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Increased survival and reproductive success associated with stereotypical behaviours in laboratory-bred bank voles (Clethrionomys glareolus)
Applied Animal Behaviour Science 121 (2009) 55–62
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Increased survival and reproductive success associated with stereotypical behaviours in laboratory-bred bank voles (Clethrionomys glareolus) Bryan Schønecker * University of Copenhagen, Department of Biology, The Animal Behaviour Group, Tagensvej 16, DK 2200 Copenhagen N, Denmark
A R T I C L E I N F O
A B S T R A C T
Article history: Accepted 11 August 2009 Available online 5 September 2009
The aim of this study was to examine whether voles performing stereotypic behaviours (Ster) differed in physical welfare from voles, which did not develop stereotypies (N-Ster). The chosen variables were reproductive success and capacity to survive barren housing conditions. Furthermore, effect of weight on proneness to develop stereotypic behaviours were examined. Singly housed Ster (n = 62) in barren cages showed superior survival when compared to similar housed N-Ster (n = 38; p = 0.002). Furthermore, Ster females (n = 25) gave birth to both a first and second litter faster than N-Ster females (n = 14; p 0.019). Litter size, number of weanlings and proportion of barren females did not differ between Ster and N-Ster, but pups from Ster experienced a higher pre-weaning mortality in the second litter (p = 0.0095). Voles classed as Ster within age 6 month (n = 55) weighed less than same aged N-Ster (n = 45) already from weaning (21 days; p = 0.0204). However, weight at weaning, whether LIGHT (weight median; n = 47) or HEAVY (weight > median; n = 53), had no effect on subsequent development of stereotypies in terms of either onset age or fraction which developed stereotypies. The results suggested that Ster had better physical welfare, as reflected in better survival, than N-Ster when housed singly and a higher reproductive success when used as breeders. ß 2009 Elsevier B.V. All rights reserved.
Keywords: Stereotypic behaviour Survival Fecundity Welfare assessment
1. Introduction Farm-, zoo- and research animals live their relatively short lives in environments rich in various types of potential stressors (Morgan and Tromborg, 2007) to which a fraction of the animals, dependant on the species and management related issues, responds by performing socalled ‘‘spontaneous’’ stereotypical behaviours. Only one paper has to my knowledge attempted to quantify the annual number of animals performing stereotypies worldwide. The author’s estimate of minimum of 87 million animals/year (Mason and Latham, 2004) and the vast majority of these are pigs and poultry.
* Present address University of Copenhagen, Faculty of Life Sciences, Department of Large Animal Sciences, The Ethology Group, Grønnega˚rdsvej 8, 1870 Frederiksberg C, Denmark. Tel.: +45 36 96 07 63. E-mail address: [email protected]. 0168-1591/$ – see front matter ß 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.applanim.2009.08.003
Although researchers have yet to agree fully on the basic definition of both animal (Low, 2003; Rushen and Mason, 2006), and human stereotypies (Rapp and Vollmer, 2005), overt stereotypies are easily recognized by observant laymen as seemingly misplaced behaviours, irrelevant for the context in which they occur. These types of behaviours seem to lack a sensible purpose, have an ‘‘automatic appearance’’ and typically occur in repetitive and vigorous bouts, which can last from seconds to hours (Carlstead and Seidensticker, 1991; Sørensen, 1987; ¨ dberg, 1986). O Stereotypies are generally perceived as indicators of relatively poor welfare (see e.g. review by Mason, 1991). Whether this perception is correct has been subject to some controversy (see e.g. Mittelman et al., 1991). In fact, a recent meta-analysis found that while stereotypies were most often linked with the poorest environments, stereotypies within these environments were most often ‘‘linked with good welfare’’ for the individuals that engaged in
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these behaviours (Mason and Latham, 2004). As suggested by Mason et al., 2007, the occurrence of stereotypies might therefore be more useful to pinpoint poor environments for the captives, than it would be to pinpoint individuals with relatively poor welfare. However, exactly what constitutes ‘‘welfare’’ has been subject to dispute for centuries (see e.g. Sandøe and Christiansen, 2008 for the necessary basis of any discussions addressing animal ethics and welfare). At present it is broadly recognized that the concept of animal welfare both has a mental and a physical aspect, interacting with each other. Attempts to estimate mental welfare can be conducted in many ways (see e.g. Baumans, 2005; Dawkins, 2003). However, as expressed by Dawkins (2006), ‘‘Animal consciousness is central to the study of animal welfare but is still, tantalizingly, the ‘‘hard problem’’ and needs to be respected as such’’. Physical welfare on the other hand can basically be equated with the biological term ‘‘fitness’’ (a special case of ‘‘inclusive fitness’’ conceptualized by Hamilton, 1964), the essence of which is that the animal leaving the largest number of viable offspring has the highest fitness. Anything that can diminish the animals potential in this regard constitutes reduced fitness and, hence, reduced welfare. Consequently, indicators of poor welfare include measures such as reduced life expectancy, impaired reproduction, disease, immunosuppression, and behavioural anomalies (Broom, 1991a,b). To sum up, there seem to be no simple truth when it comes to defining animal welfare and no single measurement can estimate welfare with confidence (Mason and Mendl, 1993). Bank voles are well suited for studies of stereotypic behaviour since they readily develop a suite of easily recognisable stereotypies, as a role of thumb provided they are born in captivity and housed in barren cages (Cooper and Nicol, 1991, 1994; Schoenecker et al., 2000; Sørensen, ¨ dberg, 1986). The 1987; Sørensen and Randrup, 1986; O smaller/more barren the cage and the more restricted concerning possibilities for social contacts, the more frequent are the voles developing stereotypies (Cooper ¨ dberg, 1987). Large et al., 1996; Sørensen, 1985, 1987; O differences in individual levels of stereotypies among bank ¨ dberg, 1986, who suggested voles were first published by O that these differences probably were due to individual genetic differences in the predisposition to interact with discrete stimuli early in life. Later experiments with selective breeding resulted in a seven-fold difference in the proportion of offspring developing stereotypies (Schoenecker and Heller, 2000) and suggests the potentials in developing lines of high/low stereotypers and search for differential gene-expression relevant to the main neurotransmitters connected with development of stereotypies (e.g. serotonin, dopamine and gamma-aminobutyric acid). Stereotypic behaviours of the types occurring in captivity have never been described among voles in nature, and only once among wild caught voles maintained in captivity (Schønecker, 2009). Beside the inherent problem of long-term observations of cryptic animals preferring to be under cover, other factors could explain this discrepancy. For instance insufficient time to develop stereotypies in the wild (see discussion in Schønecker,
2009), lack of frustrating or stressful experiences among young voles in the wild (Schoenecker and Heller, 2000) combined with negative selection pressure by predators. It is therefore difficult to interpret the apparent strong genetic component in captivity-induced development of stereotypies. If such ‘‘stereotypy-genes’’, or better ‘‘segregating units’’ (Bruell, 1962), influencing proneness to develop stereotypies in captivity could be identified, they must at least be fitness neutral in the wild and the reason for their presence could be because they are situated near other segregating units influencing trait(s) more important to the fitness of wild-living voles. Such traits could e.g. be related to fecundity. In this retrospective case-control study of data from two colonies of Danish bank voles the aim was to examine whether stereotyping voles in the laboratory could have an adaptive advantage compared with non-stereotypers as reflected in their relative weight gains through a period of 6 months, capacity to survive barren conditions, and in their reproductive success. 2. Methods 2.1. Ethical note Animal care and use conformed to institutional policies and guidelines (University of Copenhagen, Denmark) and were in accordance with the ethical guidelines proposed by ISAE Ethics Committee (2002) and the International Guiding Principles for Biomedical Research Involving Animals (1985). The studies briefly mentioned in Section 2.4 were conducted under license from the Animal Experiments Inspectorate, Denmark. 2.2. General approach This study is based on retrospective analysis of data obtained through the maintenance and observations of two separate colonies of Danish bank voles, founded and housed at the University of Copenhagen, 1995–1997 and 2000–2003. Known or suspected biases which might interfere with the results have been excluded by a priori selection of three defined subgroups (see below). 2.3. Animals and housing The first colony was founded to study heritability of proneness to develop stereotypical behaviours. Earlier work had shown single housing in barren cages to result in far more stereotypies compared to housing in enriched ¨ dberg, 1987). Barren cages (Sørensen, 1985, 1987; O housing was consequently chosen to (1) reduce the number of voles necessary to achieve a proper sample size of stereotyping offspring in F2, vis-a`-vis the recommendations of the ‘‘3Rs’’ (Russell and Burch, 1959); (2) ensure no interactions between development of stereotypies and the inevitable cage hierarchy among group housed bank voles (Sørensen, 1987) and (3) ensure a reliable estimate of first emergence of stereotypies. The second colony was founded to follow up on the accidental discovery during the work with the first colony
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of a new human model of diabetes, based on polydipsic captive bank voles (Schoenecker et al., 2000; Freimanis et al., 2003). Polydipsia is so-called excessive water intake and single housing in barren cages produced a larger fraction of polydipsic voles compared to group housing in enriched cages (38% vs. approx. 20%; Schoenecker et al., 2000; Sørensen and Randrup, 1986). Furthermore, different types of pre-weaning stressors were at the time known to modulate the frequencies of voles developing diabetes in both directions (Freimanis et al., 2003). Consequently, single housing in barren cages were again chosen to reduce the number of voles; disable any cage hierarchy related interactions with the development of diabetes and enable a reliable measurement of individual daily water intake. Briefly, founders of the two colonies (N = 166) were captured in the forests of Zealand, Denmark and housed as single pairs in transparent cages (14.5 21.5 37.5 cm) provided a wire lid with feed hopper and water bottle. Food (Altromin 1324) and water were available ad lib and the cages were supplied with a woodcutting bed and enrichment in the form of toilet paper and paper rolls. Males were always removed from the females immediately after a birth had been observed and placed in a smaller barren cage (13.5 16.0 22.5 cm). Pups from the first colony (N = 518) were weaned after 18–53 days where all pups from the second colony (N = 525) were weaned after 21 days exactly. Pups were housed singly in small barren cages, unless used as breeders. Roughly 30% of the captive born voles were on one or more occasions used as breeders, during which time they were housed as single pairs in larger enriched cages as described above. Both F1 and F2 in both colonies were completely outbred where 61% of the F3 voles in the second colony resulted from selective breedings involving single pairs of full siblings. Maintenance and observations were carried out on a daily basis and lasted typically 2–4 h/ day.
