TRENDS in Ecology & Evolution Vol.16 No.

8 August 2001
http://tree.trends.com 01695347/01/$ see front matter 2001 Elsevier Science Ltd. All rights reserved. PII: S0169-5347(01)02194-2
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Erika Zavaleta*
Harold A.Mooney
Dept of Biological
Sciences, Stanford
University, Stanford,
CA 94305, USA.
*e-mail:
zavaleta@stanford.edu
Richard J .Hobbs
School of Environmental
Science, Murdoch
University, Murdoch,
WA 6150, Australia.
I nvasi ve al i en speci es i nteract wi th other el ements of
gl obal change to cause consi derabl e damage to
managed and natural systems and to i ncur huge costs
to soci ety
1
. I n response, several measures have been
devel oped and depl oyed to control , contai n or
eradi cate a wi de range of i nvasi ve speci es i n affected
areas. Where possi bl e, ERADI CATI ON (see Gl ossary) i s
the favored approach. Control , whi ch reduces the
presence of the i nvader, and contai nment, whi ch
l i mi ts further spread, both requi re i ndefi ni te
i nvestments of ti me, tool s and money to keep an
i nvader at bay. Al though eradi cati on can requi re l arge
short-term i nvestments, successful removal can be
achi eved wi thi n months or years and gi ves the best
chance for nati ve bi odi versi ty to recover.
The resul ts of eradi cati on efforts so far are
encouragi ng and have been detai l ed recentl y
2
. Many
case studi es demonstrate success for a range of taxa,
parti cul arl y on smal l i sl ands and at l ocal scal es.
Addi ti onal exampl es i ncl ude the removal of the exoti c
l i ttl e red fi re ant Wasmannia auropunctatafrom
Santa Fe I sl and i n the Gal apagos
3
(whi ch resul ted i n
the i ncrease i n densi ty of several nati ve ant speci es),
and the nearl y compl ete removal from Laysan I sl and,
Hawai i of the exoti c annual grass Cenchrus
echinatus, whi ch once covered 30% of the vegetated
area of the i sl and (E.N. Fl i nt, unpubl i shed).
Successful eradi cati ons often l ead to dramati c
recovery of nati ve speci es and ecosystems. Removal of
i ntroduced rabbi ts from Paci fi c i sl ands off Mexi co
(C.J. Donl an, unpubl i shed) and the USA have al l owed
recovery of two rapi dl y decl i ni ng endemi c speci es of
nati ve succul ents Dudleya linearis and D. traskiae
4
.
Lowl and vegetati on on Santa Fe I sl and has recovered
steadi l y fol l owi ng the removal of exoti c goats Capra
hircusnearl y 30 years ago.
However, other cases suggest that more refined and
integrated approaches to invasive removal could
improve results. Successes are still largely confined to
small islands. The ecological context of eradication is
increasingly complex. Major damage caused by long-
established invaders, systems that are affected by
multiple invaders, and systems that are affected by
both invaders and other global changes are now
common. I n these settings, straightforward deployment
of standard eradication tools, such as poisons, trapping
and mechanical harvesting, might not accomplish the
desired level of recovery of native ecosystems
5
.
We suggest that, al though there i s a cruci al need for
the conti nued devel opment and appl i cati on of effecti ve
eradi cati on methodol ogi es, a paral l el need exi sts to
pl ace these methodol ogi es i n the context of the overal l
ecosystem that i s bei ng managed. I deal l y, there shoul d
be both: (1)pre-eradi cati on assessment, to tai l or
removal to avoi d unwanted ecol ogi cal effects; and
(2)post-removal assessment of eradi cati on effects, on
both the target organi sm and the i nvaded ecosystem.
The requi rements for successful removal of an
i nvader have been di scussed recentl y
2
. We focus on
the possi bl e i mpacts that resul t from the successful
removal of i nvasi ve speci es, regardl ess of the methods
empl oyed to remove them. We revi ewed recent
l i terature for exampl es where the successful
eradi cati on of i nvasi ves had or was l i kel y to have
i mportant secondary i mpacts, a task that was made
di ffi cul t by the rel ati vel y few veri fi ed eradi cati on
successes that i ncl uded the moni tori ng of post-
removal system behavi or.
