Z. Jagdwiss.

48 (2002), Supplement, 51-58

ISSN 0044-2887

Cemre for bTvasive Species Research, School of Biological Sciences, UniversiO' of Auckland, New Zealand

Biodiversity loss caused by invasive alien vertebrates

By M. N. CLOUT,Auckland

1 Introduction: The global spread of alien vertebrates

In recent centuries natural ecosystems throughout much of the world have been greatly
diminished and modified by human activities such as farming, fishing, forestry, industry and
urbanisation. In the face of this onslaught, and the associated growth of human populations,
native biodiversity has often declined and many vulnerable species have become extinct. The
threats to global biodiversity posed by habitat loss are now well documented, but the growth
of international trade and travel has raised another, more insidious threat: the spread of alien
species. Alien species (sometimes also referred to as "introduced", "exotic" or "non-
indigenous" species) are taxa that have been transported by human agency (either deliberately
or accidentally) outside the area where they occur naturally (IUCN, 2000). This transport is
often over large distances (eg. across oceans), but it can also involve the local movement of
species across a natural barrier.
The isolation of biotas has been a major factor in the evolution of biological diversity on
Earth. Until a few hundred years ago, species from different regions mixed only through slow
spread, occasional long-distance dispersal across oceans or other barriers, and the very rare
collision of continental landmasses. The movement by people of domestic animals and crops
began to change this a few thousand years ago. In recent centuries biogeographic boundaries
have been increasingly breached by the deliberate or accidental transport of species by humans
(CRoSBV, 1986). The rate of introduction of alien species around the world accelerated rapidly
in the twentieth century, as globalisation of trade and travel and the increased specd of
transport allowed the spread of thousands of species around the planet (BRt6m, 1998). Some
of these introductions were accidental, but many were deliberate. Vertebrates have been
introduced as domestic livestock, pets, game animals, as biological control agents, to 'enrich'
native faunas, and for purely novelty reasons (L~vER, 1994). The ecological changes resulting
from this unprecedented global exchange of species are immense, insidious and generally
irreversible (IUCN, 2000).
Although introducing alien species to a region can increase the local number of species, the
commonly associated loss of endemic species means that the net effect on global biodiversity
is negative. The ultimate effect of a complete breakdown of all biogeographic boundaries and
the free mixing of all biotas can be crudely estimated from continental species-area
relationships for various groups of species (BROWN, 1995). In this way, it can be predicted that
total homogenisation of the world's biota, through the effective joining of all of the Earth's
surface into one supercontinent, would result in a 66% reduction in land mammal diversity and
a 48% reduction in land birds. Despite the fact that such complete mixing of all biotas is
unlikely, this 'thought experiment' illustrates the potential global scale of biodiversity loss due
to introductions of alien species.
Some alien species are of course beneficial to humans, as livestock, agents of biological
control, or as the basis of industries. Others may be neither beneficial nor harmful. However,
 52

there are many examples of alien vertebrates that are ecologically or economically harmful.
Alien species that invade natural or semi-natural ecosystems and act as agents of ecological
change are termed "invasive" (IUCN, 2000). The adverse effects of invasive alien species on
native biodiversity include the disruption of natural processes, domination of natural
ecosystems, and the extinction of native species through predation, competition, habitat
change, hybfidisation, or infection with disease.

2 Invasiveness and vulnerability

Some vertebrate species are notoriously invasive, having major ecological impacts in widely
separated locations around the world. Examples include black rats (Rattus rattus), cats (Felis
catus), rabbits (Oryctolagus cuniculus) and goats (Capra hircus). More Eurasian vertebrates
have invaded other regions than vice-versa (LEVER, 1994), but this may reflect the history of
colonialism and trade rather than any innate competitive advantages of Eurasian species.
Ecosystems and regions differ markedly in the number of biological invasions that they
have suffered, and in the consequences of these invasions. Oceanic islands and other isolated
systems seem to be particularly vulnerable to invasion by alien vertebrates, with subsequent
damage to native biodiversity. Continental areas without major biogeographic barriers seem
less vulnerable. Globally, over 90% of historic bird extinctions and 35% of historic mammal
extinctions have occurred on islands (PETERS and LOVEJOY, 1990). Alien species continue to
threaten over 30% of those island vertebrates classed as threatened, but only 13% of those on
continents (BRIGHT, 1998).

