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severe range contractions and the extinction of
some species (1,2). The geographic ranges of
many species are moving toward the poles or
to higher altitudes in response to shifts in the
habitats to which these species have adapted
over relatively longer periods (1–4). It already
appears that some species are unable to dis-
perse or adapt fast enough to keep up with the
high rates of climate change (5, 6). These
organisms face increased extinction risk, and,
as a result, whole ecosystems, such as cloud
forests and coral reefs, may cease to function
in their current form (7–9).
Current conservation practices may not be
enough to avert species losses in the face of
mid- to upper-level climate projections (>3°C)
(10), because the extensive clearing and
destruction of natural habitats by humans dis-
rupts processes that underpin species dispersal
and establishment. Therefore, resource man-
agers and policy-makers must contemplate
moving species to sites where they do not cur-
rently occur or have not been known to occur
in recent history. This strategy flies in the face
of conventional conservation approaches. The
world is littered with examples where moving
species beyond their current range into natural
and agricultural landscapes has had negative
impacts. Understandably, notions of deliber-
apid climatic change has already
caused changes to the distributions of
many plants and animals, leading to
ately moving species are regarded with suspi-
cion. Our contrary view is that an increased
understanding of the habitat requirements and
distributions of some species allows us to
identify low-risk situations where the benefits
of such “assisted colonization’” can be real-
ized and adverse outcomes minimized.
Previous discussions of conservation
responses to climate change have considered
assisted colonization as an option (11, 12), but
have stopped short of providing a risk assess-
ment and management framework for how to
proceed. Such frameworks could assist in
identifying circumstances that require moder-
ate action, such as enhancement of conven-
tional conservation measures, or those that
require more extreme action, such as assisted
colonization. These frameworks need to be
robust to a range of uncertain futures (13).
Uncertainties arise in climate projections and
in how species and ecosystems will respond.
Hence, calculation of the lower and upper
bounds for the probability and cost of a range
of possible outcomes may be the best strategy.
With this in mind, we developed a deci-
sion framework that can be used to outline
potential actions under a suite of possible
future climate scenarios (see figure, below).
Determining whether a species faces signifi-
cant risk of decline or extinction under cli-
mate change requires an in-depth knowledge
of the underlying species’ biology as well
as the biological, physical, and chemical
changes occurring within its environment.
The risk of extinction for many widespread,
generalist species found across a range of
habitats may be low. In this case, the option of
moving such species outside their present
Moving species outside their historic ranges
may mitigate loss of biodiversity in the face of
global climate change.
Assisted Colonization and Rapid
O. Hoegh-Guldberg,1* L. Hughes,2S. McIntyre,3D. B. Lindenmayer,4C. Parmesan,5
H. P. Possingham,6C. D. Thomas7
1Centre for Marine Studies, Australian Research Council
Centre for Excellence in Reef Studies and the Coral Reef
Targeted Research Project, www.gefcoral.org, The
University of Queensland, St Lucia, Queensland (QLD)
4072, Australia; firstname.lastname@example.org. 2Department of
Biological Sciences, Macquarie University, New South
Wales 2109, Australia; email@example.com.
3Australian Commonwealth Scientific and Industrial
Research Organisation (CSIRO) Sustainable Ecosystems,
Post Office Box 284, Canberra Australian Capital Territory
(ACT) 2601, Australia; Sue.McIntyre@csiro.au. 4Fenner
School of Environment and Society, The Australian
National University, Canberra, ACT 0200, Australia;
firstname.lastname@example.org. 5Integrative Biology, 1
University Station C0930, University of Texas, Austin, TX
78712, USA; email@example.com. 6The Ecology
Centre, Centre for Applied Environmental Decision
Analysis, The University of Queensland, St Lucia, QLD
4072, Australia; firstname.lastname@example.org. 7Department
of Biology, University of York, Post Office Box 373, York
YO10 5YW, UK; email@example.com.
*Author for correspondence.
Is there a high risk of decline or
extinction under climate change?
Are translocation and establishment
of species technically possible?
Do benefits of translocation
outweigh the biological and
socioeconomic costs and constraints?
1 Continue and improve conventional conservation approaches.
(i) Improve landscape connectivity in required direction of
colonization, (ii) genetically enhance to improve climate
robustness of populations within existing geographic range,
and (iii) reduce local stressors on population.
3 Invoke ex situ conservation practices (e.g., store egg/sperm/seed).
Is it possible to create habitat (e.g., artificial reef, wetlands) at
higher latitudes to accommodate “natural” movement?
Will the organisms arrive on their own to new habitat?
