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A comparison of paternal behaviour in the meadow vole Microtus pennsylvanicus, the pine vole M. pinetorum and the prairie vole M. cchrogaster
Anim. Behav., 1986, 34, 519-526
A comparison of paternal behaviour in the meadow vole Microtus pennsylvanicus, the pine vole M. pinetorum and the prairie vole M. ochrogaster DIANA OLIVERAS* & MELINDA NOVAK
Department of Zoology, University of Massachusetts, Amherst, MA 01003, U.S.A.
Abstract. Paternal care in microtines has been studied infrequently and few studies have compared patterns of direct and indirect paternal investment9 The paternal behaviour of three vole species, the meadow vole (Microtuspennsylvanicus), the pine vole (M. pinetorum) and the prairie vole (M. ochrogaster) was examined in a semi-natural setting. Prairie and pine voles were found to exhibit high levels of paternal care. Prairie vole males contributed the most direct care by remaining in the natal nest for long periods of time in contact with the pups. Pine voles contributed less direct care than prairie voles as they spent less time in the natal nest with their offspring. In addition, both prairie and pine vole males were observed to groom their pups and retrieve them back to the nest area. Prairie vole males also engaged in such indirect forms of care as nest construction and maintenance, while pine voles provided indirect care in the form of tunnel construction and food caching. Meadow vole males were the least paternal of the three species and rarely engaged in either direct or indirect care. These findings support predictions that M. pennsylvanieus is promiscuous and that male and female meadow voles occupy separate territories. They are also consistent with studies which indicate that prairie and pine voles are monogamous and have a structured social organization with members interacting closely with one another9
Paternal care in rodents is thought to vary as a function of social organization and mating system, and diversity can be reflected in both the amount and type of parental activity performed by the male. For example, the quantity of paternal care is thought to be positively correlated with the probability of paternity (Trivers 1972), and thus paternal care should be more prevalent in monogamous than in promiscuous species. Male parental behaviour may also be classified into two broad categories (Kleiman 1977). Direct paternal investment, usually measured in studies of parental behaviour, consists of behaviours that have an immediate physical effect on the offspring9 These include feeding, grooming, huddling and retrieving the young9 Indirect paternal investment consists of behaviours often performed in the absence of offspring, with consequences that may be delayed for an unspecific amount of time and may affect individuals other than the young themselves9 This category includes acquisition of resources, defence of territory, construction and maintenance of nest and runways, and defence against predators. The impact of different mating systems on the quality of paternal care in rodents is not fully understood. Previous evidence indicates a wide diversity of mating systems and social organizations within the * Present address: Department of Biology, University of New Mexico, Albuquerque, NM 87131, U.S.A.
rodent genus Microtus. Based on radiotelemetric and live-trap results, the meadow vole, Microtus pennsylvanicus, appears to be promiscuous, with female voles maintaining separate territories and actively excluding adult males (Getz 1972; Madison 1978, 1980). The prairie vole, M. ochrogaster, however, is monogamous and, at normal population densities, is found in family groups (Getz & Carter 1980). Less is known about the social organization of the pine vole, M. pinetorum, but field data indicate that male and female pine voles established some form of pair bond and live in colonies composed of family members (Miller & Getz 1969; Paul 1970; FitzGerald & Madison 1983). Given such diversity of mating systems and social organizations, one might also expect variation in the amount and type of paternal care in these three species. Paternal care in microtines has been studied infrequently and only under laboratory conditions, as the natural environment of these rodents precludes measurement of such behaviour. Hartung & Dewsbury (1979) observed both meadow and prairie vole males sitting on the nest as well as licking and manipulating pups, retrieving them back to the nest area and maintaining the nest. They, as well as Wilson (1982), noted that prairie vole males spent more time huddling over their pups than meadow vole males. Despite these 519
Animal Behaviour, 34, 2
520
observations of paternal care, the authors mentioned that the experimental conditions may have influenced the behaviour of the voles, and that paternal behaviour observed in a confined laboratory setting may not reflect a male's behaviour in the field. These results differ from those of McGuire & Novak (1985) who observed meadow, prairie and pine vole pairs from underneath large, hay-covered Plexiglas-bottomed pens. Although the focus of that study was on maternal behaviour, male location was also recorded. Prairie vole males spent somewhat similar amounts of time in contact with their pups as compared to the voles in Wilson's study, but meadow vole males never huddled over their pups, nor entered the natal nest. McGuire & Novak's findings are consistent with field measures of male meadow vole activity which indicate a lack of nest cohabitation by male and female voles (Madison 1978). The above studies, however, did not compare patterns of paternal investment. It is therefore possible that the discrepant results reflect differences in the types of care provided by males of these two species. Meadow voles may contribute more indirect than direct care, while prairie voles may engage in a greater amount of direct care. The purpose of the present study was to examine the nature of paternal care expressed by meadow voles, prairie voles and pine voles. This research was conducted in the same semi-natural environment used by McGuire & Novak (1985). To determine the relative amounts of care provided by the males of each of the three species, the study focused on measures of direct paternal investment (grooming, contacting and retrieving pups) as well as several aspects of indirect paternal investment (food caching and nest and runway construction).
METHODS Subjects Six mal~female pairs from each of the following three species of microtines were studied: Mierotus pennsylvanicus (second generation offspring of voles trapped in Massachusetts), M. pinetorum (second generation offspring of voles trapped in New York) and M. oehrogaster (fifth generation offspring of voles obtained from Indiana). The data from one M. oehrogaster pair were incomplete and were therefore not used. However, the pattern of paternal care in this pair did not differ from the pattern of the remaining five pairs. Prior to this
study, the voles were kept in two large colony rooms and housed as breeding pairs in 51 x 26 x 31cm wire-mesh cages or in glass aquaria of the same dimensions. All cages had a peat and wood chip substrate with a substantial hay cover. Voles were maintained on a 14-h L: 10-h D photoperiod with lights on at 0600 hours. Water and food were available ad libitum, the diet consisting of sunflower and rye seeds and laboratory chow. In addition, the voles were given freshly sprouted rye and sunflower twice weekly. The decision to observe certain breeding pairs was based on two criteria: (1) the female was pregnant (pregnancy being determined by a 20~ weight gain) and (2) both members of the pair had successfully raised a previous litter to weaning. Immediately before placement in the observational tables, the male's entire ventral surface was dyed with black Nyanzol-D dye for easier identification.
