Kinships in a natural meadow vole population

Summary We have devised a radionuclide technique that allows the assessment of matrilineal kinship by the transfer of unique combinations of gamma-emitting radionuclides from pregnant and lactating female meadow voles (Microtus pennsylvanicus) to their offspring. A pool of prospective fathers can be established from field records of reproductively active males that were alive at the time of conception of the female's litter. Electrophoresis of 6 proteins allowed us to eliminate genetically incompatible males from the prospective pool of fathers. A log-likelihood statistic provided an estimate of the probability of paternity. In the case of numerical ties physical proximity of the males to the mother at the time of conception was used. With these techniques, we established 40 kinships in a field population of meadow voles.     

Male dominance,female choice and male copulatory behavior in two species of voles (Microtus ochrogaster and Microtus montanus)

Summary Female preferences for dominant males in prairie and montane voles were analyzed in two different test situations. In the first, prairie vole females preferentially spent time in proximity to dominant versus subordinate males which were housed behind a wire mesh screen. In a two-male tether test prairie voles females both preferentially associated and mated with dominant males. Montane voles, on the other hand, showed no preference in either test situation. The baseline copulatory behavior of naive montane vole males which became dominant differed significantly from those which became subordinate; no such differences were evident in the baseline copulatory behavior of naive praire voles. One hour following dominance testing, there was no difference evident between dominant and subordinate males of either species but there was a general facilitation of male copulatory behavior in both species, the effect being of greater magnitude in montane voles.     

Space use and social structure in meadow voles,Microtus pennsylvanicus

Summary Free-ranging, sexually mature meadow voles (Microtus pennsylvanicus) were tracked by using radiotelemetry from June through August in Front Royal, Virginia, U.S.A. Estimates of intraspecific spacing were derived from the concurrent movements of up to 16 voles. Positions were recorded hourly for 24 h, twice per week. A total of 16 male and 15 female voles were studied during sixteen 24-h sessions.The daily ranges of males (192.3±109.7 m²) were larger and more variable than those of females (68.6±39.4 m²). Males also changed locations more frequently (Fig. 2).Adult females usually maintained territories free of other females; males overlapped considerably among themselves (Fig. 2). Males temporarily moved into the areas occupied by estrous females, indicating intrasexual competition among males for access to receptive females (Fig. 3). M. pennsylvanicus appears to be promiscuous, is socially organized into territorial, maternal-young units during the breeding season, and fits the female territorial model of population regulation.     

Trichinella spiralis infection in voles alters female odor preference but not partner preference

Females may choose mates based on secondary sex traits that reflect disease resistance. Accordingly, females should be able to distinguish between unparasitized and parasitized males, and should prefer to mate with unparasitized individuals. Mate and odor preferences for uninfected males or males infected with the nematode, Trichinella spiralis, were examined among prairie voles (Microtus ochrogaster) and meadow voles (M. pennsylvanicus). In a 15-min odor preference test, only female meadow voles distinguished between bedding from parasitized and unparasitized conspecific males, and preferred to spend time with bedding from unparasitized males. Although T. spiralis infection influenced odor preference in female meadow voles, there was no effect of infection status on mate preference among either species. Testosterone and corticosterone concentrations were not different between parasitized and unparasitized males. However, among prairie voles, males that spent an increased amount of time with females during the mate preference test had elevated testosterone concentrations. Taken together, these data suggest that (1) female meadow voles can discriminate between unparasitized and parasitized males, (2) the effects of infection on steroid hormone concentrations may be masked by the effects of social interactions, and (3) parasites may represent a selective constraint on partner preference in voles; however, the life cycle of parasites may influence female preference and should be considered in studies of female preference. Received: 23 April 1998 / Accepted after revision: 25 October 1998     

Multiple paternity in meadow voles (Microtus pennsylvanicus): investigating the role of the female

