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RESEARCH ARTICLE
The Causes of the Low Breeding Success of
European Mink (Mustela lutreola) in Captivity
Kairi Kiik,
1
* Tiit Maran,
2,3
Astrid Nagl,
4
Kadri Ashford,
2
and Toomas Tammaru
1
1
Department of Zoology, Institute of Ecology and Earth Sciences, University of Tartu, Tartu, Estonia
2
Species Conservation Lab, Tallinn Zoological Gardens, Tallinn, Estonia
3
Institute of Mathematics and Natural Sciences, Tallinn University, Tallinn, Estonia
4
Department of Biomedical Sciences and Biochemistry, University of Veterinary Medicine, Vienna, Austria
High among‐individual variation in mating success often causes problems in conservation breeding programs. This is also the
case for critically endangered European mink and may jeopardize the long‐term maintenance of the species’genetic diversity
under the European mink EEP Program. In this study, breeding success of wild and captive born European minks at Tallinn
Zoological Garden are compared, and the mating behavior of the males is analyzed. Results show that wild born males
successfully mate significantly more often than captive born males (89% and 35%, respectively). On the basis of an extensive
record of mating attempts, both male aggressiveness and passivity are identified as primary causes of the observed mating
failures. All other potential determinants have only a minor role. Mating success as well as a male’s aggressiveness and
passivity are shown to depend more strongly on the male than the female partner. We did not find any evidence that the behavior
of an individual is dependent on the identity of its partner. We suggest that aggressiveness and passivity are two expressions of
abnormal behavior brought about by growing up in captivity: the same individuals are likely to display both aggressive and
passive behavior. The results point to the need to study and modify maintenance conditions and management procedures of
mink to reduce the negative impact of the captive environment on the long‐term goals of the program. Zoo Biol. XX:XX–XX,
2013. © 2013 Wiley Periodicals Inc.
Keywords: ex situ; conservation; behavior; aggression; mustelids
INTRODUCTION
A biodiversity crisis is underway. According to recent
reports, approximately 21% of extant mammal species are
classified as threatened [IUCN, 2012; www.iucnredlist.org].
Despite this gloomy picture, recent analyses show that
conservation efforts can and do make a difference. According
to Hoffmann’s [2010] calculation, in situ conservation
efforts have played a role in the case of 7% of species (68
of 928; for birds 1988–2008, mammals 1996–2008, and
amphibians 1980–2004) whose threat level has been recently
reduced [Hoffmann et al., 2010]. Sometimes efforts in situ
alone are not sufficient to secure the survival of an
endangered species [Witzenberger and Hochkirch, 2011].
Here, ex situ conservation breeding can play an important
role and has proven to be effective [Seddon, 2010; Conde
et al., 2011]. A number of cases exemplify the role
conservation breeding can have in securing the survival of
species [Pereladova et al., 1999; Alcaide et al., 2010; Biggins
et al., 2011; Lindsey et al., 2011; Zafar‐Ul et al., 2011].
Managed captive populations act also as survival insurance
for endangered species. Even after ultimate extinction in the
wild, properly managed ex situ populations provide an
opportunity to restore wild populations to existing empty
habitats [Conde et al., 2011].
A prerequisite of success in conservation breeding is
that all the animals of reproductive age can be used for
breeding when needed [Price, 1999]. However, this is not
always the case. Captive breeding programs are often plagued
by a mortality rate that is too high or irregular breeding
[Wolf et al., 2000; Dalerum et al., 2006; Hawkins and
Battaglia, 2009; Peng et al., 2009], supposedly resulting from
*Correspondence to: Kairi Kiik, Institute of Ecology and Earth Sciences, University
of Tartu, Vanemuise 46, 51014 Tartu, Estonia. E‐mail: svetsjeb@ut.ee
Received 25 August 2012; Revised 15 November 2012; Accepted 04 January
2013
DOI 10.1002/zoo.21062
Published onlinexx xx xxxx in WileyOnline Library (wileyonlinelibrary.com).
© 2013 Wiley Periodicals, Inc.