Apparatus Paternal behaviour was observed in a pair of table-like pens connected by plastic runways identical to those described by McGuire & Novak (1985). Each table was raised approximately 70 cm off the floor on either angle-iron or wooden legs. The bottoms of the pens were constructed of a 1.3-m2 Plexiglas sheet while the sides measured at least 60 cm in height and were built of Plexiglas or metal flash!ng. The pens were layered with a 10-20 cm hay cover over 5 cm of peat substrate into which preliminary runways were cleared by the experimenters. Observations were made from beneath the tables using a 'mechanic's creeper', with data being recorded on a data acquisition keyboard (MORE, Observational Systems; Seattle, Washington).
Procedure Voles placed in the observational tables were maintained under the same feeding and lighting conditions as those in the colony rooms. Each male of a pair was observed every afternoon in 15-min sessions and data were collected from the day a litter was born to 20 days post-partum. The frequency and duration of 14 different activities were recorded, as well as the location of the male during the data session. Five activities involved direct forms of paternal care. These were 'contact pup', 'groom pup', 'retrieve pup', 'approach' and 'withdraw'. Approaches were scored when the male
Oliveras & Novak." Paternal behaviour in voles was located 4 0 ~ 5 cm from the pup and one individual moved toward the other. Withdrawals were recorded when the male was located within 15 cm of a pup and one individual moved away from the other. In addition, the locations of the male in or out of the natal nest and in or out of the table containing the natal nest were recorded. Three activities involved indirect forms of paternal care. These included 'nest construction/maintenance', 'tunnel construction/maintenance' and 'food cache'. Six activities did not involve any form of paternal care and consisted of 'approach female', 'withdraw from female', 'locomote', 'passive' (a l-s pause of inactivity or longer), 'eat/drink' and 'groom self'. The data were analysed using a mixed design analysis of variance ( A N O V A ) with species as the between-subjects variable and days (1-20) as the repeated measure. Significant species effects were further analysed with a N e u m a n - K e u l s post hoc test (Kirk 1968). RESULTS Meadow, prairie and pine vole males were found to differ in the amount and type of care they provided the young. Both pine and prairie vole males were
521
more paternal than meadow vole males, contributing direct as well as indirect forms of parental care. The amount of care provided by pine and prairie vole males decreased significantly as the pups developed. M e a d o w voles performed no appreciable levels of direct care and rarely engaged in indirect forms of parental care. Pine and prairie voles were more often found in the natal nest whereas meadow voles spent most of the time in the table that did not contain the natal nest.
Direct Paternal Activities and Location Measures
Species comparisons of the frequency and duration of direct paternal behaviours and of location measures are summarized in Table I. The data analysis revealed that prairie vole males spent 52% of the 15-min session in the natal nest, pine voles spent 30% of that time there and meadow voles spent approximately 6% of the time in the natal nestl in addition, prairie and pine voles were found in the nest throughout the 20 days of observation. However, meadow voles were typically found in the nest only after the twelfth day post partum ( F = 1.56, df=38/266, P < 0 . 0 2 5 ; Fig. 1). Time spent in the table that did not contain the natal nest followed an opposite trend. Meadow
Table I. Species differences in direct paternal activities and location measures
Activities/ locations
Microtus Measure pennsylvanicus
Microtus pinetorum
Microtus ochrogaster
P
Contact pup
Freq* Durt
0.57+0.14 72.68+18.98
1.55___0.22 1.9l +0.19 0.01 186.28__+27.50 332.98+35.69 0.01
Groom pup
Freq Dur
0.01 +0.01 0.02+0.02
0.53+0-12 6.47+ 1.74
Retrieve pup
Freq Dur
0.00 _ 0.00 0.00_ 0.00
0.04 + 0.03 0.18+0.14
0.15 __+0.06 0.97+0.42
Approach pup
Freq Dur
1.37__+0.24 5.25_+0.96
0.85+0.15 2.73+0.48
1.56_+0-29 MS 5.09+__1.05 Ns
Withdraw from pup
Freq Dur
1.31 ___0.23 2.01_+0.36
0.66+0.14 1-11 +0.24
1.30___0-26 Ns 2.25_+0-47 NS
In natal nest
Freq Dur
Out of table containing natal nest
Freq Dur
0-51+0.11 0.01 10.14___2.81 0.001 Ns ys
0.12_+0.04 0.83_+0.10 1.43+0.17 0.001 52.83___17.97 273.42___31.34 468.16___37.76 0.001 1.12+0.07 663.18+33.36
1.56_+0.14 0.29+0.06 0.01 344.14+30.54 71.81_+18.85 0.001
* Freq = mean frequency of occurrence per 15-min period + sE. t Dur = mean duration + sE in s.
Animal Behaviour, 34, 2
522 Contact pup
In nest
800 -
800
700
700
_
600
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M. p e n n s ylvanicus ......... M. pinetorum ...... M. ochrogastor Figure 1. Significant differences in the parental behaviour of meadow vole, pine vole and prairie vole males across the
first 20 days of pup development. vole males spent nearly 75~ of the time out of the table containing the natal nest as compared to pine voles which were found there only 38% of the time. Prairie vole males were rarely found in that table, spending less than 10~ of the time there. Prairie vole males were in contact with their pups for longer durations than either pine or meadow vole males. Both prairie and pine voles were seen with
their pups throughout the entire observation period but the longest contact bouts were recorded mostly during the first days of observation (F=1.52, df=38/266, P<0'05; Fig. 1). Prairie voles spent over 33% of the time with their young during early development of the litter and pine voles spent slightly more than 15% of that time together with their pups. During the same period,
Oliveras & Novak: Paternal behaviour in voles however, no meadow vole was seen with the young. All of the pup-contact activities in meadow voles occurred after the tenth day post-partum, and appeared to coincide with the pups' greater mobility during later development. In addition, all prairie and pine vole males were observed grooming their pups, yet only one meadow vole male was seen grooming pups on the 13th day post-partum and for only 3 s of that particular session. The duration of pup grooming in prairie and pine voles was high during early development and decreased steadily afterward ( F = 1.48, df= 38/266, P < 0.05; Fig. t). Prairie and pine voles also retrieved their pups to the nest but no meadow vole male was ever observed retrieving any young ( F = 1.85, df= 38/ 266, P < 0-01). Pine and prairie vole males exhibited approach (F=1-76, df=38/266, P<0.01; Fig 1) and withdraw behaviour ( F = 1.75, df=38/266, P < 0-01) during both early and late development; however, in meadow voles the vast majority of such behaviour was seen only after the litter was 10 days old. This again coincided with the increased activity of the pups themselves, especially away from the nest site. A further analysis was conducted to examine sequential dependencies in the data. Approaches were subcategorized into 'male approach pup' and 'pup approach male'. Withdrawals were subcategorized into 'male withdraw from pup' and 'pup
523
withdraw from male'. The frequencies of approach were then calculated to determine if paternal care was likely to occur once the pups and male had moved into close proximity with one another. The results of this analysis are presented in Table II. Although males of all three species approached their pups the total number of those approaches was lowest for meadow voles. In addition, meadow vole males approached their pups less than pups approached the males. The opposite trend was seen in pine and prairie voles; males of those species approached their pups more often than the reverse. In meadow voles, the most likely response to follow a male's approach to a pup was the male's withdrawal from the pup. Similarly, the most frequent behaviour following a pup's approach to a male was the pup's withdrawal from the male. Pine and prairie vole males, however, remained in contact with their pups more frequently than meadow voles after an approach response. The probability of a pine or prairie vole male remaining in contact with their pups was approximately equal to, or higher than, the probability of a withdrawal response.
