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Consistency in boldness, activity and exploration at different stages of life

Consistency in boldness, activity and exploration at different stages of life Background: Animals show consistent individual behavioural patterns over time and over situations. This phenomenon has been referred to as animal personality or behavioural syndromes. Little is known about consistency of animal personalities over entire life times. We investigated the repeatability of behaviour in common voles (Microtus arvalis) at different life stages, with different time intervals, and in different situations. Animals were tested using four behavioural tests in three experimental groups: 1. before and after maturation over three months, 2. twice as adults during one week, and 3. twice as adult animals over three months, which resembles a substantial part of their entire adult life span of several months. Results: Different behaviours were correlated within and between tests and a cluster analysis showed three possible behavioural syndrome-axes, which we name boldness, exploration and activity. Activity and exploration behaviour in all tests was highly repeatable in adult animals tested over one week. In animals tested over maturation, exploration behaviour was consistent whereas activity was not. Voles that were tested as adults with a three-month interval showed the opposite pattern with stable activity but unstable exploration behaviour. Conclusions: The consistency in behaviour over time suggests that common voles do express stable personality over short time. Over longer periods however, behaviour is more flexible and depending on life stage (i.e. tested before/ after maturation or as adults) of the tested individual. Level of boldness or activity does not differ between tested groups and maintenance of variation in behavioural traits can therefore not be explained by expected future assets as reported in other studies. Keywords: Animal personality, Behavioural type, Microtus arvalis, Common vole, Plasticity, Consistency, Repeatability Background types and the connection between different behaviours in There has been increasing interest in consistent differ- a variety of contexts mean that an individual’s behaviour is ences in individual behaviour across time and/or con- not infinitely flexible [6]. From an adaptive perspective, texts. For example, animals of the same sex, weight, and limited plasticity is unexpected because heterogeneous en- population often differ consistently in their aggressive- vironments should favour the evolution of behavioural ness in different situations. This phenomenon has been plasticity rather than behavioural consistency [7,8]. Mean- referred to as behavioural syndromes [1-3] or animal while, personality and individual plasticity might also be personalities [4,5]. Behavioural syndromes are an attri- linked [9]. For example, studies on laboratory mice and bute of populations and cover rank-order differences rats show that aggressive behaviour is related to the way between individuals. A behavioural type, in contrast, animals cope with different situations. Non-aggressive describes the attributes of an individual and covers par- males seem to be more flexible in their behaviour during ticular configurations of behaviours that one individual environmental challenges compared to more aggressive expresses [1]. The presence of behavioural syndromes or males [10]. Although consistent differences in behaviour among individuals can be found in a wide range of species, * Correspondence: herde@uni-potsdam.de Department of Animal Ecology, University of Potsdam, Maulbeerallee 1, there is still not much knowledge about the origin and 14469 Potsdam, Germany the impact of personality or behavioural types. Some Department of Animal Behaviour, University of Bielefeld, Morgenbreede 45, studies indicate strong genetic bases for behavioural 33615 Bielefeld, Germany © 2013 Herde and Eccard; licensee BioMed Central Ltd. This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Herde and Eccard BMC Ecology 2013, 13:49 Page 2 of 10 http://www.biomedcentral.com/1472-6785/13/49 syndromes [11,12], others suggest that maternal effects the behaviour of individuals tested before and after mat- [13] might play a role, as well as life-history stage ad ex- uration would be less consistent compared to animals periences of the individual [3,5,7]. In particular, prior ex- tested in the same time interval as fully developed perience can influence the behaviour of an individual adults. Changes in endocrinological and neuronal sys- immediately and also later in life. For example, three- tems as well as new challenging environmental factors spined stickelbacks (Gasterosteus aculeatus) showed a like novel habitats and unfamiliar conspecifics can affect stronger behavioural correlation between aggressiveness this variation in behaviour [30,31]. and boldness after they had been exposed to a predator Contextual generality refers to ‘the extent to which [14]. Behavioural types affect the life-time reproductive scores for behaviour expressed in one context are corre- success of an individual and can be understood as a lated across individuals with scores for behaviour component of its life history [6,15-18]. Therefore it is expressed in one or more other contexts, when behav- crucial to understand ontogenetic development of ani- iour in all of the contexts is measured at the same age mal personality, whether and when during lifetime it de- and time’ [13,24]. We compared the different latencies velops, it becomes fixated, and how stable it is over an and activities measured in the four behavioural tests dur- individual’s life time. Studies on consistency over time in ing one week in adult animals (short term adult), to get birds [19,20] and insects [21-23] showed that stability an impression of a possible relationships between those and repeatability is variable for different behaviours and behaviours in common voles. We expect that measured also for the species under investigation. Hence, it cannot latencies and activities were linked to each other as it generally be assumed that consistent individual differ- has been found in other species (e.g. [10,32-35]). Pos- ences in behaviour are stable throughout life and a valid- sible behavioural syndrome axis in behaviour will be ation for different behaviours, life stages and species is shown in a dendrogram as the output of a cluster necessary. analyses. While consistency is the fundamental part of the def- inition of behavioural syndromes, many terms were used Methods for different types of consistency over time and over sit- Study system uations [24]. In this study we focussed on temporal The common vole (Microtus arvalis) is a widespread consistency, especially differential consistency, and con- fossorial rodent in Europe with a polygynandrous mating textual generality. Differential consistency refers to ‘the system. Females can share nests and form colonies with extent to which scores for behaviour in a given context sisters and/or daughters during lactation [36,37]. Fe- at a given time are correlated across individuals with males can give birth to several litters with 2–8 pups per scores for the same behaviour in the same context at a litter (mean 5.2) during one reproductive season [29]. later time’ [13,24] and can also be called repeatability. During winter, male antagonism decreases and animals We investigated the consistency over time in four behav- overwinter in mixed groups [38]. Weight of adult com- ioural tests (barrier-test, open-field, dark–light and nose- mon voles can vary between 18 to 40 g [29]. Active in-hole-test), and used common voles (Microtus arvalis) phases are distributed evenly over day and night in a 2– in different life stages as a model organism. We expect 3 hour circle with peaks in activity during twilight [39]. that the repeatability in behaviour of common voles is higher when interobservation interval is short, as it was Behavioural consistency over maturation shown for humans [25] and great tits (Parus major) The experiments of the ‘over maturation’-part of this [26,27]. It is more likely to test an animal in the same (e. study were conducted between January and July 2008 in g. reproductive) state within a short interobservation the facilities of the Department of Animal Behaviour of interval and the opportunity for developmental change the University of Bielefeld, Germany (52°02’10.72”N, 8° is high when the time between two tests is long [28]. 