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Directions in reintroduction biology
Doug P. Armstrong
1,2
and Philip J. Seddon
3,4
1
Wildlife Ecology Group, Institute of Natural Resources, Massey University, Private Bag 11222, Palmerston North, New Zealand
2
Oceania Section Chair, IUCN/SSC Reintroduction Specialist Group
3
Department of Zoology, University of Otago, PO Box 56, Dunedin, New Zealand
4
Bird Section Chair, IUCN/SSC Reintroduction Specialist Group
Reintroductions are attempts to return species to parts of
their historical ranges where they were extirpated, and
might involve release of either captive-bred or wild-
caught individuals. The poor success rate of reintroduc-
tions worldwide has led to frequent calls for greater
monitoring, and since 1990 there has beenan exponential
increase in the number of peer-reviewed publications
related to reintroduction. However, these publications
have largely been descriptive accounts or have addressed
questions retrospectively based on the available data.
Here, we advocate a more strategic approach where
research and monitoring targets questions that are ident-
ified a priori. We propose ten key questions for reintro-
duction biology, with different questions focusing at the
population, metapopulation and ecosystem level. We
explain the conceptual framework behind each question,
provide suggestions for the best methods to address
them, and identify links with the related disciplines of
restoration ecology and invasion biology. We conclude by
showing how the framework of questions can be used to
encourage a more integrated approach to reintroduction
biology.
Introduction
The term ‘reintroduction biology’ refers to research under-
taken to improve the outcomes of reintroductions and other
translocations (Box 1) carried out for conservation pur-
poses. Reintroduction attempts have occurred for at least
100 years [1], but the field of reintroduction biology was
born much later in response to the poor success of reintro-
duction programmes. Although there have been some
spectacular success stories (e.g. Ref. [2]), it became clear
during the 1980s that most reintroduction attempts were
failing and that little was being learned in the process [3–
6]. This situation led to the formation of the International
Union for Conservation of Nature and Natural Resources
Species Survival Commission (IUCN/SSC) reintroduction
specialist group (RSG; http://www.iucnsscrsg.org/) in 1988,
and to numerous calls for greater monitoring (e.g. Refs [7–
9]). The past 20 years have seen not only a substantial
increase in monitoring, but also an explosion in the number
of reintroduction-related papers in peer-reviewed journals,
from <5 per year during the early 1990s to >50 per year
currently [10].
Although the growing reintroduction literature is a
valuable source of information, it largely consists of
descriptive accounts of reintroduction programmes or
retrospective analyses [10]. Therefore, the research ques-
tions addressed have largely been driven by the monitoring
data available rather than the monitoring being driven by
the questions. Although any monitoring will produce use-
ful information, unfocused monitoring is an inefficient use
of conservation funds in comparison to monitoring
designed to address questions identified a priori [11].
Unfocused monitoring often leads to conclusions being
derived solely by induction (i.e. from post hoc detection
of patterns in data), which is notorious for leading to poor
management of wildlife [12]. Failure to identify questions a
priori might also result in the most important data not
being collected or might result in monitoring effort not
being allocated to the projects where it is most needed.
Our agenda here is to promote a more strategic
approach to reintroduction biology. Although progress in
this field depends partly on the adoption of stronger modes
of inference, this point has been made previously [10,13,14]
and we do not want to labour it here. Our point is that
reintroduction biology will progress faster if researchers
focus on the questions that need to be answered to improve
species recovery and ecosystem restoration. That is, rein-
troduction biologists should nominate the key research
questions then use the best methods available to answer
them, rather than addressing the questions that are most
easily answered or that lend themselves to the most rig-
orous science.
We propose ten key questions for reintroduction biol-
ogists to address, with different questions focusing on the
population level, metapopulation level and ecosystem level
(Figure 1). We explain the conceptual framework behind
the questions, provide suggestions for methods to address
them, and point to links with the related disciplines of
restoration ecology and invasion biology. We conclude by
showing how the framework of questions can be used to
encourage a more integrated approach to reintroduction
biology.
Key questions at the population level
Reintroduction biology has traditionally focused on the
factors determining whether reintroductions are success-
ful or not. These factors can be divided into those affecting
establishment and spread of populations, following the
division often made in invasion biology [15], but we suggest
that distinguishing between establishment and persist-
ence is more appropriate for reintroduction (Figure 1).
Persistence is more general, because it applies to
populations that are geographically bounded, and which
therefore grow through increasing density rather than
Opinion
Corresponding author: Armstrong, D.P. (D.P.Armstrong@massey.ac.nz).
