The impacts of non-native species on UK biodiversity and the effectiveness of control
Sarah J. Manchester (e-mail email@example.com).
1. The introduction of non-native species continues to cause ecological concern globally, but there have been no published reviews of their effects in the UK. Impacts in the UK are therefore reviewed, along with current legislation and guidelines relating to the introduction and control of such species.
2. A large number of non-native species have been introduced to the UK, both deliberately and accidentally, but only a small number of introduced non-native species have established and caused detrimental ecological impacts. However, general declines in UK biodiversity, and the potential effects of future climate change, may increase the susceptibility of ecosystems to invasions.
3. Detrimental impacts of non-native species on native biota have occurred through competition, predation, herbivory, habitat alteration, disease and genetic effects (i.e. hybridization). There are potential effects on genetic biodiversity as well as species biodiversity.
4. Several high profile examples highlight the technical difficulties, and financial implications, of removing an introduced species once it is established. Few UK control or eradication programmes have been successful.
5. Control might be more feasible if ‘problem’ species could be identified at an earlier stage of establishment. However, the poor success of attempts to characterize invasive species and predict which will have negative impacts highlight the individual and unpredictable nature of invasions. The difficulties of making general predictions suggest that every proposed species introduction should be subject to rigorous ecological characterization and risk assessment prior to introduction.
6. The plethora of UK legislation and guidelines developed to reduce impacts of non-native species only go part of the way towards ameliorating impact. Many species already established in the wild might cause future problems. Illegal releases and escapes of non-native species may augment feral populations or establish new colonies. While regulation of imports and releases is important, further enforcement of existing legislation and action against unlicensed releases is necessary.
For as long as humans have travelled over and between land masses, species have been transported, deliberately or inadvertently, from their native ranges to new, previously unoccupied, areas. Since the Neolithic, c. 6000 bp (Webb 1985), human migrations and trade are thought to have introduced new species to many parts of the world. However, most non-native species have been introduced into the UK since approximately ad 1500, when improved marine transportation massively increased human movements between continents (di Castri, Hansen & Debussche 1990). In addition to augmentation of the numbers of species introduced, the modes of introduction of new species became more diverse, for example as ornamental species, accidental ‘stowaways’ aboard ships, and food species. A few recent colonists of the UK have arrived spontaneously, such as the collared dove Streptopelia decaocta (Frivaldszky) (Eversham & Arnold 1992) and the fulmar Fulmarus glacialis (L.) (Williamson 1996), but most are thought to have been brought by humans.
For the purposes of this paper, terms relating to the status of a species are defined using the International Union for the Conservation of Nature (IUCN) (IUCN 1987) guidelines and the UK Committee for International Nature Conservation (UKINC) report (UKINC 1979; see also Bullock et al. 1997).
‘Native’ or ‘indigenous’ refers to a species or race that occurs naturally in an area (for this review, the UK), i.e. whose dispersal has occurred independently of deliberate human translocation. In general, a species or race thought to have occurred in an area since before the Neolithic can be considered to be native.
‘Non-native’, ‘non-indigenous’, ‘alien’ or ‘exotic’ refers to a species or race that does not occur naturally in an area, i.e. it has not previously occurred there, or its dispersal into the area has been mediated by humans (UKINC 1979; IUCN 1987; Holmes & Simons 1996). It is usually assumed that species that have colonized since the Neolithic, c. 6000 bp, are non-native (Webb 1985). In some cases, the distinction between native and non-native may not be straightforward, and often is the result of estimates of the length of time a species has been resident in the UK. For example, it not clear whether the pool frog Rana lessonae Camerano is native to the UK or has been introduced (Arnold 1995). A related issue is the distinction between non-native species introduced directly through human agency, and species colonizing through natural range expansion such as the fulmar Fulmarus glacialis. Because such species have colonized ‘naturally’, they could be considered as desirable additions to UK biodiversity. However, in some cases apparently natural colonization may have been facilitated by changes in the environment brought about by human activity.
‘Introduction’ is the deliberate or accidental release by human agency of an organism(s) into the wild by humans in areas where the species or race is not native. The term applies to translocations within the UK or into the UK from other countries.
‘The wild’ is defined as any conditions in which organisms can disperse to other sites or can breed with individuals from other populations (sensuNCC (Nature Conservancy Council) 1990).
‘Naturalised’ refers to a non-native species or race that, following escape or release, has become established in the wild in self-maintaining populations.
‘Feral’ is an organism (or its descendants) that has been kept in domestication, captivity (animals) or cultivation (plants) but which, following escape or release, now lives in the wild state. However, populations are not necessarily self-maintaining.
It is not certain exactly how many non-native species are present within the UK (Table 1), in part because estimates vary according to definitions used, and there is not complete agreement about which species are native.
Table 1. Estimates of the number of non-native species in the British Isles (England, Scotland, Wales and Ireland), Britain (England, Scotland and Wales) or individual countries
|(British Isles)||23 mammals, 24 birds, seven amphibians, three reptiles, 14 fish, 170 insects, 12 molluscs, 286 plants||Brown (1986)|
|(British Isles)||16 algae, five diatoms, one angiosperm, 31 invertebrates||Eno, Clarke & Sanderson (1997)|
|Wild (Britain)||27||Taylor (1979)|
|Naturalized (Britain)||15||Baker (1990)|
|(British Isles)||29||Marchant (1996)|
|(British Isles)||1360||Stace (1991)|
|(British Isles)||1387||Stace (1997)|
|1960–88||110 new species in this period||Rich & Woodruff (1996)|
|(England and Scotland)|
|(British Isles)||55 000 species or varieties||Nelson (1994)|
|(British Isles)||340 of 8893 species of insects and mite on the British Phytophagous Insects Data Base (Ward, Hackshaw & Clarke 1995)||L. Ward (personal communication)|
One concern about non-native species relates to their potential to cause economic losses through damage to crops or forestry. However, introductions can also have marked effects on native biodiversity. This is a global problem, particularly acute in North America (Mooney & Drake 1984), southern Africa (MacDonald, Powrie & Siegfried 1986), Australasia (Lunney & Leary 1988; Arthington 1991) and oceanic islands such as the Galapagos (Schofield 1989) and Hawaii (Mooney & Drake 1984). Specific examples include the introduced brown tree snake Boiga irregularis Merrem, which has caused range reductions and extinctions among native forest birds on the island of Guam (Savidge 1987), and the kiore Rattus exulans F., which has caused population declines, and/or extinctions, of birds, bats, tuatara, geckos, skinks, landsnails and large flightless insects in New Zealand (Atkinson & Cameron 1993). In the UK, biodiversity has not been impacted so obviously, but there are concerns nevertheless.
This paper reviews the types of non-native species introduced to the UK, the hazards to UK biodiversity arising from the establishment of non-native species, and the effectiveness of guidelines or legislation in reducing these hazards. The work is based on a broader review of species translocations in the UK (Bullock et al. 1997). The translocation of native species within the UK is outside the scope of this paper and has been reviewed previously (Hodder & Bullock 1997). The paper focuses on the effects of non-native species within Britain and Ireland, but excludes UK Overseas Territories which are dealt with elsewhere (Oldfield & Sheppard 1997).
Impacts of non-native species
Species have been introduced to the UK deliberately and accidentally (Table 2). Deliberate introductions include species used for food and other products (crops, aquaculture, timber, fur), as game, for ornamental purposes (private collections and pets), as garden plants, or for biological control. Accidental introductions have arrived in cargoes or have been otherwise carried on ships, aeroplanes or other vessels.
