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What makes a good alien? Dealing with the problems of non-native wildfowl Tony (A. D.) Fox

Mandarin galericulata Richard Allen ABSTRACT Humans have been introducing outside their native ranges as a source of food for thousands of years, but introductions of wildfowl have increased dramatically since the 1700s.The most serious consequence of this has been the extinction of endemic forms as a result of hybridisation, although competition between alien and native forms may also contribute to species loss. Globally, non-native wildfowl have yet to cause major disruption to ecosystem functions; introduce new diseases and parasites; cause anything other than local conflicts to agricultural and economic interests; or create major health and safety issues in ways that differ from native forms. The fact that this has not happened is probably simply the result of good fortune, however, since many introduced plants and have had huge consequences for ecosystems and human populations.The potential cost of greater environmental and economic damage, species extinction, and threats to the genetic and species diversity of native faunas means that we must do all we can to stop the deliberate or accidental introduction of species outside their natural range. International legislation to ensure this is remarkably good, but domestic law is generally weak, as is the political will to enforce such regulations.The case of the Ruddy Oxyura jamaicensis in will show whether control of a problem taxon can be achieved and underlines the financial consequences of dealing with introduced aliens.This paper was originally presented as the 58th Bernard Tucker Memorial Lecture to the Oxford Ornithological Society and the Ashmolean Natural History Society, in November 2008.

660 © British 102 • December 2009 • 660–679 What makes a good alien?

here is nothing new about aliens – we (Harding 2000), introduced from the have been living among them in Britain ‘fertile crescent’ of modern-day , Lebanon, Tfor a very long time. But fear not, we are parts of Jordan, Syria, Iraq, Kuwait, southeast not talking about creatures from outer space! and southwest , where these species Here, I define an alien as ‘a group of individuals originated. The Romans brought apples Malus of a species, subspecies or population that domestica (a vast improvement on native crab would not occur in an area without interference apples M. sylvestris), sweet chestnuts Castanea from humans’. This definition therefore sativa, cherries Prunus spp. (introduced to includes species like the Anas Britain between 68 and 42 years BC; Pliny 1601) platyrhynchos, which can represent a threat to and the jungle fowl Gallus gallus, which gave their own native integrity through introgression rise to modern . They probably also from domestic or other non-native forms. brought Oryctolagus cuniculus and Using this definition, humans have been cre- Common Pheasants Phasianus colchicus, which ating alien species for many thousands of years. we now know to be readily self-supporting in Initially, the process was driven by the simple the wild in Britain. Much later, Europeans need for food. The change from an essentially explored the globe, bringing more exotic food hunter-gatherer lifestyle to a sedentary existence items back to Europe including, most notably, required becoming highly adept at plant and the potato Solanum tuberosum agg., cultivated husbandry, to provide food. This relied in South America for some 7,000 years and upon cultivation of non-native alien forms brought to the Canary Islands around 1562 imported outside their normal biogeographic (Hawkes & Francisco-Ortega 1993). Not all ranges. Hull-less six-rowed barleys Hordeum aliens could thrive without human help to tip vulgare were first introduced to Britain around the balance of competitive interactions with 3,000 years BC (Clark 1967) and, by the Bronze native forms. Even so, all are good reminders of Age, spelt Triticum spelta and emmer wheat T. our long history in the introduction business dicoccon were the most commonly cultivated and the reliance upon aliens for food. Simon Stirrup 429. Egyptian Alopochen aegyptiacus, Norfolk, December 2006. Domesticated Egyptian Geese constituted the most important source of meat on tables in until about 2,300 years BC (Kear 1990). Not until the recently acquired habit of foraging on silage clamps became widespread did this alien species begin to appear in European farmyards.

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What creates an alien in the first place? in the mid 1500s, reaching Britain somewhat Ducks, geese and swans (the ) were later in the following century (Donkin 1989). among our earliest and most successful Some alien Anatidae species were therefore rela- attempts at domestication to produce tame tively easy to domesticate and rear in captivity flesh. The Anser anser was one of and were thus quick to attain importance in the the very first birds known to be domesticated, staple diet of many human societies, making some 5,000 years ago (Sossinka 1982), and is them a familiar feature of Britain and much of the source of modern farmyard geese and the Europe by the early eighteenth century. rich spoken tradition of stories and nursery But alien wildfowl really started to take off in rhymes that involve this familiar domesticated the philanthropic years of the mid 1700s, when bird (Kear 1990). The Swan Goose A. cygnoides some Europeans could suddenly travel on their of eastern Asia was also probably domesticated new-found wealth and engaged their curiosity for food at a very early stage (Crawford 1984). in finding out about the great diversity of the In all likelihood, were also brought globe. This was the time of the great British into domestication long ago in many parts of estates, when landowners wished to show off the Old World, given the wide range of Mallard- their wealth and power with impressive land- type breeds now in existence. Egyptian Geese scaped gardens and , the period when Alopochen aegyptiaca were the primary source Lancelot (‘Capability’) Brown created over 170 of avian food for the Egyptians until about exotic country gardens, complete with serpen- 2,300 years BC, finally disappearing as farm tine lakes and landscaped ponds (Turner 1999), animals only after Egypt was conquered by the complemented by stocks of exotic wildfowl. The Persians in 525 BC (Kear 1990). Farmyards were grounds of Holkham Hall, Norfolk, for therefore free of this species until free-flying example, were laid out by Brown in 1762, when naturalised birds began to forage on silage Egyptian and Geese Branta clamps in Europe in recent years. The first canadensis/hutchinsii were introduced immedi- exotic wildfowl species to be introduced into ately. As Janet Kear remarked: ‘wildfowl in cap- Europe must have been the Muscovy Duck tivity look better than other birds’; they seem to Cairina moschata, which was already widely adapt well to such conditions and many species kept throughout South America and the West breed and thrive under a variety of conditions Indies when the Conquistadores reached the (Kear 1990). The Holkham Egyptian and New World; birds were brought back to Spain Canada Geese reproduced, and unpinioned, Rebecca Nason 430. Greylag Geese Anser anser, Suffolk, May 2008. Greylag Geese were among the very first domesticated birds some 5,000 years ago (Sossinka 1982), as well as the source of many modern ‘farmyard geese’ and the rich spoken tradition of stories and nursery rhymes that involve this familiar bird (Kear 1990).