20 0169-5347/$ – see front matter ß2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.tree.2007.10.003 Available online 21 December 2007
increasing range, and also to populations that have
reached carrying capacity. The dichotomy is useful because
reintroduced populations can fail to survive the establish-
ment phase in conditions that would enable long-term
persistence once established.
Population establishment
Small release groups can fail to establish populations
owing to either chance fates of those individuals (demo-
graphic stochasticity), or to low reproduction or survival
rates at low densities (Allee effects) [16]. Therefore, the
first key question (Q1) is: ‘how is establishment probability
affected by the size and composition of the release group?’
(Figure 1). Populations might also fail to establish owing to
high post-release dispersal, or to low survival or reproduc-
tion rates while organisms recover from translocation
stress or acclimatise to the release site. These factors
are related, because high post-release dispersal and
mortality creates a large disparity between the release
group size and the effective initial population size. This
disparity can be reduced through pre- and/or post-release
management, so the second key question (Q2) is: ‘how are
post-release survival and dispersal affected by pre- and
post-release management?’ (Figure 1). This can, in turn, be
subdivided into questions about effects of specific man-
agement practices. Release strategies intended to facilitate
acclimatisation are often termed soft release [5], but it
cannot be assumed that the strategies used will have the
desired effect. For example, although it is often believed
that dispersal and/or mortality can be reduced by holding
animals at the release site for some period, the exper-
iments conducted have not generally supported this notion
(e.g. Refs [17–19]).
Questions about factors affecting post-release survival
and dispersal lend themselves to experimental investi-
gation (e.g. Refs [17–21]). It is also possible to experimen-
tally manipulate the size of the release group [22], but such
experiments require multiple reintroduction attempts and
are unlikely to be feasible with threatened species. A better
approach is usually to model the relationship based on the
available data on survival, reproduction and dispersal
rates for the species and system in question [23–25].We
caution that comparative analyses of reintroduction suc-
cess rates for multiple species and systems (e.g. Ref [6])
probably give a misleading indication of the relationship
between release group size and establishment success.
This is because low numbers are generally released when
reintroductions are perceived to have low probability of
success or if the reintroduction programmes are poorly
resourced, creating a bias toward success with large
release groups. Where post-release dispersal and mortality
are low, populations can potentially establish successfully
from <10 released individuals [26].
Habitat effects on population persistence
Regardless of the strategy used to establish a population, a
reintroduction will fail if the habitat (Box 2) at the release
site cannot support the species. Consequently, the first key
question about population persistence (Q3) is: ‘what habitat
Box 1. Reintroduction terminology
The terminology related to reintroduction is used inconsistently,
resulting in considerable confusion. We follow the original termi-
nology outlined in the IUCN position statement on the translocation
of living organisms [3]. That document defined ‘translocation’ as
any movement of living organisms from one area to another, and
recognized three types of translocation:
Introduction: movement of an organism outside its historically
known native range.
Reintroduction: intentional movement of an organism into a part
of its native range from which it has disappeared or become
extirpated in historic times.
Re-stocking: movement of individuals to build-up an existing
population.
These definitions are clear, simple and workable, with translocation
providing a useful catch-all term and the other terms being mutually
exclusive of one another. By contrast, the restriction of the term
‘translocation’ to movement of wild individuals in the later IUCN
reintroduction guidelines [9] meant that it partially overlapped with
all of the other terms and there was no general term that could be
used to describe all types of movements. Some authors (e.g. Ref
[49]) responded to this confusion by further re-defining the
terminology. However, we suggest that the best approach is to
return to the original terminology described above.
Figure 1. Ten key questions for reintroduction biology, divided into questions at the population, metapopulation and ecosystem level. Population-level questions are
divided into questions about establishment and persistence of reintroduced populations.
Opinion TRENDS in Ecology and Evolution Vol .2 3 No .1
21
conditions are needed for persistence of the reintroduced
population?’ (Figure 1). Assuming the number of organisms
released is below carrying capacity, the essential pre-requi-
site for persistence is positive growth and this should be the
main target of reintroduction programmes. The IUCN rein-
troduction guidelines [9] emphasize that the original cause
of decline must be identified and eliminated before a species
can be reintroduced to a site. Although this sounds simple,
assessing the conditions needed for growth is seldom trivial,
particularly when assessing reintroduction sites before
release (Box 2) given that no data are usually available
for the species at the site. Invasion biologists face the same
challenge when trying to predict habitats that can be
invaded (e.g. Ref [27]), thus similar habitat modelling
methods can be applied to projecting fates of invasions
and reintroductions. After release, modelling of data on
survival, reproduction and dispersal rates can be used to
estimate the rate of population growth, and to quantify
uncertainty in this relationship.
