addition to , , although it is common in Mauritania , birds and small . Carrion, (Thévenot et al. 2003; Moroccan Rarities vegetable and refuse, offal and seeds Committee www.go-south.org). Conse- are also taken. In addition, breeding birds can quently, any Sacred Ibis recorded in the wild raid neighbouring nests for and chicks, in Europe can be regarded as a former and some individuals specialise in raiding the captive, released either deliberately or acci- nests of other birds, sometimes pulling adult dentally. Such escapes remained a rare sight birds out of their nest to take the eggs or until it became more common for zoological young. Victims include , , collections to house free-flying groups of and , gulls and ibises (Clergeau & Yésou 2006; Fàbregas et al. on offshore islands, and two Endangered 2010). In recent decades, the number of species (African Spheniscus demersus escapes has led to the establishment of signif- and Cape Phalacrocorax icant non-native populations in some areas. capensis), and they will even take eggs of the Non-native species that become estab- Crocodylus niloticus (Clark lished in the wild may have a negative impact 1979; Brown et al. 1982; Harrison et al. 1997; on native species, potentially with a signifi- Hockey et al. 2005; Williams & Ward 2006). cant loss of biodiversity as well as economic impacts, and are termed ‘’ The Sacred Ibis as a non-native (e.g. Mooney & Cleland 2001, Vilà et al. 2010, The Sacred Ibis is absent from the paleonto- Martin-Albarracin et al. 2015). Accordingly, logical and archeo-zoological record in the European Parliament and the Council of Europe (Mourer-Chauviré 1993), and there is the European Union adopted a regulation to no evidence for natural vagrancy out of ‘prevent, minimise and mitigate the adverse Africa. In the early nineteenth century the impact on biodiversity of the introduction species still bred in Egypt, in the Nile Valley, and spread within the Union of invasive alien but disappeared within a few decades (del species’ (European Commission 2014). This Hoyo et al. 1992). There are no modern-day required the Commission to adopt a list of

198 British Birds 110 • April 2017 • 197–212 The Sacred Ibis in Europe: ecology and management invasive alien species of Union concern, Introductions in Europe and which came into effect in August 2016 (Euro- elsewhere pean Commission 2016). The list contains 37 Free-flying Sacred Ibises have been reported species, including three species: House from several European countries. Breeding Crow Corvus splendens, Ruddy Oxyura has occurred in the wild in France, , jamaicensis and Sacred Ibis. In addition, a , , the Netherlands and possibly pan-European research programme has iden- other nations. A number of free-ranging tified the Sacred Ibis among the invasive colonies have become established; the situa- species of main European concern (DAISIE tion in France is treated in more detail below, 2009 www.europe-aliens.org). These three but a brief summary of breeding status in species are now the subject of control and other European countries is given first. eradication programmes throughout the EU. The House Crow has established popula- Spain and Canary Islands tions in over 20 countries outside its native Sacred Ibises that escaped from Barcelona range and often rapidly attained pest status, settled in a nearby public park, where for example through of native breeding first occurred in 1974. This con- species and as a carrier of human and animal tinued throughout the 1980s and 1990s, after disease (GISD 2017). The threat posed by the which the colony was controlled, and Ruddy Duck to the conservation of the breeding was last recorded in 2001. The endangered native White-headed Duck O. breeding birds also visited nearby leucocephala in southern Europe and the con- areas including the Llobregat and Ebro deltas sequent eradication programme in the UK (Jordi Clavell in litt.). In the Canary Islands, are well known (e.g. Henderson 2009, where the species was first recorded in 1989, Holling et al. 2017). The remainder of this free-ranging ibises have nested regularly on paper considers the potential problems of Fuerteventura since at least 1997, with 2–5 established non-native Sacred Ibis popula- pairs nesting in the early 2000s (Yésou & tions. Focusing on the situation in France, Clergeau 2005) and unknown numbers since where the largest introduced population in then. the world has spread, we highlight the diffi- culties encountered in setting up an eradica- Portugal tion programme to deal with such a large and Three Sacred Ibises escaped from a zoo near widespread population. When not otherwise Coimbra in 1998; a pair nested nearby and stated, the information presented here reared three young that , after which they has been collected by the authors and their disappeared. Since 2009 the species has been institutions. observed almost year-round in the Algarve Jérôme Cabelguen 95. Sacred Ibises Threskiornis aethiopicus, Banc du Bilho, Loire estuary, France, April 2005.

British Birds 110 • April 2017 • 197–212 199 Yésou et al.