Indirect Paternal Activities
Species differences in the frequency and duration of the three indirect paternal activities are presented in Table III. Pine and prairie vole males
Table II, Probabilities of activities following approach responses
Subsequent activities
Species
Target activities
Meadow Maleapp. pup voles (63) Pup app. male (101) Pine voles
Prairie voles
Male app. pup (86) Pup app. male (16) Male app. pup (97) Pup app. male (59)
Male Pup withdraw withdraw from from Contact Groom Retrieve Tunnel/ nest-build Other pup male pup pup pup 0.56
0.28
0.08
--
--
0.06
0.02
0.18
0.46
0.16
--
--
0.05
0.15
0.32
0-05
0.32
0.05
0.01
0.11
0.14
0.13
0.25
0,31
--
--
0.31
0.33
0.03
0.26
0.03
0.11
0-16
0.07
0.15
0.19
0.19
0.02
0.03
0.27
0.15
Numbers in parentheses correspond to total number of approach responses.
524
Animal Behaviour, 34, 2
Table III. Species differences in indirect paternal activities
Activities
Microtus Measure pennsylvanicus
Nest construcFreq* tion/maintenance Dur~
0.19-+0.05 4.27+1.44
Tunnel construc- Freq tion/maintenance Dur Food cache
Freq Dur MDurw
Microtus pinetorum 1.11 • 20.20__+5.47
4-35__0.50 108.65•
9.53 +0-97 232.68_+23.25
0.00-+ 0"00 0'00• 0.00•
1.70_+ 0.61 6.21 _+2.02 1.07•
Microtus ochrogaster
P
1.81 _+0.30 61.76•
0.025 Ns
6-26-+0.70 0.05 171.35_+18-90 NS 0.08 _+0'04 NS 0.31 • NS 0.13__+0.07 0.001
* Freq = mean frequency of occurrence per 15-min period • SE. t Dur = mean duration _+SE in s. wMDur =mean bout durationisE in s.
Table IV. Species differences in non-paternal activities
Activities
Microtus Measure pennsylvanicus
Passive
Freq* Durt
Locomote
Freq Dur
Groom self Freq Dur Eat/drink
Freq Dur
9.04• 519.25_+26.50 4.65• 27-88•
Microtus pinetorum 10.45_+0-78 313.48_+26.68 10.34• 62.08•
3.51+0.25 2.97 • 0.26 103.16_--t-10.34 43.03• 1.40 _+0.22 55.58_+9-62
1.19 • 0-19 25.42_+5.36
Microtus ochrogaster
P
3.86+0.43 0.01 129.74_+20-30 0.001 4.60+0.56 29.27_+4-20
0.01 0.025
2.43+0.27 75-59•
NS 0.05
1.37 + 0.23 NS 78-74• 14.75 0.01
* Freq = mean frequency of occurrence per 15 min period • SE. I" Dur = mean duration _+SE in s.
c o n t r i b u t e d more indirect forms of paternal care t h a n m e a d o w vole males. The average b o u t of food caching p e r f o r m e d by pine voles was longer t h a n for m e a d o w voles, and pine vole males frequently b r o u g h t food to the nest area while m e a d o w vole males h a d a separate food cache. In addition, the frequency o f tunnel building activity was higher for pine voles t h a n for m e a d o w voles. Prairie vole males h a d more bouts of nest building b e h a v i o u r t h a n m e a d o w vole males.
Non-paternal Activities Species differences in the frequency a n d d u r a t i o n o f the n o n - p a t e r n a l behaviours are presented in Table IV. There were n o differences a m o n g the males in their responses to the females. Male pine
voles engaged in the longest b o u t s o f l o c o m o t o r behaviour, while male m e a d o w voles h a d the longest b o u t s o f passive b e h a v i o u r of the three species. Pine voles h a d shorter e a t / d r i n k b o u t s t h a n prairie voles a n d g r o o m e d themselves for shorter periods t h a n m e a d o w voles.