It might also be possible to use an adaptive manage-
ment approach whereby habitat conditions are manipu-
lated over time and/or space to determine requirements for
population growth. For example, the failure of New Zeal-
and hihi (Notiomystis cincta) reintroductions to islands
with regenerating forest was suspected to be a result of
insufficient food availability, so a series of food supple-
mentation experiments were performed at a release site to
estimate the effects of presence, quality and distribution of
supplementary food on the growth rate of the reintroduced
population [28]. Such adaptive management could be used
to develop criteria for future reintroduction sites, as well as
for protocols for the population under management.
Genetic effects on population persistence
Although habitat conditions will be the main drivers of
population growth, it will also be affected by the intrinsic
nature of the organisms. Therefore, the next key question
(Q4) is: ‘how will genetic makeup affect persistence of the
reintroduced population?’ (Figure 1). A population could
fail to grow from the outset if the founder group were highly
inbred or of inappropriate provenance (i.e. genetically
adapted to conditions different from those at the release
site). However, a more probable problem is reduction in
genetic diversity over time, potentially resulting in
inbreeding depression and declining immunocompetence.
Such effects are probable if populations remain small,
hence ongoing management might be needed. For example,
individuals are periodically translocated among reintro-
duced populations of some New Zealand bird species to
reduce inbreeding. Although such management will be
necessary in some instances, it can potentially have nega-
tive impacts by preventing local adaptation or by wasting
resources that could be invested elsewhere [29]. Research
is needed in this area, not only to predict how management
will affect genetic diversity of reintroduced populations
(e.g. Ref [30]), but also to predict effects on population
growth and persistence. Making such predictions requires
estimating the effects of genetic diversity on survival and
reproduction of reintroduced populations, then projecting
the impacts using population modelling. We are not aware
of any study that has done this as yet.
A conceptual framework for population establishment
and persistence
Graeme Caughley [16] noted that strategies for conserving
populations tend to follow either the small population
paradigm, which deals with the effect of smallness on
populations, or the declining population paradigm, which
deals with causes of decline and its reversal. Strategies for
establishing reintroduced populations (Q1, Q2) ultimately
boil down to ensuring that the effective initial population
size is sufficient, so fall into the small population para-
digm, and strategies for ensuring that persistence is not
compromised by genetic makeup (Q4) also largely fall
under this paradigm. However, strategies for ensuring
that habitat conditions enable persistence (Q3) are within
the declining population paradigm, because the key issue
is ensuring that the conditions causing the previous decline
have been reversed. Following Caughley’s lead, we encou-
rage reintroduction biologists to consider both paradigms
but to particularly ensure that they incorporate the declin-
ing population paradigm in their research programmes by
assessing the habitat conditions needed for persistence of
populations. Although questions about establishment are
usually easier to answer, in our experience the key factors
ultimately found to determine whether reintroductions
succeed have been habitat factors (e.g. food availability
and exotic predators).
Key questions at the metapopulation level
When strategies are extended to multiple populations of a
species, the resulting questions can be considered to be at
the metapopulation level. The term metapopulation is
traditionally used to describe networks of semi-isolated
populations connected by natural dispersal [31]. However,
conservation managers also use the term to describe net-
works of populations that can be connected by transloca-
tion [29], and any translocation involves at least a simple
metapopulation consisting of the source population and
recipient population.
Box 2. The habitat concept in reintroduction biology
Although habitat is a central concept in ecology and wildlife
management, ‘habitat’ and related terms are used inconsistently
in the literature, and usually incorrectly with respect to their original
meanings [50]. Hall et al. [50] observed that ‘habitat quality’ should
refer to the ability of the environment to provide conditions
appropriate for individual and population persistence. They also
observed that habitat quality should be explicitly linked to survival
and reproduction rates of the species in question, and should not be
equated with vegetation features. Consequently, when we refer to
‘habitat conditions’ needed for persistence of a reintroduced
population (Figure 1), we refer to all aspects of the environment,
including food, predators and parasites. This traditional use of the
habitat concept should encourage reintroduction biologists to
carefully consider the biological requirements of species rather
than focusing on rapidly assessable features such as vegetation,
and to measure habitat quality directly using post-release data on
survival and reproduction. Although sophisticated analyses can be
used to predict habitat quality before release (e.g. Ref [51]), it is
essential to consider whether the data capture the features that are
most relevant to the species, especially when the analyses rely on
rapid acquisition of data from geographical information systems.
