Vol

14 2013

Towards Integrated
Species Conservation

The endangered African wild dog (Lycaon pictus) has been restored in South Africa using an integrated species
conservation approach, including active metapopulation management. | © Rob Till

WAZA magazine Vol 14/2013

1

WAZA magazine Vol 14/2013

Markus Gusset1 & Gerald Dick2

Contents
Editorial
Markus Gusset & Gerald Dick...... 1
The One Plan Approach:
The Philosophy and
Implementation of CBSG’s
Approach to Integrated Species
Conservation Planning
Onnie Byers, Caroline Lees,
Jonathan Wilcken &Christoph Schwitzer....................2

Imprint
Editors:

Markus Gusset & Gerald Dick
WAZA Executive Office
IUCN Conservation Centre
Rue Mauverney 28
CH-1196 Gland
Switzerlandphone: +41 22 999 07 90
fax:+41 22 999 07 91
Layout and typesetting:michal@sky.cz

Integrating Assessmentof Ex Situ Management Options
into Species Conservation
Planning
Kathy Traylor-Holzer, Kristin
Leus & Philip McGowan...............6

Edition: 700 copies© WAZA 2013

The African Penguin Chick
Bolstering Project: A One Plan
Approach to Integrated
Species Conservation
Christoph Schwitzer, Nigel
Simpson, Margaret Roestorf& Richard B. Sherley.................. 23
The Golden Lion Tamarin
Conservation Programme’s
One Plan Approach
Jennifer Mickelberg &Jonathan D. Ballou.................... 27
Conservation Efforts for theEndangered Ozark Hellbender
Jeffrey A. Ettling & Jeffrey
T. Briggler.................................. 30

Managing for True Sustainabilityof Species
Robert C. Lacy,
Kathy Traylor-Holzer &Jonathan D. Ballou.................... 10

The Western Pond Turtle
in Washington: Crawling Backfrom Extirpation
Jennifer Pramuk, Fred Koontz& Harriet Allen........................... 33

The Need to Balance Ex Situ
and In Situ Conservation
John E. Fa, Stuart Harrop, Sara
Oldfield & Diana Pritchard........ 15

Saving the Devil:
One Species, One Plan
Caroline Lees, Paul Andrew,
Andrew Sharman &Onnie Byers............................... 37

Print:

Agentura NP, Staré Město,Czech Republic

Editorial

The Long Overdue Death of the
Ex Situ and In Situ Dichotomy inSpecies Conservation
Kent H. Redford,
Deborah B. Jensen &James J. Breheny.......................19

Restoring African Wild Dogs inSouth Africa: A Managed
Metapopulation Approach
Harriet T. Davies-Mostert &Markus Gusset........................... 41

Printed on FSC paper.
This edition of WAZA Magazine
is also available on
www.waza.org.

In the WAZA Vision and Corporate
Strategy Towards 2020, published in
2009, the very first operational objective includes “…the demonstrationof links between ex situ and in situ
conservation work…”. In line with thisobjective, we postulate the dawningof the era of integrated species conservation. Under this new paradigm,
conservation holistically refers toactivities aimed at sustaining biodiversity (i.e. genetic, species andecosystem diversity), whether conducted in or out of the natural habitat,
integrated across the conservation
community. Integrated conservation
works along a continuum of management intensity, including hardly any
human intervention in wild populations all the way to intensively managed populations in human care.
Many wild populations are like populations in human care – small in size,
fragmented and with limited geneflow between them. For example,
African wild dogs (Lycaon pictus) havebeen reintroduced into small, fenced
reserves in South Africa, which
necessitates periodic translocationof animals to mimic natural dispersal
and maintain gene flow (DaviesMostert & Gusset, this issue). Thismodel is referred to as a managed
metapopulation, as natural metapopulation processes such as dispersal are subject to human intervention. Metapopulation management
involves managing a set of interacting populations under a common conservation goal. Its components may
include multiple regional populations
managed in human care (including
in-country breeding programmes),
multiple wild populations (including
reintroduced populations) and evengenome resource banks.

1© Nicole Gusset-Burgener

ISSN: 2074-4528

2

WAZA Conservation Officer &International Studbook
Coordinator
WAZA Executive Director

Intensive population management
serving conservation goals thus
requires transfers of animals. Traditionally, this includes the exchangeof animals between holders of the
population in human care, import ofanimals from the wild to either bolster existing or establish new populations in human care, and export ofanimals from populations in humancare to the wild. These transfers canbe combined under one umbrella ofinteractive exchanges of animals (orgametes) between populations in thewild and in human care for mutual reinforcement. The role of populations
in human care can vary from little
interaction with wild populations all
the way to populations with extensive gene flow in both directions. This
will greatly enhance our capacity tosustain viable populations both in human care and in the wild.
The science of small population
management, developed primarily
for managing populations in humancare, is therefore of direct relevanceto field conservation. For example,
fencing is highly effective for conserving lions (Panthera leo) in Africa(Packer et al. 2013; Ecol. Lett. 16:
635–641), but fenced lion populations require human intervention
to be viable in the long term. Similarly, subpopulations of the rarest of
Africa’s carnivores, the Ethiopian wolf
(Canis simensis), are fragmented tothe extent that translocation of animals among the few remaining sites
is recommended to restore gene flow
(Gotelli et al. 2013; Anim. Conserv. 16:
234–247). As habitat fragmentation
progresses and climate change shifts
the boundaries of species’ distribution ranges, translocation is likely to
become an increasingly importantconservation tool. The skills andknowledge of experienced zoo andaquarium professionals are needed to
guide such translocation work.

© Nicole Gusset-Burgener
Cheetahs (Acinonyx jubatus) in the Serengeti.

In this edition of the WAZA Magazine,
we have compiled various conceptual
approaches to integrated species
conservation, collectively declaring the end of the ex situ and in situ
conservation dichotomy. Moreover,
several case studies of integrated
species conservation in practice arepresented. We hope that this editionof the WAZA Magazine will demonstrate links between conservationists
working at any point along the continuum of management intensity, andthereby further increase the contribution of the world zoo and aquarium
community to global biodiversity
conservation.

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WAZA magazine Vol 14/2013

WAZA magazine Vol 14/2013

One Plan Approach3

Onnie Byers1,*, Caroline Lees2, Jonathan Wilcken3 & Christoph Schwitzer4

The One Plan Approach:
The Philosophy and Implementationof CBSG’s Approach to Integrated
Species Conservation Planning
Summary
An increasing number of threatened
species are dependent on continuingmanagement for their survival. For
these species, it makes little sense to
conduct separate and independent
conservation planning efforts basedon whether these interventions takeplace in the wild, in increasingly
managed parks and reserves or inzoos. The One Plan approach proposed by the IUCN SSC Conservation
Breeding Specialist Group (CBSG)
promotes integrated species conservation planning, which considers
all populations of the species, inside

1
2

3
4
*

IUCN SSC Conservation BreedingSpecialist Group, Apple Valley, MN, USA
IUCN SSC Conservation BreedingSpecialist Group Australasia,
c/o Auckland Zoo, Auckland,
New Zealand
Auckland Zoo, Auckland, New Zealand
Bristol Zoo Gardens, Bristol, UK
E-mail for correspondence:
onnie@cbsg.org

The Needand outside their natural range,
As habitats are increasingly alteredunder all conditions of management, and wild animal and plant populaengaging all responsible parties andtions impacted by human activities,
all available resources from the verya growing number of the world’s
start of any species conservation
species are dependent on continuingplanning initiative. The One Plan
management for their survival andapproach aims to: establish new
ultimate conservation. Scott et al.
partnerships; ensure that intensively (2010) stated that 84% of the species
managed populations are as usefullisted under the US Endangered
as possible to species conservation;
Species Act could be classified asincrease the level of trust and un“conservation reliant” and will require
derstanding among conservationists continuing, species-specific interacross all conditions of management ventions. Widespread threats suchof a species; accelerate the evoluas habitat loss, poaching, invasivetion of species planning tools; andspecies and disease often lead toultimately lead species conservation
smaller, isolated populations thattowards the aspirations embodied in require conservation action, not only
the Aichi Biodiversity Targets.
to avoid extinction but to achieveconservation as defined by WAZA
(2005): “securing, for the long term,
populations of species in natural
ecosystems and habitats”, and more
specifically by Redford et al. (2011):“maintaining multiple populations
across the range of the species in
representative ecological settings,
with replicate populations in eachsetting. These populations should be
self-sustaining, healthy, and genetically robust – and therefore resilient
to climate and other environmental
changes”.

»
These threats are not only impacting currently endangered species. In
their recent analysis of the effects
of climate change on biodiversity
loss, Warren et al. (2013) found thatwithout mitigation, large range
contractions can be expected evenamong common and widespread
species, amounting to a substantial
global reduction in biodiversity andecosystem services by the end of
this century. Effective integration ofplanning, and the optimal use of limited resources, across the spectrumof management is essential if wehope to contribute to achieving the
global biodiversity targets agreed
upon by the Conference of the Parties to the Convention on Biological
Diversity in Nagoya, Japan, in 2010,
commonly referred to as the Aichi
Biodiversity Targets.

Two Plans Are Not
Better Than One
An obstacle to this, however, is thatspecies conservation planning has
traditionally followed two parallel
but separate tracks. Field biologists, wildlife managers and conservationists monitor wild populations, evaluate threats and develop
conservation strategies and actions
to conserve threatened species in
the wild. Meanwhile, the zoo andaquarium community develops longterm goals for ex situ populations,sometimes without full access to
information about the threats facedby the species’ wild counterparts
and the opportunities for supporting
those populations. While each management plan strives for viability ofa particular population, too seldom
are these plans developed together
to maximise the conservation benefits to the species.

The international zoo community
has made tremendous progress
recently on the design and development of Global Species Management
Plans (GSMPs). However, this label isa misnomer, as the population being
planned for is the global captive population, not the global population
as a whole. These programmes aredesigned to general principles usually aimed at retaining conservation
value through close managementof demographic health and genediversity. However, their planninglacks the comprehensive input fromin situ conservation managers thatwould enable customisation towards
the specific management needs ofthe species as a whole. Without this
input, GSMPs, or indeed any captive
breeding programmes, will not necessarily be large enough, geneticallydiverse enough, productive enough,in the right kinds of facilities or in
the right place at the right time toprovide the support that they could
to wild populations.
On the other hand, too many conservation planning and Red Listing workshops take place without
sufficient active involvement fromthe international zoo community.
Species conservationists working toconserve unmanaged wild populations often do not see the potential contribution from intensively
managed populations; intensively
managed populations are rarely
considered as part of wider metapopulations from the start, if at all.
Redford et al. (2011) stated that “wemust view captive management as
only a stop-gap measure in efforts
to move species up the continuum”
towards a fully conserved state.

The IUCN Red List of Threatened
Species recognises the impact of
captive stocks on a species’ conservation status in its distinction
between Extinct and Extinct in the
Wild. However, it makes no attempt
to quantify this contribution, either
at any point prior to the complete
loss of the species in the wild or atany point after, despite the fact that,as a species approaches extinctionin the wild, the chances of establishing a healthy captive programme
or of reshaping an existing one
into an appropriate programme ofmanagement become increasingly
small. When existence in the wildis threatened, then populations ofthat species, wherever they are, arepotentially of conservation value.
A status assessment that includes
and evaluates all populations ofa species, inside and outside theirnatural range, would thus be a useful
aid to planning and prioritisation.
We are all trying desperately tosave species, and the definition ofconservation is, for the most part,agreed upon. What differentiates
the captive community from otherconservation entities is its ability
to buy time. It can do this by securing populations from threatening
processes in the wild, while concurrent conservation activities battle
these threats in situ. In the majorityof cases there is no consensus on
how to remove these threats, andin many instances (e.g. for species
threatened by amphibian chytrid
fungus) we do not have the technical ability to do so. For a number of
species, captive populations could
well provide a critical and ongoingconservation resource for the foreseeable future.

4 One Plan Approach

WAZA magazine Vol 14/2013

WAZA magazine Vol 14/2013

One Plan Approach»
Where there are populations in
captivity, we must consider those
populations when developing a conservation plan. CBSG is placed at theinterface between the zoo community and the global species conservation community, has over 30 yearsof experience with species conservation planning, and can therefore
potentially bridge this gap and facilitate an improved contribution of thezoo community to successful species
conservation globally. (Fig. 1)

The One Plan
Approach Defined
Population management acrossa continuum that bridges wild andintensively managed conditions
can serve as an important tool toprogress species “up the ladder”, towards fully conserved status. CBSG,
through its One Plan approach,supports integrated species conservation planning through the joint
development of management strategies and conservation actions by all
responsible parties to produce onecomprehensive conservation planfor the species. Integrated species
planning is not a new concept: such
holistic conservation efforts have led
to several well-known conservation
successes, from golden lion tamarins
in Brazil to Puerto Rican crested
toads in the Caribbean to Arabianoryx in the Middle East. Previous
CBSG workshops for species suchas the Okinawa rail (Figs 1 and 2),
red-headed wood pigeon and blackfooted ferret developed integrated
species conservation plans acrossan interactive wild–ex situ spectrum.
Other examples include African
penguins (Schwitzer et al., thisissue) and Tasmanian devils (Leeset al., this issue). Our vision is tomake comprehensive conservation
planning more commonplace andeffective. (Fig. 2)

Fig. 1
Captive Okinawa rail with radio-transmitter.
© Kathy Traylor-Holzer

Fig. 2
Wild Okinawa rail.
© Michio Kinjyo

The Benefitsof Implementation
Assessment of threats to wild populations and evaluation of potential
strategies to address those threats
should consider the wide array of options offered by intensive population
management, and if and how thesetools might promote conservationof the species in the wild. Options
include: source populations for demographic or genetic supplementation; assurance populations against
imminent threats such as diseaseor invasive species; research populations to develop monitoring or
management techniques; and headstart programmes that temporarily
shelter juveniles from high mortality
and promote population growth. Inturn, wild populations will boost thelong-term viability of ex situ populations by supplying genetic founders
that can or must be removed fromthe wild, such as excess offspring,nuisance or injured individuals thatcannot be released or non-viable
population fragments.

The CBSG workshop process is ideally suited to implementation of the
One Plan approach. As Redford etal. (2011) note, “developing sucha positive vision with a broad rangeof stakeholders produces a positive
atmosphere, facilitates cooperation, and allows for development ofessential partnerships and politicalsupport”. In addition, the newly
revised IUCN SSC Guidelines on
the Use of Ex Situ Management forSpecies Conservation (IUCN SSC, in
prep.), in essence, call for just suchan approach, and the SSC/Global
Species Programme strategic plan,
which guides the work of CBSG andall other SSC Specialist Groups, includes among species conservation
planning targets the application of
the One Plan approach over the next
quadrennium.

The zoo and aquarium community is
actively building links with the SSC
Specialist Groups and field conservation agencies. Its members are committed to making available to theirconservation colleagues the captive
community’s specialised skills andvaluable resources to assist in conservation. The One Plan approach isa working model of how the benefitsof this conservation opportunity
can be fully realised. Our goal is topromote and routinely apply the
One Plan approach in the coming
years. The result should be integrated conservation plans that mobilise
the full suite of skills and resources
available to species in trouble, giving
them a better chance at a future in
the wild.

References
•
•

•
•

•

IUCN Species Survival Commission (IUCN SSC) (in prep.) IUCN SSC
Guidelines on the Use of Ex Situ Management for Species Conservation.
Gland: IUCN Species Survival Commission.
Redford, K. H., Amato, G., Baillie, J., Beldomenico, P., Bennett, E. L.,
Clum, N., Cook, R., Fonseca, G., Hedges, S., Launay, F., Lieberman, S.,
Mace, G. M., Murayama, A., Putnam, A., Robinson, J. G., Rosenbaum, H.,
Sanderson, E. W., Stuart, S. N., Thomas, P. & Thorbjarnarson, J. (2011)
What does it mean to successfully conserve a (vertebrate) species?
BioScience 61: 39–48.
Scott, J. M., Goble, D. D., Haines, A. M., Wiens, J. A. & Neel, M. C. (2010)
Conservation-reliant species and the future of conservation.
Conservation Letters 3: 91–97.
Warren, R., VanDerWal, J., Price, J., Welbergen, J. A., Atkinson, I.,
Ramirez-Villegas, J., Osborn, T. J., Jarvis, A., Shoo, L. P., Williams, S. E.
& Lowe, J. (2013) Quantifying the benefit of early climate change
mitigation in avoiding biodiversity loss. Nature Climate Change 3: in press.
WAZA (2005) Building a Future for Wildlife: The World Zoo and Aquarium
Conservation Strategy. Berne: WAZA.

