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Social tolerance and proximate mechanisms of dispersal among winter groups of meadow voles, Microtus pennsylvanicus
Anim. Behav., 1990, 39, 346-351
Social tolerance and proximate mechanisms of dispersal among winter groups of meadow voles, Microtus pennsylvanicus WILLIAM
J. M c S H E A
National Zoological Park, Conservation and Research Center, Front Royal, Virginia 22630, U.S.A.
Abstract. Proximate mechanisms for movement among communal groups of meadow voles were examined during two winter seasons. Radiotelemetry and live trapping were used to identify group members and monitor the movement of voles. Paired encounters between individuals removed from the field indicated that aggression neither precipitated nor prevented movement of animals between groups during winter. Dispersal most often occurred in conjuction with loss of nestmates to predation. The removal of nestmates resulted in increased home range size and movement between groups for males, but not for females. With the onset of reproduction, aggression increased toward individuals from other groups, but not toward nestmates, Winter groups did not break up with the onset of breeding, but these groups were closed to the immigration of new members.
Dispersal is an important process in the population dynamics of many species (Chepko-Sade & Halpin 1988) and has received particular attention in explaining population fluctuations in microtines (Lidicker 1975, 1985; Tamarin 1977; Beacham 1981). A problem in describing dispersal in microtines is distinguishing between dispersal movements and movements due to fluid home range boundaries (Madison 1985). However, during winter months many microtines form relatively stable communal groups, and dispersal can be more clearly defined as emigration and immigration of group individuals. Dispersal between winter communal groups does occur in at least two species of microtines, Microtus xanthagnathus (Wolff & Lidicker 1980) and M. pennsylvanicus (Madison et al. 1984). Proximate mechanisms regulating dispersal between social groups should encompass factors that precipitate dispersal of individuals from a group and factors that prevent entry of new individuals. Agonistic interactions could fall into both categories, and previous studies indicate aggression may limit movement between winter groups. Madison et al. (1984) suggested that adult female meadow voles were aggressive toward juvenile females and might regulate the dispersal of juveniles. Aggressive interactions probably do occur, as Rose (1979) reported high levels of wounding for both male and female meadow voles during winter. Rather than being regulated solely by aggression, dispersal may also occur in response to conditions within the group. A decrease in the number of group members, due either to predation or earlier 0003 3472/90/020346+06503.00/0
dispersals, may increase the likelihood of an individual dispersing (Madison 1984). A study of proximate mechanisms must describe and test specific dispersal events, with knowledge of the disperser's previous social history. This study examined the effect of two proximate causes of dispersal among winter groups of meadow voles: reductions in group size and aggressive behaviour both within and between groups. Observations of radiotracked and experimentally paired individuals were made during winter and early spring to determine the relative role of these proximate factors in triggering dispersal among groups.
METHODS A grid measuring 40 x 40 m was established within an old field habitat measuring 20 ha, surroUnded by approximately 500 ha of hayfield at the National Zoological Park's Conservation and Research Center, Front Royal, Virginia. Trap stations, consisting of two Sherman traps placed under a trap shelter, were established every 5 m within the grid. Trapping was conducted approximately once a week during winter and early spring for 2 years (1 January-21 April 1987 and 28 November 198714 April 1988). After being prebaited with apple slices the day before, traps were checked every 2 h over a 10-h period (0700-1700 hours). Captured individuals were weighed, checked for reproductive
9 1990 The Association for the Study of Animal Behaviour 346
McShea." Proximate mechanisms ofdispersal status, and marked with unique toe clips. The animals were released immediately aftercapture, unless they were used as subjects for the paired encounter experiments or radiotransmitter implants. Up to 15 voles at a time were implanted with radiotransmitters (LFl-implants, Custom Electronics) using standard techniques (Madison et al. 1985) and released back into the field within 2 h of surgery. Voles were radiotracked one to two times a week with positions determined for each animal every 1/2 h over an 8.5-h period. Upon locating an individual at the same location as a previous animal, the first animal was relocated to verify joint occupancy of the nest or feeding site. Home range size was calculated from a convex polygon encompassing all positions for an animal during each 8.5-h telemetry session. During two winters of study, a total of 61 animals from nine communal groups was radiotracked (27 radiotracking days, 243 home ranges). A communal group was defined as individuals that shared a single nest and whose home ranges significantlyoverlapped. Animals were classified as belonging to specific communal groups on the basis of radiotelemetry data; those animals that did not possess transmitters were classified on the basis of trap location. Dispersal from the group occurred when an animal no longer shared the same nest as other group members, no longer overlapped in home