with up to six birds together, but breeding The Netherlands has so far not been recorded (de Juana & Free-flying Sacred Ibises that escaped from a Garcia 2015; Gonçalo Elias in litt.). zoological park in Zuid-Holland attempted to breed in 2001, and successful breeding Italy occurred in 2002. Numbers increased to ten Breeding in the upper Po Valley, Piedmont, breeding pairs in 2003 and 15 pairs in 2007. began in 1989, and 26 pairs nested there in Eradication measures began in 2008 and only 2000, when approximately 100 individuals 4–5 pairs remained in 2009. A few birds are were present. In 2003 breeding occurred at a still at large, possibly new escapees or birds second site in the same area, with possibly arriving from Germany (Smits et al. 2010; 25–30 pairs, and a few more pairs were found Robert et al. 2013; www.cr-birding.org). at a third colony in 2004 (Yésou & Clergeau Sporadic reports of breeding birds continue, 2005). More recent information, from the most recently a single pair at De Wieden NP 2001–10 winter waterbird counts (Zenatello in 2016 (Ronald Messemaker pers. comm.). et al. 2014), which may not have monitored the whole population, revealed increased dis- Other European countries persal away from Piedmont, which led to Other free-flying colonies are known in breeding attempts in Venetia and Tuscany. Belgium (Antwerpen Zoological Garden; The highest national winter count up to 2010 Gunter de Smet in litt.) and Germany (a was 70 in 2008, but numbers have increased colony at Walsrode bird park in the 1980s since (Nicola Baccetti in litt.). In 2015 there had disappeared by the end of the 1990s, were at least 140 nests in ten colonies, with while another colony, at Munich Zoo, was the a much greater non-breeding population: likely source for birds seen in Switzerland; hundreds of ibises came in to roost at some Andreas Buchheim and Nicola Baccetti in colonies (Mauro Fasola in litt.). In late 2016, litt.). Also in Germany, 12 young Sacred a census coordinated by GPSO, the Piemon- Ibises escaped from a bird sanctuary in the tese ornithological group, found 4,068 indi- Munster area, where they were hand-raised viduals in 13 roosts in northwest Italy. The by a researcher from the Konrad-Lorenz Italian population, which remained low for Institute for Ethology; part of that group about 20 , is now suddenly booming seemingly reached the Netherlands (Smits (Gianfranco Alessandria in litt.). As yet there et al. 2010, www.michelklemann.nl/ibis/mail/ is no coordinated control programme for the ebn20001125.html). In the UK, several free- population in Italy. flying Sacred Ibises dispersed from a zoo near Jérôme Cabelguen 96. Part of the Sacred Ibis Threskiornis aethiopicus colony at Banc du Bilho, Loire estuary, April 2005.

200 British Birds 110 • April 2017 • 197–212 The Sacred Ibis in Europe: ecology and management

Dalton-in-Furness, Cumbria, and moved to the nearby coast (Ian Carter in litt.).

Releases and escapes outside Europe Since 1989 a small introduced popula- tion has persisted on Branféré Zoo Sir Bani Yas Island in the United Arab Emirates (Yésou & Clergeau 2005). A Golfe du Morbihan dozen birds that escaped from a zoo- Banc du Bilho logical garden in Lac de Grand-Lieu in the early 1990s rapidly estab- lished a thriving population, with hun- dreds of birds living in the wild by 2002 Girond estuary (Agoramoorthy & Colonies Hsu 2007; Adam Welz, large (>100 pairs) Wayne Hsu and Lucia small Liu Severinghaus in area of dispersal litt.). In the USA, five main coastal wetlands Sacred Ibises escaped from Miami Zoo, origin of escapes , in 1992 when Hurricane Andrew 0 50 100km destroyed their enclo- sure. Initially they bred in the area and Fig. 1. The location of Sacred Ibis Threskiornis aethiopicus breeding numbers grew unno- colonies in western France. ticed until they began breeding in the Everglades. Local govern- this period a breeding colony became estab- ment, and state and federal administrations lished and while the introduced adults had joined forces to eradicate the species, and their wings clipped, their offspring were left now all Sacred Ibises living in the wild in free to . At the owners’ wish, the site southern Florida, approximately 75 birds, became a zoological garden when they passed have been removed (Herring & Gawlik 2008; away. By 1990 there were 150 pairs of Sacred Johnson & McGarrity 2009). Ibises nesting in the zoo and visiting nearby wetlands, but some moved several hundred The Sacred Ibis in France kilometres along the Atlantic coast. Breeding In the 1970s, the owners of Branféré Manor, in the wild and away from Branféré Manor in southern Brittany, imported various bird was first noted at Lac de Grand-Lieu in 1993, species, including 20 Sacred Ibises that came c. 70 km from Branféré, and at Golfe du from Kenya in four deliveries between 1975 Morbihan in 1994, c. 25 km from Branféré and 1980. These were later supplemented by Manor (Marion & Marion 1994; Frémont ten birds from a French zoo in 1987. During 1995; Yésou 2005).

British Birds 110 • April 2017 • 197–212 201 Yésou et al.

No young raised at Branféré Manor have a safari park at Sigean, in 1982 (fig. 3). From been left to fly free since 1997, but sufficient 1989 onwards they were able to roam freely birds were already breeding elsewhere to within the park and breeding took place in establish a thriving population from 1991. Sightings outside the zoo became southern Brittany to the Arcachon Bay, south regular from 1995 and a colony of eight nests of Bordeaux (fig. 1, and documented in detail was found at the nearby Lac de Bages in by, for example, Yésou & Clergeau 2005, 2000, which increased to 75 pairs in 2004 and Philippon & Yésou 2012, Yésou & Reeber 105 pairs in 2005. The total population, 2014). Winter roost counts revealed c. 2,500 including immatures and non-breeders, was birds in 2003/04, and c. 3,000 in 2004/05. estimated at 370 individuals in 2007. These Breeding numbers increased steadily, birds dispersed along the Mediterranean reaching c. 1,700 pairs in 2006 (fig. 2), and coast, eventually reaching the Camargue, between 1,430 and 1,860 pairs in 2007, the where the first breeding attempt was uncertainty being linked to the initiation recorded in 2000 (Kayser et al. 2005; Yésou & of control measures. The eradication Clergeau 2005; Mouronval 2013). Ibises seen programme brought the French Atlantic in Cataluña, Spain, in the early 2000s were breeding population down to 150–160 pairs thought to come from this population (de in both 2015 and 2016, and January counts of Juana & Garcia 2015). Control measures in c. 500 in 2016 and 300–350 in 2017 (Maillard the late 2000s saw the Mediterranean popula- & Yésou 2016; Aurélie Barbotin in litt.). tion almost completely extirpated, with only Outside the breeding season the ibises two birds remaining in the wild by 2015, in range widely along the Atlantic coast, some the Camargue (Maillard & Yésou 2016). south to the foot of Pyrenees, others reaching Contrary to reports, 38 birds that escaped the English Channel coast in northern from a zoo at Saint-Jean-Cap-Ferrat in 2007 Brittany and Normandy, and a few birds were rapidly recaptured and did not supple- moving inland. A ringed bird reached the ment the Mediterranean population (Jean- Belgian border in 1999 (Clergeau et al. 2005), Marc Cugnasse in litt.). another was in the Netherlands in 2012 (Ralf Smits in litt.), and one was seen with a group Breeding biology of ten birds in Doñana National Park, Spain, Breeding colonies were established at both in the 2008 breeding season (Carlos brackish and freshwater wetlands on the Gutiérrez Expósito in litt.). Mediterranean coast, while in western France On the Mediterranean coast, eight Sacred they were found in freshwater wetlands, Ibises were imported from a zoo in the UK to various coastal sites and in private parks.