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WAZA magazine Vol 14/2013

Kathy Traylor-Holzer1,*, Kristin Leus2,3 & Philip McGowan4

WAZA magazine Vol 14/2013

Integrating Ex Situ Options

Status Review and Threat Analysis

Integrating Assessment of Ex Situ
Management Options into Species
Conservation Planning

Causes of Primary Threats(e.g. human activities)
Deterministic Primary Threats(e.g. habitat loss, poaching,disease, invasive species)

Potential Role(s) and Goals
for Ex Situ Management

Stochastic Threats(e.g. demographic variation,catastrophes, inbreeding)

Ex Situ Populationand Management Type(s)Feasibility Assessment

Impacts of Threats on Species(e.g. small N, poor survival,
poor reproduction, genetic isolation)

Summary
As the biodiversity crisis intensifies,
an increasing number of species will
likely require some form of intensive
population management in order toavoid extinction. The revised IUCNSSC Guidelines on the Use of Ex Situ
Management for Species Conservation
will provide better guidance on if andwhen ex situ activities are a beneficial
component of an overall species conservation strategy. These guidelines
outline a five-step decision-making
process that defines potential ex situ
conservation roles, the type of ex situ
activities needed to fulfil those roles,
and the feasibility, risks and likelihood of success. Ex situ management
can be used more effectively as a conservation tool if the specific ways inwhich ex situ strategies can improve
population viability or prevent extinction are identified and criticallyevaluated as part of an integrated
approach to species conservation
planning.

1
2

3
4
*

IUCN SSC Conservation BreedingSpecialist Group, Apple Valley, MN, USA
IUCN SSC Conservation BreedingSpecialist Group Europe,
c/o Copenhagen Zoo,
p/a Merksem, Belgium
European Association of Zoos andAquaria, Amsterdam, The Netherlands
Newcastle University, Newcastle
upon Tyne, UK
E-mail for correspondence:kathy@cbsg.org

Why Wild
Populations Go Extinct
Wildlife populations are increasingly
under risk of extinction. Climatechange, habitat loss, exploitation,
invasive species, disease – these
all-too-familiar threats frequently
result in wild populations becoming
small and fragmented. At this pointa new threat emerges – the added
vulnerability of small populations to
random stochastic processes (e.g. environmental variation, catastrophes,
random variation in survival and reproduction, skewed sex ratio, genetic
drift, inbreeding) that can feed backinto each other, causing a species tobe caught in the “extinction vortex”(Gilpin & Soulé 1986). Once caught
in this downward spiral, populations
may be doomed to extinction, even
if the original primary threats are
removed.
Conservation planning for species
needs to consider all threats to species survival, both long-term andimmediate, both deterministic andstochastic. As the biodiversity crisis
intensifies and wild populations decline, more species will likely require
some form of intensive management
at the level of populations and individuals to avoid extinction. Intensive
management of populations forconservation can take place acrossa broad in situ–ex situ continuum,
within and/or outside of zoos andaquariums (Baker et al. 2011; CBSG
2011). In some cases, ex situ management can play a significant role inspecies conservation and therefore
should be assessed as a possible conservation tool in species conservation
planning.

7

How Ex Situ
Activities Can Help
Ex situ conservation activities can
support species conservation andprevention of extinction in a variety
of ways, by:Offsetting the Effects of Threats. Ex
situ activities can improve the demographic and/or genetic viabilityof a wild population by ameliorating
the impacts of primary or stochastic
threats on the population, such as reduced survival, poor reproduction andgenetic isolation. Examples include
head-start programmes that remove
juveniles from the wild for ex situ
care and return them once they areless vulnerable to predators or otherthreats (e.g. hellbenders, Western
pond turtles), and cross-fostering of
captive-born neonates to wild parents (e.g. red wolves).
Addressing the Causes of PrimaryThreats. Ex situ activities can help reduce primary threats such as habitat
loss, exploitation, invasive species or
disease through specifically designed
research, training or conservation
education activities that directly andeffectively impact the causes of thesethreats (e.g. education to reduce thespread of invasive species or buyingof exotic pets, research to eradicate
or treat disease).

(benefits/costs/risks/likelihood of success)High Probability of Extinction in the Wild

Vision and Conservation Goals

Decision Analysis of Potential Conservation
Objectives and Actions (In Situ and Ex Situ)

In Situ Conservation
Objectives and Actions

Ex Situ Conservation
Objectives and Actions(if any)

One Integrated Conservation Plan
for a Species
Fig. 1
Incorporation of the decision process proposed in the revised IUCN guidelines (dark blue boxes) into
the species conservation planning process to develop one integrated plan for the species.

Buying Time. Establishment of a diverse and sustainable ex situ rescue orassurance population may be criticalin preventing species extinction when
wild population decline is relatively
steep and the chance of sufficiently
rapid reduction of primary threats isslim or uncertain or has been inadequately successful to date. Examples
include ex situ populations in response to severe disease threat (e.g.
Tasmanian devils facing facial tumour
disease, amphibian species susceptible to chytrid fungus), catastrophic
events (e.g. Perdido key beach miceat risk due to hurricanes) or continued habitat degradation (e.g. goldenheaded lion tamarins in fragmented
and degraded Atlantic Forest).
Restoring Wild Populations. Once theprimary threats have been sufficiently
addressed, ex situ populations canbe used to genetically and/or demographically re-establish wild populations (e.g. Puerto Rican crested toad,Vancouver Island marmot, Arabianoryx, Mauritius kestrel).

How the IUCN
Guidelines Can Aidin Planning
The IUCN Species Survival Commission (SSC) is finalising a revision of its
guidelines on the use of ex situ management for species conservation, coordinated by the IUCN SSC Conservation Breeding Specialist Group (CBSG)(IUCN SSC, in prep.). Although not
yet formally approved by SSC, theseguidelines are anticipated to outline
five steps for a more formal, informed
and transparent decision-making
process to provide guidance on if andwhen ex situ activities are a beneficial
component of an overall species conservation strategy. This process ideallywould be used as an integral part of,and in complement to, existing species conservation planning processes
such as CBSG’s Population and Habitat
Viability Assessment (PHVA) process
and IUCN SSC’s handbook for Strategic Planning for Species Conservation(IUCN SSC 2008) (Fig. 1).

These steps are:
1. Conduct a Thorough Status Assessment and Threat Analysis. A thorough and detailed examinationof the causal factors leading to
the primary threats, as well as
the precise effects that both theprimary and stochastic threats
have on the reproduction, survival
and distribution of the species, allows the identification of potential
intervention points for conservation action.
2. Identify Potential Ex Situ Conservation Roles. Potential intervention
points can guide the identificationof ex situ activities (as well as otherconservation actions) that can prevent or reduce negative impacts
on the wild population. This willdefine any potential conservation
roles that ex situ management canplay in the overall conservation of
the species.

»8 Integrating Ex Situ Options

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Integrating Ex Situ Options»
3. Define the Required Programme
Structure. The purpose and function of an ex situ population or
activity will determine the characteristics and dimensions of the
programme needed to fulfil theidentified conservation role(s).
4. Assess Programme Feasibility. It is
important to assess not only thepotential value of an ex situ programme, but also the resourcesand expertise needed for such exsitu activities, the costs and risks
associated with them and the feasibility and likelihood of success.
5. Make a Decision on Ex Situ Options.
The above information is used toreach a decision regarding ex situ
activities for conservation thatis informed and transparent (i.e.
demonstrates how and why thedecision was taken).
Following such a process, whereby
the need for ex situ activities is not
automatically dismissed, nor automatically included, but carefully
evaluated as a normal part of conservation planning, will ensure that any
ex situ activities selected are carefully
tailored, in form and function, to theneeds of the species.
The guidelines for the use of ex situ
management for species conservation are undergoing the final revisionand review process within IUCN SSC
and are expected to be finalised inlate 2013. These guidelines will beapplicable across taxa, to biobanks
as well as to individuals, and for situations in which ex situ management
is or is not already underway. Not
all species conservation strategies
will require an ex situ component, inthe same way that other management interventions may or may not
be required to conserve a species. In
some cases ex situ management will
be central to a conservation strategy, in others it will be of secondary
importance, supporting other interventions, and in yet others it will notfeature at all.

Case Study:
North American Bats
Many species of North American
insectivorous bats are at risk due
an emerging disease – White Nose
Syndrome (WNS) – that is rapidly
spreading across the eastern USA.
WNS infects hibernating bats and has
resulted in mortality as high as 95% inmany wild bat colonies. Up to 40 bat
species, including several threatened
species, could be vulnerable. While
rescue ex situ populations might beindicated, it is difficult to maintaininsectivorous, hibernating bats under
ex situ conditions. A collaborative
US Fish and Wildlife Service–CBSG
workshop brought a diverse groupof bat experts together to consider
the feasibility of ex situ management
options for these bat species as partof an overall conservation strategy(Traylor-Holzer et al. 2010).

Conservation goals were identified,a threat analysis was conducted
and numerous potential conservation roles of ex situ populations
were identified. The required ex situ
programme structure and expertisediffered substantially across thesedifferent roles. Table 1 outlines someexamples of how the purpose of an
ex situ bat population may requiredifferent number of individuals, number and type of facilities, different
expertise, different time frames andeven different taxa. To complete thisevaluation process, extensive data
were compiled for each bat species
regarding relevant life history, behavioural traits and existing captive
expertise to guide the assessmentof programme structure, costs andlikelihood of success. This thoroughanalysis followed the decision-making process suggested in the revised
IUCN guidelines and led to a wellinformed and documented evaluationfrom which species-specific conservation planning could be conducted andreassessed in the future.

Table 1

An example (using bats) of how the conservation role of an
ex situ population can determine the required programme structure, length,taxon, expertise and other characteristics (WNS = White Nose Syndrome).
Role
Type
Temporary rescue from Short-term holding during
imminent threat
winter hibernation
Assurance population
against extinction
Mitigation of WNS
impacts on bats
Mitigation of spread of
WNS to other sites

Long-term breeding
population as a genetic anddemographic backup
Research population forunderstanding and treating
WNS
Exhibits that raise publicawareness about spreading
WNS while exploring caves

Structure/expertise needed
Ability to hold large number of animals,
hibernate successfully through winter(off-exhibit) and release successfullyin spring
Capture sufficient founders and breed
successfully for many generations while
minimising adaption to captivity
May be able to use a related common
species and apply results and techniques
to endangered bat species
Can use a common species that is easy
to maintain in captivity, with exhibits in
multiple zoos near species habitat

How to Achieve
Integration
Ex situ management can be used
more effectively as a conservation
tool if it is part of an integrated
approach to species conservation
planning, whereby in situ and ex situ
communities together form one
overall species conservation plan,
including, where appropriate, intensive management of populations insitu and/or ex situ.
What does this mean for zoos andaquariums committed to conservation? In the ideal future world,
integrated conservation plans would
exist for all threatened species, inwhich potential conservation role(s)for ex situ management have been
carefully evaluated for appropriateness, feasibility and effectiveness.
This would facilitate regional collection planning for zoos and aquariums, at the least from the point ofview of direct ex situ conservation,
as each threatened species would
have clearly identified ex situ conservation activities, if any, and it would
be clear if and how zoos can support
those activities. This would also
ensure that all potential conservation efforts were being used to savea species from extinction.

Integrated species conservation
planning needs to come from bothsides. The field conservation community needs to embrace ex situ
management options as part ofthe larger conservation toolbox toaddress threats to wild populations
and avoid extinction. Likewise, theex situ community needs to reevaluate its existing and proposed
programmes in terms of the conservation role(s) that they can play andstructure those programmes to meetthose roles effectively (see Lacy etal., this issue). The revised IUCN SSC
Guidelines on the Use of Ex Situ Management for Species Conservation
provide a decision-making processthat can be used by both conservation communities to evaluate if andwhen to pursue ex situ management
options. When included as one component of a larger, stakeholder-inclusive species conservation planning
process (involving collaborations
between zoos, aquariums and otherex situ specialists, wildlife agencies,
researchers, non-governmentalorganisations, etc.), application ofthese guidelines can promote a truly
integrated One Plan approach (Byers
et al., this issue) to the conservationof a species. The species mentioned
as examples above are sound testimonies to this principle.
There is increasing need to strengthen the integration of in situ and exsitu conservation planning to ensure
that, whenever appropriate, ex situ
management is used to support insitu conservation to the best possible effect. When used strategically,
ex situ conservation can be a potent
tool for species conservation that
does not undermine, but complements, the imperatives of field
conservation.

References
•

•

•

•

•

•

Baker, A. M., Lacy, R. C., Leus,
K. & Traylor-Holzer, K. (2011)
Intensive management of
populations for conservation.
WAZA Magazine 12: 40–43.
Gilpin, M. E. & Soulé, M. E.
(1986) Minimum viable populations: processes of species
extinction. In: Conservation Biology: The Science of Scarcity andDiversity (ed. by Soulé, M. E.),
pp. 19–34. Sunderland, MA:
Sinauer Associates.
IUCN Species Survival Commission (IUCN SSC) (2008) Strategic
Planning for Species Conservation: A Handbook. Version 1.0.
Gland: IUCN Species Survival
Commission.
IUCN Species Survival Commission (IUCN SSC) (in prep.) IUCNSSC Guidelines on the Use of
Ex Situ Management for Species
Conservation. Gland: IUCN Species Survival Commission.
IUCN SSC Conservation Breeding Specialist Group (CBSG)(2011) Intensively Managed
Populations for Conservation
Workshop. Final workshop
report. Apple Valley, MN: IUCNSSC Conservation BreedingSpecialist Group.
Traylor-Holzer, K., Tawes, R.,
Bayless, M., Valenta, A., Rayman, N. & Songsasen, N. (eds)(2010) Insectivorous Bat Captive
Population Feasibility Workshop.
Final report. Apple Valley, MN:
IUCN SSC Conservation Breeding Specialist Group.

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Managing for True Sustainability

11

Robert C. Lacy1,*, Kathy Traylor-Holzer2 & Jonathan D. Ballou3

Managing for
True Sustainability of Species
Summary
Despite the increasing conservation need for intensive population
management, zoos are failing tomaintain sustainable and diverse exsitu populations that contribute tospecies conservation. In this paper,
we define the problems and identify
strategies and actions for meeting
this challenge.

1
2
3
*

Chicago Zoological Society,
Brookfield, IL, USA
IUCN SSC Conservation BreedingSpecialist Group, Apple Valley, MN, USA
Smithsonian Conservation Biology
Institute, Washington, DC, USA
E-mail for correspondence:
rlacy@ix.netcom.com

Isolated Ex Situ Population

Isolated Ex Situ Population

Isolated Ex Situ Population

Isolated Wild Population

Recognising
the Problems
The “wild” of our childhood is nomore. Human populations continue
to expand, habitats are increasingly
altered by human activities, invasive
species are spreading, new diseases
are emerging – and species need toadapt to these new challenges if they
are to persist. Increasingly fragmented wildlife populations are at greaterrisk and in more need of support
because they face unique threats andlack the diversity to respond. The callto action is widespread and urgent,
imploring all conservation partners
to use their resources and expertiseeffectively to advert widespread
species extinctions. Zoos (including
aquariums) have an expanding roleand responsibility to contribute tospecies conservation amid this biodiversity crisis (Baker et al. 2011).

typically has been the maintenanceof 90% gene diversity for 100 years,
usually applied to an independent
regional population. However, truesustainability is the maintenance ofa resource without depletion or lossof its value. Thus, our benchmark bywhich “sustainability” is measured
is not an indicator of true sustainability but rather acquiescence toan accepted rate of genetic decay(Ballou & Traylor-Holzer 2011; Lacy2013). Zoos cannot serve as secure
havens for averting extinction or
be used as source populations for
species conservation activities if we
accept depletion of the adaptability
that those populations will need tosurvive, and then often fail to meeteven these inadequate goals.

The increasingly necessary conservation tools of assurance populations,
reintroduction and supplementation
require sustainable ex situ populations. Unfortunately, zoos are failingto achieve this on many levels. First,
currently only a small percentage of
threatened species are held by zoos.
Second, a small percentage of species
in zoos are managed scientifically,
and, finally, few of these are considered to be managed sustainably(Traylor-Holzer 2011). Moreover, ourmeasuring stick for “sustainability”

Achieving Sustainability
Achieving success must start withclear goals, derived from a comprehensive conservation strategy forthe species that defines what thebroader community values – not justthe individual zoo or zoo association
or even the global zoo community,
but the global conservation community. What do we mean by saving
the species? Who will take responsibility for conducting each component of the conservation plan? And,
perhaps most critically, who will be
the species’ champion to make surethat we do not just watch extinction
occur? Addressing these questions
is beyond the scope of this contribution, but they need to be addressed
at a global level, species by species(IUCN SSC 2008).

Fig. 1
Small isolated populations. Small population size with poor growth (red line) and rapid lossof gene diversity (blue line) lead to increased inbreeding and instability, resulting in decreased individual
fitness, loss of genetic evolutionary potential and increased risk of population extinction.

For many species, this comprehensive species-level strategy will include
the question: What are the roles of
populations held at zoos? To serveas an effective source for restoring
healthy wild populations, ex situ
populations must be truly sustainable
and they must contain evolutionary potential to allow adaptation toa rapidly changing global environment. True population sustainability
cannot be achieved through small
isolated populations managed
through independent plans, but will
require new and integrated management approaches among interacting
populations that may transverse
a broad management continuum(Redford et al. 2012; Lacy 2013). Collaborative management among zoos,
among zoo regional programmes,
between captive and wild populations, between living individuals andgametes held in a genome resourcebank are all important components ofintegrated metapopulation management programmes that support
species conservation – a One Planapproach as discussed by Byers et al.
(this issue).
An integrated approach leads tolarger and more robust populations
that can maintain genetic variation
through periodic, well-planned exchanges, moving from a plan for slow
decay (Fig. 1) to one of sustainable
maintenance (Fig. 2). In addition, thediversity of environmental conditions
and management strategies across

such a metapopulation better allows
us to move from the narrow target ofmaintaining neutral genetic diversity
measured through pedigree analysis
to preservation of other types of variation, including behavioural, morphological, physiological and adaptive
genetic variation. Through effective
integration, a holistic metapopulation
approach can pool “resources” in the
broadest sense of the term – space,animals, genes, expertise, funds – tohave the greatest conservation
impact. It should also be obvious thatnumerous diverse, healthy, breeding
animals serving to help save species
will promote other purposes of zoos
as well.