Zoo Biology 999 : 1–7 (2013)
insufficient knowledge of species‐specific behavioral and
physiological requirements, or insufficient attention to such
requirements [Zeoli et al., 2008]. Several studies have
reported that abnormal mating behavior such as aggressive/
passive behavior toward potential mating partner is to be
blamed for poor breeding success [Wolf et al., 2000; Zhang
et al., 2004; MacKinnon et al., 2008]. Such abnormal
behavior has been reported to be caused by too small and/or
too homogeneous furnishing of the enclosure, presence of
natural enemies or humans, or social stress caused by the
physical presence of too many conspecifics [Price, 1999;
Peng et al., 2007].
The European mink (Mustela lutreola) is a critically
endangered species according to the IUCN Redlist 2012
[IUCN, 2012; www.iucnredlist.org] assessment and one of
the most endangered mammals in Europe [Temple and
Terry, 2007]. Indeed, the species has disappeared from most
parts of its former range. The main factors contributing to this
extinction are habitat loss, over‐hunting, and the invasion of a
dominant competitor, the American mink [Maran and
Henttonen, 1995; Maran, 2003, 2007; Maran et al., 2004].
In 1992, the European Endangered Species Program
(EEP) for the European mink was launched by the European
Association of Zoos and Aquaria (EAZA). The aim of this
program is to maintain—in European zoos and other breeding
facilities—85% of the original heterozygosity of the founding
individuals for 50 years. Currently, there are 218 mink in
captivity under the EEP program. Nearly half of the captive
populationof European Mink is heldat TallinnZoo,Estonia,the
population is based on 22 founders. Currently (as of
December 31, 2011) the size of the population is n¼110
individuals, genetic diversity (GD) retained is 93%, generation
time1.62yearsandeffectivepopulationsize65.6individuals.In
additionto the preservationof the geneticdiversityofthespecies
in captivity,the EEP Programalso serves as a source for a mink
reintroductionprojectsin Estonia(on the islandsof Hiiumaaand
Saaremaa) as well as in Germany [Maran et al., 2009].
In the framework of the European minkEEP program, all
known breeding events in the captive population have been
recorded. Furthermore, since 2004, thebehavior of mink during
mating attempts has been recorded at Tallinn Zoological
Garden. These two sets of data provide us a unique opportunity
to look into the effect of mating behavior on the breeding
success in captivity. In this manner, we are forming an initial
insight into the role of abnormal mating behavior in breeding
failures of the European mink. In particular, our study aims to
answer the following question: Which traits of the male and the
female (such as origin, sex and partner identity, as well as age,
number of mating attempts in 1 year) are the main determinants
of mating success?
MATERIALS/METHODS
Captive Population and Its Management
At Tallinn Zoo, all animals are housed individually in
20‐animal “modules,”aligned in two rows with 10 enclosures
(2 m 2m4 m) in each. The rows are separated by a
service corridor. The enclosures are separated from each
other by double welded, wire mesh walls. Lower parts of the
wall are covered by plywood to reduce visual contact between
the animals. The enclosures are cleaned and the animals are
fed daily.
The Effect of Origin on Breeding Success
The effect of mink origin (wild or captive) on breeding
success was analyzed on the basis of the pedigree data being
accumulated in the SPARKS database (www.isis.org). From
the 1980s until 2003, the main goal of the program had been
to increase the size of the captive population and therefore
every animal was involved in the breeding program.
Therefore we assumed that any animal which left no
offspring was an unsuccessful breeder. Breeding records
and the data about the origin of bred mink until 2003 (both
wild and captive born) were used in the analyses.
Mating Trials
A detailed analysis of the determinants of mating
success could be conducted on the basis of breeding logs
which had been kept at the Tallinn Zoological Garden since
2004. By that time, all animals were captive born. From 2004
to 2010, all mating attempts were kept track of and classified
as successful or not. Mating attempt was classified successful
if copulation was observed. Also, cases of aggressive or
passive behavior were recorded. Aggressive behavior was
defined following to Poole [1966], that is, a study on the
related European polecat. A male was considered passive if
he did not show any interest towards the female (started to
forage, explored the area, receded into nestbox and stayed
there). Additionally, the logs contained basic information
(such as age) concerning every individual involved.