5000

4000 wintering birds (individuals) breeding pairs 3000

2000

1000

0 1980 1982 1984 1986 1988 1990 1992 1994 1996 1998 2000 2002 2004 2006 Fig. 2. Population growth of the Sacred Ibis Threskiornis aethiopicus in western France from 1980 to 2006, showing breeding pairs in blue and numbers in winter (individuals) in red. Numbers reached c. 5,000 in winter 2005/06 and c. 1,700 breeding pairs in 2006. Fitted lines are exponential curves.

202 British Birds 110 • April 2017 • 197–212 The Sacred Ibis in Europe: ecology and management

breeding colonies area of dispersal main coastal wetlands

origin of escapes

Saint-Jean- Cap-Ferrat Zoo Lac de Bages Camargue

Sigean Zoo

Mediterranean Sea 0 25 50 75 100km

Fig. 3. The location of Sacred Ibis Threskiornis aethiopicus breeding colonies on the Mediterranean coast of France.

Most colonies were surrounded by water, but material was available, nests were simple in two regularly occupied parks the lawn sur- scrapes on the ground, mostly lined with rounding isolated stands of trees seemingly grass. Additional material, sometimes provided a sufficient ‘island’. Another colony including greenery, is often added during was established in a mixed heronry in a small incubation, increasing the nest diameter. At wood. Nests are most often built in trees: this stage neighbouring nests may come into willow Salix and alder Alnus in marshes, contact, forming what could be described as mostly cypress Cupressus, tamarisk Tamarix a ‘community platform’. On the ground, one and Maritime Pine Pinus pinaster, but also such platform held 246 nests on c. 120 m2 oak Quercus and chestnut Castanea, when (Yésou et al. 2006). colonies are located on dry ground. Breeding Apart from Wild Boars Sus scrofa has been noted occasionally in wet reedbeds, destroying clutches in reedbeds, which may and also on the ground, as in the case of one explain the scarcity of breeding attempts in of the most impressive aggregations of nests, this habitat, the Sacred Ibis has no obvious 735 pairs on a small (c. 0.2 ha) artificial natural predators in France. This surely con- island with little vegetation. tributed to the species’ breeding success The nesting season extends from early before the control programme began with, March to August; most clutches are laid in on average, one young or more fledged per April–May with later ones being replacement breeding attempt (at least 1.3 young per pair clutches. No marked synchrony is observed for 818 pairs in 2005, 1.0–1.2 young per pair across large colonies, but there is often a high for 1,100–1,200 pairs in 2006). Sightings of degree of synchrony among groups of (typi- ringed birds suggest that, following a failed cally) 8–15 pairs that build nests very close attempt, Sacred Ibises often move to another together (just a few tens of centimetres site to lay a replacement clutch, either within apart), as a colony subgroup. The nests, typi- the same large wetland or up to tens of kilo- cally around 30 cm in diameter, are usually metres away. made of dry plant material, such as pieces of Sacred Ibises nesting in trees often, reed, twigs or driftwood, collected close to though not always, share colonies with the site. On one island where little dry herons and similarly large, colonial species

British Birds 110 • April 2017 • 197–212 203 Yésou et al. Jérôme Cabelguen 97. A cluster of Sacred Ibis Threskiornis aethiopicus nests forming a ‘community platform’, Banc du Bilho, Loire estuary, France, April 2005.

and also breed in close proximity to large that both species preferentially settled at gulls on small islands. It has been claimed places previously occupied by their own that Eurasian Spoonbills Platalea leu- species. The results thus offered little evi- corodia were attracted by breeding Sacred dence that ibises play a role in the conser- Ibises and that the (then) locally rare vation of Spoonbills. Spoonbill population in France would benefit from the presence of ibises Diet and feeding ecology (Marion 2006). To test this, the locations In France, as in its native range, the Sacred of all nests of both species were plotted Ibis is an opportunistic feeder. Invertebrates and their period of laying recorded over generally form the majority of its varied diet, five breeding seasons at Grand-Lieu but individuals may specialise on other food (Clergeau et al. 2010a). This showed that types, at least temporarily (Clergeau et al. Spoonbills began to breed significantly 2010b). Table 1 shows the main foraging earlier than ibises (by 15–25 days), and habitats in western France. The increasing importance of freshwater marshes may reflect the spread of the invasive Red Swamp Table 1. Main foraging habitats used by Crayfish Procambarus clarkii, which is an the Sacred Ibis Threskiornis aethiopicus in western France, 2000–04 (n=98; Clergeau important item in the bird’s diet. A large et al. 2010b), and 2007–09 (n=60; ONCFS rubbish dump close to one of the main unpubl. data). colonies was regularly attracting huge numbers of ibises, up to 700 simultaneously, foraging habitats 2000–04 2007–09 until it closed in 2007. Smaller dumps agricultural landscape 28.6 % 2.4% continued to attract birds until 2010 at least, wet meadows 18.4% 4.0% in groups of up to 150 individuals. tidal habitats 22.4% 11.3% Away from these core habitats, ibises have saltpans 12.2% 19.6% also been observed feeding in a variety of rubbish dumps 9.2% 31.7% ‘human’ habitats such as slurry pits, poultry freshwater marshes 9.2% 31.0% farms and water treatment ponds, not to mention the collections and parks