Eradication:what can go wrong
Successful eradication efforts have generally benefited
biological diversity. However, there is also evidence that,
without sufficient planning, successful eradications can
have unwanted and unexpected impacts on native
species and ecosystems. These inadvertent impacts are of
many types. Excessive poisoning of non-target organisms
and transfer of poisons up food chains
6
are problems that
can result from the removal method used
7,8
. Some
eradication efforts fail because they do not eliminate the
target organism, because they either miss individuals or
do not include steps to reduce post-eradication
susceptibility to reinvasion
3
. Eradication alone might not
allow ecosystems to recover, because some invaders
change the condition of the habitat so as to render it
unsuitable for native species. For instance, in sites from
the Middle East to the western USA, high soil salinity is
caused by the invasive ice plant Mesembryanthemum
crystallinum, and tamarisk Tamarix spp., which makes
it difficult for salt-sensitive native species to re-establish
9
.
I n these cases, eradication must be followed by additional
site restoration.
Eradications of invasive species often have striking positive effects on native
biota.However,recent research has shown that species removal in isolation
can also result in unexpected changes to other ecosystem components.These
secondary effects will become more likely as numbers of interacting invaders
increase in ecosystems,and as exotics in late stages of invasion eliminate
native species and replace their functional roles.Food web and functional role
frameworks can be used to identify ecological conditions that forecast the
potential for unwanted secondary impacts.Integration of eradication into a
holistic process of assessment and restoration will help safeguard against
accidental,adverse effects on native ecosystems.
Viewing invasive species removal in a
whole-ecosystem context
Erika S.Zavaleta,Richard J .Hobbs and Harold A.Mooney
Successful eradi cati ons can al so have undesi red
effects that resul t from the successful removal of the
i nvader. I n several cases, removal of one exoti c
speci es has l ed to the establ i shment or i ncrease of one
or more other i nvasi ve speci es. For exampl e, several
eradi cati ons of exoti c herbi vores have been l i nked to
i ncreases i n exoti c pl ant popul ati ons. Removal of one
i nvader can l ead to i ncreased i mpacts of another
i nvader; for exampl e, when removal of exoti c prey
l eads to i ncreased predati on on nati ve prey by exoti c
predators
10
. Fi nal l y, removal of i nvasi ve pl ant speci es
can reduce habi tat or resources avai l abl e for nati ve
fauna i f the removal i s not accompani ed by further
restorati on measures (Box 1). These unexpected
outcomes wi l l become more probabl e both as the
vari ety of i nteracti ng i nvaders contai ned i n an
ecosystem i ncreases, and as exoti cs i n l ate stages of
i nvasi on l argel y or whol l y el i mi nate nati ve speci es
and repl ace thei r functi onal rol es. Al though
researchers have begun to expl ore the i mpl i cati ons of
mul ti pl e, i nteracti ng i nvaders, l i ttl e attenti on has
been pai d to the i mpl i cati ons of these i nteracti ons for
eradi cati on efforts.
Secondary effects:a conceptual framework
A useful basi s from whi ch to tackl e when and why
secondary effects of eradi cati on occur i s that systems
contai ni ng i nvasi ves functi on accordi ng to the same
basi c pri nci pl es as do other systems. I nvaded systems
can, therefore, be consi dered usi ng the frameworks
that are usual l y used to anal yze communi ty and
ecosystem dynami cs.
Trophic cascades in multiply invaded systems
A l arge l i terature has been devoted to how food-web
i nteracti ons l i mi t popul ati ons of producers, consumers
and predators
1113
. Much work has been done on the
rel ati ve rol es of top-down regul ati on of food-web
components by hi gher-l evel consumers or predators,
and of bottom-up regul ati on of popul ati ons by food
avai l abi l i ty or resource l i mi tati on. Evi dence from
several ecosystem types shows that both top-down and
bottom-up popul ati on regul ati on of producers and
consumers occur under some condi ti ons
1416
. The
exi stence of these regul atory l i nks can gi ve ri se to
TROPHI C CASCADES
16,17
(but see Ref. 13).
