Download C O N S E R V A T I... M U S T E L A L...

CONSER VAT ION, PERSONALIT Y AND ECOLOGY
OF T HE E UROPE AN MINK ( MUSTELA LUTREOLA )
Marianne Haage
1
© Marianne Haage, Stockholm University 2016
ISBN 978-91-7649-420-2
Cover photo by Marianne Haage
Printed in Sweden by Holmbergs, Malmö 2016
Distributor: Department of Zoology, Stockholm University
2
Conservation, personality and
ecology of the European mink
(Mustela lutreola)
Marianne Haage
3
4
To the European mink
5
6
Index
List of papers.............................................................................. 9
Abstract ....................................................................................... 11
Introduction ................................................................................ 13
Study species .......................................................................... 16
Aims ....................................................................................... 17
Methods....................................................................................... 18
Paper I .................................................................................... 18
Paper II ................................................................................... 19
Paper III ................................................................................. 20
Paper IV ................................................................................. 20
Results and discussion.............................................................. 21
Paper I .................................................................................... 21
Paper II ................................................................................... 23
Paper III ................................................................................. 25
Paper IV ................................................................................. 26
General conclusions .................................................................. 30
References .................................................................................. 31
Acknowledgements................................................................... 37
Sammanfattning på svenska .................................................... 39
Papers .......................................................................................... I-IV
7
8
The thesis is based on the following
papers, which are referred to in the
text by their Roman numerals:
I
Haage M, Bergvall UA, Maran T, Kiik K and Angerbjörn A.
2013. Situation and context impacts the expression of personality: The influence of breeding season and test context. Behav
Process 100: 103-109.
II
Haage M, Maran T, Bergvall UA, Elmhagen B and Angerbjörn
A. Evolutionary maintenance of personality – a field experiment on survival and personality. Under revision in Oecologia.
III Haage M, Angerbjörn A Elmhagen B and Maran T. An experimental approach to formation of diet preferences and individual
specialisation in European mink. Submitted to Eur J Wildlife
Res.
IV Haage M, Pasanen-Mortensen M, Sidorovich V, Angerbjörn A,
Elmhagen B. American mink in North-eastern Europe – abundances, population trends and dynamics in relation to the red
fox and otter. Manuscript.
Candidate contributions to thesis papers*
Conceived the study
Designed the study
Collected the data
Analysed the data
Manuscript preparation
I
II
III
IV
Sub.
Sub.
Sub.
Sub.
Sub.
Sub.
Sub.
Sub.
Sub.
Sub.
Sub.
Sub.
Sub.
Sub.
Sub.
Sign.
Sign.
Sub.
Sub.
Sub.
*Contribution Explanation
Min: minor - contributed in some way, but contribution was limited
Sign: significant - provided a significant contribution to the work
Sub: substantial - took the lead role and performed the majority of the work
Reprints were made with the permission of the publisher
9
10
Abstract
Loss of biodiversity is a growing problem and hence conservation of species is becoming
increasingly important. In this dissertation conservation issues related to the critically endangered European mink (Mustela lutreola) are examined in situ (in the wild) and ex situ (in
captivity) on both an individual and community level. It also contains fundamental research as
conservation contexts often allow for conclusions beyond applied biology. Individual behavioural differences, e.g. personality, can impact fitness and are hence relevant for conservation.
Paper I thus experimentally explores the structure, expression and plasticity of personality in
captive European minks. Thereafter paper II investigates if personality affects survival of
reintroduced captive-bred animals and if spatiotemporal conditions affects the relationship
between personality and survival. Paper III experimentally explores individual dietary specialism and learning in relation to novel prey as this could also impact survival. One of the
main threats to the European mink is displacement by the invasive American mink (Neovison
vison) wherefore management of American mink is important for European mink conservation. Paper IV hence analyses survey data to study whether native otters and red foxes can
suppress American mink populations in north-eastern Europe. In the results three personality
trait domains were identified in the European mink: boldness, exploration and sociability. The
domains were repeatable but plastic between the non-breeding and breeding season. Reintroduced personality-tested animals survived longer if they were bolder but the effect of exploration was either positive or negative depending on spatiotemporal conditions. This is not only
interesting for conservation but provides new insights on how individual behavioural differences could be maintained over evolutionary time. Whilst exploration is likely to be maintained by fluctuating selection pressures, the mechanism seem to vary with domain. The
feeding experiments revealed diet choices similar to those found in wild individuals as there
were both generalists and different types of specialists. Still, individuals differed in learning
time towards novel but natural prey, suggesting that reintroduced animals might differ in their
ability to find food after release. This could affect survival also and be related to personality.
Survey data revealed that American mink abundances were suppressed by those of red foxes.
Previous studies show that foxes are suppressed by lynx, and the abundance pattern of mink
in relation to red fox found here indicate the existence of a predator cascade as mink were
most abundant where lynx were abundant and vice versa. In several regions in the study area
population dynamics indicated either exploitation or interference competition as probable
mechanisms whereby foxes suppress minks. However, in many regions there were no relationships between dynamics. This could be due to that exploitation and interference competition might occur simultaneously and thus cancel each other out in the dynamics. Overall this
thesis shows the importance of considering individual traits in conservation efforts, and also
provides knowledge on the structure, plasticity and evolution of personality. As American
mink was suppressed by foxes, management efforts might be most beneficial for species
impacted by the mink if they to a larger extent are undertaken in areas with low fox abundances.
11
12
Introduction
This doctorate thesis has a conservation theme and discusses species conservation on both an individual level and on a large spatial
scale, involving multiple species. It also delves into fundamental
research regarding animal personality as conservation contexts
often allow for conclusions beyond the field of applied biology.
D
uring the history of Earth natural processes have led to five mass extinctions where over 75% of the species on the planet have gone extinct
in a geologically short period of time (Barnosky et al. 2011). However, the
accelerating species extinction rate of today is considerably higher than before the anthropogenic colonisation (Pimm et al. 1995), and it has thus been
suggested that we actually live during the sixth mass extinction (Barnosky et
al. 2011). To exemplify, 77% of large carnivores, excluding pinnipeds, are
declining, and 61% have been classified as threatened (see summary in Ripple et al. 2014). Among small carnivores only 2% of 150 species are increasing while 39 % are decreasing and merely 22% are stable. There is also a
pronounced lack of monitoring and the status is unknown for 37% of the
species (IUCN/SSC Small Carnivore Specialist Group 2016).
In order to effectively and sustainably stop the loss of biodiversity and stabilise and restore declining populations, it is necessary to empirically identify
the underlying causes. Especially as populations that become small are not
only under threat because of the actual causes of decline, but also as they are
more sensitive to stochastic events such as disease outbreaks and genetic
drift which further increases the risk of extinction (Caughley 1994). When
examining causes of decline four specific human-induced factors repeat
themselves over and over again among threatened species, and these causes
of decline have come to be known as the evil quartet (Diamond 1984). The
quartet consists of over exploitation, habitat loss (and deterioration, including pollution), the impact of invasive species on native fauna and flora and
extinction chains, i.e. when the decline of one species has a direct or indirect
negative impact on other species.
