Using assisted colonisation to conserve biodiversity and restore ecosystem function under climate change

Abstract

Assisted colonisation has received considerable attention recently, and the risks and benefits of introducing taxa to sites beyond their historical range have been vigorously debated. The debate has primarily focused on using assisted colonization to enhance the persistence of taxa that would otherwise be stranded in unsuitable habitat as a consequence of anthropogenic climate change and habitat fragmentation. However, a complementary motivation for assisted colonisation could be to relocate taxa to restore declining ecosystem processes that support biodiversity in recipient sites. We compare the benefits and risks of species introductions motivated by either goal, which we respectively term ‘push’ versus ‘pull’ strategies for introductions to preserve single species or for restoration of ecological processes. We highlight that, by focusing on push and neglecting pull options, ecologists have greatly under-estimated potential benefits and risks that may result from assisted colonisation. Assisted colonisation may receive higher priority in climate change adaptation strategies if relocated taxa perform valuable ecological functions (pull) rather than have little collateral benefit (push). Potential roles include enhancing resistance to invasion by undesired species, supporting co-dependent species, performing keystone functions, providing temporally critical resources, replacing taxa of low ecological redundancy, and avoiding time lags in the provisioning of desired functions.

Full text

Perspective
Using assisted colonisation to conserve biodiversity and restore ecosystem
function under climate change
Ian D. Lunt
a
, Margaret Byrne
b,
⇑
, Jessica J. Hellmann
c
, Nicola J. Mitchell
d
, Stephen T. Garnett
e
,
Matt W. Hayward
f
, Tara G. Martin
g
, Eve McDonald-Maddden
g,h
, Stephen E. Williams
i
, Kerstin K. Zander
e
a
Institute for Land, Water & Society, Charles Sturt University, Albury, NSW, Australia
b
Department of Environment and Conservation, Bentley, WA, Australia
c
Department of Biological Sciences, University of Notre Dame, Notre Dame, IN, USA
d
Centre for Evolutionary Biology, School of Animal Biology, University of Western Australia, Crawley, WA, Australia
e
Research Institute for The Environment and Livelihoods, Charles Darwin University, Casuarina, NT, Australia
f
Australian Wildlife Conservancy, Nichols Point, Victoria, Australia
g
Climate Adaptation Flagship, CSIRO Ecosystem Sciences, Dutton Park, Qld, Australia
h
ARC Centre for Excellence in Environmental Decisions, University of Queensland, St. Lucia, Qld, Australia
i
Centre for Tropical Biodiversity and Climate Change, James Cook University, Townsville, Qld, Australia
article info
Article history:
Received 15 April 2012
Received in revised form 6 August 2012
Accepted 24 August 2012
Keywords:
Ecological replacement
Managed relocation
Climate change adaptation
Ecosystem management
Restoration
Translocation
abstract
Assisted colonisation has received considerable attention recently, and the risks and benefits of introduc-
ing taxa to sites beyond their historical range have been vigorously debated. The debate has primarily
focused on using assisted colonization to enhance the persistence of taxa that would otherwise be
stranded in unsuitable habitat as a consequence of anthropogenic climate change and habitat fragmen-
tation. However, a complementary motivation for assisted colonisation could be to relocate taxa to
restore declining ecosystem processes that support biodiversity in recipient sites. We compare the ben-
efits and risks of species introductions motivated by either goal, which we respectively term ‘push’ versus
‘pull’ strategies for introductions to preserve single species or for restoration of ecological processes. We
highlight that, by focusing on push and neglecting pull options, ecologists have greatly under-estimated
potential benefits and risks that may result from assisted colonisation. Assisted colonisation may receive
higher priority in climate change adaptation strategies if relocated taxa perform valuable ecological func-
tions (pull) rather than have little collateral benefit (push). Potential roles include enhancing resistance to
invasion by undesired species, supporting co-dependent species, performing keystone functions, provid-
ing temporally critical resources, replacing taxa of low ecological redundancy, and avoiding time lags in
the provisioning of desired functions.