»12 Managing for True Sustainability»

WAZA magazine Vol 14/2013

Large Ex Situ Breeding Centres

WAZA magazine Vol 14/2013»

If the species biology or husbandryrequirements are not sufficiently
known to identify which actions areneeded, then:• implement research programmes
in the field or in zoos to provide
the needed data.

Supplemented Wild Population

Fig. 2
Interconnected metapopulation. Improved breeding success and periodic animal exchanges promote strong population growth (red line)
and maintenance of genetic potential (blue line), resulting in sustainable populations in both captivity and the wild.

Tailoring Solutions
to the Problem
With a clear understanding of thegoals for sustaining a species and theroles to be filled by zoo populations,the methodologies necessary to successfully fill those roles can be determined. This analysis must start withspecifying what trajectory (in termsof population size, growth, stability,
variability and resilience, and in termsof impacts on audiences) we desire
for each population – with constantreference back to the overall species’
conservation plan, rather than relying
on ad hoc justifications or a generic
template, as is the case for many of
the current breeding programmes.
Current and expected trajectories
must be compared, the reasons forany gaps between the two identified
and plans put in place to correct the
deficiencies. Listed below are several
types of deficiencies not uncommon
in managed populations, along withsome strategies for resolution.

13

Supplemented Ex Situ Population

If exhibit practices and husbandry
protocols do not result in sufficient
reproduction and survival to meet
population goals, then:• transfer animals to facilities that
can achieve those levels;• develop new or redesigned facilities, such as specialised breeding
centres; and/or• change the social management(e.g. natural social groupings,
mate choice).

Supplemented Ex Situ Population

Managing for True Sustainability

If managed populations for a species
are too small to be demographicallyand genetically robust, then a choicemust be made as to whether or not
ex situ populations will serve a conservation role for that species. If it isaffirmed that they should, then:• recruit additional zoos to manage
the species;• have each zoo maintaining thespecies commit to keeping a larger
number of individuals;• institute exchanges to link formerly disconnected ex situ populations
through joint management andmutual support;• create new specialised breeding
facilities;• establish a programme of managed and mutually beneficial
exchanges between ex situ and insitu populations; and/or• use gamete banks to increase
the genetically effective size ofa population.

If the source population that founded
the existing ex situ population was
too small or otherwise of limited
genetic diversity, of unknown history
or of uncertain taxonomy, then:• determine the taxonomy, history
and diversity of the source on
which the managed population isbased;• combine programmes for subspecies that are not reproductively
isolated or strongly differentiated,
especially if sub-specific identityof animals is uncertain or alreadymixed;• obtain new founders from otherbreeding programmes; and/or• obtain new founders from wild
populations able to sustain such
removals.

If the ex situ population is being
sustained biologically, but the positive conservation effect is not being
achieved, then:• improve integration with efforts
for wild populations;• communicate effectively to audiences to change behaviours thatare counter to conservation;
and/or• reallocate resources towards
methods that successfully counterthreats to the species.

Acting Locally
Many of the above are obvious options, many have been suggested
before and almost all either requireor are more easily achieved byinstitutions working in collaborative
partnerships – both within the zoo
community and with other conservation organisations. However, there
are many things that each institution
can do by itself and to promote theneeded partnerships.

of founders, breeding population
size and space for population growth
are adequate to sustain a geneticallydiverse and demographically robust
population. If calculations show that
this need is not being met, determine from where and how many new
founders, additional breeding spaces,
new breeding consortium partner orother resources are needed. Do not
accept an explanation that althougha population is not projected to meetgoals, there is no clear solution andtherefore management will continue
as before. If the husbandry and technologies for managing the species
well are not yet known, determine
what research needs to be supported
by your institution to answer thecritical questions. Do not assume thatsomeone will develop the techniquesthat you will need to succeed with thespecies; be proactive in pushing fora solution.

First, develop institutional animalcollections based on identified conservation needs and opportunities.
If comprehensive conservation plans(or Regional Collection Plans basedon broader input) exist for species
you are considering, use these plansto identify where your efforts aremost needed. If such plans do not
yet exist, contact IUCN SSC specialist groups, governmental agencies
and others to offer to host or support
For each species that is in your colsuch an assessment and planning.
lection because it needs protection,
Let it be known that your zoo has
make sure that your institution has
resources for species conservation –a clearly stated conservation goal.
such as expertise, access to audiences, These goals should be documented,
breeding facilities, funding – but that
understood by all involved and speyou need help to make sure that thecific regarding what purposes thoseresources are used where and how
animals are serving in the broader
they are most needed. If you do notconservation strategy for the species
know where to begin to make the(not just vaguely defined as “display”
right contacts, ask WAZA or the IUCN or “education” or “breeding”).
SSC Conservation Breeding Specialist
Group for help.
Periodically confirm that you aremeeting your institution’s goals for
For programmes that need coordinaeach species and contributing to its
tion, identify who at your zoo canoverall conservation. If you did notserve as the species manager, support meet targets, decide what further eftheir position and then hold themforts are needed. If the species statusaccountable for success. The species
is not improving in the wild, ask the
manager should develop a realistic
broader community for a reassesslong-term management plan for enment of threats and the neededsuring that the population can serve
responses. Explain to your public,
the identified goals. If the population
staff, members and trustees or loserves as insurance against loss of the cal authorities what you are doing
species, be certain that the number
for conservation of the threatened
species. Document and then explain
proudly how the programmes at yourinstitution helped to save species
for which you have accepted responsibility.

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John E. Fa1,*, Stuart Harrop2, Sara Oldfield3 & Diana Pritchard4»
Invest in the Future,
Not in the Past
True sustainability of the wildlife populations under the care of zoos is necessary for the future of zoos and thefuture of many species, but successwill require new investments in new
ideas with new partners. Our current
species management programmes
are mostly focused on holding on toremnants of the animal resources weonce had, and in many cases we are
not even meeting short-term goals.
Instead of continuing to use only
resources and methods that havebeen insufficient to date, we need todecide what animals, research, facilities, people and approaches will beneeded to achieve species conservation goals.

References
There are a number of programmes
in which zoos are already working
closely with many partners to achieve
success for species – such as the Amphibian Ark, the international golden
lion tamarin programme, a consortium working for Humboldt penguinsin Peru, efforts to prevent the lossof the Tasmanian devil to disease,restoration of the fire-bellied toad in
Denmark and Germany, and the Sumatran tiger Global Species Management Plan. We need many more suchprogrammes – so that the One Planapproach becomes the norm for species conservation by zoos rather than
exceptional models. The precarious
future for so many species demands
such an affirmative response.

•

•

•

•
•

•

Baker, A. M., Lacy, R. C., Leus,
K. & Traylor-Holzer, K. (2011)
Intensive management of
populations for conservation.
WAZA Magazine 12: 40–43.
Ballou, J. D. & Traylor-Holzer, K.
(2011) Captive populations andgenetic sustainability. WAZA
Magazine 12: 19–22.
IUCN Species Survival Commission (IUCN SSC) (2008) Strategic
Planning for Species Conservation: A Handbook. Version 1.0.
Gland: IUCN Species Survival
Commission.
Lacy, R. C. (2013) Achieving truesustainability of zoo populations. Zoo Biology 32: 19–26.
Redford, K. H., Jensen, D. B. &Breheny, J. J. (2012) Integrating
the captive and the wild. Science 338: 1157–1158.
Traylor-Holzer, K. (2011) Identifying gaps and opportunities
for inter-regional ex situ species
management. WAZA Magazine
12: 30–33.

The Need to Balance Ex Situ
and In Situ Conservation
Summary

Introduction

Ex Situ Institutions

In situ conservation is central tocontemporary global biodiversity
protection and is the predominantemphasis of international regulationand funding strategies. Ex situ approaches, in contrast, have been relegated to a subsidiary role and theirdirect contributions to conservation
have been limited. Evidence exists forthe conservation community to makea strong case for an enhanced rolefor ex situ conservation. We note theadvances occurring within institutions specialising in ex situ conservation and stress that, although muchremains to be done, many constraints
are being addressed. The evidence ofincreasing extinction rates, exacerbated by climate change, challenges
the wisdom of a heavy dependence
on in situ strategies and necessitates
increased development of ex situ
approaches. A number of different
techniques that enable species andtheir habitats to survive should now
be explored. Moreover, the relentless
loss of “the wild” may soon render
the in situ–ex situ distinction misleading, or even obsolete.

In situ and ex situ conservation areseen as two distinct approaches tothe protection of wild species. In situ
conservation, defined by the Convention on Biological Diversity (CBD)with reference to the protection of
species in their natural surroundings,
derives primarily from scientific considerations concerning the conservation benefits that accrue from theprotection of integrated habitats andecosystems. Since the 1992 Earth
Summit in Rio de Janeiro, Brazil, in
situ conservation has been designated, expressly, as the legal and institutional priority. CBD and other global
instruments and funding strategies
address a range of practices relating
to in situ measures for conservation
and relegate ex situ approaches toa subordinated supply role, as seen in
CBD Articles 8 and 9.

The vehicles of ex situ conservation
are those organisations that holdwild plants and animals and genetic
material: zoos, aquariums, botanic
gardens, arboreta and seed banks.
Although these already lay claim
to support conservation througha range of education, research andfunding activities, their potential tocontribute in more direct ways to theconservation of species has increased
with recent developments. Specifically, these organisations and their
networks have proliferated acrossthe globe, such as Botanic Gardens
Conservation International (BGCI)
and the World Association of Zoos
and Aquariums (WAZA). For example,
the International Species Information
System (ISIS) is an international nonprofit organisation serving zoos andaquariums worldwide, and manages
a comprehensive database of animal
species and their environments foranimal management and conservation goals. It records over 2 million
captive animals of almost 15,000 taxa
and 10,000 species.

1

Durrell Wildlife Conservation Trust,
Trinity, Jersey, Channel Islands &Department of Life Sciences,
Imperial College London, Ascot, UK
2 Durrell Institute of Conservationand Ecology, School of Anthropology
and Conservation, University of Kent,
Canterbury, UK
3 Botanic Gardens Conservation
International, Richmond, UK
4 School of Global Studies, Universityof Sussex, Brighton, UK* E-mail for correspondence:john.fa@durrell.org

We wish to stimulate discussions
about the need to revise the contributions that ex situ approaches canmake to conservation. We consider
that ex situ conservation has a more
important role to play, especially inthe face of the evidence of increasing extinction rates, exacerbated byclimate change. Integrated conservation management approaches
hold much potential, but we must
recognise the significance of institutional factors, not just the science,that have hitherto constrained thedevelopment of direct conservation
contributions from ex situ and integrated techniques. We also question
the continued validity of the in situ–
ex situ distinction.

»

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Balancing Ex Situ and In Situ Conservation

17

»

»
Changing the Legal
LandscapeFig. 1
Madagascar pochard.
© Gerardo Garcia

Overcoming Limitations
BGCI manages a database with records of 2,561 botanic gardens worldwide, with 1,000 of these added in thelast 10 years. These botanic gardens
cultivate 80,000 species in living
collections, and increasingly holdseed banks and in vitro collections.
Close to 700 botanic gardens havesupplied collection data to BGCI for
the global PlantSearch database that
contains 500,000 records of about
180,000 taxa. Facilities for storing andexchanging plant genetic materialof cultivated crops have also expanded, primarily in response to thefood security and resilience agenda,
conforming, inter alia, to the requirements of the International Treaty on
Plant Genetic Resources for Food andAgriculture. Whereas in the 1970s 0.5
million samples were held in 10 genebanks, now 6.1 million samples are
stored in 1,308 gene banks. These
represent infrastructural and professional advances to deal with challenges that have hitherto frustrated
the capacities of ex situ facilities.

Earlier limitations of ex situ facilities to conserve species have been
overcome given improved technicalknowledge and practices with regard
to collection strategies, genetic assessment, storage techniques andcaptive population management.
Ex situ organisations have also accumulated a portfolio of direct, tangible
impacts on conservation (Figs 1 and
2) and performance indicators havebeen refined to measure this role.
The world’s botanic gardens contain
12,000 globally threatened plant species and about 800 botanic gardens
are managed with a specific focus
on plant conservation. Many botanic
gardens also manage nature reserves
and other forms of protected areas tocombine ex situ methods with in situ
plant conservation, and have increased engagement with local communities on livelihood issues, a key
component of contemporary, holistic
conservation strategies. Botanic
gardens also play an important rolein the implementation of the Global
Strategy for Plant Conservation.

The ex situ breeding of animals orplants for direct conservation purposes has been frustrated by limitedor conflicting organisational missions. But a further move away fromthe mere possession of extensive
horticultural or exotic animal collections to one fulfilling a more active
conservation role is now thwarted
by a lack of financial incentives.
The largest source of international
biodiversity funding, the Global
Environmental Facility (the funding
mechanism of CBD), has no focal areafor ex situ activities. How to balance
the need, or preference, to generate
revenue from visitor attraction withachieving direct conservation is a central and contentious theme within
and amongst ex situ institutions.
The financial pressure is perhaps lessacute for botanical institutions, as
threatened plant species can be kept
in a relatively straightforward andinexpensive manner.

Fig. 2Ploughshare tortoise.
© Quentin Bloxam

However, this dilemma is particularly challenging for zoos (Stanley
Price & Fa 2007). Whilst claims andcounterclaims abound regarding
the nature and levels of support thatzoos actually provide to conservation (Gusset & Dick 2010), sectionsof the zoo community urge zoos
to involve themselves more in theimmediate task of saving greaternumbers of species from extinction (Fa et al. 2011), and “preserving
wildlife… through field conservation
initiatives” (Bonner 2011) as part oftheir existing multifaceted portfolio
of approaches to support conservation. This more direct contribution
can coexist with the other conservation support approaches that ex situ
facilities currently employ. While itremains to be defined how this canbe best achieved, in the case of zoos
an immediate advance would be tofocus on keeping more individualsof smaller threatened species and tocoordinate effective captive breeding programmes for them, given
their higher breeding rates andlower maintenance costs. Evidence
from European and North American
animal collections (Pritchard et al.
2012) demonstrates that this is still
not happening. The emphasis onlarge charismatic animals persists (Faet al. 2011).

Whereas international law and policy
already deals with in situ conservation in relatively complex prescriptive provisions, frameworks thatprescribe a meta-strategy for ex situ
centres have not been developed. For
example, although initiatives such as
the European Union’s Zoos Directive
support ex situ strategies and global
documents such as the World Zoo
and Aquarium Conservation Strategy
urge zoos to contribute to conservation, these fall short of effectively
linking zoos into collaborative andstrategic conservation activities. The
impact of such initiatives is limitedby the absence of effective international coordination, which necessarily, being a global issue, cannot be
addressed by the array of regional
associations and coordinated breeding programmes that currently exist.
Moreover, there is no centralised institutional mechanism to access anddisseminate data on animal genetic
resources within zoos similar to the
Food and Agriculture Organisation’s
Domestic Animal Diversity Information System. This is a tool to conserve
elements of global animal biodiversity, even though it was establishedto manage animal genetic resources
for food security and resilience strategies. Despite remaining shortcomings,
ex situ conservation has an increasingly important role to play. Current
circumstances, especially climatechange, expose the vulnerability of
our reliance on in situ approaches
that seek to maintain natural systems
and processes in specific geographical locations.

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Kent H. Redford1,*, Deborah B. Jensen2 & James J. Breheny3»
If the most important objective of
the global conservation mission, tominimise extinctions, is to be coupledsuccessfully with the wider global
agenda, including food security andhuman health, then ex situ strategies
can no longer be regarded as mere
support mechanisms for in situ conservation. Emphasis must not only be
on increasing the number of threatened species in ex situ collections, but
on assessing and ensuring the conservation value of such collections. For
plants a major issue is that about 33%
of globally threatened plant species
are cultivated only in one botanic
garden. In addition, genetically representative collections are essential
if they are to be used for recovery
and restoration work. For animals
there are known consequences of
captive environments on morphology, behaviour and physiology thatstill need resolution, but substantial
improvements have been made on
how animals should optimally be kept
in captivity (Hosey et al. 2009).