662 British Birds 102 • December 2009 • 660–679 What makes a good alien? free-flying offspring dispersed to become some cessfully self-replicating alien replacement for of the first free-flying alien wildfowl in the UK. the Greylag Goose (likely extirpated from much It was a time when it was fashionable to possess of Britain by exploitation in earlier times), was the most recently discovered representatives of able to exploit the niche of a large avian herbi- exotic floras and faunas of foreign shores. vore without serious competitors in an increas- Canada Geese from the New World were intro- ingly favourable agricultural environment. duced to many a country estate, as were Black Elsewhere, Mallards have been introduced Swans Cygnus atratus from the very far reaches throughout most of the world at some time, of the Empire (imagine the novelty value in a driven by the species’ familiarity to Europeans continent with swans only of the very purest as they themselves colonised much of the globe. white!). Later, people could afford to enjoy the In this way, the species was introduced into ornamental beauty of wildfowl in the form of by the ‘acclimatisation societies’ bright and exotic species, such as the Mandarin there, in an attempt to make their new home Duck Aix galericulata, which has now been kept feel more familiar by the presence of such Euro- in captivity for many decades and (as a frequent pean taxa – together with the non-European deliberate or unintentional escape) has now (which is now also among the established populations in several Euro- most common birds in that country), brought pean countries. The Canada Goose was also in as quarry by hunter associations. found to be a good quarry species and, as a suc- More recently still, the expansion of private

Box 1. What do we mean by an alien and how big is the problem? The working definition of an alien adopted for this paper is simple – it is a species, subspecies or geographically discrete population that would not occur in a specific geographical area without interference by humans. In reality this may mean: a taxon (i) introduced as a breeding bird to a region where it formerly occurred only outside the breeding season; (ii) one introduced entirely from outside its previous known range; (iii) one imported in captivity outside its normal range and allowed to escape; and (iv) domesticated taxa that have established themselves in the wild (Owen et al. 2006). A recent review (Banks et al. 2008) of the 77 responses to a questionnaire sent to all 116 signatories to the African-Eurasian Waterbird Agreement found that the greatest numbers of non- native waterbird species were in Europe (an average of 7.7 species per nation in 37 countries), with fewer in Asia Minor and the Middle East (4.3 species in 7 countries), Africa (1.2 in 29), Asia (0.3 in 4) and northeast Arctic Canada and Greenland (none in these two regions). Britain reported the greatest number (72 species).This article is restricted to the non-native Anatidae species, of which there are many.The most commonly introduced species to the AEWA area was the Mandarin Duck Aix galericulata, recorded in and 16 different European states. Cygnus olor, Black Swan C. atratus, Bar-headed Goose Anser indicus, Greylag Goose A. anser, Canada Goose Branta canadensis/hutchinsii, Egyptian Goose Alopochen aegyptiacus, Ruddy Tadorna ferruginea, Aix sponsa and Ruddy Duck Oxyura jamaicensis were all recorded from 10 or more countries, based on data from Blair et al. (2000) and Rehfisch et al. (2006). Canada Geese are especially long established in Europe, having been introduced to England in the seventeenth century and to Sweden and other parts of Europe since 1933 as well as to New Zealand and other parts of the globe (Callaghan & Kirby 1996). Flicking through the Wetland Bird Survey Annual Reports since 1999/2000 reveals no fewer than 56 different species of ducks, geese and swans occurring regularly as escapes or escapes/vagrants in the UK (out of 77 species listed on Category E of the BOU list), which make our regularly occurring 27 ‘native’ species look positively depauperate (e.g.Austin et al. 2008)! Nevertheless, the problem is not evenly spread over the globe – latitude is inversely correlated with non-native species richness in many groups, but there is no doubt that human population and local plant species richness both have a major influence, because we tend to occupy the most productive and biologically diverse habitats of the planet. However, the presence of high densities of humans also increases the degree of disturbance to natural habitats and the probability of importation of non-native species into the areas of the planet that we most like to occupy (McKinney 2006).