Crown Copyright Ó2012 Published by Elsevier Ltd. All rights reserved.
Contents
1. Introduction ......................................................................................................... 172
2. Push versus pull assisted colonisation . . . . . . . . . . . . . . ...................................................................... 173
3. Contrasting risk–benefit profiles ......................................................................................... 173
4. Conclusions. ......................................................................................................... 176
Acknowledgements . . . . . . . . . . ......................................................................................... 176
References . ......................................................................................................... 176
1. Introduction
Assisted colonisation (also known as assisted migration or man-
aged relocation) is one option that has been proposed to conserve
biodiversity under anticipated climate change (McLachlan et al.,
0006-3207/$ - see front matter Crown Copyright Ó2012 Published by Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.biocon.2012.08.034
⇑
Corresponding author. Address: Science Division, Department of Environment
and Conservation, Locked Bag 104, Bentley Delivery Centre, WA 6983, Australia.
Tel.: +61 8 9219 9078; fax: +61 8 9334 0327.
E-mail address: margaret.byrne@dec.wa.gov.au (M. Byrne).
Biological Conservation 157 (2013) 172–177
Contents lists available at SciVerse ScienceDirect
Biological Conservation
journal homepage: www.elsevier.com/locate/biocon

2007; Hoegh-Guldberg et al., 2008; Richardson et al., 2009). As-
sisted colonisation involves the planned introduction of a popula-
tion or species beyond its current distribution where the climate is
expected to become unsuitable into new localities where the taxon
is expected to persist under future climatic conditions (Seddon,
2010). Management under climate change will require steps after
colonisation (sensu managed relocation, Richardson et al., 2009),
but introduction is the first step in helping species relocate as
the climate changes.
The concept of assisted colonisation has generated intense de-
bate over the relative benefits and risks of moving taxa beyond
their historical range (Hoegh-Guldberg et al., 2008; Mueller and
Hellmann, 2008; Ricciardi and Simberloff, 2009; Richardson et
al., 2009; Vitt et al., 2009, 2010; Hewitt et al., 2011). The potential
benefit is the retention of biodiversity that is threatened by climate
change, but introduced populations could cause unanticipated
ecological or economic damage (Mueller and Hellmann, 2008;
Ricciardi and Simberloff, 2009; Sandler, 2010). To date, the assisted
colonisation literature has focused primarily on a single rationale:
to enhance the survival prospects of the taxon being moved, or
small numbers of inter-dependent taxa, such as butterflies and
host plants (Hellmann, 2002). However, here we suggest that as-
sisted colonisation could also be undertaken to achieve a very dif-
ferent conservation goal – to maintain declining ecosystem
processes. Adopting the terminology of Seddon (2010), this type
of assisted colonisation would be classified as ecological replace-
ment – the release of ‘a species outside its historic range in order
to fill an ecological niche left vacant by the extirpation of a native
species’, and is akin to the ‘anticipatory restoration’ activities pro-
posed by Manning et al. (2009). This goal may become prominent
in future climate change adaptation programs as the impacts of cli-
mate change become more severe, but the juxtaposition of goals
has not been considered in the assisted colonisation literature
and demands benefit–risk evaluation.
In addition to direct physiological effects on organisms and
associated changes to fitness, climate change will affect many spe-
cies through indirect impacts on ecosystem structure, functions
and processes (Diaz and Cabido, 1997; Petchey et al., 1999; Dale
et al., 2001; Gilman et al., 2010). Changes in the abundance of dom-
inant, foundation and keystone species will alter ecosystem pro-
cesses that will, in turn, affect many associated organisms.
Declines in dominant forest trees, for example, lead to changes in
micro-climatic conditions, nutrient and water cycles, habitat struc-
ture, and disturbances such as fire regimes (Cochrane, 2003; Foley
et al., 2007; Van Mantgem et al., 2009).