29’23.12”O). We used 17 laboratory-born common voles Here, we compared wild captured adult animals that (9 males, 8 females; Table 1), bred from originally wild were either tested twice within one week (‘adult short voles that were trapped in 2007 in Bielefeld. Animals term’) or a second time after a period of three month were kept in breeding rooms with light adjusted to sea- (‘adult long term’). The maximum life span of voles sonal day length Rooms were not heated except for frost (genera Microtus) is around 17 month [29] but due to periods to prevent freezing of water bottles. Animals massive predation all over the year and in every develop- were kept singly after being weaned from their mothers mental state, individuals often die much earlier. There- in standard makrolon cages (Ehret GmbH Germany, Typ fore, an interobservation interval of three month covers III: 42 cm × 27 cm × 16 cm), containing wood shavings, nearly a whole life span of a common vole. hay and paper rolls for shelter. Water and food pellets Since maturation is a sensitive phase during individual (Altromin international, Germany; standard laboratory development in many species, we further expected, that mice food) were available ad libitum. The first testing Herde and Eccard BMC Ecology 2013, 13:49 Page 3 of 10 http://www.biomedcentral.com/1472-6785/13/49 Table 1 Consistency over time in behaviour of common voles in four tests in three experimental groups Test Variable Definition Mean ± SD over maturation adult - short term adult - long term Nr pN r pN r p s s s Barrier Latency Latency to jump over barrier 44.51 ± 68.8 17 0.699 0.01 168 0.409 <0.01 48 0.122 1.00 (466) Activity 1-0 sampling every 10 sec. 19.43 ± 8.09 17 0.205 0.43 151 0.441 <0.01 41 0.561 <0.01 (418) Crossing frequency No. of crossing barrier per minute 2.64 ± 2.94 168 0.581 <0.01 48 0.636 0.03 (432) Open field Latency unsafe zone Latency to go in middle zone 132.19 ± 80.49 157 0.388 <0.01 47 0.229 1.00 (408) Activity 1-0 sampling every 10 sec. 19.96 ± 7.57 164 0.543 <0.01 47 0.515 0.05 (422) Time safe zone 1-0 sampling every 10 sec. 24.93 ± 5.51 164 0.354 <0.01 47 0.179 1.00 (422) Dark–light Latency into light Latency to go in light compartment 90.22 ± 169.54 164 0.572 <0.01 25 0.28 1.00 (378) Time in light Time spend in light zone [sec] 104.22 ± 161.9 164 0.388 <0.01 25 0.737 0.01 (378) Hole Latency one hole Latency to find one hole 86.66 ± 65.36 132 0.34 0.01 10 0.091 1.00 (284) Latency four holes Latency to find all four holes 237.32 ± 71.89 132 0.372 <0.01 10 0.119 1.00 (284) Number nose No. of nose-in-hole events 10.63 ± 6.89 132 0.558 <0.01 10 −0.031 1.00 (284) Mean ± standard deviation (SD) was calculated from all conducted tests. Number of conducted tests is given in parentheses. Spearman rank correlations coefficient (r ) was calculated between first and second testing. P-values were adjusted for multiple testing with Holm correction. Significant correlations are in bold (p < 0.05). period started when animals were 62 ± 20 days old and Lactating females and juveniles were immediately re- immature (visual inspection for closed vagina or abdom- leased at the trapping side. Animals were housed singly inal testes). Animals were habituated to the experimental at room temperature (15-25°C, changing with season) room (20-23°C and artificial lighting) two hours before and natural seasonal photoperiod in same cage- testing, and the barrier-test (description below) was con- conditions as described above immediately after trap- ducted under direct observation. This procedure was re- ping. Water and food pellets (ssniff V1594 R/M-H Ered peated in a second testing period 90 days later when all II) were available ad libitum and the diet was enriched animals had matured (open vagina or scrotal testes). with carrots, potatoes and fresh grass. Testing phases started 3–6 weeks after the animals were captured and all pregnant-captured females had given birth and had Behavioural consistency in adulthood weaned their young. Weanlings were released at the ori- The experiments on adult voles were conducted between ginal trapping side of the mother. April and November 2010 and February and September In 2010, 168 adult common voles (88 males, 80 fe- 2011 in the field station of the Department of Animal males; Table 1) were tested two times in four behav- Ecology of the University of Potsdam, Germany (52° ioural tests (description below) within one week to test 26’21.83”N, 13°00’44.14”O). the consistency of vole behaviour during a short period We captured 248 common voles with live traps (group ‘short term adult’). (Ugglan special No2, Grahnab, Sweden) from meadows Forty-eight adult common voles captured in 2010 around Potsdam. Traps were always baited with rolled (8 males, 21 females) and 2011 (11 males, 8 females; oats (as food) and apple (as water reserve) and were Table 1) were used to test the consistency of the behav- checked every 12 hours during trapping periods. iour over 2–3 months (group ‘long term adult’). All Captured, adult voles were brought to the laboratory. Herde and Eccard BMC Ecology 2013, 13:49 Page 4 of 10 http://www.biomedcentral.com/1472-6785/13/49 animals were tested once in the barrier-test and the “unsafe” for small mammals [42]. The animal was placed open-field (description below) 3–6 weeks after trapping. in the middle of the arena in a tube. The tube was lifted Afterwards, the animals were marked individually with and the test duration of 5 minutes started at the mo- a unique passive integrated transponder (‘PIT’;Trovan ment the vole reached the wall of the arena the first ID-100; 2.12 mm × 11.5 mm, 0.1 g) implanted at the time. Latency to re-enter the “unsafe” middle of the neck. We found no evidence for negative effects of the arena was measured. If animals did not move to the un- implantation on the animals. Marked voles were trans- safe zone within 5 minutes, latency was set to the max- ferred to 0.25 ha outdoor enclosures with natural vege- imum of 300 seconds (15.2% of all performed test). In tation and natural avian predation (enclosures were not addition, activity (max. 30 active samples) and time in netted) in groups of 8 animals (4 males, 4 females) per the safe wall zone of the arena (max. 30 samples in the enclosure. After 5–6 weeks, we trapped the voles back safe area) were recorded with instantaneous 1-0- from the enclosures. Voles were transferred to the la- sampling every 10 seconds. boratory again and were tested a second round in barrier-test and open-field 3–6 weeks later. Dark–light-test A black plastic box (30 cm × 30 cm × 15 cm) with an Behavioural tests entrance hole (4 cm × 5 cm) was placed upside down For the behavioural testing, we modified standard la- into a larger white plastic box (65 cm × 50 cm × 30 cm). boratory tests that were originally used to test emotion- The animal was placed in the black box and the latency ality or fearfulness in mice and rats, which are now to come out of the dark (‘latency into light’) and the commonly used in studies on behavioural syndromes in time to go back (‘time in light’) in a maximum time of other species [4]. We adjusted the set-ups of the barrier- 10 minutes were measured. If animals did not leave the test [40,41], open-field test [42] and dark–light-test [43] dark box within 10 minutes, latency was set to the max- for the needs and skills of non-climbing, subterranean, imum of 600 seconds (8.99% of all performed tests). wild-captured voles. In addition, we invented the nose- in-hole-test (similar to hole-board test in [33]; thereafter Hole-test called hole-test) to investigate exploration behaviour. A vole was placed in the middle of a standard makrolon Variables that were tested reflect mainly boldness, ex- cage (like housing cage, without bedding) with 4 holes ploration and activity of the tested animals. Tests were (1 cm diameter in 1 cm height), one in each corner. directly observed between 0800 and 1800 hours with a Over 5 minutes, the latency to first ‘nose-in-hole’-event, minimum of two hours rest for the animals between the latency to explore all 4 holes, and the total number tests. of nose-in-hole-events (thereafter called ‘number holes’) were measured. If animals did not stick its nose in a hole Barrier-test within 5 minutes, latency was set to the maximum of A semi-transparent plastic box (45 cm × 22 cm × 300 seconds (4.55% of all performed tests). The same 25 cm) was divided into two equal compartments by a was true if they did not discover all 4 holes within the 4.5 cm high barrier (grey PVC). According to a pseudo- test period (44.72% of all performed tests). random schedule, the animal was placed in one of the compartments and the latency was measured until the Statistical methods animal crossed the barrier from one compartment to the Many measured variables were distributed in a skewed other. If animals did not jump over the barrier within manner (a few similar to bimodal distributions) rather 5 minutes,% latency was set to the maximum of 300 sec- than a normal one (Kolmogorow-Smirnow-test). There- onds (2.58% of all performed tests). The activity of the fore, we mainly used non-parametric statistics. Compari- animal was recorded every 10 seconds with instantan- sons between experimental groups were calculated with eous 1-0-sampling (max. 30 active samples). Addition- Kruskal-Wallis-test and accordingly between testing ally, the number of crossings was counted for all adult rounds with Wilcoxon-signed-rank-test. Sex differences individuals (in 2010 and 2011). The variable ‘crossing were tested with Mann–Whitney-U-test. Spearman rank frequency’ (crossings per minute during time interval left order correlations were used to test for consistency of after substraction of latency) was calculated for the behaviours in two consecutive tests, thereby avoiding the analyses. problem of mean level changes due to habituation. Cor- relations were compared between the three experimental Open-field groups or sexes (only for adult animals, sample size of We used a round metal arena (1 m diameter, wall 35 cm over maturation group was too small to divide by sex) high) as an open-field with a safe wall zone (20 cm wide) with z-test. Variables with significant correlation coeffi- and an middle zone, that is known to be perceived as cients between first and second tests in the ‘short term Herde and Eccard BMC Ecology 2013, 13:49 Page 5 of 10 http://www.biomedcentral.com/1472-6785/13/49 adult’-group were included in analyses of behavioural (Spearman rank