British Birds 102 • December 2009 • 660–679 663 What makes a good alien? collections of waterbirds has increased the nental Europe, apparently resulting largely from numbers of escaped exotic birds, especially in the population establishing in Britain. In Spain, Europe. Intercontinental transport now enables the arrival of the Ruddy Duck threatened the us to move the flora and fauna of the world outstandingly successful conservation efforts to around with an ease never before possible and pull the White-headed Duck Oxyura leuco- the increasing pressures of the global food cephala back from the brink of extinction in industry and the enhanced affluence of com- western Europe. Soon after the arrival of the munities across the globe mean that movement Ruddy Duck there, hybrids between the two of birds occurs now on a scale unimaginable in species were found and there was a clear risk of earlier times. Although most introduced birds creating a swarm of Oxyura ducks of seem not to settle and establish viable popula- mixed genotype, resulting in the certain disap- tions in unfamiliar territory (Lever 1987; Kear pearance of the White-headed Duck as the 1990), this does of course mean that the risk of genetic entity we recognise today (Muñoz- deliberate or unintentional introductions of Fuentes et al. 2006). exotic wildfowl around the world is now greater The White-headed Duck represented an than ever before (see Box 1). endangered taxon dependent on ephemeral Mediterranean wetlands. It had become a flag- Why all the fuss – how do aliens affect our ship for habitat conservation in a part of the flora and fauna? world where the pressures of drinking water Aliens are frequently cited as causing a wide supply, agriculture and climate change are range of problems to the native flora and fauna placing enormous strains on water manage- they become established within, as well as ment. All the positive ground won in the battle causing specific problems for us and the agri- to protect the White-headed Duck was suddenly cultural systems upon which we depend. Frus- potentially undermined by the arrival of the tratingly, there is generally very little good Ruddy Duck. Conservation plans for the White- supporting evidence for many of the effects for headed Duck highlighted the need for action to which aliens stand accused. Let us explore some save the species (Anstey 1989; Green & Hughes of the mechanisms by which aliens are sup- 1996; Li & Mundkur 2002; Hughes et al. 2006), posed to have had effects on native organisms which led to the development of a strategy to and systems. eradicate the Ruddy Duck from the Western Palearctic (see Henderson 2009). Hybridisation Recent estimates of the cost of the Ruddy Bibby (2000) found it chilling that aliens were Duck eradication have been in the order of £3.6 ‘the only form of pollution which sponta- to £5.4 million, a very substantial amount of neously self-replicates’, but perhaps even more money in relation to other conservation insidious is that some aliens hybridise with budgets. However, it is perhaps instructive to native forms to create a potentially bleak route compare the relative costs of control of a species to the extinction of the latter. Much of the focus like the Ruddy Duck with those of other groups on problems associated with introduced wild- to put the problem in perspective. In the UK, it fowl has arisen from the highly controversial is estimated that, of the very many invasive (but now extensively well-researched) case plant species that have become established, just study of the Ruddy Duck Oxyura jamaicensis. nine cause really serious economic conse- As described in more detail elsewhere in this quences, amounting to an expenditure of £300 issue (Henderson 2009, pp. 680–690), Ruddy million per annum (Williamson 2002). Intri- Ducks escaping from captivity in England in guingly, this compares with the adverse costs of the middle part of the twentieth century led to native plant species (most significantly agricul- the establishment of a feral population of 6,000 tural weeds) of over twice that amount, but individuals by 2000 (Kershaw & Hughes 2002; resulting from a very much broader range of Hughes et al. 2006). This in itself caused no species and conflicts. obvious problems in Britain, since there were Although the ‘Ruddy Duck issue’ is perhaps no apparent competitive or other adverse inter- the most well-known hybridisation problem actions with the native avifauna (Hughes 1992). faced by the Anatidae in western Europe, it is by Of far greater concern was the increasing no means an isolated case. Unlike the accidental numbers of Ruddy Ducks occurring in conti- introductions of Ruddy Ducks to western

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Europe, Mallard introductions have been pur- hybridise with a vast array of dabbling ducks poseful through vast areas of the planet where that the need is very much to protect species the species was not formerly native. This exten- from the direct threat of extinction through the sive introduction has contributed to the decline creation of hybrid swarms (Rhymer 2006). This of dabbling ducks of many forms within their is especially the case where previously isolated native range (see Box 2). taxa are exposed to congeners that are more The major problem is that although classi- abundant and/or aggressive. Of course, some cally ‘good’ bird species can be considered sepa- degree of flow is normal, indeed healthy, rable on the basis of their inability to hybridise between different populations to ensure diver- (e.g. Helbig et al. 2002), the reality is that even sity and support the fundamental processes of very distinct species within the same are evolution (Arnold 1997). However, ‘sudden’ capable of producing fertile hybrids, despite shock hybridisation of an isolated form con- genetic evidence of prolonged separation (Price fronted by exposure to a dominant congener 2006). Genetic studies suggest that Ruddy presents the risk of extinction by introgression Ducks have been geographically isolated from (resulting in a hybrid swarm that threatens the White-headed Ducks for some 2–5 million genetic integrity of the original form) or years (McCracken et al. 2000), yet we know to (where hybrid offspring are infertile) from our cost that these ‘good’ species will inter- other effects on the fitness of the less dominant breed. In other words, the fact that two taxa species that may equally exacerbate rarity or have been subject to prolonged separation, and result in extinction (Allendorf et al. 2001; have had time to accumulate highly specific Rhymer 2006). adaptations to the respective environments in This is really the main issue – not whether which they have evolved, does not necessarily we as humans prefer to see the White-headed mean that the two cannot hybridise. Indeed, it Duck as a species because we like it and prefer it is clear from the ability of the Mallard to over a hybrid swarm of crosses with Ruddy www.-photography.co.uk Mike Lane Mike 431. Male White-headed Duck Oxyura leucocephala, Spain, April 2005.Towards the end of the twentieth century, the White-headed Duck had become an icon for wetland conservation management in southern Europe. In Spain, the species had been successfully dragged from the brink of looming extinction as a result of over- hunting and habitat destruction. In a part of the world where water-resource management is complex and difficult, the saving of a species that depended on ephemeral Mediterranean wetlands was rightly regarded as a major triumph. All of these conservation gains were suddenly potentially compromised by the appearance in the region of the alien Ruddy Duck O. jamaicensis, and a new threat: hybridisation.

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Box 2. Hybridisation problems caused by Mallards. The Mallard Anas platyrhynchos in particular has been introduced purposefully for hunting or other reasons in many parts of the globe. Even in continental North America, where the Mallard was originally native, the introduction of the species to areas not formerly occupied has wrought havoc with the duck populations of that continent. For instance, introductions, in combination with changing land use that has reduced the amount of prairie parkland habitat favoured by its close relative, the North A. rubripes, and increasing artificial and urban wetlands that favour Mallards, have brought two formerly isolated species into increasing proximity and encouraged genetic introgression (Kirby et al. 2001, 2004; Mank et al. 2004). However, it remains the subject of considerable controversy as to the extent to which these factors affect the relative abundance of the two species (Heusmann 1974, 1988; Meredino et al. 1993). Escaped and introduced Mallards have hybridised with the local subspecies of the Mottled Duck in (the so-called ‘Florida Duck’ A. fulvigula fulvigula; Mazourek & Gray 1994) and the Gulf Coast (A. f. maculosa). Both of these sympatric forms are derived from the North American Black Duck and as all these subspecies belong to a ‘mallardine’ clade they readily produce fertile hybrids with Black Ducks and Mallards (McCracken et al. 2001). The resultant gene flow is increasingly involving more introgression with Mallards, but on top of this, habitat destruction and excessive hunting could eventually reduce the Mottled Duck to the point where the hybridisation with Mallards would threaten to make it disappear as a distinct taxon (Rhymer & Simberloff 1996). Introductions and changes in land use have encouraged the expansion of the Mallard into parts of northern , facilitating hybridisation with the Mexican Duck A. diazi, which formerly bred in areas where the Mallard was only a winter visitor, and was therefore genetically isolated (Aldrich & Baer 1970; Hubbard 1977). Such was the subsequent degree of introgression between the two species that the American Ornithologists’ Union declared the two forms conspecific 25 years ago (AOU 1983), despite apparently pure forms of diazi just managing to survive in central Mexico (McCracken et al. 2001). Mallards introduced to have hybridised with the local dabbling duck, the Koloa A. wyvilliana, to the point that only one population (that on the island of Kauai) is not polluted by the Mallard genotype, which tends to dominate the hybrid swarms created everywhere else (Rhymer 2001).The Grey Duck A. superciliosa superciliosa was originally an important hunting quarry species in New Zealand, but since the 1990s has been listed as endangered, simply because it now verges on extinction through competition and hybridisation with Mallards, ironically introduced for sport (Rhymer et al. 1994, 2004; Williams & Basse 2006) and the same could well happen in , where the same species is also present (A. superciliosa rogersi; Paton et al. 1992, Rhymer et al. 1994). The endangered endemic Meller’s Duck A. melleri of Madagascar is threatened by hybridisation with -farm Mallards kept by indigenous peoples on Lac Alaotra, a prime site for the rare species (Young & Rhymer 1998). Deliberate and accidental introductions of the Mallard to southern Africa are also starting to threaten the genetic integrity of the Yellow-billed Duck A. undulata undulata (Rhymer 2006) and BirdLife South Africa supports a Mallard eradication programme (Berruti 1992).