When combined with the use of simple terrestrial
food webs
6
(Fig. 1), this framework helps to explain how
many animal eradications have allowed population
recovery of native species. Removal of an exotic
predator can release native prey from strong top-down
regulation, increasing prey abundance with potential
cascading impacts on other food-web components,
including native predators (Fig. 1b). Similarly, exotic
herbivores in the absence of predators can become
sufficiently abundant to exert top-down pressure on
native plants
14
. Removal of these herbivores can lead to
rapid recovery of native plant populations
4
.
Predatorprey interactions
However, the presence of mul ti pl e i nvaders at
di fferent trophi c l evel s compl i cates matters. Consi der
the case where an exoti c predator and an exoti c prey
speci es co-occur (Fi g. 1c). Removal of the i nvasi ve
predator onl y coul d l ead to MESOPREDATOR RELEASE
(rel ease of the i nvasi ve prey from top-down
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Exotic saltcedar Tamarix spp. shrubs have replaced much of the native riparian
vegetation of the arid western USA, where they consume large quantities of
water, narrow river channels, salinize soil and degrade wildlife habitat
a
.
Saltcedar removal has been repeatedly delayed in parts of its range
because it provides significant nesting habitat for an endangered native
songbird
b
. The southwestern willow flycatcher Empidonax trailii extimus,
currently reduced to fewer than 500 breeding pairs, nested historically in
riparian cottonwood(Populus spp.)willow (Salixspp.) stands in the
southwestern USA (Refs c,d). Urbanization, agriculture, fire, water
diversion and livestock grazing all contributed to the decline of its native
habitat
b
. The replacement of much of the habitat that remained by saltcedar
required the flycatcher to make use of the invader, which it seems to prefer
in some areas, despite its reduced breeding success
e,f
.
Stepwise saltcedar removal could strongly benefit the flycatcher by giving
native trees the opportunity to re-establish and provide replacement
habitat
g
. However, some saltcedar-invaded areas might no longer be able
to support native vegetation, because lowered water tables and saline
soils, the results of saltcedar dominance, might complicate native
re-establishment
hj
. Region-wide flood suppression hinders
re-establishment of flood-associated native species such as cottonwoods
and increases the likelihood of saltcedar reinvasion
j,k
.
Managers are confident that, if accompanied by planning and careful
restoration, saltcedar removal can benefit the endangered flycatcher as well
as other native species
g
. However, poorly planned removal without steps
such as flooding and vegetation restoration, might fail, harming an
endangered species in the process.
References
a Zaval eta, E.S. (2000) Val ui ng ecosystem servi ces l ost to Tamarixi nvasi on i n the Uni ted
States. I n I nvasiveSpecies in a Changing World (Mooney, H.A. and Hobbs, R.J., eds),
pp. 261300, I sl and Press
b USFWS (1997) Endangered and threatened wi l dl i fe and pl ants; fi nal determi nati on of
cri ti cal habi tat for the southwestern wi l l ow fl ycatcher. Fed. Reg. 62, 3912939147
c Rosenberg, K.V. et al. (1991) Birds of theLower Colorado River Valley, University of Arizona
Press
d Sogge, M.K. et al. (1997) ASouthwestern Willow Flycatcher Natural History Summary
and Survey Protocol, Nati onal Park Servi ce
e DeLoach, C.J. et al. (1999) I n Ecological I nteractions in theBiological Control of Saltcedar
(Tamari x sp.) in theUS: Toward a New Understanding, US Department of Agri cul ture
f McKernan, R.L. and Braden, G. (1999) Status, Distribution, and Habitat Affinities of the
Southwestern Willow Flycatcher Along theColorado River; Year 3 1998, US Dept of the
I nteri orBureau of Recl amati on
g Dudl ey, T.L. et al. (2001) Saltcedar I nvasion of Western Riparian Areas: I mpacts and
New Prospects for Control, US Department of Agri cul ture
h Jackson, J. et al. (1990) Assessment of theSalinity Toleranceof Eight Sonoran Desert
Riparian Trees and Shrubs, US Dept of the I nteri orBureau of Recl amati on
i Shafroth, P.B. et al. (1995) Effects of sal i ni ty on establ i shment of Populus fremontii
(cottonwood) and Tamarix ramosissima(sal tcedar) i n southwestern Uni ted States.