correlations, all r > 0.34, all p < 0.001; types. P-values were adjusted for multiple testing by details of correlation, mean and SD present in Table 1). using a Holm correction [44]. The results for the other two groups were less consistent For barrier-test variables ‘activity’ and ‘latency’ repeat- (Table 1). For the animals tested ‘over maturation’ corre- ability was separately calculated as intraclass correlation lations between the first and second round were found coefficient (ANOVA-based repeatability; R ) for the in the latency of the barrier test (r = 0.699, p = 0.001) A s three experimental groups. Barrier-test ‘latency’ was but not its activity (r = 0.205, p = 0.43). The ‘long term log10-transformed to obtain normally distributed data; adult’-voles showed repeatable behaviour in activity of ‘activity’ was normally distributed. As described in Lessells the barrier-test (‘activity’ and ‘crossing frequency’), &Boag [45], R was based on variance components open-field (‘activity’)and dark–light-test (‘time in light’) from a one-way ANOVA with individual as a factor and (all r > 0.515, all p <0.05), but not in latency variables each variable as dependent variable. Its standard errors of the same tests. In the hole-test, no variable was con- were tested with R-package ‘rptR’ following Nakawaga & sistent over time for this group. Schielzeth [46]. In the barrier-test we found no difference between the To identify possible associations among behavioural three experimental groups (Kruskal-Wallis test by group: variables, we calculated a Spearman rank correlation latency round1 Chi = 2.733, df = 2, p = 0.255; round 2 2 2 matrix among all variables from all behavioural tests Chi = 2.9288, df = 2, p = 0.2312; activity round 1 Chi = from the first testing round of the ‘short term adult’- 2.9525, df = 2, p = 0.229; round 2 Chi = 0.8214, df = 2, p = group (see Additional file 1). We computed an agglom- 0.6632) but latency was significantly lower in the second erative cluster analysis with the ‘cluster’ package and the testing round than in the first for the two groups with ‘agnes’ function of the R statistical environment with adult animals if compared within individuals (Wilcoxon ‘manhattan’ clustering with complete linkage, similar to signed rank test: short term adult V = 10107, N = 168, Gyuris et al. [47] and Tremmel & Müller [35]. The re- p < 0.001; long term adult V = 871, N = 48, p = 0.001; sults of the cluster analysis are shown by a dendrogram, Figure 1A) and activity was reduced (short term adult which lists all of the variables and indicates at what level V = 5638, N = 151, p = 0.021; long term adult V = 595.5, of similarity any two clusters were joined (‘height’). The N = 41, p = 0.004), Both was not the case in the animals height of the link (‘U’) represents the distance between that were tested over maturation (latency: V = 110, N = 17, the two clusters that contain those objects, i.e. the p = 0.118; activity: V = 47, N = 17, p = 0.477). shorter the U the more similar the variables are to each Measured latency in barrier-test was repeatable for voles other. that were tested before and after maturation (R =0.63, All analyses were carried out with R 2.14 (The R SE = 0.148, N = 17, p = 0.002) and over one week as adults Foundation for Statistical Computing, Vienna, Austria, (R = 0.27, SE = 0.072, N = 149, p < 0.001), but not for http://www.R-project.org). Values of p were two tailed adults that were tested after three months (R = 0.045, throughout and the accepted significance level was p < 0.05. SE = 0.145, N = 41, p = 0.379) (Figure 2). Repeatability of activity in the barrier-test showed the opposite pattern: Ethical standards animals that were tested over adolescence showed no con- In 2008 all animals were housed and all experiments were sistent activity (R = 0.258, SE = 0.23, N = 17, p = 0,145), conducted under permission of the Landesamt für Natur, whereas all tested adults were consistently active, both Umwelt und Verbraucherschutz Nordrhein-Westfalen over one week (R = 0.387, SE = 0.069, N = 166, p < 0.001) (reference number 9.93.2.10.42.07.069). All animals in and three months (R = 0.457, 0.118, N = 48, p < 0.001) 2010 and 2011 were captured under permission of the (Figure 2). These results were supported by correlations Landesumweltamt Brandenburg (reference number RW- presented in Table 1. 7.1 24.01.01.10). Experiments in 2010 and 2011 were con- ducted under the permission of the Landesamt für Consistency over situations Umwelt, Gesundheit und Verbraucherschutz Brandenburg On the basis of the correlation matrix (see Additional (reference number V3-2347-44-2011). After the experi- file 1) and the calculated cluster analysis on the mea- ments, the animals either stayed in the laboratory for fur- sured variables of the ‘short term adult’-group, three ther experiments, or were released at the original trapping clusters with following variables can be described as pos- site, as specified in the trapping permissions. sible structures of behavioural syndromes (Figure 3): 1. barrier latency, dark–light latency into light, and open- Results field latency and time safe zone; 2. hole latency for one Consistency over time and four holes; 3. barrier crossing frequency and activity, All behavioural variables in the ‘short-term adult’ group open-field activity, dark–light time in light and number were highly correlated between the first and second test of nose-in-hole events. The variables in the first arm Herde and Eccard BMC Ecology 2013, 13:49 Page 6 of 10 http://www.biomedcentral.com/1472-6785/13/49 AB Over Short Term Long Term Over Short Term Long Term Maturation Adult Adult Maturation Adult Adult Figure 1 Comparison between first and second barrier-test within experimental groups of common voles. A) Barrier Latency [sec], B) Barrier Activity [1-0-sampling]. Significant differences in Wilcoxon signed rank test were indicated by stars. represent latency measures. They might be considered barrier and stayed in the safe zone of the open-field as a kind of shy-bold axis of common voles behavioural arena for a shorter time, compared to their shyer conspe- syndromes, which we have called ‘boldness’. The bolder cifics Close to this cluster is a second arm which includes animals entered the unsafe zone in the open-field and latencies only of the hole-test. The faster a vole sticks its the dark–light-test earlier, jumped earlier over the head through the holes, the more explorative the animal 0.0 0.5 1.0 1.5 2.0 2.5 0 5 10 15 20 25 30 Barrier Activity 1 Barrier log-Latency 1 Figure 2 Correlation between behavioural variables measured in first and second barrier-test. Latency (left side; range 0–300 sec.) and activity (right side; max. 30 active samples) for each of the three experimental groups of tested common voles are shown. Correlations coefficient (r ) and p-values for correlations are represented in Table 1. Lines indicate significant correlations (p < 0.05; adjusted for multiple testing). BarrierLatency Long Term Adult Short Term Adult Over Maturation log-Latency 2 log-Latency 2 log-Latency 2 0.0 0.5 1.0 1.5 2.0 2.5 0.0 0.5 1.0 1.5 2.0 2.5 0.0 0.5 1.0 1.5 2.0 2.5 BarrierActivity Activity 2 Activity 2 Activity 2 0 5 10 15 20 25 30 0 5 10 15 20 25 30 0 510 15 20 25 30 Herde and Eccard BMC Ecology 2013, 13:49 Page 7 of 10 http://www.biomedcentral.com/1472-6785/13/49 1 3 Figure 3 Dendrogram for the relationships between measured variables in the ‘short term adult’-group (N = 168) according to the cluster analysis. Height of each U represents the distance between two variables and is based on correlation coefficients of Spearman correlation matrix (see Additional file 1). Groupings indicate possible behavioural syndrome structure (agglomerative coefficient 0.64). is. Therefore, those latencies are associated with explor- Since rank order of scores is maintained across con- ation behaviour and are closely related to the boldness texts in adult animals, i.e. all activities and according la- variables. Thus, we called both clusters together ‘bold- tencies form one arm of the dendrogram (Figure 3), ness/exploration’-axes. The third cluster is more uniform, contextual generality was high [24]. With a combination it contains all measured activities of all tests and can of activity and boldness/exploration as dimensions of be- therefore be named ‘activity’-cluster. Animals that are ac- havioural syndromes we obtained results very similar to tive in the open-field are also the more active ones in the studies in voles and other small mammals. Lantová et al. barrier-test. They jumped over the barrier more often and [38] also found a connection between activity and bold- spent more time in light. ness in different behavioural tests in a captive common There were also indications for a connection between vole population. Similar axes can also be seen in grey boldness and the activity clusters. Common voles which mouse lemurs (Mircrocebus murinus) [32] and Siberian had, for example, short latencies to enter the unsafe chipmunks (Tamias sibiricus) [48] in wild populations. zone in the open-field, did also jump at the barrier at Other vole species showed consistent individual differ- higher frequency, i.e. show higher activity (Spearman ences in activity (meadow vole (Microtus pennsylvanicus rank correlation r = −0.327, N = 164, p < 0.01). [49]; root voles M. oeconomus) [50]) like adult animals in our study. Therefore, it can be assumed that boldness and activity are very common personality axis in small Sex differences