Table 2. Categories of introduced species in the UK, with reasons for introduction and examples
|Fish and shellfish||Angling||Competition; predation; habitat alteration; spread of disease||Grass carp Ctenopharygdon idella (Valenciennes); common carp Cyprinus carpio L.; oysters Crassostrea gigas; crayfish Astacus leptodactylus Eschscholtz and Pacifastacus lenuisculus; rainbow trout Onchorhynchus mykiss Walbaum|
|Aquaculture|| || |
|Invertebrates||Biological control||Few adverse effects||See Table 11|
|Wildfowl and game (e.g. mammals, birds, fish)||Species introduced for hunting, shooting, fishing, falconry||Herbivory; habitat alteration/damage; predation; competition; genetic impacts||Pheasant Phasianus colchicus L.; fallow deer Dama dama L.; rabbit Oryctolagus cuniculus; zander Stizostedion lucioperca|
|Birds, mammals, fish, amphibians, reptiles, plants, invertebrates, etc.||Amenity/ornamental planting; zoological/botanical/private collections||Herbivory; competition; hybridization||Pondweed: Canadian waterweed Elodea canadensis Michx; Australian swamp stonecrop Crassula helmsii|
Park and garden plants: Rhododendron ponticum; Japanese knotweed Fallopia japonica; Indian balsam Impatiens glandulifera Royle; giant hogweed Heracleum mantegazzianum; horse chestnut Aesculus hippocastanum
Aquarium/Ornamental: Goldfish Carassius auratus Gibelio; red swamp crayfish Procambarus clarkii Girard
Cage birds/wildfowl: Ring-necked parakeet Psittacula krameri (Scopoli); Mandarin duck Aix galericulata (L.); Canada goose Branta canadensis; ruddy duck Oxyura jamaicensis; little owl Athene noctua; pink-footed goose A. brachyrynchus; red-crested pochard Netta rufina
Deer park species: Muntjac Muntiacus reevesi (Ogilby); Japanese sika deer Cervus nippon nippon Temmink; North American grey squirrel Sciurus carolinensis
|Mammals fish birds, etc.||Food; pets and domestic animals; pest control||Habitat damage; predation||Cats Felis catus L.; dogs Canis familiaris L.; sheep Ovis aries L.; cattle Bos taurus L.; rabbits Oryctolagus cuniculus; goldfish Carassius auratus; Roman snail Helix pomatia L.|
|Trees||Forestry||Soil/stream acidification; reduced native diversity||European larch Larix decidua Mill.; sitka spruce Picea sitchensis (Bong.) Carr.; Douglas fir Pseudotsuga menziesii (Mirb.) Franco; sweet chestnut Castanea sativa Mill.|
|Plants||Utility plants; crop/pasture improvement||Hybridization||Most agricultural crops, i.e. maize Zea mays L., wheat Triticum aestivum L., tomatoes Lycopersicon esculentum Mill., medicinal plants. Also species introduced for pasture improvement|
|Mammals||Fur||Herbivory; predation; reduced floristic diversity||Mink Mustela vision; coypu Myocastor coypus; muskrat Ondatra zibethicus; rabbit Oryctolagus cuniculus|
|Mammals, invertebrates, algae, parasites, plants, crustaceans, disease organisms, etc.||None – accidental introductions||Competition; predation; herbivory; habitat alteration; transfer of disease||Shipping, e.g. in ballast, cargo or on the hull: crustacean Elminius modestus Darwin; black rat Rattus rattus (L.); algae |
Containerized plants: New Zealand flatworm Artioposthia triangulata; Australian flatworm Australoplana sanguinea var alba (Moseley)
With imported fish/shellfish: Alga Sargassum muticum; crayfish plague fungus Aphanomyces astaci Schikora
With imported timber: Dutch elm disease Ceratomyces ulmi
With imported bees: Bee ectoparasite Varroa jacobsoni
? Rabbit myxoma virus; cynipid gall wasp Andricus quercuscalicis Burgsdorf
Hodder & Bullock (1997) derived a set of definitions designed to describe all aspects of biodiversity and reflecting the Global Biodiversity Assessment (Hengeveld et al. 1995), and these form the basis of our assessment of impacts on biodiversity. The UK has been fortunate so far, in that the majority of recently introduced non-native species have not caused major adverse ecological impacts (Table 3; Brown & Williamson 1986; Kornberg & Williamson 1987). In fact, some charismatic non-native species, such as the little owl Athene noctua Scopoli or the horse chestnut Aesculus hippocastanum L., are now widely accepted as part of UK biodiversity. There is little evidence that introductions to the UK have led to species extinctions, as witnessed in other countries (Savidge 1987; Atkinson & Cameron 1993). On a global scale the most severe impacts of non-native species have occurred on remote islands, where the native flora and fauna is depauperate and isolated and susceptible to invasion (Drake & Mooney 1989). The biota of the UK is essentially continental in character (Pennington 1969) and native species are unlikely to be excluded throughout their whole range by non-native invaders.
Table 3. Benign or beneficial species
|Rose-ringed parakeet Psittacula krameri||Increasing since the 1960s, and is likely to become a serious crop pest, but there is little evidence that it will affect UK biodiversity (Feare 1996)|
|Slender speedwell Veronica filiformis Sm.||Widespread grassland plant introduced from the Caucasus, is not regarded as having any negative impact on native biodiversity (Akeroyd 1994)|
|Cynipid gall wasp Andricus quercuscalicis||Will have little effect on populations of host, oak Quercus robur L., despite large effects on acorn production. Does not compete with native cynipids for acorns (Hails & Crawley 1991)|
|Rabbit Oryctolagus cuniculus||Grazing of chalk downland and breckland has positive effect on native biodiversity. Extinction of the British population of the large blue butterfly Maculina arion (L.), blamed partly on declines caused by myxomatosis in the 1950s (see above). The early successional grazed habitat was replaced with taller grassland which no longer supported the butterfly (Sheail 1991). The loss of an important prey species may have affected predators such as buzzards Buteo buteo L. (Moore 1957)|
|Mandarin duck Aix galericulata and Roman snail Helix pomatia||Some non-native species subject to conservation measures in their native ranges. Ex-situ populations may represent important refugia meriting positive conservation action|
|In the past, speculated that the feral population of Mandarin duck in Britain may have outnumbered that within China (Lever 1977). More recently, estimated that the British population might number 7000 birds, three times greater than any previous estimate, and potentially at least one-third of the world population. If this were indeed the case, and the population continues to increase in Britain, conservation measures for this species should consider not only the population in its home range of the Far East, but that present within this country also (Davies 1988)|
However, certain species introduced to the UK have caused problems for biodiversity, some of which have a high profile. These include the ruddy duck Oxyura jamaicensis Gmelin, Canada goose Branta canadensis L., grey squirrel Sciurus carolinensis Gmelin, coypu Myocastor coypus Molina, North American signal crayfish Pacifastacus leniusculus Dana, zander Stizostedion lucioperca L., Rhododendron ponticum L., Japanese knotweed Fallopia japonica Houtt Ronse Decraene, Australian swamp stonecrop Crassula helmsii T. Kirk and the New Zealand flatworm Artioposthia triangulata Dendy.