range, and remained apart for at least a week. No animals categorized as dispersers returned to their old group over the course of the study. In addition to making weekly home range estimates, I verified the locations of all animals equipped with radiotransmitters on all trapping days and sporadically during the week (Fig. 1). Upon failure to locate a signal, the area (300 m 2 to 1 km 2) surrounding the trapping grid was systematically checked. Once the signal was located, I determined whether the animal was alive, or whether only the transmitter package remained. The wax coating on the transmitter (necessary for implantation) permitted determination of cause of death. Transmitters found with tooth impressions in the wax, or within carnivore scats, were classified as predator deaths; transmitters found within carcasses, or without bite marks, were classified as unknown mortality; live animals that did not return to their original group for more than 1 week were classified as dispersed and animals whose transmitters were never located were classified as disappeared. The study period was post-priori
2c
347
(a)
P DD
35~ I I I
$
D D
40
M?.~ M ?PP P P I L : _ ~ ~ I _ L - L - t _ J ~ L_ L J -.J--I
(b)
z 30
25 2o ~5 M P DP 5 PP P? ? D" P pPP P 9P 0____ I I I ~ . l : ' ~ l _ ~ 2 1 " ~ L [--L'E-LL I I Dec I Jan I Feb I Mar I Apr Date
Figure 1. The periods of loss for radiotracked volesduring the winters of 1987(a) and 1988(b). For each animal, loss was categorized as due to predation (P), dispersal (D), unknown mortality (M) or disappearance (?) (see Methods). 9 number of animals captured within study area; O: dates when the location of all animals equipped with radiotransmitters was verified. Records of loss are positioned between the last date an animal's position was verified and the first date its fate was discovered. divided into equal segments (20 days each) to examine the distribution of events resulting in group loss. The tolerance of a nesting animal toward nest entry of other voles was tested by staging paired encounters between individuals within the population. A nestbox with nest material and food was placed within a 28-1itre aquarium. Upon capture, a test animal was placed in the aquarium at the field site and allowed at least 15 min in the nestbox before a second animal, also captured from the grid, was added to the aquarium. An observer recorded whether the second animal was allowed entry into the nestbox or whether a fight ensued. If the resident allowed the second animal to enter the nestbox, the pair was allowed to remain together for an additional 30 min to 2 h before being returned to the points of capture. All aggressive interactions occurred as soon as the second animal attempted entry into the nestbox. Fifty-nine individuals were used for the tests and most animals were tested only once a trapping day. For those animals used twice during a trapping day (N = 16), the outcome of the
Animal Behaviour, 39, 2
348
Table L The result of attempted entry of an experimental animal into a nestbox occupied by either a nestmate or an animal from a different communal nest Season Experimental animals Source Nestmates Non-nestmates Non-nestmates*
Winter
Spring
Sex
Nested
Fought
Nested
Fought
Same Different Same Different Same Different
30 24 36 40 3 3
0 0 7 0 18 12
29 15 9 18
3 2 24 4
*One test animal reproductively active and not a member of any communal group.
first test could not significantly predict the outcome of the second test (discriminant analysis, F=0-04, P > 0.05) and thus, these results were included in the analysis. The response of animals to the loss of nestmates was examined by comparing the home range size of animals before and after the removal of nestmates. The experimental procedure involved three steps. Animals were radiotracked on day 1 according to the procedure previously described. On day 2 the population was trapped and communal groups were assigned to experimental categories; one group had the male members removed, one group had the female members removed and at least one group had no members removed. Removed individuals were placed in aquaria with their nestmates, food and water. On day 3 the remaining individuals were radiotracked again and changes in home range size were computed. At the conclusion of day 3, removed individuals were returned to their nests and in all cases rejoined the communal group. At least 1 week later, the process was repeated with the groups rotating through the experimental categories. An attempt was made to remove all individuals of the same sex from the experimental groups, but this was not always successful. Therefore, the results are presented as removal of nestmates, and not as removal of all nestmates of the opposite sex. In all cases, the nests being tested contained two or three animals after the removal of individuals. The start of the breeding season in spring was defined on the basis of the appearance of scrotal testes in males and the appearance of a perforated vagina in females. Each year there was a period of
2-3 weeks over which animals within the population began to exhibit these traits. Reference to early breeding season describes only the period after at least 75% of the population showed signs of reproductive activity (21 March 1987 and 18 March 1988). RESULTS