It is clear from the evil quartet (see Diamond 1984) that conflict between
humans and wildlife often arises due to the utilisation and competition over
resources and space. Counteracting conservation problems is thus complex
13
but there is a multitude of techniques and efforts which can be undertaken on
various levels. For example, conservation efforts can be aimed at levels
ranging from individual focused protection to community level or conserving whole ecosystems in the form of national parks. Furthermore, efforts can
be focused on conservation in situ i.e. in the wild, or ex situ, i.e. in captivity,
or as a combination of the two (IUCN 2016). Combining in situ and ex situ
conservation can indeed be necessary if the species is completely extinct in
the wild or absent from large parts of its original distribution area. However,
despite existing conservation efforts many species continue to decline and
there is often a lack of knowledge on the causes. Efforts must thus be intensified and also made more effective.
A widely used method to restore and stabilise declining populations is reintroductions and translocations of animals. This method may be undertaken
completely in situ if wild animals are translocated to new suitable sites, but
is commonly combined with ex situ conservation where captive bred animals
are released into the wild. To determine whether a reintroduction programme
is successful or not it is necessary to monitor released animals, and although
many projects have been successful, a large proportion suffer from high
mortality rates (Fisher and Lindenmayer 2000; Breitenmoser et al. 2001;
Letty et al. 2007). This is not only problematic for the conservation goals but
is also a problem for animal welfare (Harrington et al. 2013). General individual characters, such as age and sex, are often considered in reintroductions (e.g. Maran et al 2009). However, although individual differences in
behaviour, i.e. non-human animal personality1, impact fitness (e.g. Smith
and Blumstein 2008) and have been suggested to be important in conservation (Watters and Meehan 2007), only two empirical examples exist
(Bremner-Harrison et al. 2004 and Paper II).
Non-human animal personality (hereafter ‘personality’) is defined as repeatable individual differences in behaviour that should be stable over different
contexts and situations. Personalities are heritable to some extent and under
the influence of additive genetic variation (Fairbanks et al. 2004; van Oers et
al. 2005; Rogers et al. 2008; Taylor et al. 2012; Fawcett et al. 2014; Johnson
et al. 2015). The expression of personality can be divided into groups of
correlated behaviours called personality trait domains. Examples of domains
include exploration (exploratory behaviour in novel environments), boldness
(risk-taking) and sociability (non-antagonistic behaviours towards conspecifics; Sih et al. 2004; Réale et al. 2007). The evolution of personalities and the
1
Also known as behavioural syndromes, temperament and copying styles
14
maintenance of this behavioural variation has been discussed in theoretical
studies (Wolf et al. 2007; Wolf and Weissing 2010; 2012) but empirical
studies are very rare (Dingemanse et al. 2004; Boon et al. 2007) and the subject is to date poorly understood.
Radio-tracking of reintroduced swift foxes (Vulpes velox) has revealed that
bold foxes run a higher risk of early death after release in comparison to
shyer individuals. However, in the captive source population bold individuals had a higher reproduction success which could mean that captivity causes
a selection pressure for boldness and indirectly reduces reintroduction success (Bremner-Harrison et al. 2004). The study indicates that personality
could be an important tool in reintroductions and also an aspect to consider
in captive breeding. However, other individual traits could also be important
to consider. For example, individual dietary specialism and plasticity towards novel food could affect survival in reintroductions.
Ecosystems are complex organisations with a multitude of direct and indirect
species interactions. Hence, focusing conservation efforts on individuals and
single species may not be enough to succeed with conservation goals (Linell
and Strand 2000). In addition to the natural complexity of food webs, humans have both intentionally and unintentionally introduced alien species to
ecosystems (e.g. Bonesi and Palazon 2007). This is often a conservation
issue as invasions can result in trophic cascades2 (Croll et al. 2005; Fey et al.
2009) and invasive predators can have disproportionally strong impact on
prey species compared to native predators (Salo et al. 2007) and also displaced inferior predators (Maran and Henttonen 1995; Maran et al. 1998).
Likely since the prey species have not evolved antipredator traits against the
novel predators (Fey et al. 2010). Native predators have, however, been suggested to buffer invasions, wherefore management decisions concerning
invasive species could gain from knowledge on these species interactions.
Especially as predator cascades can occur where large predators may limit
medium-sized ones through different forms of competition, thus releasing
small predators from competition with the medium-sized predators (Levi and
Wilmers 2012).
2
When the addition or removal of a species affects underlying trophic levels directly and
indirectly
15
Study species
The European mink
The European mink (Mustela lutreola; Fig 1) is a small feeding generalist
carnivore. It is solitary living and inhabits fresh water courses such as
brooks, river banks and wetlands and is considered to be a habitat specialist.
The breeding season of the polyestrous species occurs in March to April and
the kits are born in late May to early June. Juveniles disperse from the litter
2.5-4 months after birth (Youngman 1990; Amstislavsky et al. 2009; Nagl et
al. 2015). The species has gone extinct in the vast majority of its former area
of distribution. The main threats can all be found in the evil quartet (Diamond 1984) and consist of habitat loss, past overexploitation in the form of
hunting and displacement by the invasive American mink (Neovison vison;
Maran and Henttonen 1995; Maran et al. 1998). The European mink is critically endangered (IUCN 2016) and is listed on Appendix II of the Bern
Convention.
Photo: Marianne Haage
Photo: Karla García Bustos
Fig.1. European minks, to the left in captivity and to the right post release.
Due to its endangered status there are conservation programmes aimed at the
European mink. For example Tallinn Zoological Gardens in Estonia hosts a
captive breeding facility and provides animals for reintroductions on the
islands Hiiumaa and Saaremaa, which have both been cleared from American mink. A small population has been established on Hiiumaa but postrelease survival is generally poor. Predation is the major cause of death (Maran et al. 2009) and on an individual level survival patterns cannot be explained by movement patterns (Harrington et al. 2014), age at release, soft or
hard release3, type of housing pre-release or how many previous generations
3
In hard release animals are released to the wild directly from captive conditions. Soft release
includes some form of training or habituation wild conditions, for example, with the help of
naturalised enclosures on site that the animal can leave gradually.
16
of an individual that have been raised in captivity. Only sex has been shown
to have an effect on survival (Maran et al. 2009).
The American mink
In paper IV the American mink (Fig. 2) is the focal study species. It is a
small sized generalist carnivore that inhabits shorelines, including both salt
and fresh water bodies of various types. Due to its fur the American mink
was introduced to Europe in the 1920s via fur farms and introductions
(mainly in the former Soviet Union), and is now established in large parts of
the continent (Kauhala 1996; Bonesi and Palazon 2007). The American mink
is regarded as a pest species when invasive. It can cause trophic cascades
(Fey et al. 2009) and has a negative impact on several species of rodents,
ground-nesting birds and displaces slightly smaller and less robust European
mink (Nordström et al. 2002; 2003; Jefferies 2003; Banks et al. 2004; 2005;
Maran and Henttonen 1995; Maran et al. 1998; Sidorovich and Macdonald
2001).
Invasive American mink has been suggested to
be affected negatively by native red fox (Vulpes vulpes) and otters (Lutra lutra). Carlsson
et al. (2010) observed inversed mink and fox
population trends during the crash and recovery phase of the red fox during a sarcoptic
mange epizootic and suggested that exploitation competition could be the mechanism of
Photo: Ulf Antonsson
interaction. Otters have also been suggested to
Fig.2. American mink
have a negative impact in previous studies
(Bonesi and Macdonald 2004; McDonald et al. 2007). However, later studies
suggest that the American mink shifts to a more terrestrial diet and becomes
increasingly diurnal to avoid competition, and although body conditions
worsens slightly in the presence of otters abundances remain unchanged
(Harrington et al. 2009). The net effect of fox and otter on the American
mink remains unknown.