Moving Forward
Independently of debates concerning
the scientific merits of ex situ approaches, there are other entrenchedobstacles to an enhanced role forex situ techniques. Prevailing in situ
conservation work is institutionalised
through myriad public and privategroups that operate at local, national and international levels. The
large international organisations

that characterise conservation science and practice exert influence oninternational conservation policy andfacilitate the flow of funding. Borrowing from policy analysis, we canappreciate how the interests of suchgroups of conservation organisations
may become linked to the perpetuation of particular policy interventions
around the in situ paradigm. Integrating techniques from both in situ andex situ approaches may contributeto removing the professional chasmthat has for so long divided ex situ
and in situ specialists.
Recognition of an expanded role forex situ conservation techniques will
necessarily involve a re-evaluation of
accepted concepts and the related
legal prescriptions concerning themeaning of what constitutes therange of a species. Range may become meaningless for those species
for which predictions imply rapid
and unpredictable perturbations intheir former natural surroundings.
This presents a profound challenge
to the notion of in situ conservationand may result in the distinction
between ex situ and in situ conservation blurring to the point of disappearing altogether. It is conceivablethat a more nuanced appreciation
may emerge that goes beyond thisfalse dichotomy to identify instead
how best to harness respective andcomplementary techniques.

Acknowledgements
This article is adapted from Pritchard
et al. (2012). We are grateful toa great number of colleagues who
have contributed to our thinking with
their insightful discussions on thesubject.

References
•

•

•

•

•

•

Bonner, J. P. (2011) Vision andfuture of zoos: keynote given
at EAZA Annual Conference.
WAZA News 2011/1: 2–4.
Fa, J. E., Funk, S. M. &O’Connell, D. (2011) Zoo Conservation Biology. Cambridge:
Cambridge University Press.
Gusset, M. & Dick, G. (2010)
Biodiversity conservation
projects supported by the world
zoo and aquarium community.
In: Building a Future for Wildlife:
Zoos and Aquariums Committed
to Biodiversity Conservation (ed.
by Dick, G. & Gusset, M.), pp.
57–60. Gland: WAZA Executive
Office.
Hosey, G., Melfi, V. & Pankhurst,
S. (2009) Zoo Animals: Behaviour, Management and Welfare.
Oxford: Oxford University Press.
Pritchard, D. J., Fa, J. E. Oldfield, S. & Harrop, S. R. (2012)
Bring the captive closer to thewild: redefining the role of ex
situ conservation. Oryx 46:
18–23.
Stanley Price, M. R. & Fa, J. E.
(2007) Reintroductions fromzoos: a conservation guiding
light or shooting star? In: Zoos
in the 21st Century: Catalysts forConservation? (ed. by Zimmermann, A., Hatchwell, M., Dickie,
L. & West, C.), pp. 155–177.
Cambridge: Cambridge University Press.

The Long Overdue Deathof the Ex Situ and In Situ Dichotomy
in Species Conservation
Summary
Successful species conservation has
munity, from simple display andusually been defined as avoiding exhusbandry to a focus on genetic andtinction. Rather than manage extincpopulation management of captive
populations, so that they might servetion risk, it is imperative to provide
asassurance colonies or sources fora positive, science-based definition
reintroduction
into the wild.
of success that recognises the role ofhuman alteration of the natural world.
The conservation biology focus on
Remarkable changes to most of theextinction and its avoidance has been
world’s ecosystems have caused thecodified in science and policy and has
distinction between in situ and ex situ
served as the basis for education andconservation that has long shaped
zoo programmes to become obsolete. action. IUCN regularly updates the
Red Lists, and as scientists we report
The old dichotomy has been supamongst
ourselves and to the publicplanted by hybrid approaches thathow
many
more species are “close to
create new, key roles for zoos andtheedge”.
While
many of the agenzoo professionals to play in successful
cies responsible for managing endanspecies conservation.
gered species are required to create
recovery plans, there is no standard
approachto these plans, nor have
The Importance
plans
been
completed for the majorityof Defining Successof species. In the zoo community, few
of the species that are cooperatively
Despite all that has been written on
managed by regional programmes
species conservation, little attenhave
clearly articulated conservation
tion has been paid to the question ofgoals
and definitions of success.
what success would look like. Instead
the focus has been on what failure
If we wish to create a conservation
would look like – extinction. This factreflects conservation biology’s origins practice that will not continually be
addressing species in crisis, we need
as a “crisis discipline”, desperate toa proactive definition of successful
get the world’s attention focused
species conservation that incorpoon loss of ecosystems and species.
rates the major biological attributes
The rise of conservation biology alsoofsuccess. In a recent paper, Redford
marked a change in the zoo comet al. (2011) offered such a definition.
They proposed that successful species
conservation be defined as “maintaining multiple populations across therange of the species in representative
ecologicalsettings, with replicate
1 Archipelago Consulting, Portland,
populations
in each setting. These
ME, USApopulations
should be self-sustaining,
2 Woodland Park Zoo, Seattle, WA, USA
healthyandgeneticallyrobust – and
3 Wildlife Conservation Society, Bronx,
therefore
resilienttoclimateandNY, USAother
environmental
changes”.
* E-mail for correspondence:
redfordkh@gmail.com

A successfully conserved species
would have the following six attributes:
1. be demographically and ecologically self-sustaining;
2. be genetically robust;
3. have healthy populations;
4. have representative populations
distributed across the historical
range in ecologically representative settings;
5. have replicate populations withineach ecological setting; and6. be resilient across the range.
This sort of a positive, proactive viewof species conservation may help turnaway the pessimism gripping muchof conservation and build enthusiasm
for new creative solutions. Working
with a broad range of stakeholders
towards a positive view of successmay help achieve the partnershipand collaborative conservation that isrequired for success. Recent advances in conservation psychology haveemphasised the critical importance ofhope in bringing about such change.
We need to bring a modicum of hopeto species conservation.

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20 Dichotomy in Species Conservation

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Dichotomy in Species Conservation

»

21

»

This rapidly transforming world
demands a transformed view of species conservation. In today’s world,
not all of the six attributes detailed
above can be achieved for all species.
The reasons for this vary according
to the circumstances and history of
the species and the nature of theirinteractions with human-dominatedstructures and processes. Yet, it isstill vital to create a framework fordefining success for this range ofcircumstances. Redford et al. (2011)
laid out five general states along
a continuum of the type and extent
of ways that species are reliant on human interventions, both directed andnon-directed. Each state differentiallyachieves the six conditions enumerated above (Table 1).

Relationship between states of conservation and attributesof fully conserved species (adapted from Redford et al. 2011).

Healthy

GeneticallyrobustResilient acrossrange

Self-sustaining
Conservation dependent
Lightly management
Intensively managed
Captive managed

Attributes
Self-sustaining

StatesReplicated

The version of ecology taught in the
1960s and 1970s presented a worldin which ecosystems returned toa stable equilibrium after perturbation. In this view of the world, allconservation had to do was remove
outside stresses and success would
be accomplished. We have come tounderstand that the natural world is
not organised this way and there are
multiple stable points, disequilibrium
conditions and constant change –making conservation much moredifficult than we originally thought. In
this world, conserving a species is nolonger as simple as removing human
influences. We have come to recognise the extent to which many species
have become reliant on the direct
and indirect ways and magnitudes
in which humans manage the world,
including changed land use patterns,
alteration of landscapes (e.g. dams),
creation of new physical structures,
availability of alternate foods, presence of new competitors and mutualists, and changed flows of energy andnutrients.

Table 1

Representative

A Changing World
Demands New
Approaches

XX
XX
X
X
O

XX
XX
X
X
O

XX
X
X
O
O

XX
XX
X
O
O

XX
X
X
O
O

XX
X
O
O
O

XX = fully conserved | X = partially conserved | O = minimally or not conserved.
These are modal values that will vary on a species-by-species basis.

4. Conservation dependent
The states range from species comspecies: species that will almost
pletely reliant on directed humanalways need significant conservamanagement to species able to thrivetion directed not at management
without directed human intervention.
ofintra-specific aspects such
The states are:asfeeding, breeding or habitat
1. Captive managed species: spemanagement,
but at extrinsic faccies found exclusively in captivity
tors
requiringchangesin humanand reliant on caregivers for food,
behaviour.
Speciesin
thiscategoryhusbandry and propagation. Theyaretypified
by
being
of
significant
do not manifest many or any ofcommercial value, such as thethe six attributes except for those
Africanforest elephant.
derived from management actions.
5.
Self-sustaining
species: theAn example is the Socorro dove.
final
state
is
one
in which spe2. Intensively managed species:
cies
express
fulllevelsof all the
species that are found in the wild
conservation
attributes
and canbut are reliant on direct humanbe
expectedtosurvivewithlittleintervention at the individual and
to
no
human
subsidy
directed
population levels through augintra-specifically or extrinsically.
mentation from captive populaAn
example of this is the peregrinetions or very extensive, directedfalcon.
habitat manipulation. An example
in this category is the Chinese
Although this classification was develalligator.
oped at the species level, it can be ap3. Lightly managed species: species
plied to different populations withinthat rely on a relatively limited set
a species. As has been pointed out,of human interventions directed
species like the Arabian oryx haveat both population enhancement
populations that represent almost all
and influencing extrinsic factors,ofthese stages.
such as habitat management, but
are largely capable of maintaining
themselves. An example in thiscategory is the corncrake.

The Role of Zoos and
Zoo Professionals inthis Changed WorldAs this list of general states of conservation makes clear, the world does
not consist of species found only inthe wild or only in zoos. They are
instead found in a bewildering arrayof combinations of reliance on humanaction for conservation or reliance on
cessation of human action for conservation. And species conservation faces a panoply of new challenges fromemerging diseases to climate change
impacts. So, why then does theconservation community in general,and the zoo community in particular,
insist on dichotomising conservation
as either in situ or ex situ?
This dichotomy is not only incorrect, it under-represents the actualand potential ways in which captive
collections and their curators cancontribute to species conservation.
In a recent article (Redford et al.
2012), we documented some of the
myriad ways that species biologists
are addressing conservation, using
approaches that are hybrids between
in situ and ex situ. Using tools andmethods developed and tested inzoos, such approaches include:• rearing butterfly pupae in captivity
and releasing adults into nature(Fig. 1);• hatching and head-starting turtles
before returning them to nature;• provisioning of next boxes anddouble-clutching of eggs;• integrating captive-bred animals
into wild social groups;• transporting individual animals
between populations to minimise
inbreeding (Fig. 2);• capturing, medically treating andreleasing individual wild animals;• transporting resistant individuals
from otherwise diseased populations to establish new diseaseresistant populations; and• collecting wild animals’ gametes,combining in vitro and implanting
into captive animals so the young
can be released in the wild.

Fig. 1
Oregon silverspot butterfly.
© Erin Sullivan/Woodland Park Zoo

What characterises these approaches
is the melding of traditional zoo techniques in non-zoo settings to achieve
forms of species conservation thatare hybrid in their nature.

Why We Want
Everything to Be Either
One Thing or Another
There seems to be a unique humandesire to divide everything into nonoverlapping binary categories. Just
think about politics, or religion, or
race, or gender or most other aspectsof human life.

This habit seems to also apply to
species conservation with the twocategories of in situ and ex situ. We
seem to insist that all species conservation must belong to one or theother of these categories, with little
regard given to the possibility thatsome things do not fit into one or
another category. This type of thinking is hampering us as we seek toredefine the role of zoos and captive
collections in the reality of the worldin which we now find ourselves. Let
us declare the death and burial of thefalse dichotomy between in situ andex situ conservation!

22 Dichotomy in Species Conservation

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Christoph Schwitzer1,*, Nigel Simpson1, Margaret Roestorf2 & Richard B. Sherley3»

The African Penguin Chick Bolstering
Project: A One Plan Approach toIntegrated Species Conservation

It’s Just Not the SameWorld Anymore
The world in which the concepts ofin situ and ex situ were developed is
no longer the world we inhabit. The
emerging set of changes brought
about by climate change, the increasing control humans are exerting on
the natural world and the rise of new
genetic technologies such as synthetic biology are all working to turntomorrow’s world into a new world– new with threats and new with opportunities. Just as hybrids between
populations and between species
often are successful at invading newenvironments, it is time for creative
solutions for species conservation
success to emerge from blending
between once distinct endeavours.
Examples of this “blended conservation” include DNA fingerprinting
techniques developed from captive
populations that are allowing field
scientists to track wild populations
using non-invasive methods, or to
identify the country of origin of illegally poached ivory. The rise in thepossibility of restoring extinct species,
or rescuing extinct alleles from museum specimens and reintroducing
them into dwindling populations, will
force us to give up the world of thepast. And technology can allow us tostore genetic material from functionally extinct species today to preserve
our options for the future.

Fig. 2
Oregon spotted frog.
© Ryan Hawk/Woodland Park Zoo

Species conservation in this century
will challenge us to define successacross the gradient of human-dominated lands and waters, acknowledging that different levels of intervention will be needed to achieve success.
Zoo professionals have a lot to contribute to both setting the goals andachieving the outcomes. And in sodoing, we are in a position to redefine
success for zoos themselves – creating the modern zoo that generates
support for, and is actively engaged
in, the conservation of species andecosystems.
Both the world and the understanding that gave rise to the easy dichotomy of in situ and ex situ havedisappeared. We need new understanding, new science and new waysof communicating the imperativesof species conservation in this newworld and the key role that zoos andzoo professionals can play.

References•

Redford, K. H., Amato, G., Baillie, J., Beldomenico, P., Bennett, E. L., Clum, N., Cook, R.,
Fonseca, G., Hedges, S., Launay,
F., Lieberman, S., Mace, G. M.,
Murayama, A., Putnam, A.,
Robinson, J. G., Rosenbaum, H.,
Sanderson, E. W., Stuart, S. N.,
Thomas, P. & Thorbjarnarson, J.
(2011) What does it mean tosuccessfully conserve a (vertebrate) species? BioScience 61:
39–48.
• Redford, K. H., Jensen, D. B. &Breheny, J. J. (2012) Integrating
the captive and the wild. Science 338: 1157–1158.

Summary

Introduction

The population of African penguins(Spheniscus demersus) has seen
a rapid and ongoing decline in recent
decades, probably caused by a severe
food shortage due to overfishingand to movement of sardine andanchovy stocks away from the penguins’ breeding colonies. The Chick
Bolstering Project has two main aims:
addressing the ongoing population
decline by supplementing extant wildcolonies with locally hand-reared
birds; and investigating the factorsthat determine breeding site fidelity
in African penguins through monitoring released birds, thus enabling
the artificial establishment of new
breeding colonies of African penguinsin places more suitable for their longterm survival. The international zoo
and aquarium community is contributing technical expertise and practical help with hand-rearing chicks inSouth Africa, and it is envisaged thatthe captive populations will eventually contribute to stocking penguin
colonies and bolstering the wild population. The Chick Bolstering Project is
an example of the One Plan approach
to integrated species conservation
promoted by the IUCN SSC Conservation Breeding Specialist Group.

The African penguin (Spheniscus
demersus) is the only penguin species
found in Africa. Historically, the species has ranged along the westernand southern coasts of southern
Africa from Port Elizabeth to Namibia,
with an estimated population sizein the order of one million breedingpairs in the 1920s. It has, however,been hit by a number of humanrelated activities over the years, withdevastating effects on the populations. The species is now classified
as Endangered on the IUCN Red
List of Threatened Species (BirdLife
International 2012). The population
decline has accelerated in the recent
past, with an estimated 61% loss
over 28 years or three generations.
The remaining 26,000 breeding pairs
left in the wild are distributed in 28
colonies in South Africa and Namibia(Crawford et al. 2011), with only sevenislands supporting 80% of the global
population. It is clear that, unless action is taken, there is a substantial riskthat the species will become extinct.

1
2

3

*

Bristol Zoo Gardens, Bristol, UK
Southern African Foundation for
the Conservation of Coastal Birds(SANCCOB), Bloubergrandt,
South Africa
Animal Demography Unit, Departmentof Biological Sciences, University ofCape Town, Rondebosch, South Africa
E-mail for correspondence:cschwitzer@bcsf.org.uk

There have been large, long-termchanges in regional populations ofAfrican penguins, which may havebeen influenced by changes in theavailability of food (Crawford et al.
2008). One of the reasons for the
recent population decline is thought
to be a spatial mismatch between thebreeding localities of the penguins in
the Western Cape and the availabilityof small pelagic fish following the displacement of stocks to the east (Crawford et al. 2008, 2011). The latter may
be the consequence of an ecosystemshift in the current around the South
African Cape, the southern Benguela
upwelling system, which itself may be
due to anthropogenic factors including global climate change.

As a result, although their prey –anchovy (Engraulis encrasicolus) andsardine (Sardinops sagax) – may still
be abundant, it is generally out ofreach of the penguins breeding on
South Africa’s west coast both during
the pre-moult and pre-breeding period, when they must quickly rebuild
their energy reserves, and during thebreeding season, when they are tied
to foraging within a distance of about
20–30 km from the colony to deliver
food to the nestlings (Petersen et al.
2006). This seems to have impacted
on the ability of parent birds to raise
high-quality offspring (Sherley et al.
2013) and has taken its toll on adultsurvival (Crawford et al. 2011). In
addition, the absence of energy-richadult sardine and anchovy on South
Africa’s west coast and in Namibia
may also be impacting negatively on
juvenile survival, as fledglings seem
to preferentially disperse into theseonce profitable areas (Sherley et al. inpress).
The formation of new colonies ofAfrican penguins is a rare event,recorded only three times (excluding re-colonisation of two islands) in
the last 150 years. It is desirable tomaintain extant colonies of African
penguins, so that they can provide
foci for immigration of birds in theevent of future changes in the distribution of prey resources. The loss ofa colony may not be reversible in the
short term. For example, African penguins stopped breeding at Robben
Island in the late 1700s, and breeding
did not recommence there until 1983
(Petersen et al. 2006).