The impacts of introductions on biodiversity may be categorized according to whether the introduction has had negative, positive or no impact upon native biota. Despite the apparently widely held belief that non-native species are without exception detrimental to native ecosystems (Rose 1979; IUCN 1987; Ruesink et al. 1995), they can be beneficial, for example when used for land reclamation (Daehler & Gordon 1997). Negative impacts may be further categorized according to the mechanism by which species are affected. For example, competitive impacts arise when non-native invaders and native species compete for resources (Table 4). Herbivores may directly affect plant populations through grazing and trampling, and have indirect effects by altering habitat (see below) (Table 5). Non-native species may predate upon native species, or themselves be predated upon, for example where high densities of farmed fish attract predators and scavengers (Table 6). Introduced species may be parasites or pathogens (Table 7). Alteration of habitat form or function, such as alteration of water table, fire regime, soil properties or vegetation structure, can make habitats unsuitable for native species (Table 8).
Table 4. Negative impacts of non-native species on UK biodiversity: competition
|Long-clawed or Turkish crayfish Astacus leptodactylus, North American signal crayfish Pacifastacus leniusculus||White-clawed/Atlantic stream crayfish Austropotamobius pallipes (Lereboullet)||Introduced species expanding its range, often into waters previously occupied by the native species (Holdich & Reeve 1991) which is then often eliminated through competition (Hobbs, Jass & Huner 1989)|
|Rhododendron ponticum||Woodland, grassland, heath||Invasions into oak Quercus petraea (Matt.) Liebl. and holly Ilex aquifolium L. woodland may inhibit native woodland regeneration (Usher 1987; Thomson et al. 1993). Lowland heath vegetation and soils changed enormously by invasion (Mitchell et al. 1997)|
|Giant hogweed Heracleum mantegazzianum; Japanese knotweed Fallopia japonica; Indian balsam Impatiens glandulifera; Australian swamp stonecrop Crassula helmsii||Native flora||Prolific vegetative growth (Dodd et al. 1994). Form dense stands that shade out and replace native flora (Beerling, Bailey & Connolly 1994; Beerling & Perrins 1993; Dawson & Warman 1987)|
|North American grey squirrel Sciurus carolinensis||Red squirrel Sciurus vulgaris L.||Red replaced by grey over much of former range (Usher, Crawford & Banwell 1992; Lurz, Garson & Rushton 1995). Grey have feeding advantage in deciduous woods (Gurnell 1983, 1989) possibly due to better ability to tolerate phytotoxins in acorns (Kenward & Holm 1993)|
|Seaweed Sargassum muticum||Native coastal species||Has spread quickly along south coast of England (Eno, Clarke & Sanderson 1997). Likely to displace native species, as it is does on French Atlantic coast, e.g. Laminaria saccharina (L.) Lamour, Zostera marina L.|
Table 5. Negative impacts of non-native species on UK biodiversity: herbivory
|Canada geese Branta canadensis||Reed bed, saltmarsh and other vegetation||Damage by overgrazing (Wattaola, Allan & Feare 1996)|
|Muskrat Ondatra zibethicus; coypu Myocastor coypus||Reed swamps||Damaged reed swamps in the Norfolk Broads by grazing before elimination (Boorman & Fuller 1981; Gosling & Baker 1989).|
|Fallow deer Dama dama||Woodlands||Grazing damages coppice regrowth in woodlands (Kay 1993)|
|Muntjac Muntiacus reevesi||Woodlands||Grazing mainly impacts vegetation (Chapman, Harris & Stanford 1994). Indirect effects on invertebrates (Pollard & Cooke 1994)|
|Cynipid gall wasp Andricus quercuscalicis||Oak Quercus robur L.||Production of the ‘knopper gall’ on acorns of Quercus robur can reduce fecundity. Long-term effects on oak populations unknown (Hails & Crawley 1991)|
Table 6. Negative impacts of non-native species on UK biodiversity: predator effects
|Zander Stizostedion lucioperca||Native fish species, particularly in eastern England||Can cause substantial population reductions of native fish, particularly where there is a reduced diversity of prey species, i.e. all UK waters containing zander (Maitland & Campbell 1992; Hickley 1986)|
|Feral mink Mustela vison||Water vole Arvicola terrestris (L.); native birds, mammals and fish along waterways||Impacts some waterbird species but magnitude of effects on many species unknown (Woodroffe, Lawton & Davidson 1990; Ferreras & Macdonald, 1999). Significant inverse correlation between mink, and water vole, activity. Probable that in the long run mink will depress water vole numbers|
|New Zealand flatworm Artioposthia triangulata; Australian flatworm Australoplana sanguinea var alba||Earthworms||May reduce earthworm populations to undetectable levels, thus impacting soil processes (Cannon et al. 1999)|
|Attraction of predators|
|Farmed non-native fish||Tern Sterna spp.||Tern breeding colonies in Scotland displaced from sea loch islands by gulls attracted to farmed fish (Beveridge, Ross & Kelly 1994)|
|Farmed non-native fish||Wild fish stock||Shags Phalacrocorax aristotelis (L.) attracted to fish farms. Most fish eaten near the farms were wild native species that congregated around the fish cages (Carss 1993)|
Table 7. Negative impacts of non-native species on UK biodiversity: parasites and pathogens
|Bee ectoparasite Varroa jacobsoni||Native bees||Causes large declines in commercial hives. May affect native bee species (Oldroyd 1999; Pearce 1998). Plant species may be indirectly affected by declines in pollinators (Allen-Wardell et al. 1998)|
|Pathogenic fungus Aphanomyces astaci (crayfish plague)||Atlantic stream crayfish Austropotamobius pallipes||North American signal crayfish Pacifastacus leniusculus (plague vector) immune to effects of fungus, but European, Asiatic or Australasian crayfish susceptible (Holdich & Reeve 1991). Outbreak of the disease in a population may quickly lead to complete mortality (Soderback 1995). Many indigenous British crayfish populations eliminated by plague and sites in Ireland have been affected (Holdich & Roger 1997)|
|Myxoma virus Myxomatosis cuniculi||Rabbit Oryctolagus cuniculus||First reported outbreak in 1953 caused nearly 100% mortality (Armour & Thompson 1955). Effects now decreasing: virus strains currently in Britain less virulent than original strains; genetic resistance to virus detected in wild in 1970, and increasing (Trout et al. 1992)|
|Dutch elm disease fungus Ceratocystis ulmi||Elm trees Ulmus spp.||Spread by beetles of the genus Scolytus, or through roots of adjacent trees. Greatly reduced numbers of elm trees in much of England and Wales. Indirectly affected invertebrates dependant on elm, and many farmland birds (Osborne 1985)|
Table 8. Negative impacts of non-native species on UK biodiversity: habitat alteration
|Common carp Cyprinus carpio and goldfish Carassius auratus||Native species||Bottom-feeding fish increase water turbidity by churning sediment while feeding (Richardson & Whoriskey 1992)|
|Grass carp Ctenopharygdon idella; red swamp crayfish Procambarus clarkii||Macrophytes/reed beds and dependent species||Cause extensive damage to macrophytes. Completely remove submerged vegetation and reed beds in some places (Stott 1974; Crivelli 1995)|
|Non-native conifers/plantations||Aquatic freshwater biota||Planting on poorly buffered acid/acid-sensitive soils partly blamed for increased acidification of uplands. Subsequent felling generates more acidic stream water (Neal et al. 1992)|
|Coypu Myocastor coypus and muskrat Ondatra zibethicus||Aquatic and riparian fauna and flora||Caused extensive damage to watercourses and riverbanks by burrowing (Sheail 1988; Gosling & Baker 1989)|
Finally, genetic impacts may arise through hybridization of non-native species with related native species (Table 9). The change in genetic constitution and in phenotype can be considered a loss in biodiversity, while hybridization may affect the adaptedness of native species to the local environment. Genetic effects may be caused indirectly through fragmentation and reduction in the abundance of native populations, leading to a loss of genetic variation due to genetic bottlenecks. Examples of hybridization have been more frequently reported for species of birds, although fish, mammals and plants may also be affected.