Opinion TRENDS in Ecology and Evolution Vol .2 3 No .1
22
Impact on source populations
Although reintroduction biology has traditionally focused
on the fates of the reintroduced populations, the potential
benefits of establishing these populations need to be
balanced against the impact to source populations regard-
less of whether they are captive [32] or wild [33]. Therefore,
the first key question at the metapopulation level (Q5) is:
‘how heavily should source populations be harvested?’
(Figure 1). This can be addressed through population
modelling, but accurate projections require a good under-
standing of populations’ regulatory mechanisms (i.e. the
compensatory increases in survival and/or reproduction
following density reduction). Harvesting provides density
manipulations that are invaluable for understanding these
mechanisms, so lends itself to adaptive management. For
example, the North Island robin (Petroica longipes) popu-
lation on Tiritiri Matangi Island is being repeatedly
harvested for reintroduction to other sites, and the infor-
mation gained from each density manipulation is used to
refine the model used to recommend the size and frequency
of subsequent harvests [33].
Allocation of translocated individuals among sites
Moving beyond a single source and recipient population,
species recovery programmes often involve multiple rein-
troductions and many potential reintroduction sites.
Therefore, another key question (Q6) is: ‘what is the
optimal allocation of translocated individuals among
sites?’ (Figure 1). In our experience such allocations are
decided on an ad hoc basis during recovery group meetings,
but they could potentially be decided using theoretically
derived optimisation strategies [34]. Similar methods
could also potentially be used to decide the optimal allo-
cation of management effort among sites.
Using translocation to compensate for isolation
The final key question at the metapopulation level (Q7) is:
‘should translocation be used to compensate for isolation?’
(Figure 1). This is always considered, at least implicitly,
because reintroduction is unnecessary if the species is
likely to recolonise the site naturally. What is rarely
considered is the fact that some local extinctions could
be owing primarily to metapopulation dynamics following
habitat fragmentation, meaning that translocation could
be used to restore distributions without management of
habitat. However, if the local extinctions were owing to
local declines in habitat quality, this strategy would be
disastrous. Addressing this issue requires methods for
resolving the roles of habitat quality and metapopulation
dynamics in species declines, an endeavour that is by no
means trivial [35].
Key questions at the ecosystem level
Although the goal of reintroduction has traditionally been
species recovery, reintroductions increasingly occur within
the context of ecosystem restoration programmes. Despite
this, there has been surprisingly little overlap between the
disciplines of reintroduction biology and restoration
ecology [36]. The reintroduction literature has taken a
single-species perspective and focused on animals [37],
whereas the restoration literature has focused on abiotic
factors and vegetation [38,39]. We suggest that there are
three key questions for reintroduction biology at the eco-
system level, and all of these bridge the two disciplines.
Historic range of target species and its parasites
The first key question at the ecosystem level (Q8) is: ‘are
the target species/taxon and its parasites native to the
ecosystem?’ (Figure 1). The IUCN reintroduction guide-
lines [9] stress that the organisms used for reintroduction
should be as close as possible genetically to those originally
found in the area, and that introducing (Box 1) a species
outside its historic range should be considered only if there
is no suitable habitat available within that range. Asses-
sing the historic ranges and genetic provenances of species
proposed for translocation is, therefore, a fundamental
part of reintroduction biology. However, the parasites
carried by a species are considered from a veterinary
perspective, usually with no consideration as to whether
those parasites already occur at the release site [40] or
occurred there historically. The key foci of disease-screen-
ing procedures should be to restore host–parasite relation-
ships and prevent introduction of non-native parasites, so
need to be accompanied by research designed to recon-
struct historic distributions of parasites.
These issues are likely to become increasingly complex
in the future, given that global climate change is shifting
the distributions of suitable habitat for many species [41].
At least some programmes will have to focus less on
restoring what was originally found at a site and instead
foucs on facilitating development of ecosystems suitable for
new climatic regimes.
Ecosystem effects of releases
The next key question (Q9) is: ‘how will the ecosystem be
affected by the target species and its parasites?’ (Figure 1).
This is closely related to Q8, because it can be argued that
the primary goal of translocations should be to restore
ecosystem function rather than species composition.
