Springer-VerlagTokyohttp://www.springer.de101640289-07711439-5444Journal
of EthologyJ
EtholLifeSciences21110.1007/s10164-006-0211-9
J Ethol (2007) 25:95–98 DOI 10.1007/s10164-006-0211-9
© Japan Ethological Society and Springer-Verlag Tokyo 2006
SHORT COMMUNICATION
V. Ricankova • R. Sumbera • F. Sedlacek
Familiarity and partner preferences in female common voles, Microtus arvalis
Received: January 4, 2006 / Accepted: April 26, 2006 / Published online: May 24, 2006 Japan Ethological Society and Springer-Verlag 2006
Abstract Captive female common voles (Microtus arvalis) had a clear social preference for familiar males in a standard preference test. Cohabitation for a short period resulted in preferences for familiar partners, and females spent eight times more time in body contact with a familiar male than with an unfamiliar male. Females also displayed strangerdirected aggression. Our results suggest that the common vole is a species with selective partner preferences and a tendency to form tight social relationships and stable male–female associations. Key words Social organization · Aggression · Common voles · Mate choice · Pair bond
Introduction Familiarity is an important phenomenon affecting aggression, kin recognition, mate choice, and group formation in microtine voles (e.g. Krebs 1970; DeVries et al. 1997; Yu et al. 2004). Functionally, social familiarity is thought to reduce aggressive tendencies and to promote pair-bond formation and mating. In the laboratory, pair bonding is indexed by two easily defined types of behavior: 1. partner preferences in a choice apparatus (Ferguson et al. 1986; Shapiro et al. 1986; Newman and Halpin 1988); and 2. selective aggression directed toward intruders but not family members (Getz et al. 1981).
V. Ricankova (*) · R. Sumbera · F. Sedlacek Department of Zoology, Faculty of Biological Sciences, University of South Bohemia, Brani sˇovská 31, 37005 Ceske Budejovice, Czech Republic Tel. +420-387-772240; Fax +420-385-310366 e-mail:
[email protected] F. Sedlacek Institute of Systems Biology and Ecology, Na Sádkách 7, 37005 Ceske Budejovice, Czech Republic
The effect of familiarity on female social preferences among microtines has been examined in monogamous prairie voles (Microtus ochrogaster) and in polygamous meadow voles (M. pennsylvanicus) and montane voles (M. montanus) (Shapiro et al. 1986; Williams et al. 1992; Salo and Dewsbury 1995; Carter and Roberts 1997). Monogamous female prairie voles had no preference based on familiarity without mating, whereas polygamous montane voles spent more time with the unfamiliar male (Shapiro et al. 1986). More careful examination of laboratory results revealed, however, that although so-called monogamous prairie vole females were willing to mate with an unfamiliar male they rarely remained in physical contact with the stranger after mating (Carter and Roberts 1997). In the experiment examining multi-male mating by paired and unpaired female prairie voles, females mated most often with males with whom they spent the most time. Social preference was thus a good predictor of sexual preference (Wolff et al. 2002). In contrast, polygamous species had much less social contact than did monogamous prairie voles and did not develop clear partner preferences (Wilson 1982; Ferguson et al. 1986; Shapiro et al. 1986). Although North American species have been studied in detail, there is relatively little information about partner preferences and pair-bond formation in Eurasian microtines. Among Eurasian microtines, the common vole M. arvalis is the most widespread Palearctic vole species. This species has been a subject of many studies of, mainly, population changes, disease and parasite spreading, and predator–prey relationships (Krebs 1970; Hoogenboom and Dijkstra 1987; Millon and Bretagnolle 2005). Although reproduction strategies and patterns of mate choice may significantly affect population dynamics, mating behavior in common voles remains unstudied and data relating to social organization vary substantially. The objective of this study was to determine whether female common voles are capable of forming selective partner preferences with the opposite sex partner under laboratory conditions.