Ducks, but whether we should allow a species Demographic ascendancy introduced artificially to eradicate the genetic Even if there is no direct genetic exchange adaptation accumulated over many thousands between a native and an alien form, there may of years through our carelessness over a handful be differences in the ability of the two forms of decades. Mallards will continue to thrive in which mean that the balance of breeding the heartlands of Europe and North America, success over death rate favours the more rapid but the endemic forms that disappear into the expansion of one species where both compete resulting hybrid swarms will mean the eradica- for the same resources. One of the few examples tion of genetic information of native forms that of where such an analysis has been undertaken may well show unique adaptations to local is with regard to the Grey Duck Anas supercil- environments. In this way we are losing genetic iosa and the Mallard in New Zealand, where diversity within the system, just as vitally as we Williams & Basse (2006) suggested that greater are physically losing species as they disappear breeding success and recruitment and/or into these hybrid swarms. annual survival rates of Mallards would give

666 British Birds 102 • December 2009 • 660–679 What makes a good alien? www.neilfitzgeraldphoto.co.nz Neil Fitzgerald 432. The Grey Duck Anas superciliosa was originally an important hunting quarry species in New Zealand. Since the 1990s, it has been listed as endangered, because it now verges on extinction as a result of competition and hybridisation with the Mallard A. platyrhynchos, ironically introduced there for sport. K.A. Rodgers 433. Throughout many parts of New Zealand it is becoming difficult to find individuals of pure Grey Duck Anas superciliosa phenotype, so widespread has introgression with Mallards A. platyrhynchos become.This is certainly true in the Auckland area, where this adult female and her brood were photographed. Despite her prominent facial stripes, the traces of Mallard ancestry in this bird are all too obvious.

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them an edge over Grey Ducks. Their review of Competition the available data suggested no significant dif- Although many alien waterfowl are accused of ference in annual adult survival estimates some form of competition with native forms, (partly because of the poor precision of the esti- evidence to this effect is rarely forthcoming. mates), but that annual Mallard recruitment Indeed, the demonstration of competitive rates in the 1960s and 1970s averaged approxi- effects between two species is difficult enough mately 15% above the levels needed to maintain under any circumstances, and almost impos- a stable population size (i.e. against contem- sible to be convincing without some form of porary survival rates) while those of the Grey complex modelling of the interactions or Duck were 5% below (Williams & Basse 2006). manipulation experiments. All too often, one This discussion was somewhat academic since species has disappeared following the arrival of genetic introgression (which created a hybrid another before any such effects can be demon- swarm dominated by the Mallard phenotype) strated. It has often been speculated that the was already threatening to exterminate the Grey interspecific aggression between Canada Geese Duck and its phenotype from New Zealand and Greylag Geese has some effect on the native after not much more than 100 years (Thomson species in particular (Madsen & Andersson 1922; Williams & Basse 2006). 1990). However, the only study of these interac- tions in Sweden showed that despite the fact that Canada Geese evicted Greylags from their territories, both species were increasing within the study area (Fabricius et al. 1974). In recent years, the natu- ralised Canada Goose and re- establishing Greylag Goose have also shown parallel increases in abundance throughout much of England (Austin et al. 2008). We should therefore prudently conclude that at those densities there was no apparent interspecific effect, although we cannot be sure that in the absence of the Canada Geese, Greylags would not have increased even faster, nor can we come to conclusions about what happens under conditions of differing relative densities of the two species. Only for the Grey Duck in New Zealand is there some evidence that Mallards have been www.nature-photography.co.uk responsible for the displace- ment of a native species (Williams & Basse 2006). In Mike Lane Mike this case, the 10–15% difference 434. Greater Canada Goose Branta canadensis,Warwickshire, January 2006. Canada Geese were introduced to many newly created country in mass and 10% difference in estates in Britain in the eighteenth and nineteenth centuries. A good linear measurements means quarry species and a successfully self-replicating alien replacement for the that Mallards can use their size Greylag Goose Anser anser (itself probably eliminated from much of Britain advantage to physically displace previously through over-exploitation), the Canada Goose was seemingly and exclude Grey Ducks at able to exploit the niche of a large avian herbivore without serious competition in the agricultural landscapes of the twentieth century. feeding sites (Marchant &