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African Penguin

25»

The CBP also aims to develop local exIn several South African penguin
breeding colonies, including Dyer and pertise in hatching eggs and rearing
penguin chicks for potential future
Robben islands, penguin chicks thatreintroduction of captive-bred birds.
hatch late in the season (SeptemberToachieve this, a chick-rearing unit
onwards) are frequently abandonedhasbeen established at SANCCOB,
by their parents when the latter begin
theimplementing
partner of thethe annual moult. Adult penguins fast
projectinSouth
Africa(Fig. 1). Fromduring moult and cannot feed chicks
its
inception,the
CBP
included
allthat remain in the nest, thus these
populationsofAfricanpenguins
intochicks would be unlikely to survive if
theplanning
exercise,
both
insideandleft in the wild; the majority of themoutsidetheir
naturalrange,
and
under
would die through a lack of food or
all conditions of management. The
unfavourable conditions. The Chickproject partners made a large effort
Bolstering Project (CBP) was set up
toengage with all responsible parties,
by the Bristol Zoological Society andusing
resources and expertise fromthe Southern African Foundation forthezoo
and aquarium community,
the Conservation of Coastal Birds
academiccommunity, rehabilitation(SANCCOB), along with the Univercentres,
policymakers, colony mansity of Cape Town’s Animal Demogagers
and
other
stakeholders. The
raphy Unit, national and regional
CBP
is
thus
an
examplefor the One
governmental agencies, authorities
Plan
approachtointegrated
speciesmanaging penguin colonies and otherconservation
promoted
by
the
IUCN
partners. Its aim is to investigate the
SSC
Conservation
Breeding
Specialist
efficacy of using hand-reared chicks,
Group (see Byers et al., this issue).
abandoned by their parents in theWestern Cape, to bolster decliningcolonies, as well as to develop the infrastructure and knowledge required
to artificially establish new penguin
colonies on South Africa’s south coast,
closer to the current centres of gravity of small pelagic fish.

Using a combination of literature
review and analysis of banding andre-sighting data held in various
databases, the project aims to answer
research questions such as: what proportion of chicks that fledge in a given year return to breed at any colony;what proportion of parent-rearedchicks return to breed at their natalcolony and what proportion disperse
to other sites; and at what stage during the development of a chick doesit learn its natal colony? Collaborating researchers from the University

Achievements
The CBP started in 2006, when 841
chicks abandoned by moulting
parents had to be removed from theDyer Island, Robben Island and Stony
Point colonies. Since then, until the
2012/2013 release season, SANCCOB
had hand-reared 2,535 chicks abandoned by moulting parents as part of
the CBP. The success rate between
2006 and 2012 was 77% (1,962 out of
2,535; Table 1). Through the CBP, financial and operational support was madeavailable in 2010 and 2011 to Penguins
Eastern Cape and to the South African
Marine Rehabilitation and Education
Centre to support chick-rearing efforts
in the Eastern Cape.

2011 1712012 322
Total 2,535

90
173
1,962

53
54
77

Medianduration of stay
until release (days)

Table 1 African penguin chicks adof Cape Town’s Animal Demography
mitted to and released by SANCCOB
Unit attach satellite tracking devices
as part of the Chick Bolstering Projectto hand-reared chicks on release as
well as to parent-reared chicks before (source: Nola Parsons, SANCCOB).
fledging. The use of such devices will
help to identify foraging areas thatare important to juveniles shortly
after fledging. It will also help answer
the question if hand-reared chicks
show similar foraging behaviour toYearparent-reared chicks after they fledge, 2006 841
765
91
42
and if juveniles moult at colonies
2007 481
351
73
422008 9084
93
36
in close proximity to good foraging
2009
147
127
86
36
areas or if they return to their natal
2010 483
372
77
56
colonies.
Percentage
released

Fig. 1African penguin chick hand-reared from the egg at SANCCOB’s chick-rearing unit.
© Romy Klusener/SANCCOB

Abandoned penguin chicks, as well as
chicks below a certain body condition
score, are being collected from different island and mainland colonies
at the end of the breeding season by
the relevant colony managers. Since
larger chicks have a significantly
higher chance of survival, require lessfrequent feeding and are less likely toneed veterinary interventions, somecolony managers collect all remaining
chicks from a colony once a certain
percentage of adults has gone intomoult. The fledglings are then handreared at SANCCOB’s rehabilitation
centre in Table View, Cape Town, andreleased back into the wild after
about 1–2 months in captivity in December/January, when conditions aremost suitable for their survival. The
birds are banded using silicone flipper
bands and released into their colonies of origin or into different extant
colonies, and their movements andsubsequent breeding behaviour arethen monitored to determine the factors that lead to breeding site fidelity
in the species.

Number released

Evidence from recent studies suggests that the (re)introduction of
fledgling chicks can have a significant
impact on conserving wild penguin
populations (Barham et al. 2008);
chicks that were hand-reared andreleased showed equal survivorshipto breeding age and higher fecundity than parent-reared birds. Thissuggests that increasing the numberof fledgling birds, through handrearing and release, could help arrest
the decline in overall numbers andbolster the population. Based on this,and on the slow inherent dispersal
ability of the species and a lack ofnatural disturbance-free sites along
the South African coast, the artificial
establishment of a new, protected
mainland African penguin breedingcolony closer to the current centreof gravity of the small pelagic fishstocks has been proposed (BirdLife
International 2012). African penguins
show a marked site fidelity, but it isunknown at which point in a penguin’s life history this is determined. It
is thus imperative that we understandthe mechanisms that lead fledgling
penguins to return to the colonies inwhich they hatched, or to disperse
to other sites as breeding adults.
However, the period from fledging
until around three to four years ofage has not been sufficiently studied,and there are still large gaps in our
knowledge (Sherley et al. in press).

Methods

Number admitted

The Chick Bolstering
Project

54
49

Of all chicks released by SANCCOB
from 2001 to 2010, 1,708 were individually banded with flipper bands.
So far, 76 of these chicks have been
re-sighted at least once, most ofthem in the Western Cape. This relatively small number is not surprising,
given that fledgling penguins spend
about three to four years at sea before they settle in one of the colonies
to start breeding. Data on site fidelity
are thus only starting to accumulate,and it will be another few years untila large enough sample is available toallow rigorous analysis. In addition,
21 fledglings (eight hand-reared and13 parent-reared) from South Africa
and Namibia have been tracked withsatellite transmitters between 2011and early 2013 (Fig. 2), and a further
29 will be tracked throughout South
Africa in the latter half of 2013.

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Jennifer Mickelberg1,* & Jonathan D. Ballou2»

The Golden Lion Tamarin
Conservation Programme’s
One Plan Approach

A purpose-built chick-rearing unit at
SANCCOB was officially opened in
November 2011 and became operational in January 2012. It consists ofa preparation area, an incubation
room and a chick room. The building is separate from the rest of the
SANCCOB facility to help prevent the
spread of disease. It allows handrearing penguin chicks “from the egg”
and is a major step towards using
eggs from captive-bred penguins forbolstering the wild population.
The aims of the CBP have been incorporated into the draft of a national
Biodiversity Management Plan forthe species, to be signed off by theSouth African government in 2013,as a priority for conservation action.
The project partners are leadinga working group on hand-rearing andrelease that has been formed under
this framework.

Summary

Fig. 2African penguin chick with satellite tracking device.
© Cheryl-Samantha Owen

Acknowledgements

References

This project is a partnership between
the Bristol Zoological Society and
SANCCOB, as well as the South
African Department of Environmental Affairs (Oceans and Coasts), theAnimal Demography Unit at the
University of Cape Town, CapeNature,
Robben Island Museum and IFAW. It
is supported by 26 zoos and aquariums as well as by different trusts andfoundations. The authors are gratefulto Nola Parsons for providing admittance and release statistics.

•

•
•

•

•
•

•

Barham, P. J., Underhill, L. G., Crawford, R. J. M., Altwegg, R., Leshoro,
T. M., Bolton, D. A, Dyer, B. M. & Upfold, L. (2008) The efficacy of handrearing penguin chicks: evidence from African penguins (Spheniscus
demersus) orphaned in the Treasure oil spill in 2000. Bird Conservation
International 18: 144–152.
BirdLife International (2012) Spheniscus demersus. In: IUCN Red Listof Threatened Species. Version 2012.2. <www.iucnredlist.org>.
Crawford, R. J. M., Sabarros, P. S., Fairweather, T., Underhill, L. G. &Wolfaardt, A. C. (2008) Implications for seabirds off South Africa ofa long-term change in the distribution of sardine. African Journal of Marine Science 30: 177–184.
Crawford, R. J. M., Altwegg, R., Barham, B. J., Barham, P. J., Durant, J. M.,
Dyer, B. M., Geldenhuys, D., Makhado, A. B., Pichegru, L., Ryan, P. G., Underhill, L. G., Upfold, L., Visagie, J., Waller, L. J. & Whittington, P. A. (2011)
Collapse of South Africa’s penguins in the early 21st century.
African Journal of Marine Science 33: 139−156.
Petersen, S. L., Ryan, P. G. & Grémillet, D. (2006) Is food availability limiting African Penguins Spheniscus demersus at Boulders? A comparison of
foraging effort at mainland and island colonies. Ibis 148: 14–26.
Sherley, R. B., Underhill, L. G., Barham, B. J., Barham, P. J., Coetzee, J. C.,
Crawford, R. J. M., Dyer, B. M., Leshoro, T. M. & Upfold, L. (2013) Influence of local and regional prey availability on breeding performance ofAfrican penguins Spheniscus demersus. Marine Ecology Progress Series
473: 291–301.
Sherley, R. B., Ludynia, K., Lamont, T., Roux, J.-P., Crawford, R. J. M. &Underhill, L. G. (in press) The initial journey of an endangered penguin:
implications for seabird conservation. Endangered Species Research.

Introduction

In the 1970s, the golden lion tamarin
Captive populations can serve a vari(Leontopithecus rosalia) population
ety of functions including education,
was estimated at only 200 individuresearch and as a reservoir for wildals, with a declining captive populapopulations. The role of captive popution. Serious efforts were needed
lations in conserving endangered
if golden lion tamarins were going
species is not new; in fact, the field
to be conserved. Over the last fourof conservation biology was founded
decades, conservation strategies forin partnership with the zoo comthe golden lion tamarin have involved munity. As wild populations become
collaborations between zoos, nonsmaller and more isolated, the tools
governmental organisations, fieldand science used to manage captive
biologist, governments and many
populations can be of value whenothers. The programme has usedmanaging wild populations (Redfordan integrated approach, managing
et al. 2012). This integration between
ex situ and in situ populations underin situ and ex situ programmes isa single goal and a unified set ofincreasingly important. Recently,
priorities. Under this approach, thethe IUCN SSC Conservation Breedcaptive population is stable and theing Specialist Group put forth thewild population has increased to
One Plan approach to conservation
approximately 1,700 individuals. Alplanning (Byers et al., this issue). This
though the golden lion tamarin is still
approach involves creating holisendangered and in need of conservatic conservation action plans thattion due to the fragmented landscape, integrate, not distinguish, ex situ
this integrated approach has led toand in situ programme strategies forthe success observed up to this point
species. There are examples that exist
and continues to be the backbone forof species where this type of integolden lion tamarin conservation.
gration is occurring already, such as
black-footed ferrets (Mustela nigripes)
and California condors (Gymnogyps
californianus). Another example is theFig. 1Golden lion tamarins.
© Meghan Murphy/Smithsonian National Zoo

1
2*

Zoo Atlanta, Atlanta, GA, USA
Smithsonian Conservation Biology
Institute, Washington, DC, USA
E-mail for correspondence:jmickelberg@zooatlanta.org

golden lion tamarin (Leontopithecus
rosalia), which has been managed as
one metapopulation, integrating insitu and ex situ programmes (Fig. 1).
The golden lion tamarin is a small,endangered primate endemic to the
Atlantic Coastal Forest of Brazil. Living just 70 km northwest of the city of
Rio de Janeiro, golden lion tamarins
inhabit a highly fragmented forest
where less than 7% of the original
forest remains (Kleiman & Rylands
2002). Due to deforestation and thepet trade, only a few hundred animals
were estimated to be living in theearly 1970s when a conservation programme to protect golden lion tamarins began. The primary objective of
this programme was to prevent theextinction of golden lion tamarins
and further loss of their habitat, thelowland coastal forest. What has
unfolded over the past four decades
is a holistic conservation programmethat includes the integration of wild
and captive management and isbased on collaborations between biologists, private landowners, governments, zoos and many other stakeholders (Kleiman & Rylands 2002).

»

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Golden Lion Tamarin»

Population Growth
Population
Growth800

A Model for
Collaboration andIntegration
In 1972, the Saving the Lion Marmoset conference, held at the Smithsonian National Zoo, brought together
international biologists working withlion tamarins in efforts to develop
a conservation strategy for golden
lion tamarins. One focus of that strategy was to develop a healthy captive
population capable of supporting
reintroduction (Kleiman & Rylands
2002). This meeting was a turning
point for the golden lion tamarin
and led to long-term international
collaborations between biologists
whose goals were united in attempting to increase the population in situ
and ex situ and prevent what seemed
to be the impending extinction of
the golden lion tamarin. The partnerships that developed at this meeting
formed the basis for the integrationof the in situ and ex situ programmes.

Overall, the programme has served
as an excellent model for AZA’s SSP
Program. In just a few years, IRMC
had morphed into a committee that
included national and international
experts on all aspects of golden lion
tamarin biology and conservation,in situ and ex situ. In 1990, a decree
made this committee the official advisor to the Brazilian government and,in later years, the committee wasrenamed the International Committee for the Conservation and Management of Lion Tamarins (ICCM) by
the Brazilian environmental agency(Kleiman & Rylands 2002). ICCM
met annually to review all aspectsof golden lion tamarin biology andconservation and made recommendations for actions related to both insitu and ex situ populations. With theBrazilian government owning captive
and wild golden lion tamarins, andone international committee making
management recommendations forex situ and in situ, there was a clear
integration between the two populations under one single set of goals
and priorities – a One Plan approach(Byers et al., this issue).

Reintroduction
In 1984, the link between ex situ
and in situ programmes was further
strengthened when captive golden
lion tamarins were used to augment
the wild population. The Golden Lion
Tamarin Reintroduction Program
began in efforts to increase thenumber of golden lion tamarins in
the population, increase the genetic
diversity through careful selection ofreintroduction candidates and also
increase habitat available for golden
lion tamarins (Beck & Martins 2003).
Reintroduction ended in 2000 after
a total of 147 captive animals andsix confiscated animals had beenreleased (Beck & Martins 2003). At
this point, the population was growing well on its own and there wasno longer suitable habitat withincommuting distance. The reintroduced animals have left a descendant
population of over 700 individuals of
which over 99% are wild-born (Fig.
2; Mickelberg 2011). This population
continues to expand and makes up
more than a third of the entire wild
population.
Through reintroduction, the ex situ
population became an integrated
component of the golden lion tamarin metapopulation. Reintroduction
included the careful selection ofindividuals based on their potential
genetic contribution to the reintroduced and captive populations.
The best reintroduction candidates
would be those individuals that were
genetically over-represented in
the captive population and underrepresented in the reintroduced
population; these individuals would
have the greatest positive impact on
the genetic diversity in both the captive and reintroduced population, if
reintroduced. By using this technique
for selecting animals, the captive
population has served as a demographic and genetic resource for thewild population and has contributed
significantly to the overall viability of
the golden lion tamarin metapopulation (Mickelberg 2011).

Translating
Captive Management
to Wild Management
The population of reintroduced golden
lion tamarins has been extensively
monitored for the last 25 years. A large
percentage of the groups living inthese areas have been monitored andcaptured every six months to determine group composition and for theplacement of radio telemetry collars,permanent tattoos and temporary dye
markings. These historical records provide continuous data on group composition, births, deaths and migrants
to and from the study groups. These
data are not unlike the data collected
for captive populations. In fact, manyof the tools used for managing captive
populations have been applied for the
management of the wild population.
Golden lion tamarins live in highly
fragmented habitat with, in somecases, only a few groups living in
a forest fragment, not unlike zoo
populations with individuals spreadout between zoos. For effective
conservation and population viability,
these populations need to be connected in order to maintain genetic
diversity and population viability. One
technique the golden lion tamarinprogramme has used is following thesame strategy used for developing
captive breeding plans. Using theinventory information, a pedigree
database using the software Single
Population Animal Records Keeping
System (SPARKS) is used to generate and maintain a studbook for the
reintroduced and a large componentof the wild population. Pedigree
analysis using the software PMx has
been employed to help assess thestatus of the reintroduced population
as well as direct management strategies to best connect populations(Mickelberg 2011). As the populationof golden lion tamarins gets larger, it
will become increasingly difficult toobtain reliable pedigree information.
However, this provides an example of
how pedigree analysis can be a powerful tool for assessing the genetic
status of small populations in situ.