DISCUSSION The results reveal that of the three species, prairie a n d pine vole males are intimately involved in raising the young a n d contribute substantially to the rearing process. Prairie voles exhibited the highest level o f direct paternal care by r e m a i n i n g in the n a t a l nest in contact with the pups. They also constructed a n d m a i n t a i n e d the nest area. Pine
Oliveras & Novak: Paternal behaviour in voles voles provided slightly less direct care than prairie voles but the males maintained the runway system and cached food near the nest site. Meadow voles were the least paternal of the three species, contributing negligible amounts of direct care. They spent the majority of the time away from the natal nest and typically withdrew from the pups whenever any offspring approached them. Meadow vole males of the present study were most often found by themselves and seldom engaged in any activity other than grooming, resting or eating. These findings are consistent with results obtained in semi-natural and field studies on microtines (Thomas & Birney 1979; Getz & Carter 1980; Getz et al. 1981; McGuire & Novak 1985). However, they differ from the laboratory results of Hartung & Dewsbury (1979) and Wilson (1982) in which meadow vole males were observed to display paternal activity. The occurrence of paternal care displayed by meadow vole males of these two studies may have been promoted by forced tolerance between males and females as a result of limited space and lack of cover. The findings of this study also support previous predictions made on the social systems of these rodents. The high levels of paternal care displayed by prairie vole males are consistent with results from field and laboratory experiments which indicate that prairie voles are monogamous (Thomas & Birney 1979; Getz & Carter 1980; Getz et al. 1981; Wilson 1982; see also Dewsbury 1981). In addition, the results indicate that prairie voles have a highly structured social system wherein members live together and interact closely and frequently with one another. Prairie vole males in this study spent most of the time performing various paternal activities; two of them constructed a second nest and brooded at least one pup there while the female stayed with the remaining pups in the primary nest. The young were moved between the primary and secondary nests by both adults, thus ensuring that all pups were nursed. Similar observations by Thomas & Birney (1979) also indicate a high level of cooperation between the parents. Studies examining the social organization of M. pinetorum indicate that pine voles live in family groups and establish a pair bond (Paul 1970; FitzGerald & Madison 1983). The levels of paternal care displayed by voles in this study are consistent with interpretations that pine voles have a structured social system. Field observations on M. pennsylvanicus indicate
525
that the meadow vole is promiscuous and Madison (1980) has postulated that the social organization of meadow voles during the breeding season consists of territorial mother-offspring units. Meadow vole males of the present study nested apart from the females and were actively chased by them whenever they approached the vicinity of the natal nest. Separate nesting by the sexes was noted by Wilson (1982) and McGuire & Novak (1985) and intraspecific aggression was also reported by Getz (1962) and McGuire & Novak (1985); these observations are consistent with evidence that freeranging male and female voles occupy different territories. Paternal care in mammals has been correlated with monogamous mating systems and structured social organizations (Dewsbury 1981). Species with males that provide parental care also share certain developmental and ecological traits that differ from characteristics of species whose males do not engage in parental activities. Species occupying stable environments tend to have structured social organizations and low reproductive rates, while species living in unstable environments typically have a less structured social system and higher reproductive rates (Eisenberg 1965). Free-ranging pine and prairie voles live in stable habitats while meadow voles occupy relatively unstable environments, and the average number of pups per litter for pine, prairie and meadow voles is 2-3, 3'6 and 5"1 pups respectively (Innes 1978). Species living in stable environments also mature at slower rates than those living in unstable habitats (Eisenberg 1965; Kleiman 1977). McGuire & Novak (1985) recorded data on behavioural parameters of development in these voles, and found that meadow vole pups were the first to permanently stop nursing and to eat solid food; pine voles were the last to perform these activities while prairie voles were intermediate. The developmental and behavioural characteristics of meadow voles seemingly make them well adapted to colonizing vacated areas. Their rapid growth, promiscuous mating system and high reproductive potential would allow them to exploit temporarily abundant resources and maximize their productivity. Pine and prairie voles, on the other hand, live in more stable environments where resources are more consistently exploited. Their delayed maturation and structured social system would allow them to use available resources efficiently; in addition, their smaller litter sizes and
Animal Behaviour, 34, 2
526
increased level o f paternal care would also ensure that the young receive the full benefit o f the limited resources. ACKNOWLEDGMENTS We t h a n k George F. Drake for his assistance in the re-formatting o f data and in the p e r f o r m a n c e of sequential analyses o f behaviours.
REFERENCES Dewsbury, D. A. 1981. An exercise in the prediction of monogamy in the field from laboratory data on 42 species of muroid rodents. Biologist, 63, 138 162. Eisenberg, J. F. 1965. The social organization of mammals. Handb. Zool., 8, 1-191. FitzGerald, R. W. & Madison, D. M. 1983. Social organization of a free-ranging population of pine voles, Microtus pinetorum. Behav. Ecol. Sociobiol., 13, 183187. Getz, L. L. 1962. Aggressive behavior of the meadow and prairie voles. J. Mammal., 43, 351 358. Getz, L. L. 1972. Social structure and aggressive behavior in a population of Microtus pennsylvanicus. J. Mammal., 53, 310 317. Getz, L. L. & Carter, C. S. 1980. Social organization in Mierotus ochrogaster populations. Biologist, 62, 56-69. Getz, L. L., Carter, C. S. & Gavish, L. 1981. The mating system of the prairie vole, Microtus ochrogaster: field and laboratory evidence for pair-bonding. Behav. Ecol. Sociobiol., 8, 189-194. Hartung, T. G. & Dewsbury, D. A. 1979. Paternal behavior in six species of muroid rodents. Behav. Neur. Biol., 26, 466-478.
Innes, D. G. L. 1978. A reexamination of litter size in some North American microtines. Can. J. Zool., 56, 1488 1496. Kirk, R. 1968. Experimental Design." Procedures for the Behavioral Sciences. Belmont, California: Brooks-Cole Publishing. Kleiman, D. G. 1977. Monogamy in mammals. Q. Rev. Biol., 52, 36-69. McGuire, B. A. & Novak, M. A. 1985. A comparison of maternal behaviour in the meadow vole (Microtus pennsylvanicus), prairie vole (M. ochrogaster) and pine vole (M. pinetorum). Anim. Behav., 32, 113~1141. Madison, D. M. 1978. Movement indicators of reproductive events among female meadow voles as revealed by radiotelemetry. J. Mammal., 59, 835-843. Madison, D. M. 1980. Space use and social structure in meadow voles, Microtus pennsylvanicus. Behav. Ecol. Sociobiol., 7, 65 71. Miller, D. H. & Getz, L. L. 1969. Life-history notes on Mierotus pinetorum in central Connecticut. J. Mammal., 50, 772784. Paul, J. R. 1970. Observations on the ecology, population and reproductive biology of the pine vole, Microtus pinetorum, in North Carolina. Rep. Invest. Ill. St. Mus., 20, 1-28. Thomas, J. A. & Birney, E. C. 1979. Parental care and mating system of the prairie vole, Microtus ochrogaster. Behav. Ecol. Sociobiol., 5, 171-186. Trivers, R. 1972. Parental investment and sexual selection. In: Sexual Selection and the Descent of Man, 1871-1971 (Ed. by B. Campbell), pp. 136-179. Chicago: Aldine Press. Wilson, S. C. 1982. Parent-young contact in prairie and meadow voles. J. MammaL, 63, 300-305.
