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The survival of captive-born animals in restoration programmes – Case studyof the endangered European mink
Mustela lutreola
Tiit Maran
a,b,
*
, Madis Põdra
b
, Merje Põlma
a
, David W. Macdonald
c
a
Species Conservation Lab, Tallinn Zoological Gardens, Paldiski Road 145, 13522 Tallinn, Estonia
b
Institute of Mathematics and Natural Sciences, Tallinn University, Narva Road 25, Tallinn 10120, Estonia
c
Wildlife Conservation Research Unit, Department of Zoology, University of Oxford, Tubney House, Abingdon Road, Tubney, Oxon OX13 5QL, UK 
a r t i c l e i n f o
 Article history:
Received 22 May 2008Received in revised form 17 February 2009Accepted 3 March 2009Available online 5 April 2009
Keywords:
Survival analysisEstoniaRe-introductionFailure time analysesKaplan–Meier estimatesCox proportional regression
a b s t r a c t
As part of a conservation initiative, captive-bred individuals of the endangered European mink
Mustelalutreola
werereleasedtoaBalticisland‘sanctuary’,HiiumaaIsland(Estonia), andtheirsurvival wasmon-itoredovereightyears. Altogether,54releasedminkwereequippedwithradio-collarsbetween2000and2003 and their survival and causes of death were studied as a function of sex, age, housing conditionsbefore release and number of generations in captivity. Mortality was greatest (
$
50%) during 1–1.5monthsfollowingrelease.Thesurvivalofmaleswassignificantlyhigherthanthatoffemales(25%declinein 21 days, and 10 days, for males and females, respectively). Releasing pregnant females appeared to bean unsuccessful strategy. There was no evidence that the number of generations for which the lineage of the released individuals had been bred in captivity had any effect on survival. The main cause of deathwas other carnivores and raptors, although this broad categorization may conceal a diversity of fatal sce-narios.WerecommendforthefuturethattheEuropeanminkbeingpreparedforreleaseshouldbemaintainedin large naturalistic enclosures beforehand, that a preponderance of females should be released, and thatthe indications that younger animals make better candidates for release should be investigated.
Ó
2009 Elsevier Ltd. All rights reserved.
1. Introduction
Restoration is a major element of practical conservation, andthe release of captive-born individuals into the wild can be animportant component of it. Indeed, re-introduction biology is animportant emergent field (Seddon,1999; Seddon et al., 2007) andthere is a growing number of reviews of release methodologiesand their effectiveness (e.g.Breitenmoser et al., 2001; Griffith etal., 1989; Reading and Clark, 1996; Seddon et al., 2005).In a classic review byGriffith et al. (1989), 700 release opera-tions conducted in 1973–1986 were considered with respect tosuch variables as the number of founders, availability of shelters,origin of founders (captive versus wild animals), taxonomic originof the animals, repeated releases versus a single operation.Juleet al. (2008)recently showed that the use of wild animals in carni-vore restoration is, in general, significantly more successful thanthe use of captive-bred animals. Further, analysing the releases of carnivores,Reading and Clark (1996)concluded that too often thefocus is on biological variables, while sociological and organiza-tional variables are unwisely neglected (see alsoMacdonald et al.2002a,b).However,Breitenmoser et al. (2001)express doubts as to thevalidity of such generalisations as they are often based on incom-plete information, andSeddon (1999)emphasises difficulties andinconsistencies in defining re-introduction success. Despite thesecaveats, the survival of the released animals is surely a fundamen-tal benchmark of success, and evidence as to the factors associatedwith their fates will contribute usefully to the adaptive manage-ment of future releases.The factors potentially influencing the survival of released ani-mals can be divided into four classes: (a) biological variables, e.g.age and sex; (b) pre-release factors, e.g. maintenance conditions,pre-conditioning, experience with humans; (c) release methodol-ogy, e.g. along a continuumbetween hard and soft releases; (d) re-lease site characteristics, e.g. availability of suitable shelter andhabitat, abundance of predators, availability of food resourcesand level of disturbance. These categories may interact with oneanother in their influence on survival.Systematic studies of the post-release survival of captive-born mammals, and especially Carnivores, are few. The effect of 
0006-3207/$ - see front matter
Ó
2009 Elsevier Ltd. All rights reserved.doi:10.1016/j.biocon.2009.03.003
*
Corresponding author. Address: Species Conservation Lab, Tallinn ZoologicalGardens, Paldiski Road 145, 13522 Tallinn, Estonia. Tel.: +372 6943318; fax: +3726578990.