Multiple paternity in single litters conceived in the wild was recently demonstrated in meadow voles (Microtuspennsylvanicus). In this study, we used an experimental approach (males tethered and females allowed to mate freely with one or several males) to investigate the role of female meadow voles in multiple paternity. We found that among 29 (of 39) females that copulated during our experiment, 79.3% chose to mate with more than one male. Female behavior in meadow voles thus clearly promotes multiple paternity and their role is an active one. Some of the hypotheses explaining promiscuity in meadow voles should be reconsidered in light of this result. We do not know the primary determinant of female mate choice, but male body mass played a secondary role in driving female preferences. The partial dependence between male body mass and female choice, coupled with the active role played by females, indicates that intersexual selection has the potential for reinforcing the effects of intrasexual selection (male-male dominance relationships) in this species. Finally, we demonstrate that the time period over which tests are conducted is an important part of the design of experiments aimed at understanding the role of females in multiple paternity. Received: 14 April 1998 / Accepted after revision: 12 September 1998     

Spatial organization and mating system of Microtus townsendii

Summary Space use by individual Townsend's voles, Microtus townsendii, was investigated in spring and summer by means of radiotelemetry and intensive live trapping in undisturbed grasslands near Vancouver, British Columbia. Home ranges of males were larger than those of females; females had significantly larger ranges in spring than in summer. Most males and females maintained territories free of individuals of the same sex in spring. Male-female pairs had their exclusive territories closely overlapping each other. The 1:1 operational sex ratio and the spatial association of pairs of males and females suggest that the voles were monogamous in the spring of 1988 and that 50% of the males were monogamous in the spring of 1989. In summer, there was more intrasexual overlap between home ranges of males and females and female ranges were considerably smaller than those of males. Females were more philopatric than males and females thought to be members of the same family group lived adjacent to each other or had overlapping home ranges. Males overlapped with more than one female in summer, but most females still overlapped with only one male, which suggests that the mating system is polygynous in summer. Thirty-five percent of the philopatric females became pregnant for the first time when the male spatially associated with their mother in the spring was still alive and thus could potentially have mated with their fathers. Male and female territoriality in spring is the proximate mechanism for the limitation of breeding density by spacing behaviour.[/p] Offprint requests to: C.J. Krebs     

Different escape tactics of two vole species affect the success of the hunting predator, the least weasel

In the ongoing evolutionary arms race between predators and their prey, successful escape from the predator leads to the evolution of improved escape tactics in prey, but also predators become more effective in following and attacking the prey. Antipredatory behavior of prey is considered to be the strongest towards their most dangerous predators. However, prey species can differ both in vulnerability and efficiency of escape to a shared predator. We studied escape reactions of two vole species, the bank vole (Myodes glareolus) and the field vole (Microtus agrestis), under a simulated predation risk of the least weasel (Mustela nivalis nivalis). We conducted a laboratory experiment where a vole was given a possibility to escape from a weasel by fleeing to a horizontal tunnel or climbing the tree. Subsequently to the vole escape decision, we released a weasel to the same tunnel system to test how the weasel succeeded in following the vole. Weasel presence changed the behavior of voles as especially bank voles escaped by climbing. Instead, the majority of field voles fled into the ground-layer tunnel. The different escape tactics of the voles affected the success of the weasel, because climbing voles were less often successfully followed. We suggest that the difference in escape tactics has evolved as an adaptation to different habitats; meadow-exploiting field voles using ground-level escape while bank voles living in three-dimensional forest habitat frequently use arboreal escape tactics. This is likely to lead to different habitat-dependent vulnerabilities to predation in Microtus and Myodes vole species.     