(Received 16 October 1984; revised 15 February 1985; MS. number." A4404)
A comparison of paternal behaviour in the meadow vole Microtus pennsylvanicus, the pine vole M. pinetorum and the prairie vole M. ochrogaster DIANA OLIVERAS* & MELINDA NOVAK
Department of Zoology, University of Massachusetts, Amherst, MA 01003, U.S.A.
Abstract. Paternal care in microtines has been studied infrequently and few studies have compared patterns of direct and indirect paternal investment9 The paternal behaviour of three vole species, the meadow vole (Microtuspennsylvanicus), the pine vole (M. pinetorum) and the prairie vole (M. ochrogaster) was examined in a semi-natural setting. Prairie and pine voles were found to exhibit high levels of paternal care. Prairie vole males contributed the most direct care by remaining in the natal nest for long periods of time in contact with the pups. Pine voles contributed less direct care than prairie voles as they spent less time in the natal nest with their offspring. In addition, both prairie and pine vole males were observed to groom their pups and retrieve them back to the nest area. Prairie vole males also engaged in such indirect forms of care as nest construction and maintenance, while pine voles provided indirect care in the form of tunnel construction and food caching. Meadow vole males were the least paternal of the three species and rarely engaged in either direct or indirect care. These findings support predictions that M. pennsylvanieus is promiscuous and that male and female meadow voles occupy separate territories. They are also consistent with studies which indicate that prairie and pine voles are monogamous and have a structured social organization with members interacting closely with one another9
Paternal care in rodents is thought to vary as a function of social organization and mating system, and diversity can be reflected in both the amount and type of parental activity performed by the male. For example, the quantity of paternal care is thought to be positively correlated with the probability of paternity (Trivers 1972), and thus paternal care should be more prevalent in monogamous than in promiscuous species. Male parental behaviour may also be classified into two broad categories (Kleiman 1977). Direct paternal investment, usually measured in studies of parental behaviour, consists of behaviours that have an immediate physical effect on the offspring9 These include feeding, grooming, huddling and retrieving the young9 Indirect paternal investment consists of behaviours often performed in the absence of offspring, with consequences that may be delayed for an unspecific amount of time and may affect individuals other than the young themselves9 This category includes acquisition of resources, defence of territory, construction and maintenance of nest and runways, and defence against predators. The impact of different mating systems on the quality of paternal care in rodents is not fully understood. Previous evidence indicates a wide diversity of mating systems and social organizations within the * Present address: Department of Biology, University of New Mexico, Albuquerque, NM 87131, U.S.A.
rodent genus Microtus. Based on radiotelemetric and live-trap results, the meadow vole, Microtus pennsylvanicus, appears to be promiscuous, with female voles maintaining separate territories and actively excluding adult males (Getz 1972; Madison 1978, 1980). The prairie vole, M. ochrogaster, however, is monogamous and, at normal population densities, is found in family groups (Getz & Carter 1980). Less is known about the social organization of the pine vole, M. pinetorum, but field data indicate that male and female pine voles established some form of pair bond and live in colonies composed of family members (Miller & Getz 1969; Paul 1970; FitzGerald & Madison 1983). Given such diversity of mating systems and social organizations, one might also expect variation in the amount and type of paternal care in these three species. Paternal care in microtines has been studied infrequently and only under laboratory conditions, as the natural environment of these rodents precludes measurement of such behaviour. Hartung & Dewsbury (1979) observed both meadow and prairie vole males sitting on the nest as well as licking and manipulating pups, retrieving them back to the nest area and maintaining the nest. They, as well as Wilson (1982), noted that prairie vole males spent more time huddling over their pups than meadow vole males. Despite these 519
Animal Behaviour, 34, 2
520
observations of paternal care, the authors mentioned that the experimental conditions may have influenced the behaviour of the voles, and that paternal behaviour observed in a confined laboratory setting may not reflect a male's behaviour in the field. These results differ from those of McGuire & Novak (1985) who observed meadow, prairie and pine vole pairs from underneath large, hay-covered Plexiglas-bottomed pens. Although the focus of that study was on maternal behaviour, male location was also recorded. Prairie vole males spent somewhat similar amounts of time in contact with their pups as compared to the voles in Wilson's study, but meadow vole males never huddled over their pups, nor entered the natal nest. McGuire & Novak's findings are consistent with field measures of male meadow vole activity which indicate a lack of nest cohabitation by male and female voles (Madison 1978). The above studies, however, did not compare patterns of paternal investment. It is therefore possible that the discrepant results reflect differences in the types of care provided by males of these two species. Meadow voles may contribute more indirect than direct care, while prairie voles may engage in a greater amount of direct care. The purpose of the present study was to examine the nature of paternal care expressed by meadow voles, prairie voles and pine voles. This research was conducted in the same semi-natural environment used by McGuire & Novak (1985). To determine the relative amounts of care provided by the males of each of the three species, the study focused on measures of direct paternal investment (grooming, contacting and retrieving pups) as well as several aspects of indirect paternal investment (food caching and nest and runway construction).
METHODS Subjects Six mal~female pairs from each of the following three species of microtines were studied: Mierotus pennsylvanicus (second generation offspring of voles trapped in Massachusetts), M. pinetorum (second generation offspring of voles trapped in New York) and M. oehrogaster (fifth generation offspring of voles obtained from Indiana). The data from one M. oehrogaster pair were incomplete and were therefore not used. However, the pattern of paternal care in this pair did not differ from the pattern of the remaining five pairs. Prior to this
study, the voles were kept in two large colony rooms and housed as breeding pairs in 51 x 26 x 31cm wire-mesh cages or in glass aquaria of the same dimensions. All cages had a peat and wood chip substrate with a substantial hay cover. Voles were maintained on a 14-h L: 10-h D photoperiod with lights on at 0600 hours. Water and food were available ad libitum, the diet consisting of sunflower and rye seeds and laboratory chow. In addition, the voles were given freshly sprouted rye and sunflower twice weekly. The decision to observe certain breeding pairs was based on two criteria: (1) the female was pregnant (pregnancy being determined by a 20~ weight gain) and (2) both members of the pair had successfully raised a previous litter to weaning. Immediately before placement in the observational tables, the male's entire ventral surface was dyed with black Nyanzol-D dye for easier identification.