mammals. Sex differences were found only in barrier and open-field As predicted, the length of the interobservation inter- activity where male common voles where more active val had an influence on the repeatability of behaviours in than females (barrier activity: males 21 ± 8, females 19 ± 8 common voles. Animals that were tested over intervals active samples; Mann–Whitney-U = 2249.0, N = 151, of three months, over maturation or as adults, showed p = 0.026; open-field activity: males 22 ± 7, females 19 ± 8 less consistent behaviours than animals tested twice dur- active samples, Mann–Whitney-U = 2602.5, N = 164, ing one week (Table 1). Surprisingly, activity and bold- p = 0.014). In all other behaviours males and females ness/exploration behaviour differed in their behavioural behaved equally. Comparison of Spearman correla- consistency, depending on the age of the tested animal. tions that were calculated separately for adult males This may possibly be explained by differences in experi- and females showed no difference in consistency over ences, their expected life span, or developmental change time between sexes (z-test, all p > 0.3). such as maturation. Young voles tested over maturation lived in stable cap- tive conditions before and over the experiment. They Discussion had stable latencies while exploring the barrier-test but Our results demonstrate the presence of behavioural syndromes in common voles (Microtus arvalis). We do not show repeatable activity. It is possible that the la- boratory environment with limited space for experien- showed that behaviour in different tests was consistent cing or exercising movement did not stimulate the over time (Figure 2) and over situations (Figure 3). height 135 7 Barrier latency Dark-light latency into light Open-field latency Open-field time safe zone Hole latency one hole Hole latency four holes Barrier crossing frequency Barrier activity Open-field activity Dark-light time in light Hole number nose Herde and Eccard BMC Ecology 2013, 13:49 Page 8 of 10 http://www.biomedcentral.com/1472-6785/13/49 formation of stable activity types. We compared captive future assets (Figure 1). Studies on field crickets (Gryllus bred animals with wild caught ones in this study by the integer) [21] and grey mouse lemurs [32] support that a reason that adequate age estimation is not possible in trade-off between current and future reproduction can wild-caught voles and immature young voles were diffi- lead to personality variation. To investigate why behaviour cult to trap in nature. Due to habituation to captive con- of common voles is not adjusted like predicted in the asset ditions and lower diversity of situations one could protection theory, the differences in behaviour between expect that captive animals show even more stable be- young and older voles should be observed in natural pop- haviours [51] but Bell et al. [28] found repeatability of ulations with fluctuating densities and active competition. behaviour was higher when measured under natural The differences in differential consistency in the three conditions. Besides, another reason for the missing experimental groups suggest that the link of activity and consistency over time is that some effects cannot be de- boldness/exploration can be decoupled during ontogeny. tected with small sample sizes. To proof this result on in- This makes sense when environmental conditions expe- consistency in boldness in more natural conditions (e.g. in rienced by juveniles differ substantially from those expe- monitored outdoor enclosures) and with a larger sample rienced by adults [3], particularly in traits that are more size would be challenging for future studies. sensitive to the environment (e.g. behavioural traits like Adult voles captured from the wild and maintained in activity or boldness) compared to morphological or semi-wild outdoor enclosures, showed repeatability in physiological traits [28]. In voles, annual population dy- boldness/exploration behaviour only over a short period namics with different conditions depending on the sea- of time, but less so over three months. In contrast activ- son of birth are typical: Animals that were born in ity patterns were stable, which is surprising because ac- spring/summer mature at an age of weeks, whereas indi- tivity has been reported as one of the least repeatable viduals born in late summer/autumn overwinter as im- behaviours [28] (but see [34]). It could be that explor- matures and start reproduction in the following spring ation and boldness can be adapted more easily to at an age of months [56-59]. During seasons not only current environmental conditions like predator presence environmental conditions change (e.g. density, food or food availability, which may have differed between availability) but also asset protection should play a role conditions in the wild, which animals experienced prior in development of behavioural traits, like discussed to the first testing and in the enclosures, prior to the above and elsewhere [60]. Therefore, the importance of second testing. Experiences can either enhance stability studies in natural conditions should not be neglected. It by reinforcing a package of traits, or experiences may is likely that especially young individuals could show dif- modify behavioural types [3]. In a small prey animal, like ferent development of behavioural traits in unstable or the common vole, this flexibility could be very important heterogeneous environments. Environmental conditions to survive in the wild where force trade-offs between, for affect both life history [61] and behavioural type expres- instance, exploring resources and avoiding predators. sion [15,62], and future studies should consider both. This flexibility is less important in the laboratory where Male common voles were more active in two of four conditions were stable. We suggest that activity pat- tests than females. The voles’ breeding system with pro- terns were developed after maturation as we could not miscuously mating females may explain this difference see them in young animals but in adults. Studies on as discussed in Eccard & Herde [60]. Differences in killifish (Kryptolebias marmoratus) [52] and Sibirian consistency over time between the sexes were not found dwarf hamsters (Phodopus sungorus) [34] showed also although this would not be unexpected as this was found an age effect on behavioural types and developmental in two bird species [12,63]. flexibility while damselflies (Lestes congener)showde- velopmental consistency in boldness and activity per- taining through metamorphosis [53]. Conclusions Current theoretical models discuss that differences in Common voles showed consistent individual differences state in combination with state-dependent behaviour can in their behaviour. Over short periods, repeatability as explain stable differences in behavioural traits [54]. For well as contextual generality was high. Over longer pe- example, animals should differ in their risk-taking be- riods, long in relation to the animals’ life span, stability haviour if they do either focus on current or on future of traits may be dependent of life stage of the animal reproduction. Individuals with expected low future re- but also external factors like stability of the surround- productive success (i.e. low asset) should take more risk ing environment. The research on animal personality as they have not much to lose [32,54,55]. Meanwhile, in and behavioural syndromes requires longitudinal stud- our study, juvenile voles, that should have high assets to ies (e.g. capture-mark-recapture) to follow the variation protect, did not have lower boldness or higher activity in behaviour and its consistency over a life span under scores compared to adult animals with expected lower natural conditions [13]. Herde and Eccard BMC Ecology 2013, 13:49 Page 9 of 10 http://www.biomedcentral.com/1472-6785/13/49 Additional file 13. Stamps JA, Groothuis TGG: Developmental perspectives on personality: implications for ecological and evolutionary studies of individual differences. Phil Trans R Soc B 2010, 365(1560):4029–4041. Additional file 1: Spearman correlation matrix of first testing round 14. Bell AM, Sih A: Exposure to predation generates personality in three- for all measured variables in the ‘short term adult’-group. spined sticklebacks (Gasterosteus aculeatus). Ecol Lett 2007, 10(9):828–834. 15. Boon AK, Reale D, Boutin S: The interaction between personality, offspring fitness and food abundance in North American red squirrels. Abbreviations Ecol Lett 2007, 10(11):1094–1104. PIT: Passive integrated transponder; ANOVA: Analysis of Variance; R : ANOVA- 16. Dingemanse NJ, Reale D: Natural selection and animal personality. 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Anim Behav 2009, 77(5):1041–1050. • Immediate publication on acceptance doi:10.1186/1472-6785-13-49 • Inclusion in PubMed, CAS, Scopus and Google Scholar Cite this article as: Herde and Eccard: Consistency in boldness, activity and exploration at different stages of life. BMC Ecology 2013 13:49. • Research which is freely available for redistribution Submit your manuscript at www.biomedcentral.com/submit http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png BMC Ecology Springer Journals

Consistency in boldness, activity and exploration at different stages of life

BMC Ecology , Volume 13 (1) – Dec 7, 2013

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Copyright © 2013 by Herde and Eccard; licensee BioMed Central Ltd.
