Journal of Applied Ecology

2009,

46

, 73–81 doi: 10.1111/j.1365-2664.2008.01601.x

© 2009 The Authors. Journal compilation © 2009 British Ecological Society

Blackwell Publishing LtdIndirect effects of invasive species removal devastate
World Heritage Island

Dana M. Bergstrom

1

*, Arko Lucieer

2

, Kate Kiefer

1

, Jane Wasley

1

, Lee Belbin

3

,
Tore K. Pedersen

1,2

and Steven L. Chown

4

1

Australian Antarctic Division, Department of the Environment, Water, Heritage and the Arts, 203 Channel Highway,
Kingston 7050, Australia;

2

School of Geography and Environmental Studies, University of Tasmania, Private Bag 76,
Hobart 7001, Tasmania, Australia;

3

Blatant Fabrications Pty Ltd, Hobart, Tasmania, Australia; and

4

Centre for Invasion

Biology, Department of Botany and Zoology, Stellenbosch University, Private Bag X1, Matieland 7602, South Africa

Summary

1.

Owing to the detrimental impacts of invasive alien species, their control is often a priority for
conservation management. Whereas the potential for unforeseen consequences of management is
recognized, their associated complexity and costs are less widely appreciated.

2.

We demonstrate that theoretically plausible trophic cascades associated with invasive species
removal not only take place in reality, but can also result in rapid and drastic landscape-wide
changes to ecosystems.

3.

Using a combination of population data from of an invasive herbivore, plot-scale vegetation
analyses, and satellite imagery, we show how a management intervention to eradicate a mesopredator
has inadvertently and rapidly precipitated landscape-wide change on sub-Antarctic Macquarie Island.
This happened despite the eradication being positioned within an integrated pest management
framework. Following eradication of cats

Felis catus

in 2001, rabbit

Oryctolagus cuniculus

numbers
increased substantially although a control action was in place (

Myxoma

virus), resulting in island-wide
ecosystem effects.

4.

Synthesis and applications

. Our results highlight an important lesson for conservation agencies
working to eradicate invasive species globally; that is, risk assessment of management interventions
must explicitly consider and plan for their indirect effects, or face substantial subsequent costs. On
Macquarie Island, the cost of further conservation action will exceed AU$24 million.

Key-words:

invasive species, cats, rabbits, sub-Antarctic, trophic cascade

Introduction

Biological invasions can lead to large-scale alterations in
ecosystem functioning. On oceanic islands, these impacts
may extend from species extinctions (Blackburn

et al

. 2004)
to more complex outcomes such as a switch from competition
to predation-dominated systems (Roemer, Donlan & Cour-
champ 2002), and in extreme cases to ‘meltdown’ of ecosystems
(O’Dowd, Green & Lake 2003). Where island systems rely on
marine-derived nutrient subsidies via seabirds, as is often the
case, the effects of invasive predators may also propagate to the
base of food webs, altering soil nutrient content, plant and soil
faunal species composition, and community characteristics.
Impacts of this kind have been recorded in a range of systems
including the Aleutians following the introduction of both
Arctic foxes

Alopex lagopus

(Croll

et al

. 2005; Maron

et al

.
2006) and rats

Rattus norvegicus

(Kurle, Croll & Tershy 2008),
the offshore islands of New Zealand owing to

R. norvegicus

and

R. rattus

invasions (Fukami

et al

. 2006), and the sub-Antarctic
islands owing to the introduction of cats (e.g. Crafford &
Scholtz 1987). Invasions of rats (Jones

et al

. 2008) and cats
(Nogales

et al

. 2004) on many islands have had similar impacts
due to their detrimental effects on seabird populations (Cour-
champ, Chapuis & Pascal 2003).
Consequently, control or eradication of invasive alien
species is widely undertaken and recommended (Courchamp

et al

. 2003; Nogales

et al

. 2004). The preferred outcome of
such interventions is the recovery of indigenous species or
ecosystems following the removal of an alien transformer.
However, management action may have other unintended
consequences. Removal of top predators may cause meso-
predator release, resulting in significant, often inadvertent

*Correspondence author. E-mail: dana.bergstrom@aad.gov.au

74

D. M. Bergstrom

et al.

© 2009 The Authors. Journal compilation © 2009 British Ecological Society,

Journal of Applied Ecology

,

46

, 73–81

consequences (Courchamp, Langlais & Sugihara 1999;
Courchamp

et al

. 2003), which can only be remedied by
further control of the mesopredator. For example, on New
Zealand’s Little Barrier Island, removal of cats resulted in
reduced breeding success of Cook’s petrel

Pterodroma cookii

,
which only increased following rat eradication (Rayner

et al

.
2007). Other impacts might also include the release of
invasive plants from herbivores (D’Antonio & Vitousek 1992).
Trophic cascades, or the extension of effects of changes in one
species’ abundance across multiple links in the food web, are
being increasingly recognized as a consequence of the effects
of eradication (Zavaleta, Hobbs & Mooney 2001; Duffy

et al

.
2007). Although the potential for such indirect effects
following management interventions is now recognized
(Zavaleta 2002; Blackburn

et al

. 2004) and has been modelled
in several contexts (e.g. Courchamp

et al

. 1999; Tompkins
& Veltman 2006), real-world examples remain relatively
uncommon. Moreover, even where the potential for such
effects is recognized by managers, the way in which these
might play out may be unexpected, given simultaneous
management interventions for several invasive species in an
area and variation among sites in the area being managed
(e.g. Rayner

et al

. 2007). Theory emphasizes the significance
of indirect effects in governing ecosystem dynamics, and
the sensitivity of these dynamics to species interactions, the
initial conditions of the system, and the ways in which
ongoing changes interact to affect the state of the system
(Chase 2007; Jordán

et al

. 2008). Moreover, it also recognizes
that the complexity of the outcomes is such that predictive
ability may often be low (Montoya, Pimm & Solé 2006).
Clearly, the unexpected consequences of management inter-
ventions are one aspect of this lack of predictability and
need to form part of the risk assessment process for all
management interventions.
Here, we combine population data on invasive herbivorous
rabbits