Role of Aggression During the winter periods, no aggression was shown between nestmates placed within the test arena (Table I). Although there were aggressive interactions, between individuals from different communal nests, the amount was not significantly different from that seen in tests involving nestmates (3(2= 3-67, df= 1, N = 137 paired encounters, P>0.10). All aggressive behaviour in nonreproductive individuals was between individuals of the same sex. Aggressive interactions between test individuals increased when at least one individual was reproductively active (Table I; ZZ=103"83, df=l, P<0-01). Each year a small percentage of the population (5-10%), all large males, remained reproductively active (i.e. scrotal) into the winter. These individuals did not nest with other radiotracked animals. Unlike aggression between non-reproductive voles, which was sex-biased, reproductive males were generally equally aggressive toward males and females (X2=0"43, df=l, P>0.10). In contrast to tests conducted over the winter months, paired encounters conducted after the
McShea: Proximate mechanisms of dispersal onset of breeding showed more aggression directed toward individuals from other groups, as opposed to individuals from the same nest (Z2 = 19-63, df= 1, P < 0-01; Table I). From winter to spring, aggressive encounters did not increase between nestmates (Z2=5"78, df= 1, P>0.10), but individuals from different groups did show a significant increase in aggression (Z2=25.46, df= 1, P<0.01). As with aggressive interactions during the winter, aggressive interactions between non-communalmembers were most common between indivduals of the same sex (Z2= 15-80, df= 1, P < 0-05). Voles did not shift to individual nesting with the onset of breeding. The ratio of communal nests, male-female pairs and single nests showed an increase in male-female pairs with the onset of breeding (four communal, two pairs and no singles in winter, compared with three communal, four pairs and one single in spring), but the sample size was insufficient to test for significance. All of the voles nesting together after the onset of breeding were nestmates during the winter. Impact of Loss of Nestmates
The pattern of loss within the population was clumped, with group losses occurring during discrete periods (Fig. 1). After dividing both winters into 20-day segments, the distribution of population losses was not equally distributed among the 12 time periods (~2 = 32"28, df= 11, P < 0-01; coefficient of dispersion= 2.69). Of the eight eases of dispersal observed, six occurred in conjunction with loss of animals due to predation. Within the groups, 74% (45) of the 61 radiotracked animals were lost to predation, disappearance, dispersal or unknown mortality (N= 18, 16, 8 and 3, respectively). When group loss was simulated through selective removal of nestmates, the remain!ng males increased their home range movements within 24 h of removal, while the home ranges of females showed no significant change (Mann-Whitney Utest, U=264 and 192, respectively, r~s; Table II). Significantlymore experimental males than females were nesting with members of other groups within 24 h of nestmate removal (nine out of 19 and one out of 17, respectively. Z z =8-22, df= 1, P<0.05). For the eight natural dispersal events recorded, all six males were later captured with other individuals, while the two females were not. Dispersals ranged in distance from 30 to 80 m (~'_+SE= 47.0_ 6.3 m). The sex of dispersers onto the grid was not biased during winter (seven males and five females), but
349
Table II. Response of individuals within 24 h of removal of nestmates
Test animal Direction of change in Male Female home range sizet Control* Removal Control Removal Decrease No change Increase
1 18 I
0 11 8
0 18 1
3 11 2
*Control individuals had no nestmates removed. tChange considered significantif greater than a factor of two. with onset of spring, more new males dispersed onto the grid than did females (12 males and one female).
DISCUSSION Aggression does not appear to regulate movement between communal nests during the winter, but may inhibit dispersal into groups after the onset of breeding in the spring. Large, reproductively active males engaged in aggressive interactions during the winter, but did not comprise a significantpercentage of this population. Large-bodied individuals are common during population peaks (Taitt & Krebs 1985), and aggression may play a greater role in regulating dispersal at that time. After the onset of breeding, most agonistic interactions were between individuals of the same sex. Both males and females were aggressive toward unfamiliar individuals of the same sex that attempted entry to the experimental nest. This aggression would essentially close groups toward immigration of new members. Increased aggression between individuals of the same sex with the onset of breeding does not necessarily indicate the ultimate cause for dispersal is similar for each sex. For females, increased aggression would be predicted by the territorial social organization of females during the breeding season (Madison 1980). Males, however, are not territorial during the breeding season (Madison 1980) and male dispersal in early spring may result from competition for mates. Increased malefemale pairs with the onset of breeding supports this hypothesis. Male biased dispersal with the
350
Animal Behaviour, 39, 2