Although the IUCN reintroduction guidelines [9] make
provision for introducing species to new areas to satisfy
species recovery goals (see above), a better justification
might be to restore the functional roles of extinct species
[42]. Research designed to project impacts of translocated
species is needed to justify such introductions, to deter-
mine which parasites it is most important to screen for, and
to prioritise reintroduction of ecosystem engineers [43] and
other species crucial to ecosystem function. Studies doc-
umenting previous ecosystem-level impacts of reintroduc-
tions [44,45] are relevant here, as are methods developed
by invasion biologists for projecting impacts of new species
on ecosystems [46].
Order of reintroductions
The final key question (Q10) is: ‘how does the order of
reintroductions affect the ultimate species composition?’
(Figure 1). This question comes up frequently in the course
of restoration programmes conducted in New Zealand, but
decisions are currently made based on intuition. Because
the question often concerns species at different trophic
levels, one promising area for research is the functional
responses between predator and prey species that are
Opinion TRENDS in Ecology and Evolution Vol .2 3 No .1
23
likely to be reintroduced [47], because these responses
could determine the ability of the predator and prey to
coexist in relation to their initial densities.
The future of reintroduction biology
Reintroduction biology will always have a strong emphasis
on case studies because there is no substitute for local
knowledge of species and systems. Although meta-analyses
might have a greater role in future research, useful meta-
analyses depend on good data from individual case studies,
and comparative analyses of simple statistics – such as
success rates – will produce misleading or trivial results
in the absence of such data. Our agenda here is to promote a
more strategic approach so that the maximum value can be
derived from the case studies being conducted. We envision
five ways in which a more strategic approach can be devel-
oped using our proposed framework of questions.
First, as we emphasized at the outset, designing
monitoring to address questions identified a priori will
increase the amount of useful knowledge obtained from
limited conservation funds.
Second, if researchers consider our full framework of
questions, the scope of reintroduction research will
increase dramatically. Reintroduction research [10] has
so far focused on only four of the ten key questions we
propose (Q1–Q3, Q5), with little attention given to meta-
population- and ecosystem-level questions.
Third, the framework of questions can be used to
improve communication between reintroduction research-
ers and practitioners. For example, the standard operating
procedures for New Zealand translocations are currently
being revised to ensure that practitioners consider the
questions suggested here. Practitioners might be able to
answer most of the questions based on prior expert knowl-
edge and then to seek research support to address ques-
tions where the greatest uncertainty exists.
Fourth, the framework of questions will encourage
researchers and practitioners to think beyond their own
projects. That is, monitoring programmes can be designed
not just to address the key questions identified for the
current reintroduction, but to address questions of interest
to other projects throughout the world. Some reintroduc-
tions provide ideal model systems to address general ques-
tions and it is important to take advantage of these
systems.
Fifth, the framework of questions will encourage
researchers and practitioners to build on the previous
research. Consideration of questions to address will lead
to consultation of previous research results, and those
results can be taken into account when designing both
management and monitoring strategies. Prior data could
also be incorporated into subsequent analysis, and recent
developments in Bayesian analysis [48] provide a promis-
ing methodology for doing this. For example, population
growth rates (Q3, Q4) under a particular management
regime could be estimated not just from monitoring data
for the current reintroduction, but also incorporating prior
estimates, potentially improving the precision of the
estimates.
A common thread in our suggestions for a strategic
approach to reintroduction biology is greater integration
through communication between people and projects.
Reintroduction is a challenging endeavour in which diffi-
cult decisions often need to be made based on few data. The
best response to this challenge is to make the best use of
our research resources by working together.
Acknowledgements
We thank Tim Caro, John Ewen, Ian Jamieson, Heather Koldewey,
Richard Maloney, Dorian Moro, Kevin Parker and Sally Walker for
comments on earlier versions.
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Free journals for developing countries
The WHO and six medical journal publishers have launched the Health InterNetwork Access to
Research Initiative, which enables nearly 70 of the world’s poorest countries to gain free access
to biomedical literature through the internet.
The science publishers, Blackwell, Elsevier, Harcourt Worldwide STM group, Wolters Kluwer
International Health and Science, Springer-Verlag and John Wiley, were approached by the WHO
and the British Medical Journal in 2001. Initially, more than 1500 journals were made available for
free or at significantly reduced prices to universities, medical schools, and research and public
institutions in developing countries. In 2002, 22 additional publishers joined, and more than 2000
journals are now available. Currently more than 70 publishers are participating in the program.
Gro Harlem Brundtland, the former director-general of the WHO, said that this initiative was
‘‘perhaps the biggest step ever taken towards reducing the health information gap between rich
and poor countries’’.
For more information, visit www.who.int/hinari
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