Table 9. Negative impacts of non-native species on UK biodiversity: genetic
|White-headed duck (in Spain) Oxyura leucocephala||Ruddy duck Oxyura jamaicensis||Hybridization with western Europe's most important breeding population of white-headed duck may lead to genetic introgression and extinction of white-headed (Hughes 1996)|
|Wild fish populations||Farmed fish||Hybridization may introduce maladaptive genes to wild populations, possibly leading to introgression of gene pools and subsequent inbreeding (Beveridge, Ross & Kelly 1994; Ferguson, Danzmann & Allendorf 1988; Leary et al. 1984)|
|Red deer Cervus elaphus L.||Japanese sika deer Cervus nippon nippon||Genetic integrity of Scottish mainland red deer threatened by the continued range expansion, and continuing hybridization with, sika deer (Abernethy 1994)|
Predicting invasiveness and invasibility
Of established non-native species in the UK, only 8·5% of vertebrates, 6·5% of insects and 13·6% of plants were described as having pest status by Brown (1986). Williamson's (1992, 1993) ‘tens rule’ (see below) suggests that only about 10% of established non-natives are invasive and may become pest species. However, it is not clear what proportion of these species actually do cause nature conservation problems, as ‘pest’ status generally reflects potential to cause economic losses rather than impacts on biodiversity. Whatever the figures are, it is clear that most established non-native species have no significant effect on UK fauna and flora. This may be partly because many species are uncommon and have established over only small areas.
Williamson's (1992, 1993) tens rule suggests that 10% of non-natives imported into a region appear in the wild, 10% of these establish, and 10% of the establishing species, i.e. 0·1% of imported species, are invasive. This rule of thumb holds in Great Britain for angiosperms (Williamson 1993) and pines (Williamson & Fitter 1996a), and in other groups in other parts of the world (Lonsdale 1994; Williamson & Fitter 1996b). However, to achieve these fits, Williamson (1996) took 10% as being 5–20%, giving a 64-fold variation in the predicted proportion of introduced species that become invasive (0·0125–0·8%). In addition, there are a significant number of cases for which the tens rule does not hold (Williamson & Fitter 1996b; Williamson 1996). Nevertheless, the rule reflects the fact that only a small proportion of introduced species establish in the wild.
Characteristics of successful invaders
There have been several attempts to determine the characteristics of a successful invader (Williamson 1996). Morphological, physiological and life-history traits might predict the probability of a non-native species becoming more or less invasive when introduced to a new region. Williamson & Fitter (1996a) found the only differences between native species and non-native invaders in the British flora were that the non-natives were larger (height, spread, leaf area index) and had an earlier age at first flowering. Crawley, Harvey & Purvis (1996) carried out a more sophisticated analysis, again comparing native and non-native British plants, but found only that the latter were taller, had larger seeds and more protracted seed dormancy. These analyses are of limited relevance because they compare native with successful non-native species. A better test might be to compare invasive and non-invasive non-native species. Rejmanek & Richardson (1996) carried out such an analysis by comparing invasive and non-invasive pines (in the genus Pinus) in the USA and found that the former had greater seed mass, faster growth and more frequent seeding.
Ehrlich (1986) reported that successful vertebrate invaders are likely to be vagile species, generalist in their feeding habits, with short generation times, high population genetic variation and the ability to function in a wide range of physical conditions. O'Connor (1987) found that successful bird invaders in Britain tended be species with a larger clutch size and lesser propensity for long-distance migration than unsuccessful invaders. For insects, Lawton & Brown (1986) reported that size was related to the probability of successful invasion, but the relationship was too weak to be of predictive value. Simberloff (1989) could make no generalizations about the invasive potential of insect species.
Given the lack of clearly identifiable characteristics associated with the property of invasiveness, could other predictors be used? It has been suggested that an invasion will only be successful where the climate of the region being invaded is similar to that of a species' native region. However, both Williamson (1996) and Mack (1996) found as many exceptions to this rule as there are supporting cases. It is possible that genetic and breeding characters, such as inbreeding, asexuality, polyploidy or heterozygosity, are related to invasiveness. However, invaders of the British flora are not characterized by particular genetic characteristics (Gray 1986). Williamson (1996) concluded that genetic studies offered no generalities of predictive use. Species that are more abundant and have a larger range in their native region might be expected to be more invasive, because these parameters can be seen as a surrogate for wide ecological amplitude or good dispersal. Williamson (1996) reported some evidence to support this hypothesis, but concluded that it does not have good predictive potential.
Finally, certain families (e.g. the Poaceae and Asteraceae in plants) and genera (e.g. Bromus, Cirsium, Poa) contain a majority of the world's problem species (Mack 1996). Because related species share traits, species from these taxa might be expected to be more invasive than species from other taxa. A similar idea is that if a species has been a successful invader of a region then its congenerics might be invasive as well. Mack (1996) and Williamson (1996) reported that there are too many exceptions for these to be useful rules.
Determinants of community invasibility
Ecologists have been more successful characterizing communities in terms of their invasibility, i.e. their susceptibility to colonization by non-native plant species. It is widely accepted that disturbed habitats, such as urban wasteland, arable fields and riverbanks, are generally more readily invaded (Smallwood 1994). Conversely, undisturbed natural and semi-natural communities tend to contain few, if any, recently introduced invasive non-native species. Thus plant communities may be ranked in terms of their invasibility, based upon the proportion of bare ground and on the frequency and intensity of soil disturbance (Crawley 1987). The length of time that has elapsed since the last major disturbance, i.e. the successional age of the site, will also influence the alien flora (Crawley 1987). Thus, disturbed urban sites tend to have a higher proportion of non-native species than unmanaged native woodland. Drawing upon the evidence of pine invasions, Richardson, Williams & Hobbs (1994) found that the most widespread invaders were those with attributes allowing populations to persist in habitats subjected to frequent disturbance.
All ecological communities are invasible to some extent and can be ranked accordingly (Crawley 1987; Usher et al. 1988). The rate at which plant communities are invaded will also be determined by biogeographic factors, such as the size of the available pool of non-native species and the rate of population immigration. This in turn will itself depend upon the isolation of the site and the size of the target community (Crawley 1987).
Inability to predict invasions
It is not possible to arrive at general conclusions about links between species' attributes and invasive ability. While there is some information on the susceptibility of different habitat types to invasion, predictions of precisely which habitats will be invaded, by which species, and which of those habitats will be most affected by such invasions, cannot be made with any degree of certainty. This suggests that only a detailed ecological study of a species and its potential habitats can allow accurate prediction of the invasiveness of an introduced species (Crawley 1987; von Broembsen 1989; Simberloff 1989; Ruesink et al. 1995; Williamson & Fitter 1996b; Mack 1996; Williamson 1996). This was the general conclusion of the SCOPE (Scientific Committee on Problems of the Environment of the International Council of Scientific Unions) programme on biological invasions (Kornberg & Williamson 1987; Drake & Mooney 1989).