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Higgins 1990; Williams & Basse 2006). Mallards Grey Ducks were just as adept at exploiting dominate access to food at public feeding sites these modified or artificial habitats and it may and usurp Grey Ducks from nest-sites as well, be that the physical or behavioural displace- with the result that sites formerly occupied ment of the Grey Duck by the Mallard is more solely by the endemic have been taken over by to blame in enabling the invading species to Mallards following colonisation, with ultimate occupy the full range of habitats that the Grey loss of the native Grey Duck from large areas of Ducks formerly had to themselves in New formerly occupied territory. Zealand (Williams & Basse 2006). There is also much speculation about how the influence of humans can affect the relative Interference to ecosystem function abundance of different habitats that may tip the Although not strictly confined to non-native competitive balance between two species in wildfowl, information relating to the extra favour of the alien. Again, the well-studied case loading of nutrient inputs to wetlands subject of the Mallard and Grey Duck in New Zealand to artificial stocking and introduction of wild- offers some evidence in this respect. The New fowl suggest that artificially high concentrations Zealand environment has altered radically since of these birds could add significantly to the the arrival of European colonists, especially mobilisation of carbon, nitrogen and phos- through the loss of a quarter of indigenous phorus in freshwater systems (Callaghan & and their replacement largely by inten- Kirby 1996). This conclusion was made largely sively managed and pastoral agricul- on the basis that waterbirds are often the prin- ture (Wards 1976). Almost 90% of natural cipal source of nitrogen and phosphorus in wetlands (to which the Grey Duck traditionally systems (e.g. Manny et al. 1994, Marion et al. resorted) had been lost by 1970 causing a direct 1994) and that concentrations of phosphorus in reduction in range and abundance (Balham particular have such consequences for fresh- 1952; Cromarty & Scott 1996). It has been sug- water trophic systems that relatively modest gested that Mallards are better able to exploit increases can significantly degrade wetland bio- artificial wetlands, such as stock ponds in open diversity (Søndergaard et al. 2005; Jensen et al. habitats and urban waters, but the fact is that 2006). However, convincing case studies Simon Stirrup 435. Muscovy Duck Cairina moschata, Cambridgeshire, August 2006. Among the first exotic wildfowl species to be introduced into Europe must have been the Muscovy Duck, already widely kept throughout South America and the when the Conquistadores reached the New World; birds were brought back to Spain in the mid 1500s, reaching Britain somewhat later in the following century (Donkin 1989).

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demonstrating cause and effect are frustratingly With this possible exception, few if any rare and we have to accept that large concentra- introduced alien waterfowl have caused any tions of native waterbirds aggregated at critical major effects to ecosystem function in the way sites will have precisely the same effect. Recent that, for example, the alien Water Hyacinth studies in Denmark showed that lakes stocked Eichhornia crassipes has caused serious and with reared Mallards for hunting had signifi- widespread damage to freshwater ecosystems in cantly higher phosphorus concentrations in the Africa, the USA, Australia and India (Gopal water than those not subject to stocking, but 1987) or the introduction of predators such as again it was not possible to establish cause and the American Mustela vison to Britain has effect, especially because variation among affected the population dynamics of native prey unstocked lakes was so high (Noer et al. 2008). species (e.g. Craik 1997). The literature is awash These authors also cautioned that any effects with appalling tales of how the introduction of from Mallard stocking on lake biodiversity was predators has had catastrophic effects on the highly dependent on nutrient status, with ecosystems, flora and fauna of island complexes acidic, nutrient-poor waterbodies being more in particular (e.g. Holdaway 1999, Croll et al. sensitive to change as a result of relatively 2005, Kurle et al. 2008). Who would have modest elevations in phosphorus concentrations. thought that the introduction of the humble House Mouse Mus musculus could threaten a population of Tristan Albatrosses Diomedea dabbenena (Wanless et al. 2007)? While it is hard to imagine that introduced water- fowl could seriously affect ecosystem function, the fact that this has not happened to date is purely good fortune and it is essential to maintain vigi- lance to avoid problems in the future.

Disease and parasites Recent concern over highly pathogenic avian has again brought home how per- ilously little we know about the prevalence and ecology of the most common of avian dis- eases, and parasites sit very close behind. We have little idea which avian species could potentially be vectors for which pathogens or parasites, nor can we predict what effect these may have once established else- where on native species. It has taken several years of

Kit Day painstaking research to show 436. Grey perdix, Norfolk, March 2007. The impact that infection by the caecal of alien species is not always readily apparent. Research has shown that infection by the caecal nematode Heterakis gallinarum from farm- nematode Heterakis gallinarum reared Common Pheasants Phasianus colchicus influences the worm from farm-reared Common burdens of wild Grey , thus supporting the hypothesis that Pheasants determines the worm parasite-mediated apparent competition with the Pheasant may be a burdens of wild Grey Partridges factor contributing to declines of Grey Partridges in Britain (Tompkins et al. 2002). Perdix perdix, supporting the

670 British Birds 102 • December 2009 • 660–679 What makes a good alien? hypothesis that parasite-mediated apparent shown to have serious consequences for our competition with the Pheasant may be a factor native fauna, for example. While there are well- contributing to declines of Grey Partridges in documented cases of the impacts of species Britain (Tompkins et al. 2002). Some native such as the Canada Goose on agriculture in Hawaiian species, for instance, are now con- areas in which they have been established, it is fined to higher altitudes because these are the generally possible to find ways of resolving local only refuge from diseases hosted by introduced ‘pest’ conflicts that fall well short of total eradi- avian species in the lowlands (Bibby 2000); cation. The effects on native flora and fauna are others have been driven to extinction by Avian less easy to demonstrate and are very much less relictum (LaPointe et al. well understood away from the direct genetic, 2005). Introduction and stocking of wildfowl demographic or behaviour effects we have con- often concentrate naïve birds at artificially high sidered above. There are reports of Canada densities, which greatly enhance the probabili- Geese damaging reedbeds in England through ties of rapid spread of waterborne pathogens. grazing or trampling and suggestions of Duck Viral Enteritis (DVE or duck plague), for changes to water chemistry as a result of example, has been associated almost exclusively with captive- reared or non-migratory water- fowl in Europe, Asia and North America, and Mallards and Muscovy Ducks are especially susceptible (Gough 1984; Brand 1988; Brand & Docherty 1988; Gough & Alexander 1990). Sporadic outbreaks in wild waterbirds often follow contact with captive or released individuals, but asymptomatic birds can also spread the virus for years through deposition of their faeces (Burgess et al. 1979; Burgess & Yuill 1982). Thus, escapes from captivity and the release of wildfowl for hunting have the potential to promote the incidence of DVE in wild populations with potentially catastrophic effects.