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Materials and methods Subjects The common voles (M. arvalis) tested were first-to-third generations of offspring of ancestors caught near the town Zliv in South Bohemia. Animals were housed in standard polycarbonate rodent cages (Velaz T3, T4) with wood shavings as bedding. They had access to mixed grain and alfalfa pellets (ST1 and MOK Velaz, Prague) and water ad libitum. Food was supplemented with hay, fresh grass, and carrot. Animals were kept under natural photoperiod and temperature cycles. Most experiments were conducted during the Central Europe summer and early autumn of 1998 and 1999. Thirty-eight male and nineteen females were used for this experiment. All animals were laboratory bred, at least 40 days old, with no previous sexual experience. Before testing, the animals were housed in same-sex sibling groups. Brothers from the same litter only were used in all experiments, to reduce differences between males other than familiarity. Tested males and females in one experiment were unrelated. Each male and female was subject to testing in one experiment only and females had no previous exposure to either stimulus male before testing. Apparatus and procedure The test cage was a clear glass terrarium (60 × 30 × 30 cm). The outer sides of its walls were covered with white paper to isolate the interior space visually. The apparatus was divided into three equal-sized compartments – end compartments for the males and a central neutral area. Two days before testing, males were anesthetized with ether, fitted with collars made of key-chain material, tethered, and given 1-h adaptation to the tether procedure and apparatus. On the day before testing, females were allowed 1-h exploration of the test cage in the absence of males. On the day of testing the first male was placed in the test cage and permitted 20 min for habituation. After this adaptation period a female was placed into the neutral area to become familiar with the first male. After 30 min the female was removed from the test cage and the second male was tethered and allowed 20 min for habituation. The female was then reintroduced and her behavior was observed for the subsequent 30 min (according to Salo and Dewsbury 1995). Experiments were videotaped. Wood shavings used as bedding were changed before each test and the whole apparatus was cleaned with ethanol and water between trials. The experimental field was illuminated by a single 25-W red light bulb. Female behavior was categorized for each male separately – familiar versus unfamiliar male (Salo and Dewsbury 1995). Female behavior was classified according to the categories: – sniffing (olfactory exploration of the face, anogenital region, or other body areas), – aggression (attacks, boxing, and biting behavior),
– side-by-side contact (sitting or lying stationary in contact with one another), – mounting, – visiting male’s area (time spent in the area of each male), and – time spent in the neutral arena (mostly exploration activity). During the test, the frequency (number), total duration (in seconds), and the first occurrence of a particular activity – latency – for all behaviors were recorded using “Activities” version 2.1 software for behavioral studies (Donat and Vrba 1993). The Wilcoxon matched-pair test was used to compare female behavioral responses to familiar versus unfamiliar stimulus voles. Statistica 5.1. for Windows was used for all analyses.
Results The results obtained are summarized in Tables 1, 2, and 3. Female common voles spent only a short time in the neutral section of the arena during experiments. The mean time spent there was 67.33 s (SE = 20.98) i.e. 3.74% of the length of the experiments. Tested females clearly distinguished between familiar and unfamiliar males. They spent more time visiting the familiar male’s area (P = 0.024) and they spent eight times more time in contact with a familiar male (P = 0.003) (Table 1). Duration of aggressive behavior aimed at an unfamiliar male was longer than aggression toward a familiar male, although the difference was not statistically significant (P = 0.074). Frequency of aggressive acts aimed at unfamiliar males was significantly higher (P = 0.046), even though contact and visit frequency was more evenly distributed between familiar and unfamiliar males (Table 2). Females sniffed an unfamiliar male more frequently and mounting frequency was also higher for unfamiliar males, although the differences were not statistically significant. The remarkable difference between mean duration and frequency of mounting for familiar and unfamiliar males (cf. Tables 1, 2) was caused by two unfamiliar males frequently mounting females. Removing these values from analysis did not change the significance (Z = 0.70, P = 0.48 for mounting duration and Z = 0.34, P = 0.74 for mounting frequency). Females first sniffed the familiar male (P = 0.031). Latency of the first body contact with a familiar partner was shorter than with an unfamiliar partner (P = 0.053) (Table 3). Copulation was observed in one experiment only and the female copulated with both males. The experiment was removed from the analysis.