Great Basin Nat. 55, 5865
j Tayl or, J.P. and McDani el , K.C. (1998) Restorati on of sal tcedar i nfested fl ood pl ai ns on
the Bosque del Apache Nati onal Wi l dl i fe Refuge. Weed Technol. 12, 345352
k Stromberg, J. (1998) Dynami cs of Fremont cottonwood (Populus fremontii) and sal tcedar
(Tamarix chinensis) popul ati on al ong the San Pedro Ri ver, Ari zona. J . Arid Environ. 40,
133155
Box 1.When a harmful exotic harbors an endangered native species
regul ati on) (Fi g. 1d). I f the exoti c prey consume nati ve
speci es, the removal of the exoti c top predator coul d
l ead to net negati ve i mpacts on nati ve popul ati ons of
conservati on val ue
18
. For exampl e, exoti c cats on
Stewart I sl and, New Zeal and, prey upon the kakapo
Strigops habroptilus, an endangered fl i ghtl ess parrot.
However, the di et of the cats consi sts overwhel mi ngl y
of the three speci es of exoti c rats on the i sl and
19
. Cat
eradi cati on woul d probabl y i ncrease the i mpact of
rats on the kakapo as wel l as on other nati ve bi ota
unl ess rats were si mul taneousl y removed. The
potenti al for mesopredator rel ease fol l owi ng cat
eradi cati on i s wi despread. I ntroduced rats Rattus
spp., house mi ce Mus musculus, and/or rabbi ts
Oryctolagus cuniculus co-occur wi th exoti c cats on 22
i sl ands where the di ets of cats have been studi ed. I n
nearl y every case, cats exert i mportant top-down
control s on these other exoti cs by preyi ng heavi l y on
rabbi ts i f they are present, and heavi l y on rats i f
rabbi ts are not present
20
(Tabl e 1). Mi ce are al so an
i mportant part of the di et of feral cat on i sl ands at
temperate, but not tropi cal , l ati tudes
20
. The potenti al
for these trophi c effects i s probabl y strongest on
i sl ands l acki ng nati ve predators; however, i t appl i es,
i n pri nci pl e, to any system i n whi ch exoti c predator
popul ati ons take advantage of abundant exoti c prey.
The effects of mesopredator rel ease can cascade to
al ter ecosystem-scal e properti es as wel l as al teri ng
nati ve popul ati ons. Studi es before cat eradi cati on on
subantarcti c Mari on I sl and showed that the cats ate
many exoti c house mi ce, whi ch prey heavi l y upon a
fl i ghtl ess endemi c moth Pringleophaga marioni,
whi ch i s i mportant to nutri ent cycl i ng
2123
. Removal
of the cats onl y mi ght have al l owed i ncreases i n
mouse popul ati ons, causi ng cascadi ng decl i nes i n
endemi c moth abundance and, ul ti matel y, changes i n
soi l nutri ent avai l abi l i ty.
When exoti c predators and prey co-occur,
eradi cati on of onl y the exoti c prey can al so cause
probl ems by forci ng the predator to swi tch to nati ve
prey. I n New Zeal and, i ntroduced rats R. rattusand
possums Trichosurus vulpecular are an i mportant
part of the di et of the stoat Mustela ermina, an exoti c
mustel i d
10
. Efforts to remove al l three speci es by
poi soni ng the prey speci es had an unexpected resul t:
the stoat popul ati ons were not el i mi nated by
ei ther the prey eradi cati on or the poi son appl i cati on
and, i n the absence of abundant exoti c prey, the stoats
swi tched thei r di ets to nati ve bi rds and bi rd eggs.