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development of stereotypies among voles (Cooper and Nicol, 1994). Further observations addressed various measures related to fecundity, age of ‘‘natural death’’ or ‘‘exit’’ from the colony. ‘‘Natural death’’ is used to designate any unexplained death, i.e. deaths without obvious cause or prior signs of deteriorated health and moribundity, and affected 257 (21%) of the 1209 voles in the colonies. ‘‘Exit’’ from the colony could be due to a number of reasons. The prime reason was culling, or translocation to original trapsite, for logistic reasons (lack of available space/cages; final termination of colonies) or no further scientific purposes (562 voles; 46%) followed by transfers to the care of other researchers (188 voles; 16%). 142 voles (12%) were sacrificed in order to provide biological samples in relation to our further studies of our new diabetic human model and 46 voles (4%) died in accidents, e.g. during attempt to escape, or a defect water bottle flooding the cage. Five voles (0.4%) died as a consequence of stressful encounters with aggressive cage mates and 7 voles (0.6%) were euthanized for humane reasons (see Section 2.5). Only pups from the second colony were weighed when weaned and some of the second colony F1 (N = 118) were in addition weighed at the ages 1, 2, 3, 4, 5, and 6 months during which time all were singly housed. 2.5. Humane endpoints If a vole showed a moribund appearance, or seemed to be in a state of pain and suffering, it was anaesthetized in a mixture of CO2 and O2, followed by cervical translocation. Voles used to provide biological samples were sacrificed in a similar manner. Moribundity could be indicated by a combination of lethargic movements, abnormal lowering of attention to surroundings, tousled fur or e.g. significantly decreased ADW among diabetic voles. All voles present in the facility were routinely inspected visually at the end of the day for any signs of distress, disease or pain.
2.4. Observations and classifications 2.6. Selection of data The average daily water intakes (ADW) were calculated for all solitary voles from weaning and until death/exit. Water bottles were weighed and changed at least once a week and data and exact time for the procedure were then used by a standard database program (Filemaker v.2.1 for Mac) to calculate the ADW since it had been shown that an ADW exceeding 21 ml is a reliable marker of type 1 diabetes in Danish bank voles (Freimanis et al., 2003; Niklasson et al., 2003; Schoenecker et al., 2000; Schønecker et al., submitted). The most common types of stereotyped behaviours among Danish bank voles were (decreasing order) backward somersaulting, high-speed jumping, pacing following a fixed route and windscreen wiper movement (Schoenecker et al., 2000). Non-diabetic voles, which exhibited any such stereotypies in bouts of at least five repetitions, were classed as Ster and age of first observation were noted. The vole was then moved away from the still non-stereotyping voles (classed N-Ster), primarily to make it easier to spot new cases of Ster secondary, to mitigate any influence by a possible ‘‘neighbour effect’’ on
The following three groups (A–C; N total = 169; n males/ females = 37/76 (F1) and 31/25 (F2)) have been selected for further analysis and since 18 voles are included in two groups (11 appears in both A and B; 7 appears in both A and C), the total of groups (N = 187) exceeds the actual number of voles considered in this retrospective study. 2.6.1. Group A: This group is used to analyse if Ster and N-Ster differs in weight gain between weaning and age 6 months (Section 3.1 and Table 1). The voles were weighed at weaning and at the ages of 1, 2, 3, 4, 5 and 6 months. Since it is reasonable to assume an interaction between development of diabetes and development in weight, only data from voles which remained non-diabetic, and survived, all through the 6 months weighing period are included in Group A. Furthermore, since pups from diabetic females weighs more when weaned at age 21 days than pups from nondiabetic females (Schønecker et al., submitted), only pups from non-diabetic females have been included. This
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Table 1 Weight (g) of Ster and N-Ster from group A (n = 40) when weaned and through their first 6 months. Weights are expressed as 25/50/75 percentiles with the actual number of Sters/N-Sters a given month in square brackets (A). The two columns marked (B) describe weights of voles according to their final classing as either Ster (n = 18) or N-Ster (n = 22) at age 6 months. Pair-wise test results are presented in p (A) and p (B).
Weaning 1 Month 2 Month 3 Month 4 Month 5 Month 6 Month
Ster (A)
N-Ster (A)
N.A. [0] N.A. [0] 18.4/22.3/24.8 17.0/18.4/22.3 18.9/19.7/22.6 19.4/21.0/22.6 20.7/22.7/26.2
11.0/11.9/12.6 15.4/16.9/18.7 18.0/20.5/23.3 18.7/21.3/24.8 20.5/22.2/25.5 22.2/23.7/27.4 22.7/25.7/29.0
[7] [11] [16] [18] [18]
[40] [40] [33] [29] [24] [22] [22]
selection results in data from 20 F1 males and 20 females from the second colony which all remained singly housed for the first 6 months. A total of 18 voles (n males/ females = 6/12) were classed as Ster within 6 months and first sign of stereotypical behaviours were observed between the first and second month. 2.6.2. Group B: This group is used to (1) study any interaction between weight at weaning and subsequent development of stereotypical behaviours (Section 3.2) and (2) analyze survival of Ster and N-Ster voles using the Kaplan–Meier method (Section 3.3). All breeders have been excluded from this group since breeders differ in several important variables (e.g. individual number and age of pairings). All offspring from diabetic females are excluded, as are all captive born voles, which were not weighed when weaned. This selection reduce the sample size to 54 males and 46 females from the second colony (F1 and F2), all weaned at the age of 21 days and all housed singly in small barren cages. They weighed 11.04 1.43 g (mean SD) when weaned and were subsequently classed as either LIGHT (weight mean weight) or HEAVY weanlings (weight > mean weight). Proneness to develop stereotypical behaviour in captivity has a strong heritable component (Schoenecker and Heller, 2000) and it is therefore relevant at this point to note that the proportion of offspring from Ster parents was statistically the same among both LIGHT and HEAVY weanlings (43% vs. 40% respectively, Chi = 0.088, df = 1, p = 0.7662). Sixty-two of these 100 Group B voles were eventually classed as Ster and remained a median of 489.5 days (25/75 quartiles = 454/652) in captivity. The remaining 38 N-Ster spend 255 days (median) in captivity (25/75 quartiles = 109/555). Lengths of captivity differed significantly (Z = 2.941, p = 0.0033). 2.6.3. Group C: This group is used to analyse variables of relevance to fecundity (Section 3.4 and Table 2). Only data from (nondiabetic) females classed as either Ster or N-Ster both when paired and when exiting the colony are included. All breeding pairs were un-related and consisted of either two Sters or N-Sters, leaving data from 28 Ster and 19 N-Ster females for analysis. Bank voles exhibit post-partum oestrus (Clarke and Hellwing, 1983) and data from any such resultant litters are included. The median ages for first pairing were 178 days and 180 days respectively (25/75
p (A)
Ster (B)
N-Ster (B)
p (B)
N.A. N.A. 0.6057 0.1418 0.0727 0.0045 0.0363
10.9/11.6/12.2 14.9/16.0/16.7 17.2/18.3/22.4 17.0/18.3/22.1 18.1/19.4/22.6 19.4/21.0/22.6 20.7/22.7/26.3
11.0/12.1/13.0 16.9/18,6/19,5 19.8/21.7/24.2 19.6/21.7/25.9 21.4/22.5/25.6 22.2/23.7/27.4 22.7/25.7/29.0
0.1735 0.0003 0.0296 0.0098 0.0114 0.0045 0.0363
quartiles (days) = 171/244 (Ster) and 159/278 (N-Ster); Z = 0.358, p = 0.7205). The two groups of females did not differ either in their weight when weaned, or in the time they spend in the colonies (Z 1.17, p 0.242 in both cases). Finally, barren and fertile voles did not differ regarding the age when mated, either within the Ster, NSter or when both classes were pooled (Z 1.388, p 0.1653) 2.7. Statistics With few exceptions, data did not satisfy requirements to parametric tests so non-parametric tests were mainly used instead. These were the Mann–Whitney U-test (differences in weight developments and fecundity related measures); Chi Square (incidence of Ster among LIGHT/ HEAVY weanlings; incidence of ‘‘natural death’’ among Ster/N-Ster adults; pre-weaning mortalities); Fisher Exact (pre-weaning mortalities; fraction of barren/unreceptive females among Ster and N-Ster) and the Kaplan–Meier method of survival analysis (onset age of Ster dependant on status as LIGHT/HEAVY weanling; longevity). Pairwise tests in the Kaplan–Meier analysis were always performed using the Breslow-Gehan-Wilcoxon test. A t-test is used in Section 3.2. Data are described using 25, 50 and 75 percentiles except if normal distributed. All tests were two-tailed and corrected for ties if necessary. Level of significance was set a priori at 0.05.