5 Wait and facilitate establishment (protect organisms as they arrive).
6 Undertake translocation (assisted migration).
Go to options 2 and 3
Mig M ration
HabHabHabHab HabHabHabHabHa HabHabHabHabHabHabHabHabHabHab HaHab ababHabHabHaHabHababH b b b b ab bHab bHab bHabH H HababHab b H H HaH HabHababHaH bHabHab b bHababHab b bH bHabH H bitaitaita itaitaitaita itaitait ita taitaitaitaita itaitaitaitait ita ita taitaitai itaitait ita itaita t ita ta itaita a a ai i i i i i it i i i it i ita at t t t t t t t t t t t t t t t t t t t t t t t t t t t t t t t t t t
Decision framework for assessing possible species translocation.Assessing the feasibility of whether or not
to attempt the movement of a species to prevent its extinction or ecosystem collapse.
Published by AAAS
on August 20, 2008
18 JULY 2008VOL 321SCIENCEwww.sciencemag.org Download full-text
ranges would be dismissed. Some species
will also disperse sufficiently to maintain
large populations and range sizes (for exam-
ple, highly dispersive insects or birds with
generalist life histories) and others may adapt
in situ (14). Where species are perceived as
being at moderate risk from climate change,
improvements in connectivity to actual or
potential habitat at higher latitudes and alti-
tudes may be sufficient (15).
Moving widespread species within their
ranges might, nonetheless, be an important
conservation option, especially where signifi-
cant ecotypic differentiation exists. Moving
individuals from “warm-adapted” popula-
tions to historically colder locations may
increase the probability of subsequent adapta-
tion as the climate changes. For example,
staghorn corals (Acroporidae) have wide lati-
tudinal ranges, with low-latitude populations
having higher temperature tolerances than
those at higher latitudes(15, 16). Populations
of staghorn (Acropora) corals have already
been lost from some high-latitude locations
because of increasing thermal stress and
declining water quality, and hence, introduc-
ing lower-latitude, heat-adapted genotypes to
these degraded sites may hold little risk (16).
Latitudinal and altitudinal clines in geneti-
cally based thermal adaptation are equally
common on land, e.g., in fruit flies (17) and
butterflies (18). Careful introduction of low-
latitude forms of a species may help to pre-
serve it at higher latitude and altitude, as the
Assisted colonization should also be con-
sidered for species whose ranges have
become highly fragmented. Movement in the
direction required by climate change may be
blocked by human-dominated landscapes
[e.g., the endangered Quino checkerspot
butterfly, Euphydryas editha quino (19)].
Dispersal processes that have been disrupted
by loss of habitat connectivity could be
restored by colonization.
Species that are confined to disappearing
habitats present the greatest challenge. Many
montane species, for example, face elimina-
tion of their habitat as suitable climatic condi-
tions migrate upward and off the top of moun-
tain ranges (7, 9, 20). In other cases, the shift
of environmental envelopes in a poleward
direction may be thwarted by natural barriers
(e.g., North African species needing to cross
the Mediterranean). In both cases, transloca-
tion of species to locations outside their his-
toric range where conditions will be suitable
in the medium- to long-term may be the only
strategy to prevent extinction.
The assisted colonization of species to a
new site depends on additional factors. The
first is whether the establishment of species at
the target location is technically feasible, and
whether the biophysical characteristics of the
new location match the needs of the species. In
cases where translocation is technically impos-
sible or is prohibitively expensive (21), it may
be possible to respond by constructing suitable
habitat at potential sites for natural coloniza-
tion. The movement of many coral reef species
to higher latitudes, for example, may depend on
the presence of benthic structure as opposed to
an existing biological community. It might be
practical, at small scales, to establish artificial,
three-dimensional reef structures ahead of
migrating coral, fish, and invertebrate species.
On land, it may be possible to restore degraded
land with habitats not originally present.
Clearly, however, there are financial and other
logistic constraints, especially at the scale of the
world’s ecosystems(10, 22).
One of the most serious risks associated
with assisted colonization is the potential for
creating new pest problems at the target site.
Introduced organisms can also carry diseases
and parasites or can alter the genetic structure
and breeding systems of local populations.