3 Effects on biodiversity

In several parts of the world the threats to biodiversity caused by alien species rank alongside
habitat loss in importance. In the United States more than 40% of the 958 taxa on the
"Threatened or Endangered List" are threatened primarily by competition or predation by
invasive species and in New Zealand invasive species are listed as the primary threat for 57%
of the 359 taxa that are classed as threatened by the New Zealand Departmcnt of Conservation
(M.N. CLOUT,unpublished data).
The ultimate impact of the introduction of alien species on global biodiversity is the
extinction of native species. Here there is a stark contrast between the effects of invasive
animals and plants. There are many examples of extinctions caused by invasive animals, but
very few (if any) examples of extinctions which have been caused solely by plant invaders,
despite the very large number of invasive plants worldwide.
Alien vertebrates may affect native biodiversity in several ways: by fccding on native
species (predation or herbivory), competing with them for vital resources, altering habitats,
carrying diseases, and hybridising with native species. Alien species also interact with one
another, so the effects on native biodiversity can be subtle and unexpected. The following
examples of illustrate the range of threats that invasive alien vertebrates can pose:

A. Predation
The introduction of vertebrate predators has frequently caused extinctions of native animal
species. Notorious examples of such predators include stoats (Mustela nivalis), Nile perch
(Lares nilotica), domestic cats (Felis catus) and black rats (Rattus rattus).
Stoats were introduced to New Zealand from Britain in the 1880s, in a misguided attempt
 53

at biological control of rabbits, themselves introduced a few decades earlier. The stoats did not
control rabbits, but (together with introduced rats and cats) they contributed to the extinction
of at least nine endemic bird species and still threaten several others (CLouT, 1999).
Nile perch were introduced to Lake Victoria to establish a fishery, but have devastated the
haplochromine cichlid fishes that evolved there. Over 200 of the 300-500 species of cichlid in
the lake are now extinct or severely threatened due to predation by the introduced perch
(GOLDSCHMIDT,1996).
Feral and domestic cats have been transported around the world and have proved to be
devastating predators of ground-nesting or flightless birds, and small mammals. On many
oceanic islands around the world they have depleted breeding populations of seabirds and
endemic landbirds. In New Zealand, cats have been implicated in the extinctions of at least six
species of island endemic birds, and some 70 populations of insular birds (KING, 1984). In
Australia, predation by cats falls most heavily on small native mammals, especially those
weighing <220g. Cats are strongly implicated in the nineteenth century extinctions of at least
six species of native Australian rodents (Pseudomys and Notomys) (DICKMAN, 1993).
A clear example of the negative effects of an alien rat species is the accidental introduction
of black rats (R. rattus) to Big South Cape Island in southern New Zealand. No rodents or
other alien predators were present when black rats reached this island in 1962. The rat
population irrupted and rapidly eliminated five endemic bird species (including the only
known population of the bush wren (Xenicus longipes), a large flightless weevil and the last
known population of the greater short-tailed bat (Mystacina robusta) (KING, 1984).
The additional prey provided by an alien species can exacerbate the impacts of invasive
predators on vulnerable native species. An example is the introduction of rabbits to
subantarctic Macquarie Island, which apparently provided alternative prey for previously
introduced feral cats. Prior to the rabbit introduction, the cat population was sufficiently low
to permit coexistence with native fauna, but the rabbit population apparently supported an
increase in numbers of cats, which hunted the endemic Macquarie Island parakeet
(Cyanoramphus sp.) to extinction shortly after the rabbit introduction (TAYLOR, 1979).

