Experimental manipulation of breeding density and litter size: effects on reproductive success in the bank vole

1. Reproductive success of individual females may be determined by density-dependent effects, especially in species where territory provides the resources for a reproducing female and territory size is inversely density-dependent.
2. We manipulated simultaneously the reproductive effort (litter size manipulation: ± 0 and + 2 pups) and breeding density (low and high) of nursing female bank voles Clethrionomys glareolus in outdoor enclosures. We studied whether the reproductive success (number and quality of offspring) of individual females is density-dependent, and whether females can compensate for increased reproductive effort when not limited by saturated breeding density.
3. The females nursing their young in the low density weaned significantly more offspring than females in the high density, independent of litter manipulation.
4. Litter enlargements did not increase the number of weanlings per female, but offspring from enlarged litters had lower weight than control litters.
5. In the reduced density females increased the size of their home range, but litter manipulation had no significant effect on spacing behaviour of females. Increased home range size did not result in heavier weanlings.
6. Mother's failure to successfully wean any offspring was more common in the high density treatment, whereas litter manipulation or mother's weight did not affect weaning success.
7. We conclude that reproductive success of bank vole females is negatively density-dependent in terms of number, but not in the quality of weanlings.
8. The nursing effort of females (i.e. the ability to provide enough food for pups) seems not to be limited by density-dependent factors.     

Offspring growth, survival and reproductive success in the bank vole: a litter size manipulation experiment

To estimate the optimality of brood size, it is essential to study the effects of brood size manipulation on offspring survival and reproductive success. Moreover, testing the generality of the hypothesis of reproductive costs requires experimental data from a diversity of organisms. Here I present data on the growth, survival and reproductive success of bank vole Clethrionomys glareolus individuals from manipulated litters. Furthermore, the survival of mothers whose litter size was manipulated was studied. At weaning, the mean weight of pups from enlarged litters was lower and from reduced litters higher compared to control litters. After winter, at the start of the breeding season, individuals from enlarged litters, especially males, were still lighter than individuals from the other two treatments. Litter enlargements did not increase the number of reproducing female offspring per mother, nor did the litter sizes of female offspring differ between treatments. There were no differences between treatments in winter survival of offspring after weaning, but among female offspring, weaning weight explained the survival probabilities over winter. A higher weight of females at winter determined the probability of starting to reproduce in spring. The survival of mothers did not seem to be influenced by litter manipulation performed the previous year. According to the results, mothers nursing enlarged or reduced litters do not gain any fitness benefits in terms of number of offspring surviving to breeding. The results are consistent with the majority of experiments conducted in birds, which have found costs of enlarged brood appearing as offspring trade-offs rather than parent trade-offs. Received: 14 December 1997 / Accepted: 1 March 1998     

Maternal investment in relation to sex ratio and offspring number in a small mammal – a case for Trivers and Willard theory?

1.  Optimal parental sex allocation depends on the balance between the costs of investing into sons vs. daughters and the benefits calculated as fitness returns. The outcome of this equation varies with the life history of the species, as well as the state of the individual and the quality of the environment.
2.  We studied maternal allocation and subsequent fecundity costs of bank voles, Myodes glareolus , by manipulating both the postnatal sex ratio (all-male/all-female litters) and the quality of rearing environment (through manipulation of litter size by −2/+2 pups) of their offspring in a laboratory setting.
3.  We found that mothers clearly biased their allocation to female rather than male offspring regardless of their own body condition. Male pups had a significantly lower growth rate than female pups, so that at weaning, males from enlarged litters were the smallest. Mothers produced more milk for female litters and also defended them more intensively than male offspring.
4.  The results agree with the predictions based on the bank vole life history: there will be selection for greater investment in daughters rather than sons, as a larger size seems to be more influencial for female reproductive success in this species. Our finding could be a general rule in highly polygynous, but weakly dimorphic small mammals where females are territorial.
5.  The results disagree with the narrow sense Trivers & Willard hypothesis, which states that in polygynous mammals that show higher variation in male than in female reproductive success, high-quality mothers are expected to invest more in sons than in daughters.     

Determinants of reproductive success in voles: space use in relation to food and litter size manipulation

Spacing behaviour of female mammals is suggested to depend on the distribution and abundance of food. In addition, food limitation has been found to constrain the reproductive success of females. However, whether females maximize their reproductive success by adjusting space use in relation to current food availability and reproductive effort (e.g. litter size) has not been experimentally studied. We examined these questions by manipulating simultaneously food resources (control vs. food supplementation) and litter sizes (control vs. plus two pups) of territorial female bank voles (Clethrionomys glareolus) in large outdoor enclosures. Females with supplementary food had smaller home ranges (foraging area) and home range overlaps than control females, whereas litter size manipulation had no effect on space use. In contrast, the size of territory (exclusive area) was not affected by food supplementation or litter size manipulation. As we have previously shown elsewhere, extra food increases the reproductive success of bank vole females in terms of size and proportion of weaned offspring. According to the present data, greater overlap of female home ranges had a negative effect on reproductive success of females, particularly on survival of offspring. We conclude that higher food availability increases the reproductive success of bank vole females, and this effect may be mediated through lower vulnerability of offspring to direct killing and/or detrimental effects from other females in the population. Moreover, it seems that when density of conspecifics is controlled for, home range sizes of females, but not territoriality, is related to food resources in Clethrionomys voles.     