Table 2 Fecundity measures derived from pairs of Ster and N-Ster from group C. Duration of gestation period (GP), size of litters, number of weanlings and pre-weaning pup mortality (PM) in both first litter and second litters resulting from post-partum matings. Data presented as 25/50/75 quartiles with number of valid observations in square brackets. Number of dead (D) and weaned (W) pups are shown in parentheses and pair-wise test results are presented in column p. N-Ster breedings
Ster breedings
p
GP 1st litter n born n weaned 1st litter PM
20/23.5/46 [14] 4/4.5/5 [14] 3.75/4/4.25 [13] 18% (11D/51W)
19/19/21 [25] 3/4/5 [25] 2.5/4/5 [24] 17% (17D/84W)
0.0190 0.7062 0.7790 0.8811
GP 2nd litter n born n weaned 2nd litter PM
19/20/21 [10] 4/5.5/6 [10] 4/5/6 [10] 6% (3D/48W)
18/19/19 [12] 4.5/6.5/7 [12] 2.5/6/7 [11] 23% (17D/56W)
0.0053 0.2403 0.4540 0.0095
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3. Results 3.1. Development in weight (Ster vs. N-Ster) the first 6 months All though voles classed as Ster from Group A (n = 40) were lighter (numerically) already from the third month, this difference in median weight only reached significance during the fifth and sixth month (see Table 1). However, grouping the voles according to their final class as Ster (n = 18) or NSter (n = 22) at age 6 months showed that individuals that subsequently developed stereotypies were significantly lighter already by the first month and through the remaining period. Lastly, LIGHT weanlings (weight median when weaned; n = 20) from group A continued to weigh less than HEAVY weanlings (weight > median when weaned; n = 20) from age 1 months to the last weighing at age 6 months (2.097 Z 3.167; 0.0015 p 0.036). 3.2. Weight at weaning and subsequent development of stereotypies In order to see whether weight at weaning could influence the age at which stereotypical behaviours developed, a larger sub-group (Group B: n = 100) were likewise classed according to their weight at weaning as either LIGHT (n = 47) or HEAVY (n = 53) weanlings. Comparing data from LIGHT with HEAVY voles in a survival analysis showed no significant difference regarding onset age of stereotypical behaviours (Chi = 1.476, p = 0.2244), a result which was repeated in subsequent comparings of onset ages among LIGHT and HEAVY voles descending from either two Ster (n = 32) or two N-Ster (n = 28) parents (Chi 0.166, df = 1, p 0.4176 in both cases). Lastly, there were also no difference between LIGHT (n Ster/total = 19/31) and HEAVY (n Ster/total = 17/38) pups regarding the number classed as Ster at age 6 months (Chi = 0.329, df = 1, p = 0.5665). Where Section 3.1 showed that 6 months old voles classed as Ster were lighter than those classed as N-Ster already from the age of 1 month, group B extend the finding to a significant lighter weight of Ster already at the time of weaning at age 21 days (mean SD (g) = 11.333 1.449 (N-Ster; n = 55) vs. 10.671 1.33 (Ster; n = 45); t = 2.357, df = 98, p = 0.0204). 3.3. Survival of Ster and N-Ster There were no sex differences in group B survival within voles classed at exit as Ster (n = 62), N-Ster (n = 38), or when both classes of voles were pooled (three tests: Chi 3.71, df = 1, p 0.0541) so the groups could be directly compared. The two lines in Fig. 1 describes the fraction of Sters and N-sters alive as a function of time and shows a superior survival of Sters (Chi = 9.588, p = 0.0020). Even though the Sters were housed in barren cages for almost twice as long time as the N-Sters (see Section 2.6), they tended to have a lower frequency of ‘‘natural deaths’’ (7 Ster vs. 10 N-Ster; Chi = 3.77, p = 0.0522). Considering voles classed as Ster weighed significantly less than those classed as N-Ster, and LIGHT weanlings
Fig. 1. Kaplan–Meier survival curves for 38 N-Ster (filled circles = 10 events of deaths without obvious causes) and 62 Ster (open squares = 7 events of deaths without obvious causes). The abscissa denotes ages in days and the ordinate denotes the fraction of survivors.
continued as a group to be LIGHT adults (Section 3.1), weight might be a confounding variable, influencing survival. A subsequent survival analysis showed no significant influence of weight at weaning among either the Sters (n LIGHT/HEAVY = 31/31; Chi = 0.344, df = 1, p = 0.5576); the N-Sters (n LIGHT/HEAVY = 16/22; Chi = 0.102, df = 1, p = 0.7494) or both classes pooled together (n LIGHT/HEAVY = 47/53; Chi = 0.079, df = 1, p = 0.7787). 3.4. Fecundity of Ster and N-Ster As seen in Table 2, Ster females (group C) delivered and weaned statistically the same number of pups, as N-Ster females (p > 0.05 in both cases). However, the time it took to deliver the first litter, and the time between the births of first and second litters were significantly shorter among the Ster females (Z 2.345, p 0.0190 in both cases). Preweaning mortalities were statistically the same in the first litters (17–18%) where the highest second litter pup mortalities were seen among offspring from Sters (23% vs. 6%; Chi = 6.724, df = 1, p = 0.0095). The prevalence of barren/unreceptive females was statistically the same between Ster and N-Ster females (%/n barren/n total; Ster vs. N-Ster: 11%/3/28 vs. 26%/5/19; Chi = 1.951, df = 1, p = 0.1625). 4. Discussion The main results of this study were that voles which eventually developed stereotypies (1) weighed less when weaned at age 21 days than permanent non-stereotypers (2) delivered their litters faster (shorter gestation period) and (3) showed increased survival under barren housing conditions. Furthermore, previous findings of an association
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between low weight at weaning and low weight in adulthood (Wu¨rbel and Stauffacher, 1997) were replicated in this study. Reduced growth is one of the measures indicating poor welfare (Broom, 1991a,b). Stereotypers in this study weighed significantly less than same-age non-stereotypers, raising the question whether increased proneness to develop stereotypies are linked to lighter weight or, alternatively, whether the performance of stereotypies per se cause lighter weight. The possibility that stereotypers are lighter (and fitter) simply because they usually spend hours with these ¨ dberg, 1986; pers. physically challenging behaviours (O observations) would a priori appear the most parsimonious explanation. Analogous to the result of this study, Jeppesen et al., 2004 found that stereotyping female adult mink weighed significantly less than mink showing no stereotypies and, in addition, found indications that it was in fact the stereotypies per se which caused the reduction in bodyweight. On the other hand it could be that relatively lower weight at weaning somehow predisposed the animal to develop stereotypies. Studies using ICR mice had shown that low weight at weaning reduces fitness in the longterm leading to the hypothesis that lighter weanlings are more prone to develop stereotypies due to a higher motivation to rejoin their mother and suckle (Latham and Mason, 2004, Wu¨rbel and Stauffacher, 1997). Lighter weanlings should, accordingly, be more motivated to engage in vigorous escape attempts taking the forms of rearings, lid climbing or jumps. These activities could lead to a progressive sensitization of specific neural pathways (vis-a`-vis a suggestion by Dantzer, 1986) and subsequently a higher probability of developing into stereotypies (Wu¨rbel and Stauffacher, 1998). Prematurely weaned ICR mice had in fact been shown to perform stereotypic wire-gnawing at a higher level as adults than ICR mice with a higher weight as weanlings (Wu¨rbel and Stauffacher, 1997). Taken together, my results just partly support the hypothesis that smaller weanlings should be predisposed to develop stereotypies. Voles classed as stereotypers at age 6 months did in fact weigh less already when weaned at age 21 days compared to those classed as nonstereotypers. However, neither age at onset, nor incidences of stereotypies were significantly influenced by the weight at weaning in these voles. Jeppesen et al., 2004 likewise found no correlation between weight at weaning and subsequent proneness to develop stereotypies in their study on mink. However, voles do show a trend to increase the intensity by which they perform their stereotypies with age and levels of stereotypies closely follow levels of ¨ dberg, 1986; personal observation). general activity (O Furthermore, Danish bank voles show a major peak of both stereotypies and general activity at 22.30–01.00 (Schoenecker and Heller, 2003) and screening for new stereotypers were for practical reasons carried out during the day. Studies employing electronic surveillance during the dark hours would consequently be better suited to provide a conclusive answer to the question of whether low weight at weaning predispose the voles to develop stereotypies.