B. Herbivory
Introduced mammalian herbivores can have especially severe effects on island floras that have
evolved without physical or chemical protection against such animals.
Introduced deer cause damage to native ecosystems in many parts of the world. For
example, in New Zealand, red deer (Cervus elaphus) (introduced as game animals) continue
to inhibit the regeneration of native forests, even when reduced to low densities (NUGENTet
al., 2001).
Introduced goats are also a major threat to native vegetation on many islands around the
world. On the Atlantic island of St Helena they have exterminated at least ten of the island's
33 known species of endemic plants and endanger a further 18 (LEVER, 1994). Feral sheep can
cause similar problems. On Hawaii, mouflon (Ovis musimon), introduced for sporting
purposes, cause severe damage to vulnerable endemic plants.
As with predation, extinction through herbivory requires not only that the affected species
is particularly vulnerable or palatable, but generally that the herbivore has other abundant
(albeit less vulnerable or less palatable) food sources to support it. A population of herbivores
with alternative food resources is more likely to destroy the last individuals of a declining
plant species.
 54

C. Competition and habitat alteration

Alien vertebrates may compete with native ones directly, by aggression and displacement
("interference competition"), and indirectly, through removal or more efficient use of key
resources ("resource competition").
An example of resource competition is the replacement of native red squirrels (Sciurus
vulgaris) in Britain and northern Italy by alien grey squirrels (S. carolinensis) from North
America. The grey squirrel apparently forages more efficiently in deciduous woodlands and
anthropogenic habitats (WILLIAMSON,1996).
Habitat alteration caused by introduced vertebrates may also affect native biodiversity, both
directly through uprooting or grazing of plants and indirectly through reducing the extent and
quality of habitats on which specialist animals and plants depend.
Introduced vertebrates may fhcilitate invasions by alien plants, either by directly dispersing
plant seeds or by causing habitat changes that aid their establishment. Feral European pigs
consume the fruits (and hence disperse seeds) of invasive plant species in Hawaii, Mauritius,
New Zealand, Australia and other places where they have been introduced. The rooting
damage caused by pigs also favours establishment of many of these invasive plants. Mimosa
pigra, a leguminous shrub from Central America, produces many small seeds that are easily
dispersed by water. It is now severely invasive on flood plains in northern Australia (Low,
1999), lbllowing disruption and damage by feral Asian water buffalo, which improved the
conditions for germination ofM. pigra seedlings,

D. Hybridisation
Hybridisation and introgression with alien vertebrates can threaten native species that are
closely related to the invader, leading to "genetic swamping" when the native species is much
rarer than the aIien invader.
An example of the negative effects of hybridisation is the threat posed by introduced North
American ruddy ducks (Oxyurajamaieensis) to the rare white-headed duck (O. leucaeephala)
in the western Mediterranean. Ruddy ducks were introduced to the United Kingdom in 1948,
established a feral population and in the 1990s began to colonise the range of the native white-
headed duck in the western Mediterranean. The risk to the white-headed duck from the ruddy
duck has arisen because the two species hybridise readily. Male ruddy ducks are more
aggressive and apparently more successful in obtaining matings. Ruddy ducks are also less
demanding in their ecological requirements. Left unchecked, it is likely that they would
genetically swamp the white-headed duck population within a relatively short time (Hu6nEs,
1993).
Another example of hybridisation and introgrcssion is also provided by an interaction
between duck species. The widespread introduction of mallards (Arias plaO,rhynchos) from
North America and Europe and their hybridisation with closely related native species threatens
the existence (as distinct taxa) of the New Zealand grey duck (Anas superciliosa) and the
Hawaiian duck (A. p. ~yvilliana) (LEVER, 1994).

E. Disease vectors
Introduccd diseases can severely affect native species. Often these pathogens are carried by
(and inadvertently introduced with) other alien species which are themselves either resistant
or non-susceptible to the disease.
Avian malaria and birdpox (probably introduced with songbirds from Asia) are widely
regarded as major factors in the declines and extinctions of native birds in lowland habitats of
Hawaii. Avian malaria is transmitted by mosquitoes (Culex quinquefasciatus), which were
 55

accidentally introduccd to Hawaii in 1826. Several species of native Hawaiian birds now
persist only at higher altitudes where these disease-carrying alien insects are absent.
The rinderpest virus was accidentally introduced to Africa with imports of domestic cattle
in the late 1880s. Several species of native African ungulates were devastated by it, with
infection rates reaching 90% and many populations being severely reduced. Rinderpest still
continues to affect the distributions of some native ungulates in Africa (DoBsoN, 1995).