Wi thout prey eradi cati on, the co-occurrence of
exoti c predators and exoti c prey can i mpact heavi l y on
nati ve prey popul ati ons by HYPERPREDATI ON. The
avai l abi l i ty of abundant exoti c prey can i nfl ate exoti c
predator popul ati ons, whi ch then i ncrease thei r
consumpti on of i ndi genous speci es
24
. Thi s
phenomenon was fi rst el aborated to expl ai n why
nati ve Austral i an mammal s suffered popul ati on
decl i nes i n areas i nvaded by cats onl y i f exoti c rabbi t
and mouse densi ti es were al so hi gh
25
. The removal of
exoti c prey to curb hyperpredati on of nati ve speci es
by exoti c predators has been suggested
26
. However,
managers must consi der careful l y whether nati ve
popul ati ons can wi thstand further, temporary
i ncreases i n predati on when the i nfl ated predator
popul ati on no l onger has exoti c prey to sustai n i t.
Herbivoreplant interactions
When exoti c herbi vores and pl ants co-occur (Fi g. 1d),
control or eradi cati on of onl y the exoti c pl ants coul d,
i n theory, l ead to i ncreased exoti c herbi vory on nati ve
pl ants. However, we do not know of a case i n whi ch
thi s has occurred. Thi s mi ght refl ect the pauci ty of
successful pl ant eradi cati ons, the pri ori ti zati on of
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TRENDS in Ecology & Evolution
Plant 1 Plant 2 Plant 3 Plant 4
Consumer 1 Consumer 2 Consumer 3
Predator 1 Predator 2 Predator 3
Plant 1 Plant 2 Plant 3 Plant 4
Consumer 1 Consumer 2 Consumer 3
Predator 1 Predator 2 Predator 3
Plant 3 Plant 4
Consumer 1 Consumer 2 Consumer 3
Predator 1 Predator 2 Predator 3
Plant 1 Plant 2 Plant 3 Plant 4
Consumer 1 Consumer 2 Consumer 3
Predator 1 Predator 2 Predator 3
(a)
(b)
(c)
(d)
(e)
(f)
Plant 1 Plant 2 Plant 3 Plant 4
Consumer 1 Consumer 2 Consumer 3
Predator 1 Predator 2 Predator 3
Plant 1 Plant 2 Plant 3 Plant 4
Consumer 1 Consumer 2 Consumer 3
Predator 1 Predator 2 Predator 3
Plant 1 Plant 2
Fig.1.Idealized food webs
indicating trophic
interactions between
species. Closed boxes
represent exotic species
and open boxes represent
native species. Arrow
thickness indicates the
strength of trophic
interaction. Font size
represents population
size. (a)shows a
community containing a
single exotic predator. In
(b), removal of this
predator increases native
prey populations.
(c)shows a community
containing both an exotic
predator and an exotic
herbivore. In (d), removal
of only the exotic predator
releases the exotic
herbivore population, with
cascading impacts on two
plant species. (e)shows a
community containing
both an exotic herbivore
and an exotic plant
species. In (f), removal of
the exotic herbivore only
releases the exotic plant
population.
Table 1.Importance of exotic rats in the diet of introduced cats on islands
a
Islands without Occurrence of Islands with Occurrence of
introduced rabbits rats in diet (%) introduced rabbits
b
rats in diet (%)
Galapagos: Isabela 73 Gran Canaria 4
Santa Cruz 88 Te Wharau, NZ 3
Lord Howe 87 Kourarau, NZ Trace
Raoul 86 Orongorongo, NZ 50
Little Barrier 39 Mackenzie, NZ 2
Stewart 93 Kerguelen 0
Campbell 95 Macquarie 3
a
Data from Ref. 20.
b
Abbreviation: NZ, New Zealand.
ani mal removal s from mul ti pl y i nvaded ecosystems,
or an absence of stri ct bottom-up regul ati on of exoti c
herbi vores by pl ant bi omass avai l abi l i ty.