Aims
The general aim of this doctorate thesis was to contribute knowledge useful
for the conservation of the critically endangered European mink on both an
individual and ecosystem level, including both in- and ex-situ conservation.
Since conservation contexts often allow for fundamental research, there were
also explicit theoretical hypotheses. Paper I tests if European mink display
17
personality and then explores the structure and plasticity of personality by
comparing personality expression between the non-breeding and breeding
season. Since personality testing can be difficult and caveats needs to be
explored test methods are also considered, for example, the significance of
test context for personality expression. Paper II investigates if post-release
survival in reintroduced European minks is affected by personality, and if
spatiotemporal conditions influence the relationship between survival and
personality. As this is interesting for the evolution of personalities, maintenance of personality over evolutionary time is a major theme of the paper.
To further examine European mink ecology and factors that could affect
survival, individual diet choices and learning ability towards unfamiliar prey
was tested in paper III. Since one of the major causes of decline for the
European mink is the invasion of the American mink, paper IV investigates
if native predators can suppress American mink and discusses intraguild
interactions.
Methods
Paper I, II and III were based on studies on European mink at the conservation breeding facility of Tallinn Zoological Gardens (off-public) in Estonia.
All animal testing was performed at the breeding facility and reintroductions
and radio-tracking took place on the islands of Saaremaa (2012) and Hiiumaa (2013) in the Baltic Sea. The releases were part of a conservation project
on European mink and before the releases both islands were cleared/free
from American mink (Maran et al. 2009; also see under “Study species”).
None of the studies required permissions for animal testing according to EUlegalisation and Estonian law but animal welfare was of course deeply considered in the experimental designs. In paper IV the American mink was the
focal study species and the study was based on previously collected survey
data.
Paper I
In paper I the structure of personality in European mink was examined and
we also investigated if the expression of personality varies over contexts and
situations. We employed four different behavioural tests including novel
object tests, novel arena tests and mirror stimulus tests both in the home
enclosures of the animals and in a novel environment to test the impact of
test context. The novel object test was repeated to gain a measure of repeatability and thus the animals were subject to five trials although there were in
18
total four different tests. To examine the effect of situation this set of experiments was performed once in the non-breeding season (NovemberDecember; N = 80) and once in the breeding season (March-April; N = 68).
In total 21 different behaviours were measured (Table 1) and each trial lasted
4 min. The animals were scored the first time they performed a specific behaviour. The earlier in the trial that the behaviour was first displayed, the
higher was the score. The scoring system is easy to use and the scores are
rather uncomplicated to analyse, which is of importance in conservation as
future testing can then be performed by staff with little scientific training.
The method also minimises the risk of measurement errors. For example,
hesitant individuals who eventually do a behaviour repeatedly will not get
higher scores than individuals who immediately perform behaviours with no
hesitation. Such individuals are likely to hold different positions on behavioural continuums.
To identify personality trait domains all single behaviours collected during
the experiments were analysed with principal component analysis (PCA).
The outcome of the analysis was then used to calculate scores for each individual for each personality trait domain. We used general linear models to
analyse if personality was related to sex, body weight or age class and if
season had an influence on the expression of personality. In the models we
included interactions for sex and season and sex and age class.
Paper II
In paper II we investigated effects of personality on survival in reintroduced
European mink. We also tested if personality effects were influenced by
spatiotemporal conditions by releasing animals in two different locations and
years and controlled for effects of sex. In both years animals were personality tested pre-release (August) in captivity, using a slightly modified version
of the set of experiments used in paper I. Thereafter the animals were fitted
with radio-collars and transported to the release sites (late August to early
September) to be released under monitoring via radio-tracking. In 2012 (N =
10) animals were released on the island of Saaremaa and in 2013 on Hiiumaa
(N = 15). Monitoring lasted for 60 days where after surviving animals were
recaptured for collar removal and then released again on the capture sites.
Dead animals were examined by a veterinarian to determine cause of death.
Personality scores were calculated as in paper I. A general linear model was
then built to analyse the relationships between survival and personality, sex
19
and release year/island. A survival analysis was performed to depict survival
patterns and rates in the different years.
Paper III
In paper III feeding specialisation was studied in captive European mink (N
= 9). All animals had the same upbringing and had received the same diets
previous to the study. Cafeteria experiments were used to test preferences for
one prey species (Baltic herring, Clupea harengus membras) that was known
to the captive-bred animals and two natural prey species (noble crayfish
(Astacus astacus), mouse (Mus musculus) that they had not experienced
previously. In order to investigate learning times the experiments were repeated (N = 28). In the trials we recorded what the European minks chose to
eat and what they rejected, i.e. what they did neither cache nor eat.
The sample size was relatively small (N = 9) wherefore we reduced the
number of variables (N = 6, eating or rejecting each prey,) using PCA to get
more reliable statistical analyses. As the frequencies of rejections were negatively related to the frequencies of each eaten prey species, the eating variables were regarded to sufficiently reflect the outcomes of the trials and rejections were thus excluded from the following analyses. Chi2-tests were used
to test differences between individuals and prey items in preference. For the
whole group of European mink, changes in diet choices over time were also
analysed with non-parametric spearman rank correlations. Individual changes in preference over time were analysed with logistic regressions. In an
attempt to quantify specialists and generalist we calculated the proportion of
trials when a prey item was eaten. However, we only considered trials following the trial when the prey item was tasted for the first time, as it would
not be useful to measure how many times an item was preferred before the
animals even knew what it actually tasted like.
Paper IV
In paper IV we analysed the relationship between the American mink, red
fox and Eurasian otter in North-eastern Europe with respect to abundances,
population dynamics and trends. We also controlled for climate and productivity effects. We used survey data from 18 regions in Finland (N = 15),
Estonia (N = 1) and Belarus (N = 2). In Estonia the survey data were complemented with hunting bags with a one year time lag as these data were
strongly correlated to the survey data.
20
General linear models were built to test a) if abundances of American mink
were related to those of red fox or otter, primary productivity and the presence of coast b) if population trends of American mink were related to those
of red fox or otter, primary productivity, the presence of coast and c) if
American mink population dynamics in each region were related to those of
red fox or otter, winter and summer mean temperatures and the North Atlantic oscillation index (NAO). In the abundance model we only used Finnish
data as the data were required to have the same unit. Estonian data were only
used to analyse population trends as the survey data from there were based
on the opinion of hunters throughout the country. In contrast the Finnish data
were comprised of snow tracking along set transects and the Belarusian data
were based on track surveys. Based on the results of cross-correlation analyses a time lag of one year was included as well as unlagged data in the population dynamics models.
Results and discussion
Paper I
The PCA revealed three personality trait domains consisting of boldness,
sociability and exploration (Table 1). All domains were repeatable between
situations, i.e. the non-breeding and breeding season. Furthermore, repeatability was also confirmed within situations for the novel object test that was
performed twice (with different stimuli) in each situation. Therefore we draw
the conclusion that European minks display personality.