Damage to agriculture and habitats The Rose-ringed Parakeet Psittacula krameri has been established in England as a breeding species for almost 40 years (Pithon & Dytham 1999;

Butler 2003). Yet, while the Kit Day spectacle of free-flying para- 437. Rose-ringed Parakeet Psittacula krameri, Kent, March 2006. Rose-ringed Parakeets are an undeniably spectacular addition to the keets is enjoyed by many, the avifauna of some parts of southeast England, whether it be as the great birds have become unnervingly flocks coming into roost at Esher rugby club or as birds seen at close numerous, to the extent that it range monopolising garden feeders. Established for almost 40 years as would be hard to eradicate the a breeding bird in England, this alien species has become unnervingly species should it become a real numerous, however, to the extent that it would be hard to eradicate should it become a significant agricultural pest or be shown to have pest to fruit production or be serious consequences for our native fauna.

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Box 3. International legislation relating to introductions of non-native species. In the UK, several international conventions and legislative instruments have something to say about aliens and the introduction of non-native species.The most important are as follows: EU Birds Directive (1979) Article 11 ‘Member States shall see that any introduction of species of bird which do not occur naturally in the wild state in the European territory of the Member States does not prejudice the local flora and fauna.’ Bern Convention (1979) Article 11 (2) Contracting parties undertake… ‘to strictly control the introduction of non-native species’. Convention on Biological Diversity (Rio 1992) Article 8 (h) Contracting parties are committed to action to… ‘prevent the introduction of, control or eradicate those alien species which threaten ecosystems, habitats or species’. African-Eurasian Migratory Waterbird Agreement (1999) Article III Contracting parties shall… ‘prohibit the deliberate introduction of non-native waterbird species into the environment and take all appropriate measures to prevent the unintentional release of such species if this introduction would prejudice the of wild flora and fauna; when non-native waterbird species have already been introduced… shall take all appropriate measures to prevent these species from being a potential threat to indigenous species’. deposition of nutrients by such geese (e.g. introductions of alien waterbirds still occur. Owen et al. 2006), but the true ecological or While there could be some interpretation financial extent of these effects, although hard needed over what constitutes ‘appropriate to measure, are probably local. measures to prevent these species from being a potential threat to indigenous species’, the Health and safety requirements on governments within the Some alien species, particularly the Canada African-Eurasian Waterbird Agreement Goose outside its native range, have been (AEWA) area are clear. The existence of these reported causing damage to amenity areas, cre- international conventions, treaties, agreements ating threats to public health in parks and water and policies are sufficient to provide a supra- areas and threats to air safety (Watola et al. national framework to prevent introductions 1996; Owen et al. 2006). However, most of these and control introduced species where these largely site-based local conflicts can potentially have become established. However, a recent be resolved by local management options, review of legislation at national and provincial rather than providing grounds for wide-scale level found this largely inadequate because few extirpation of alien waterfowl species. signatory states to international instruments incorporate their principles into their own What about legislation to help with these domestic legislation (Shaw 2006). Obviously, problems? legislation is not the only solution to the The unintentional, accidental or deliberate problem. However, given the limited resources introduction of non-native wildfowl has already of most administrations to enforce nature con- occurred in many parts of the world so, in some servation legislation under normal circum- cases, use of legislation now would be closing stances, such a legislative framework provides the stable door after the horse has bolted. Most the impetus for action by government agencies, countries in the world now have environmental and the key lever that conservationists and non- legislation designed to protect indigenous flora governmental organisations can use in critical and fauna and general biodiversity, some of situations. which specifically addresses introduced non- native forms. Hence, there are a number of How do we deal with problematic aliens once international agreements and conventions established? which oblige the UK Government to take In the continental USA, 50,000 alien species certain steps with respect to introduced wild- have been recorded as free-living, and even if fowl (Box 3), although despite such obligations only a small fraction of these cause problems, it

672 British Birds 102 • December 2009 • 660–679 What makes a good alien? is clear that the effect is potentially significant. Canada Geese from the vicinity of airports or The ‘Tens Rule’ states that only around 10% of amenity . However, where biodiver- the species that arrive will become established sity or other legislation to protect wildlife is and, of these, only about 10% will have an eco- being seriously compromised by the presence of logical effect (Williamson 1996). Non-native an alien form, clearly the problem deserves an species in the USA are thought to have con- appropriate and prompt response. In situations tributed to declines among 42% of threatened where hybrid introgression into a genome or species, also costing the economy $137 billion direct competition threatens the very existence per year (Pimentel et al. 2000). Alien or intro- and integrity of a species, this seems to be a duced non-native species are ranked as the clear case where eradication is a justified and single most important factor affecting biodiver- appropriate response to the level of threat. sity after habitat loss (Simberloff 2004). Where In 1996, the Council of Europe published a it is clear that there is a need to deal with a non- landmark set of 23 action plans for the most native form that threatens some aspect of the globally threatened bird species on the conti- native biodiversity, how can we deal with such nent, which included one for the White-headed problem aliens? The answer to this deceptively Duck (Green & Hughes 1996). Part of the simple question is ‘with great difficulty’ and in action-planning process is to consider threats the case of the Defra project to reduce the and risks to the various species, flag up the Ruddy Duck population in the UK, ‘at huge solutions and develop a prioritised set of expense’.In situations where aliens have become actions to improve on the current conservation established and there is no measurable or per- status of each of these species. The White- ceived conflict, perhaps there is no reason to headed Duck plan urged Britain to undertake a act; even so, when aliens are established at low Ruddy Duck control programme as quickly as population levels, future problems may not yet possible, starting with the regional trials and be apparent. Where there is local conflict analo- continuing to the national scale if these were gous to that inflicted by native fauna, local shown to be effective. The Bern Convention management solutions can generally be found – subsequently produced a strategy for the com- for example removing grazing non-native plete eradication of the Ruddy Duck in the Simon Stirrup 438. Male Mandarin Duck Aix galericulata, New , Hampshire, April 2007. A recent review found that the most commonly introduced species to the AEWA (African-Eurasian Waterbird Agreement) area was the Mandarin, recorded in South Africa and no fewer than 16 different European states (Banks et al. 2008).