onset of breeding has been reported for several microtine species (M. californicus, Lidicker 1973; M. xanthognathus, Wolff & Lidicker 1980; M. townsendii, Beacham 1981). During winter, dispersal between groups coincided with the disappearance, or death due to predation, of other group members. Simulation of group loss through selective removal of group members resulted in increased home range size and dispersal by male meadow voles. Previous studies have shown that meadow voles shift their home range in response to the short-tailed shrew, Blarina brevicanda, a potential predator (Fulk 1972), and M. xanthognathus disperse between groups in response to nest disturbance (Wolff, personal communication). Predation has been identified as a possible regulator of population numbers (Pearson t985; Hansson 1988) and may also act as a trigger for dispersal from winter groups. Males showed a greater likelihood to disperse than females and engaged in almost all movement between groups. These differences are consistent with the data from the reproductive season. Females are territorial, have smaller home range sizes and exhibit fewer shifts in the centre of their activities than do males (Madison 1980). Sheridan & Tamarin (1988) found that reproductive fitness was positively correlated with site tenacity for female meadow voles. In contrast, males probably compete for access to females during the breeding season (Sheridan & Tamarin 1988) and their site tenacity during winter should be lower. The net result of sex differences in site tenacity is that by the end of winter most groups are composed of females that started the winter within the group, and unrelated males that have dispersed into the group. Paired encounters and radiotelemetry data from early spring indicate a high degree of tolerance between meadow voles that overwintered together. This is in sharp contrast to aggression reported within summer populations of meadow voles (Turner & Iverson 1973; Madison 1980; Webster & Brooks 1981). Changes in tolerance toward outside unfamiliar individuals may be the key to the transition from social tolerance in the winter to social intolerance in the summer. The lifespan of a meadow vole is brief under normal circumstances. Rose & Dueser (1980) reported an average lifespan of 16-27 weeks for individuals within six populations of meadow voles. Only 26% (16) of animals in this study survived from winter to spring breeding within the same group. Tolerance
shown toward group members does not change from winter to spring, but rather the number of familiar individuals dwindles with passage of time. The existence of spring breeding pairs of females (McShea & Madison 1984) may depend on the rate of turnover within the population. Winter communal nests promote development of social bonds in a normally intolerant species, but increased aggression toward unfamiliar individuals prevents the formation of new social bonds, and therefore the persistence of this social organization. These findings contribute to the study of microtine populations because they reinforce the idea that environment, including social history, influence social organization and behaviour (Lott 1984; McGuire 1988). Environmentalfactors in the spring (e.g. predation rates, flooding) may determine the rate of population turnover and thereby the rate at which the population converts to a territorial individual-nestorganization.
ACKNOWLEDGMENTS Assistance in the field was provided by Erin Muths and Bev Bryant. Betty McGuire, Jerry Wolff, Vickie MacDonald, Jack Cranford and one anonymous referee provided helpful comments on the manuscript. This work was conducted with the financial support of the National Zoological Park and Friends of the National Zoo.
REFERENCES
Beacham, T. D. 1981. Some demographic aspects of dispersers in fluctuating populations of the vole Mierotus townsendii. Oikos, 36, 272 280. Chepko-Sade, B. D. & Halpin, Z. T. 1988. Mammalian Dispersal Patterns: The Effects of Social Structure on Population Genetics. Chicago: University of Chicago Press. Fulk, G. W. 1972.The effect of shrews on space utilization of voles. J. Mammal., 53, 461-478. Hansson, L. 1988.The domestic cat as a possiblemodifier of vole dynamics. Mammalia, 52, 159-164. Lidicker, W. Z., Jr. 1973. Regulation of numbers in an island population of the California vole, a problem of community dynamics. Ecol. Mongr., 43, 271-302. Lidicker, W. Z., Jr. 1975. The role of dispersal in the demography. In: Small Mammals: Their Production and Population Dynamics (Ed. by F. B. Golley, K. Petrusewicz & L. Ryszkowski), pp. 103-128. Cambridge: Cambridge UniversityPress. Lidicker, W. Z., Jr. 1985. Dispersal. In: Biology of New Worm Microtus (Ed. by R. H. Tamarin), pp. 420~53.
McShea: Proximate mechanisms o f dispersal Shippensburg, Pennsylvania: American Society of Mammalogists. Lott, D. F. 1984. Intraspecific variation in the social systems of wild vertebrates. Behaviour, 88, 266-325. McGuire, B. 1988. The effects of cross-fostering on the parental behavior of meadow voles (Microtus pennsylvanicus). J. MammaL, 69, 332 341. McShea, W. J. & Madison, D. M. 1984. Communal nesting by reproductively active females in a spring population of Microtus pennsylvanicus. Can. J. Zool., 62, 344-346. Madison, D. M. 1980. Space use and social structure in meadow voles, Microtus pennsylvanicus. Behav. Ecol. Sociobiol., 7, 65-71. Madison, D. M. 1984. Group nesting and its ecological and evolutionary significance in over-wintering microtine rodents. In: Winter Ecology of Small Mammals (Ed. by J. F. Merritt), pp. 285-291. Pittsburgh: Carnegie Museum Press. Madison, D. M. 1985. Activity Rythms and Spacing. In: Biology of New WorMMicrotus (Ed. by R. H. Tamarin), pp. 373-454. Shippensburg, Pennsylvania: American Society of Mammalogists. Madison, D. M., Fitzgerald, R. W. & McShea, W. J. 1984. Dynamics of social nesting in overwintering meadow voles (Microtus pennsylvanicus): possible consequences for population cycling. Behav. Ecol. Sociobiol., 15, 9-17. Madison, D. M., FitsGerald, R. W. & McShea, W. J. 1985. A user's guide to the successful radiotracking of small rodents in the field. In: Proceedings of the Fifth International Conference on Wildlife Biotelemetry (Ed. by F. M. Long), pp. 28-39. Laramie: University of Wyoming.