4 Multiple impacts of brushtail possums in New Zealand

Some invasive vertebrates have multiple impacts. An example is the common brushtail
possum (Trichosurus vulpecula), an arboreal Australian marsupial which was introduced to
New Zealand in a series of liberations between 1858 and 1900 to establish a fur trade (CLOUT
and ERICKSEN,2000). In New Zealand, the possum has fewer competitors for food and shelter,
no natural predators, and only 14 species of parasites compared with 76 in Australia. As a
consequence, it maintains population densities that are 10 times higher than those prevailing
in its native Australia. Possums are now officially recognised as major pests in New Zealand
because of their negative influences on native biodiversity and their role as a vector of bovine
tuberculosis (CLOUT, 1999). Their selective browsing can change the composition and
structure of native forests through defoliation and progressive elimination of the most
palatable food plants (PAYTON, 2000). Some endemic plants (eg. Dactylanthlts tavlori.
Peraxilla spp.) are now threatened with local extinction because of possum damage.
Competition for fruit and the destruction of flowers of preferred species also has an adverse
effect on the food resources of native birds. Finally, possums are now also known to be
significant predators of the eggs and nestlings of some threatened native bird species (SADLEIR,
2000). Because of these multiple impacts, there is now widespread control of possums in New
Zealand. The main control technique is poisoning, including the aerial broadcasting of toxic
baits containing 1080 (sodium monofluoroacetate) over large areas of native forest.

5 Action against alien vertebrates

Although the number of harmful invasions of alien vertebrates continues to increase, there
have been some successes in establishing international agreements to reduce these threats. The
UN Convention on Biological Diversity states that: "each Contracting Party shall prevent the
introduction of, control or eradicate those alien species which threaten ecosystems, habitats or
species." (Article 8 (h)). In response to this, the World Conservation Union (IUCN) has
published a set of guidelines on the prevention of biodiversity loss due to biological invasion
(IUCN, 2000). These guidelines stress the importance of preventing further invasions, the need
to raise awareness, the special risks to islands, the value of effective quarantine, the need for
early detection of new invasions, the best choice of control measures and the merits of early
eradication where possible.
Where eradication can be achieved, on islands or where biological invasions are otherwise
contained, it is possible to derive major benefits for native biodiversity. An example is tile
recent removal of all invasive mammals from Campbell Island, in the subantarctic region to
the south of New Zealand. This large island (11,300 ha) was settled in the mid-nineteenth
century, leading to the introduction of sheep, cattle, cats and Norway rats (Rattus norvegicus).
An inmaediatc result of the introduction of vertebrate predators was the disappearance from
 56

Campbell Island of the endemic snipe (Coenocotypha aucklandica) and flightless teal (Anas
attcklandiea), which survived only on adjacent small islands. Farming on Campbell Island was
soon abandoned as uneconomic, but populations of feral livestock remained as its legacy. With
the establishment of Campbell Island as a nature reserve, interest grew in the potential for
ecological restoration through the removal of alien mammals. The first to be eradicated (in
1984) was the small population of feral cattle (VEITCHand BELL, 1990). This was followed (in
1991) by the removal of all remaining sheep. Feral cats had always been relatively uncommon
on Campbell Island, possibly because of the cold, wet climate. Following the eradication of
feral livestock, the native vegetation recovered and became denser. This dcnser vegetation
may have made hunting and keeping dry even harder for the remaining cats. Whatever the
reason, the cat population had died out by 1999, leaving only the rats. In July 2001, the NZ
Department of Conservation distributed 120 tonnes of pellet baits (containing brodifacoum
anticoagulant) across Campbell Island from helicopters. Early indications are that this
poisoning operation (the largest of its kind anywhere) was successful in killing all rats.
Campbell Island is again free of all alien vertebrates and it is planned to restore the endemic
snipe and teal to the island as soon as the rat eradication is continued.