Regulation of the release of non-native species
A number of pieces of UK legislation directly concern the keeping, release and control of non-native species, reflecting European Community (EC) legislation and international agreements, notably the EC Habitats Directive, the Convention on Biological Diversity and the Bern Convention. However, contrary to many international statements, introductions are regulated rather than prohibited under UK law (Table 10). The most important piece of legislation is the Wildlife and Countryside Act 1981 [enforced in Northern Ireland under the Wildlife (Northern Ireland) Order 1985]. Under Section 14 of this Act, it an offence to release or to allow to escape into the wild any animal ‘of a kind’ that is not normally resident in or is not a regular visitor to Great Britain or Northern Ireland in a wild state (Department of the Environment 1997). However, the release of non-native plants in general is not prohibited. In addition, there are non-native plant and animal species that have become widely established in the UK (i.e. that are normally resident) that it is nevertheless illegal to release or to allow to escape in order to prevent increased numbers of these species in the wild. The species are listed in Schedule 9, which is revised regularly and at the moment comprises 12 mammals, 15 birds (excluding three native species; Hodder & Bullock 1997), three reptiles, seven amphibians, six fish and four invertebrates. Also on the Schedule are two non-native vascular plant species and eight non-native marine algae, which it is an offence to plant or cause to grow in the wild. Again, these are species that have established in the wild in the UK.
Table 10. UK Legislation relevant to non-native species
|Fish Health Regulations 1992|
|Fish Health (Amendment) Regulations 1997|
|Fish Health Regulations (Northern Ireland) 1993||To prohibit the import of live or dead fish or shellfish (Mollusca or Crustacea), their eggs or gametes, from zones within the EC not approved as free of certain diseases. Imports must be licensed and licensing conditions by MAFF (1999) lay down rules aimed at preventing the transfer of diseases of fish, molluscs and crustaceans in aquaculture|
|The Shellfish and Specified Fish (Third Country Imports) Order 1992||Similar function as the Fish Health Regulations, but for imports from outside the EC|
|Control of Pesticide Regulations 1986||Covers releases of alien fungi, viruses, bacteria, protozoa and other micro-organisms as biological control agents. MAFF (and its equivalents) license the releases of such organisms, and have arranged that applications for releases will be seen by ACRE (who advise on releases of alien animals and plants) prior to advising MAFF|
|Destructive Imported Animals Act 1932||(Amended by the Destructive Imported Animals Act 1932 (Amendment) Regulations 1992) Further restricts the import (rather than release) and keeping of certain mammals, e.g. muskrats, coypus, grey squirrels, minks, Arctic foxes and ‘non-indigenous rabbits’. MAFF may license imports for research or exhibition|
|Zoo Licensing Act 1981|
|Dangerous Wild Animals Act 1976||These both require precautions against the escape of captive non-native species considered to be dangerous to humans|
|Animal Health Act 1981||MAFF, or equivalent, can make orders to prevent introduction of disease through import of animals, carcasses, eggs or other animate or inanimate entity by which disease may be transmitted. Aimed at domesticated animals, but could be used to control imports of wild animals|
|The Import of Live Fish (Scotland) Act 1978|
|Import of Live Fish Act 1980||Specific regulations for fish imports. The Secretary of State can make orders prohibiting, or requiring licences for the import, keeping or release of live fish or fish eggs of alien species which may harm the habitat, compete with or prey on freshwater fish, shellfish or salmon Salmo salar L. The statutory conservation agencies are consulted before such orders are made|
|Fisheries Act (Northern Ireland) 1966||Empowers the Department of Agriculture of Northern Ireland to prohibit the introduction, unless under permit, into certain waters of fish species detrimental to that fishery|
|Plant Health Act 1967|
|Plant Health (Great Britain) Order 1995||These regulations are designed to control pests and diseases of agricultural, horticultural and forestry plants, but the legislation can cover wild plants also. MAFF, the Secretaries of State in Scotland and Wales and, for matters relating to forestry, the Forestry Commission are given powers to prevent or control plant pests (harmful insects, bacteria, fungi, plants, animals and all agents causative of transmissible disease). Powers include removal, treatment or destruction of infected plants or seeds, prohibition of keeping live pest individuals, prohibition of import of pests; powers of entry and inspection.|
|Control of Pesticides Regulations 1986||Replaced by Plant Protection Products Regulations 1995|
Licences can, however, be issued to permit release of a prohibited non-native species. Applications for releases of non-native species are assessed, appraising the risks associated with the release based on a simple risk assessment of the likelihood of certain harmful incidents occurring as a result of the release (negligible, low, moderate or high) and the potential amount of harm occurring as a consequence (negligible, low, medium or severe). Such assessment is based on information about the biology of the species involved and the circumstances of the release. Assessments examine such factors as the persistence of the species in the wild, competitive advantages over native species, effects on non-target prey or hosts, potential to invade other communities and ability to show rapid population increase.
Standard licences for release are issued with conditions, allowing the release of a single species or race into one or more named sites only for a specific named purpose. Other conditions usually include freedom from disease, need to notify the Secretary of State of spread outside of the release site, and use only of the donor sites named in the application. The licences are always for limited periods of time (usually several months), after which releases cannot continue without a further licence and, unless explicitly allowed in the licence (e.g. when a release is to establish a self-sustaining population), the released organism(s) must be removed. The most common reason for release is for use in biological control (Table 11).
Table 11. Outcomes of recent applications to the Department of the Environment for release of non-native organisms in the UK. Taken from the Newsletter of the Advisory Committee on Releases to the Environment (website http://www.environment.detr.gov.uk/acre/news.htm). In some cases the Latin name for the species was not given
|Fallopia japonica (Japanese knotweed)||1995||Experiment||Yes|
|Predatory fly||1995||Insect control||No (insufficient information to assess risk)|
|Bombyx mori L. (silkworm)||1996||Not given||Yes|
|Chinese praying mantis||1996||Not given||No (risk from establishment in the wild)|
|Glis glis L. (fat dormouse)||1996||Experiment||Yes|
|Danaus plexippus L. (monarch butterfly)||1996||Filming||Yes|
|Amblyseius degenerans (Berlese) (predatory mite)||1996||Thrips control in greenhouses||Yes|
|Macrolophus caliginosus Wagner (predatory bug)||1996||Whitefly control in greenhouses||Yes|
|Amblyseius californicus (McGregor) (predatory mite)||1997||Whitefly control in greenhouses||Yes|
|Delphastus catalinae (Horn) (predatory beetle)||1997||Whitefly control in greenhouses||Yes|
|Rhizophagus grandis Gyll (predatory beetle)||1997||Control of spruce bark beetle Dendroctonus micans Kug. in spruce woods||Yes|
|Muntiacus reevesi (muntjac)||1997||10 licences to release Hospitalized deer||Yes|
|10 cricket species||1997||Not given||No (not given)|
|Glossina palpalis Robineau Desvoidy (tsetse fly)||1997||To test radar tracking (flies were disease free and mouthparts were removed)||Yes|
|Triturus carniflex (Laur.) (Italian crested newt)||1997||Re-release of captured animals during study of impacts on native newts Triturus cristatus (Laur.)||Yes|
Problems with uk legislation concerning introductions
The Wildlife and Countryside Act 1981 does not make provision for compulsory pre-introduction testing of potential environmental impacts of introduced species. This type of screening provides a great deal of relevant information, and may be essential to assess fully the risks of some proposed introductions (IUCN 1987). Current procedures make use of existing information only.