35t
Pearson, O. P. 1985. Predation. In: Biology of New Worm Microtus (Ed. by R. H. Tamarin), pp. 535 566. Shippensburg, Pennsylvania: American Society of Mammalogists. Rose, R. K. 1979. Levels of wounding in the meadow voles Microtus pennsylvanicus. J. Mammal., 60, 37-45. Rose, R. K. & Dueser, R. D. 1980. Lifespan of virginia meadow voles. J. Mammal., 61,760-763. Sheridan, M. & Tamarin, R. H. 1988. Space use, longevity and reproductive success in meadow voles. Behav. Ecol. Sociobiol., 22, 85-90. Taitt, M. J. & Krebs, C. J. 1985. Population dynamics and cycles. In: Biology of New WorldMicrotus (Ed. by R. H. Tamarin), pp. 567-620. Shippensburg, Pennsylvania: American Society of Mammalogists. Tamarin, R. H. 1977. Dispersal in island and mainland voles. Ecology, 58, 1044-1054. Turner, B. N. & Iverson, S. L. 1973. The annual cycle of aggression in male Microtus pennsylvanicus, and its relation to population parameters. Ecology, 54, 967-981. Webster, A. B. & Brooks, R. J. 1981. Social behavior of Microtuspennsylvanicus in relation to seasonal changes in demography. J. Mammal., 62, 738-751. Wolff, J. O. & Lidicker, W. J., Jr. 1980. Population ecology of the taiga vole, Microtus xanthognathus, in interior Alaska. Can. J. Zool., 58, 1800-1812.
(Received 13 February 1989; initial acceptance 20 March 1989;final acceptance 5 May 1989; MS. number: A5407)
Social tolerance and proximate mechanisms of dispersal among winter groups of meadow voles, Microtus pennsylvanicus WILLIAM
J. M c S H E A
National Zoological Park, Conservation and Research Center, Front Royal, Virginia 22630, U.S.A.
Abstract. Proximate mechanisms for movement among communal groups of meadow voles were examined during two winter seasons. Radiotelemetry and live trapping were used to identify group members and monitor the movement of voles. Paired encounters between individuals removed from the field indicated that aggression neither precipitated nor prevented movement of animals between groups during winter. Dispersal most often occurred in conjuction with loss of nestmates to predation. The removal of nestmates resulted in increased home range size and movement between groups for males, but not for females. With the onset of reproduction, aggression increased toward individuals from other groups, but not toward nestmates, Winter groups did not break up with the onset of breeding, but these groups were closed to the immigration of new members.
Dispersal is an important process in the population dynamics of many species (Chepko-Sade & Halpin 1988) and has received particular attention in explaining population fluctuations in microtines (Lidicker 1975, 1985; Tamarin 1977; Beacham 1981). A problem in describing dispersal in microtines is distinguishing between dispersal movements and movements due to fluid home range boundaries (Madison 1985). However, during winter months many microtines form relatively stable communal groups, and dispersal can be more clearly defined as emigration and immigration of group individuals. Dispersal between winter communal groups does occur in at least two species of microtines, Microtus xanthagnathus (Wolff & Lidicker 1980) and M. pennsylvanicus (Madison et al. 1984). Proximate mechanisms regulating dispersal between social groups should encompass factors that precipitate dispersal of individuals from a group and factors that prevent entry of new individuals. Agonistic interactions could fall into both categories, and previous studies indicate aggression may limit movement between winter groups. Madison et al. (1984) suggested that adult female meadow voles were aggressive toward juvenile females and might regulate the dispersal of juveniles. Aggressive interactions probably do occur, as Rose (1979) reported high levels of wounding for both male and female meadow voles during winter. Rather than being regulated solely by aggression, dispersal may also occur in response to conditions within the group. A decrease in the number of group members, due either to predation or earlier 0003 3472/90/020346+06503.00/0
dispersals, may increase the likelihood of an individual dispersing (Madison 1984). A study of proximate mechanisms must describe and test specific dispersal events, with knowledge of the disperser's previous social history. This study examined the effect of two proximate causes of dispersal among winter groups of meadow voles: reductions in group size and aggressive behaviour both within and between groups. Observations of radiotracked and experimentally paired individuals were made during winter and early spring to determine the relative role of these proximate factors in triggering dispersal among groups.