Performing the mirror stimulus test in both the home enclosure and a novel
arena revealed that the expression of personality can be context dependent.
In the home enclosures boldness was displayed whereas sociability was
mainly expressed in the novel arena (Table 1). Réale et al. (2007) suggested
that personality trait domains should be defined based on the ecological situation where behaviours were recorded. Here it is ecologically feasible to
assume that the behaviour changes depending on whether the encounter occurs in the own territory or outside of it as the territory is an important resource and therefore worth taking risks for. If a conspecific is encountered
outside of the territory the risk probably lies in being attacked and injured,
and a non-aggressive approach might lessen the risk.
This finding also shows the importance of experiment design when examining personality in animals. It is recommendable to use multiple methods to
21
measure multiple personality trait domains and statistically analyse which
single behaviours that form domains instead of deciding what a test
measures without confirmatory testing.
Sex did not affect the expression of sociability in the non-breeding season
but in all other cases males generally scored higher than females on the personality trait domains (Non-breeding season: Pboldness = 0.033; Pexploration =
0.0025; breeding season: Pboldness < 0.0001; Pexploration < 0.0001; Psociability <
0.0001; Fig. 3). The variation was however considerable and both sexes
were present in all parts of the behavioural continuums. Body weight had no
impact on personality and the only effect of age was in an interaction with
sex in the breeding season (P = 0.045). This implies that the causation of
personality is not related to age and body weight.
Although personality was repeatable between situations, the expression of
personality changed plastically from the non-breeding season to the breeding
season. Males became more explorative (P = 0.028) and also bolder whilst
females became shyer (P = 0.0029; Fig. X). The results are in accordance
with the actual breeding behaviour of the European mink. Although active
approaches happen, females usually wait and hide whilst males wander in
search of females in oestrus (pers. comm. Nagl A).
Fig. 3. European mink differences in boldness, sociability and exploration between the nonbreeding (N = 80) and breeding season (N = 68). * Marks significant sex differences within
season and dashed lines show significant sex differences between seasons. Lined squares
mark females and filled squares mark males. Personality scores are presented in z-scores
(note that the minimum/maximum score varies between domains).
22
Table 1. Varimax rotated principal components based on 21 behavioural measures from
personality experiments on captive European mink (Nfemale = 40; Nmale = 40). The experiments
were performed in the non-breading seasonin November and December 2009. Bold values
indicate salient loadings (≥ 0.4) are marked in boldface. If several salient loadings occurred
for same behavior the highest value was marked.
Experiment
Measure
a
Novel object
in home
enclosure
Mirror image
stimuli in
home
enclosure
Mirror image
stimuli in
novel arena
Novel
arena
Latency
b
Approach
c
Sniff
Attack/bite object
Carry object away
Latency a
Look d
Sniff c
e
Push/dig/scratch
Attack/bite mirror
Latency a
imaged
Look
Sniff c
Mark f
Hiss
e
Push/dig/scratch
Attack/bite mirror
Latency a
image
g
Zones visited
Hiss
Mark f
Explained variation
Proportion of total
Boldness
Sociability
Exploration
-0.860
0.875
0.821
0.731
0.761
-0.660
0.626
0.636
0.559
0.438
-0.097
0.048
0.124
0.099
-0.161
-0.031
0.013
-0.257
-0.087
0.081
0.058
-0.112
0.053
-0.321
0.439
0.396
0.229
-0.117
-0.866
0.911
0.895
0.811
0.276
0.210
0.136
-0.468
-0.175
0.170
0.155
0.025
0.047
0.304
-0.316
-0.311
-0.307
-0.079
-0.107
0.076
0.065
0.110
-0.118
0.550
0.479
-0.574
0.153
0.010
0.075
5.120
0.248
0.462
0.088
0.369
4.303
0.205
0.595
0.625
0.336
2.242
0.107
a) Latency in s to leave the nesting/transport box. b) The body is positioned towards the object at a
maximum distance of 20 cm. c) Sniffing at the novel object or mirror image. See text for more information. d) Looking at the mirror image. See text for more information. e) Scratch, push or dig at the
mirror image. f) Visible markings including anal drags. g) The number of zones visited.
Paper II
Boldness was positively related to days survived (N = 19; p = 0.0080; ß =
0.38) in the released and radio-tracked European minks. There was also a
significant interaction between year/island and exploration (N = 19; p =
0.0061) as exploration had a negative impact in 2012 (N = 9; ß = -0.55) and
a positive impact in 2013 (N = 10; ß = 0.76; Fig. 4). Survival was also influenced directly by release year/island (N = 19; p < 0.001; ß = 0.52) with no
long-term survival in 2012 but with many surviving individuals in 2013.
Sociability had no effect on survival, as would be expected in a solitaryliving species. Overall the model had a high adjusted R2 of 0.78.
23
Days survived - both
years
Days survived - 2012
Days survived - 2013
70
60
50
40
30
20
10
0
70
60
50
40
30
20
10
0
70
60
50
40
30
20
10
0
-10 -8 -6 -4 -2 0 2 4 6 8
Boldness
-10 -8 -6 -4 -2 0 2 4 6 8
Sociability
-10 -8 -6 -4 -2 0 2 4 6 8
Exploration
Fig. 4. The relationship between personality and survival in European mink reintroduced in
Estonia. Significant effects are marked with trend lines. Animals were released on the island
Saaremaa in 2012 (N = 10) and on the island Hiiumaa in 2013 (N = 15). Personality measurements were taken in captivity pre-release and monitoring post-release was done by radiotracking. The trend lines show that spatiotemporal conditions affected the effect direction of
exploration but not boldness. Filled circles denote 2013 and open squares 2012. The triangle
shows an individual which collar sent a mortality signal from an underground tunnel. The
death could thus not be verified and the individual was not included in any analyses. Lost
animals were also excluded.
In 2012 one animal was lost and nine found dead. The average days survived
was 15 days and the cumulative survival for the 60 days of radio-tracking
was 0 %. In 2013 seven animals survived throughout the radio-tracking period, three were found dead and four were lost. One additional animal likely
died but as the body could not be retrieved to confirm the death this individual was excluded from all analyses. The average days survived was 48 days
and the cumulative survival for the 60 days of radio-tracking was 73 %. The
main cause of death was intraguild killings (83 %).
The results show that it is important to consider personality in conservation
as both boldness and exploration affected survival. However, the matter is
complicated by the influence of spatiotemporal conditions that caused exploration to be negative for survival in 2012 and positive in 2013. For conservation purposes the exact causation of spatiotemporal effects should be identi24
fied as it affects survival both directly and indirectly. It is possible that the
cause was related to weather as the summer was cold and wet in 2012 and
warmer and dryer in 2013. Another explanation could be that red fox densities are higher on Saaremaa than Hiiumaa, but on the other hand pine martens were more common on Hiiumaa (pers. comm. Maran T), and albeit
foxes kill European mink more frequently than martens we still found a marten-killed mink on Hiiumaa. The predator impact is thus somewhat difficult
to pinpoint. However, for the sake of conservation the results of this study
should be used to investigate how personality is best considered in reintroduction.
The fact that exploration was influenced by spatiotemporal conditions is
interesting from an evolutionary point of view. It is possible that exploration
is selected for via survival and that varying conditions creates a fluctuating
selection pressure which maintains variation in exploration. Only two previous studies have also shown empirically that spatiotemporal variation in
conditions could maintain personality (Dingemanse et al. 2004; Boon et al.