The EC Birds and Habitats Directives, the Bern Convention and the Convention on Biological Diversity all make statements concerning the introduction of non-native species, with no taxonomic restrictions. However, while the Wildlife and Countryside Act 1981 and the Wildlife (Northern Ireland) Order 1985 prohibit the release of any animal not ordinarily resident in the UK, they make no general provision against the release of non-native plant species. The only specific provisions in UK law against the introduction of non-native plants are the short lists of named plant species in Schedule 9. There is no good conservation reason for this omission; non-native plants pose no less a threat than animals. There is a massive influx of non-native plant species to the UK, mostly from horticultural, forestry and agricultural imports. New cultivars and species of crop and forestry plants are being introduced with no controls with respect to conservation, whereas genetically modified crop plants are subject to strict controls by virtue of the molecular techniques used, rather than any greater potential for harm from such plants.
Schedule 9 species
Certain non-native animal species have established breeding populations in the wild but are not on Schedule 9. The barnacle goose Branta leucopsis (Bechstein), greylag goose Anser anser (L.), snow goose A. coerulescens (L.), pink-footed goose A. brachyrynchus Baillon and red-crested pochard Netta rufina Pallas are considered to be on the brink, or have started, forming feral populations in the UK and these might need to be scheduled (Holmes & Simon 1996).
Enforcement of the Wildlife and Countryside Act 1981
There are a large number of illegal releases or escapes from private collections of non-native species in the UK. This problem is especially well documented for birds (Holmes & Simons 1996). While imports or releases applied for under the Wildlife and Countryside Act 1981 are well regulated, enforcement of relevant legislation against unlicensed releases is poorly implemented. Holmes & Simons (1996) point out that there is great confusion over the interpretation of the Wildlife and Countryside Act 1981, and this contributes to a reluctance to enforce the Act.
Control of non-native species
The EC Habitats Directive and the Convention on Biological Diversity both require control of non-native populations. While it is an offence to release, or allow to escape, the species listed in Section 14 of the Wildlife and Countryside Act 1981, there is no explicit requirement for their control in the wild. In fact, other provisions of the Act (i.e. Section 1) mean that once a bird is viewed as ‘ordinarily resident’ in Great Britain it is protected, although this applies only to birds and not to other animals. Similar problems could apply to the control of resident non-native plants, as there is a general prohibition in the Wildlife and Countryside Act 1981 against uprooting any wild plant.
At this time accidental introductions are an unquantified, but probably major, source of non-native species and are also the most difficult to regulate. Eno, Clarke & Sanderson (1997) stated that most introductions of non-native marine algae and invertebrates into the UK have been unintentional. It is likely that the proportion is lower for other species, especially vertebrates, but it is probably still high for terrestrial plants and invertebrates. Problem non-native species that have come into the UK through accidental importation include the varroa mite Varroa jacobsoni (Oudemans), which probably arrived on imported bees (Oldroyd 1999), New Zealand flatworm Artioposthia triangulata, which probably arrived in containerized plants (Cannon et al. 1999), Dutch elm disease Ceratomyces ulmi Ellis & Halst., which was introduced in imported timber (Osborne 1985), and the alga Sargassum muticum (Yendo) Fensholt, which arrived in commercial introductions of oysters Crassostrea gigas (Thunberg) (Eno, Clarke & Sanderson 1997). Most accidental marine introductions are carried on the hulls or in the ballast of ships, or as contaminants of cargo (Eno, Clarke & Sanderson 1997).
IUCN (1987) guidelines expressed concern over accidental introductions, especially to islands and isolated habitats, and stated that many accidental introductions are avoidable. For instance, better seed cleaning has reduced the incidence of weed seeds in imported grain, and increased vigilance during packing and transport of cargo might lead to early removal of stowaways. The International Maritime Organisation (1993)‘Guidelines for preventing the introduction of unwanted aquatic organisms and pathogens from ships’ ballast water and sediment discharges' deals specifically with the introduction of aquatic plants, animals, disease bacteria and viruses in ballast water. Possible procedures include ensuring that only clean ballast water and a minimal amount of sediment is taken on to a ship, and that contaminated ballast water is not released except into disposal or treatment facilities; ballast water is sampled before discharge into sensitive areas, and ships' crews and other relevant persons are well-informed.
The guidelines were drafted to advise governments of the appropriate measures to take against such discharges, but the UK Government has not implemented these measures. Even for those taxa covered by the Wildlife and Countryside Act 1981, which also prohibits accidental release (i.e. ‘allow to escape’), enforcement is difficult with no specific protocols in place. de Klemm (1996), in a review of legislation in European countries, addressed accidental introductions in detail and proposed a wide range of legal measures to decrease the risk of such accidents.
Guidelines for the release of non-native species
In addition to legislation, some UK and international conservation organizations have developed position statements and guidelines relating to introductions (Appendix 2). However, these policies and guidelines are not currently implemented by law and represent, at best, agreed codes of conduct. Until recently the UK statutory conservation agencies (English Nature, Scottish Natural Heritage and the Countryside Council for Wales) have not had policy documents on introductions. The Joint Nature Conservation Committee (JNCC; the joint forum of the three statutory agencies) has been developing its own policy following review of the present situation (Bullock et al. 1997). The forerunner of the three statutory conservation agencies, the Nature Conservancy Council (NCC), conducted an internal ‘Review of NCC policy on species translocations in Great Britain’ (NCC 1990), but this was not adopted formally and has not been published. Discussion documents, e.g. Stubbs (1988) and UKINC (1979), suggesting what such a policy should contain, have been published. International guidelines have been adopted by IUCN and these are contained in the IUCN (1987)‘Position statement on translocation of living organisms’. For licensing purposes the UK's statutory agencies take the IUCN guidelines as a basis for policy.
The guidelines suggest that intentional introduction of non-native species should only be considered if clear benefits to humans or natural communities can be foreseen and if no native species is considered suitable for the purpose for which the introduction is being made. Introductions should not be carried out into habitats not already perceptibly altered by humans, for example islands, lakes, seas, oceans, centres of endemism or any semi-natural habitat, unless there are exceptional reasons for doing so. Introductions into habitat created by humans (for example arable land, ley grassland, forest plantations or other predominantly monocultural systems) are permissible following assessment of effects on surrounding semi-natural or natural habitats.
The IUCN (1987) guidelines state that planning of an introduction should involve assessment of the probability of an increase in numbers of the introduced species to a level that damages the environment, and the probability of invasion into other habitats. Plans should also consider how the introduction will proceed during all phases of the biological and climatic cycles of the area of release; the capacity of the non-native species to affect native species by breeding with them; whether the non-native is host to diseases or parasites that can spread to other species in the area of release; and the probability of a negative effect on the continued existence or stability of native populations through predation, competition or other means. The methods for control of the introduced species (if needed) should be investigated and subjected to risk analysis. No introduction should be made for which no acceptable control is possible. The environmental, aesthetic or economic benefits of the introduction should be compared to the possible disadvantages. A controlled experimental introduction should be made, in which the same stock should be used as that to be introduced extensively; the organisms should be free of diseases or parasites that could spread to other species; the performance of the introduced species and its affects on other species should be measured; and the suitability of the introduction should be reassessed in the light of the results. Finally, the extensive introduction should be closely monitored and arrangements made to restrict, control, or eradicate the species if necessary.
The IUCN (1987) guidelines also state that where non-native species are already present, those of no apparent benefit to humans and with negative environmental effects should be eradicated. Priority areas for eradication of such species are islands with a high percentage of endemics, centres of endemism, areas with high species diversity or other ecological diversity, and areas in which a threatened endemic is negatively affected by the non-native species.