METHODS A grid measuring 40 x 40 m was established within an old field habitat measuring 20 ha, surroUnded by approximately 500 ha of hayfield at the National Zoological Park's Conservation and Research Center, Front Royal, Virginia. Trap stations, consisting of two Sherman traps placed under a trap shelter, were established every 5 m within the grid. Trapping was conducted approximately once a week during winter and early spring for 2 years (1 January-21 April 1987 and 28 November 198714 April 1988). After being prebaited with apple slices the day before, traps were checked every 2 h over a 10-h period (0700-1700 hours). Captured individuals were weighed, checked for reproductive
9 1990 The Association for the Study of Animal Behaviour 346
McShea." Proximate mechanisms ofdispersal status, and marked with unique toe clips. The animals were released immediately aftercapture, unless they were used as subjects for the paired encounter experiments or radiotransmitter implants. Up to 15 voles at a time were implanted with radiotransmitters (LFl-implants, Custom Electronics) using standard techniques (Madison et al. 1985) and released back into the field within 2 h of surgery. Voles were radiotracked one to two times a week with positions determined for each animal every 1/2 h over an 8.5-h period. Upon locating an individual at the same location as a previous animal, the first animal was relocated to verify joint occupancy of the nest or feeding site. Home range size was calculated from a convex polygon encompassing all positions for an animal during each 8.5-h telemetry session. During two winters of study, a total of 61 animals from nine communal groups was radiotracked (27 radiotracking days, 243 home ranges). A communal group was defined as individuals that shared a single nest and whose home ranges significantlyoverlapped. Animals were classified as belonging to specific communal groups on the basis of radiotelemetry data; those animals that did not possess transmitters were classified on the basis of trap location. Dispersal from the group occurred when an animal no longer shared the same nest as other group members, no longer overlapped in home range, and remained apart for at least a week. No animals categorized as dispersers returned to their old group over the course of the study. In addition to making weekly home range estimates, I verified the locations of all animals equipped with radiotransmitters on all trapping days and sporadically during the week (Fig. 1). Upon failure to locate a signal, the area (300 m 2 to 1 km 2) surrounding the trapping grid was systematically checked. Once the signal was located, I determined whether the animal was alive, or whether only the transmitter package remained. The wax coating on the transmitter (necessary for implantation) permitted determination of cause of death. Transmitters found with tooth impressions in the wax, or within carnivore scats, were classified as predator deaths; transmitters found within carcasses, or without bite marks, were classified as unknown mortality; live animals that did not return to their original group for more than 1 week were classified as dispersed and animals whose transmitters were never located were classified as disappeared. The study period was post-priori
2c
347
(a)
P DD
35~ I I I
$
D D
40
M?.~ M ?PP P P I L : _ ~ ~ I _ L - L - t _ J ~ L_ L J -.J--I
(b)
z 30
25 2o ~5 M P DP 5 PP P? ? D" P pPP P 9P 0____ I I I ~ . l : ' ~ l _ ~ 2 1 " ~ L [--L'E-LL I I Dec I Jan I Feb I Mar I Apr Date
Figure 1. The periods of loss for radiotracked volesduring the winters of 1987(a) and 1988(b). For each animal, loss was categorized as due to predation (P), dispersal (D), unknown mortality (M) or disappearance (?) (see Methods). 9 number of animals captured within study area; O: dates when the location of all animals equipped with radiotransmitters was verified. Records of loss are positioned between the last date an animal's position was verified and the first date its fate was discovered. divided into equal segments (20 days each) to examine the distribution of events resulting in group loss. The tolerance of a nesting animal toward nest entry of other voles was tested by staging paired encounters between individuals within the population. A nestbox with nest material and food was placed within a 28-1itre aquarium. Upon capture, a test animal was placed in the aquarium at the field site and allowed at least 15 min in the nestbox before a second animal, also captured from the grid, was added to the aquarium. An observer recorded whether the second animal was allowed entry into the nestbox or whether a fight ensued. If the resident allowed the second animal to enter the nestbox, the pair was allowed to remain together for an additional 30 min to 2 h before being returned to the points of capture. All aggressive interactions occurred as soon as the second animal attempted entry into the nestbox. Fifty-nine individuals were used for the tests and most animals were tested only once a trapping day. For those animals used twice during a trapping day (N = 16), the outcome of the
Animal Behaviour, 39, 2
348
Table L The result of attempted entry of an experimental animal into a nestbox occupied by either a nestmate or an animal from a different communal nest Season Experimental animals Source Nestmates Non-nestmates Non-nestmates*
Winter
Spring
Sex
Nested
Fought
Nested
Fought
Same Different Same Different Same Different
30 24 36 40 3 3
0 0 7 0 18 12
29 15 9 18
3 2 24 4
*One test animal reproductively active and not a member of any communal group.