A mating trial was initiated when a female reached
oestrus, and a designated male partner was placed in her cage.
The selection of male partners was based on the analyses
conducted with the PM2000 software [Pollak et al., 2002]. An
observer monitored the couple until copulation occurred.
Subsequently, the animals were left to stay together for a few
days. The trials with no copulation lasted one hour after
which the animals were separated. In the cases of aggression,
the trials were terminated and the animals were immediately
separated to avoid injuries to the female. In such trials, the
male was scored as having behaved aggressively in the
particular mating attempt. If the attack was not very serious
and thus the female was not particularly disturbed, the trial
was continued for the predetermined time (1 hr), but the male
was still scored as having behaved aggressively. The animals
were also separated after an hour of observation if the male
was acting passively, that is, if the male did not pay any
attention to the female. In these cases, the male was scored as
passive for that breeding attempt.
To find out the effect of aggressive or passive behavior
of the male on mating success, the latter (as a binary variable:
2Kiik et al.
Zoo Biology
copulation observed or not) was analyzed as dependent on
“aggression index”or “passivity index”of the male (see
Table 1 for definitions of variables). In the analyses, each
mating attempt was treated as one observation. Several
additional independent variables were included in the model
(Table 1). For example, it is reasonable to assume that the
previous mating experience of the female (having encoun-
tered an aggressive/passive male earlier or not) can affect the
outcome of an on‐going mating attempt, assuming that a
female’s behavior has some impact on mating success at all.
In order to check whether aggressive males tend to act
normally or rather passively in those mating attempts in
which aggressive behavior does not occur, the analysis was
repeated on a reduced data matrix. In particular, the trials in
which the male was acting aggressively were excluded. The
relationship between mating success or passive behavior
(both binary variables) and the male’s“aggression index”
was analyzed in a model with the same set of additional
independent variables (Table 1). An analogous analysis was
conducted to study the behavior of passive males during their
non‐passive breeding attempts. That is, the relationship
between mating success or aggressive behavior and the
male’s“passivity index”was studied using the data matrix
with all the passive attempts omitted.
In all analyses with a binary dependent variable
(successful/unsuccessful; aggressive/nonaggressive, etc.)
mixed generalized linear models were applied. Statistical
analyses were performed with SAS/STAT 9.2 (SAS Institute,
Inc., Cary, NC) software using the procedure glimmix. Male
and female identities were used as random factors. Degrees of
freedom were estimated using the Kenward–Roger method
[Littell et al., 2002] to avoid overestimation—due to repeated
measurements on particular individuals.
RESULTS
The Effect of Origin on Breeding Success
There was a significant (x
2
¼38.3; df ¼1; P<0.001)
association between the origin (wild vs. captive born) of male
European minks: 23 out of 201 captive born males had
successfully bred at least once in their lifetime (11%), while
wild born males respective numbers were 13 out of 20 (65%;
Fig. 1). For females, no such association was found
(x2¼0.02; df ¼1; P¼0.89): 100 out of 229 captive born
females (44%) bred at least once successfully. The
corresponding figures for wild born females were 7 and 15
(53%), respectively (Fig. 2).
Aggressive and Passive Behavior in Mating
Attempt
Our final matrix for 2004–2010 contained data on 579
mating events, 147 (25%) of which were classified as
successful. There were data on mating attempts of 96 males
TABLE 1. Independent variables used in the analyses to explain the variation in mating success
Effect Level of variation Mean SD Min Max
Male
Aggression index
a
i 0.26 0.35 0 1
Passivity index
a
i 0.35 0.38 0 1
Age
b
ma 2.02 1.3 1 9
Attempt
c
ma 2.72 2.04 1 13
Female
Experienced passivity
d
i 0.27 0.27 0 1
Experienced aggressiveness
d
i 0.13 0.19 0 1
Age
b
ma 2.9 1.8 1 9
Attempt
c
ma 2.68 1.86 1 9
Earlier experienced aggressiveness
e
ma 0.4 0 1
Earlier experienced passivity
e
ma 0.6 0 1
Some variables varied at the level of particular mating attempts (ma) while some had values attached to particular individuals(i).