A field test of the Bruce effect in the monogamous prairie vole (Microtus ochrogaster)

The Bruce effect is a widely studied reproductive phenomenon in rodents in which exposure of pregnant females to unknown males causes termination of the current pregnancy. The Bruce effect has been reported from numerous studies in the laboratory, and one field study with the promiscuous gray-tailed vole, Microtus canicaudus, failed to support it. We conducted a field study with the monogamous prairie vole, M. ochrogaster, to determine if complete replacement of the male population every 10-14 days affected pregnancy and juvenile recruitment. The mean days to first parturition for control and treatment females were 36.8 and 44.4 days. Fifty-five percent of control females and 33% of treatment females conceived within the first 14 days of the study. All control females and 79% of treatment females successfully delivered at least one litter. These differences between treatment and control populations provide minimal support for the Bruce effect when compared with results from laboratory studies. Nulliparous females may have experienced some pregnancy disruption, but not parous females. Removal of mates, rather than exposure to strange males, may have contributed more to the lower reproductive success of treatment females than exposure to strange males. Treatment females, however, had lower juvenile recruitment than controls, which may have been due to infanticide from strange males. Our results are more similar to those of the field study of the gray-tailed vole than predicted, based on laboratory studies of prairie voles.     

Tradeoffs between courtship, fighting, and antipredatory behavior by a lizard, Eumeces laticeps

Male fitness in many species depends strongly on social behaviors needed to obtain fertilizations and prevent loss of fertilizations to other males, but courtship, copulation, and fighting may incur increased risk of predation. When demands for reproductive and antipredatory behaviors conflict, fitness may be maximized by accepting some degree of risk to enhance reproductive success. To examine such tradeoffs, I introduced tethered conspecific males or females to adult male broad-headed skinks, Eumeces laticeps, in the field and observed how close they allowed a simulated predator (me) to approach before fleeing, or their latency to approach an introduced female located at different distances from the predator. When conspecific males were introduced, isolated and mate-guarding males initiated agonistic behaviors and permitted closer approach than control males, and mate-guarding males permitted closer approach than isolated males. When females were introduced, both isolated and mate-guarding males courted the introduced females and isolated males permitted closer approach than did mate-guarding males. These results for introduced males and females suggest that increasing risk was accepted when reproductive benefits were greater. Latency for isolated males to approach a conspecific female was greater when the predator was closer to the female, further suggesting sensitivity to predation risk during a reproductive opportunity. Relationships between reproductive and antipredatory behaviors have been studied much less than those between feeding and antipredatory behaviors, but this study indicates that animals balance increased risk of predation with the opportunity to perform several reproductively important behaviors. Received: 5 March 1999 / Received in revised form: 15 July 1999 / Accepted: 25 July 1999     

A field test of the effects of familiarity and relatedness on social associations and reproduction in prairie voles

Inbreeding depression is a well-documented phenomenon. In animals, one means of avoiding the costs of inbreeding is through the recognition and avoidance of kin as mates. Prairie voles (Microtus ochrogaster) are short-lived, socially monogamous rodents that demonstrate inbreeding depression in the laboratory. Field data indicate that pair formation in nature is opportunistic but pairing among close relatives seems uncommon. We examined the role of relatedness and familiarity on prairie vole social associations and reproduction by placing adult voles into 0.1-ha enclosures with familiar siblings, unfamiliar siblings, and unrelated, unfamiliar conspecifics. Live-trapping data indicated that indices of social pair bonding were random with respect to relatedness and familiarity. Among females whose litters were sired by a single male, litters were significantly more likely to be sired by unfamiliar than familiar males, but the number of litters sired by males that were unrelated to their partner was not different from the number of litters sired by males that were related to their partner. Additionally, females that produced offspring with familiar siblings were significantly more likely to have litters with multiple paternity than females not producing offspring with familiar siblings. However, multiple paternity was not influenced by relatedness of sires. Finally, older individuals were more likely to produce offspring with each other than with younger individuals. Our findings suggest that prior association is a more important mechanism of inbreeding avoidance than phenotype matching for prairie voles mating under ecologically relevant conditions.     