204 British Birds 110 • April 2017 • 197–212 The Sacred Ibis in Europe: ecology and management

they originated from (in western France of the Red Swamp Crayfish was responsible Branféré Zoo deliberately fed ibises up to for a sharp increase in the Sacred Ibis popu- 2002). lation in western France. Yet this is not Sacred Ibises can feed alone but most supported by the available evidence, with a often forage in small groups, up to a few tens steady rate of ibis population growth main- of individuals. Less commonly, up to 200 can tained beyond the initial crayfish boom in be seen foraging together in the same wet the late 1990s (fig. 2). Marion also claimed meadow or marsh. Typically, they feed in that predation by Sacred Ibises on crayfish single-species groups but will also mix with helps to limit the latter’s spread, but again other species, most often , Herring this appears unfounded. Many other species Larus argentatus and Black-headed Gulls feed on the crayfish, and it seems that cray- Chroicocephalus ridibundus and, in farmland, fish dynamics are mostly controlled by the Egret ibis and Eurasian survival of young individuals, at a stage Curlew Numenius arquata. where they are too small to attract avian Analysis of stomach contents and regurgi- predators. tates of birds in France by Clergeau et al. Predation by Sacred Ibises of the nests (2010b) has shown that the most frequently and/or chicks of a variety of bird species has occurring food items are , particularly been observed in France, including Mallard dipterans and their larvae (e.g. mosquitoes, platyrhynchos, Garganey A. querqued - midges, gnats), beetles, crayfish, refuse waste ula, Shag Phalacrocorax aristotelis, Cattle and (e.g. meat, bread, vegetables), and plant Little , Night nycticorax matter including crops such as maize. Other and Squacco Herons Ardeola ralloides, Black- food items include , molluscs (gas- winged Stilt Himantopus himantopus, tropods and bivalves, particularly mussels), Northern Lapwing Vanellus vanellus, (), isopods, , Common Redshank Tringa totanus, Black shrimps, fish, amphibians (in particular Chlidonias niger, Sandwich sandvi- Bufo bufo and probably censis and Common Terns S. hirundo, and newts), small mammals and birds. Dry Black-headed and Herring Gulls. Predation is animal food was found in the stomach con- sometimes opportunistic, but there are docu- tents of ibises that continued to feed within mented instances of Sacred Ibises deliberately the wildlife park they originated from. and systematically searching for eggs or Marion (2013) suggested that the spread chicks. Jérôme Cabelguen Jérôme Cabelguen 98 & 99. Sacred Ibis Threskiornis aethiopicus nests, containing newly hatched and small chicks, Banc du Bilho, Loire estuary, France, April 2005.

British Birds 110 • April 2017 • 197–212 205 Yésou et al. Georges Georges Olioso 100. Sacred Ibises Threskiornis aethiopicus picking through the bins of a burger restaurant in Sigean, southern France, in May 2005, demonstrating their catholic diet and ability to live alongside humans. Threats to biodiversity An eradication programme for the Sacred Ibises have caused widespread destruc- Sacred Ibis in France tion at some Sandwich and Black In 1993, the manager of Branféré Zoo colonies; predation within heronries, and of alerted the Ministry of the Environment to nests has also been reported, and local the proliferation of free-flying Sacred Ibises declines in breeding populations of these released by the previous owners, but species became apparent in some areas where received no response. (Conservation biolo- Sacred Ibises occurred (Kayser et al. 2005; gists also recognised the potential threats Vaslin 2005; Clergeau et al. 2010b; unpubl. posed and also informed the Ministry, in data). This was an early warning sign of the both 1994 and 1996, again without potential wider impact of the ibises on native response.) Meanwhile, Branféré Zoo insti- species. In addition to direct predation, gated their own recapture and pinioning groups of foraging ibises wading through programme in 1994, and by the end of 1996 marsh tern colonies have unintentionally but all the free-flying ibises in the zoo had been repeatedly destroyed nests. Besides caught. At that stage, however, many birds, there are potential impacts on other remained at large elsewhere. wildlife groups, especially amphibians. Eventually, in April 2004, a regional Farmers, particularly those rearing cattle meeting gathered NGOs and public bodies and , expressed concern that growing involved in the management of protected numbers of Sacred Ibises might be significant areas, at which participants agreed that the carriers of disease. It is known that livestock developing Sacred Ibis population might be pathogens are carried by the related Aus- of conservation concern. In December tralian White Ibis T. molucca (Epstein et al. 2004 the Ministry of the Environment 2007) and that avian tuberculosis has been requested INRA and ONCFS, two French detected in captive Sacred Ibises (Dvorska et public bodies in charge of rural and al. 2007). Sacred Ibises regularly feed at wildlife management, to produce a risk rubbish dumps and can also commute to assessment with proposals for manage- farmland, which may exacerbate the ment. This report discussed the pros and problem. Studies have shown that the risk of cons of four management scenarios, the Sacred Ibis to farm is only mod- ranging from taking no action to organ- erate, except in cases where specific outbreaks ising the species’ eradication at a national of an avian disease are causing concern scale (Clergeau et al. 2005). In November (Bastian et al. 2010a,b), although Vorimore et 2005, the avifauna commission of CNPN, al. (2013) described a pathogen new to the national advisory body, unanimously science from non-native Sacred Ibises. recommended the eradication of the