2007). However, in this study boldness did not vary and sociability did not
affect survival in any year/island. This suggests that different personality
trait domains are maintained by different mechanisms, which has never been
shown before.
In swift fox reintroductions boldness was shown to heighten the risk of early
death (Bremner-Harrison et al. 2004) and meta-analyses of relationships
between personality and fitness indicate the same pattern (Smith and Blumstein 2008). For the European mink the pattern was the opposite, however. It
is possible that small sized predators face different challenges than medium
sized or large predators and therefore must have different strategies. No matter the cause, this finding still points out the hazard of generalising between
species. Finally, sex had no effect in contrast to previous studies (Maran et
al. 2009). A probable explanation to this is that the sex effect is mediated by
sex differences in personality (see Paper I) and that the composition of animals in this study was chosen based on personality primarily and sex secondarily.
Paper III
Overall in the diet experiment the European minks ate mouse in 2.7% of the
trials, fish in 47% of the trials, and crayfish in 50% of the trials. Chi2-tests
showed that the three different prey species were eaten in different ratios (p
< 0.001). Individuals ate different amounts of fish (p = 0.0017) and crayfish
25
(p < 0.001). The overall diet
preference changed over
time as crayfish became
more popular (spearman
rank correlation: p < 0.001;
R = 0.89) and fish was eaten
less (spearman rank correlation: p = 0.0067; R = -0.50).
Individual learning times
toward novel prey varied
and are presented in Fig.5.
According to our method of
quantifying specialists and
generalists three individuals
were crayfish specialists (Nm
Fig. 5. Log-regression relationships between trial (N
= 2; Nf = 1), two fish spe= 28) and prey species eaten by captive European
mink (N = 9). Solid lines indicate crayfish, evenly
cialists (Nm = 1; Nf = 1) and
dashed lines fish and unevenly dashed lines mouse. A
four generalists (Nm = 2; Nf
black line denotes significance (p ≤ 0.05) and grey
= 2; Table 4). These obserlines non-significance. F is short for females and M
vations are similar to those
for males.
made on wild specimens
(Sidorovich et al. 2001; Põdra et al. 2012).
To summarise we found different strategies and learning times in the captive-bred animals although they all had the same up-bringing and food supply previous to the experiment. The findings thus suggest that individual
variation in preferences can be related to innate differences. Also, learning
contributes to individual specialisation but varied among individuals. This
difference could indicate individual variation in behavioural plasticity, which
in turn is a trait that has been connected to personality (Benus et al. 1987;
Rodriguez-Prieto et al. 2010; Herborn et al. 2014). As personality can impact
survival in reintroductions (Bremner-Harrison et al. 2004; Paper II) this finding could be of relevance in conservation.
Paper IV
American mink and red fox abundances were negatively related in the 15
Finnish regions (p = 0.0042; beta = -0.69). There were no effects on longterm population trends of American mink (Fig. 6).
26
a) Abundances (Tracks/10 km * 24h)
0,3
American mink
American mink
0,3
0,2
0,1
0,2
0,1
0,0
0,0
0
2
4
6
8
0,0
10 12 14
0,1
0,2
0,3
0,4
Eurasian otter
Red fox
0,3
0,3
0,2
0,2
American mink
American mink
b) Population trends (linear slope coefficients)
0,1
0,0
-0,1
0,1
0,0
-0,1
-0,2
-0,2
-0,3
-0,3
-0,3 -0,2 -0,1 0,0 0,1 0,2 0,3
-0,3 -0,2 -0,1 0,0 0,1 0,2 0,3
Red fox
Eurasian otter
Fig. 6. Relationships between a) abundances (Nregion = 15) and b) population trends (Nregion
= 18) of American mink with red fox or otter in North-eastern Europe (general linear models). Trend lines mark significant effects.
Population dynamics of otters and minks in the different regions were significantly correlated in 8 out of 17 regions (47%) and in 4 regions between
foxes and minks (24%). Climate had effects in only two regions (12%). Six
positive correlations with otter were found in Pohjois-Savo and PohjoisKarjala in eastern Finland, in Pohjanmaa in Western Finland (with a one
year time lag), the northernmost region Lappi and in both Belarusian regions
Lovat and Volka (with a one year time lag). In Rannikko-Pohjanmaa and
Etelä-Savo in Finland there were negative correlations with otter with a one
and two year lag respectively. Red fox dynamics were positively related to
American mink dynamics in Pohjois-Häme, Lappi and Oulu in Finland. In
Oulu there was also a negative relationship when a one year lag was considered, similarily to Varsinais-Suomi. For detailes see Fig. 6 and Table 2.
27
Table 2. The population dynamics of American mink vs. the effect of otter and red fox population dynamics and climate variables. Population dynamics are represented by the residuals of
linear trends for each region. The final models were selected by stepwise removal of nonsignificant terms and the original model was: 'American mink ~ red fox + otter + mean summer temperature + mean winter temperature + mean winter NAO (North Atlantic Oscillation)'. Time lags of 1 year were also included for species data. The models for Kainuu, EteläSavo, Satakunta, Keski-suomi, Etelä-Häme and Uusimaa were n.s.
Region
Variable
p
Beta
etasquared
Whole
Partial
eta-
Power
squared
model
adj.
R
2
Red fox
p<0.001 0.52
0.27
0.39
0.96
Otter
p<0.001 0.55
0.30
0.42
0.98
Red fox
0.0048
0.23
0.31
0.85
Red fox lag +1 0.042
-0.35 0.11
0.18
0.54
Winter temp.
0.015
-0.44 0.16
0.24
0.72
Pohjois-Karjala
Otter
0.048
0.38
0.15
0.15
0.52
0.11
Pohjois-Savo
Otter
0.027
0.43
0.18
0.18
0.62
0.15
Etelä-Savo
Otter lag +2*
0.0069
-0.53 0.28
0.28
0.81
0.25
Pohjanmaa
Otter lag +1
0.0019
0.58
0.34
0.34
0.92
0.31
Rannikko-Pohjanmaa Otter lag +1
0.024
-0.44 0.19
0.19
0.64
0.16
Pohjois-Häme
Red fox
0.0050
0.52
0.27
0.27
0.84
0.24
Varsinais-Suomi
Red fox lag +1 0.0050
-0.53 0.28
0.28
0.84
0.25
Kaakkois-Suomi
Summer temp. 0.041
0.40
0.16
0.16
0.55
0.13
Lovat
Otter
0.040
0.43
0.19
0.19
0.55
0.15
Volka
Otter lag +1
p<0.001 0.62
0.38
0.38
0.97
0.36
Lappi
Oulu
0.54
0.52
0.37
* Cross-correlation analysis revealed a strong +2 lag for otter in the site of Pohjois-Savo only,
hence an exception was made from only using lags of +1 or no lag (0) ,which was the otherwise dominating patterns of cross-correlation
28
F) Eurasian otter
E) Red fox
D) American mink
A) American mink
Abundances (Tracks/10 km * 24h)
0
0.4
B) Red fox
Population trends (standardized slopes of survey data)
-0.1
G) Climate effects
0
14
I) Eurasian otter, lag 0 and +1
0 (+)
Abundances (Tracks/10 km * 24h)
2
0.1
H) Red fox, lag 0 and +1
0 (+)
0 (+)
1* (-)
WT
(-)
1 (-)
C) Eurasian otter
1(+)
0(+) 0 (+)
2 (-)
0(+)
ST
1(-)
0 (+)
1 (+)
Abundances (Tracks/10 km * 24h)
0
0.4
p-values on effects on American mink population dynamics
≤0.001
≤0.01
≤0.05
>0.05
Fig 6. Abundances and long-term population trends of American mink, red fox and otter,
including effects of climate, in North-eastern Europe. In G): WT = mean winter temperature, ST = mean summer temperature. In H) and I) ‘0’ denotes non-lagged effects and
higher numbers denote lagged effects. Effect direction is given in parenthesis and colouration is striped if two variables are significant whilst their level of significance differs. ‘*’
indicates the highest p-value.