Length polymorphism at the avpr1a locus is correlated with male reproductive behavior in a natural population of prairie voles (Microtus ochrogaster)

Laboratory studies have shown that vasopressin can influence sociosexual behavior through its action on the vasopressin 1a receptor (V1aR). There is substantial evidence that the length of a microsatellite in the gene (avpr1a) encoding for the V1aR can affect social attachment to females and paternal behavior in male prairie voles under laboratory conditions. However, previous field studies of prairie voles have failed to detect a strong effect of the length of a male’s avpr1a allele on their sociosexual behavior, but these studies are typically much shorter than the average prairie vole breeding lifespan. We examined the relationship between male avpr1a microsatellite allele length and sociosexual behavior in a natural population of prairie voles for 15 weeks, closer to the lifespan of prairie voles in nature. Contrary to predictions, we found that males with the longest avpr1a microsatellite alleles were significantly more likely to sire offspring with more than one female and to sire offspring that survived until trappable age than males with the shortest avpr1a microsatellite allele lengths. This relationship was the strongest for males with the longest tenure on the study site. As in previous field studies, we did not find evidence of a relationship between a male’s avpr1a genotype and any index of social behavior including male residency status or the number of females with which males associate. This is the first study to support the hypothesis that a male’s avpr1a genotype is a factor underlying variation in the genetic mating system of prairie voles under natural conditions.     

Male turnover reduces population growth: an enclosure experiment on voles

Turnover of individuals is assumed to cause disruptions of social organization, followed by reduced reproduction and survival. We tested how male turnover (removal of resident males and their replacement by unfamiliar males) affected population performance in experimental root vole (Microtus oeconomus) populations. The treatment simulated predation of adult males, with the subsequent replacement by immigrants, and provided insight into the interaction between extrinsic (i.e., predation) and intrinsic (i.e., social organization) factors. We showed that recruitment and female survival dramatically declined and that reproduction commenced slightly later in treatment populations compared with control populations. The treatment nearly halved the population growth rate. We suspect that recruitment failed due to infanticidal immigrating males. Reduced female survival was particularly apparent in treatment populations in which females exhibited a high degree of spatial overlap. Our experimental results show how males may significantly shape population dynamics and suggest how predation and social factors interact mechanistically.     

A test of male mating and hunting success in the kestrel: the advantages of smallness?

We tested female choice for male wing and tarsus length and body mass in the kestrel (Falco tinnunculus), a species in which males average about 10% smaller than females. We also studied how male characters are related to their hunting success. In the laboratory, females preferred lighter males with shorter tarsi as mates, if the difference in those characters between competing males was larger than average. Lighter and shorter-winged males seemed to be better hunters than heavier and longer-winged males. Field observations in a year in which voles were scarce suggested that shorter-winged males were also better food providers in courtship feeding than longer-winged males,although in good vole years such a relationship was not found. We argue that females may prefer to pair with smaller males, because they have higher flight performance and better hunting success than heavier males. By doing so, females may gain direct breeding advantages. We conclude that both female choosiness and the hunting efficiency of males well contribute to reversed sexual size dimorphism (RSD, females larger than males) in the kestrel. Received: 18 July 1995/Accepted after revision: 17 August 1996     

Foraging decisions of American robins: somatic and reproductive tradeoffs

Summary Breeding units (occupants of a nest including at least one reproductive female) within two free-living populations of the prairie vole, Microtus ochrogaster, were monitored by live-trapping at nest during two 28-h periods each week from October 1980 to March 1984. Data are presented for 281 breeding units from all seasons, at high and low population densities and during breeding and nonbreeding periods. Fifty percent of the breeding units were monogamous (single resident reproductive male and female), 27% consisted of a single reproductive female with no resident adult male and 23% included more than one resident adult male and/or female (complex units). Monogamous units were present in the same proportions during breeding and nonbreeding periods. The number of monogamous units was significantly greater at low population densities than at high densities. During winter there were relatively more complex units and fewer single female units than during the rest of the year. Monogamous pairs remained together for an average of 42 days. Seventy-eight percent of these pairs were disbanded by the death of one or both members. There were few overlaps of the home ranges of adjacent breeding units. Significantly more nests were visited by nonresident males than by females, and the intervals between visits by males were significantly shorter than those for visits by females. Males visited single female units significantly more often than units with one or more resident males. Survival of juveniles was generally very low; 38% and 34% of young males and females, respectively, that were trapped survived until 30 days of age. Of young females remaining at the natal nest at low population densities, only 17.6% were reproductively activated; 77.1% of such females became reproductively activated at high densities. All young females that dispersed from the natal nest became reproductive.     