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Life Sciences; Ecology; Life Sciences, general
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1472-6785
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24314274
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Abstract

Background: Animals show consistent individual behavioural patterns over time and over situations. This phenomenon has been referred to as animal personality or behavioural syndromes. Little is known about consistency of animal personalities over entire life times. We investigated the repeatability of behaviour in common voles (Microtus arvalis) at different life stages, with different time intervals, and in different situations. Animals were tested using four behavioural tests in three experimental groups: 1. before and after maturation over three months, 2. twice as adults during one week, and 3. twice as adult animals over three months, which resembles a substantial part of their entire adult life span of several months. Results: Different behaviours were correlated within and between tests and a cluster analysis showed three possible behavioural syndrome-axes, which we name boldness, exploration and activity. Activity and exploration behaviour in all tests was highly repeatable in adult animals tested over one week. In animals tested over maturation, exploration behaviour was consistent whereas activity was not. Voles that were tested as adults with a three-month interval showed the opposite pattern with stable activity but unstable exploration behaviour. Conclusions: The consistency in behaviour over time suggests that common voles do express stable personality over short time. Over longer periods however, behaviour is more flexible and depending on life stage (i.e. tested before/ after maturation or as adults) of the tested individual. Level of boldness or activity does not differ between tested groups and maintenance of variation in behavioural traits can therefore not be explained by expected future assets as reported in other studies. Keywords: Animal personality, Behavioural type, Microtus arvalis, Common vole, Plasticity, Consistency, Repeatability Background types and the connection between different behaviours in There has been increasing interest in consistent differ- a variety of contexts mean that an individual’s behaviour is ences in individual behaviour across time and/or con- not infinitely flexible [6]. From an adaptive perspective, texts. For example, animals of the same sex, weight, and limited plasticity is unexpected because heterogeneous en- population often differ consistently in their aggressive- vironments should favour the evolution of behavioural ness in different situations. This phenomenon has been plasticity rather than behavioural consistency [7,8]. Mean- referred to as behavioural syndromes [1-3] or animal while, personality and individual plasticity might also be personalities [4,5]. Behavioural syndromes are an attri- linked [9]. For example, studies on laboratory mice and bute of populations and cover rank-order differences rats show that aggressive behaviour is related to the way between individuals. A behavioural type, in contrast, animals cope with different situations. Non-aggressive describes the attributes of an individual and covers par- males seem to be more flexible in their behaviour during ticular configurations of behaviours that one individual environmental challenges compared to more aggressive expresses [1]. The presence of behavioural syndromes or males [10]. Although consistent differences in behaviour among individuals can be found in a wide range of species, * Correspondence: herde@uni-potsdam.de Department of Animal Ecology, University of Potsdam, Maulbeerallee 1, there is still not much knowledge about the origin and 14469 Potsdam, Germany the impact of personality or behavioural types. Some Department of Animal Behaviour, University of Bielefeld, Morgenbreede 45, studies indicate strong genetic bases for behavioural 33615 Bielefeld, Germany © 2013 Herde and Eccard; licensee BioMed Central Ltd. This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Herde and Eccard BMC Ecology 2013, 13:49 Page 2 of 10 http://www.biomedcentral.com/1472-6785/13/49 syndromes [11,12], others suggest that maternal effects the behaviour of individuals tested before and after mat- [13] might play a role, as well as life-history stage ad ex- uration would be less consistent compared to animals periences of the individual [3,5,7]. In particular, prior ex- tested in the same time interval as fully developed perience can influence the behaviour of an individual adults. Changes in endocrinological and neuronal sys- immediately and also later in life. For example, three- tems as well as new challenging environmental factors spined stickelbacks (Gasterosteus aculeatus) showed a like novel habitats and unfamiliar conspecifics can affect stronger behavioural correlation between aggressiveness this variation in behaviour [30,31]. and boldness after they had been exposed to a predator Contextual generality refers to ‘the extent to which [14]. Behavioural types affect the life-time reproductive scores for behaviour expressed in one context are corre- success of an individual and can be understood as a lated across individuals with scores for behaviour component of its life history [6,15-18]. Therefore it is expressed in one or more other contexts, when behav- crucial to understand ontogenetic development of ani- iour in all of the contexts is measured at the same age mal personality, whether and when during lifetime it de- and time’ [13,24]. We compared the different latencies velops, it becomes fixated, and how stable it is over an and activities measured in the four behavioural tests dur- individual’s life time. Studies on consistency over time in ing one week in adult animals (short term adult), to get birds [19,20] and insects [21-23] showed that stability an impression of a possible relationships between those and repeatability is variable for different behaviours and behaviours in common voles. We expect that measured also for the species under investigation. Hence, it cannot latencies and activities were linked to each other as it generally be assumed that consistent individual differ- has been found in other species (e.g. [10,32-35]). Pos- ences in behaviour are stable throughout life and a valid- sible behavioural syndrome axis in behaviour will be ation for different behaviours, life stages and species is shown in a dendrogram as the output of a cluster necessary. analyses. While consistency is the fundamental part of the def- inition of behavioural syndromes, many terms were used Methods for different types of consistency over time and over sit- Study system uations [24]. In this study we focussed on temporal The common vole (Microtus arvalis) is a widespread consistency, especially differential consistency, and con- fossorial rodent in Europe with a polygynandrous mating textual generality. Differential consistency refers to ‘the system. Females can share nests and form colonies with extent to which scores for behaviour in a given context sisters and/or daughters during lactation [36,37]. Fe- at a given time are correlated across individuals with males can give birth to several litters with 2–8 pups per scores for the same behaviour in the same context at a litter (mean 5.2) during one reproductive season [29]. later time’ [13,24] and can also be called repeatability. During winter, male antagonism decreases and animals We investigated the consistency over time in four behav- overwinter in mixed groups [38]. Weight of adult com- ioural tests (barrier-test, open-field, dark–light and nose- mon voles can vary between 18 to 40 g [29]. Active in-hole-test), and used common voles (Microtus arvalis) phases are distributed evenly over day and night in a 2– in different life stages as a model organism. We expect 3 hour circle with peaks in activity during twilight [39]. that the repeatability in behaviour of common voles is higher when interobservation interval is short, as it was Behavioural consistency over maturation shown for humans [25] and great tits (Parus major) The experiments of the ‘over maturation’-part of this [26,27]. It is more likely to test an animal in the same (e. study were conducted between January and July 2008 in g. reproductive) state within a short interobservation the facilities of the Department of Animal Behaviour of interval and the opportunity for developmental change the University of Bielefeld, Germany (52°02’10.72”N, 8° is high when the time between two tests is long [28]. 