Apparatus Paternal behaviour was observed in a pair of table-like pens connected by plastic runways identical to those described by McGuire & Novak (1985). Each table was raised approximately 70 cm off the floor on either angle-iron or wooden legs. The bottoms of the pens were constructed of a 1.3-m2 Plexiglas sheet while the sides measured at least 60 cm in height and were built of Plexiglas or metal flash!ng. The pens were layered with a 10-20 cm hay cover over 5 cm of peat substrate into which preliminary runways were cleared by the experimenters. Observations were made from beneath the tables using a 'mechanic's creeper', with data being recorded on a data acquisition keyboard (MORE, Observational Systems; Seattle, Washington).
Procedure Voles placed in the observational tables were maintained under the same feeding and lighting conditions as those in the colony rooms. Each male of a pair was observed every afternoon in 15-min sessions and data were collected from the day a litter was born to 20 days post-partum. The frequency and duration of 14 different activities were recorded, as well as the location of the male during the data session. Five activities involved direct forms of paternal care. These were 'contact pup', 'groom pup', 'retrieve pup', 'approach' and 'withdraw'. Approaches were scored when the male
Oliveras & Novak." Paternal behaviour in voles was located 4 0 ~ 5 cm from the pup and one individual moved toward the other. Withdrawals were recorded when the male was located within 15 cm of a pup and one individual moved away from the other. In addition, the locations of the male in or out of the natal nest and in or out of the table containing the natal nest were recorded. Three activities involved indirect forms of paternal care. These included 'nest construction/maintenance', 'tunnel construction/maintenance' and 'food cache'. Six activities did not involve any form of paternal care and consisted of 'approach female', 'withdraw from female', 'locomote', 'passive' (a l-s pause of inactivity or longer), 'eat/drink' and 'groom self'. The data were analysed using a mixed design analysis of variance ( A N O V A ) with species as the between-subjects variable and days (1-20) as the repeated measure. Significant species effects were further analysed with a N e u m a n - K e u l s post hoc test (Kirk 1968). RESULTS Meadow, prairie and pine vole males were found to differ in the amount and type of care they provided the young. Both pine and prairie vole males were
521
more paternal than meadow vole males, contributing direct as well as indirect forms of parental care. The amount of care provided by pine and prairie vole males decreased significantly as the pups developed. M e a d o w voles performed no appreciable levels of direct care and rarely engaged in indirect forms of parental care. Pine and prairie voles were more often found in the natal nest whereas meadow voles spent most of the time in the table that did not contain the natal nest.
Direct Paternal Activities and Location Measures
Species comparisons of the frequency and duration of direct paternal behaviours and of location measures are summarized in Table I. The data analysis revealed that prairie vole males spent 52% of the 15-min session in the natal nest, pine voles spent 30% of that time there and meadow voles spent approximately 6% of the time in the natal nestl in addition, prairie and pine voles were found in the nest throughout the 20 days of observation. However, meadow voles were typically found in the nest only after the twelfth day post partum ( F = 1.56, df=38/266, P < 0 . 0 2 5 ; Fig. 1). Time spent in the table that did not contain the natal nest followed an opposite trend. Meadow
Table I. Species differences in direct paternal activities and location measures
Activities/ locations
Microtus Measure pennsylvanicus
Microtus pinetorum
Microtus ochrogaster
P
Contact pup
Freq* Durt
0.57+0.14 72.68+18.98
1.55___0.22 1.9l +0.19 0.01 186.28__+27.50 332.98+35.69 0.01
Groom pup
Freq Dur
0.01 +0.01 0.02+0.02
0.53+0-12 6.47+ 1.74
Retrieve pup
Freq Dur
0.00 _ 0.00 0.00_ 0.00
0.04 + 0.03 0.18+0.14
0.15 __+0.06 0.97+0.42
Approach pup
Freq Dur
1.37__+0.24 5.25_+0.96
0.85+0.15 2.73+0.48
1.56_+0-29 MS 5.09+__1.05 Ns
Withdraw from pup
Freq Dur
1.31 ___0.23 2.01_+0.36
0.66+0.14 1-11 +0.24
1.30___0-26 Ns 2.25_+0-47 NS
In natal nest
Freq Dur
Out of table containing natal nest
Freq Dur
0-51+0.11 0.01 10.14___2.81 0.001 Ns ys
0.12_+0.04 0.83_+0.10 1.43+0.17 0.001 52.83___17.97 273.42___31.34 468.16___37.76 0.001 1.12+0.07 663.18+33.36
1.56_+0.14 0.29+0.06 0.01 344.14+30.54 71.81_+18.85 0.001
* Freq = mean frequency of occurrence per 15-min period + sE. t Dur = mean duration + sE in s.
Animal Behaviour, 34, 2
522 Contact pup
In nest
800 -
800
700
700
_
600
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M. p e n n s ylvanicus ......... M. pinetorum ...... M. ochrogastor Figure 1. Significant differences in the parental behaviour of meadow vole, pine vole and prairie vole males across the
first 20 days of pup development. vole males spent nearly 75~ of the time out of the table containing the natal nest as compared to pine voles which were found there only 38% of the time. Prairie vole males were rarely found in that table, spending less than 10~ of the time there. Prairie vole males were in contact with their pups for longer durations than either pine or meadow vole males. Both prairie and pine voles were seen with
their pups throughout the entire observation period but the longest contact bouts were recorded mostly during the first days of observation (F=1.52, df=38/266, P<0'05; Fig. 1). Prairie voles spent over 33% of the time with their young during early development of the litter and pine voles spent slightly more than 15% of that time together with their pups. During the same period,
Oliveras & Novak: Paternal behaviour in voles however, no meadow vole was seen with the young. All of the pup-contact activities in meadow voles occurred after the tenth day post-partum, and appeared to coincide with the pups' greater mobility during later development. In addition, all prairie and pine vole males were observed grooming their pups, yet only one meadow vole male was seen grooming pups on the 13th day post-partum and for only 3 s of that particular session. The duration of pup grooming in prairie and pine voles was high during early development and decreased steadily afterward ( F = 1.48, df= 38/266, P < 0.05; Fig. t). Prairie and pine voles also retrieved their pups to the nest but no meadow vole male was ever observed retrieving any young ( F = 1.85, df= 38/ 266, P < 0-01). Pine and prairie vole males exhibited approach (F=1-76, df=38/266, P<0.01; Fig 1) and withdraw behaviour ( F = 1.75, df=38/266, P < 0-01) during both early and late development; however, in meadow voles the vast majority of such behaviour was seen only after the litter was 10 days old. This again coincided with the increased activity of the pups themselves, especially away from the nest site. A further analysis was conducted to examine sequential dependencies in the data. Approaches were subcategorized into 'male approach pup' and 'pup approach male'. Withdrawals were subcategorized into 'male withdraw from pup' and 'pup
523
withdraw from male'. The frequencies of approach were then calculated to determine if paternal care was likely to occur once the pups and male had moved into close proximity with one another. The results of this analysis are presented in Table II. Although males of all three species approached their pups the total number of those approaches was lowest for meadow voles. In addition, meadow vole males approached their pups less than pups approached the males. The opposite trend was seen in pine and prairie voles; males of those species approached their pups more often than the reverse. In meadow voles, the most likely response to follow a male's approach to a pup was the male's withdrawal from the pup. Similarly, the most frequent behaviour following a pup's approach to a male was the pup's withdrawal from the male. Pine and prairie vole males, however, remained in contact with their pups more frequently than meadow voles after an approach response. The probability of a pine or prairie vole male remaining in contact with their pups was approximately equal to, or higher than, the probability of a withdrawal response.