first test could not significantly predict the outcome of the second test (discriminant analysis, F=0-04, P > 0.05) and thus, these results were included in the analysis. The response of animals to the loss of nestmates was examined by comparing the home range size of animals before and after the removal of nestmates. The experimental procedure involved three steps. Animals were radiotracked on day 1 according to the procedure previously described. On day 2 the population was trapped and communal groups were assigned to experimental categories; one group had the male members removed, one group had the female members removed and at least one group had no members removed. Removed individuals were placed in aquaria with their nestmates, food and water. On day 3 the remaining individuals were radiotracked again and changes in home range size were computed. At the conclusion of day 3, removed individuals were returned to their nests and in all cases rejoined the communal group. At least 1 week later, the process was repeated with the groups rotating through the experimental categories. An attempt was made to remove all individuals of the same sex from the experimental groups, but this was not always successful. Therefore, the results are presented as removal of nestmates, and not as removal of all nestmates of the opposite sex. In all cases, the nests being tested contained two or three animals after the removal of individuals. The start of the breeding season in spring was defined on the basis of the appearance of scrotal testes in males and the appearance of a perforated vagina in females. Each year there was a period of
2-3 weeks over which animals within the population began to exhibit these traits. Reference to early breeding season describes only the period after at least 75% of the population showed signs of reproductive activity (21 March 1987 and 18 March 1988). RESULTS
Role of Aggression During the winter periods, no aggression was shown between nestmates placed within the test arena (Table I). Although there were aggressive interactions, between individuals from different communal nests, the amount was not significantly different from that seen in tests involving nestmates (3(2= 3-67, df= 1, N = 137 paired encounters, P>0.10). All aggressive behaviour in nonreproductive individuals was between individuals of the same sex. Aggressive interactions between test individuals increased when at least one individual was reproductively active (Table I; ZZ=103"83, df=l, P<0-01). Each year a small percentage of the population (5-10%), all large males, remained reproductively active (i.e. scrotal) into the winter. These individuals did not nest with other radiotracked animals. Unlike aggression between non-reproductive voles, which was sex-biased, reproductive males were generally equally aggressive toward males and females (X2=0"43, df=l, P>0.10). In contrast to tests conducted over the winter months, paired encounters conducted after the
McShea: Proximate mechanisms of dispersal onset of breeding showed more aggression directed toward individuals from other groups, as opposed to individuals from the same nest (Z2 = 19-63, df= 1, P < 0-01; Table I). From winter to spring, aggressive encounters did not increase between nestmates (Z2=5"78, df= 1, P>0.10), but individuals from different groups did show a significant increase in aggression (Z2=25.46, df= 1, P<0.01). As with aggressive interactions during the winter, aggressive interactions between non-communalmembers were most common between indivduals of the same sex (Z2= 15-80, df= 1, P < 0-05). Voles did not shift to individual nesting with the onset of breeding. The ratio of communal nests, male-female pairs and single nests showed an increase in male-female pairs with the onset of breeding (four communal, two pairs and no singles in winter, compared with three communal, four pairs and one single in spring), but the sample size was insufficient to test for significance. All of the voles nesting together after the onset of breeding were nestmates during the winter. Impact of Loss of Nestmates
The pattern of loss within the population was clumped, with group losses occurring during discrete periods (Fig. 1). After dividing both winters into 20-day segments, the distribution of population losses was not equally distributed among the 12 time periods (~2 = 32"28, df= 11, P < 0-01; coefficient of dispersion= 2.69). Of the eight eases of dispersal observed, six occurred in conjunction with loss of animals due to predation. Within the groups, 74% (45) of the 61 radiotracked animals were lost to predation, disappearance, dispersal or unknown mortality (N= 18, 16, 8 and 3, respectively). When group loss was simulated through selective removal of nestmates, the remain!ng males increased their home range movements within 24 h of removal, while the home ranges of females showed no significant change (Mann-Whitney Utest, U=264 and 192, respectively, r~s; Table II). Significantlymore experimental males than females were nesting with members of other groups within 24 h of nestmate removal (nine out of 19 and one out of 17, respectively. Z z =8-22, df= 1, P<0.05). For the eight natural dispersal events recorded, all six males were later captured with other individuals, while the two females were not. Dispersals ranged in distance from 30 to 80 m (~'_+SE= 47.0_ 6.3 m). The sex of dispersers onto the grid was not biased during winter (seven males and five females), but
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Table II. Response of individuals within 24 h of removal of nestmates
Test animal Direction of change in Male Female home range sizet Control* Removal Control Removal Decrease No change Increase
1 18 I
0 11 8
0 18 1
3 11 2
*Control individuals had no nestmates removed. tChange considered significantif greater than a factor of two. with onset of spring, more new males dispersed onto the grid than did females (12 males and one female).