Control of non-native species
Although the evidence suggests that only a small proportion of non-native species cause adverse effects, the risk of damage in some cases makes a precautionary approach advisable. Of added concern are the possible future effects of non-native species. The general decline in UK biodiversity (declines in species number and abundance, disruption and loss of semi-natural communities, habitat loss and fragmentation, etc.) may render ecosystems more susceptible to adverse effects of introductions of non-native species in the future. Climate change may bring about more specific increases in the risks from non-native introductions, as conditions become better suited to introduced species that are not currently affecting biodiversity to a great degree (Hill et al. 1994). For example, predicted rises in temperature may permit many species to increase their ranges.
The biodiversity of the UK should not be the only concern. For example, the main threat from the ruddy duck Oxyura jamaicensis is that it hybridizes with the white-headed duck Oxyura leucocephala (Scopoli), which is not found in the UK but is a native species of conservation interest in continental Europe (Hughes 1996). However, the UK still has the largest ruddy duck population (an order of magnitude larger than that on continental Europe) and is the major source of colonists into Europe. Likewise, the New Zealand flatworm Artioposthia triangulata might spread from the UK to other European countries, where it could have great effects on native biodiversity (Cannon et al. 1999). It is therefore important to develop effective control strategies that can be used if necessary.
There have been relatively few successful control/eradication programmes against problem species (see below), and certainly not against species targeted solely because of their negative impacts on biodiversity. Control measures are generally not implemented until a species becomes a problem, by which stage they are very expensive and require extensive research into the ecological, economic and political aspects of the problem. More proactive approaches would be more effective.
Baker (1990) states that many problem species of naturalized mammals have been expensive to eradicate or control and, indeed, most attempts to remove such introduced species have failed. For example, the attempt to eradicate mink Mustela vison Schreber in the UK was abandoned in 1970 after only 5 years (Thompson 1971). Research into the control of rabbits Oryctolagus cuniculus L. found no successful or acceptable means of wide-scale control (Sheail 1991). Myxomatosis appeared to be a method for the complete extermination of the rabbit, but some individuals survived infection and, following an initial crash, population numbers have recovered. The coypu Myocastor coypus and muskrat Ondatra zibethicus L. were eradicated by control programmes following assessments of the effort required, the costs involved and the likely chances of success (Gosling & Baker 1989). Control was only possible because populations were confined to reasonably small areas of Britain with no immigration from elsewhere (unlike mink and rabbits). Moreover, the Ministry of Agriculture, Fisheries and Food (MAFF) provided sufficient funds for the eradication of coypu because of the agricultural damage being caused rather than to prevent ecological damage.
A variety of methods has been used in attempts to control the Canada goose Branta canadensis in the UK, but all present problems (Owen 1990). Egg collection is time consuming. Poisoning would be very effective but would be unpopular with the general public on a large scale. Increased shooting on wintering grounds could be used, but Canada geese are not popular targets for shooters. In addition, geese are often concentrated in protected areas. Wildfowling on such legally protected sites is seen as a potentially damaging operation. While existing levels of shooting activity are likely to be acceptable as they are in accordance with traditional practice, any increase would contravene the provisions of the Wildlife and Countryside Act 1981 (Owen 1990).
Control of the ruddy duck Oxyura jamaicensis is a more urgent priority, as it is still spreading and the threat to the white-headed duck Oxyura leucocephala is severe (Hughes 1996). National and international working groups have called for its control. However, while some organizations have proposed that shooting during the breeding season would be a viable method, others dispute this (Hughes 1996). A White-headed Duck Task Force, comprising UK government departments and conservation organizations, has recommended that a trial of methods to control ruddy duck, including shooting and trapping, should be initiated (http://www.wildlife-countryside.detr.gov.uk/whd/index.htm).
Control of plants is also problematical. Rhododendron ponticum control would require large-scale clearance, followed by spraying of regrowth. An estimate of the cost of a rhododendron control programme in the Snowdonia National Park by Gritten (1995) suggested that the initial clearance and follow-up spraying programmes would cost about £42 million (1992 prices). Dispersal of another non-native invasive plant, the giant hogweed Heracleum mantegazzianum Somm. Et Lev., is almost entirely by seed and so a control programme would need to prevent plants setting seed (Dodd et al. 1994). Due to extensive seed banks and possible long-term viability of seeds, any control programme would need to have follow-up monitoring and control for at least 7 years after the initial control measures using herbicide or cutting. The plant could be eradicated if a committed and co-ordinated control programme, using appropriate techniques, was implemented (Dodd et al. 1994; Collingham et al. 2000). Effective control of Japanese knotweed Fallopia japonica requires that rhizomes, as well as individual plants, are killed. There are very few examples of eradication of this plant, and successful control requires perseverance (Gritten 1988; de Waal 1995).
Every proposed introduction of non-native species to the UK should be assessed carefully, using a case-by-case approach to risk assessment. This is clearly necessary because of the existing risk of adverse ecological impacts of non-native species, the potential for increased risk due to future climate or other environmental change, the difficulty in naming the distinguishing characteristics of a potentially invasive species, and the problems of control.
This approach is characterized in the phrase ‘guilty until proved innocent’, which was applied by Ruesink et al. (1995) to non-native species. While some organizations oppose introductions outright, others provide guidelines on good practice. The conservation organization guidelines covering the introduction of non-native species are thorough, and suggested assessment procedures, such as those given by the International Council for the Exploration of the Sea (ICES) (1995) and IUCN (1987) (see Appendix 1), should be followed closely to ensure that harmful organisms are screened out before introduction. The information requirements for licences to release, market or keep in uncontained conditions (i.e. with the risk of escape to the wild) non-native species under the Wildlife and Countryside Act 1981 are similar to these (Department of the Environment 1997).
Assessment of the potential impact of an introduction on native biota requires a thorough understanding of the biology and ecology of each candidate for introduction, together with knowledge of the native species at the receptor site and in the UK. Risk assessments should consider the potential for escape of the non-native species from the receptor site; the potential for the non-native to establish and spread in the wild; assessments of likelihood and consequences of hybridization with native species; ecological consequences of establishment and spread in the wild; and potential for control and risk management.
The fact that it is hard to make general predictions about the characteristics of a successful invader indicates that future research should concentrate more on specific cases rather than the investigation of general theories. This approach was proposed by Gilpin (1990) in a review of the synthesis of the SCOPE programme on biological invasions (Drake & Mooney 1989). However, generic work, such as that by Williamson & Fitter (1996a,b) and Williamson (1996), should continue in order to pursue possibilities for a predictive approach. Research on specific cases should address the potential risk of proposed introductions according to guidelines for risk assessment from NCC (1990), IUCN (1987) and ICES (1995).
Research could use experimental introductions (as are used for genetically modified organisms), assessment of comparable case studies, and modelling. Techniques for modelling of invasion and spread are advanced (Williamson 1989, 1996). In addition, the development of geographic information systems to determine the distribution of appropriate habitat for a species and to model the expected rate and pattern of spread (Carey & Brown 1994; Rushton et al. 1997, 2000) will prove useful. Modelling of gene flow and thus possibilities of hybridization is also advanced (Gliddon 1994).