Reduced life expectancy is another commonly employed measure of poor physical welfare (Broom, 1991a,b). In this study, stereotyping bank voles showed superior survival capacity as compared to that of non-stereotypers. To my knowledge, only three other studies have touched upon the issue of differential survival between stereotyping and nonstereotyping bank voles. Cooper and Nicol (1996, citing Cooper 1992) state ‘‘There was no difference in mortality or fecundity of laboratory and wild caught voles, so there appeared to be no selective advantage to stereotyping.’’ Also Sørensen and Randrup, 1986 noted a significantly increased mortality among wild caught voles due to their frequent development of polydipsia when compared to laboratory born bank voles, of which some developed stereotypies. In retrospect this observation of differential survival must have been confounded by the inclusion of diabetic voles, which do have considerable reduced life expectancies compared to that of non-diabetics (Schoe¨ dberg, 1987 noted two necker et al. submitted). Lastly, O deaths among 44 stereotyping voles before age 60 days and three deaths before age 90 days among 132 nonstereotyping voles. A possible explanation for the superior survival of the stereotypers could be their relative lighter weight since it has been known for many years that lighter animals live longer than more heavy/obese animals (Heilbronn and Ravussin, 2003; McCay et al., 1935). However, considering that light weanlings remained light adults and that there were no significant differences in survival between light and heavy weanlings, the conclusion must be that development of stereotypies per se was a beneficial factor for the voles when kept under these impoverished conditions. Whether the mechanism by which stereotypies influence survival is due to a better physical condition or if mental processes interact with physical welfare should not be determined based on this study. At this point it is relevant to note that Buchalczyk, 1970 found average life spans to be 604 days for reproducing pairs; 363.5 days for barren pairs and 185.25 days for voles housed in single sex communal cages (6–8 animals/cage). My unpublished data shows that both stereotypers and non-stereotypers, when used as breeders for shorter or longer periods, increased their survival to the point of virtually no mortality (4/126 deaths among stereotypers; 0/83 deaths among nonstereotypers). Both groups, furthermore, spend significantly longer time in captivity (median captivity stereotypers/non-stereotypers: 480/499 days) than the voles described in group B. Lastly, both reduced fertility and gestation periods are typically considered indications of poor physical welfare (Broom, 1991a,b). Stereotyping female bank voles showed the shortest interval between introduction of the male and subsequent birth of a litter and a shorter gestation period when mated post-partum. The numbers of pup’s born/ weanlings were statistically the same among stereotypers and non-stereotypers in this study, as was the proportion of barren or unreceptive females. To my knowledge, again only two other studies besides Cooper and Nicol (1996, citing Cooper 1992) has mentioned the issue of fecundity among stereotyping and non-stereotyping bank voles. Sørensen and Randrup, 1986 noted how stereotypies interfered with
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the normal nurturing by the mother since she would sometimes perform stereotypies while carrying the pup in her mouth, usually leading to the death of the pup and ¨ dberg, 1987 noticed a mortality of 21.8% before the age O of 30 days (not separating between stereotypers and non-stereotypers). In this study, pup mortalities in the first litter were statistically the same between stereotypers and non-stereotypers where the second litters showed significantly increased pup mortality among offspring from stereotypers. The subject has been studied in mink (Bildsøe et al., 1991; Hansen, 1993; Jeppesen et al., 2004), where stereotypers deliver, and wean, larger litters than nonstereotypers, while experiencing less pup mortality. However, the observations of differential fecundity in the 2004 study could best be explained by the lower bodyweight of the stereotypers since leaner mink were more fertile than more obese mink, irrespective of stereotypic status. A later study on mink from another farm found no difference in reproduction between high- and low-stereotyping lines, which point to the importance of farm management (Svendsen et al., 2007). 5. Conclusion This study shows that stereotypies among bank voles were associated with both superior survival and a shorter interval between consecutive births when compared to that of non-stereotypers, both factors suggestive of higher physical welfare. However, the mechanism by which stereotypies influence these factors should not be determined based on this study. Bank voles show, as mentioned, indications of heritability behind proneness to develop stereotypies (Schoenecker and Heller, 2000), just as do deer mice (Powell et al., 1999) and African striped mice (Jones et al., 2008; Schwaibold and Pillay, 2001), and models such as these would also for this reason seem well suited for further basic research in the fundamentals of stereotypical behaviours and its consequences. Acknowledgement I would like to thank Jan Ladewig for commenting previous drafts and general support; Knud Erik Heller for past discussions and for providing the necessary facilities to house the vole colony and Jens Lodal for lending equipment to capture the voles. Lastly I would like to thank two anonymous referees for their valuable comments. The study was in part supported by donations from the Danish Research Council and Apodemus AB, neither of which had any influence on either study, analysis or interpretations/ presentation. References Baumans, V., 2005. Science-based assessment of animal welfare: laboratory animals. Rev. Sci. Technol. 24, 503–513. Bildsøe, M., Heller, K.E., Jeppesen, L.L., 1991. Effects of immobility stress and food restriction on stereotypies in low and high stereotyping female ranch mink. Behav. Process. 25, 179–189. Broom, D.M., 1991a. Animal welfare: concepts and measurement. J. Anim. Sci. 69, 4167–4175. Broom, D.M., 1991b. Assesing welfare and suffering. Behav. Process. 25, 117–123.
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Bruell, J.H., 1962. Dominance and segregation in the inheritance of quantitative behavior in mice. In: Bliss, E.L. (Ed.), Roots of Behavior. Harper & Row, New York, pp. 48–62. Buchalczyk, A., 1970. Reproduction, mortality and longevity of the bank vole under laboratory conditions. Acta Theriologica 15, 153–176. Carlstead, K., Seidensticker, J., 1991. Seasonal variation in stereotypic pacing in an American black bear Ursus americanus. Behav. Process. 25, 155–161. Clarke, J.R., Hellwing, S., 1983. Fertility of the post-partum bank vole (Clethrionomys glareolus). J. Reprod. Fertil. 68, 241–246. Cooper, J.J., 1992. The Behavioural Analysis of Stereotypic Behaviour in the Bank Vole. PhD Thesis, University of Bristol, UK. Cooper, J.J., Nicol, C.J., 1996. Stereotypic behaviour in wild caught and laboratory bred bank voles (Clethrionomys glareolus). Anim. Welf. 5, 245–257. Cooper, J.J., Nicol, C.J., 1991. Stereotypic behaviour affects environmental preference in bank voles (Clethrionomys glareolus). Anim. Behav. 41, 971–977. Cooper, J.J., Nicol, C.J., 1994. Neighbour effects on the development of locomotor stereotypies in bank voles (Clethrionomys glareolus). Anim. Behav. 47, 214–216. Cooper, J.J., Nicol, C.J., 1996. Stereotypic behaviour in wild caught and laboratory bred bank voles (Clethrionomys glareolus). Anim. Welf. 5, 245–257. ¨ dberg, F., Nicol, C.J., 1996. Limitations on the effectiveness of Cooper, J.J., O environmental improvement in reducing stereotypic behaviour in bank voles (Clethrionomys glareolus). Appl. Anim. Behav. Sci. 48, 237– 248. Dantzer, R., 1986. Behavioral, physiological, and functional aspects of stereotyped behavior: a review and a re-interpretation. J. Anim. Sci. 62, 1776–1786. Dawkins, M.S., 2003. Behaviour as a tool in the assessment of animal welfare. Zoology (Jena) 106, 383–387. Dawkins, M.S., 2006. A user’s guide to animal welfare science. Trends. Ecol. Evol. 21, 77–82. Freimanis, T., Heller, K.E., Schønecker, B., Bildsøe, M., 2003. Effects of postnatal stress on the development of type 1 diabetes in bank voles (Clethrionomys glareolus). Int. J. Exp. Diabesity Res. 4, 21–25. Hamilton, W.D., 1964. The genetical evolution of social behaviour. I. J. Theor. Biol. 7, 1–16. Hansen, C.P.B., 1993. Stereotypies in ranch mink: the effects of genes, litter size and neighbours. Behav. Process. 29, 165–178. Heilbronn, L.K., Ravussin, E., 2003. Calorie restriction and aging: review of the literature and implications for studies in humans. Am. J. Clin. Nutr. 78, 361–369. Jeppesen, L.L., Heller, K.E., Bildsøe, M., 2004. Stereotypies in female farm mink (Mustela vison) may be genetically transmitted and associated with higher fertility due to effects on body weight. Appl. Anim. Behav. Sci. 86, 137–143. Jones, M., van Lierop, M., Pillay, N., 2008. All a mother’s fault? Transmission of stereotypy in striped mice Rhabdomys. Appl. Anim. Behav. Sci. 115, 82–89. Latham, N., Mason, G., 2004. From house mouse to mouse house: the behavioural biology of free-living Mus musculus and its implications in the laboratory. Appl. Anim. Behav. Sci. 86, 261–289. Low, M., 2003. Stereotypies and behavioural medicine: confusions in current thinking. Aust. Vet. J. 81, 192–198. Mason, G.J., 1991. Stereotypies and suffering. Behav. Proces. 25, 103–115. Mason, G., Mendl, M., 1993. Why is there no simple way of Measuring Animal Welfare? Anim. Welf. 2, 301–319. Mason, G.J., Latham, N.R., 2004. Can’t stop, won’t stop: is stereotypy a reliable animal welfare indicator? Anim. Welf. 13, 57–69. Mason, G., Clubb, R., Latham, N., Vickery, S., 2007. Why and how should we use environmental enrichment to tackle stereotypic behaviour? Appl. Anim. Behav. Sci. 102, 163–188. McCay, C.M., Crowell, M.F., Maynard, L.A., 1935. The effect of retarded growth upon the length of life span and upon the ultimate body size. J. Nutr. 10, 63–79. Mittelman, G., Jones, G.H., Robbins, T.W., 1991. Sensitisation of amphetamine-stereotypies reduces plasma corticosterone: implication for stereotypy as a coping response. Behav. Neural Biol. 56, 170–182. Morgan, K.N., Tromborg, C.T., 2007. Sources of stress in captivity. Appl. Anim. Behav. Sci. 102, 262–302. Niklasson, B., Heller, K.E., Schønecker, B., Bildsøe, M., Daniels, T., Hampe, C.S., Widlund, P., Simonson, W.T., Schaefer, J.B., Rutledge, E., Bekris, L., ¨ rtqvist, E., Persson, B., Lernmark, A˚., Lindberg, A.M., Johansson, S., O 2003. Development of type 1 diabetes in wild bank voles associated with islet autoantibodies and the novel ljungan virus. Int. J. Exp. Diabesity Res. 4, 35–44. Powell, S.B., Newman, H.A., Pendergast, J.F., Lewis, M.H., 1999. A rodent model of spontaneous stereotypy: initial characterization