Oryctolagus cuniculus

(L.), plot-scale vegetation analyses,
climate analysis and landscape change detection techniques
using satellite imagery, to show how a local management
intervention, the eradication of feral cats

Felis catus

L., has
precipitated a trophic cascade leading to rapid, landscape-
wide ecosystem changes on sub-Antarctic Macquarie Island.
Specifically, we first review evidence demonstrating that cats
consumed substantial numbers of rabbits prior to their
eradication. Next, we show that since the eradication of cats,
rabbit numbers on the island have increased significantly.
We then provide evidence of impacts of rabbits on vegetation
via grazing, at both plot and landscape scale between 2000
and 2007, which cannot be attributed to other causes, such as
climate change or seasonal variation. In combination, these
data demonstrate that the removal of cats has resulted in an
increase in rabbit abundance, which has led to substantial
local and landscape-scale changes in vegetation. Although
this trophic cascade was predictable given the history of
rabbit impacts on both this and other islands (Costin &
Moore 1960; Flux & Fullagar 1992; Courchamp

et al

. 2003),
and was not entirely unexpected (Brothers & Copson 1988),
its extent was not fully anticipated. Indeed, management
reviews predicted ongoing restoration of the vegetation
following the introduction of

Myxoma

virus. We discuss why
this trophic cascade was not fully anticipated and what steps
might be taken to prevent a similar situation as further rabbit
control (to eradication) is implemented.

Materials and methods

STUDY



S ITE



AND



H ISTORY

World Heritage Macquarie Island (54

°

30

′

S, 158

°

57

′

E) is an oceanic
island in the sub-Antarctic region (Bergstrom & Chown 1999). Low-
lying, 34 km long and with a cool, maritime climate (Pendlebury &
Barnes-Keoghan 2007), it is covered in tundra-like vegetation,
featuring tussock grasses, megaherbs and bryophytes (Selkirk,
Seppelt & Selkirk 1990).
Rabbits were introduced to the island in 1878 by sealing gangs.
They initially reached very high numbers and became the main prey
of cats, which had been introduced 60 years previously (Cumpston
1968; Jones 1977; Flux & Fullagar 1992; Copson & Whinam 2001).
Hyperpredation probably resulted in the extinction of two flightless
bird species (an endemic parakeet and endemic rail, Taylor 1979).
Extensive grazing by rabbits was documented at least by the early
1950s (Taylor 1955) and by 1960, the effects were catastrophic, with
a prediction that the, ‘... grassland vegetation on Macquarie Island
is doomed to destruction’ (Costin & Moore 1960). Management of
rabbits commenced in 1968 with the introduction of the European
rabbit flea

Spilopsyllus cuniculi

(vector of the

Myxoma

virus), but it took
10 years for the flea to become widespread. The rabbit population
peaked at 130 000 in 1978 (Copson & Whinam 2001), the year when

Myxoma

virus was introduced. Unfavourable environmental con-
ditions required annual releases of the virus (Brothers & Copson
1988), but eventually rabbit numbers dropped to less than 20 000.
Island vegetation had recovered substantially 8–10 years after virus
release (Copson & Whinam 1998), and management reviews
predicted the return of several highly palatable plant species (Copson
& Whinam 2001).

Myxoma

virus spreading ceased in October 2006,
due to technical reasons.
By the mid-1980s, it had become clear that prey-switching by cats,
given decreases in rabbit availability, was detrimentally affecting
seabird populations (Copson & Whinam 2001). A cat eradication
programme commenced in 1985 and was expanded in 1998. Between
1985 and 1995, approximately 124 cats were killed per year and it was
estimated that the recruitment rate matched the kill rate (Copson 2002).
The eradication rate increased to

c

. 220 cats per year for the next 3 years,
dropping to 99 cat kills in 1999, and a single cat (the last cat) shot in
2000. Rabbit numbers then increased rapidly, and in a little more
than 5 years, they have substantially altered large areas of the island
(Scott & Kirkpatrick 2008), making its future conservation signifi-
cance questionable in the absence of further action (Miller 2007).

CAT



PREDATION



AND



RABBIT



POPULATION



ESTIMATES

Using the methods of Jones (1977), estimates of the consumption
by cats of rabbits, rats and mice were calculated for 1997, based on
estimated cat daily food intake and the proportion of food items
reported for the gut content of 49 cats examined from the 157 shot
in that year (consumption data reported in Copson & Whinam 2001;
see Supporting Methods in Supporting Information). Estimates of
annual rabbit population size were supplied by Parks and Wildlife
Service, Tasmania (PWS). Their estimates are based on monthly