When exotic herbivores and plants co-occur,
eradication of the herbivores only can lead to release of
exotic plants from top-down control (Fig. 1f). I n nearly
all documented cases where exotic plants co-occur with
exotic herbivores on islands, herbivore removal has had
mixed results for native vegetation (but see Refs 27,28).
Feral herbivore removal from Santa Catalina I sland,
Channel I sland National Park, led to an increase in
native species richness, but also to large absolute and
relative increases in cover by exotic annuals
29
. Rabbit
eradication on Round I sland, Mauritius, led to strong
recovery of three endemic or locally restricted tree
species (Latania loddigesii, Pandanus vandermeerschii
and Hyophorbe lagenicaulis) and six reptile species [two
skinks (Leiolopismatelfaririi and Scelotesbojerii), three
geckos (Phelsuma guentheri, P. ornataand Nactus
serpensinsula) and a snake (Casarea dussumerii)],
including five endemics
30
. However, rabbit removal also
caused the spectacular release of a previously sparse
exotic grass Chloris barbata, rendering it a significant
component of the vegetation on the island
30
(Box 2).
Asiatic water buffalo Bubalus bubaliseradication from
Kakadu National Park, Australia spurred large-scale
regeneration of the wetlands of the park
31
. However,
alien plant species also proliferated, in particular,
introduced para grass Brachiaria mutica, which now
covers approximately 10% of the major floodplain
habitats in the park.
Al though the removal of feral pi gs Sus scrofa,
sheep Ovis ariesand goats has al l owed some nati ve
pl ant speci es to recover sl i ghtl y i n Hawai i
32
, many
Hawai i an l owl and grassl ands have responded to
ungul ate removal wi th i ncreases i n the cover of
fl ammabl e exoti c grasses
33
. Accompanyi ng i ncreases
i n fi re frequency accel erate a posi ti ve feedback l oop
among i nvasi ve grass establ i shment, fi re, and l oss of
nati ve woodl ands and forest
34
.
The effects of exoti c herbi vore removal on nati ve
vegetati on, under certai n ci rcumstances, mi ght al so
have i ndi rect negati ve effects, because of the presence
of other exoti c ani mal s. Rabbi t removal on Macquari e
I sl and i n the Southern Ocean l ed to major i ncreases
i n cover by a nati ve tussock grass Poa foliosa, whi ch i s
the preferred habi tat of the i ntroduced shi p rat.
Tussock expansi on coul d bri ng the rats i nto contact
wi th burrow-nesti ng bi rd col oni es on the i sl and,
whi ch have escaped rat predati on so far
35
.
Herbivore removal from islands has strong negative
effects on vegetation in some cases. The removal of
sheep and cattle Bos taurusfrom Santa Cruz I sland led
to an explosive expansion of exotic fennel Foeniculum
vulgare, starthistle Centaurea solstitialis, and other
introduced herbs, increases in relative cover of exotics,
but the observable recovery of only one native species,
Bishop pine Pinus muricata, after nine years of
monitoring
3638
. Moreover, the sudden expansion of
exotic forbs provided abundant food for feral European
bee Apis mellifera, colonies, and complicated eventual
bee eradication from the island
39
. The greatest potential
for negative impacts on native vegetation perhaps
exists when herbivore eradication removes the
disturbance that is necessary to suppress
establishment of late successional (tree or shrub)
exotics
40
. The removal of feral cattle from degraded
grasslands on San Cristobal I sland in the Galapagos
allowed previously suppressed exotic guava Psidium
guajavato grow rapidly into dense, extensive thickets
41
.
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Before their extinction, two species of
giant tortoise (Geocholone triserrata and
G. inepta), endemic to the Mascarene
Islands, browsed the native vegetation
and dispersed fruits of endemic trees such
as the Ile aux Aigrettes ebony Diospyros
egrettarum. Trade in tortoise meat,
together with the introduction of rats and
pigs in the 16th18th centuries, extirpated
the native browsers from the archipelago.