206 British Birds 110 • April 2017 • 197–212 The Sacred Ibis in Europe: ecology and management

Sacred Ibis throughout France. Results of the eradication It was initially proposed that the eradica- programme tion programme should be undertaken by In 2006, when the eradication programme hunters, but this was unacceptable to LPO was (temporarily) postponed, LPO arranged (the BirdLife partner in France) and other for Sacred Ibis eggs to be collected from what conservation organisations, who feared that was then the main colony, at Banc du Bilho, any large white bird, including egrets and an island in the Loire estuary (fig. 1). A total Spoonbills, would also be shot. The eradica- of 1,223 eggs were collected from 663 nests. tion programme was temporarily postponed However, replacement clutches were laid and, before CNPN recommended that it be since these were not removed, overall pro- carried out by the national wildlife service, ductivity at the colony remained high. ONCFS, beginning in 2007. ONCFS removal was thus deemed inefficient as a employs c. 1,400 environment officers who measure to reduce the population signifi- are responsible for the implementation of cantly. In 2007, ONCFS explored a number environmental regulations, including the of methods for eradication, and a pro- monitoring and policing of hunting. Once gramme of shooting was launched in 2008. the revised eradication programme had However, since officers are not permitted to been approved by all the mandatory advi- shoot ibises in nature reserves, there was little sory bodies at national and regional levels, impact on overall numbers in 2008; the and no opposition was forthcoming from numbers killed was almost matched by the conservationists, the programme recom- hundreds of young fledged from Lac de menced. Grand-Lieu (which, after culling at other The eradication project enabled France to sites, has been the main breeding site meet its international commitments, namely for Sacred Ibises since 2009). Since 2009, a the Bern Convention on the Conservation of programme of egg sterilisation at Grand-Lieu European Wildlife and Natural Habitats and has ensured that most eggs do not hatch. AEWA (the Agreement on the Conservation Done twice during the breeding season, this of African-Eurasian Migratory Waterbirds), has ensured that the vast majority of initial which both demand that signatory parties and replacement clutches do not hatch, and eliminate when they pose has resulted in a marked reduction in the a threat to native species. number of fledged young. Elsewhere, most

5000 breeding pairs birds shot 4000 sterilised clutches January count

3000

2000

1000

0 2006 2007 2008 2009 2010 2011 2012 2013 2014 2015 2016 2017 Fig. 4. Sacred Ibis Threskiornis aethiopicus populations in France, 2006–17, showing the decline in the number of breeding pairs and non-breeding individuals (January count) present during the eradication programme, as well as number of birds shot and clutches sterilised.

British Birds 110 • April 2017 • 197–212 207 Yésou et al.

tion of the programme more difficult. The average number of ibises culled per day decreased from 33 per officer in 2008 to 9–10 in 2012–13. The increased effort required per bird makes it difficult to predict when complete eradi- cation will be achieved. On the Mediterranean coast, 485 ibises have been removed from the wild, 395 Denis Lacourpaille killed and 90 captured alive and placed in an . The latter were birds that con- tinued to feed at the wildlife parks from which they origi- nated. Alpha-chloralose was mixed with animal food in order to capture them (the drug is used to stupefy the birds, which can then be cap- tured and allowed to recover). Most culling took place in 2007 and 2008, and by 2010 no Sacred Ibises remained

Denis Lacourpaille outside the Camargue, where 101 & 102. Decoys used to attract Sacred Ibises Threskiornis fewer than 20 birds were still aethiopicus during culling operations in western France, May 2013. present. These birds ranged over a wide area, often vis- birds were shot, either on the ground at iting sites where access was difficult or where feeding sites or near colonies, when flying to they were associated with sensitive species, and from foraging areas. Great care was taken which meant that control was much more to avoid disturbance to other species and col- problematic. Despite those difficulties, only lateral damage. Hence, very little work was two ibises were still alive by the end of 2015. carried out at roost sites, which usually contain other species. The cost of eradication In western France, a total of 8,237 Sacred The full cost of the eradication programme Ibises were culled between 2007 and 2016, has yet to be fully established. In the Mediter- and 3,334 clutches of eggs were sterilised at ranean, the cost of culling 173 of the 395 the Lac de Grand-Lieu colony in 2009–16. individuals removed (44%) has been esti- This led to a marked population decline (fig. mated at c. €50,000 (Mouronval 2013), 4) and, in January 2017, only c. 300–350 which would extrapolate to c. €114,000 for birds were attending winter roost sites. The the entire population. In western France, the Grand-Lieu reserve is the only breeding site cost of the cull and the egg sterilisation pro- still regularly occupied in western France, gramme, together with associated adminis- after operations at alternative breeding sites tration costs, was estimated at c. €400,000 led to their abandonment. Non-breeding over the five-year period, 2008–12. Although birds continue to disperse over much of the the number of ibises has been significantly area occupied before the eradication pro- reduced, the annual cost of the eradication gramme began, but in much smaller groups. programme may now rise as more effort is This, and the fact that the ibises have become required to remove the remaining birds in an less approachable over time, makes comple- increasingly small, widely dispersed, and now