Indirect Paternal Activities
Species differences in the frequency and duration of the three indirect paternal activities are presented in Table III. Pine and prairie vole males
Table II, Probabilities of activities following approach responses
Subsequent activities
Species
Target activities
Meadow Maleapp. pup voles (63) Pup app. male (101) Pine voles
Prairie voles
Male app. pup (86) Pup app. male (16) Male app. pup (97) Pup app. male (59)
Male Pup withdraw withdraw from from Contact Groom Retrieve Tunnel/ nest-build Other pup male pup pup pup 0.56
0.28
0.08
--
--
0.06
0.02
0.18
0.46
0.16
--
--
0.05
0.15
0.32
0-05
0.32
0.05
0.01
0.11
0.14
0.13
0.25
0,31
--
--
0.31
0.33
0.03
0.26
0.03
0.11
0-16
0.07
0.15
0.19
0.19
0.02
0.03
0.27
0.15
Numbers in parentheses correspond to total number of approach responses.
524
Animal Behaviour, 34, 2
Table III. Species differences in indirect paternal activities
Activities
Microtus Measure pennsylvanicus
Nest construcFreq* tion/maintenance Dur~
0.19-+0.05 4.27+1.44
Tunnel construc- Freq tion/maintenance Dur Food cache
Freq Dur MDurw
Microtus pinetorum 1.11 • 20.20__+5.47
4-35__0.50 108.65•
9.53 +0-97 232.68_+23.25
0.00-+ 0"00 0'00• 0.00•
1.70_+ 0.61 6.21 _+2.02 1.07•
Microtus ochrogaster
P
1.81 _+0.30 61.76•
0.025 Ns
6-26-+0.70 0.05 171.35_+18-90 NS 0.08 _+0'04 NS 0.31 • NS 0.13__+0.07 0.001
* Freq = mean frequency of occurrence per 15-min period • SE. t Dur = mean duration _+SE in s. wMDur =mean bout durationisE in s.
Table IV. Species differences in non-paternal activities
Activities
Microtus Measure pennsylvanicus
Passive
Freq* Durt
Locomote
Freq Dur
Groom self Freq Dur Eat/drink
Freq Dur
9.04• 519.25_+26.50 4.65• 27-88•
Microtus pinetorum 10.45_+0-78 313.48_+26.68 10.34• 62.08•
3.51+0.25 2.97 • 0.26 103.16_--t-10.34 43.03• 1.40 _+0.22 55.58_+9-62
1.19 • 0-19 25.42_+5.36
Microtus ochrogaster
P
3.86+0.43 0.01 129.74_+20-30 0.001 4.60+0.56 29.27_+4-20
0.01 0.025
2.43+0.27 75-59•
NS 0.05
1.37 + 0.23 NS 78-74• 14.75 0.01
* Freq = mean frequency of occurrence per 15 min period • SE. I" Dur = mean duration _+SE in s.
c o n t r i b u t e d more indirect forms of paternal care t h a n m e a d o w vole males. The average b o u t of food caching p e r f o r m e d by pine voles was longer t h a n for m e a d o w voles, and pine vole males frequently b r o u g h t food to the nest area while m e a d o w vole males h a d a separate food cache. In addition, the frequency o f tunnel building activity was higher for pine voles t h a n for m e a d o w voles. Prairie vole males h a d more bouts of nest building b e h a v i o u r t h a n m e a d o w vole males.
Non-paternal Activities Species differences in the frequency a n d d u r a t i o n o f the n o n - p a t e r n a l behaviours are presented in Table IV. There were n o differences a m o n g the males in their responses to the females. Male pine
voles engaged in the longest b o u t s o f l o c o m o t o r behaviour, while male m e a d o w voles h a d the longest b o u t s o f passive b e h a v i o u r of the three species. Pine voles h a d shorter e a t / d r i n k b o u t s t h a n prairie voles a n d g r o o m e d themselves for shorter periods t h a n m e a d o w voles.