However, most major pest problems have
been created by continent-to-continent and
continent-to-island translocations or by the
transfer of organisms between distinct bio-
geographic regions within continents (e.g.,
Nile perch to Lake Victoria). Clearly, risks
escalate as species are moved across biogeo-
graphical boundaries. Introduction of the
cane toad, Bufo marinus, from its native range
in tropical America to Australia and various
tropical parts of the world has been disas-
trous. This is not the scale of translocation
that is being proposed here; we are not recom-
mending placing rhino herds in Arizona or
polar bears in Antarctica. We are, however,
advocating serious consideration of moving
populations from areas where species are
seriously threatened by climate change to
other parts of the same broad biogeographic
region (i.e., broad geographic regions that
share similar groups of organisms).
In addition to the ecological risks, socio-
economic concerns must be considered in deci-
sions to move threatened species. Financial or
human safety constraints, for example, may
make a species’introduction undesirable. It is
likely to be unacceptable to move threatened
large carnivores or toxic plants into regions that
are important for grazing livestock. Ex situ
conservation (storage of frozen gametes) may
be the only practical option for these species
until more suitable habitat can be found or
developed in the future.
The reality of a rapidly changing climate
has caught many natural-resource managers
and policy-makers unprepared. In the past, the
assisted migration of a species outside its cur-
rent range was rarely considered to be an
acceptable conservation measure, with the
exception of moving species to small, preda-
tor- or other threat-free islands (23). Larger-
scale translocations might now be needed.
Consequently, the conservation community
needs to move beyond the preservation or
restoration of species and ecosystems in situ.
Assisted colonization will always carry some
risk, but these risks must be weighed against
those of extinction and ecosystem loss.
We must contemplate the possibility that
some regions of the Earth will experience
high levels of warming (>4°C) within the next
100 years, as well as altered precipitation (10)
and ocean acidity (8). Under these circum-
stances, the future for many species and
ecosystems is so bleak that assisted coloniza-
tion might be their best chance. These strate-
gies will, however, require careful thought and
will need to be backed up by detailed scien-
tific understanding if they are to succeed.
They must also be accompanied by strategies
that address the myriad of other threats in addi-
tion to climate change that also endanger
species and ecosystems.
1. C. Parmesan, Annu. Rev. Ecol. Evol. Syst. 37, 637 (2006).
2. C. Parmesan, G. Yohe, Nature 421, 37 (2003).
3. L. Hughes, Trends Ecol. Evol. 15, 56 (2000).
4. G. -R. Walther et al., Nature 416, 389 (2002).
5. M. S. Warren et al., Nature 414, 65 (2001).
6. R. Menéndez et al., Proc. R. Soc. London Ser. B. 273,
7. D.W. Hilbert, B. Ostendorf, M. S. Hopkins, Austral. Ecol.
26, 590 (2001).
8. O. Hoegh-Guldberg et al., Science 318, 1737 (2007).
9. J. A. Pounds, M. P. L. Fogden, J. H. Campbell, Nature
398, 611 (1999).
10. Intergovernmental Panel on Climate Change (IPCC),
Climate Change 2007: The Physical Science Basis,
Contribution of Working Group I to the Fourth
Assessment Report of the IPCC, S. Solomon et al., Eds.
(Cambridge Univ. Press, New York, 2007).
11. M. L. Hunter, Conserv. Biol. 21, 1356 (2007).
12. J. S. McLachlan, J. J. Hellmann, M. W. Schwartz, Conserv.
Biol. 21, 297 (2007).
13. J. Rosenhead, in Rational Analysis for a Problematic World,
J. Rosenhead, Ed. (Wiley, New York, 1989), pp. 193–218.
14. D. K. Skelly et al., Conserv. Biol. 21, 1353 (2007).
15. A. D. Manning, in Managing and Designing Landscapes
for Conservation, D. B. Lindenmayer and R. J. Hobbs,
Eds. (Blackwell Publishing, Oxford, 2007), pp. 349–364.
16. R. Berkelmans, M. J. H. van Oppen, Proc. R. Soc. London
Ser. B. 273, 2305 (2006).
17. J. Balanyá et al., Science 313, 1773 (2006).
18. J. G. Kingsolver, K. R. Massie, G. J. Ragland, M. H. Smith,
J. Evol. Biol. 20, 892 (2007).
19. C. Parmesan, Nature 382, 765 (1996).
20. S. E. Williams, E. E. Bolitho, S. Fox, Proc. R. Soc. London
Ser. B. 270, 1887 (2003).
21. J. Fischer, D. B. Lindenmayer, Biol. Conserv. 96, 1
22. M. Scholze, W. Knorr, N. W. Arnell, I. C. Prentice, Proc.
Natl. Acad. Sci. U.S.A. 103, 13116 (2006).
23. D. T. Blumstein, J. Biogeogr. 29, 685 (2002).
Published by AAAS
on August 20, 2008