E-mail addresses:
tiit.maran@tallinnlv.ee(T. Maran),madis.podra@yahoo.es(M. Põdra),merje.polma@tallinnlv.ee(M. Põlma),david.macdonald@zoo.ox.ac.uk (D.W. Macdonald).Biological Conservation 142 (2009) 1685–1692
Contents lists available atScienceDirect
Biological Conservation
journal homepage:www.elsevier.com/locate/biocon
 
pre-release training and housing has been studied on Black-footedferret
Mustela nigripes
(Biggins et al., 1998a, 1999; Vargas et al.,1998).Swedishstudieshaveshownthattranslocatedwild-bornot-ters
Lutra lutra
havehigher survival thandore-introducedcaptive-born otters (Sjoasen 1996, 1997).Hellstedt and Kallio (2005)dem- onstrated experimentally that the survival of released weasels
Mustela nivalis
improved when young animals were released dur-ing the periods of high food abundance, whileBremner-Harrisonet al. (2004)report that important predictors of the survival of re-leasedswiftfoxes
Vulpes velox
aretheextentoftheirhabituationtocaptivity and measures of their ‘boldness’.European mink is a slender, small, dark-colored, semi-aquaticmustelid that once inhabited streams and rivers throughout Eur-ope. It inhabits riparian zones along small rivers and streams inforested landscapes and seldom moves further than 100m fromriverbank(Danilov and Tumanov, 1976). Todaythe Europeanminkis globally endangered, and critically endangered within the Euro-pean Union (Temple and Terry, 2007). Principal threats to its sur-vival are habitat loss, over-exploitation and the impact of thealien American mink
Neovison vison
(Maran and Henttonen,1995; Maran et al., 1998; Sidorovich, 2001; Sidorovich and Mac-Donald, 2001). There are no data on the survival of captive-bredEuropeanminkinthewild.In2000,aspartofaprogrammetocon-serve the European mink, we initiated an experimental release of captive-bred individuals into an island sanctuary, Hiiumaa in theBaltic Sea (Macdonaldet al., 2002c; Maran, 2006). This experimentallowed us to test the impact of biological and pre-release factorson the survival of released individuals.Our wider approach to European mink conservation, and thebackground to the Hiiumaa experiment, is given inMacdonaldet al. (2002c)and inMaran(2003, 2006). In summary, since 2000, European mink bred at a special conservation breeding facility atTallinn Zoological Gardens (Estonia) have been released to the is-land of Hiiumaa. The research aim of these releases has been tostudy the factors relevant to establishing island populations of the Europeanmink as a means of safeguarding themfromthe neg-ative impacts of the invasive American mink (Sidorovich et al.,1999).The experiment contrasted the survival outcomes of alternativereleaseprocesses,intermsofanimalselection,theirpre-condition-ing, while the release methodology and release site selection fol-lowed identical protocols. The release procedure is detailed inMaran (2006). For each released individual we noted the age, sex,number of generations in captivity, housing conditions before re-lease and pregnancy of released females. Radio-tracking data re-vealed the causes of mortality and facilitated the retrospectiveanalysis of survival, the effect of the dependent variables on sur-vival and the dependence of survival on these variables.Our study aims to answer the following questions:1. What is the survival rate of released mink and how does itchange with time since release?2. Do age, sex of an individual, and the conditions in which it iskept prior to release, affect its subsequent survival in the wild?3. What are causes of mortality?
2. Methods
 2.1. Study area
Hiiumaa Island, with an area of 1019km
2
and a coastline of 326km,islocatedintheBalticSeaintheAtlanticcontinentalregionoftheTemperateZone(Fig.1).Theclimateischaracterizedbymildwinters (average temperature
À
3.5–
À
4.5
°
C) and warm summers(+16.5–+17
°
C). The annual precipitation ranged in 1961–2002 be-tween 400 and 825 (average 625) mm (Põdra and Maran, 2003).Theshortest distanceto themainlandis22kmandtootherlar-ger islands (Vormsi and Saaremaa) – 9km and 5km, respectively.As of 2001, the island had a human population of 11335 (11.1inhabitants/km
2
), dispersed between three small towns and 182villages (www.hiiumaa.ee; as of 15.02.2009).
Fig. 1.
Location of Hiiumaa Island.1686
T. Maran et al./Biological Conservation 142 (2009) 1685–1692
 
Forestcoversaround70%oftheisland,andmorethan22naturereserves encompass over 20% of the land area (www.eelis.ee; as of 15.02.2009).