a
Aggression
index (mean aggressiveness) of each particular male was presented as the share of the male’s aggressive attempts from the number of all his
mating attempts in the data base (0, never aggressive; 1, always aggressive). Passivity index (mean male passiveness) was calculated
analogously.
b
The age of the animal at the moment of the mating attempt (years).
c
Order number of the mating attempt. For each male the
numeration starts from one every breeding season and increases by one with every mating attempt. An analogous index for the female was
calculated similarly.
d
Mean female experienced aggressiveness was presented as the share of mating attempts in the data set in which the male
partner had been aggressive. Mean experienced passivity was calculated analogously.
e
Earlier experienced aggressiveness is a binary variable
telling if the female partner has, or has not, previous experience with an aggressive mating attempt. Earlier experienced passivity has an
analogous meaning.
Fig. 1. Wild and captiveborn male European minkswith successful
breedings at least once in their lifetime.
Abnormal Mating Behaviour in European Mink 3
Zoo Biology
and 84 females. Males were recorded to be aggressive on 103
occasions and passive during 203 mating events. Of all failed
mating attempts (432), 24% were judged to have been
unsuccessful because of aggressive behavior of the male
partner, whereas in 47% the cause was passive behavior of the
male, that is, a failure to be interested in the female. Only
four aggressivetrials resulted in successful mating. In total67%
of studied males failed in every mating attempt in their life (64
of 96).
As judged on the basis of estimates of among individual
variance, and respective standard errors, mating success, as
well as the occurrence of both aggressive and passive
behavior, depended remarkably more on the male than the
female participant of the mating event (Table 2). No evidence
was found that the behavior of an individual was dependent
upon the identity of its partner: the female by male interaction
term was estimated to be zero for mating success,
aggressiveness and passiveness in analyses analogous to
those in Table 2.
To study the determinants of mating success (as a
binary variable, one value for each mating attempt),
generalized linear models with 10 independent factors
(Table 1) were fitted first. The model was subsequently
simplified in a stepwise manner so that only statistically
significant effects remained (Table 3). Indeed, both the
passiveness and aggressiveness indices of the male were the
primary determinants of mating success, whereas similar
indices calculated for the female partner had a weaker though
still a statistically significant effect.
However, our analyses described above contained a
certain element of potential logical circularity. Indeed, as
most mating failed because of a male having been either
aggressive or passive, one may argue that a relationship
between mating success and abnormal male behavior might
partly result from the actual definition of successful mating.
To overcome this problem, we re‐scored male aggressiveness
and passiveness as binary variables (e.g., the value one of
aggressiveness was assigned to a male if he had been
observed to behave aggressively at least once). Thereafter, we
omitted these particular mating events which had served as
the basis of such judgment (i.e., mating events in which a
male had first been observed to be aggressive or passive) from
the database, and repeated the analysis (Table 3). The results
were not qualitatively different. Male aggressiveness and
passiveness retained its statistically significant effect on
mating success (Table 4).
Additionally, we tested whether a male which tends to
be aggressive is likely to behave passively on those occasions
it happens not to be aggressive, and vice versa. For this
purpose we created a subset of data with all aggressive
matings excluded, and found that both mating success
(F
1,137.3
¼12.97; P¼0.0004, in an analysis analogous that in
Table 3) and passiveness (F
1,156.4
¼9.03; P¼0.0031) were,
indeed, higher in the more aggressive males. Analogously, in
a data subset with passive mating occasions excluded, the
passiveness score of a male negatively affected mating
success (F
1,79.22
¼28.91; P<0.0001) and positively affected
the probability to behave aggressively (F
1,103.3
¼8.08;
P¼0.005).