29’23.12”O). We used 17 laboratory-born common voles Here, we compared wild captured adult animals that (9 males, 8 females; Table 1), bred from originally wild were either tested twice within one week (‘adult short voles that were trapped in 2007 in Bielefeld. Animals term’) or a second time after a period of three month were kept in breeding rooms with light adjusted to sea- (‘adult long term’). The maximum life span of voles sonal day length Rooms were not heated except for frost (genera Microtus) is around 17 month [29] but due to periods to prevent freezing of water bottles. Animals massive predation all over the year and in every develop- were kept singly after being weaned from their mothers mental state, individuals often die much earlier. There- in standard makrolon cages (Ehret GmbH Germany, Typ fore, an interobservation interval of three month covers III: 42 cm × 27 cm × 16 cm), containing wood shavings, nearly a whole life span of a common vole. hay and paper rolls for shelter. Water and food pellets Since maturation is a sensitive phase during individual (Altromin international, Germany; standard laboratory development in many species, we further expected, that mice food) were available ad libitum. The first testing Herde and Eccard BMC Ecology 2013, 13:49 Page 3 of 10 http://www.biomedcentral.com/1472-6785/13/49 Table 1 Consistency over time in behaviour of common voles in four tests in three experimental groups Test Variable Definition Mean ± SD over maturation adult - short term adult - long term Nr pN r pN r p s s s Barrier Latency Latency to jump over barrier 44.51 ± 68.8 17 0.699 0.01 168 0.409 <0.01 48 0.122 1.00 (466) Activity 1-0 sampling every 10 sec. 19.43 ± 8.09 17 0.205 0.43 151 0.441 <0.01 41 0.561 <0.01 (418) Crossing frequency No. of crossing barrier per minute 2.64 ± 2.94 168 0.581 <0.01 48 0.636 0.03 (432) Open field Latency unsafe zone Latency to go in middle zone 132.19 ± 80.49 157 0.388 <0.01 47 0.229 1.00 (408) Activity 1-0 sampling every 10 sec. 19.96 ± 7.57 164 0.543 <0.01 47 0.515 0.05 (422) Time safe zone 1-0 sampling every 10 sec. 24.93 ± 5.51 164 0.354 <0.01 47 0.179 1.00 (422) Dark–light Latency into light Latency to go in light compartment 90.22 ± 169.54 164 0.572 <0.01 25 0.28 1.00 (378) Time in light Time spend in light zone [sec] 104.22 ± 161.9 164 0.388 <0.01 25 0.737 0.01 (378) Hole Latency one hole Latency to find one hole 86.66 ± 65.36 132 0.34 0.01 10 0.091 1.00 (284) Latency four holes Latency to find all four holes 237.32 ± 71.89 132 0.372 <0.01 10 0.119 1.00 (284) Number nose No. of nose-in-hole events 10.63 ± 6.89 132 0.558 <0.01 10 −0.031 1.00 (284) Mean ± standard deviation (SD) was calculated from all conducted tests. Number of conducted tests is given in parentheses. Spearman rank correlations coefficient (r ) was calculated between first and second testing. P-values were adjusted for multiple testing with Holm correction. Significant correlations are in bold (p < 0.05). period started when animals were 62 ± 20 days old and Lactating females and juveniles were immediately re- immature (visual inspection for closed vagina or abdom- leased at the trapping side. Animals were housed singly inal testes). Animals were habituated to the experimental at room temperature (15-25°C, changing with season) room (20-23°C and artificial lighting) two hours before and natural seasonal photoperiod in same cage- testing, and the barrier-test (description below) was con- conditions as described above immediately after trap- ducted under direct observation. This procedure was re- ping. Water and food pellets (ssniff V1594 R/M-H Ered peated in a second testing period 90 days later when all II) were available ad libitum and the diet was enriched animals had matured (open vagina or scrotal testes). with carrots, potatoes and fresh grass. Testing phases started 3–6 weeks after the animals were captured and all pregnant-captured females had given birth and had Behavioural consistency in adulthood weaned their young. Weanlings were released at the ori- The experiments on adult voles were conducted between ginal trapping side of the mother. April and November 2010 and February and September In 2010, 168 adult common voles (88 males, 80 fe- 2011 in the field station of the Department of Animal males; Table 1) were tested two times in four behav- Ecology of the University of Potsdam, Germany (52° ioural tests (description below) within one week to test 26’21.83”N, 13°00’44.14”O). the consistency of vole behaviour during a short period We captured 248 common voles with live traps (group ‘short term adult’). (Ugglan special No2, Grahnab, Sweden) from meadows Forty-eight adult common voles captured in 2010 around Potsdam. Traps were always baited with rolled (8 males, 21 females) and 2011 (11 males, 8 females; oats (as food) and apple (as water reserve) and were Table 1) were used to test the consistency of the behav- checked every 12 hours during trapping periods. iour over 2–3 months (group ‘long term adult’). All Captured, adult voles were brought to the laboratory. Herde and Eccard BMC Ecology 2013, 13:49 Page 4 of 10 http://www.biomedcentral.com/1472-6785/13/49 animals were tested once in the barrier-test and the “unsafe” for small mammals [42]. The animal was placed open-field (description below) 3–6 weeks after trapping. in the middle of the arena in a tube. The tube was lifted Afterwards, the animals were marked individually with and the test duration of 5 minutes started at the mo- a unique passive integrated transponder (‘PIT’;Trovan ment the vole reached the wall of the arena the first ID-100; 2.12 mm × 11.5 mm, 0.1 g) implanted at the time. Latency to re-enter the “unsafe” middle of the neck. We found no evidence for negative effects of the arena was measured. If animals did not move to the un- implantation on the animals. Marked voles were trans- safe zone within 5 minutes, latency was set to the max- ferred to 0.25 ha outdoor enclosures with natural vege- imum of 300 seconds (15.2% of all performed test). In tation and natural avian predation (enclosures were not addition, activity (max. 30 active samples) and time in netted) in groups of 8 animals (4 males, 4 females) per the safe wall zone of the arena (max. 30 samples in the enclosure. After 5–6 weeks, we trapped the voles back safe area) were recorded with instantaneous 1-0- from the enclosures. Voles were transferred to the la- sampling every 10 seconds. boratory again and were tested a second round in barrier-test and open-field 3–6 weeks later. Dark–light-test A black plastic box (30 cm × 30 cm × 15 cm) with an Behavioural tests entrance hole (4 cm × 5 cm) was placed upside down For the behavioural testing, we modified standard la- into a larger white plastic box (65 cm × 50 cm × 30 cm). boratory tests that were originally used to test emotion- The animal was placed in the black box and the latency ality or fearfulness in mice and rats, which are now to come out of the dark (‘latency into light’) and the commonly used in studies on behavioural syndromes in time to go back (‘time in light’) in a maximum time of other species [4]. We adjusted the set-ups of the barrier- 10 minutes were measured. If animals did not leave the test [40,41], open-field test [42] and dark–light-test [43] dark box within 10 minutes, latency was set to the max- for the needs and skills of non-climbing, subterranean, imum of 600 seconds (8.99% of all performed tests). wild-captured voles. In addition, we invented the nose- in-hole-test (similar to hole-board test in [33]; thereafter Hole-test called hole-test) to investigate exploration behaviour. A vole was placed in the middle of a standard makrolon Variables that were tested reflect mainly boldness, ex- cage (like housing cage, without bedding) with 4 holes ploration and activity of the tested animals. Tests were (1 cm diameter in 1 cm height), one in each corner. directly observed between 0800 and 1800 hours with a Over 5 minutes, the latency to first ‘nose-in-hole’-event, minimum of two hours rest for the animals between the latency to explore all 4 holes, and the total number tests. of nose-in-hole-events (thereafter called ‘number holes’) were measured. If animals did not stick its nose in a hole Barrier-test within 5 minutes, latency was set to the maximum of A semi-transparent plastic box (45 cm × 22 cm × 300 seconds (4.55% of all performed tests). The same 25 cm) was divided into two equal compartments by a was true if they did not discover all 4 holes within the 4.5 cm high barrier (grey PVC). According to a pseudo- test period (44.72% of all performed tests). random schedule, the animal was placed in one of the compartments and the latency was measured until the Statistical methods animal crossed the barrier from one compartment to the Many measured variables were distributed in a skewed other. If animals did not jump over the barrier within manner (a few similar to bimodal distributions) rather 5 minutes,% latency was set to the maximum of 300 sec- than a normal one (Kolmogorow-Smirnow-test). There- onds (2.58% of all performed tests). The activity of the fore, we mainly used non-parametric statistics. Compari- animal was recorded every 10 seconds with instantan- sons between experimental groups were calculated with eous 1-0-sampling (max. 30 active samples). Addition- Kruskal-Wallis-test and accordingly between testing ally, the number of crossings was counted for all adult rounds with Wilcoxon-signed-rank-test. Sex differences individuals (in 2010 and 2011). The variable ‘crossing were tested with Mann–Whitney-U-test. Spearman rank frequency’ (crossings per minute during time interval left order correlations were used to test for consistency of after substraction of latency) was calculated for the behaviours in two consecutive tests, thereby avoiding the analyses. problem of mean level changes due to habituation. Cor- relations were compared between the three experimental Open-field groups or sexes (only for adult animals, sample size of We used a round metal arena (1 m diameter, wall 35 cm over maturation group was too small to divide by sex) high) as an open-field with a safe wall zone (20 cm wide) with z-test. Variables with significant correlation coeffi- and an middle zone, that is known to be perceived as cients between first and second tests in the ‘short term Herde and Eccard BMC Ecology 2013, 13:49 Page 5 of 10 http://www.biomedcentral.com/1472-6785/13/49 adult’-group were included in analyses of behavioural (Spearman rank correlations, all r > 0.34, all p < 0.001; types. P-values were adjusted for multiple testing by details of correlation, mean and SD present in Table 1). using a Holm correction [44]. The results for the other two groups were less consistent For barrier-test variables ‘activity’ and ‘latency’ repeat- (Table 1). For the animals tested ‘over maturation’ corre- ability