208 British Birds 110 • April 2017 • 197–212 The Sacred Ibis in Europe: ecology and management wary population. Additional costs, not incor- programme to eradicate thousands of birds porated in the above estimate, include, for can be and is surely the greatest incentive for example, those linked to studies carried out widespread adoption of EU regulations – alongside the programme, such as popula- that no escapes from captive populations are tion surveys, and the costs of the associated permitted, and that programmes are devel- legal and scientific framework. oped to remove the introduced populations throughout Europe. Clearly, retrieving the Conclusions current situation in Italy will not be cheap. In France and elsewhere, the adaptability of In the UK, the Non-native Species the Sacred Ibis, in particular its ability to Secretariat (www.nonnativespecies.org) is thrive in close proximity to humans, has responsible for controlling and managing the meant that introduced populations can potential by non-native species become established quickly. Such popula- and has an action plan which aims to tions may bring significant conservation prevent the Sacred Ibis becoming an problems. Events in the Netherlands and established non-native species (www.non Florida show that effective colonisation can nativespecies.org//downloadDocument. arise from a very small founder population, cfm?id=942). In the first instance, any free- only five birds in the latter case, and that the flying Sacred Ibis should be reported to the population growth rate can be even greater Centre for Ecology & Hydrology (www.brc. than that observed in France (Smits et al. ac.uk/risc/alert.php?species=sacred_ibis). In 2010); the events in both France and Italy 2014, following a police investigation, the show that numbers in the wild can remain local zoo in Cumbria referred to earlier in low for a long time before a sudden marked this article was fined over £5,000 for allowing increase. Only a rapid response will enable free-flying birds to escape. The owner shot a such populations to be controlled, which was number of the free-flying birds when the case in both the Netherlands and the informed he was being investigated, but was USA, and also in Spain. The situation in still prosecuted for allowing birds to escape western France shows just how costly a during the previous few years. This is a rare Roberto Zaffi 103. Hybrid Sacred Ibis Threskiornis aethiopicus x Platalea alba, Punte Alberete, Po Delta, Italy, August 2008. Ringed as a pullus in 2008 in the Valle Mandriole reserve near Ravenna, this bird was seen up to 2010 at least. No hybrids have been observed in western France, where Sacred Ibises and Eurasian Spoonbills P. leucorodia can share the same colony but differ in the timing of breeding.

British Birds 110 • April 2017 • 197–212 209 Yésou et al. Richard Chandler 104. Sacred Ibis Threskiornis aethiopicus, Cley, Norfolk, June 2012. Such birds are reported not infrequently in the UK, and may originate either from non-native populations on the Continent, most likely France, or from collections closer to home.

example of the enforcement of legislation to Nantes. www.oncfs.gouv.fr/IMG/pdf/ prevent non-native species becoming estab- rapport_ibis_pathogenes.pdf Bonn, D. 2005. Waterfowl return to Iraq’s recovering lished, and shows just how seriously the marshlands. Frontiers in Ecology and the Environment potential threat from this species was consid- 3: 409. ered to be. Brown, L. H., Urban, E. K., & Newman, K. (eds.). 1982. The Birds of Africa. Vol. 1. Academic Press, London. Acknowledgments Clark, R. A. 1979. The food of the Sacred Ibis at Pretoria, Transvaal. Ostrich 50: 104–111. We would like to thank the many observers, too — & Clark, A. 1979. Daily and seasonal movements of numerous to mention individually, who assisted and the Sacred Ibis at Pretoria, Transvaal. Ostrich 50: 94– monitored this programme, and the conservation 103. societies and institutions who have provided Clergeau, P., & Yésou, P. 2006. Behavioural flexibility and information for the risk assessment process. We also numerous potential sources of introduction for the thank ONCFS environment officers and staff for their Sacred Ibis: causes of concern in Western Europe? ongoing involvement in the implementation of the Biological Invasions 8: 1381–1388. eradication programme, and in particular Dominique —, —, & Chadenas, C. 2005. Ibis sacré (Threskiornis Aribert (now at LPO, BirdLife partner in France), Jean- aethiopicus). Etat actuel et impacts potentiels des Marc Cugnasse, Louis-Gérard d’Escrienne, Denis populations introduites en France métropolitaine. Lacourpaille, Jean-Baptiste Mouronval and Luc Simon. Rapport d’expertise collective au MEDD/Diren Pays de la Loire et Bretagne, contrat 137 44–10/60 References du 06/12/2004. Rennes et Nantes, INRA & Agoramoorthy, G., & Hsu, M. J. 2007. Ritual releasing of ONCFS. www.oncfs.gouv.fr/IMG/pdf/ wild animals threatens island ecology. Human ibis_INRA_ONCFS.pdf Ecology 35: 251–254. —, Fourcy, D., Reeber, S., & Yésou, P. 2010a. New but Bastian, S., Passet, A., Lagrange, P., Laroucau, K., Pellerin, nice? Do alien Sacred Ibises Threskiornis aethiopicus J. L., Yésou, P., Hars, J., Clergeau, P., Bazus, J., & L’Hostis, stabilize nesting colonies of native Spoonbills M. 2010a. Contact of livestock with an invasive Platalea leucorodia at Grand-Lieu Lake, France? species, the Sacred Ibis (Threskiornis aethiopicus) – Oryx 44: 533–538. a multidisciplinary approach for risk assessment. —, Reeber, S., Bastian, S., & Yésou, P. 2010b. Le profil 9th EWDA Conference, 13–16 September 2010. alimentaire de l’ibis sacré Threskiornis aethiopicus Vlieland, Netherlands. introduit en France métropolitaine: espèce —, Yésou, P., Clergeau, P., Laroucau, K., Pellerin, J. L., généraliste ou spécialiste? Revue d’Ecologie Hars, J., Bazus, J., Passet, A., Lagrange, P., & L’Hostis, (Terre&Vie) 65: 331–342. M. 2010b. Eléments pour l’évaluation des risques de Juana, E., & Garcia, E. 2015. The Birds of the Iberian sanitaires liés aux Ibis sacrés en France. Oniris, Peninsula. Christopher Helm, London.