Sperm competition and the level of polyandry in a bushcricket with large nuptial gifts

Variation in paternity due to sperm competition or post-copulatory female choice has a major influence on animal mating system evolution and on the levels of genetic variability in natural populations. However, there are relatively few studies comparing the outcome of sperm-competition experiments in the laboratory with natural variation in polyandry among families from the field. In the bushcricket Ephippiger ephippiger, females mate multiply, and the males provide them with a large, nutritious, and probably expensive, donation at mating. We examined paternity in a series of laboratory matings, where females mated with two males, and amongst a series of families collected from a natural population. In the laboratory, paternity was highly bimodally distributed: 24% of families had offspring fathered by the first male to mate, 68% by the second male (in only 8% was paternity shared). In the field, paternity was more mixed: only 27% of families had a single father, 14% had more than two fathers, whilst 59% had two fathers. While unsuccessful matings may contribute to the highly biased paternity in the laboratory, they cannot fully explain the high incidence of complete P2 families. Nonrandom sperm utilisation is therefore likely. Greater sperm mixing in the field probably results from females mating with more males, but the distribution of paternity also reflects an active process of nonrandom sperm utilisation. Confidence of paternity due to last male advantage may be relatively high in this species, and therefore may have facilitated the evolution of the large spermatophore in E. ephippiger.Communicated by D. Gwynne     

Trade-off between fitness components in males of the polygynous butterfly Callophrys xami (Lycaenidae): the effect of multiple mating on longevity

The differential costs of mating paid by males and females influence the nature and strength of sexual selection. In butterflies, males invest a relatively large amount of time and resources in each mating, but male survival costs of mating have not been demonstrated. I present the results of experiments designed to measure the effect of different aspects of mating on male longevity in the polygynous butterfly Callophrys xami. In experiment 1, I compared the longevity of pairs of males that produced similar amounts of spermatophore, but that mated at different rates, a different numbers of times, and that produced spermatophores at different rates, and found that the longevity of ”low-mating-rate” males was not different from that of ”high-mating-rate” males. In experiment 2, the longevity of virgin males was not significantly different from that of multiply mated males. In experiment 3, I used resource-limited males resulting from experimental food limitation of last-instar larvae; resource-limited virgin males lived significantly more days than resource-limited multiply mated males. Since ecological costs of mating (e.g., disease transmission, predation risk) were excluded in the experiment, diminished male longevity was a product of physiological costs of sexual interactions. These results suggest that the cost of ejaculate production is an important cause of longevity reduction when there are resource limitations; however, the role of other possible physiological costs of mating in longevity reduction is still unknown. Received: 21 March 2000 / Accepted: 26 August 2000     

Edge Effects and Isolation: Red-Backed Voles on Forest Remnants

Negative effects of habitat edge have been advanced as an important proximate cause of extinction, and a growing literature calls attention to the matrix surrounding habitat remnants as a critical factor determining population persistence. I examined spatial distribution of California red-backed voles ( Clethrionomys californicus ) on 13 forest remnants and five control sites in southwestern Oregon. The species was virtually isolated on remnants, making little use of the regenerating clearcuts surrounding the remnants. The effects of the clearcut also impinged on the remnants as edge effects: six times more voles were captured per trap in the interior of remnants than on the edge. Consequently, the density of voles per unit area on remnants increased with remnant size, despite the potential buildup of population density in small isolates due to limited emigration. I explored potential mechanisms of the negative edge effect on voles and found that the biomass of coarse woody debris, per se, did not explain the vole distribution because both number and volume of logs increased from the interior to the edge of remnants. However, the distribution of the vole's primary food item, hypogeous sporocarps of mycorrhizal fungi, did correspond to the vole edge effect     