was separately calculated as intraclass correlation lations between the first and second round were found coefficient (ANOVA-based repeatability; R ) for the in the latency of the barrier test (r = 0.699, p = 0.001) A s three experimental groups. Barrier-test ‘latency’ was but not its activity (r = 0.205, p = 0.43). The ‘long term log10-transformed to obtain normally distributed data; adult’-voles showed repeatable behaviour in activity of ‘activity’ was normally distributed. As described in Lessells the barrier-test (‘activity’ and ‘crossing frequency’), &Boag [45], R was based on variance components open-field (‘activity’)and dark–light-test (‘time in light’) from a one-way ANOVA with individual as a factor and (all r > 0.515, all p <0.05), but not in latency variables each variable as dependent variable. Its standard errors of the same tests. In the hole-test, no variable was con- were tested with R-package ‘rptR’ following Nakawaga & sistent over time for this group. Schielzeth [46]. In the barrier-test we found no difference between the To identify possible associations among behavioural three experimental groups (Kruskal-Wallis test by group: variables, we calculated a Spearman rank correlation latency round1 Chi = 2.733, df = 2, p = 0.255; round 2 2 2 matrix among all variables from all behavioural tests Chi = 2.9288, df = 2, p = 0.2312; activity round 1 Chi = from the first testing round of the ‘short term adult’- 2.9525, df = 2, p = 0.229; round 2 Chi = 0.8214, df = 2, p = group (see Additional file 1). We computed an agglom- 0.6632) but latency was significantly lower in the second erative cluster analysis with the ‘cluster’ package and the testing round than in the first for the two groups with ‘agnes’ function of the R statistical environment with adult animals if compared within individuals (Wilcoxon ‘manhattan’ clustering with complete linkage, similar to signed rank test: short term adult V = 10107, N = 168, Gyuris et al. [47] and Tremmel & Müller [35]. The re- p < 0.001; long term adult V = 871, N = 48, p = 0.001; sults of the cluster analysis are shown by a dendrogram, Figure 1A) and activity was reduced (short term adult which lists all of the variables and indicates at what level V = 5638, N = 151, p = 0.021; long term adult V = 595.5, of similarity any two clusters were joined (‘height’). The N = 41, p = 0.004), Both was not the case in the animals height of the link (‘U’) represents the distance between that were tested over maturation (latency: V = 110, N = 17, the two clusters that contain those objects, i.e. the p = 0.118; activity: V = 47, N = 17, p = 0.477). shorter the U the more similar the variables are to each Measured latency in barrier-test was repeatable for voles other. that were tested before and after maturation (R =0.63, All analyses were carried out with R 2.14 (The R SE = 0.148, N = 17, p = 0.002) and over one week as adults Foundation for Statistical Computing, Vienna, Austria, (R = 0.27, SE = 0.072, N = 149, p < 0.001), but not for http://www.R-project.org). Values of p were two tailed adults that were tested after three months (R = 0.045, throughout and the accepted significance level was p < 0.05. SE = 0.145, N = 41, p = 0.379) (Figure 2). Repeatability of activity in the barrier-test showed the opposite pattern: Ethical standards animals that were tested over adolescence showed no con- In 2008 all animals were housed and all experiments were sistent activity (R = 0.258, SE = 0.23, N = 17, p = 0,145), conducted under permission of the Landesamt für Natur, whereas all tested adults were consistently active, both Umwelt und Verbraucherschutz Nordrhein-Westfalen over one week (R = 0.387, SE = 0.069, N = 166, p < 0.001) (reference number 9.93.2.10.42.07.069). All animals in and three months (R = 0.457, 0.118, N = 48, p < 0.001) 2010 and 2011 were captured under permission of the (Figure 2). These results were supported by correlations Landesumweltamt Brandenburg (reference number RW- presented in Table 1. 7.1 24.01.01.10). Experiments in 2010 and 2011 were con- ducted under the permission of the Landesamt für Consistency over situations Umwelt, Gesundheit und Verbraucherschutz Brandenburg On the basis of the correlation matrix (see Additional (reference number V3-2347-44-2011). After the experi- file 1) and the calculated cluster analysis on the mea- ments, the animals either stayed in the laboratory for fur- sured variables of the ‘short term adult’-group, three ther experiments, or were released at the original trapping clusters with following variables can be described as pos- site, as specified in the trapping permissions. sible structures of behavioural syndromes (Figure 3): 1. barrier latency, dark–light latency into light, and open- Results field latency and time safe zone; 2. hole latency for one Consistency over time and four holes; 3. barrier crossing frequency and activity, All behavioural variables in the ‘short-term adult’ group open-field activity, dark–light time in light and number were highly correlated between the first and second test of nose-in-hole events. The variables in the first arm Herde and Eccard BMC Ecology 2013, 13:49 Page 6 of 10 http://www.biomedcentral.com/1472-6785/13/49 AB Over Short Term Long Term Over Short Term Long Term Maturation Adult Adult Maturation Adult Adult Figure 1 Comparison between first and second barrier-test within experimental groups of common voles. A) Barrier Latency [sec], B) Barrier Activity [1-0-sampling]. Significant differences in Wilcoxon signed rank test were indicated by stars. represent latency measures. They might be considered barrier and stayed in the safe zone of the open-field as a kind of shy-bold axis of common voles behavioural arena for a shorter time, compared to their shyer conspe- syndromes, which we have called ‘boldness’. The bolder cifics Close to this cluster is a second arm which includes animals entered the unsafe zone in the open-field and latencies only of the hole-test. The faster a vole sticks its the dark–light-test earlier, jumped earlier over the head through the holes, the more explorative the animal 0.0 0.5 1.0 1.5 2.0 2.5 0 5 10 15 20 25 30 Barrier Activity 1 Barrier log-Latency 1 Figure 2 Correlation between behavioural variables measured in first and second barrier-test. Latency (left side; range 0–300 sec.) and activity (right side; max. 30 active samples) for each of the three experimental groups of tested common voles are shown. Correlations coefficient (r ) and p-values for correlations are represented in Table 1. Lines indicate significant correlations (p < 0.05; adjusted for multiple testing). BarrierLatency Long Term Adult Short Term Adult Over Maturation log-Latency 2 log-Latency 2 log-Latency 2 0.0 0.5 1.0 1.5 2.0 2.5 0.0 0.5 1.0 1.5 2.0 2.5 0.0 0.5 1.0 1.5 2.0 2.5 BarrierActivity Activity 2 Activity 2 Activity 2 0 5 10 15 20 25 30 0 5 10 15 20 25 30 0 510 15 20 25 30 Herde and Eccard BMC Ecology 2013, 13:49 Page 7 of 10 http://www.biomedcentral.com/1472-6785/13/49 1 3 Figure 3 Dendrogram for the relationships between measured variables in the ‘short term adult’-group (N = 168) according to the cluster analysis. Height of each U represents the distance between two variables and is based on correlation coefficients of Spearman correlation matrix (see Additional file 1). Groupings indicate possible behavioural syndrome structure (agglomerative coefficient 0.64). is. Therefore, those latencies are associated with explor- Since rank order of scores is maintained across con- ation behaviour and are closely related to the boldness texts in adult animals, i.e. all activities and according la- variables. Thus, we called both clusters together ‘bold- tencies form one arm of the dendrogram (Figure 3), ness/exploration’-axes. The third cluster is more uniform, contextual generality was high [24]. With a combination it contains all measured activities of all tests and can of activity and boldness/exploration as dimensions of be- therefore be named ‘activity’-cluster. Animals that are ac- havioural syndromes we obtained results very similar to tive in the open-field are also the more active ones in the studies in voles and other small mammals. Lantová et al. barrier-test. They jumped over the barrier more often and [38] also found a connection between activity and bold- spent more time in light. ness in different behavioural tests in a captive common There were also indications for a connection between vole population. Similar axes can also be seen in grey boldness and the activity clusters. Common voles which mouse lemurs (Mircrocebus murinus) [32] and Siberian had, for example, short latencies to enter the unsafe chipmunks (Tamias sibiricus) [48] in wild populations. zone in the open-field, did also jump at the barrier at Other vole species showed consistent individual differ- higher frequency, i.e. show higher activity (Spearman ences in activity (meadow vole (Microtus pennsylvanicus rank correlation r = −0.327, N = 164, p < 0.01). [49]; root voles M. oeconomus) [50]) like adult animals in our study. Therefore, it can be assumed that boldness and activity are very common personality axis in small Sex differences mammals. Sex differences were found only in barrier and open-field As predicted, the length of the interobservation inter- activity where male common voles where more active val had an influence on the repeatability of behaviours in than females (barrier activity: males 21 ± 8, females 19 ± 8 common voles. Animals that were tested over intervals active samples; Mann–Whitney-U = 2249.0, N = 151, of three months, over maturation or as adults, showed p = 0.026; open-field activity: males 22 ± 7, females 19 ± 8 less consistent behaviours than animals tested twice dur- active