DISCUSSION
Mating success appears to be critical in a European
mink captive breeding program. For example, in 2010, only
40% of attempted males copulated with a female and in 2009,
the percentage was 43. This study shows that breeding
success is positively autocorrelated among breeding seasons,
so a high proportion (67%) of males fail to pass their genes on
to succeeding generations (64 of 96 males studied from 2004
to 2010). An inevitable outcome is a reduced genetic diversity
in the population. The evidence accumulated from 1980 to
2003, when the European mink population at Tallinn
Zoological Garden consisted of both captive born and wild
born individuals, shows convincingly that mating failures
were primarily attributable to captive born males. This
suggests that the origin of the animals, rather than immediate
environmental conditions during breeding attempts, is
decisive in the minks’breeding performance. Indeed, in
the related black‐footed ferret (Mustela nigripes), it has been
found that the behavior of the animals changes considerably
between the first and all the following generations in captivity
[Biggins, 2000]. Based on literature and our results, it
appears reasonable to assume that growing up in a captive
Fig. 2. Wild and captive born female European minks with
successful breedings at least once in their lifetime.
TABLE 2. Estimates of the effects of individual males (SE)
and females on the outcome of each mating attempt (a binary
variable: successful or not) as provided by generalized linear
model with male and female identity as random factors
Dependent variable Estimate of variance SE
Mating success Female 0.202 0.207
Male 2.01 0.51
Aggressiveness Female 0 Not estimable
Male 0.75 0.34
Passivity Female 0.056 0.11
Male 1.61 0.41
There were no fixed factors in the model.
4Kiik et al.
Zoo Biology
environment influences behavioral patterns in European
minks and these changes in behavior are the likely reason for
a low breeding success. However, as a number of captive
born mink bred successfully, it is obvious that the origin alone
is not the only determinant of (un)successful mating, but it is
also a function of unknown factor(s) that the mink experience
in captivity.
Detailed behavioral observations conducted from 2004
to 2010 allowed us to identify that, indeed, passivity and
aggression in captive born males were the main reasons for
failure in European mink breeding: (1) 24% of all failed
mating attempts were judged as unsuccessful because of
aggressive behavior in the male partner; (2) 47% of all mating
attempts failed because of the male’s passive behavior (i.e., a
failure to be interested in the female). Aggressive or passive
behavior in the male described far more variation in the
outcome of mating events than did any other explanatory
variables considered (e.g., age, previous experience of the
female—see Table 1). In addition, our results suggest that
passivity and aggression are two alternative expressions of
the same phenomenon: the males’behavioral inability to
mate. The males with a record of aggressive behavior were
also more likely to behave passively in non‐aggressive trials
and vice versa. Similar to our findings, mating failures have
also been identified as the cause of captive breeding problems
in black‐footed ferrets [Wolf et al., 2000]. Indeed, in the case
of black‐footed ferrets, the mating failure is, in addition to
physiological disorders, also attributable to abnormal
behavior. Males are either incapable of taking the proper
mating position or they are aggressive toward females.
Our results show that the outcome of a mating attempt
depends largely on the male partner. The decisive role of male
behavior in determining mating success has also been
reported for southern lesser galagos (Galago moholi;
Lipschitz et al., 2001] and for Giant pandas [Zhang
et al., 2004]. However, some other studies have shown the
opposite—the more important role of female behavior in
defining mating success. For instance, Poole [1966] reports
that the male European polecat (Mustela putorius)is
aggressive towards a female only if the latter rejects her
partner [Poole, 1966]. This does not hold for European mink,
as males have repeatedly been observed to be aggressive
towards female partner which is clearly interested in mating.
Furthermore, our data do not allow us to conclude that the
behavior of a male is altered with different female partners.
One of our hypotheses is that social stress [Blanchard
et al., 2001] is a factor which causes the abnormal behavior of
European mink raised in captivity. Indeed, the European
mink is known to lead a solitary life style in the wild
[Youngman, 1990]. However, in captivity, mink are usually
accommodated in enclosures close to each other so that
olfactory, visual and audio signals of the close presence of
conspecific reach them all the time. This might cause
stress resulting in distorted mating behavior. Such negative
effects of social stress resulting in low mating success
has been reported in captive wolverines, Gulo gulo [Dalerum
et al., 2006], black rhinoceroses, Diceros bicornis [Carlstead
et al., 1999], and various small felids [Mellen, 1991].