The results support previous findings (Harrington et al. 2009; Carlsson et al.
(2010) as the red fox but not otter seem to limit American minks. Relationships between population dynamics in the different regions in the study area
suggest that both exploitation and interference competition van be mechanisms whereby foxes suppress minks. However, in many there were no relationships between the population dynamics. This could be due to that exploitation and interference competition might occur simultaneously in some
regions and thus cancel each other out in the dynamics.
29
Climate effects were scarce which could be related to the highly generalistic
nature of the American mink. The species has, for example, been able to
colonise areas with varying climate throughout Europe, from Portugal and
Spain to northern Finland (Bonesi and Palazon 2007).
The findings indicate the existence of a predator cascade such as is described
in Levi and Wilmers (2012). The red fox has been shown to be suppressed
by interference competition with lynx (Lynx lynx; Sunde et al. 1999; Helldin
et al. 2006) and is therefore rare in eastern Finland where lynx are abundant
(Elmhagen et al. 2010). Here the mink abundances were highest in eastern
Finland where lynx are most abundant, but lowest in the southern parts
where foxes are most abundant. This indicates that lynx releases minks from
being limited by foxes. Such cascades could influence the buffering capacity
of native predators. Regarding conservation, it is possible that management
efforts might be most beneficial for species that are negatively impacted by
minks if they to a larger extent are undertaken in areas with low fox abundances.
General conclusions
This thesis reveals the structure and plasticity of personality in European
mink, and shows that personality can affect survival in reintroductions.
However, it is also important to heed spatiotemporal influences as they can
impact survival directly and indirectly, the latter by influencing in which
direction a personality trait domain affects survival. Individual dietary specialisation is also confirmed in the European mink, in concurrence with data
from the wild. However, there was also individual variation in learning times
towards novel but natural prey species. Such individual variation might affect survival in reintroductions and also be connected to personality.
Overall, paper I-III shows the importance of considering individual characteristics in conservation and also contributes with knowledge on the selection, structure and plastic nature of personality. Individual characteristics
such as age or sex are often considered in conservation but the two only
studies on the impact of behavioural differences, e.g. Bremner-Harrison et
al. (2004) and paper II, shows that this concept has much more to give. Reducing mortality and hence enhancing the success of conservation efforts is
also not only cost effective but important for animal welfare as well.
30
However, in order to restore a declining population it is also necessary to
remove the causes of decline. The invasive American mink is one of the
major causes of decline for the European mink and knowledge on the ecology of the American mink is thus important for management decisions which
hopefully could benefit the European mink, or at least maintain the few sanctuaries still left. The results here showed that the red fox can suppress the
American mink whilst the otter showed no or very weak such tendencies.
American mink control might thus be of especial importance in areas with
low red fox abundances.
Finally, research has much to gain from a combined approach of conservation and fundamental research. Although there are of course limitations and
caveats it is cost effective to study fundamental questions and conservation
problems simultaneously. Functioning conservation programmes also provides access to animals, often in large quantities. Moreover, conservation
efforts such as reintroductions provide a basis for field experiments where
animals are easily accessed pre-release for tests and measurements with no
bias towards so called trap happy individuals, which can be a problem in the
wild. Comparative studies of animals in the wild and in captivity can also
help in confirming hypotheses by providing evidence both from the field and
from controlled experiments.
References
Amstislavsky S, Lindeberg H, Ternovskaya Y, Zavjalov E, Zudova G, Klochkov D,
Gerlinskaya L. 2009. Reproduction in the European mink, Mustela lutreola:
oestrous cyclicity and early pregnancy. Reprod Dom Anim 44: 489-498.
Banks PB, Norrdahl K, Nordström M, Korpimäki E. 2004. Dynamic impacts of feral
mink predation on vole metapopulations in the outer archipelago of the Baltic Sea. Oikos 105: 79-88.
Banks PB, Nordström M, Ahola M, Korpimäki E. 2005. Variable impacts of alien
mink predation on birds, mammals and amphibians of the Finnish archipelago: a long-term experimental study. In: IX International Mammalogical
Congress. Sapporo, Japan.
Barnosky AD, Matzke N, Tomiya S, Wogan GOU, Swartz B, Quental TB, Marshall
C, McGuire JL, Lindsey EL, Maguire KC, Mersey B, Ferrer EA. 2011.
Has the Earth's sixth mass extinction already arrived? Nature 471: 51-57.
31
Benus RF, Koolhaas JM, Van Oortmerssen GA. 1987. Individual differences in
behavioural reaction to a changing environment in mice and rats. Behaviour
100:105-121
Bonesi L, Macdonald DW. 2004. Impact of released Eurasian otters on a population
of American mink: a test using an experimental approach. Oikos 106:9-18.
Bonesi L, Palazon S. 2007. The American mink in Europe: Status, impacts, and
control. Biol Conserv 134: 470-483.
Boon AK, Rèale D, Boutin S. 2007. The interaction between personality, offspring
fitness and food abundance in North American red squirrels. Ecol Lett 10:
1094-1104.
Bremner-Harrison S, Prodohl PA, Elwood RW. 2004. Behavioural trait assessment
as a release criterion: boldness predicts early death in a reintroduction programme of captive-bred swift fox (Vulpes velox). Anim Conserv 7: 313320.
Caughley G. 1994. Directions in Conservation Biology. J Anim Ecol 63: 215-244.
Croll DA, Maron JL, Estes JA, Danner EM, Byrd GV. 2005. Introduced Predators
Transform Subarctic Islands from Grassland to Tundra. Science 307: 19591961.
Diamond J. 1984. “Normal” extinctions of isolated populations. In: Nitecki M (ed),
Extinctions. pp 191- 246. University of Chicago press, Chicago.
Dingemanse NJ, Both C, Drent PJ, Tinbergen JM. 2004. Fitness consequences of
avian personalities in a fluctuating environment. Proc R Soc Lond B 271:
847-852.
Elmhagen B, Ludwig G, Rushton SP, Helle P, Lindén H. 2010. Top predators, mesopredators and their prey: interference ecosystems along bioclimatic productivity gradients. J Anim Ecol 79: 785-794.
Fairbanks LA, Newman TK, Bailey JN, Jorgensen MJ, Breidenthal SE, Ophoff RA,
Comuzzie AG, Martin LJ, Rogers J. 2004. Genetic contributions to social
impulsivity and aggressiveness in vervet monkeys. Biol Psychiatry 55: 642647.