samples, Mann–Whitney-U = 2602.5, N = 164, ing one week (Table 1). Surprisingly, activity and bold- p = 0.014). In all other behaviours males and females ness/exploration behaviour differed in their behavioural behaved equally. Comparison of Spearman correla- consistency, depending on the age of the tested animal. tions that were calculated separately for adult males This may possibly be explained by differences in experi- and females showed no difference in consistency over ences, their expected life span, or developmental change time between sexes (z-test, all p > 0.3). such as maturation. Young voles tested over maturation lived in stable cap- tive conditions before and over the experiment. They Discussion had stable latencies while exploring the barrier-test but Our results demonstrate the presence of behavioural syndromes in common voles (Microtus arvalis). We do not show repeatable activity. It is possible that the la- boratory environment with limited space for experien- showed that behaviour in different tests was consistent cing or exercising movement did not stimulate the over time (Figure 2) and over situations (Figure 3). height 135 7 Barrier latency Dark-light latency into light Open-field latency Open-field time safe zone Hole latency one hole Hole latency four holes Barrier crossing frequency Barrier activity Open-field activity Dark-light time in light Hole number nose Herde and Eccard BMC Ecology 2013, 13:49 Page 8 of 10 http://www.biomedcentral.com/1472-6785/13/49 formation of stable activity types. We compared captive future assets (Figure 1). Studies on field crickets (Gryllus bred animals with wild caught ones in this study by the integer) [21] and grey mouse lemurs [32] support that a reason that adequate age estimation is not possible in trade-off between current and future reproduction can wild-caught voles and immature young voles were diffi- lead to personality variation. To investigate why behaviour cult to trap in nature. Due to habituation to captive con- of common voles is not adjusted like predicted in the asset ditions and lower diversity of situations one could protection theory, the differences in behaviour between expect that captive animals show even more stable be- young and older voles should be observed in natural pop- haviours [51] but Bell et al. [28] found repeatability of ulations with fluctuating densities and active competition. behaviour was higher when measured under natural The differences in differential consistency in the three conditions. Besides, another reason for the missing experimental groups suggest that the link of activity and consistency over time is that some effects cannot be de- boldness/exploration can be decoupled during ontogeny. tected with small sample sizes. To proof this result on in- This makes sense when environmental conditions expe- consistency in boldness in more natural conditions (e.g. in rienced by juveniles differ substantially from those expe- monitored outdoor enclosures) and with a larger sample rienced by adults [3], particularly in traits that are more size would be challenging for future studies. sensitive to the environment (e.g. behavioural traits like Adult voles captured from the wild and maintained in activity or boldness) compared to morphological or semi-wild outdoor enclosures, showed repeatability in physiological traits [28]. In voles, annual population dy- boldness/exploration behaviour only over a short period namics with different conditions depending on the sea- of time, but less so over three months. In contrast activ- son of birth are typical: Animals that were born in ity patterns were stable, which is surprising because ac- spring/summer mature at an age of weeks, whereas indi- tivity has been reported as one of the least repeatable viduals born in late summer/autumn overwinter as im- behaviours [28] (but see [34]). It could be that explor- matures and start reproduction in the following spring ation and boldness can be adapted more easily to at an age of months [56-59]. During seasons not only current environmental conditions like predator presence environmental conditions change (e.g. density, food or food availability, which may have differed between availability) but also asset protection should play a role conditions in the wild, which animals experienced prior in development of behavioural traits, like discussed to the first testing and in the enclosures, prior to the above and elsewhere [60]. Therefore, the importance of second testing. Experiences can either enhance stability studies in natural conditions should not be neglected. It by reinforcing a package of traits, or experiences may is likely that especially young individuals could show dif- modify behavioural types [3]. In a small prey animal, like ferent development of behavioural traits in unstable or the common vole, this flexibility could be very important heterogeneous environments. Environmental conditions to survive in the wild where force trade-offs between, for affect both life history [61] and behavioural type expres- instance, exploring resources and avoiding predators. sion [15,62], and future studies should consider both. This flexibility is less important in the laboratory where Male common voles were more active in two of four conditions were stable. We suggest that activity pat- tests than females. The voles’ breeding system with pro- terns were developed after maturation as we could not miscuously mating females may explain this difference see them in young animals but in adults. Studies on as discussed in Eccard & Herde [60]. Differences in killifish (Kryptolebias marmoratus) [52] and Sibirian consistency over time between the sexes were not found dwarf hamsters (Phodopus sungorus) [34] showed also although this would not be unexpected as this was found an age effect on behavioural types and developmental in two bird species [12,63]. flexibility while damselflies (Lestes congener)showde- velopmental consistency in boldness and activity per- taining through metamorphosis [53]. Conclusions Current theoretical models discuss that differences in Common voles showed consistent individual differences state in combination with state-dependent behaviour can in their behaviour. Over short periods, repeatability as explain stable differences in behavioural traits [54]. For well as contextual generality was high. Over longer pe- example, animals should differ in their risk-taking be- riods, long in relation to the animals’ life span, stability haviour if they do either focus on current or on future of traits may be dependent of life stage of the animal reproduction. Individuals with expected low future re- but also external factors like stability of the surround- productive success (i.e. low asset) should take more risk ing environment. The research on animal personality as they have not much to lose [32,54,55]. Meanwhile, in and behavioural syndromes requires longitudinal stud- our study, juvenile voles, that should have high assets to ies (e.g. capture-mark-recapture) to follow the variation protect, did not have lower boldness or higher activity in behaviour and its consistency over a life span under scores compared to adult animals with expected lower natural conditions [13]. Herde and Eccard BMC Ecology 2013, 13:49 Page 9 of 10 http://www.biomedcentral.com/1472-6785/13/49 Additional file 13. Stamps JA, Groothuis TGG: Developmental perspectives on personality: implications for ecological and evolutionary studies of individual differences. Phil Trans R Soc B 2010, 365(1560):4029–4041. Additional file 1: Spearman correlation matrix of first testing round 14. Bell AM, Sih A: Exposure to predation generates personality in three- for all measured variables in the ‘short term adult’-group. spined sticklebacks (Gasterosteus aculeatus). Ecol Lett 2007, 10(9):828–834. 15. Boon AK, Reale D, Boutin S: The interaction between personality, offspring fitness and food abundance in North American red squirrels. Abbreviations Ecol Lett 2007, 10(11):1094–1104. PIT: Passive integrated transponder; ANOVA: Analysis of Variance; R : ANOVA- 16. Dingemanse NJ, Reale D: Natural selection and animal personality. Behav based repeatability; SE: Standard error; r : Spearman rank correlations 2005, 142:1159–1184. coefficient; SD: Standard deviation. 17. Quinn JL, Patrick SC, Bouwhuis S, Wilkin TA, Sheldon BC: Heterogeneous selection on a heritable temperament trait in a variable environment. Competing interests J Anim Ecol 2009, 78(6):1203–1215. The authors declare that they have no competing interests. 18. Reale D, Garant D, Humphries MM, Bergeron P, Careau V, Montiglio PO: Personality and the emergence of the pace-of-life syndrome concept at the population level. Phil Trans R Soc B 2010, 365(1560):4051–4063. Authors’ contributions 19. David M, Auclair Y, Cezilly F: Assessing short- and long-term repeatability AH and JAE designed the study. AH performed the research, analysed the and stability of personality in captive zebra finches using longitudinal data and wrote the manuscript. Both authors read and approved the final data. Ethol 2012, 118(10):932–942. paper. 20. 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Anim Behav 2009, 77(5):1041–1050. • Immediate publication on acceptance doi:10.1186/1472-6785-13-49 • Inclusion in PubMed, CAS, Scopus and Google Scholar Cite this article as: Herde and Eccard: Consistency in boldness, activity and exploration at different stages of life. BMC Ecology 2013 13:49. • Research which is freely available for redistribution Submit your manuscript at www.biomedcentral.com/submit

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BMC EcologySpringer Journals

Published: Dec 7, 2013

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