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Svendsen, P.M., Hansen, B.K., Malmkvist, J., Hansen, S.W., Palmed, R., Jeppesen, L.L., 2007. Selection against stereotypic behaviour may have contradictory consequences for the welfare of farm mink (Mustela vison). Appl. Anim. Behav. Sci. 107, 110–119. Sørensen, G., 1985. Environmental influences on stereotyped activities and structure of hierachy in bank voles (Clethrionomys glareolus): An ethological - psychiatric study. In: Banathy, B.H. (Ed.), Proceedings Socierty for General Systems Research, International Conference (U.S.A.) Vol. 1, Systems Inquiring: Theory, Philosophy, Methodology. Intersystems Publications, Salinas, pp. 74–77. Sørensen, G., 1987. Stereotyped behaviour, hyperaggressiveness and ‘‘tyrannic’’ hierarchy induced in bank voles (Clethrionomys glareolus) by a restricted cage milieu. Prog. Neuropsychopharmacol. Biol. Psychiatry 11, 9–21. Sørensen, G., Randrup, A., 1986. Possible protective value of severe psychopathology against lethal effects of an unfavourable milieu. Stress Med. 2, 103–105. Wu¨rbel, H., Stauffacher, M., 1997. Age and weight at weaning affect corticosterone level and development of stereotypies in ICR-mice. Anim. Behav. 53, 891–900. Wu¨rbel, H., Stauffacher, M., 1998. Physical condition at weaning affects exploratory behaviour and stereotypy development in laboratory mice. Behav. Process. 43, 61–69. ¨ dberg, F., 1986. The jumping stereotypy in the bank vole (Clethrionomys O glareolus). Biol. Behav. 11, 130–143. ¨ dberg, F.O., 1987. The influence of cage size and environmental enrichO ment on the development of stereotypies in bank voles (Clethrionomys glareolus). Behav. Process. 14, 155–173.
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Applied Animal Behaviour Science journal homepage: www.elsevier.com/locate/applanim
Increased survival and reproductive success associated with stereotypical behaviours in laboratory-bred bank voles (Clethrionomys glareolus) Bryan Schønecker * University of Copenhagen, Department of Biology, The Animal Behaviour Group, Tagensvej 16, DK 2200 Copenhagen N, Denmark
A R T I C L E I N F O
A B S T R A C T
Article history: Accepted 11 August 2009 Available online 5 September 2009
The aim of this study was to examine whether voles performing stereotypic behaviours (Ster) differed in physical welfare from voles, which did not develop stereotypies (N-Ster). The chosen variables were reproductive success and capacity to survive barren housing conditions. Furthermore, effect of weight on proneness to develop stereotypic behaviours were examined. Singly housed Ster (n = 62) in barren cages showed superior survival when compared to similar housed N-Ster (n = 38; p = 0.002). Furthermore, Ster females (n = 25) gave birth to both a first and second litter faster than N-Ster females (n = 14; p 0.019). Litter size, number of weanlings and proportion of barren females did not differ between Ster and N-Ster, but pups from Ster experienced a higher pre-weaning mortality in the second litter (p = 0.0095). Voles classed as Ster within age 6 month (n = 55) weighed less than same aged N-Ster (n = 45) already from weaning (21 days; p = 0.0204). However, weight at weaning, whether LIGHT (weight median; n = 47) or HEAVY (weight > median; n = 53), had no effect on subsequent development of stereotypies in terms of either onset age or fraction which developed stereotypies. The results suggested that Ster had better physical welfare, as reflected in better survival, than N-Ster when housed singly and a higher reproductive success when used as breeders. ß 2009 Elsevier B.V. All rights reserved.
Keywords: Stereotypic behaviour Survival Fecundity Welfare assessment
1. Introduction Farm-, zoo- and research animals live their relatively short lives in environments rich in various types of potential stressors (Morgan and Tromborg, 2007) to which a fraction of the animals, dependant on the species and management related issues, responds by performing socalled ‘‘spontaneous’’ stereotypical behaviours. Only one paper has to my knowledge attempted to quantify the annual number of animals performing stereotypies worldwide. The author’s estimate of minimum of 87 million animals/year (Mason and Latham, 2004) and the vast majority of these are pigs and poultry.
* Present address University of Copenhagen, Faculty of Life Sciences, Department of Large Animal Sciences, The Ethology Group, Grønnega˚rdsvej 8, 1870 Frederiksberg C, Denmark. Tel.: +45 36 96 07 63. E-mail address: [email protected]. 0168-1591/$ – see front matter ß 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.applanim.2009.08.003
Although researchers have yet to agree fully on the basic definition of both animal (Low, 2003; Rushen and Mason, 2006), and human stereotypies (Rapp and Vollmer, 2005), overt stereotypies are easily recognized by observant laymen as seemingly misplaced behaviours, irrelevant for the context in which they occur. These types of behaviours seem to lack a sensible purpose, have an ‘‘automatic appearance’’ and typically occur in repetitive and vigorous bouts, which can last from seconds to hours (Carlstead and Seidensticker, 1991; Sørensen, 1987; ¨ dberg, 1986). O Stereotypies are generally perceived as indicators of relatively poor welfare (see e.g. review by Mason, 1991). Whether this perception is correct has been subject to some controversy (see e.g. Mittelman et al., 1991). In fact, a recent meta-analysis found that while stereotypies were most often linked with the poorest environments, stereotypies within these environments were most often ‘‘linked with good welfare’’ for the individuals that engaged in
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these behaviours (Mason and Latham, 2004). As suggested by Mason et al., 2007, the occurrence of stereotypies might therefore be more useful to pinpoint poor environments for the captives, than it would be to pinpoint individuals with relatively poor welfare. However, exactly what constitutes ‘‘welfare’’ has been subject to dispute for centuries (see e.g. Sandøe and Christiansen, 2008 for the necessary basis of any discussions addressing animal ethics and welfare). At present it is broadly recognized that the concept of animal welfare both has a mental and a physical aspect, interacting with each other. Attempts to estimate mental welfare can be conducted in many ways (see e.g. Baumans, 2005; Dawkins, 2003). However, as expressed by Dawkins (2006), ‘‘Animal consciousness is central to the study of animal welfare but is still, tantalizingly, the ‘‘hard problem’’ and needs to be respected as such’’. Physical welfare on the other hand can basically be equated with the biological term ‘‘fitness’’ (a special case of ‘‘inclusive fitness’’ conceptualized by Hamilton, 1964), the essence of which is that the animal leaving the largest number of viable offspring has the highest fitness. Anything that can diminish the animals potential in this regard constitutes reduced fitness and, hence, reduced welfare. Consequently, indicators of poor welfare include measures such as reduced life expectancy, impaired reproduction, disease, immunosuppression, and behavioural anomalies (Broom, 1991a,b). To sum up, there seem to be no simple truth when it comes to defining animal welfare and no single measurement can estimate welfare with confidence (Mason and Mendl, 1993). Bank voles are well suited for studies of stereotypic behaviour since they readily develop a suite of easily recognisable stereotypies, as a role of thumb provided they are born in captivity and housed in barren cages (Cooper and Nicol, 1991, 1994; Schoenecker et al., 2000; Sørensen, ¨ dberg, 1986). The 1987; Sørensen and Randrup, 1986; O smaller/more barren the cage and the more restricted concerning possibilities for social contacts, the more frequent are the voles developing stereotypies (Cooper ¨ dberg, 1987). Large et al., 1996; Sørensen, 1985, 1987; O differences in individual levels of stereotypies among bank ¨ dberg, 1986, who suggested voles were first published by O that these differences probably were due to individual genetic differences in the predisposition to interact with discrete stimuli early in life. Later experiments with selective breeding resulted in a seven-fold difference in the proportion of offspring developing stereotypies (Schoenecker and Heller, 2000) and suggests the potentials in developing lines of high/low stereotypers and search for differential gene-expression relevant to the main neurotransmitters connected with development of stereotypies (e.g. serotonin, dopamine and gamma-aminobutyric acid). Stereotypic behaviours of the types occurring in captivity have never been described among voles in nature, and only once among wild caught voles maintained in captivity (Schønecker, 2009). Beside the inherent problem of long-term observations of cryptic animals preferring to be under cover, other factors could explain this discrepancy. For instance insufficient time to develop stereotypies in the wild (see discussion in Schønecker,