Reviews of climate change adaptation strategies include a wide
range of approaches for maintaining ecological processes such as
nutrient cycling, hydrology, species interactions, habitat provision,
dispersal and disturbances (Millar et al., 2007; Bennett et al., 2009;
Mawdsley et al., 2009; Steffen et al., 2009; Lindenmayer et al.,
2010). Additionally, landscape and restoration ecologists have pro-
posed that vegetation be established and restored across local and
regional scales to enhance ecological processes and functions that
may in turn maintain biodiversity (Hobbs and Harris, 2001; Millar
et al., 2007; Manning et al., 2009; Seddon, 2010). Proposals to use
assisted colonisation for ecosystem benefit are not widely encom-
passed by the existing literature and its decision frameworks
(Sandler, 2010). We suggest that acknowledgement of a broader
array of motivations for assisted colonisation will enhance our
ability to contribute to the development of national and regional
climate change adaptation strategies.
Therefore, we contrast two rationales for introductions of species
outside their historical ranges: (1) direct conservation of one or
more species diminished in their native range and (2) restoration
or maintenance of a declining ecosystem function, and consider
how these rationales could be combined. We restrict our attention
to introductions for conservation purposes, but our framework
could also encompass a wider range of goals, including utilitarian
services such as timber production (McKenney et al., 2009).
2. Push versus pull assisted colonisation
For simplicity, we characterize these two contrasting rationales
for assisted colonisation as ‘push’ and ‘pull’ strategies (Fig. 1). Push
strategies that focus on conserving individual taxa or small groups
of inter-dependent taxa are already widely discussed in the as-
sisted colonisation literature. In these cases, issues such as rarity
and threat guide the selection of target taxa, and populations are
‘pushed’ into one or more localities where it is expected that they
will maintain viable populations for an extended period under cli-
mate change (e.g. Willis et al., 2009). Risk assessments are required
to ensure that informed decisions are made to relocate taxa such
that there is minimal impact on other species where they are intro-
duced (Burbidge et al., 2011).
In contrast, assisted colonisation that is also motivated by a de-
sire to restore ecosystem function should expect to have an appre-
ciable impact at the recipient site. In such ‘pull’ scenarios, desired
ecosystem functions and potential recipient sites would first be
identified, and appropriate candidate species would then be
‘pulled’ into recipient sites to maintain or restore the specified
function (Fig. 1). Relocation of taxa may be undertaken to deliver
ecological functions that are directly affected by climate change,
or where climate change exacerbates other causes of decline, such
as fragmentation or salinisation. For example, consider a tree spe-
cies that is declining (directly or indirectly) due to climate change
and provides nest holes to a bird community. Pull assisted coloni-
sation would ask which species of tree might persist regionally in
the future to provide nesting habitat for birds, and could include
the option to introduce multiple species, if a range of species are
capable of performing the desired function. Indeed, bet-hedging
approaches that relocate multiple taxa and genotypes may be pru-
dent given uncertainties about future species performances under
climate change (Beale et al., 2008). Relocation of multiple taxa will
also be important for co-dependent species, such as insects and
their host plants or species and their parasites.
In push + pull assisted colonisation, selection of species would
be guided by the function to be performed in the recipient site,
as well as the conservation status of the relocated species. Oppor-
tunities for push + pull assisted colonisation may be limited where
rare taxa have restricted distributions due to biological constraints
because they are unlikely to have the capacity to influence ecosys-
tem processes strongly in recipient sites. However, there may be
greater opportunities to maximize conservation outcomes using
‘push + pull’ assisted colonisation in landscapes where historical
stochasticity has been a major driver of rarity (Yates et al., 2007).
While further research is required to develop decision support
tools to guide pull assisted colonisation strategies, this approach
may receive high priority where relocated taxa: (1) perform ‘key-
stone’ functions that generate a cascade of ecological services
(e.g. ecosystem engineers); (2) provide ecosystem services that
are unique or have low levels of ecological redundancy; (3) provide
functions that take long periods to become effective, e.g. hollow-
bearing trees; (4) enhance resistance to invasion by undesired
species; (5) fill temporal resource gaps driven by climate-driven
phenological shifts; and (6) maintain valued species that are highly
dependent on other species. Descriptions and examples of these
functions are provided in Table 1.