700

Reintroduced

600
500

Captive
400

Reintroduction
300

Captive
200
100
0
1980
1981
1982
1983
1984
1985
1986
1987
1988
1989
1990
1991
1992
1993
1994
1995
1996
1997
1998
1999
2000
2001
2002
2003
2004
2005
2006
2007
2008
2009
2010

In the 1970s, with less than 90 golden
lion tamarins in captivity, the population was small and not self-sustaining(Kleiman & Rylands 2002). Reproduction efforts were unsuccessful,survivorship was poor and the importations from the wild population had
been eliminated in order to support
the in situ conservation efforts. With
modifications in husbandry, the captive population of golden lion tamarins increased and in the 1980s began
to stabilise (Kleiman & Rylands 2002).
At that point, management of thecaptive population moved to a moregenetically based management
strategy to maintain genetic diversity.
With a healthy captive population
and an understanding of the wild
population from field research, reintroduction became a real possibility.

By the 1980s, due to improved husbandry and management, the captive
population was increasing exponentially. Recognising the importanceof cooperation between zoos, theInternational Research and Management Committee (IRMC) was formed
in 1981 under the guidance of Devra
Kleiman (Kleiman & Rylands 2002).
Representatives from several institutions that were at the time holding orowning golden lion tamarins joined
this committee with the primary
focus on managing the global captive
population. This committee established a formal cooperative breeding agreement that all recipientsof golden lion tamarins had to sign(and which is still in effect) in order toreceive golden lion tamarins.

Population Size

Buildinga Captive Population

Year
Fig. 2
Population growth in the reintroduced and captive population since 1980.
Population numbers for the reintroduced population were
estimated based on annual census data.

The cross-pollination of knowledge
and tools between in situ and exsitu programmes has assisted in therecovery of the golden lion tamarin.
In 2003, the status of the golden
lion tamarin was downgraded from
Critically Endangered to Endangered.
Currently, there are approximately
1,700 golden lion tamarins living in
the wild and about 500 golden lion
tamarins living in 150 zoos around theworld. While the golden lion tamarin
is making a recovery, the battle tosave the golden lion tamarin is notover. With the limited forest available,
the population will always need closemonitoring at the least, but throughthe integration of in situ and ex situ
programmes, we move closer to protecting this species in perpetuity.

References
•

•

•

•

Beck, B. & Martins, A. (2003)
Annual Report of the Golden
Lion Tamarin Reintroduction. Unpublished report. Washington,
DC: Smithsonian National Zoo.
Kleiman, D. G. & Rylands, A. B.
(eds) (2002) Lion Tamarins: Biology and Conservation. Washington, DC: Smithsonian Institution Press.
Mickelberg, J. (2011) Understanding and managing isolation in a fragmented populationof golden lion tamarins. PhD
dissertation, George Mason
University, Fairfax, VA.
Redford, K. H., Jensen, D. B. &Breheny, J. J. (2012) Integrating
the captive and the wild. Science 338: 1157–1158.

29

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WAZA magazine Vol 14/2013

Ozark Hellbender31

Jeffrey A. Ettling1,* & Jeffrey T. Briggler2

Conservation Efforts for theEndangered Ozark Hellbender
Summary

Introduction

The Ozark hellbender (Cryptobranchus alleganiensis bishopi) is anendangered aquatic salamanderthat inhabits cold-water streams in
the Ozark Highlands. Due to drastic
population declines over the past 40
years, the Ozark Hellbender Working
Group was established to develop
a recovery plan for the species. It wasdetermined that without intervention, including a captive propagation programme, it was likely thatthe species would go extinct in thenear future. Due to interagency
collaboration, significant progresshas occurred with refined hatching
and husbandry protocols, expansionof rearing facilities, construction of
artificial breeding streams, devoted
funding and dedicated staff. Alongwith the world’s first captive breeding of Ozark hellbenders in 2011
and subsequent remarkable captive
breeding in 2012, together with wildcollected eggs, over 4,000 larvae/juveniles have been produced and/or
raised at Saint Louis Zoo. To date, 102
juvenile Ozark hellbenders reared at
Saint Louis Zoo have been released
into the wild to augment remaining
populations. Based on the success ofthe captive propagation programme,
post-release survival and dedicatedindividuals of various organisations,the future of the Ozark hellbender islooking optimistic.

Hellbenders are large aquatic salamanders that can reach lengths up
to 50 cm and are long-lived (25–
30 years). There are two subspeciesof hellbender: the eastern hellbender(Cryptobranchus alleganiensis alleganiensis), which has a distribution
from southern New York state south
to Georgia and west to Missouri, andthe Ozark hellbender (C. a. bishopi)(Fig. 1), which only occurs in the
Ozark Highlands of south-central
Missouri and adjacent north-central
Arkansas. Missouri is the only place inthe USA where both subspecies occur.
The closest relatives of the hellbender
are the Chinese giant salamander(Andrias davidianus) and the Japanese
giant salamander (A. japonicus).

1

WildCare Institute, Saint Louis Zoo,
St. Louis, MO, USA
2 Missouri Department of Conservation,
Jefferson City, MO, USA* E-mail for correspondence:
ettling@stlzoo.org

Hellbenders inhabit cool, highly
oxygenated, fast-flowing streams.
They are perfectly adapted for a fully
aquatic existence with a dorsal ventrally flattened body and rudder-like
tail. The conspicuous folds of skin on
the sides of the body and legs areused to absorb dissolved oxygen fromthe water. While they do have lungs,
they are small and primarily used tohelp with buoyancy. They are primarily nocturnal and spend the daylight
hours under large rocks or in bedrock
crevices on the river bottom, where
they forage principally on crayfish.

Fig. 1
Adult Ozark hellbender.
© Ray Meibaum/Saint Louis Zoo»
Hellbender populations in Missouri
have declined by more than 70% overthe past 40 years, with a prominent
shift in the age structure where large,
mature individuals mostly predominate and young age classes are virtually absent (Wheeler et al. 2003; Briggler et al. 2007, 2010). While it has
been hard to pinpoint a single causeof the population decline, it appears
to be a combination of factors including habitat degradation, disease,degraded water quality, over-collection and predation by non-nativefish (USFWS 2011). As a result of thisdecline, both subspecies were listed
as critically imperilled and state endangered in Missouri in 2003, and theOzark hellbender was recently listed
as endangered under the Endangered
Species Act (USFWS 2011).
While the carrying capacity of Ozark
streams has been estimated at 11,000
specimens, current estimates ofOzark hellbenders remaining in thewild are less than 600 individuals. The
results of a Population and Habitat Viability Assessment (PHVA), facilitatedby the IUCN SSC Conservation Breeding Specialist Group, indicate that all
hellbender populations have a highrisk of extinction (above 96%) overthe next 75 years, unless populations
can be bolstered (Briggler et al. 2007).
A comprehensive conservation strategy, to ensure the long-term survivaland recovery of the Ozark hellbender,
was developed by the Ozark Hellbender Working Group, which is comprised of state and federal agencies,
universities, zoos, non-governmental
agencies and interested individuals(Briggler et al. 2010). While addressing the reasons for the decline in thewild, it was determined that captive
propagation and head-starting were
essential to the long-term recovery of
the Ozark hellbender.

Captive Propagationand Head-starting
A captive propagation and head-start
programme for the Ozark hellbender
was initiated by the Saint Louis Zoo’s
WildCare Institute Ron Goellner
Center for Hellbender Conservationand the Missouri Department of Conservation in 2002 (Briggler et al. 2011).
The programme was designed to rear
individuals for increasing wild populations through augmentation and, if
necessary, reintroduction. While recruitment is limited in the wild, some
egg clutches have been discovered
annually in recent years. Portions ofthese clutches have been brought toSaint Louis Zoo and/or the Missouri
Department of Conservation Shepherd of the Hills Fish Hatchery for
hatching and head-starting efforts.
Currently, over 1,500 Ozark hellbenders hatched from wild-collected eggs
are being raised at Saint Louis Zoo for
future releases.
Although these head-started individuals are essential to the recovery
efforts for the Ozark hellbender, thelarger goal is captive reproduction,a feat that had never been achieved.
To help reach the goal of captive reproduction, Saint Louis Zoo constructed an indoor stream (9.7 × 1.7 × 0.6 m)
in 2002 and two outdoor streams(11.3 × 1.5 × 1.4 m and 11.7 × 1.8 × 1.4 m)
in 2011. Breeding stock was obtained
from three genetically distinct Missouri Ozark rivers: the North Fork of
the White River, Eleven Point Riverand Current River. These three populations are each housed separately
in one the aforementioned artificial
streams. Simulation of natural habitat(i.e. gravel bottom, shelter rocks
and artificial nesting chambers) andseasonal environmental conditions(i.e. photoperiod, water temperature,
precipitation patterns and water
quality parameters) were mimicked
to induce breeding activity. Every
year since 2007 hellbenders have laideggs, but were not being fertilised by
the males. However, a milestone wasachieved on 18 October 2011 when

two clutches of fertilised eggs (Fig. 2)
from the Eleven Point River population were discovered in one of theoutdoor streams. This was the world’s
first captive breeding of the species,
thus resulting in approximately 150
larvae.
An even greater achievement
occurred the following year withbreeding success in all three streams.
Between 22 September and 1 October 2012, eight Ozark hellbenders laid
eggs: three clutches from the Current
River, three clutches from the North
Fork of the White River and two
clutches from the Eleven Point River.
There were approximately 2,800 fertile eggs from the combined clutches,from which 2,500 larvae hatched. The
significance of this second breeding
was that all three river populations ofOzark hellbender reproduced, including the North Fork of the White River
population that has been maintainedindoors for the past eight years.
These successes have paved theway for bolstering wild populations
through augmentation.

Augmentation of Wild
Populations
Success of any propagation effort isto eventually release animals backinto their native habitat. The firstrelease of captive-raised Ozark hellbenders occurred in 2008 in the North
Fork of the White River. Thirty-six
juveniles that had been hatched fromeggs collected in 2002 and raised at
Saint Louis Zoo were released at two
locations with varying rock composition. Over the next year to year anda half, these individuals were tracked
using radio-telemetry to determine
the feasibility of head-starting
juvenile hellbenders. The results ofthe study demonstrated that these
captive-reared hellbenders had highsurvivorship (75% and 48%), had established home ranges, were growing
and were demonstrating reproductive cycling at the same time as thewild population (Briggler et al. 2012).

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Jennifer Pramuk1,*, Fred Koontz1 & Harriet Allen2»
References•

Fig. 2
Well-developed Ozark hellbender embryos.
© Mark Wanner/Saint Louis Zoo•

Conclusions: Hopefor Hellbenders
The success of this first release suggests that augmenting wild populations with captive, head-started animals can be successful and that they
can survive in the wild (Briggler et
al. 2012). This has led to subsequent
releases in 2012 of an additional 66
Ozark hellbender juveniles in the
North Fork of the White River. These
animals will be monitored long-term
to not only evaluate survivorship andacclimation to the wild, but also togain a better understanding of thefactors contributing to their decline(i.e. amphibian chytrid fungus infection rates, abnormality rates, heavy
metal accumulation, reproductive
and stress hormones, etc.). Withless than 600 Ozark hellbenders
estimated to remain in the wild, the4,000 larvae and juveniles currently
being raised at Saint Louis Zoo will
make a substantial contribution to
the long-term recovery of the species
over the next five years.

The success of this conservation
programme is due to the dedication
and resourcefulness of many individuals, institutions and organisations,
including (but not limited to) SaintLouis Zoo (keepers, veterinarians, life
support staff), Missouri Departmentof Conservation, US Fish and Wildlife
Service, US Forest Service, National
Park Service and Arkansas Game andFish Commission. Through teamwork
and persistence, the aforementioned
partners and several universities,
which constitute the Ozark Hellbender Working Group, are making
great strides towards the recovery of
the Ozark hellbender through active
research, including monitoring of
populations, investigating abnormalities, exploring potential interactions
with predators, assessing healthconditions and sperm quality, andevaluating the frequency and distribution of diseases (e.g. amphibian
chytrid fungus, ranavirus). As well as
the remarkable achievements of the
propagation efforts at the Ron Goellner Center for Hellbender Conservation, WildCare Institute, Saint Louis
Zoo. These achievements will not
only buy time to further address thedecline of this species, but will likely
be the “safety net” needed to savethis unique native of the cold-water
streams of the Ozark Highlands.

•

•

•

Briggler, J., Utrup, J., Davidson,
C., Humphries, J., Groves, J.,
Johnson, T., Ettling, J., Wanner,
M., Traylor-Holzer, K., Reed, D.,
Lindgren, V. & Byers, O. (eds)(2007) Hellbender Populationand Habitat Viability Assessment: Final Report. Apple Valley,
MN: IUCN SSC Conservation
Breeding Specialist Group.
Briggler, J. T., Crabill, T., Irwin,
K. J., Davidson, C., Utrup, J. &Salveter, A. (eds) (2010) Hellbender Conservation Strategy:
An Action Plan for the Recoveryof the Ozark and Eastern Hellbender in the Ozark Highlands ofMissouri and Arkansas. Jefferson
City, MO: Ozark HellbenderWorking Group.
Briggler, J. T., Crabill, T. L., Irwin,
K. J., Davidson, C., Civiello, J. A.,
Wanner, M. D., Schuette, C. D.,
Armstrong, S. L., Grant, V., Davidson, T. & Ettling, J. A. (2012)
Propagation, Augmentation,
and Reintroduction Plan for the
Ozark Hellbender (Cryptobranchus alleganiensis bishopi).
Jefferson City, MO: Ozark Hellbender Propagation Committee.
US Fish and Wildlife Service(USFWS) (2011) Endangered
and threatened wildlife andplants; endangered status for
the Ozark hellbender salamander. Federal Register 76: 61956.
Wheeler, B. A., Prosen, E., Mathis, A. & Wilkinson, R. F. (2003)
Population declines of a longlived salamander: a 20+-year
study of hellbenders, Cryptobranchus alleganiensis. Biological Conservation 109: 151−156.

The Western Pond Turtle
in Washington: Crawling Backfrom Extirpation
Summary

Introduction

The western pond turtle (Actinemys
marmorata) was once abundant
throughout the lowland areas of British Columbia and Washington’s Puget
Sound, through western Oregon,
California and into the northernmost
areas of Baja California. Historically,
this turtle was only one of two native
freshwater turtles in the Pacific Coast
states of the USA. Today, the turtle isin decline throughout its range fromthreats including habitat alterationand presence of invasive species toemerging disease. In Washington, because of particularly dramatic population declines, the species was listed by
the state as endangered in 1993. Overthe past two decades, stakeholders inWashington have worked to save thisspecies from extinction through a twopronged ex situ and in situ approach,combining head-starting and reintroduction, habitat improvement, control
of predators and invasive species, andpopulation monitoring and research.
The 20th anniversary of the listing was
an opportune time to systematicallyexamine progress to date and employ
science-based methods to assess
population viability and set management priorities for this intensively
managed programme. An IUCN SSC
Conservation Breeding Specialist
Group-facilitated Population and Habitat Viability Assessment workshop,
held in late 2012, aided the recovery
team in accomplishing this goal.

Populations of the western pond
turtle (Actinemys marmorata),
a medium-sized aquatic species
that at one time ranged from British Columbia to Baja California, aredeclining throughout their range (fora species review, see Ernst & Lovich2009). Lowland prairie wetlands,
the environment type required by
the turtle, is the most endangered
habitat in Washington state, having
been largely converted to agriculture
and housing. By 1990, the species in
Washington was close to becoming
extirpated with fewer than 150 turtles
surviving, primarily from decades of
uncontrolled habitat alteration andcommercial collecting for food, butalso from an unknown respiratory disease that was causing a rapid decline
in one of the two remaining populations state-wide, both located in the
Columbia River Gorge.

1
2*

Woodland Park Zoo, Seattle, WA, USA
Washington Department of Fish andWildlife, Olympia, WA, USA
E-mail for correspondence:
jennifer.pramuk@zoo.org

In 1990, in response to the disease
outbreak and low population numbers, Woodland Park Zoo and the
Washington Department of Fish andWildlife (WDFW) partnered in a triage
effort to bring a founder population
into captivity for treatment and establishment of an ex situ programme.
At the same time, WDFW initiatedan in situ plan for species recovery
that included habitat improvement,
control of predators and invasive
species, and population monitoring
and research. From the onset, theinitiative has been a collaborative one,
involving many organisations andindividuals, too numerous to list here.
Key agencies, in addition to WDFW,
include the US Fish and Wildlife
Service, US Forest Service, Washington State Parks and The Nature
Conservancy. Since 2000, Oregon
Zoo has supported and participatedsignificantly in both in situ and ex situ
activities; Point Defiance Zoo andSeattle Aquarium have assisted in thepast. Frank Slavens (former reptile
curator at Woodland Park Zoo) and
Kate Slavens (former WDFW biologist) have played key roles, as have
WDFW biologists David Anderson,
Michelle Tirhi and Jeffrey Skriletz.

»

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Western Pond Turtle

35»
PHVA: A Planning
Tool for Intensively
Managed Species

Western Pond
Turtle Recovery
in Washington State
The Washington State Recovery Planfor the Western Pond Turtle (Hays etal. 1999) provides the frameworkthat guides recovery actions for the
species. Recovery goals, objectives,
strategies and tasks are outlinedin the plan, as well as a primer on
the species’ biology. The goal of the
programme is to re-establish selfsustaining populations of western
pond turtles in two regions of thestate: Puget Sound and the ColumbiaRiver Gorge. Complete recovery is defined as requiring seven establishedpopulations (three in Puget Soundand four in the Columbia River Gorge)of more than 200 turtles comprising
no more than 70% adults sustained
through natural recruitment. In addition, recovery will ensure that boththe associated wetlands and uplandnesting habitat at all sites are securefrom excessive human development
and disturbance.