2009), lack of frustrating or stressful experiences among young voles in the wild (Schoenecker and Heller, 2000) combined with negative selection pressure by predators. It is therefore difficult to interpret the apparent strong genetic component in captivity-induced development of stereotypies. If such ‘‘stereotypy-genes’’, or better ‘‘segregating units’’ (Bruell, 1962), influencing proneness to develop stereotypies in captivity could be identified, they must at least be fitness neutral in the wild and the reason for their presence could be because they are situated near other segregating units influencing trait(s) more important to the fitness of wild-living voles. Such traits could e.g. be related to fecundity. In this retrospective case-control study of data from two colonies of Danish bank voles the aim was to examine whether stereotyping voles in the laboratory could have an adaptive advantage compared with non-stereotypers as reflected in their relative weight gains through a period of 6 months, capacity to survive barren conditions, and in their reproductive success. 2. Methods 2.1. Ethical note Animal care and use conformed to institutional policies and guidelines (University of Copenhagen, Denmark) and were in accordance with the ethical guidelines proposed by ISAE Ethics Committee (2002) and the International Guiding Principles for Biomedical Research Involving Animals (1985). The studies briefly mentioned in Section 2.4 were conducted under license from the Animal Experiments Inspectorate, Denmark. 2.2. General approach This study is based on retrospective analysis of data obtained through the maintenance and observations of two separate colonies of Danish bank voles, founded and housed at the University of Copenhagen, 1995–1997 and 2000–2003. Known or suspected biases which might interfere with the results have been excluded by a priori selection of three defined subgroups (see below). 2.3. Animals and housing The first colony was founded to study heritability of proneness to develop stereotypical behaviours. Earlier work had shown single housing in barren cages to result in far more stereotypies compared to housing in enriched ¨ dberg, 1987). Barren cages (Sørensen, 1985, 1987; O housing was consequently chosen to (1) reduce the number of voles necessary to achieve a proper sample size of stereotyping offspring in F2, vis-a`-vis the recommendations of the ‘‘3Rs’’ (Russell and Burch, 1959); (2) ensure no interactions between development of stereotypies and the inevitable cage hierarchy among group housed bank voles (Sørensen, 1987) and (3) ensure a reliable estimate of first emergence of stereotypies. The second colony was founded to follow up on the accidental discovery during the work with the first colony
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of a new human model of diabetes, based on polydipsic captive bank voles (Schoenecker et al., 2000; Freimanis et al., 2003). Polydipsia is so-called excessive water intake and single housing in barren cages produced a larger fraction of polydipsic voles compared to group housing in enriched cages (38% vs. approx. 20%; Schoenecker et al., 2000; Sørensen and Randrup, 1986). Furthermore, different types of pre-weaning stressors were at the time known to modulate the frequencies of voles developing diabetes in both directions (Freimanis et al., 2003). Consequently, single housing in barren cages were again chosen to reduce the number of voles; disable any cage hierarchy related interactions with the development of diabetes and enable a reliable measurement of individual daily water intake. Briefly, founders of the two colonies (N = 166) were captured in the forests of Zealand, Denmark and housed as single pairs in transparent cages (14.5 21.5 37.5 cm) provided a wire lid with feed hopper and water bottle. Food (Altromin 1324) and water were available ad lib and the cages were supplied with a woodcutting bed and enrichment in the form of toilet paper and paper rolls. Males were always removed from the females immediately after a birth had been observed and placed in a smaller barren cage (13.5 16.0 22.5 cm). Pups from the first colony (N = 518) were weaned after 18–53 days where all pups from the second colony (N = 525) were weaned after 21 days exactly. Pups were housed singly in small barren cages, unless used as breeders. Roughly 30% of the captive born voles were on one or more occasions used as breeders, during which time they were housed as single pairs in larger enriched cages as described above. Both F1 and F2 in both colonies were completely outbred where 61% of the F3 voles in the second colony resulted from selective breedings involving single pairs of full siblings. Maintenance and observations were carried out on a daily basis and lasted typically 2–4 h/ day.
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development of stereotypies among voles (Cooper and Nicol, 1994). Further observations addressed various measures related to fecundity, age of ‘‘natural death’’ or ‘‘exit’’ from the colony. ‘‘Natural death’’ is used to designate any unexplained death, i.e. deaths without obvious cause or prior signs of deteriorated health and moribundity, and affected 257 (21%) of the 1209 voles in the colonies. ‘‘Exit’’ from the colony could be due to a number of reasons. The prime reason was culling, or translocation to original trapsite, for logistic reasons (lack of available space/cages; final termination of colonies) or no further scientific purposes (562 voles; 46%) followed by transfers to the care of other researchers (188 voles; 16%). 142 voles (12%) were sacrificed in order to provide biological samples in relation to our further studies of our new diabetic human model and 46 voles (4%) died in accidents, e.g. during attempt to escape, or a defect water bottle flooding the cage. Five voles (0.4%) died as a consequence of stressful encounters with aggressive cage mates and 7 voles (0.6%) were euthanized for humane reasons (see Section 2.5). Only pups from the second colony were weighed when weaned and some of the second colony F1 (N = 118) were in addition weighed at the ages 1, 2, 3, 4, 5, and 6 months during which time all were singly housed. 2.5. Humane endpoints If a vole showed a moribund appearance, or seemed to be in a state of pain and suffering, it was anaesthetized in a mixture of CO2 and O2, followed by cervical translocation. Voles used to provide biological samples were sacrificed in a similar manner. Moribundity could be indicated by a combination of lethargic movements, abnormal lowering of attention to surroundings, tousled fur or e.g. significantly decreased ADW among diabetic voles. All voles present in the facility were routinely inspected visually at the end of the day for any signs of distress, disease or pain.
2.4. Observations and classifications 2.6. Selection of data The average daily water intakes (ADW) were calculated for all solitary voles from weaning and until death/exit. Water bottles were weighed and changed at least once a week and data and exact time for the procedure were then used by a standard database program (Filemaker v.2.1 for Mac) to calculate the ADW since it had been shown that an ADW exceeding 21 ml is a reliable marker of type 1 diabetes in Danish bank voles (Freimanis et al., 2003; Niklasson et al., 2003; Schoenecker et al., 2000; Schønecker et al., submitted). The most common types of stereotyped behaviours among Danish bank voles were (decreasing order) backward somersaulting, high-speed jumping, pacing following a fixed route and windscreen wiper movement (Schoenecker et al., 2000). Non-diabetic voles, which exhibited any such stereotypies in bouts of at least five repetitions, were classed as Ster and age of first observation were noted. The vole was then moved away from the still non-stereotyping voles (classed N-Ster), primarily to make it easier to spot new cases of Ster secondary, to mitigate any influence by a possible ‘‘neighbour effect’’ on
The following three groups (A–C; N total = 169; n males/ females = 37/76 (F1) and 31/25 (F2)) have been selected for further analysis and since 18 voles are included in two groups (11 appears in both A and B; 7 appears in both A and C), the total of groups (N = 187) exceeds the actual number of voles considered in this retrospective study. 2.6.1. Group A: This group is used to analyse if Ster and N-Ster differs in weight gain between weaning and age 6 months (Section 3.1 and Table 1). The voles were weighed at weaning and at the ages of 1, 2, 3, 4, 5 and 6 months. Since it is reasonable to assume an interaction between development of diabetes and development in weight, only data from voles which remained non-diabetic, and survived, all through the 6 months weighing period are included in Group A. Furthermore, since pups from diabetic females weighs more when weaned at age 21 days than pups from nondiabetic females (Schønecker et al., submitted), only pups from non-diabetic females have been included. This
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Table 1 Weight (g) of Ster and N-Ster from group A (n = 40) when weaned and through their first 6 months. Weights are expressed as 25/50/75 percentiles with the actual number of Sters/N-Sters a given month in square brackets (A). The two columns marked (B) describe weights of voles according to their final classing as either Ster (n = 18) or N-Ster (n = 22) at age 6 months. Pair-wise test results are presented in p (A) and p (B).