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Western Palearctic (Hughes et al. 1999). Hence, certain as the toll taken by mink and introduced at the international level, a thorough assessment rats to offshore seabird colonies, where the of the impacts of allowing this particular alien control of ‘vermin’ is not opposed by those who to remain was undertaken, a set of prioritised prefer to see breeding seabird colonies restored actions were forthcoming and it was up to by their removal. Control of animals is national agencies to take measures to fulfil the unpleasant; even those responsible for the needs. As a result of co-ordinated international Ruddy Duck cull have had severe misgivings actions and financial support under the EU Life about shooting a non-quarry species during the Programme, 11 different states were taking breeding season when it shows little fear of action against Ruddy Ducks by 2002 and birds humans. But are we not being overly senti- have been controlled in Iceland, Belgium, mental when we object to culling introduced , , Spain, Morocco and Britain species such as the Ruddy Duck? After all, we (Hughes et al. 2006; CSL 2007). This pro- permit our cats to slaughter an estimated 25–29 gramme has been carefully researched and million birds every year (Woods et al. 2003), we planned from the outset and surely represents unintentionally kill up to 27 million birds on an appropriate (if unfortunate) response to the our roads every year (Erritzoe et al. 2003), problem in hand. Let the Ruddy Duck continue several million more birds are shot annually for to increase and the White-headed Duck would sport, and many more birds die as a direct result probably disappear as a species. This decision of various human activities without a thought. by the UK Government has been highly contro- Surely culling 1,000–2,000 Ruddy Ducks per versial and several conservation bodies have lost year for a short period is worth the effort? If we members who resigned over the organisation’s are serious about saving the White-headed support for the eradication programme. Yet the Duck, there are simply no other choices. threat from the Ruddy Duck is as real and as www.nature-photography.co.uk Mike Lane Mike 439. Female Ruddy Duck Oxyura jamaicensis, Arizona, USA, January 2009. Having quickly established a British population numbering around 6,000 birds by the end of the twentieth century, following accidental releases from the WWT headquarters at Slimbridge, the Ruddy Duck has become the subject of an intensely controversial eradication programme, designed to safeguard the Globally Threatened White-headed Duck O. leucocephala population in southern Europe.

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What makes a good alien – what determines petuating populations (Banks et al. 2008). That its distribution and abundance? certainly does not mean that they will not do so If we could predict what makes a ‘good alien’,we in the future. could perhaps identify species that are more Nonetheless, some aspects of ecology may likely to be successful and potentially destruc- help to identify the potential success of an tive in their invasiveness; in turn, it would then introduced alien. The humble Mallard, for be easier to prevent the establishment of certain example, has been widely domesticated and taxa in the first place, or be more effective in introduced throughout much of the known targeting actions once established. One sug- world with devastating consequences. It is a gested approach is to look for life-history traits species that willingly hybridises with at least that characterise rare or invasive species, con- two species of goose, 41 different duck species, sidering these types at opposite ends of a spec- fowl and even chickens (Rehfisch et al. trum (Van Kleunen & Richardson 2007). In 2006) as well as indulging in homosexual practice, however, it is very difficult to identify necrophilia (Moeliker 2001), so here surely is a what features affect the ability of an exotic to species to handle with extreme caution. As we thrive outside its normal range. For example, saw in the cases of the North American Black most ducks are relatively short-lived but have Duck Anas rubripes and the Grey Duck, the large clutch sizes (compared with geese or species is also able to adapt to opportunities swans), which in theory makes them better able from human activities on available wetland to expand their populations rapidly once first environments: loss of parkland habitat in North established into new habitats where some America and possibly the creation of pastoral feature of ecological space was unoccupied and agricultural and stock ponds in New Zealand permitted their colonisation. Yet life-history may have favoured the invasive Mallard over the traits are moulded by the very ecological native forms in two different continents. context that an organism finds itself in. The demography (i.e. the balance between survival How do we deal with the problem in the and reproductive output that determines how future? fast the population changes from year to year) We now have no excuse. We are aware of the of Canada Geese in their native North America issues raised by introduced species and we see may be very different from that in Europe, the havoc they can wreak. We are painfully where predation pressures, competition from aware of the most troublesome species and the other geese and food availability are not the enormous costs of fixing some of the problems same. By inhabiting wooded wetlands in they cause (such as the Ruddy Duck in Europe). southern England, the Mandarin exploits a food For yet others, like the Grey Duck of New resource (including acorns) and nesting Zealand, we may well be far too late to be able resources (cavities, partly enhanced by the pro- to save very much at all before a unique sub- vision of artificial nestboxes) that are free of species of bird completely disappears into a competition from other Anatidae, while in hybrid swarm where the genotype is dominated North America introduced Mandarins would by the Mallard phenotype. The fact is that when potentially suffer greater competition with dealing with established aliens, prevention is far native Wood Ducks Aix sponsa. And who would better than cure – we need to stop all further have guessed that Egyptian Geese would find an introductions of non-native forms; and, where opportunity unexploited by most birds in they have occurred, ensure that the species do feeding on the exposed faces of silage clamps? not spread. We have good information systems The freedom from competition from native in place now, including the new EU consortium forms undoubtedly has a major influence on DAISIE (Delivering Alien Invasive Inventories the demography of an invasive species, which for Europe; www.europe-aliens.org) created to may be difficult to predict from conditions in address the need to gather and integrate infor- its native range. As Colin Bibby put it ‘intro- mation on current invasions across Europe duced species have a nasty habit of being through the development of an online, peer- unpredictable’ (Bibby 2000), despite the fact reviewed database of alien species. In Britain, that relatively few of the 56 alien wildfowl the Non-native Species Secretariat is developing recorded in the UK in the last nine years have the Non-native Species Strategy, covering successfully established themselves as self-per- all taxa and launched in May 2008