3. Contrasting risk–benefit profiles
Assisted colonisation for goals of conservation introduction
or ecological replacement both share a common mechanism of
I.D. Lunt et al. / Biological Conservation 157 (2013) 172–177 173

relocating taxa (or genotypes) beyond their historical range in or-
der to conserve biodiversity under climate change. Nevertheless,
we recognise that the two approaches have very different risk
and benefit profiles.
Assisted colonisation for species conservation benefits the relo-
cated taxon only, and minimal (if any) collateral benefits are envis-
aged for other taxa or processes in recipient sites. Indeed, the
current assisted colonisation literature emphasizes the need to
avoid relocations that may alter the composition, structure or func-
tion of recipient sites in a major way (Mueller and Hellmann, 2008;
Ricciardi and Simberloff, 2009). Nevertheless, push assisted coloni-
sation may present risks to recipient sites and ecosystems (and
potentially to the broader environment and economy) if relocated
taxa have negative impacts on other species and those impacts
spread to additional locations (Ricciardi and Simberloff, 2009;
Richardson et al., 2009). Thus, the risk–benefit profile for push as-
sisted colonisation is one of localized benefit and potentially wide
risks (akin to private benefits versus public risks in human enter-
prises), depending on the taxa under consideration (Hoegh-Guld-
berg et al., 2008; Ricciardi and Simberloff, 2009; Richardson et
al., 2009; Burbidge et al., 2011).
By focusing on the conservation of threatened species as
motivation for assisted colonization, ecologists may greatly un-
der-estimate potential benefits that may arise from such intro-
ductions in providing ecosystem services. In contrast to push
assisted colonisation, taxa also introduced as ecological replace-
ments for a degraded component of an ecosystem could have
multiple beneficiaries – including all taxa that benefit from the
environmental functions or processes that relocated species
provide. Thus, the potential biodiversity benefits provided by
push + pull assisted colonisation are far greater if their impact
flows broadly across an ecosystem. Because maintenance of eco-
system processes is a key component of climate change adapta-
tion strategies (Millar et al., 2007; Mawdsley et al., 2009; Steffen
et al., 2009; Lindenmayer et al., 2010), assisted colonisations that
maintain ecosystem function may be prioritized above those that
conserve threatened species, if relocation costs are similar, ben-
efits are greater and risks deemed acceptable. Combined strate-
gies that focus on threatened species conservation and
maintenance of ecosystem function may also rate highly under
constrained management budgets, given potential benefits to
both the relocated species and recipient ecosystems.
However, assisted colonisation intended to have a significant
collateral impact also presents far greater risks, since relocated
taxa are intended to have a substantial, as opposed to negligible,
impact on specified ecosystem processes in recipient sites. For
example, a relocated species could be structurally dominant or a
keystone species, which would be unlikely to be relocated under
current decision support frameworks for assisted colonisation
(Hoegh-Guldberg et al., 2008; Richardson et al., 2009). Candidate
taxa for assisted colonisation could now include taxa with high im-
pact but low dispersal capacity, to minimize the potential for relo-
cated taxa to spread to unwanted areas. In some cases, dispersal
risks may be moderated by landscape context (McIntyre, 2011).
For example, assisted colonisations designed to have an apprecia-
ble collateral impact might receive greater attention in degraded
remnants in fragmented landscapes, where risks to existing taxa
are lower and where such introductions would build upon existing
interventions designed to enhance regional biodiversity (Fischer et
al., 2006; Lindenmayer et al., 2010).
A
B
C
Fig. 1. Contrasting types of assisted colonisation. In (a) specific species assisted colonisation – a specified taxon threatened with decline under climate change is moved
(‘pushed’) into one or more optional recipient sites where future persistence is predicted to be high. In (b) ecological replacement assisted colonization – one or more taxa are
relocated (‘pulled’) to a specified recipient site to maintain or restore an ecosystem process and/or function in the recipient site that is declining due to climate change. In (c)
assisted colonisation is used to ‘push’ a threatened taxon into a recipient site, but in so doing restores an ecosystem process and/or function that is declining due to climate
change, thus achieving outcomes from options (a and b). Dark shading in arrows indicates whether the introduction is motivated by concerns about source populations (a;
push), recipient sites (b; pull), or both (c; push + pull).