6 Conclusions

In many parts of the world (including Europe and Asia) there is very little awareness of the
negative effects of introducing alien species, including game animals. Often, little distinction
is made between native and alien species, and misguided attempts at 'faunal enrichment'
continue. Experience shows that, whilst it is difficult to predict the exact outcomes of a
vertebrate introduction, the consequences for native biodivcrsity are typically negative.
Although it is sometimes possible to eradicate alien vertebrates from islands or to eliminate
new populations, practical and ethical considerations sometimes make this difficult. A prime
example is the current spread of the grey squirrel in northern Italy, which could have been
prevented, contained or eradicated by earlier action (GENOVESland BERTOLINO,2001), but now
potcntially threatens tree crops and native squirrels throughout western Europe. This and other
examples summarised here illustrate why strict regulation of introductions is necessary and
why the precautionary principle should always be carefully applied before any introduction is
made.

Acknowledgements

I thank ELEFTHERIOSHADJISTERKOTISand the organisers of the XXVth IUGB Congress for

supporting my attendance at this meeting, and CAROLAWARNERfor assistance with manuscript
preparation,

Summary

The introduction of invasive alien vertebrates is a major cause of the loss of native biodiversity
in many regions of the world. The threats posed by them are especially severe on oceanic
islands and other isolated ecosystems, in which there are many examples of extinctions or
declines of native species caused by alien vertebrates. Predatory mammals are the worst
offenders, but mammalian herbivores can also cause biodiversity loss and may provide the
 57

prey base to support invasive predators. There are also some notorious examples of alien birds,
reptiles and fish that threaten native biodiversity. The adverse effects of invasive alien
vertebrates are illustrated by specific examples from New Zealand, including the multiple
impacts of Australian brushtail possums (Trichosurus vulpecula). Invasive vertebrates can
sometimes be eradicated in the early phases of establishment and can be removed from islands
or other isolated areas. However, given the uncertainty about the effects of alien species, the
best policy is to adopt the precautionary principle and avoid making introductions without
prior rigorous assessment of the risks to native biodiversity.

Key words: Alien vertebrates, native species, biodiversity, New Zealand

Zusammenfassung

Der Verlust der Biodiversitdt durch das Ehldr#lgen fi'emder Wirbeltierarten

Die Einftihrung gebietsfremder Wirbeltierarten ist eine Hauptursache ffir den Verlust der
einheimischen biologischen Vielfalt in vielen Gebieten der Erde. Die yon solchen Vorgfingen
ausgehende Gef~ihrdung ist besonders hoch auf ozeanischen Inseln und in andcren isolierten
Okosystemen, tiir die viele Beispiele des Aussterbcns oder des Riickgangs cinheimischer
Arten durch das Eindringen gebietsfremder Wirbeltiere existieren. Raubs'auger haben den
gravierendsten Einfluss, aber auch herbivore S~iugetiere k6nncn Biodiversitfits-Verlustc
verursachen sowie als Beute die Nahrungsbasis Nr eindringcnde Raubtierc darstellen. Es gibt
auch einige bekannte Beispiele f'tir die Bedrohung der einheimischen Biodivcrsit~it durch
gcbictsfremde V6gel, Reptilicn und Fische. Die negativcn Auswirkungen des Eindringens
gcbietsfremdcr Wirbeltierc wcrden anhand spezifischcr Beispiclc aus Neusecland erl/iutert,
darunter auch die vielf~iltigen Einfltisse des australischen Fuchskusu (Trichosttrus vulpeclda).
Manchmal gelingt die Ausrottung eingedrungener Wirbeltierarten, bevor diese auf lnseln oder
in anderen isolierten Gegenden richtig Ful3 fassen k6nnen. In Anbetracht der Unsicherheit der
yon gebietsfremden Wirbeltieren ausgehenden Wirkungen, sollte entsprechend dem Vorsorge-
Prinzip das Einbringcn yon Arten ohne vorherige grfindliche Untersuchungen der Risiken f'dr
die einheimische Biodiversitfit unterbleiben.

Schliissehv6rter: Gebietsfremde Wirbeltierc, einheimischc Arten, Biodivcrsit~it, Neuseeland

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A u t h o r J~"address: M.N. CLOUL Centre for Invasive Species Research, School of Biological
Sciences, University of Auckland, PB 92019, Auckland, New Zealand.