Introduced goats Capra hircus and
rabbits Oryctolagus cuniculus replaced the
tortoises as herbivores, suppressing
numerous introduced grazing-intolerant
plant species until the late 20th century.
However, the eradication of exotic
herbivores from Round Island and Ile aux
Aigrettes in the 1970s and 1980s released
populations of exotic weeds such as
Chloris barbataon Round Island and false
acacia Leucaena leucocephalaon Ile aux
Aigrettes. Native tussock-forming grasses
declined on Round Island, and increasingly
tall exotic vegetation threatened low-
growing endemics such as Aerva
congesta, nowfound only on Round
Island.
To restore and maintain native
vegetation, scientists at the Mauritian
Wildlife Foundation are exploring the
introduction of a taxonomic and functional
substitute for the extinct tortoises, the
Aldabran tortoise G. gigantia (Fig. I). Four
adult Aldabran tortoises were released
into a fenced enclosure on Ile aux
Aigrettes in November 2000, and the first
post-introduction vegetation survey took
place in May 2001. Viable fruits of the
endemic ebony have already been found
dispersed in tortoise feces away from
parent trees. It is hoped that the
introduced tortoises will not only shift the
competitive balance in favor of native
plants, but also restore the broader
functional roles of their extinct congeners
in the ecosystems of the Mascarene
archipelago.
Reference
a North, S.G. et al. (1994) Changes i n the
vegetati on and repti l e popul ati ons on Round
I sl and, Mauri ti us, fol l owi ng eradi cati on of
rabbi ts. Biol. Conserv. 67, 2128
Box 2.Replacing extinct herbivores in the Mascarene Islands
I
I n most setti ngs, removi ng i ntroduced herbi vores
i s an i mportant and reasonabl e fi rst step i n ecosystem
restorati on. However, i n some cases (parti cul arl y on
i sl ands wi thout nati ve herbi vores), herbi vore removal
mi ght actual l y cause harm i f there are no concurrent
efforts to control exoti c vegetati on (Fi g. 2). The
cl earest benefi ts from exoti c herbi vore removal are
l i kel y to occur i n setti ngs that are sti l l domi nated by
nati ve vegetati on. I n other setti ngs, cl ose moni tori ng
after herbi vore removal , as wel l as pre-eradi cati on
assessment, can hel p reduce unexpected negati ve
consequences of the removal of i nvasi ves
42
.
Native species dependence in exotic-dominated habitats
I ncreasi ngl y, exoti c speci es have been present i n
ecosystems for l ong enough to domi nate or repl ace
nati ve speci es and habi tats. I n these cases, an
ecosystem or functi onal framework mi ght be useful i n
whi ch one asks whether removal of the i nvader wi l l
l argel y or enti rel y remove from the system a functi on
necessary to other bi ota i n i t. For exampl e, an
i nvasi ve pl ant speci es mi ght provi de usabl e habi tat
for nati ve fauna i n the absence of ori gi nal vegetati on.
Rapi d removal of the i nvader wi thout restori ng nati ve
vegetati on mi ght not onl y i ncrease the chances of a
new i nvasi on, but al so l eave nati ve fauna wi thout
cover or food. Several exampl es of the potenti al for
thi s type of probl em have been descri bed
43
. However,
exampl es of successful eradi cati ons that actual l y l ed
to such habi tat l oss have not been i denti fi ed. Thi s
most probabl y refl ects the l ack of successful
eradi cati ons of pl ants, whi ch usual l y provi de habi tat
for other bi ota. The case of Tamarix(Box 1) i l l ustrates
how, under certai n condi ti ons, consi derati on of thi s
ki nd of undesi rabl e i mpact can be i mportant.
Conclusion
The type of species being removed, the degree to which
it has replaced native taxa, and the presence of other
non-native species can affect the eventual impacts of
removal of an invasive species. Managers can take some
simple steps to reduce surprise outcomes. Pre-
assessment, including qualitative evaluation of:
(1)trophic interactions among exotics and between
natives and exotics; and (2)potential functional roles of
exotics, is necessary for managers to anticipate the need
for special planning. Post-eradication monitoring is also
extremely valuable, not least because it allows
managers to document the positive outcomes of
eradication successes. I t also provides the opportunity
to learn from mistakes and gives managers the chance
to curtail negative effects before they become severe.