174 I.D. Lunt et al. / Biological Conservation 157 (2013) 172–177

Existing decision support tools for assisted colonisation may
be relatively easily expanded to accommodate a goal of ecosys-
tem restoration. For example, the decision making framework
developed by Richardson et al. (2009) requires the addition
of diminished ecosystem function as a potential motivation for
undertaking assisted colonisation, plus the expansion of the con-
cept of ‘focal impact’ to include collateral benefits (not just col-
lateral impacts). Populating these frameworks for push + pull
assisted colonization will require a revised approach to the eval-
uation of potential impacts. For example, impacts that are gener-
ally considered as risks in assisted colonisation motivated to
benefit a threatened taxon would be considered as potential
benefits in movement of species to achieve ecosystem function.
In any risk evaluation, the relevant comparison is not of assisted
colonisation against the status quo, but assisted colonisation
against anticipated losses under continuing climate change
(Schwartz et al., 2009). The uncertainties inherent in assessment
of the scale and direction of climate change itself, and the vulner-
ability of species to that change, are key factors in assessment of
push assisted colonisation adaptation strategies. For assisted colo-
nisation designed to have push + pull impacts, additional uncer-
tainties occur in relation to the potential for selected taxa to
establish self-perpetuating populations that contribute to ecologi-
cal function at a site within an appropriate time frame.
If assessments reveal that the benefits of undertaking either
assisted colonisation option outweigh the risks, then the question
becomes one of timing of implementation and monitoring of im-
pacts. McDonald-Madden et al. (2011) present a quantitative
framework to guide when to move species in push assisted coloni-
sation activities, based on population dynamics in the source hab-
itat, predicted dynamics in recipient sites, the cost of relocation
and species recovery potential. Additional factors need to be con-
sidered to accommodate push + pull assisted colonisation, includ-
ing the predicted dynamics of declining ecosystem processes, the
thresholds at which major change may occur, and the need to bal-
ance the delivery of the ecological function with the climate suit-
ability for the selected species. Development of success criteria
for evaluation of push assisted colonisation is relatively straight-
forward (Burbidge et al., 2011). For push + pull assisted colonisa-
tion there is the added challenge of monitoring for the continued
delivery of an ecological function with the potential complexities
of interdependences among biotic and abiotic components of the
ecosystem.
Further consideration needs to be given to the economic costs
and benefits associated with all forms of assisted colonisation. This
paper has emphasized the ecological value of species in sustaining
ecosystem services and supporting species interactions. These ser-
vices have economic value as well. For example, species that pro-
Table 1
Example functions potentially vulnerable to climate change that could be enhanced by assisted colonisation.