Fawcett GL, Dettmer AM, Kay D, Raveendran M, Higley JD, Ryan ND, Cameron
JL, Rogers J. 2014. Quantitative genetics of response to novelty and other
stimuli by infant rhesus macaques (Macaca mulatta) across three behavioral assessments. Int J Primatol 35: 325-339.
Fey K, Banks PB, Oksanen L, Korpimäki E. 2009. Does removal of an alien predator from small islands in the Baltic Sea induce a trophic cascade? Ecography
32:546-552.
Fey K, Banks P, Korpimäki E. 2010. Alien Mink Predation and Colonisation Processes of Rodent Prey on Small Islands of the Baltic Sea: Does Prey Naïveté Matter? International Journal of Ecology doi:10.1155/2010/984396
IUCN. 2016. IUCN Red List of Threatened species. http://www.iucnredlist.org
[2016-04-02]
32
IUCN/SSC Small Carnivore Specialist Group. 2016. http://www.iucn-scsg.org
[2016-03-27]
Johnson Z, Brent L, Alvarenga JC, Comuzzie AG, Shelledy W, Ramirez S, Cox L,
Mahaney MC, Huang YY, Mann JJ, Kaplan JR, Rogers J (2015) Genetic
influences on response to novel objects and dimensions of personality in
Papio baboons. Behav Genet 45: 215-227.
Harrington, L. A., Harrington, A. L., Yamaguchi, N., Thom, M. D., Ferreras, P.,
Windham, T. R. and Macdonald, D. W. 2009. The impact of native competitors on an alien invasive: temporal niche shifts to avoid interspecific aggression? Ecology 90: 1207-1216.
Harrington LA, Moehrenschlager A, Gelling M, Atkinson RPD, Hughes J, Macdonald DW. 2013. Conflicting and complementary ethics of animal welfare
considerations in reintroductions. Conserv Biol 27: 486-500.
Helldin JO, Liberg O, Glöersen G. 2006. Lynx (Lynx lynx) killing red foxes (Vulpes
vulpes) in boreal Sweden – frequency and population effects. J Zool 270:
657-663.
Herborn KA, Heidinger BJ, Alexander L, Arnold KE. 2014. Personality predicts
behavioral flexibility in a fluctuating, natural environment. Behav Ecol 25:
1374-1379
Jefferies, D. J. 2003. The water vole and mink survey of britain1996–1998 with a
history of the long term changes in the status of both species and their causes. T1he Vincent Wildlife Trust, Ledbury, UK.
Kauhala, K. 1996. Distributional history of the American mink (Mustela vison) in
Finland with special reference to the trends in otter (Lutra lutra) populations. Ann. Zool. Fenn. 33: 283-291.
Letty J, Marchandeau S, Aubineau J. 2007. Problems encountered by individuals in
animal translocations: Lessons from field Studies. Ecoscience 14: 420-431.
Levi T, Wilmers CC. 2012. Wolves-coyotes-foxes: a cascade among carnivores.
Ecology 93: 921-929.
Linnell JD, Strand O. 2000. Interference interactions, co-existence and conservation
of mammalian carnivores. Divers Distrib 6: 169-176.
Maran T, Henttonen H. 1995. Why is the European mink, Mustela lutreola disappearing? – A review of the process and hypotheses. Ann Zool Fenn 32: 4754.
Maran T, Macdonald DW, Kruuk H, Sidorovich V, Rozhnov V. 1998. The continuing decline of the European mink, Mustela lutreola: evidence for the intraguild aggression hypothesis. Behaviour and Ecology of Riparian Mammals.
Symp Zool Soc Lond 71: 297-324.
Maran T, Põdra M, Põlma M, Macdonald DW (2009) The survival of captive-born
animals in restoration programmes – Case study of the endangered European mink Mustela lutreola. Biol Conserv 142: 1685-1692.
33
McDonald, R. A., O'Hara, K. and Morrish, D. J. 2007. Decline of invasive alien
mink (Mustela vison) is concurrent with recovery of native otters (Lutra lutra). Divers. Distrib. 13: 92-98.
Nagl A, Kneidinger N, Kiik K, Lindeberg H, Maran T, Schwarzenberger F (2015)
Noninvasive monitoring of female reproductive hormone metabolites in the
endangered European mink (Mustela lutreola). Theriogenology 84: 1472–
1481.
Nordström, M., Hogmander, J., Laine, J., Nummelin, J., Laanetu, N. and Korpimäki,
E. 2003. Effects of feral mink removal on seabirds, waders and passerines
on small islands of the Baltic Sea. Biol. Conserv. 109, 359-368.
Nordström, M., Hogmander, J., Nummelin, J., Laine, J., Laanetu, N. and Korpimäki,
E., 2002. Variable responses of waterfowl breeding populations to longterm removal of introduced American mink. Ecography 25: 385-394.
Pimm SL, Russell GJ, Gittleman JL and Brooks TM. 1995. The Future of Biodiversity. Science 269: 347-350.
Põdra M, Maran T, Sidorovich VE, Johnson PJ, Macdonald DW. 2012. Restoration
programmes and the development of a natural diet: a case study of captivebred European mink. Eur J Wildl Res 59: 93-104.
Réale D, Reader SM, Sols D, McDougall PT, Dingemanse NJ. 2007. Integratinganimal temperament within ecology and evolution. Biol Rev 82: 291318.
Ripple WJ, Estes JA, Beschta RL, Wilmers CC, Ritchie EG, Hebblewhite M, Berger
J, Elmhagen B, Letnic M, Nelson MP, Schmitz OJ, Smith DW, Wallach
AD, Wirsing AJ. 2014. Status and ecological effects of the world’s largest
carnivores. Science 343: 1241-1484.
Rodriguez-Prieto I, Martin J, Fernandez-Juricic E. 2010. Individual variation in
behavioural plasticity: direct and indirect effects of boldness, exploration
and sociability on habituation to predators in lizards. Proc Roy Soc Lond B
Bio, 278:266-273.
Rogers J, Shelton SE, Shelledy W, Garcia R, Kalin NH (2008) Genetic influences
on behavioral inhibition and anxiety in juvenile rhesus macaques. Genes
Brain Behav 7: 463-469.
Salo, P., Korpimäki, E., Banks, P. B., Nordström, M. and Dickman, C. R. 2007.
Alien predators are more dangerous than native predators to prey populations. Proc. R. Soc. B 274: 1237-1243.
Sidorovich, V. and Macdonald, D. W. 2001. Density dynamics and changes in habitat use by the European mink and other native mustelids in connection with
the American mink expansion in Belarus. Neth. J. Zool. 51: 107-126.
Sidorovich VE, MacDonald DW, Pikulik MM, Kruuk H. 2001. Individual feeding
specialization in the European mink, Mustela lutreola and the American
mink, M. vison in north-eastern Belarus. Folia Zool 50: 27-42.
Sih A, Bell AM, Johnson JC, Ziemba, RE. 2004. Behavioral syndromes: an integrative overview. Q Rev Biol 79: 241-277.
34
Smith BR, Blumstein TR. 2008. Fitness consequences of personality: a metaanalysis. Behav Ecol 19: 448-455.
Sunde P, Overskaug K, Kvamet T. 1999. Intraguild predation of lynxes on foxes:
evidence of interference competition? Ecography 22: 521-523.