Fig. 1Since 1991, 1,300 western pond turtles have been head-started and released,
growing the wild population from 150 to an estimated 1,500 turtles.
© Ryan Hawk/Woodland Park Zoo

Recovery strategies include thefollowing goals: survey and monitor populations; enhance numbers
through captive breeding/headstarting, creating new populations,controlling invasive bullfrogs andother predators and minimising human disturbance; improve habitat;
conduct research; manage data andinformation; conduct public conservation education; and evaluate andenforce relevant wildlife regulations.
In 14 years, significant progress has
been made in all of these areas. Each
year, the recovery team meets toreview progress and set plans for the
coming field season.
Today, primarily through head-startingand habitat acquisition, the number ofwestern pond turtles in Washington
has grown from 150 (1990 census)
to an estimated 1,500 (Fig. 1). The
number of populations has increased
through reintroduction from just two
Columbia River Gorge locations in1990 to six sites, two in Puget Soundand four in the Columbia River Gorge
today. Since 1991, head-starting eachyear uses wild-collected eggs andhatchlings, which are maintained at
the zoo for 10 months until the turtles
are large enough to avoid being eaten

by non-native bullfrogs. In mid-summer, the team collects morphometricdata on the hatchlings – they are permanently identified with transponders
and shell notches – and released into
the wild. In the past 22 years, morethan 1,300 hatchlings have been released to the wild and reintroduced at
all six population sites. Also essential
has been the acquisition or permitted
use of 735 acres of habitat at the fieldsites, including locations in four different state counties.
Other significant in situ and ex situ
actions, besides habitat acquisition,
have included: efforts to control
invasive North American bullfrogs(Lithobates catesbeianus) through egg
mass collection and adult removal
at Sondino, the only site currently
with more than 200 turtles; removalof invasive plants at several sites toimprove upland habitat; nest site enhancement through grass plantingsand soil improvement; population
monitoring through annual assessments; research on survivability(Vander Haegen et al. 2009); andpublic education and interpretation
at Woodland Park Zoo and Oregon
Zoo, including significant local media
each year on hatchling release days.

Integrating in situ and ex situ approaches within any one species
recovery programme is complex andrequires synchronous management
practices. In the case of the western pond turtle in Washington, therecovery challenge has been exacerbated by the slow reproduction andconcomitant population recovery
of a long-lived reptile, and the othersignificant threats still facing the species. Recently the team has observed
yet another threat: an emerging
condition known as Ulcerative Shell
Disease. This disease of yet unknown
cause affects the turtles by eroding
the underlying bone of the carapace
and plastron, with advanced cases
affecting the spine and leading tolowered fitness, paralysis and evendeath. All of these threats combined
require the team to optimise its insitu and ex situ resources.
In 2012, the team sought the assistance of the IUCN SSC Conservation
Breeding Specialist Group (CBSG) to
conduct a Population and Habitat Viability Assessment (PHVA) workshop(Fig. 2). The purpose was to investigate the present and future state of
the western pond turtle in Washington
and bring together relevant stakeholders, including WDFW, partnering zoos
and others working on similar recovery efforts for the species in California.
The PHVA was designed to address
four specific goals: employ sciencebased methodology, including Vortex
modelling to evaluate the current
population status; identify optimal
management alternatives to enhance
species viability (e.g. determine therelative efficacy of continued headstarting, habitat management andefforts to reduce bullfrog populations);
prioritise future research; and identify
ways to improve communication andprogramme implementation. Workshop funding was provided by Woodland Park Zoo, Oregon Zoo, Northwest
Zoo and Aquarium Alliance and WDFW.

The PHVA workshop process isdesigned to optimise productivity
over a short time frame while accommodating a diversity of stakeholders with often vastly different
backgrounds and opinions. This
three-day workshop, attended by
30 participants, was held in Olympia,
Washington from 13 until 15 November 2012 and was expertly facilitatedby three representatives from CBSG.
The workshop process is initiatedwith a discussion of threats facing therecovery species and developmentof a threat diagram. This interactive
activity engages the participants andprovides a starting point to aid thecollective understanding of threats tospecies recovery.
Following this initial exercise, theparticipants are divided into working
groups according to their expertise.
These working groups participate inbrainstorming sessions to tackle specific issues confronting species recovery. For example, the working groups
were assembled to address current
western pond turtle population
status, habitat, population viability
analysis and ex situ conservation andhusbandry. Working groups prioritiseproblem statements relating to theiridentified issues and then assemble
data, and prepare short and longterm goals for addressing problems.
Plenary sessions then serve to provide a report out to the larger groupduring which the facilitators encourage and lead discussions on thegroups’ findings. The facilitators also
provide a thorough explanation of
the Vortex software and population
viability assessment analyses, key tounderstanding the current and futurestates of the recovery species andfor informing workshop proceedings.
These analyses are performed ondata provided by workshop participants and gathered from publishedliterature prior to the meeting.

The PHVA report is in preparation
and when complete will be available
through the CBSG website. Many
actions and important observations
were identified, with the following
subset deemed of highest priority:
the epidemiology, prevalence andeffects of Ulcerative Shell Disease
are poorly understood and require
immediate attention and research;
there is a greater need for in situ andex situ data and information sharing
between stakeholders; an additional
population site should be added within the next five years; low juvenile
recruitment and the threat of invasive
bullfrogs were determined as key factors influencing population viability;
adult females are critically importantto the long-term survivability of thewild population; and habitat restoration for salmon could be negatively
influencing turtle recovery at somesites and should be evaluated.

Conclusions
For more than two decades, a combined in situ and ex situ species recovery programme in Washington for thewestern pond turtle has shown promising results. While the species is not
fully recovered, it is no longer on thebrink of extinction. The programme’s
collaborative public–private partnership between state agencies, federal
agencies, non-governmental organisations and zoo-based conservation
organisations has demonstrated theeffectiveness of combining the expertise of multiple stakeholders andfacility resources. A continuing impediment to progress has been how
to best organise and manage suchcomplex efforts, especially in a challenging fiscal environment. To thisend, we recommend the importanceof a well-conceived recovery plan,
regular communication among teammembers and periodic populationlevel analyses to inform management
planning.

36 Western Pond Turtle

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Caroline Lees1,*, Paul Andrew2, Andrew Sharman3 & Onnie Byers4»

Saving the Devil:
One Species, One Plan
Summary

Fig. 2
A Population and Habitat Viability Assessment workshop conducted in 2012 helped the recovery teamassign priority in situ and ex situ management actions.
© Fred Koontz/Woodland Park Zoo

Based on our PVHA experience, we
recommend it as a tool for improving
population-level analyses of intensively managed threatened species.
In addition to the analyses, we foundthat a surprisingly important benefitof the PHVA was that it provided
a forum for summarising collective
knowledge and discussing prioritised
threats and needed actions. In preparation for the PHVA, for example,
stakeholders for the first time wererequired to collate demographic andgenetic data from each recovery sitein order to perform the modelling
exercises. Also, prior to the workshop, little communication existed
between the California and Washington ex situ western pond turtle
programmes, but now these organisations are sharing their husbandry
data and expertise and are working
towards streamlining best practices.

An important team-building outcomeof the PHVA was forming thematic
subgroups that are expected tocontinue addressing action plans andtimelines. For example, an effort isunderway to quantify the prevalenceand epidemiology of Ulcerative Shell
Disease. Another product of theworkshop has been the developmentof new Internet-based tools (website
and listserv) that will aid communication efforts among stakeholders.
In summary, efforts to recover theendangered western pond turtle in
Washington will continue with a mix
of in situ and ex situ approaches,
which bring together the resourcesof multiple government agencies andconservation organisations, including zoos of the region. The team also
aims to build on its two-decade historical foundation of cooperation andadaptive management. Programmepartners expect that momentum andproducts resulting from the PHVA will
greatly aid these efforts.

References•

Ernst, C. H. & Lovich, J. E. (2009)
Turtles of the United States andCanada, 2nd ed. Baltimore, MD:
John Hopkins University Press.
• Hays, D. W., McAllister, K. R.,
Richardson, S. A. & Stinson,
D. W. (1999) Washington State
Recovery Plan for the Western
Pond Turtle. Olympia, WA:
Washington Department ofFish and Wildlife.
• Vander Haegen, W. M., Clark,
S. L., Perillo, K. M., Anderson, D. P. & Allen, H. L. (2009)
Survival and causes of mortality of head-started western
pond turtles on Pierce National
Wildlife Refuge, Washington.
Journal of Wildlife Management73: 1402–1406.

Tasmanian devils (Sarcophilus harrisii)
are at risk of extinction from a disease
known as Devil Facial Tumour Disease
and, at current rates of spread, species extinction is predicted in 25 to 30
years. An insurance population has
been established, which is designed
to take the species through thisextinction event and provide for full
ecological recovery. This programmecomprises a metapopulation of captive, free-ranging and wild populations, linked through strategic animal
movements. The development of thisapproach to recovery closely follows
the One Plan approach advocatedby CBSG, in its careful inclusion fromthe outset “of all populations of thespecies, inside and outside theirnatural range, under all conditions ofmanagement, engaging all responsible parties and all available resourcesfrom the very start of the species
conservation planning process”. To
date, this programme has achieved
a number of significant milestones
and is now moving from insurance toecological recovery.

1

2
3

4
*

IUCN SSC Conservation BreedingSpecialist Group Australasia,
c/o Auckland Zoo, Auckland,
New Zealand
Taronga Zoo, Sydney, Australia
Australian Antarctic Division,Commonwealth of Australia, Kingston,Australia (formerly Save the Tasmanian
Devil Program, Department of Primary
Industries, Parks, Water andEnvironment, Tasmania)
IUCN SSC Conservation BreedingSpecialist Group, Apple Valley, MN, USA
E-mail for correspondence:
caroline@cbsgaustralasia.org

Devil Facial
Tumour Disease
Tasmanian devils (Sarcophilus harrisii)
were once common across mainland Australia, but are now confinedto the island of Tasmania (Fig. 1).
Although considered common in thewild until the 1990s, they are now at
risk of extinction due to a previously
unknown Devil Facial Tumour Disease(DFTD). DFTD is a transmissible
cancer, passed between individuals
through biting, which is common
around social feeds and the breeding season. Since first observationsof DFTD in the mid to late 1990s,
the disease “front” has continued
to move across the island, reducing
some affected populations by up to
90% (DPIPWE 2013).
In 2003, regional zoo representatives,
along with interested field researchers, ecologists, disease specialists andrelevant non-government organisations, were invited to a governmentorganised workshop in Tasmania,

aimed at building a shared understanding of the disease issue, what
was known about it, what could or
should be done, and who might bewilling and able to help. Little was
known about the disease at that time:
there was no diagnostic test, incubation times were uncertain, modes
and rates of transmission werelargely unknown and, consequently,
there was no agreed prognosis forlong-term impact on species survival. In response to this, and in close
collaboration with the Tasmanian
wildlife agency, the zoo community
agreed to revamp its regional captive
population, which at the time was foreducational display, into a short-term
insurance programme designed tospan a period during which further
research and monitoring would
evaluate the nature and likely impactof the disease. Depending on theoutcomes of this, the captive population could either be wound down or
ramped up to provide more substantial support.

Fig. 1
Tasmanian devil.
© Roger Smith

38 Tasmanian Devil

A Short-term
Insurance Population

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A Change of Plan

In 2007, the Tasmanian government
Through the Australasian zoo associa- called a meeting of scientists totion, a 10-year insurance programme
consolidate what had been learned
was established, aimed at retaining
since 2003 about DFTD and its impact.
90% of wild source gene diversity for
The conclusions of this meeting
10 years. Analyses indicated that thiswere stark. The disease had moved
would require around 30 wild-caught
swiftly across the devil’s range, withfounders, sufficient carrying capacity
up to 90% of animals lost in affected
for 150 individuals and a programme
populations. No resistance in the wildof close genetic management. Four
had been encountered, with unusucore breeding centres were desigally low levels of gene diversity acrossnated, one in each of four Australian
the species cited as a likely reason
states. Each comprised a primary
for the apparently undifferentiatedbreeding zoo, with other local zoos
response between individuals. Spesupporting as satellite breedingcies extinction was predicted in 25 toand holding facilities. Restricted
30 years. It was immediately apparent
to zoo community representatives
animal exchanges between these“silos” in the early stages provided
that the existing insurance population
an additional layer of biosecurity,
would be inadequate to cater for thefacilitated inbreeding management
predicted extinction event. Tasmanianand smoothed logistics. Devils had
wildlife agency authorities were notified and work began to reshape theproved in the past to be a challenging species to work with. To provide
programme around more ambitious
the necessary regional up-skilling,goals better suited to the species’ preTrowunna Wildlife Park, the only
dicament. The IUCN SSC Conservainstitution to have demonstrated
tion Breeding Specialist Group (CBSG)
long-term successful management
was consulted and a programme wasof the species, established an on-site
developed that would be capable oftraining course in devil management
sustaining the species through an
and breeding, to which all participatextinction event and into full ecologiing institutions sent keeping staff
cal recovery. The following goals were
before receiving programme animals. agreed (for 50 years):
By 2007, founders had been received • to be free of DFTD;
and two seasons of litters produced.
• retention of 95% of a representative sample of wild gene diversity;• retention of wild behaviours;• retention of devil-associated floraand fauna (commensal, symbiotic
and parasitic); and• the ability to generate a harvest
for release.
Application of population genetics
theory, consideration of the opportunities and constraints around foundercollection presented by the species’unique predicament and discussionsof what wild and captive resources
might be mobilised through Tasmanian, Australian and international
networks, led to a new insurance
programme strategy. The new model(Fig. 2.) was of a metapopulation
comprising a mix of the following
management styles:

Intensively Managed Captive Populations (Baker et al. 2011). Those inwhich population size, structure andpairings for breeding are closely
controlled to maximise stability andretention of genetic diversity. Animals do not normally share the same
space throughout the breeding season. Natural selection is not assumed
and selection of any kind is actively
avoided. For a given population size,
retention of genetic diversity overgenerations is expected to be relatively high.
Free-range Enclosure Populations.
These have an intermediate levelof management. Groups of animals
are housed together, occupying thesame enclosure space throughout thebreeding season. Stocking densities
are higher than those reported forwild populations. Natural selection
is not assumed but may operate tosome extent. For a given population
size, retention of genetic diversity is
expected to fall in between that for
captive and wild populations.
Isolated Wild Populations. These
occupy large and/or relatively inaccessible natural areas within theformer range of Tasmanian devils.
Boundaries may be human-made or
natural (e.g. water). Management isminimal and there is limited ability to
track population parameters. Natural
selection is expected to be operating. Retention of genetic diversity is
expected to be lower than that of theother two management styles.
It was envisaged that these components would articulate through centralised monitoring and managementof demographic and genetic characteristics, and by the strategic movement and management of animals to
optimise these towards agreed goals.
An increased founder base of 150
wild-caught individuals was agreedon (based on Marshall & Brown 1975),
reflecting more ambitious genetic
goals both with regard to retained

WAZA magazine Vol 14/2013

Tasmanian Devil»

CaptiveWild
isolated

Freeranging

Fig. 2
Target profile of the Tasmanian devil insurance metapopulation:founders = 150, total effective size Ne = 500, total census size (variable) N = 1,500–5,000.

heterozygosity and sampled allelicdiversity, and taking into account thenegligible impact that this extraction
would have on the prognosis for wild
stocks. It was anticipated that the
new long-term genetic goals could be
met with an effective population sizeof Ne = 500, expected to equate toan actual size of approximately 1,500
captive, 2,500 free-ranging or 5,000
wild animals (due to the differential
gene retention abilities of the threemanagement styles), or to some intermediate number reflecting a combination of these three categories. It
was agreed that this size would need
to be reached only once it became nolonger possible to collect devils fromthe wild to supplement gene diversity.
This three-pronged approach to management capitalises on the strengths
and compensates for the weaknessesof each individual management style(Table 1). Once all three components
are in place, and of sufficient size, allinsurance population goals should be
met and the species should be moving towards ecological recovery.

Table 1

Relative strengths and weaknesses of metapopulation components(comparisons are based on populations of equal size):= not provided for, = partially provided for, = provided for(DFTD = Devil Facial Tumour Disease).
Intensively managed captive
populations
Secure from DFTDHigh gene diversity retention
100% wild behaviour
Associated flora and fauna
Natural selection enabled

Free-range enclosure
populations
Secure from DFTDHigh gene diversity retention
100% wild behaviour
Associated flora and fauna
Natural selection enabled

In 2008, after assisting with theredesign of the programme, CBSG
was invited to convene a planningworkshop aimed at moving the newstrategy to implementation. The
workshop, sponsored by Taronga Zoo
and the Tasmanian Department ofPrimary Industries, Parks, Water andEnvironment, brought together 40
field staff, researchers, zoo community leaders, cultural leaders andpolicy makers to work out how andwhere the new programme would
be deployed, and who would be
involved. Working groups considered:
which Tasmanian islands and peninsulas might be suitable for housing
disease-free animals; what the local
and international zoo community

39

Isolated wild populations
Secure from DFTDHigh gene diversity retention
100% wild behaviour
Associated flora and fauna
Natural selection enabled

could provide in terms of space andresources; where the strengths andweaknesses in biosecurity might bein such a metapopulation and how
best to manage this; and how the
proposition of large, free-ranging
populations could be tackled. Importantly at this meeting, a proposal fora free-ranging facility on mainland
Australia was unveiled and developed(CBSG 2008). The resulting blueprint
for large-scale, cost-effective devil
management has since been realised as Devil Ark, a project operated
through Gosford Reptile Park thatis proving to be a highly successful
management model.