Functional issue for ecosystem Description Example(s)
Loss of keystone species Keystone species interact strongly with other
functions and generate a cascade of ecological
services
Many forests and woodlands in Australia are dominated by long-lived
Eucalyptus trees. These dominant, ‘foundation’ species control functions and
processes including stand structure and micro-climate, water and nutrient
cycling and fire behavior (Manning et al., 2006). Species replace each other
across climatic gradients so readily lend themselves to assisted colonisation
in anticipation of climate change
Five species of prairie dogs Cynomys spp. have a strong influence on the
functioning of grassland ecosystems in North America but have declined by
98% in the last 200 years (Hoogland, 2006). The existence of climate-related
relictual populations (Mead et al., 2010) suggests natural dispersal has been
too slow to keep up with historical climate change. There may be potential
to assist movement of different prairie dog species to retain ecosystem
services as future climates change
Loss of a unique ecosystem service Provision of ecosystem services with low
ecological redundancy that support the
persistence of other species
Larvae of the endangered European longhorn beetle affect a profound
change on the microstructure of the bark of the wild oak, enabling numerous
other endangered insects to flourish in the beetle’s presence (Buse et al.,
2008). Assisted colonisation of the European Longhorn beetle could generate
collateral benefits to invertebrate fauna at the recipient site
Sheep grazing is an essential to conservation of the Chalkhill Blue butterfly
Polyommatus coridon in the UK (Brereton et al., 2008). If conditions become
too warm for existing races of sheep on the downs, there are several others
that could be brought in as replacements (Gibbons and Lindenmayer, 2002)
Loss of a function that has a time
lag to effectiveness
Functions that take decades or longer to establish
and become effective
Tree hollows provide nesting habitat and retreat sites in almost all forest
types, with approximately 10–31% of reptiles, amphibians, birds and
mammals utilizing tree hollows in Australian ecosystems (Gibbons and
Lindenmayer, 2002). Declining tree species could be replaced with warmer-
or drier-adapted species
Biological control agent becoming
increasingly ineffective in a
changing climate
Species whose introduction to a recipient
ecosystem could prevent or reduce the invasion
of undesired species
Lesser St John’s Wort beetles are effective biological control agents in cold
climates but need to be replaced with Great St John’s Wort beetles for
effective St John’s wort (Hypericum perforatum) control in Mediterranean
climates (Schöpsa et al., 1996)
Increasing temporally mismatch of
resources
Functions that fill temporal resource gaps driven
by climate-driven phenological shifts
Plant species flowering at various times of the year provide resources for
pollinators. Banksia baxterii is one of the few plants that flower in autumn in
south western Australia and is major nectar resource for vertebrate
pollinators, particularly honey possums, a distinct lineage of marsupials. It is
vulnerable to increasing temperature (Yates et al., 2009) and may need to be
replaced by other autumn flowering plants
Maintenance of co-dependence
among species
Functions provided by one species that both
maintain and depend on functions provided by
other species
Terrestrial orchids have strong mutualistic dependence on pollinators that
tends to be site specific (unlike the mutualism with fungi; Waterman et al.,
2011) so that neither orchid nor pollinator could be moved without the
other. Similarly many pollinators have a host of other specializations that
would also need to be considered in assisted colonisation (Pemberton, 2010)
I.D. Lunt et al. / Biological Conservation 157 (2013) 172–177 175

mote pollination services might increase agricultural value. To our
knowledge, no one has investigated economic outcomes from as-
sisted colonization, but it may be possible for particular species
and ecosystems.
This conceptual integration of push + pull motivations in as-
sisted colonisation activities may help to reinforce synergies be-
tween the contrasting theoretical frameworks that underlie the
two approaches (Fig. 2). Push assisted colonisation draws heavily
on single-species population biology, invasion ecology, and an
extensive literature on management of threatened species and
small and declining populations (Simberloff, 1998; Parker et al.,
1999; Purvis et al., 2000). By contrast, push + pull assisted coloni-
sation has stronger theoretical foundations in landscape and resto-
ration ecology at ecosystem scales (Noss, 1990; Fischer et al., 2006;
Hobbs and Cramer, 2008; Lindenmayer et al., 2008). From an inva-
sion ecology perspective, introduction of a high impact taxon is
usually seen as inherently undesirable, whereas introduction of a
functional dominant is commonly viewed as a critical component
of a successful restoration strategy. Clearly, a wide range of intel-
lectual traditions will need to be drawn upon to manage assisted
colonisation effectively and safely within climate change adapta-
tion strategies for biodiversity conservation.
4. Conclusions
We emphasise that we are not promoting the adoption of any
particular assisted colonisation strategy, and we advocate that all
assisted colonisation activities must be subject to comprehensive
risk assessments and ongoing monitoring and management.
However, we encourage ecologists and managers to consider
how assisted colonisation could be adopted to achieve broader
goals than the persistence of a single, or just a few, threatened
species.
Acknowledgements
The perspective presented in this paper was developed at a
workshop on assisted colonisation supported by the Terrestrial
Biodiversity Adaptation Research Network of the National Climate
Change Adaptation Research Facility (NCCARF) in Australia.
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