More frequent ecological studies that take advantage of
eradication programss as being large-scale ecosystem
experiments will speed the accumulation of knowledge
about system responses to exotic species removals.
Speci fi c gui dance for tai l ori ng eradi cati on efforts to
compl ex si tuati ons i s emergi ng. I n the case of
stoatratopossum eradi cati on i n New Zeal and
10
,
fol l ow-up study showed that the ti mi ng and method of
poi soni ng used were i mportant i n determi ni ng stoat
popul ati on decl i nes (as a resul t of secondary poi soni ng)
as wel l as determi ni ng effects on nati ve bi rds
44
. A
model of i nteracti ons between exoti c cats and rabbi ts
found that si mul taneous removal of both speci es
maxi mi zed the chances of success, but suggested that
the next best al ternati ve was to remove rabbi ts fi rst
and cats l ater
26
. Data from several cases show that
attempts to restore a nati ve speci es wi thout removi ng
al l i nvaders that consume i t are l i kel y to fai l
45
. Many
attempts to rei ntroduce nati ve marsupi al s to areas
from whi ch they have been exti rpated have fai l ed
because of the presence of uncontrol l ed exoti c
terrestri al predators such as cats and foxes Vulpes
fulva. Success rates of rei ntroducti ons are an order of
magni tude greater (82% versus 8%) on i sl ands wi thout
exoti c predators
46
. As they accumul ate, these ki nds of
anal yses whether based on post-eradi cati on data or
model ed on ecol ogi cal pri nci pl es wi l l enabl e the
desi gn of better eradi cati on and restorati on strategi es.
I nvasi ve speci es eradi cati on i s an i ncreasi ngl y
i mportant component of the conservati on and
management of natural ecosystems. However, in
natural systems, a shift in emphasis from strict invasives
management towards broader ecosystem restorati on
goals is required. This will place more emphasis on the
full diagnosis of causal factors and the desired ecological
outcomes of eradications
47
. As knowledge about
effective eradication methods accumulates, attention
should turn to combining such methods with broader
ecological principles to form cost-effective removal
strategies that accomplish overall restoration goals.
TRENDS in Ecology & Evolution Vol.16 No.8 August 2001
http://tree.trends.com
458 Review
TRENDS in Ecology & Evolution
(b)
(a)
Fig.2.An adverse effect
of eradication. The
photographs show a
camp site on Sarigan
Island, Commonwealth of
the Northern Mariana
Islands, before(a) and
after (b) successful
eradication of feral goats
Capra hircus and pigs Sus
scrofa in 1998 explosively
released a previously
undetected exotic vine
Operculina ventricosa.
Arrows in (b) indicate the
locations of the two
buildings visible in (a).
Reproduced, with
permission, from Curt
Kessler, Zoology
Unlimited.
Acknowledgements
We thank Curt Kessler,
J osh Donlan, J ohn
Mauremootoo, Robert
Bensted-Smith, Bernie
Tershy, Rick Van Dam,
Dick Veitch, and Ingrid
Parker and her lab group
for their helpful input.
TRENDS in Ecology & Evolution Vol.16 No.8 August 2001
http://tree.trends.com
459 Review
Eradication:removal of every individual and
propagule of an invasive species so that only
reintroduction could allow its return.
Hyperpredation:abnormally high predation of
indigenous prey species by a predator population that
is inflated by the availability of highly abundant exotic
prey.
Mesopredator release:rise in a population of one
species caused by the removal of a species that preys
upon it. It can lead to a net increase in predation on
native populations of conservation concern
a
.
Trophic cascade:when changes in one species affect
the abundances of other species across more than one
link in the food web
b
.
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b Pace, M.L. et al. (1999) Trophi c cascades
reveal ed i n di verse ecosystems. Trends Ecol.
Evol. 14, 483488
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