Additionally, research should focus on assessment of current changes in the status of non-native species resident in the wild and potential methods for control. The response to problem non-native species in the UK is generally reactive. However, models of invasions show that if action is taken while populations are small, few and restricted in distribution, it is more likely to be effective at restricting spread and persistence (Williamson 1989). A proactive approach would restrict damage to biodiversity and probably be cheaper than subsequent containment, control or eradication.
One approach would be to restrict or prevent the further release of any non-native species, but this is not always in the interests of all members of society. Another would be to aim to control or eradicate all non-native species established in the wild, but this could be over-cautious and expensive and might meet with widespread opposition. The optimum approach would combine a precautionary principle concerning approval of releases with a policy of no action until a problem is predicted or detected in its early stages. To allow early detection, or even prediction, of problems of spread and/or negative effects on biodiversity, specific studies of the ecology of species and the mechanisms of their spread into new areas are needed, along with assessments of their effects on biodiversity. Population studies would also help the rapid development of control measures that can be implemented immediately problems are perceived, thus avoiding the loss of time in gathering ecological data after the species has become a problem.
Such detailed studies would be impossible for all non-native species in the UK, but such a review of the ecology and status of all such species (as carried out by Eno, Clarke & Sanderson 1997 on UK marine organisms) would allow identification of potential problem species that justified more detailed investigation. The distribution records held by the UK Biological Records Centre could be used to determine changes in the distributions of non-native species (Harding 1990).
Long-established and biogeographically stable non-native species that do not cause conservation problems should not necessarily be a cause for concern. However, a small number of non-native species do cause conservation problems for native flora and fauna. Given the difficulties associated with the control or eradication of these problem species, invasive non-native species should be prevented from establishing in the wild and increasing in numbers.
There are insufficient UK legislative provisions for the control of non-native species established in the wild. Current legislation needs enforcing, and rewriting where it is known to be ineffective. In addition, a case-by-case approach to risk assessment should be used for all proposed introductions of non-native species. Assessment procedures such as those suggested by ICES (1995) or IUCN (1987) would screen out harmful organisms prior to introduction. A proactive approach to assessing and managing future risks from non-native species (whether intentionally or unintentionally introduced) would limit damage to biodiversity and is likely to be more cost-effective than reactive control measures.
Research has shown that no generalizations can be made about the characteristics of invasive non-native species that hold for all cases. Thus future research needs to address specific cases. Identification of potential problem species will be possible only following reviews of the ecology of species, assessment of potential effects on biodiversity, and population studies to determine processes of dispersal and spread and to aid in the development of effective control measures before they are needed.
This review was partly funded by the Joint Nature Conservation Committee of the UK. However, the views expressed are entirely those of the authors. Many individuals contributed information for the review, but we wish to thank particularly: Bill Parish, Alan Gray, Kathy Hodder, Ian McLean, Margaret Palmer and Nigel Webb.
Received 26 April 1998; revision received 9 March 2000
International legislation and conventions concerning introductions of non-native species
|European Community (EC) directives|
|•||Directive 79/409 on the Conservation of Wild Birds requires member states to ensure that any introduction of non-native bird species does not prejudice the local flora and fauna|
|•||Article 22b of the EC Habitats Directive requires measures to regulate the deliberate introduction of non-native species|
|•||The EC Fish Health Directive 91/67 prohibits import of fish material, live or dead, from zones within the EC not approved as free of certain diseases|
|•||EC Directive 77/93 (amended by 91/683 in response to the removal of frontiers in the European Union) concerns the passage of organisms harmful to plants and plant products, and calls for bans on introductions of certain organisms. This is primarily concerned with agroeconomic implications of pest introductions|
|•||The Bern Convention on Conservation of European Wildlife and Natural Habitats requires that the introduction of non-native species be controlled|
|•||Recommendation R(84)14 of the Council of Europe Concerning the Introduction of Non-Native Species was based on the Bern Convention. It calls on member states to prohibit the introduction of non-native species into the natural environment, with possible exceptions only if an expert study of the consequences has been carried out. Accidental introductions should be prevented as far as possible|
|•||The Convention on Biological Diversity requires that the introduction of non-native species that threaten ecosystems, habitats or species should be prevented or that such species should be controlled or eradicated. The Bonn Convention on the Conservation of Migratory Species of Wild Animals encourages similar measures against non-native species that threaten endangered migratory species. The parties to the Bonn Convention have been negotiating an Agreement of African/Eurasian waterfowl (de Klemm 1996; Holmes & Simons 1996) that contains a provision that would require the parties to prohibit the deliberate introduction of exotic species, to take steps to prevent their accidental introduction and to prevent species already introduced from endangering native species|
|•||The 1982 United Nations Convention on the Law of the Sea, enforced in 1994, requires that the member states take all measures necessary to prevent and control the intentional or accidental introduction of alien species (and ‘new’ species, i.e. genetically modified organisms) that could cause harm to the marine environment|
|•||The Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES) developed a list of endangered species for which a permit system controls international trade. Trade is either prohibited (Appendix 1 species) or regulated (Appendices II and III). CITES was implemented in the EC in 1984 by Regulation 3626/82, and in the UK by the Endangered Species (Import and Export) Act 1976, the Control of Trade in Endangered Species Regulations (Enforcement) 1985, and the Control of Trade in Endangered Species Regulations (Designation of Ports of Entry) 1985|
Additional guidelines drawn up by british and international organizations
|Stubbs (1988) Towards an introductions policy|
|This was produced by Wildlife Link on behalf of 15 UK conservation organizations, and contained guidelines for assessing introductions, reintroductions and re-enforcements|
|UKINC (1979) Wildlife introductions to Great Britain (Linn report)|
|An independent ‘Working group on introductions’ reviewed introduction, reintroduction and re-enforcement (restocking), and recommended the establishment of an ‘Introductions Authority’ to assess and monitor introductions and to develop guidelines|
|Conservation Committee of the British Herpetological Society (1983)Herpetofauna Translocations in Britain – a Policy|
|These guidelines on the introduction of herpetofauna outlined acceptable translocations and reasons for introduction|
|NCC (1990) Review of NCC Policy on Species Translocations in Great Britain|
|This was a discussion document that suggested extensive revisions of NCC policy. It was based on the belief that some alien species have posed problems as pests, carriers of disease or competitors with native species. However, it has not been formally adopted|
|ICES (1995) ICES code of practice on the introductions and transfers of marine organisms 1994|
|These guidelines were developed for the translocation of fish, molluscs, crustaceans and plants for marine aquaculture. It recommends that a risk assessment be carried out prior to introduction, with subsequent monitoring|
|ICES (1988)Codes of practice and manual of procedures for consideration of introductions and transfers of marine and freshwater organisms|
|This contains the most recent code of practice of the European Inland Fisheries Advisory Committee (EIFAC), the body that advises on introductions and translocations for aquaculture within European inland waters. It recommends that containment measures be used to ensure the introduced species remains within the watercourse/waterbody into which it was released|
|International Maritime Organization (1993) Guidelines for preventing the introduction of unwanted aquatic organisms and pathogens from ships' ballast water and sediment discharges|
|The guidelines discuss procedures to prevent translocation of unwanted aquatic plants, animals, disease bacteria and viruses within ballast water, and advise on appropriate measures to take against discharges of ballast water from ships|
|North Atlantic Salmon Conservation Organization (1995) Introductions and transfers including the amendments proposed by the European Union|
|Aimed at salmon Salmo salar restocking and translocation, but also recommends risk evaluation prior to introduction of non-indigenous fish into rivers containing Atlantic salmon, and that ICES and EIFAC codes of practice are followed if the introduction proceeds|