DISCUSSION The results reveal that of the three species, prairie a n d pine vole males are intimately involved in raising the young a n d contribute substantially to the rearing process. Prairie voles exhibited the highest level o f direct paternal care by r e m a i n i n g in the n a t a l nest in contact with the pups. They also constructed a n d m a i n t a i n e d the nest area. Pine
Oliveras & Novak: Paternal behaviour in voles voles provided slightly less direct care than prairie voles but the males maintained the runway system and cached food near the nest site. Meadow voles were the least paternal of the three species, contributing negligible amounts of direct care. They spent the majority of the time away from the natal nest and typically withdrew from the pups whenever any offspring approached them. Meadow vole males of the present study were most often found by themselves and seldom engaged in any activity other than grooming, resting or eating. These findings are consistent with results obtained in semi-natural and field studies on microtines (Thomas & Birney 1979; Getz & Carter 1980; Getz et al. 1981; McGuire & Novak 1985). However, they differ from the laboratory results of Hartung & Dewsbury (1979) and Wilson (1982) in which meadow vole males were observed to display paternal activity. The occurrence of paternal care displayed by meadow vole males of these two studies may have been promoted by forced tolerance between males and females as a result of limited space and lack of cover. The findings of this study also support previous predictions made on the social systems of these rodents. The high levels of paternal care displayed by prairie vole males are consistent with results from field and laboratory experiments which indicate that prairie voles are monogamous (Thomas & Birney 1979; Getz & Carter 1980; Getz et al. 1981; Wilson 1982; see also Dewsbury 1981). In addition, the results indicate that prairie voles have a highly structured social system wherein members live together and interact closely and frequently with one another. Prairie vole males in this study spent most of the time performing various paternal activities; two of them constructed a second nest and brooded at least one pup there while the female stayed with the remaining pups in the primary nest. The young were moved between the primary and secondary nests by both adults, thus ensuring that all pups were nursed. Similar observations by Thomas & Birney (1979) also indicate a high level of cooperation between the parents. Studies examining the social organization of M. pinetorum indicate that pine voles live in family groups and establish a pair bond (Paul 1970; FitzGerald & Madison 1983). The levels of paternal care displayed by voles in this study are consistent with interpretations that pine voles have a structured social system. Field observations on M. pennsylvanicus indicate
525
that the meadow vole is promiscuous and Madison (1980) has postulated that the social organization of meadow voles during the breeding season consists of territorial mother-offspring units. Meadow vole males of the present study nested apart from the females and were actively chased by them whenever they approached the vicinity of the natal nest. Separate nesting by the sexes was noted by Wilson (1982) and McGuire & Novak (1985) and intraspecific aggression was also reported by Getz (1962) and McGuire & Novak (1985); these observations are consistent with evidence that freeranging male and female voles occupy different territories. Paternal care in mammals has been correlated with monogamous mating systems and structured social organizations (Dewsbury 1981). Species with males that provide parental care also share certain developmental and ecological traits that differ from characteristics of species whose males do not engage in parental activities. Species occupying stable environments tend to have structured social organizations and low reproductive rates, while species living in unstable environments typically have a less structured social system and higher reproductive rates (Eisenberg 1965). Free-ranging pine and prairie voles live in stable habitats while meadow voles occupy relatively unstable environments, and the average number of pups per litter for pine, prairie and meadow voles is 2-3, 3'6 and 5"1 pups respectively (Innes 1978). Species living in stable environments also mature at slower rates than those living in unstable habitats (Eisenberg 1965; Kleiman 1977). McGuire & Novak (1985) recorded data on behavioural parameters of development in these voles, and found that meadow vole pups were the first to permanently stop nursing and to eat solid food; pine voles were the last to perform these activities while prairie voles were intermediate. The developmental and behavioural characteristics of meadow voles seemingly make them well adapted to colonizing vacated areas. Their rapid growth, promiscuous mating system and high reproductive potential would allow them to exploit temporarily abundant resources and maximize their productivity. Pine and prairie voles, on the other hand, live in more stable environments where resources are more consistently exploited. Their delayed maturation and structured social system would allow them to use available resources efficiently; in addition, their smaller litter sizes and
Animal Behaviour, 34, 2
526
increased level o f paternal care would also ensure that the young receive the full benefit o f the limited resources. ACKNOWLEDGMENTS We t h a n k George F. Drake for his assistance in the re-formatting o f data and in the p e r f o r m a n c e of sequential analyses o f behaviours.
REFERENCES Dewsbury, D. A. 1981. An exercise in the prediction of monogamy in the field from laboratory data on 42 species of muroid rodents. Biologist, 63, 138 162. Eisenberg, J. F. 1965. The social organization of mammals. Handb. Zool., 8, 1-191. FitzGerald, R. W. & Madison, D. M. 1983. Social organization of a free-ranging population of pine voles, Microtus pinetorum. Behav. Ecol. Sociobiol., 13, 183187. Getz, L. L. 1962. Aggressive behavior of the meadow and prairie voles. J. Mammal., 43, 351 358. Getz, L. L. 1972. Social structure and aggressive behavior in a population of Microtus pennsylvanicus. J. Mammal., 53, 310 317. Getz, L. L. & Carter, C. S. 1980. Social organization in Mierotus ochrogaster populations. Biologist, 62, 56-69. Getz, L. L., Carter, C. S. & Gavish, L. 1981. The mating system of the prairie vole, Microtus ochrogaster: field and laboratory evidence for pair-bonding. Behav. Ecol. Sociobiol., 8, 189-194. Hartung, T. G. & Dewsbury, D. A. 1979. Paternal behavior in six species of muroid rodents. Behav. Neur. Biol., 26, 466-478.
Innes, D. G. L. 1978. A reexamination of litter size in some North American microtines. Can. J. Zool., 56, 1488 1496. Kirk, R. 1968. Experimental Design." Procedures for the Behavioral Sciences. Belmont, California: Brooks-Cole Publishing. Kleiman, D. G. 1977. Monogamy in mammals. Q. Rev. Biol., 52, 36-69. McGuire, B. A. & Novak, M. A. 1985. A comparison of maternal behaviour in the meadow vole (Microtus pennsylvanicus), prairie vole (M. ochrogaster) and pine vole (M. pinetorum). Anim. Behav., 32, 113~1141. Madison, D. M. 1978. Movement indicators of reproductive events among female meadow voles as revealed by radiotelemetry. J. Mammal., 59, 835-843. Madison, D. M. 1980. Space use and social structure in meadow voles, Microtus pennsylvanicus. Behav. Ecol. Sociobiol., 7, 65 71. Miller, D. H. & Getz, L. L. 1969. Life-history notes on Mierotus pinetorum in central Connecticut. J. Mammal., 50, 772784. Paul, J. R. 1970. Observations on the ecology, population and reproductive biology of the pine vole, Microtus pinetorum, in North Carolina. Rep. Invest. Ill. St. Mus., 20, 1-28. Thomas, J. A. & Birney, E. C. 1979. Parental care and mating system of the prairie vole, Microtus ochrogaster. Behav. Ecol. Sociobiol., 5, 171-186. Trivers, R. 1972. Parental investment and sexual selection. In: Sexual Selection and the Descent of Man, 1871-1971 (Ed. by B. Campbell), pp. 136-179. Chicago: Aldine Press. Wilson, S. C. 1982. Parent-young contact in prairie and meadow voles. J. MammaL, 63, 300-305.
(Received 16 October 1984; revised 15 February 1985; MS. number." A4404)