Weaning 1 Month 2 Month 3 Month 4 Month 5 Month 6 Month
Ster (A)
N-Ster (A)
N.A. [0] N.A. [0] 18.4/22.3/24.8 17.0/18.4/22.3 18.9/19.7/22.6 19.4/21.0/22.6 20.7/22.7/26.2
11.0/11.9/12.6 15.4/16.9/18.7 18.0/20.5/23.3 18.7/21.3/24.8 20.5/22.2/25.5 22.2/23.7/27.4 22.7/25.7/29.0
[7] [11] [16] [18] [18]
[40] [40] [33] [29] [24] [22] [22]
selection results in data from 20 F1 males and 20 females from the second colony which all remained singly housed for the first 6 months. A total of 18 voles (n males/ females = 6/12) were classed as Ster within 6 months and first sign of stereotypical behaviours were observed between the first and second month. 2.6.2. Group B: This group is used to (1) study any interaction between weight at weaning and subsequent development of stereotypical behaviours (Section 3.2) and (2) analyze survival of Ster and N-Ster voles using the Kaplan–Meier method (Section 3.3). All breeders have been excluded from this group since breeders differ in several important variables (e.g. individual number and age of pairings). All offspring from diabetic females are excluded, as are all captive born voles, which were not weighed when weaned. This selection reduce the sample size to 54 males and 46 females from the second colony (F1 and F2), all weaned at the age of 21 days and all housed singly in small barren cages. They weighed 11.04 1.43 g (mean SD) when weaned and were subsequently classed as either LIGHT (weight mean weight) or HEAVY weanlings (weight > mean weight). Proneness to develop stereotypical behaviour in captivity has a strong heritable component (Schoenecker and Heller, 2000) and it is therefore relevant at this point to note that the proportion of offspring from Ster parents was statistically the same among both LIGHT and HEAVY weanlings (43% vs. 40% respectively, Chi = 0.088, df = 1, p = 0.7662). Sixty-two of these 100 Group B voles were eventually classed as Ster and remained a median of 489.5 days (25/75 quartiles = 454/652) in captivity. The remaining 38 N-Ster spend 255 days (median) in captivity (25/75 quartiles = 109/555). Lengths of captivity differed significantly (Z = 2.941, p = 0.0033). 2.6.3. Group C: This group is used to analyse variables of relevance to fecundity (Section 3.4 and Table 2). Only data from (nondiabetic) females classed as either Ster or N-Ster both when paired and when exiting the colony are included. All breeding pairs were un-related and consisted of either two Sters or N-Sters, leaving data from 28 Ster and 19 N-Ster females for analysis. Bank voles exhibit post-partum oestrus (Clarke and Hellwing, 1983) and data from any such resultant litters are included. The median ages for first pairing were 178 days and 180 days respectively (25/75
p (A)
Ster (B)
N-Ster (B)
p (B)
N.A. N.A. 0.6057 0.1418 0.0727 0.0045 0.0363
10.9/11.6/12.2 14.9/16.0/16.7 17.2/18.3/22.4 17.0/18.3/22.1 18.1/19.4/22.6 19.4/21.0/22.6 20.7/22.7/26.3
11.0/12.1/13.0 16.9/18,6/19,5 19.8/21.7/24.2 19.6/21.7/25.9 21.4/22.5/25.6 22.2/23.7/27.4 22.7/25.7/29.0
0.1735 0.0003 0.0296 0.0098 0.0114 0.0045 0.0363
quartiles (days) = 171/244 (Ster) and 159/278 (N-Ster); Z = 0.358, p = 0.7205). The two groups of females did not differ either in their weight when weaned, or in the time they spend in the colonies (Z 1.17, p 0.242 in both cases). Finally, barren and fertile voles did not differ regarding the age when mated, either within the Ster, NSter or when both classes were pooled (Z 1.388, p 0.1653) 2.7. Statistics With few exceptions, data did not satisfy requirements to parametric tests so non-parametric tests were mainly used instead. These were the Mann–Whitney U-test (differences in weight developments and fecundity related measures); Chi Square (incidence of Ster among LIGHT/ HEAVY weanlings; incidence of ‘‘natural death’’ among Ster/N-Ster adults; pre-weaning mortalities); Fisher Exact (pre-weaning mortalities; fraction of barren/unreceptive females among Ster and N-Ster) and the Kaplan–Meier method of survival analysis (onset age of Ster dependant on status as LIGHT/HEAVY weanling; longevity). Pairwise tests in the Kaplan–Meier analysis were always performed using the Breslow-Gehan-Wilcoxon test. A t-test is used in Section 3.2. Data are described using 25, 50 and 75 percentiles except if normal distributed. All tests were two-tailed and corrected for ties if necessary. Level of significance was set a priori at 0.05.
Table 2 Fecundity measures derived from pairs of Ster and N-Ster from group C. Duration of gestation period (GP), size of litters, number of weanlings and pre-weaning pup mortality (PM) in both first litter and second litters resulting from post-partum matings. Data presented as 25/50/75 quartiles with number of valid observations in square brackets. Number of dead (D) and weaned (W) pups are shown in parentheses and pair-wise test results are presented in column p. N-Ster breedings
Ster breedings
p
GP 1st litter n born n weaned 1st litter PM
20/23.5/46 [14] 4/4.5/5 [14] 3.75/4/4.25 [13] 18% (11D/51W)
19/19/21 [25] 3/4/5 [25] 2.5/4/5 [24] 17% (17D/84W)
0.0190 0.7062 0.7790 0.8811
GP 2nd litter n born n weaned 2nd litter PM
19/20/21 [10] 4/5.5/6 [10] 4/5/6 [10] 6% (3D/48W)
18/19/19 [12] 4.5/6.5/7 [12] 2.5/6/7 [11] 23% (17D/56W)
0.0053 0.2403 0.4540 0.0095
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3. Results 3.1. Development in weight (Ster vs. N-Ster) the first 6 months All though voles classed as Ster from Group A (n = 40) were lighter (numerically) already from the third month, this difference in median weight only reached significance during the fifth and sixth month (see Table 1). However, grouping the voles according to their final class as Ster (n = 18) or NSter (n = 22) at age 6 months showed that individuals that subsequently developed stereotypies were significantly lighter already by the first month and through the remaining period. Lastly, LIGHT weanlings (weight median when weaned; n = 20) from group A continued to weigh less than HEAVY weanlings (weight > median when weaned; n = 20) from age 1 months to the last weighing at age 6 months (2.097 Z 3.167; 0.0015 p 0.036). 3.2. Weight at weaning and subsequent development of stereotypies In order to see whether weight at weaning could influence the age at which stereotypical behaviours developed, a larger sub-group (Group B: n = 100) were likewise classed according to their weight at weaning as either LIGHT (n = 47) or HEAVY (n = 53) weanlings. Comparing data from LIGHT with HEAVY voles in a survival analysis showed no significant difference regarding onset age of stereotypical behaviours (Chi = 1.476, p = 0.2244), a result which was repeated in subsequent comparings of onset ages among LIGHT and HEAVY voles descending from either two Ster (n = 32) or two N-Ster (n = 28) parents (Chi 0.166, df = 1, p 0.4176 in both cases). Lastly, there were also no difference between LIGHT (n Ster/total = 19/31) and HEAVY (n Ster/total = 17/38) pups regarding the number classed as Ster at age 6 months (Chi = 0.329, df = 1, p = 0.5665). Where Section 3.1 showed that 6 months old voles classed as Ster were lighter than those classed as N-Ster already from the age of 1 month, group B extend the finding to a significant lighter weight of Ster already at the time of weaning at age 21 days (mean SD (g) = 11.333 1.449 (N-Ster; n = 55) vs. 10.671 1.33 (Ster; n = 45); t = 2.357, df = 98, p = 0.0204). 3.3. Survival of Ster and N-Ster There were no sex differences in group B survival within voles classed at exit as Ster (n = 62), N-Ster (n = 38), or when both classes of voles were pooled (three tests: Chi 3.71, df = 1, p 0.0541) so the groups could be directly compared. The two lines in Fig. 1 describes the fraction of Sters and N-sters alive as a function of time and shows a superior survival of Sters (Chi = 9.588, p = 0.0020). Even though the Sters were housed in barren cages for almost twice as long time as the N-Sters (see Section 2.6), they tended to have a lower frequency of ‘‘natural deaths’’ (7 Ster vs. 10 N-Ster; Chi = 3.77, p = 0.0522). Considering voles classed as Ster weighed significantly less than those classed as N-Ster, and LIGHT weanlings
Fig. 1. Kaplan–Meier survival curves for 38 N-Ster (filled circles = 10 events of deaths without obvious causes) and 62 Ster (open squares = 7 events of deaths without obvious causes). The abscissa denotes ages in days and the ordinate denotes the fraction of survivors.