Discussion The results of this study support the opinion that the common vole, M. arvalis, is a social species with a tendency to
97 Table 1. Preferences of female common voles for familiar versus unfamiliar males (Wilcoxon matched-pair test). Total duration (s) of female behavioral activity during a 30 min experiment Familiar (N = 18)
Measure
Contact Mounting Sniffing Aggression Visit
Unfamiliar (N = 18)
M
SE
M
SE
896.6 1.78 28.3 3.87 12,039.7
165.9 0.87 7.56 1.84 1,454.5
104.0 6.86 39.5 12.7 5,327.6
43.7 4.59 11.2 4.44 1,328.9
Z
P
2.94 0.46 0.15 1.78 2.25
0.003** 0.65 0.87 0.074 0.024*
P based on Wilcoxon matched-pair test; M mean, SE standard error *P < 0.05; **P < 0.01
Table 2. Preferences of female common voles for familiar versus unfamiliar males (Wilcoxon matched-pair test). Frequency (no.) of female behavioral activity during a 30 min experiment Measure
Contact Mounting Sniffing Aggression Visit
Familiar (N = 18)
Unfamiliar (N = 18)
M
SE
M
SE
7.26 0.89 14.3 2.74 8.05
1.41 0.35 3.19 1.14 2.25
5.31 4.0 24.4 9.74 7.95
2.07 2.55 7.35 3.42 2.71
Z
P
1.31 0.77 0.85 1.98 1.38
0.19 0.44 0.39 0.046* 0.17
P based on Wilcoxon matched-pair test; M mean, SE standard error *P < 0.05
Table 3. Preferences of female common voles for familiar versus unfamiliar males (Wilcoxon matched-pair test). Time from the start of the experiment(s) to the first recorded behavioral event of the female Measure
Contact Mounting Sniffing Aggression
Familiar (N = 18)
Unfamiliar (N = 18)
M
SE
M
SE
402.7 1319.9 363.1 1288.0
154.0 172.6 123.7 178.7
901.0 1248.2 734.2 1072.8
185.1 173.2 194.3 201.1
Z
P
1.94 0.05 2.16 1.17
0.053 0.96 0.031* 0.24
P based on Wilcoxon matched-pair test; M mean, SE standard error *P < 0.05
form stable male–female associations. Females had a social preference for familiar males and also displayed strangerdirected aggression. Cohabitation for a relatively short period of 30 min without mating resulted in preferences for a familiar male partner. Amount of time spent in body contact may be regarded as a measure of pair-bond tendency of the particular species. In general, a subject exhibits partner preference when it spends twice as much time in body contact with a familiar animal than with unfamiliar conspecifics (Insel et al. 1995). Female common voles spent eight times as much time in contact with a familiar male than with an unfamiliar male (Table 1). Female preferences were not because of the absence of exploration activity – each of the tested females visited both males.
Moreover, female common voles spent less than 4% of the total time in unsocial activity in the neutral arena, whereas monogamous female prairie voles (M. ochrogaster) spent as much as 13% of the total time in the neutral area and promiscuous montane vole females (M. montanus) up to 45% of the total time, in experiments with comparable design (Shapiro et al. 1986). Reduced unsocial activity and pronounced contact seeking behavior probably suggest strong tendencies of common voles to establish tight social bonds. Our results are in agreement with findings that common voles form family groups and males may remain with females on a long-term basis and take care of the offspring (Bashenina 1962; Mackin-Rogalska 1979; Gromov 2005). The pair bond between adult male and female is regarded as weak, however (Zorenko 1979; Boyce and Boyce 1988; Gromov 2004). DeJonge (1982) found that common vole males and females form stable pairs and defend a common territory under laboratory conditions. Males may remain with pregnant and nursing females and give some care to sucklings (DeJonge 1982). Nevertheless, social preferences observed during laboratory experiments cannot always be regarded a clear-cut measure of species’ social and mating systems and intraspecific social systems may vary as a function of environmental conditions (Lott 1991). For example, nonmonogamous species may engage in facultative partner preferences and parenting to offset the costs associated with harsher breeding conditions. Results from previous laboratory experiments reveal that even nonmonogamous meadow voles are capable of developing selective partner preferences and stranger-directed aggression (Parker et al. 2001). These abilities may have evolved to maximize reproductive success during the colder months of the year or under low population density during the summer breeding season. This selection may have favored the capacity of common voles, also, to facultatively display “monogamous” or “nonmonogamous” reproductive strategies. Although mating is not essential for partner-preference formation in monogamous prairie voles, preferences developed more rapidly when mating occurred (Williams et al. 1992; DeVries and Carter 1999). In our experiment, common vole females had remarkable social preferences for familiar males after cohabitation for 30 min only. For monogamous female prairie voles, cohabitation for 1 h was not sufficient for creation
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of social preferences for a male partner (DeVries and Carter 1999). Both male and female prairie voles required cohabitation for at least 6 h for establishment of significant partner preferences. Familiarity does not affect the amount of female aggressive interactions toward a stimulus male in polygamous meadow voles (Ferkin 1988). Parker et al. (2001) found that 24 h of social cohabitation was sufficient to reduce aggression toward partners in meadow vole females, but strangerdirected aggression appeared later, after delivery of the litter. Our results show that common vole females can establish stranger-directed aggression after only a short (30 min) cohabitation period. Eightfold differences between time spent in body contact with a familiar male compared with an unfamiliar male, and short latencies in sniffing and contact behavior directed to familiar males, suggest that familiarity probably plays an important role in the social behavior of M. arvalis. Although laboratory research does not conclusively prove that captive behavior occurs under free-living conditions, our laboratory evidence suggests pair-bond formation in M. arvalis may also occur in the wild. Thorough field study would help to clarify ambiguous aspects of social and mating behavior of common voles. Acknowledgements We thank Milena Prokopová, Lenka Bar cˇiová, Libor Weiter, and Katarina Luká cˇová for assistance with data processing and animal capture. We are grateful to Gil Dryden for correcting the English text. This research was supported by an institutional grant of ministry of education MSM 6007665801 and by a grant of the Czech Science Foundation GACR 206/05/2655.
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