Besides creating social stress, the captive conditions
may also influence an animal’s behavior through the effects
of size and environmental diversity of an enclosure. Indeed, it
TABLE 3. Generalized linear model for mating success (as binary variable) in captive European minks
Effect
Full model Reduced model
ddf FPddf FP
Male
Aggression index 81 25.31 <0.0001 92.73 24.68 <0.0001
Passivity index 81.48 63.90 <0.0001 87.35 63.95 <0.0001
Age 207.8 0.06 0.81
Attempt 307.9 10.50 0.001 294.2 10.59 0.001
Female
Experienced aggressiveness 115.8 13.07 0.0004 86.35 15.83 0.0001
Experienced passivity 101.9 10.35 0.002 84.15 9.04 0.004
Age 138.9 3.04 0.08
Attempt 567 1.72 0.19 572 4.74 0.03
Earlier experienced aggressiveness 188.3 0.25 0.62
Earlier experienced passivity 270 1.35 0.25
The left column shows the full model, the right column is the reduced model containing statistically significant effects only. Female and male
identities were included as random factors. See Table 1 for definitions of the variables, and descriptive statistics.
TABLE 4. Generalized linear model for mating success with
male aggressiveness and passivity scored as binary variables
Effect ddf FP
Aggressiveness (1/0) 82.97 9 0.0036
Passivity (1/0) 93.08 32.72 <0.0001
Experienced aggressiveness 453 15.54 <0.0001
Experienced passivity 453 18.47 <0.0001
Attempt (male) 453 8.06 0.0047
Attempt (female) 453 6.06 0.0142
Mating events having served as the basis of classifying males as
aggressive or passive were omitted to avoid logical circularity.
Abnormal Mating Behaviour in European Mink 5
Zoo Biology
has been found that increasing the size and environmental
enrichment of the cage positively affects the breeding success
of giant pandas by raising the proportion of breeding events
with normal mating behavior [Peng et al., 2007].
For European minks, no data are currently available to
study immediate environmental factors associated with
abnormal mating behavior, or those eliciting males’aggres-
sive and passive behavior during breeding attempts.
Nevertheless, a manipulative study is feasible here, as the
sizes of the enclosures and their environmental diversity can
be easily changed (e.g., we may change the enrichment and/or
size of an enclosure and test whether or not there are any
changes with relation to breeding behavior). Knowing that
mating success primarily depends on male behavior and that
the same males are behaving aggressively and passively
allows us to properly identify target variables in such studies.
CONCLUSIONS
1. The negative effect of captive conditions on mating success in
European Mink was much more expressed in captive born
animals than in wild born animals: 89% of all captive born
males failed in breeding in contrast to 35% of wild born
males.
2. Abnormal mating behavior was the strongest predictor of
breeding failure in captivity. Twenty‐four percent of all
recorded failures in mating were associated with aggres-
siveness and 47% with passiveness.
3. Mating success, as well as aggressiveness and passivity, were
all shown to depend much more strongly on the male than on
the female partner.
4. No evidence was found that the behavior of an individual was
dependent on the identity of its partner.
5. Passivity and aggressiveness are suggested to be two
alternative expressions of the males’behavioral inability to
mate. The aggressive males tended to behave passively in
non‐aggressive situations, and vice versa.
ACKNOWLEDGMENTS
We thank Hendrik Proosa for technical support in data
organisation and Bob Shelton for linguistic corrections. The
study was supported by Foundation LUTREOLA, EAZA
Carnivore Campaign, Thoiry Zoological Park, GaiaPark,
Zoological Society for Conservation of Species and
Populations, Estonian Environmental Board and targeted
financing project SF0180122s08 and by the European Union
through the European Regional Development Fund (Center
of Excellence FIBIR).
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