 2.1.1. Fauna
In addition to the European mink, the mammal fauna of the is-landincludeseightcarnivorespecies–weasel
M. nivalis
,stoat
Mus-tela erminea
, pine marten
Martes martes
, otter
L. lutra
, raccoon dog
Nyctereutes procyonoides
, red fox
Vulpes vulpes
, lynx
Felis lynx
andwolf 
Canis lupus
. There are records of earlier occurrence of polecat
Mustela putorius
and American mink
Neovison vison
in the islandbut the American mink was eradicated in 1998–2000 (Macdonaldet al., 2002c). Other semi-aquatic mammals include beaver
Castor  fiber 
, northern water vole
Arvicola terrestris
and water shrew
Neo-mys fodiens
. At least eight species of small rodents have been re-corded in Hiiumaa (Põdra and Maran, 2003).The possible competitors and predators of the European minkamong the local raptors are white-tailed eagle
Haliaetus albicilla
,golden eagle
Aquila chrysaetos
, eagle owl
Bubo bubo
, Ural owl
Strixuralensis
,commonbuzzard
Buteo buteo
,northerngoshawk
 Accipiter  gentilis
, northern harrier
Circus cyaneus
, Montagu’s harrier
Circus pygargus
and marsh harrier
Circus aeruginosus
(Põdra and Maran,2003).Amphibians are represented by five species. Common frog
Ranatemporaria
, moor frog
Rana arvalis
and common toad
Bufo bufo
arecommon. Natterjack toad
Bufo calamita
and commonnewt
Triturusvulgaris
are rare. Reptiles are represented by common viper
Viperaberus
, grass snake
Natrix natrix
, slowworm
 Anguis fragilis
andcom-mon lizard
Lacerta vivipara
(Põdra and Maran, 2003).The following fish species have been recorded in the inlandwater bodies of Hiiumaa:
Esox lucius, Perca fluviatilis, Gymnocepha-lus cernus, Salmo trutta, Lota lota, Anguilla anguilla, Gasterosteusaculeatus, Pungitiuspungitius, Rutilusrutilus, Leuciscusleuciscus, Leu-ciscus idus, Leucaspius delineatus, Carassius carassius, Tinca tinca,Lamperta fluviatilis.
Populations of crayfish
Astacus astacus
exist infour water courses (Põdra and Maran, 2003).
 2.1.2. Inland water bodies
There are 40 bigger streams or rivers (with the total length of 326km) in the island and
$
100km of bigger drainage ditchesand 13 lakes with the total length of shoreline of 
$
25km (Põdraand Maran, 2003).
 2.2. Origin of released animals
The released animals were bornin captivity at the conservationbreeding facility of Tallinn Zoological Gardens, which is coordi-nated by the European mink EEP programme (European Endan-gered Species Program under the European Association of Zoosand Aquaria,www.eaza.net). The captive management followstheEuropeanminkEEPcaptivebreedingandhusbandryguidelines(unpublished document: accepted by, and lodged with, EuropeanminkEEPanimal committeein2005). Thefoundersof theEEPcap-tive population originate from Tver, Vologda, Pskov, Novgorod andLeningrad Regions of Russia. These regions are considered to beinhabited by one subspecies –
M. lutreola novikovi
(Heptner et al.,1967) though the validity of subspecies for
M. lutreola
has beenquestioned (Michaux et al., 2005; Youngman, 1982).
 2.3. Methodology of release
Before release, the animals were provided an opportunity tocatch the prey they were likely to encounter on the island, andtheir contact with humans (keepers) was reduced to a minimum(human presence was restricted to unavoidable husbandry). Fur-ther, the animals were checked for their ability to swim and, asnecessary, ‘coached’ through encouraging the use of artificialponds (seeMacdonald et al., 2002cfor details). Releases followeda hard release protocol – transportation from the breeding facilityto the release area, where individuals were set free in the mostsuitable habitats – that is riverbanks of small rivers or canalswith lush riparian vegetation and abundant prey. Transport wasover a distance of 
c 
. 150km and lasted some four to five hours,including a 1.5-h ferry trip. The majority of the radio-tracked re-leased individuals travelled widely, the survivors settling inestablished home ranges after 1–2 months (Macdonald et al.,2002c).
 2.4. Radio-tracking 
Fifty-four out of the 172 released mink were equipped withradio-collars (Biotrack, UK;Table 1). In open terrain the signalswere detectable at
$
1km, and in woodland at
$
600m. The life-span of transmitters was around six month and their weight(14g)constituted
$
2%ofmaleand
$
3%offemaleweight.Thesam-ple size was reduced due to some transmitter failures and, as iscommonplace in radio-tracking studies of mustelines, becausethe thick neck and narrow head of the mink resulted in occasionalloss of radio-collars (Table 2).ThereceiversusedwereTR-4(Telonics;USA)andR-1000(Com-munication Specialist; USA).After the release, the animals’ locations were recorded 1–3times a day during the first week, every day during the next 20days, every two days during the second and third month, and oncea week thereafter. The status of the free-living mink was regularlymonitored by spring and autumn live-trapping (Table 2).
 2.5. Survival analyses
Live-trapping records revealed that a proportion of the releasedanimals survived for up to 39 months. However, for the sake of consistency, we included only radio-tracked individuals in theseanalyses,butexcludedeightjuvenilesreleasedexceptionallyinau-tumn(Table 2). Failuretimeanalyseswereusedtostudythesurvivalofanimalsafter release and the effect of co-variables on their survival. Theanimals were divided into groups by variable values (age class,sex, enclosure of origin, number of generations in captivity, year
 Table 1
Number of released European mink in 2000–2003.
Year Number of releases With radio-collarsMales Females Total released In summer In autumnNon-pregnant Pregnant2000 8 9 0
17
9 8 172001 19 22 0
41
41 0 232002 23 19 12
54
39 15 122003 32 14 14
60
42 18 2Total 82 64 26 172 131 41 54
T. Maran et al./Biological Conservation 142 (2009) 1685–1692
1687
of 00

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