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(www.nonnativespecies.org). Their work relies the process), there are interim conservation on fundamental knowledge about the nature guidelines in place to assist states in avoiding and extent of the problem, so we need to be introductions of non-native waterbirds, which, better at recording and monitoring non-native if followed, can go a long way to minimising the species in Britain to contribute to the develop- problems and for dealing with serious issues ment of these initiatives. This is the key role for when they arise (Box 4). birders, submitting counts via county bird I must end on a personal note, because I clubs, WeBS counts, atlas work or the Rare agree emphatically with the late Colin Bibby Breeding Birds Panel. Linking information on (2000) when he said that the problem of intro- the status of aliens at both country- and duced species was an important and neglected Europe-wide levels as well as globally should area of British ornithology. Quite apart from improve understanding and prediction of inva- the ecological or economic damage that they sion dynamics and help to prevent their spread may or may not do, I simply do not like to see into new areas (Pysek & Hulme 2005). We have alien species. We have seen the damage wrought some good international legislation in place to by the American Mink, Coypu Myocastor coypus do this, especially the Convention of Biological and Grey Squirrel Sciurus carolinensis and, to Diversity and, in the specific case of wildfowl me, the fact that we tolerate the presence of and the Africa-Eurasia region, AEWA, but there aliens represents the lack of care we increasingly is a desperate need for improvement when show for our natural biodiversity. They repre- translating this into domestic legislation and sent a form of litter (and in many cases self-sus- into effective action on the ground. It is clear taining, increasing litter at that), which we have that current legislation needs to be further aug- carelessly tossed into the rich natural ecosys- mented and far more strictly enforced. We must tems that are still adapting to the conditions stop escape events, whether they are accidental that have existed only since the last glaciation. or deliberate, in order to reduce the likelihood This reflects our increasing disregard for our of new aliens becoming established in the environment and our distance from nature. We future. But we must be (i) ready to eradicate have been lazy and sentimental in our attitude these escapes where their presence represents a to escapes and deliberate introductions, but we clear threat to native biodiversity and (ii) to do need to think again. The scientific and conser- so at the early stages before a population is self- vation communities have not been good at sustaining. Thanks to the great foresight of the leading public understanding of the problems UK Government and the African-Eurasian caused by non-native species. An understand- Waterbird Agreement Secretariat (who funded able lack of public support for any killing of

Box 4. Outline summary of the interim AEWA guidelines on the avoidance of introductions of non-native waterbird species (summarised from Owen et al. 2006). 1. Establish baseline information on importation, captive holdings and established free-living populations of non-native waterbird species. 2. Develop and maintain monitoring programmes to periodically revise the baseline information. 3. Undertake environmental risk assessment to establish levels of potential threat posed by each non-native waterbird species, so as to prioritise action. 4. Establish or improve legislation to prevent the deliberate introduction of non-native waterbird species and allow their control where established populations exist. 5. Introduce measures to prevent escapes of non-native waterbird species from captive collections. 6. Introduce measures to prevent the import of high-risk waterbird species, where the risk is established as a result of the risk assessment undertaken in (3) above, backing legislation with enforcement. 7. Design control strategies to limit or remove high-risk non-native waterbird species, test and report on their feasibility. Implement education programmes and raise awareness among key stakeholders, derive public support for control measures where implemented and establish monitoring systems to track success of such control measures.

676 British Birds 102 • December 2009 • 660–679 What makes a good alien? animals has also created a lack of political will persistently infected with duck plague virus. Avian to tackle the control of non-native species. At Diseases 26: 40–46. —, Ossa, J., & Yuill,T. M. 1979. Duck plague: a carrier state in least we now have the international legislation wildfowl. Avian Diseases 23: 940–949. to do something about them, even though Butler, C. J. 2003. Population biology of the introduced national legislation remains woefully inade- Rose-ringed Parakeet Psittacula krameri in the UK. Unpublished D. Phil thesis, University of Oxford. quate. We need to be vigilant and not to be Callaghan, D. A., & Kirby, J. S. 1996. Releases of Anatidae for afraid to take action to stop many of these hunting and the effects on wetland diversity – a review exotics before they get too numerous and their and evaluation. Gibier Faune Sauvage, Game and Wildlife impacts become a problem. We fail to do so at 13: 1049–1068. Central Science Laboratory (CSL). 2007.Third Ruddy our peril. Duck Eradication Bulletin, September 2007. http:// www.nonnativespecies.org/Ruddy_Duck/index.cfm Acknowledgments Clark, H. H. 1967.The origin and early history of the It was a great honour to be asked to present the Bernard cultivated barleys: a botanical and archaeological Tucker Memorial Lecture and I thank Andy Gosler and synthesis. Agricultural History Review 15: 1–18. George Candelin for their kind invitation and hospitality. Craik, C. 1997. Long-term effects of American Mink Thanks to the audience of the Oxford Ornithological Mustela vison on seabirds in western Scotland. Society and the Ashmolean Natural History Society for Bird Study 44: 303–309. enduring my presentation, but especially for contributing Crawford, R. D. 1984. Geese. In: Mason, I. L. (ed.), Evolution to the lively discussion afterwards. My thanks too go to of Domesticated Animals, pp. 345–349. Longman, Baz Hughes, John Marchant and David Stroud for their London. very helpful comments on an earlier draft, Roger Croll, D. A., Maron, J. L., Estes, J. E., Danner, E. M., & Byrd, Riddington for his encouragement and to the photo- G.V. 2005. Introduced predators transform subarctic graphers who provided images for the paper. islands from grassland to tundra. Science 307: 1959–1961. Cromarty, P.,& Scott, D. A. 1996. A Directory of Wetlands in References New Zealand. Department of Conservation,Wellington. Aldrich, J.W., & Baer, K. P.1970. Status and speciation in the Donkin, R. A. 1989. The Muscovy Duck, Cairina moschata Mexican Duck Anas diazi.Wilson Bull. 82: 63–73. domestica. Origins, dispersal, and associated aspects of Allendorf, F.W., Leary, R. F., Spruell, P., & Wenburg, J. K. 2001. the geography of domestication. Balkema, Rotterdam. The problems with hybrids: setting conservation Erritzoe, J., Mazgajski,T. D., & Rejt, L. 2003. Bird casualties on guidelines. 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