40 Tasmanian Devil

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41

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Harriet T. Davies-Mostert1,2,* & Markus Gusset2,3»
The CBSG planning workshop gave
the insurance population its current
shape and catalysed its implementation. It currently comprises approximately 500 individuals, with around
75% held in intensively managed
captive facilities, 20% in free-ranging
enclosures and 5% recently released
to a protected island site. This releasesignals a new phase in the project: in
addition to this initial island release,wild peninsulas are beginning to beisolated through fencing, cleared of
diseased devils and restocked withdisease-free animals. Although theareas that can be isolated in this way
in the immediate future are a small
proportion of the devil’s range, thisdevelopment begins to shift the
project from insurance into ecologicalrecovery, securing a future for devils
in Tasmania.

• The captive community wasinvited into discussions as soon as
it became evident that the species
was in trouble.
• The captive community responded
by evaluating and reshaping its existing captive programme towards
conservation goals: new targets,new founders, new facilities andcentralised up-skilling for animal
management staff.
• As part of the recognised stakeholder group, the team for captive
programme coordination wasmade aware immediately of thedramatic change in status andprognosis for wild populations four
years into the programme.
• The team understood and responded to the change by initiating an immediate redesign of the
programme in collaboration within situ partners and CBSG.
This programme has required and• Ex situ and in situ stakeholders,received an outstanding level of comregulatory and resourcing bodies
mitment, investment and participaunderstood and supported thetion from the zoo industry. It has also
redesign and collectively moved
challenged government and otherit towards its current level of imagencies to embark on activities
plementation. Key to this was thethat were novel and in many ways
2008 CBSG-facilitated Population
conflicted with current thinking andand Habitat Viability Assessment
wildlife management practices. Gain(PHVA) workshop, outcomes froming approval for these activities has
which continue to guide managerequired commitment and persisment strategy.
tence from project staff, which was• Representatives from the zoo
underpinned by an unyielding confiand field communities continue
dence in the science, process and efto meet regularly with governfort that went into the development
ment representatives to reviewof the insurance metapopulation
progress and challenges acrossplan. The success can be attributed
the mosaic of management thatto the integrated One Plan approach
constitutes the Tasmanian devil
adopted by the Save the Tasmanianrecovery effort. CBSG serves as an
Devil Program, widely advocated byindependent and neutral advisor
CBSG and discussed elsewhere (Byon small population management
ers et al., this issue). Features of thestrategy across the management
project that illustrate the practice andcontinuum.
benefits of a One Plan approach, andin particular the effective articulation
Although Tasmanian devils are farof zoo, CBSG and wildlife agency
from secure in the wild, this excepstrengths, are:tional level of investment in a disease-free metapopulation of wild,
free-ranging and captive populations,
underpinned by a One Plan approach,
is not only buying time for the species
but is actively contributing to its reestablishment in the wild.

References•

Baker, A. M., Lacy, R. C., Leus, K.
& Traylor-Holzer, K. (2011) Intensive management of populations for conservation. WAZA
Magazine 12: 40–43.
• DPIPWE (2013) Website of theSave the Tasmanian Devil Program http://www.tassiedevil.
com.au/tasdevil.nsf (accessed
21 May 2013).
• IUCN SSC Conservation Breeding Specialist Group (CBSG)(2008) Tasmanian Devil PHVA
Final Report. Apple Valley, MN:
IUCN SSC Conservation Breeding Specialist Group.
• Marshall, D. R. & Brown, A. H. D.
(1975) Optimum samplingstrategies in genetic conservation. In: Crop Genetic Resources
for Today and Tomorrow (ed. byFrankel, O. H. & Hawkes, J. G.),
pp. 53–80. Cambridge: Cambridge University Press.

Restoring African Wild Dogs
in South Africa: A Managed
Metapopulation Approach
Summary

Introduction

Over the past 15 years, the numberof endangered African wild dogs
(Lycaon pictus) in South Africa has
increased by nearly 50% throughthe active reintroduction of animals
into suitable state-protected areasand private reserves. These new,isolated populations are managed
collectively as a managed metapopulation, linked through artificiallymediated dispersal. Founding stock
for reintroductions has comprised
both wild-caught and captive-bredanimals and this has unearthed some
useful lessons about the in situ-ex situ
interface. Chief among these is theneed for an a priori strategy for ex situ
support of the programme, essential
to avoid uncoordinated and ad hoc
use of captive-bred animals, and toensure the long-term demographic
and genetic viability of this nationally
important wild dog population.

The managed metapopulation approach to African wild dog (Lycaon
pictus) conservation in South Africa is
an innovative restoration programme
to increase the population size anddistribution range of this endangered
canid (Fig.1). The programme makes
use of South Africa’s unusual conservation landscape – unique among
African nations for its preponderanceof private fenced reserves. The approach was formulated in 1998 on theback of recommendations emanatingfrom a Population and Habitat Viability Assessment (PHVA) workshop,
facilitated by the IUCN SSC Conservation Breeding Specialist Group, whichemphasised the importance of establishing a second viable population ofwild dogs in South Africa, in addition
to the only large contiguous population occurring in Kruger National Park
(Mills et al. 1998).

1

Endangered Wildlife Trust,
Johannesburg, South Africa
2 Wildlife Conservation Research Unit,
Department of Zoology, Universityof Oxford, Oxford, UK
3 World Association of Zoos andAquariums, Gland, Switzerland* E-mail for correspondence:
harrietd@ewt.org.za»

The absence of suitably large areas tosupport another viable population led
to the decision to establish a networkof small populations in private andstate-owned fenced reserves acrossthe country. These populations, although not viable individually, would
be connected through artificiallymediated dispersal, with the goalof establishing at least nine packs
in 10 years. The Wild Dog Advisory
Group South Africa – a network ofconservation authorities, managers,
researchers and other stakeholders – was set up to achieve this goalby identifying metapopulation sites,
coordinating reintroductions andguiding subsequent population interventions.

Fig. 1African wild dogs.
© Rob Till

42 African Wild Dog

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African Wild Dog

43

»

»

Fig. 2 Map of South Africa showing the reserves participating in the managed wild dog metapopulation,
1998–2012 (grey legend entries indicate reserves that have withdrawn from the programme).

Wild dogs are highly social canids,
living in packs of two to 30 adults thatconsist of a dominant breeding pairand their young and non-breeding
helpers. Litters are typically produced annually and until the pups area year old, they depend on older packmembers to provide them with meatfrom kills. Hunting is cooperative,
and this allows capture of larger preythan would be possible by individuals
hunting alone. New packs form whensingle-sex dispersing groups (of eithersex) leave their natal packs and meetup with unrelated dispersing groupsof the opposite sex. This process of
new pack formation, and the wild
dogs’ inherent sociality, have bothcontributed to the ease in which new
packs for reintroduction and population augmentation are artificiallycreated.

The Use of
Captive-bred Animals in
Wild Dog Conservation
Management
Between 1998 and 2012, the number of reserves participating in the
managed metapopulation fluctuatedbetween two and nine (Fig. 2). Total
wild dog numbers peaked at morethan 230 individuals in 2005, and havemaintained above 150 individuals in
more than 12 breeding packs since
September 2009.
Although reintroduction may not be
a high priority in the wild dog conservation toolbox, wild dog reintroductions had taken place throughout
the region long before the formal
adoption of the managed metapopulation approach in South Africa. These
included sites in South Africa, Namibia, Zimbabwe and Kenya. These
early interventions were not part ofa coordinated programme, and manyof them failed for biological and/or
non-biological reasons. The former
included lack of social integration
within artificially assembled packs
leading to pack dissolution or fission
following release, as well as the useof captive-bred animals that lacked
the social and hunting behaviours
necessary for survival in the wild
(Gusset et al. 2006). The latter included anthropogenic mortality asa result of inadequate sensitisation
to the process among neighbouringcommunities.

Partly as a result of these early
failures, it was initially intended
that wild-caught founding stock for
managed metapopulation reintroductions would be obtained from thefree-ranging population in Kruger
National Park. However, as time wentby, it became apparent that there
were other, more readily accessible
sources of founding animals, and that
it was not necessary to risk the potential impacts on the source populationof wild dogs in Kruger National Park
(Davies-Mostert et al. 2009). Only
two of the 96 founding individuals(2%) were sourced from Kruger National Park; the remainder comprised
wild-caught animals relocated from
unprotected areas following conflictwith game and livestock farmers(49%), captive-bred animals fromfacilities in South Africa and Botswana (24%), and pups from littersborn in holding enclosures while theirparents were awaiting translocation
and/or release (25%).

Lessons Learned
About the In Situ–Ex Situ
InterfaceIn the 15 years since initiation of the
managed metapopulation approach,captive-bred animals have madea more significant contribution than
was first anticipated, and some key
lessons have emerged about the
integration of in situ and ex situ management (Gusset et al. 2008). These
relate to the relevance of a strategic
direction for the in situ–ex situ interface, the variety of technical skills
acquired for intensive in situ management, the identification and uptakeof cross-cutting population management tools, and the potential longterm contribution of captive facilities
to metapopulation persistence.

A Significant Contribution in the Absence of Strategy. Although captivebred animals comprised almost
a quarter of all founder animals in
the managed metapopulation, thiswas largely by chance rather thandue to a particular ex situ breeding
and release strategy. There has neverbeen a coordinated breeding planfor ex situ wild dogs intended forrelease; partly because the frequency
of augmentation of ex situ animals
was relatively low (and has become
lower) and because there was anunderstanding that sourcing wildcaught animals from subpopulation
reserves was preferable. However,there were a number of occasions
when suitable wild-caught individuals were not available to resolve
demographic issues within subpopulations, and in these instances there
were always facilities that could be
relied upon to provide animals, freeof charge. So was a strategy necessary? Given the need to ensure both
demographic and genetic viability
in the long term, and the increasing
complexity as the number of individuals and subpopulations has grown,
there is an argument to be made forformally incorporating ex situ facilities to ensure a supply of geneticallysuitable founders in the future.
Building Technical Competencies. In
order to achieve the goal of establishing and maintaining at least nine wild
dog packs outside of Kruger Nationalpark, wild dog populations have been
re-established or augmented on atleast 33 occasions. These experiences have provided a fruitful testing
ground for fine-tuning our technicalcapacity to mimic wild dog dispersal
and new pack formation, and someclear lessons have emerged (Gusset
et al. 2006). Chief among these is theimportance of strong social cohesion among members of artificiallyformed packs, now widely recognised as a principle driver of packpersistence. Wild dogs are obligatesocial animals, with hunting and pup
provisioning (including guarding)highly dependent on pack members
working closely as a team. Bonds canbe tested and strengthened during
a holding period, in which new packmates are kept together in an enclosure for several weeks or months
prior to release. This has been a boon
for the recovery programme: bybonding captive-bred individuals withfew life skills to hunting- and predator-savvy wild-caught animals, theprogramme has been able to bolster
the number of animals available forrelease. There are many examples
of how captive-bred animals havelearned the requisite skills for survival
from their wild-caught pack mates.
Ex Situ Tools for Better In Situ Management. In many ways, the managed
metapopulation closely parallels
a managed captive population: animals are moved among subpopulations based on demographic andgenetic criteria and translocations are
conducted to optimise these (Gusset
et al. 2009). The only major differenceis that the adaptive forces of selection (including predation, disease andmate choice) operate more influentially on the one than the other. There
are a number of ex situ population
management tools that are widelyused in the management of animalcollection across the world; however,these tools were not identified or
adopted from the initiation of the
programme. In the first few years, thepopulation size was small enough andmonitored closely enough to keep
track of individuals, and translocation
decisions were based on informal expert judgements about relationships
between individuals and populations.

44 African Wild Dog

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References
However, as the metapopulation
grew in size (individuals, packs
and subpopulations), and there
was turnover among management
personnel, it became more challenging to implement this “seat of thepants” methodology. A key lesson
from this is the importance of formal
population management tools toimprove population management
efficiency, and reduce the possibilityof poor judgements due to lack ofrobust data on population structure.
Recent genetic studies suggest thatthe “seat of the pants” approach has
been adequate to maintain levels ofgene diversity higher than those in
the free-ranging population in Kruger
National Park, which means it is not
too late to implement tools for future
management.
The Real Role of Captive Facilities.
Many captive breeding facilities inSouth Africa justify their existencewith claims that they are breeding
animals for release into the wild. Thisis sometimes a smoke-screen for generating entrance fees and even donations from misinformed members of
the public. This is illustrated by thefact that the number of wild dogs in
captivity in South Africa is unknown:even properly registered facilities
have a poor record of submitting
population records to studbooks, andunregistered facilities are a complete
black hole. While one or two facilities
have made a meaningful contribution to in situ conservation efforts
through the provision of wild dogs
when necessary (see above), captive
breeding is not the panacea for wild
dog conservation that so many claim
it to be. Rather, facilities have an important advocacy and awareness roleto play in educating members of the
public about the real threats facing
wild dogs and other large carnivores(primarily habitat loss and fragmentation, and direct persecution). It isa role that should be emphasised.

The Way Forward
for Metapopulation
Management ofLarge Carnivores
South Africa has a chequered past interms of large carnivore conservation:
there exist huge expanses of land
where cheetahs (Acinonyx jubatus)
and wild dogs have been completely
extirpated, and lion (Panthera leo)
populations only occur in a handfulof fenced protected areas. However,this unfortunate situation has givenrise (out of necessity) to the development of innovative restoration
programmes that have recovered
extirpated range for large carnivores
through reintroductions into fenced
reserves throughout the country. The
motivation for these reintroductions
differs widely among species: cheetahs and lions have typically been
reintroduced to generate income
from ecotourism, whereas the wild
dog programme met a strategic
conservation need. However, many ofthe lessons learned are transferrable
across species (Gusset 2009), and thisis true for the integration of in situ
and ex situ approaches for large carnivore management. Unfortunately,
the uptake of these lessons is likely
to become more urgent as humanpopulation growth and associatedpressures on natural resources put
the squeeze on large carnivore populations (particularly wide-ranging species) across the globe, and intensive
management becomes increasingly
inevitable.

Acknowledgements
We acknowledge members of theWild Dog Advisory Group South
Africa for their ongoing participationin the managed metapopulation programme for wild dogs. Special thanks
to Brendan Whittington-Jones for
useful discussions on this subject.

•

•

•

•

•

•

Davies-Mostert, H. T., Mills,
M. G. L. & Macdonald, D. W.
(2009) A critical assessment ofSouth Africa’s managed metapopulation recovery strategy for
African wild dogs. In: Reintroduction of Top-order Predators(ed. by Hayward, M. W. & Somers, M. J.), pp. 10–42. Oxford:
Wiley-Blackwell.
Gusset, M. (2009) A framework
for evaluating reintroduction
success in carnivores: lessons
from African wild dogs. In: Reintroduction of Top-order Predators (ed. by Hayward, M. W. &Somers, M. J.), pp. 307–320.
Oxford: Wiley-Blackwell.
Gusset, M., Slotow, R. & Somers, M. J. (2006) Divided we
fail: the importance of social
integration for the re-introduction of endangered African wild
dogs (Lycaon pictus). Journal of
Zoology, London 270: 502–511.
Gusset, M., Ryan, S. J., Hofmeyr,M., van Dyk, G., Davies-Mostert, H. T., Graf, J. A., Owen,
C., Szykman, M., Macdonald,
D. W., Monfort, S. L., Wildt,
D. E., Maddock, A. H., Mills,
M. G. L., Slotow, R. & Somers,
M. J. (2008) Efforts going to thedogs? Evaluating attempts tore-introduce endangered wild
dogs in South Africa. Journal ofApplied Ecology 45: 100–108.
Gusset, M., Jakoby, O., Müller,
M. S., Somers, M. J., Slotow, R.
& Grimm, V. (2009) Dogs on
the catwalk: modelling re-introduction and translocation ofendangered wild dogs in South
Africa. Biological Conservation
142: 2774–2781.
Mills, M. G. L., Ellis, S., Woodroffe, R., Maddock, A., Stander,P., Rasmussen, G., Pole, A.,
Fletcher, P., Bruford, M., Wildt,
D., Macdonald, D. & Seal, U.
(eds) (1998) Population and
Habitat Viability Assessment for
the African Wild Dog (Lycaon
pictus) in Southern Africa. Finalworkshop report. Apple Valley,
MN: IUCN SSC Conservation
Breeding Specialist Group.

© Nicole Gusset-Burgener
Southern yellow-billed hornbill (Tockus leucomelas) in the Okavango Delta.

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ISSN: 2074-4528