210 British Birds 110 • April 2017 • 197–212 The Sacred Ibis in Europe: ecology and management del Hoyo, J., Elliott, A., & Sargatal, J. (eds.). 1992. méditerranéen français: impact sur l’avifaune. Handbook of the Birds of the World. Vol. 1. Lynx Ornithos 12: 84–86. Edicions, Barcelona. Kopij, G. 1999. Breeding ecology of the Sacred Ibis Delivering Alien Invasive Species Inventories for Threskiornis aethiopicus in the Free State, South Africa. Europe (DAISIE). 2009. Handbook of Alien Species in South African Journal of Wildlife Research 29: 25–30. Europe. Springer, Dordrecht. Maillard, J. F., & Yésou, P. 2016. Etat des populations Dvorska, L., Matlova, L., Ayele, W. Y., Fischer, O. A., d’Ibis sacré (Threskiornis aethiopicus) en France en Amemori, T., Weston, R. T., Alvarez, J., Beran, V., janvier 2016 et bilan des mesures de lutte mises Moravkova, M., & Pavlik, I. 2007. Avian tuberculosis œuvre au cours de l’année 2015. ONCFS report to in naturally infected captive water birds of the the French administration. Ardeideae and families studied by Marion, L. 2006. Status of the breeding population of serotyping, IS901 RFLP typing, and virulence for Spoonbills in France and relation with Sacred Ibis. poultry. Veterinary Microbiology 119: 366–374. Spoonbill Network Newsletter 4: 36–40. Epstein, J. H., McKee, J., Shaw, P., Hicks, V., Micalizzi, G., — 2013. Is the Sacred Ibis a real threat to Daszak, P., Kilpatrick, A. M., & Kaufman, G. 2007. biodiversity? Long-term study of its diet in non- The (Threskiornis molucca) as native areas compared to native areas. a reservoir of zoonotic and livestock pathogens. Comptes Rendus Biologies 336(4): 207–220. EcoHealth 3: 290–298. — & Marion, P. 1994. Première installation spontanée European Commission. 2014. Regulation (EU) No. d’une colonie d’Ibis sacré Threskiornis aethiopicus au 1143/2014 of the European Parliament and of the lac de Grand-Lieu. Alauda 62: 275–280. Council of 22 October 2014 on the prevention Martin-Albarracin, V. L., Amico, G. C., Simberloff, D., & and management of the introduction and spread of Nuñez, M. A. 2015. Impact of non-native birds on invasive alien species. http://eur-lex.europa.eu/ native ecosystems: a global analysis. PLoS ONE 10 legal-content/EN/TXT/?uri=CELEX:32014R1143 (11): e0143070. doi:10.1371/journal.pone.0143070. — 2016. Commission implementing regulation (EU) Mooney, H. A., & Cleland, E. E. 2001. The evolutionary 2016/1141 of 13 July 2016 adopting a list of impact of invasive species. Proc. Natl. Acad. Sci. 98: invasive alien species of Union concern pursuant to 5446–5451. Regulation (EU) No. 1143/2014 of the European Mourer-Chauviré, C. 1993. The Pleistocene avifauna of Parliament and of the Council. Official Journal of the Europe. Archeofauna 2: 53–66. European Union L 189/4 14.7.2016. Mouronval, J. B. 2013. Eradication de l’Ibis sacré http://eur-lex.europa.eu/legal-content/EN/TXT/ (Threskiornis aethiopicus) du pourtour ?uri=CELEX:32016R1141#document1 méditerranéen français. ONCFS internal report, Fàbregas, M. C., Guillén-Salazar, F., & Garcés-Narro, C. Le Sambuc. 2010. The risk of zoological parks as potential Philippon, P., & Yésou, P. 2012. Ibis sacré. In: Groupe pathways for the introduction of non-indigenous ornithologique breton (coord.), Atlas des oiseaux species. Biological Invasions 12: 3627–3636. nicheurs de Bretagne, pp. 447–448. Delachaux & Frémont, J. Y. 1995. L’Ibis sacré Threskiornis aethiopicus: Niestlé, Paris. une nouvelle espèce nicheuse pour la France. Robert, H., Lafontaine, R-M., Delsinne, T., & Beudels- Ornithos 2: 44–45. Jamar, R. C. 2013. Risk Analysis of the Sacred Ibis Global Invasive Species Database (GISD). 2017. Threskiornis aethiopicus (Latham 1790). Risk analysis Species profile: Corvus splendens. report of non-native organisms in Belgium from the www.iucngisd.org/gisd/species.php?sc=1199 Royal Belgian Institute of Natural Sciences for the Hancock, J. A., Kushlan, J. A., & Kahl, M. P. 1992. , Federal Public Service Health, Food chain safety and Ibises and Spoonbills of the World. Academic Press, Environment. Royal Belgian Institute of Natural London. Sciences, Brussels. Harrison, J. A., Allan, D. G., Underhill, L. G., Herremans, Smits, R. R., van Horssen, P., & van der Winden, J. 2010. M., Tree, A. J., Parker, V., & Brown, C. J. (eds.). 1997. A Risk Analysis of the Sacred Ibis in the Netherlands. The Atlas of Southern African Birds. Vol. 1. BirdLife Including biology and management options of this South Africa, Johannesburg. invasive species. Bureau Waardenburg, Culemborg. Henderson, I. 2009. Progress of the UK Ruddy Duck Thévenot, M., Vernon, R., & Bergier, P. 2003. The Birds of eradication programme. Brit. Birds 102: 680–690. Morocco. BOU, Tring. Herring, G., & Gawlik, D. E. 2008. Potential for Underhill, L. G., Tree, A. J., Oschadleus, H. D., & Parker, V. successful population establishment of the 1999. Review of Ring Recoveries of Waterbirds in nonindigenous Sacred Ibis in the Florida Everglades. Southern Africa. Avian Demography Unit, University Biological Invasions 10: 969–976. of Cape Town. Hockey, P. A. R., Dean, W. R. J., & Ryan, P. G. (eds.). 2005. Urban, E. K. 1974. Breeding of Sacred Ibis at the Lake Roberts Birds of Southern Africa. 7th edn. Trustees of Shala, Ethiopia. Ibis 116: 265–277. the John Voelcker Bird Book Fund, Cape Town. Vaslin, M. 2005. Prédation de l’Ibis sacré Threskiornis Holling, M., & the Rare Breeding Birds Panel. 2017. aethiopicus sur des colonies de sternes et de Non-native breeding birds in the UK in 2012–14. guifettes. Ornithos 12: 106–109. Brit. Birds 110: 92–108. Vilà, M., Basnou, C., Pysek, P., Josefsson, M., Genovesi, P., Johnson, S. A., & McGarrity, M. 2009. Florida’s Introduced Gollasch, S., Nentwig, W., Olenin, S., Roques, A., Roy, Birds: Sacred Ibis (Threskiornis aethiopicus). D., Hulme, P. E., & DAISIE partners. 2010. How well Publication WEC 267, Florida Cooperative do we understand the impacts of alien species on Extension Service, University of Florida, Gainesville. ecosystem services? A pan-European, cross-taxa Kayser, Y., Clément, D., & Gauthier-Clerc, M. 2005. L’Ibis assessment. Frontiers in Ecology and the Environment sacré Threskiornis aethiopicus sur le littoral 8: 135–144.