continued as a group to be LIGHT adults (Section 3.1), weight might be a confounding variable, influencing survival. A subsequent survival analysis showed no significant influence of weight at weaning among either the Sters (n LIGHT/HEAVY = 31/31; Chi = 0.344, df = 1, p = 0.5576); the N-Sters (n LIGHT/HEAVY = 16/22; Chi = 0.102, df = 1, p = 0.7494) or both classes pooled together (n LIGHT/HEAVY = 47/53; Chi = 0.079, df = 1, p = 0.7787). 3.4. Fecundity of Ster and N-Ster As seen in Table 2, Ster females (group C) delivered and weaned statistically the same number of pups, as N-Ster females (p > 0.05 in both cases). However, the time it took to deliver the first litter, and the time between the births of first and second litters were significantly shorter among the Ster females (Z 2.345, p 0.0190 in both cases). Preweaning mortalities were statistically the same in the first litters (17–18%) where the highest second litter pup mortalities were seen among offspring from Sters (23% vs. 6%; Chi = 6.724, df = 1, p = 0.0095). The prevalence of barren/unreceptive females was statistically the same between Ster and N-Ster females (%/n barren/n total; Ster vs. N-Ster: 11%/3/28 vs. 26%/5/19; Chi = 1.951, df = 1, p = 0.1625). 4. Discussion The main results of this study were that voles which eventually developed stereotypies (1) weighed less when weaned at age 21 days than permanent non-stereotypers (2) delivered their litters faster (shorter gestation period) and (3) showed increased survival under barren housing conditions. Furthermore, previous findings of an association
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between low weight at weaning and low weight in adulthood (Wu¨rbel and Stauffacher, 1997) were replicated in this study. Reduced growth is one of the measures indicating poor welfare (Broom, 1991a,b). Stereotypers in this study weighed significantly less than same-age non-stereotypers, raising the question whether increased proneness to develop stereotypies are linked to lighter weight or, alternatively, whether the performance of stereotypies per se cause lighter weight. The possibility that stereotypers are lighter (and fitter) simply because they usually spend hours with these ¨ dberg, 1986; pers. physically challenging behaviours (O observations) would a priori appear the most parsimonious explanation. Analogous to the result of this study, Jeppesen et al., 2004 found that stereotyping female adult mink weighed significantly less than mink showing no stereotypies and, in addition, found indications that it was in fact the stereotypies per se which caused the reduction in bodyweight. On the other hand it could be that relatively lower weight at weaning somehow predisposed the animal to develop stereotypies. Studies using ICR mice had shown that low weight at weaning reduces fitness in the longterm leading to the hypothesis that lighter weanlings are more prone to develop stereotypies due to a higher motivation to rejoin their mother and suckle (Latham and Mason, 2004, Wu¨rbel and Stauffacher, 1997). Lighter weanlings should, accordingly, be more motivated to engage in vigorous escape attempts taking the forms of rearings, lid climbing or jumps. These activities could lead to a progressive sensitization of specific neural pathways (vis-a`-vis a suggestion by Dantzer, 1986) and subsequently a higher probability of developing into stereotypies (Wu¨rbel and Stauffacher, 1998). Prematurely weaned ICR mice had in fact been shown to perform stereotypic wire-gnawing at a higher level as adults than ICR mice with a higher weight as weanlings (Wu¨rbel and Stauffacher, 1997). Taken together, my results just partly support the hypothesis that smaller weanlings should be predisposed to develop stereotypies. Voles classed as stereotypers at age 6 months did in fact weigh less already when weaned at age 21 days compared to those classed as nonstereotypers. However, neither age at onset, nor incidences of stereotypies were significantly influenced by the weight at weaning in these voles. Jeppesen et al., 2004 likewise found no correlation between weight at weaning and subsequent proneness to develop stereotypies in their study on mink. However, voles do show a trend to increase the intensity by which they perform their stereotypies with age and levels of stereotypies closely follow levels of ¨ dberg, 1986; personal observation). general activity (O Furthermore, Danish bank voles show a major peak of both stereotypies and general activity at 22.30–01.00 (Schoenecker and Heller, 2003) and screening for new stereotypers were for practical reasons carried out during the day. Studies employing electronic surveillance during the dark hours would consequently be better suited to provide a conclusive answer to the question of whether low weight at weaning predispose the voles to develop stereotypies.
Reduced life expectancy is another commonly employed measure of poor physical welfare (Broom, 1991a,b). In this study, stereotyping bank voles showed superior survival capacity as compared to that of non-stereotypers. To my knowledge, only three other studies have touched upon the issue of differential survival between stereotyping and nonstereotyping bank voles. Cooper and Nicol (1996, citing Cooper 1992) state ‘‘There was no difference in mortality or fecundity of laboratory and wild caught voles, so there appeared to be no selective advantage to stereotyping.’’ Also Sørensen and Randrup, 1986 noted a significantly increased mortality among wild caught voles due to their frequent development of polydipsia when compared to laboratory born bank voles, of which some developed stereotypies. In retrospect this observation of differential survival must have been confounded by the inclusion of diabetic voles, which do have considerable reduced life expectancies compared to that of non-diabetics (Schoe¨ dberg, 1987 noted two necker et al. submitted). Lastly, O deaths among 44 stereotyping voles before age 60 days and three deaths before age 90 days among 132 nonstereotyping voles. A possible explanation for the superior survival of the stereotypers could be their relative lighter weight since it has been known for many years that lighter animals live longer than more heavy/obese animals (Heilbronn and Ravussin, 2003; McCay et al., 1935). However, considering that light weanlings remained light adults and that there were no significant differences in survival between light and heavy weanlings, the conclusion must be that development of stereotypies per se was a beneficial factor for the voles when kept under these impoverished conditions. Whether the mechanism by which stereotypies influence survival is due to a better physical condition or if mental processes interact with physical welfare should not be determined based on this study. At this point it is relevant to note that Buchalczyk, 1970 found average life spans to be 604 days for reproducing pairs; 363.5 days for barren pairs and 185.25 days for voles housed in single sex communal cages (6–8 animals/cage). My unpublished data shows that both stereotypers and non-stereotypers, when used as breeders for shorter or longer periods, increased their survival to the point of virtually no mortality (4/126 deaths among stereotypers; 0/83 deaths among nonstereotypers). Both groups, furthermore, spend significantly longer time in captivity (median captivity stereotypers/non-stereotypers: 480/499 days) than the voles described in group B. Lastly, both reduced fertility and gestation periods are typically considered indications of poor physical welfare (Broom, 1991a,b). Stereotyping female bank voles showed the shortest interval between introduction of the male and subsequent birth of a litter and a shorter gestation period when mated post-partum. The numbers of pup’s born/ weanlings were statistically the same among stereotypers and non-stereotypers in this study, as was the proportion of barren or unreceptive females. To my knowledge, again only two other studies besides Cooper and Nicol (1996, citing Cooper 1992) has mentioned the issue of fecundity among stereotyping and non-stereotyping bank voles. Sørensen and Randrup, 1986 noted how stereotypies interfered with
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the normal nurturing by the mother since she would sometimes perform stereotypies while carrying the pup in her mouth, usually leading to the death of the pup and ¨ dberg, 1987 noticed a mortality of 21.8% before the age O of 30 days (not separating between stereotypers and non-stereotypers). In this study, pup mortalities in the first litter were statistically the same between stereotypers and non-stereotypers where the second litters showed significantly increased pup mortality among offspring from stereotypers. The subject has been studied in mink (Bildsøe et al., 1991; Hansen, 1993; Jeppesen et al., 2004), where stereotypers deliver, and wean, larger litters than nonstereotypers, while experiencing less pup mortality. However, the observations of differential fecundity in the 2004 study could best be explained by the lower bodyweight of the stereotypers since leaner mink were more fertile than more obese mink, irrespective of stereotypic status. A later study on mink from another farm found no difference in reproduction between high- and low-stereotyping lines, which point to the importance of farm management (Svendsen et al., 2007). 5. Conclusion This study shows that stereotypies among bank voles were associated with both superior survival and a shorter interval between consecutive births when compared to that of non-stereotypers, both factors suggestive of higher physical welfare. However, the mechanism by which stereotypies influence these factors should not be determined based on this study. Bank voles show, as mentioned, indications of heritability behind proneness to develop stereotypies (Schoenecker and Heller, 2000), just as do deer mice (Powell et al., 1999) and African striped mice (Jones et al., 2008; Schwaibold and Pillay, 2001), and models such as these would also for this reason seem well suited for further basic research in the fundamentals of stereotypical behaviours and its consequences. Acknowledgement I would like to thank Jan Ladewig for commenting previous drafts and general support; Knud Erik Heller for past discussions and for providing the necessary facilities to house the vole colony and Jens Lodal for lending equipment to capture the voles. Lastly I would like to thank two anonymous referees for their valuable comments. The study was in part supported by donations from the Danish Research Council and Apodemus AB, neither of which had any influence on either study, analysis or interpretations/ presentation. References Baumans, V., 2005. Science-based assessment of animal welfare: laboratory animals. Rev. Sci. Technol. 24, 503–513. Bildsøe, M., Heller, K.E., Jeppesen, L.L., 1991. Effects of immobility stress and food restriction on stereotypies in low and high stereotyping female ranch mink. Behav. Process. 25, 179–189. Broom, D.M., 1991a. Animal welfare: concepts and measurement. J. Anim. Sci. 69, 4167–4175. Broom, D.M., 1991b. Assesing welfare and suffering. Behav. Process. 25, 117–123.
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