Taylor RW, Boon AK, Dantzer B, Réale D, Humphries MM, Boutin S, Gorrell JC,
Coltman DW, McAdam AG (2012) Low heritabilities, but genetic and
maternal correlations between red squirrel behaviours. J Evol Biol 25: 614624.
van Oers K, de Jong G, van Noordwijk AJ, Kempenaers B, Drent PJ (2005) Contribution of genetics to the study of animal personalities: a review of case studies. Behaviour 142: 1185-1206.
Watters JV, Meehan CL. 2007. Different strokes: Can managing behavioral types
increase post-release success? Appl Anim Behav Sci 102: 364-379.
Wolf M, van Doorn GS, Leimar O, Weissing FJ. 2007. Life-history trade-offs favour the evolution of animal personalities. Nature 447: 581-585.
Wolf M, Weissing FJ. 2010. An explanatory framework for adaptive personality
differences. Philos Trans R Soc B 365: 3959-3968.
Wolf M, Weissing FJ. 2012. Animal personalities: consequences for ecology and
evolution. TREE 27: 452-461.
Youngman PM. 1990. Mustela lutreola. Mammalian Species 362: 1-3.
35
36
Acknowledgement
First of all I wish to thank my supervisors Bodil and Anders of course! and
also my main collaborators Ulrika and Tiit for all the help and opportunities
along the way! You have all meant a lot. Thanks also to my follow up group
Love and Birgitta.
I want to thank my dear family consisting of my boyfriend Anders, brother
Johan, mum Pirjo and dad Magnus for being there and being them, serving
me fantastic food, and for bearing with all the mink talk. I have also received
support from my other relatives and I am grateful to you all, and I especially
want to thank Arja for believing in me.
I also have many friends and colleagues that have been wonderful and supportive. I wonder what ever I would have done without my dear Sandra and
Johanna? Thank you for everything! And Karin and Emma, Agnes and Pär,
thank you for dragging me out of my personal mink swamp into the real
world every now and then, it has been much appreciated! Yjing-Chuck, you
are one of my oldest and best friends and your support means the world to
me. Astrid, there can truly be no better mink-partner-in-crime than you!
Ylva, I delight in all the (literally) historical moments we have had! Also
many thanks to Alexander S, Kristin and Marianne PM and all other valued
colleagues and friends. This of course includes Gunilla, Sonja and Anna who
have provided me with excellent food and company when teaching field
courses! I feel obliged to also thank my furry friend Osvald for all the supportive (or hungry?) meowing and purring.
In the field and while doing experiments I have had invaluable help and ever
so much fun with Åsa, Andreola, Kairi, Mireia and Carla, I wish you the
best, and also a thanks to Marko and Martin and many, many others who
have also helped. The staff at Tallinn Zoo deserves many thanks as well, you
do hard and admirable work.
For financial support and hence opportunities, I am very grateful to Helge
Ax:son Johnsons Foundation, the Swedish Institute, Tullbergs stipend for
biological research, C F Liljevalch J:ors travelling stipend, The Royal Swedish Academy of Science: Stiftelsen Regnells zoologiska gåvomedel, Alice
och Lars Siléns fond and K & A Wallenbergs Foundation.
Finally, how very bleak would not my life be if I had never met the European minks themselves? I cannot, and do not want to imagine a world without
you.
37
38
Sammanfattning på svenska
Förlusten av biologisk mångfald är ett växande problem och därmed blir
arbetet med att bevara arter allt viktigare. Den här avhandlingen behandlar
bevarandefrågor som rör den akut utrotningshotade flodillern (Mustela lutreola). Frågeställningarna täcker bevarandeaspekter både in situ (i det vilda)
och ex situ (i fångenskap) samt sträcker sig från individnivå till samhällsnivå. Vidare tar avhandlingen även upp frågor inom grundforskning eftersom bevarandesammanhang ofta ger möjligheter att dra slutsatser bortom
den tillämpade biologin.
Individuella beteendeskillnader, t.ex. personlighet, kan påverka överlevnad
och reproduktionsframgång och är därmed relevanta att beakta i bevarandesammanhang. Artikel I utforskar således experimentellt personlighetens
struktur, uttryck och plasticitet hos flodillrar i fångenskap. Artikel II undersöker därefter om personlighet påverkar överlevnad hos djur som har reintroducerats och om spatiotemporala förhållanden påverkar relationen mellan
personlighet och överlevnad. Artikel III undersöker med hjälp av experiment individuell dietspecialisering och inlärning i relation till nya (men naturliga) byten hos flodillrar i fångenskap eftersom detta också skulle kunna
påverka överlevnad vid reintroduktion. Ett av de största hoten mot flodillern
är konkurrens med den invasiva minken (Neovison vison) och förvaltning av
mink är därför viktig för bevarandet av flodillern. Rovdjur kan begränsa
andra (oftast mindre) rovdjur och artikel IV undersöker med hjälp av inventeringsdata från nordöstra Europa om de inhemska rovdjuren utter och rödräv kan begränsa minkpopulationer.
Tre personlighetsdomäner identifierades hos flodiller: djärvhet, utforskningsbenägenhet och socialitet. Domänerna var repeterbara men plastiska
mellan icke mellan icke-parnings och parningssäsong. Reintroducerade djur
levde längre om de var djärva men effekten av utforskningsbenägenhet var
antingen positiv eller negativ beroende på spatiotemporala förhållanden.
Detta är inte bara intressant inom bevarandebiologi, utan ger nya insikter om
hur individuella beteendeskillnader upprätthålls över evolutionär tid.
Födoexperimenten påvisade att dietmönster hos djur i fångeskap speglar
vilda individers dietval eftersom fanns liknande proportioner av generalister
och olika typer av specialister. Dock skiljde sig individer åt i inlärningstid
gentemot nya (men naturliga) byten, vilket tyder på att reintroducerade djur
kan ha varierande svårigheter att hitta mat efter utsläpp. Detta skulle kunna
påverka överlevnaden och är antagligen relaterat till personlighet.
39
Analyser av inventeringsdata visade att minkbestånd begränsas av rödräv.
Enligt tidigare studier begränsas rävar i sin tur av lodjur och abundansmönstret i artikel IV för mink i förhållande till rödräv tyder på att det finns en
rovdjurskaskad då minken var vanligast där lodjur var vanliga och vice
versa. Även om analys av arternas populationsdynamik i olika regioner i
studieområdet tydde på att exploaterings och interferenskonkurrens är troliga
som begränsande mekanismer, så fanns det i många regioner ingen relation
alls mellan arternas dynamik. Detta tyder antingen på svag konkurrens eller
på att det finns mekanismer som inte återspeglas i dynamiken.
På det stora hela belyser denna avhandling vikten av att ta hänsyn till individuell variation vid bevarandeåtgärder. Dessutom bidrar den också med kunskap om personlighetens struktur, plasticitet och evolution. Då minken regleras av räv kan det hända att det är fördelaktigast för arter som drabbas av
minkens framfart om förvaltningsåtgärder mot mink genomförs i högre grad
i rödrävsglesa och lodjurstäta områden. Sådana åtgärder kan antagligen inte
utrota minken men kanske bromsa in minkens spridning och på så sätt
skydda de få platser där flodillern fortfarande förekommer i vilt tillstånd.
40