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Vorimore, F., Hsia, R. C., Huot-Creasy, H., Bastian, S., — & Clergeau, P. 2005. Sacred Ibis: a new invasive Deruyter, L., Passet, A., Sachse, K., Bavoil, P., Myers, species in Europe. Birding World 18: 517–526. G., & Laroucau, K. 2013. Isolation of a new — & Reeber, S. 2014. Ibis sacré Threskiornis aethiopicus. Chlamydia species from the feral Sacred Ibis In: Marchadour, B. (coord.), Oiseaux nicheurs des (Threskiornis aethiopicus): Chlamydia ibidis. PLoS Pays de la Loire, pp. 112–113. Delachaux & Niestlé, ONE 8(9): e74823. Paris. doi:10.1371/journal.pone.0074823 —, Cabelguen, J., & Potiron, J. L. 2006. Quelques Williams, A. J., & Ward, V. L. 2006. Sacred Ibis and Gray aspects de la reproduction de l’ibis sacré predation of Cape Cormorant eggs and Threskiornis aethiopicus dans l’estuaire de la Loire. chicks; and a review of ciconiiform birds as Alauda 74: 421–427. predators. Waterbirds 29: 321–327. Zenatello, M., Baccetti, N., & Borghesi, F. 2014. Risultati Yésou, P. 2005. L’Ibis sacré Threskiornis aethiopicus dans dei censimenti degli uccelli acquatici svernanti in Italia. l’ouest de la France: historique et statut actuel. Distribuzione, stima e trend delle popolazioni nel Ornithos 12: 81–83. 2001–2010. ISPRA, Serie Rapporti, 206/2014.

Pierre Yésou, ONCFS, Cellule technique Bretagne et Pays de la Loire, CS 42355, 44323 Nantes cedex 3, France; e-mail [email protected] Philippe Clergeau, UMR CESCO, Département Ecologie et gestion de la Biodiversité, Muséum National d’Histoire Naturelle, 55 rue Buffon, 75005 Paris, France Suzanne Bastian, Département de Santé des Animaux d’Elevage et Santé Publique, UMR 1300 Oniris/INRA Biologie Epidémiologie et Analyse de Risques, CS 40706, 44307 Nantes cedex, France Sébastien Reeber, Réserve naturelle nationale du Lac de Grand-Lieu, Société Nationale de Protection de la Nature, La Chaussée, 44830 Bouaye, France Jean-François Maillard, ONCFS, Direction de la recherche et de l’expertise, 5 rue de Saint-Thibaud, Domaine de Saint-Benoît, 78610 Auffargis, France

Pierre Yésou has had a long career in the study of waterbirds, particularly shearwaters and gulls, and the conservation of their habitats. Recently retired, he continues to act as an environmental advisor. Philippe Clergeau is Professor at the Natural History Museum in Paris. He previously conducted research at INRA, working on invasive species, their impact (especially in agricultural systems) and management. Current research interests include urban biodiversity and ecological landscape planning. Suzanne Bastian is a Senior Lecturer at ONIRIS, the National Veterinary School in Nantes and a researcher in biology, epidemiology and risk analysis on animal health, studying both wild and domestic species. Sébastien Reeber is in charge of scientific research, in particular bird surveys, for Société Nationale de Protection de la Nature at the Grand-Lieu reserve, which hosts the largest colony of Sacred Ibises in France. Jean-François Maillard coordinates the work on alien invasive species at ONCFS, focusing on mammals and birds, and he contributes to the formulation of national policy. Regarding the Sacred Ibis, he supervises the implementation of decisions made by the Ministry of Environment. Request

William MacGillivray’s History of British Birds – have you seen this? In 1924 the London booksellers Henry Sotheran issued for sale a catalogue of the books that had belonged to Major W. H. Mullens, the leading ornithological bibliographer of the time. Among the items being offered was a unique set of the first three volumes of William MacGillivray’s History of British Birds (issued in 1837, 1839 & 1840). What made this set special is that it was MacGillivray’s personal set, ‘containing a great amount of fresh information in the author’s own handwriting throughout the three volumes, but more so in Vols. 1 and 3. The text has not only been corrected by a matter of single words, writer’s and printer’s errors, etc., but whole passages have been cancelled and fresh material substituted in the margins. In addition many leaves and slips have been loosely pasted in, filled with extra material, the whole being in MacGillivray’s handwriting and obviously intended for an enlarged and revised edition.’ Alan Knox ([email protected]) has been working on MacGillivray for some time now and would like to locate these volumes if possible. It is not known who Sotheran sold them to and they may now be in private hands or in a library.

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