Massive and distinctive effects of meadow voles on grassland vegetation

We ask whether vole herbivory in experimental grassland plots is sufficient to create an unpalatable community. In a six-year experiment, meadow voles (Microtus pennsylvanicus) reduced plant standing crop between 30% and 72%, well within the range of ungulate effects. Moreover, meadow voles reduced their available forage species by changing the plant community composition: four grass species and a legume upon which they foraged declined sharply in cover and/or number of individuals, five forbs avoided by voles increased, and two forbs neither declined nor increased with either measure. Reductions of diversity occurred when voles first defoliated the plots in 2000 but disappeared as plant species avoided by voles replaced vulnerable plants. Within six years, meadow voles created plant communities dominated by species that they did not eat.     

Is the antipredatory response in behaviour reflected in stress measured in faecal corticosteroids in a small rodent?

Predation risk has been shown to alter various behaviours in prey. Risk alters activity, habitat use and foraging, and weight decrease might be a consequence of that. In mammals, studies on physiological measures affected by risk of predation, other than weight, are rare. We studied in two separate laboratory experiments foraging, hoarding behaviour and expression of stress measured non-invasively from the faeces in the bank vole (Clethrionomys glareolus), a common boreal rodent. Voles were exposed to predation risk using odours of the least weasels (Mustela nivalis nivalis). Distilled water served as control. In the first experiment, we found that foraging effort, measured as sunflower seeds taken from seed trays filled with sand, was significantly lower in trays scented with weasel odour. Both immediate consumption of seeds and hoarding were affected negatively by the weasel odour. Females hoarded significantly more than males in autumn. In the second experiment, the negative effect of weasel odour on foraging was consistent over a 3-day experiment, but the strongest effect was observed in the first night. Foraging increased over the time of the experiment, which might reflect either energetic compensation during a longer period of risk, predicted in the predation risk allocation hypothesis, or habituation to the odour-simulated risk. Despite decreased foraging under predation risk, stress measured as corticosteroid metabolite concentration in vole faeces was not affected by the weasel odour treatment. In conclusion, we were able to verify predation-risk-mediated changes in the foraging effort of bank voles but no physiological stress response was measured non-invasively, probably due to great individual variation in secretion of stress hormones.     

Delayed breeding in the cooperatively breeding Florida scrub-jay (Aphelocoma coerulescens): inhibition or the absence of stimulation?

To determine whether fundamental differences exist in the reproductive physiology of breeder and nonbreeder Florida scrub-jays (Aphelocoma coerulescens), we compared plasma levels of testosterone (T) and luteinizing hormone (LH) in males, and estradiol (E₂) and LH in females. Although male breeders had higher overall T and larger testes, nonbreeders’ T paralleled that of breeders, and their testes were more than an order of magnitude larger than regressed testes. Breeder and nonbreeder males had equivalent baseline LH, and equivalent changes in LH following a gonadotropin-releasing hormone (cGnRH-I) challenge. The T, LH and GnRH challenge data indicate that nonbreeder males have functional hypothalamo-pituitary-gonadal (HPG) axes. We found no hormonal evidence of inbreeding suppression in males: nonbreeders that did not live with their mothers and those that did had similar T. Male nonbreeders that were exposed to E₂-implanted females had higher T than did controls, suggesting that the lack of within-pair stimulation is a key factor in whether an individual delays breeding. Female nonbreeders had E₂ titres equal to or higher than breeders and neither basal LH nor LH following GnRH challenge differed by breeding status. Nonbreeders’ ovarian follicles were smaller than breeders’, but were larger than they would be during the non-breeding season. These data suggest that nonbreeders were primed for breeding and were simply waiting for an opportunity or a required stimulus. Female nonbreeders that lived in a territory with an unrelated male breeder had significantly higher E₂ than those that remained with their fathers. Similarly, nonbreeders that were captured away from their home territories had elevated E₂. However, nonbreeders that lived with their fathers had E₂ that was equivalent to breeding females, suggesting that inbreeding avoidance may not be the primary factor leading to delayed breeding in females. Received: 13 June 1995 /Accepted after revision: 27 April 1996