DISCUSSION Aggression does not appear to regulate movement between communal nests during the winter, but may inhibit dispersal into groups after the onset of breeding in the spring. Large, reproductively active males engaged in aggressive interactions during the winter, but did not comprise a significantpercentage of this population. Large-bodied individuals are common during population peaks (Taitt & Krebs 1985), and aggression may play a greater role in regulating dispersal at that time. After the onset of breeding, most agonistic interactions were between individuals of the same sex. Both males and females were aggressive toward unfamiliar individuals of the same sex that attempted entry to the experimental nest. This aggression would essentially close groups toward immigration of new members. Increased aggression between individuals of the same sex with the onset of breeding does not necessarily indicate the ultimate cause for dispersal is similar for each sex. For females, increased aggression would be predicted by the territorial social organization of females during the breeding season (Madison 1980). Males, however, are not territorial during the breeding season (Madison 1980) and male dispersal in early spring may result from competition for mates. Increased malefemale pairs with the onset of breeding supports this hypothesis. Male biased dispersal with the
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Animal Behaviour, 39, 2
onset of breeding has been reported for several microtine species (M. californicus, Lidicker 1973; M. xanthognathus, Wolff & Lidicker 1980; M. townsendii, Beacham 1981). During winter, dispersal between groups coincided with the disappearance, or death due to predation, of other group members. Simulation of group loss through selective removal of group members resulted in increased home range size and dispersal by male meadow voles. Previous studies have shown that meadow voles shift their home range in response to the short-tailed shrew, Blarina brevicanda, a potential predator (Fulk 1972), and M. xanthognathus disperse between groups in response to nest disturbance (Wolff, personal communication). Predation has been identified as a possible regulator of population numbers (Pearson t985; Hansson 1988) and may also act as a trigger for dispersal from winter groups. Males showed a greater likelihood to disperse than females and engaged in almost all movement between groups. These differences are consistent with the data from the reproductive season. Females are territorial, have smaller home range sizes and exhibit fewer shifts in the centre of their activities than do males (Madison 1980). Sheridan & Tamarin (1988) found that reproductive fitness was positively correlated with site tenacity for female meadow voles. In contrast, males probably compete for access to females during the breeding season (Sheridan & Tamarin 1988) and their site tenacity during winter should be lower. The net result of sex differences in site tenacity is that by the end of winter most groups are composed of females that started the winter within the group, and unrelated males that have dispersed into the group. Paired encounters and radiotelemetry data from early spring indicate a high degree of tolerance between meadow voles that overwintered together. This is in sharp contrast to aggression reported within summer populations of meadow voles (Turner & Iverson 1973; Madison 1980; Webster & Brooks 1981). Changes in tolerance toward outside unfamiliar individuals may be the key to the transition from social tolerance in the winter to social intolerance in the summer. The lifespan of a meadow vole is brief under normal circumstances. Rose & Dueser (1980) reported an average lifespan of 16-27 weeks for individuals within six populations of meadow voles. Only 26% (16) of animals in this study survived from winter to spring breeding within the same group. Tolerance
shown toward group members does not change from winter to spring, but rather the number of familiar individuals dwindles with passage of time. The existence of spring breeding pairs of females (McShea & Madison 1984) may depend on the rate of turnover within the population. Winter communal nests promote development of social bonds in a normally intolerant species, but increased aggression toward unfamiliar individuals prevents the formation of new social bonds, and therefore the persistence of this social organization. These findings contribute to the study of microtine populations because they reinforce the idea that environment, including social history, influence social organization and behaviour (Lott 1984; McGuire 1988). Environmentalfactors in the spring (e.g. predation rates, flooding) may determine the rate of population turnover and thereby the rate at which the population converts to a territorial individual-nestorganization.
ACKNOWLEDGMENTS Assistance in the field was provided by Erin Muths and Bev Bryant. Betty McGuire, Jerry Wolff, Vickie MacDonald, Jack Cranford and one anonymous referee provided helpful comments on the manuscript. This work was conducted with the financial support of the National Zoological Park and Friends of the National Zoo.
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(Received 13 February 1989; initial acceptance 20 March 1989;final acceptance 5 May 1989; MS. number: A5407)