Age-dependent reproductive costs and the role of breeding skills in the Collared flycatcher

This study addressed whether there are any age‐related differences in reproductive costs. Of especial interest was whether young individuals increased their reproductive effort, and thereby their reproductive cost, as much as older birds when brood size was enlarged. To address these questions, a brood‐size manipulation experiment with reciprocal cross‐fostering of nestlings of young and middle‐aged female Collared flycatchers, Ficedula albicollis, was performed on the Swedish island of Gotland. Nestlings’ body mass, tarsus length and survival were recorded to estimate the parental ability and parental effort of the experimental female birds. Female survival and clutch size were recorded in the following years to estimate reproductive costs. We found that middle‐aged female flycatchers coped better with enlarged broods than younger females or invested more in reproduction. In the following year, young female birds that had raised enlarged broods laid smaller clutches than the females from all the other experimental groups. This result shows that the young female birds pay higher reproductive costs than the middle‐aged females. Both young and middle‐aged female flycatchers seemed to increase their reproductive effort when brood size was increased. However, such an increase resulted in higher reproductive costs for the young females. The difference in reproductive costs between birds of different ages is most likely a result of insufficient breeding skills of the young individuals.     

Hormonal manipulation of offspring number: maternal effort and reproductive costs

We used exogenous gonadotropin hormones to physiologically enlarge litter size in the bank vole (Clethrionomys glareolus). This method allowed the study design to include possible production costs of reproduction and a trade-off between offspring number and body size at birth. Furthermore, progeny rearing and survival and postpartum survival of the females took place in outdoor enclosures to capture salient naturalistic effects that might be present during the fall and early winter. The aim of the study was to assess the effects of the manipulation on the growth and survival of the offspring and on the reproductive effort, survival, and future fecundity of the mothers. Mean offspring body size was smaller in enlarged litters compared to control litters at weaning, but the differences disappeared by the winter. Differences in litter sizes disappeared before weaning age due to higher mortality in enlarged litters. In addition to the effects of the litter size, offspring performance was probably also influenced by the ability of the mother to support the litter. Experimental females had higher reproductive effort at birth, and they also tended to have higher mortality during nursing. Combined effects of high reproductive effort at birth and high investment in nursing the litter entailed costs for the experimental females in terms of decreased probability of producing a second litter and a decreased body mass gain. Thus, enlarged litter size had both survival and fecundity costs for the mothers. Our results suggest that the evolution of litter size and reproductive effort is determined by reproductive costs for the mothers as well as by a trade-off between offspring number and quality.     

Nest-building by the virgin female mouse exposed to ultrasound from inaccessible pups

When a naïve virgin female mouse is exposed to an inaccessible litter so that it perceives the odour and the ultrasounds from the pups, its nest-building behaviour undergoes changes that are different from changes occurring in a control condition providing exposure to an inaccessible adult female. Virgin females exposed to a litter built their nest as near as possible to the pups. Other characteristics of their nest-building behaviour were influenced differently according to the type of ultrasound that the pups were emitting. In a condition where pups were mainly calling in response to cold, virgin females built heavier nests than control females. When mainly calls in response to handling were given by the pups, the females built lighter nests than control females. Finally, there was also some suggestion that the females exposed to ultrasounds from handled pups tended to chew the nest-material more than either control females or females exposed to ultrasound from cooled pups.     

Do Laboratory Mouse Females that Lose Their Litters Behave Differently around Parturition?

Efficiency in laboratory mouse breeding is hampered by poor reproductive performance, including the loss of entire litters shortly after birth. However, the underlying mechanisms are not yet fully understood and establishing the cause of death in laboratory mouse pups can be complicated. Newborn mouse pups are generally hidden in nests, dead pups are often eaten by the female, and the widespread practice of leaving periparturient females undisturbed complicates inspection, which may delay the discovery of pup loss. In order to efficiently prevent problems with litter loss, it is important to find key factors for survival. We investigated differences in periparturient behavior between female laboratory mice whose pups survived until weaning and females whose entire litters were lost. Video recordings of 82 primiparous females of the C57BL/6 strain or knockouts with C57BL/6 background were used. The mice were observed from 24 h before until 24 h after parturition and female behaviors coded using a pre-established ethogram. The relationship between behavior and survival was analyzed using logistic models, where litter survival was regressed on the proportion of 30-s observations with at least one occurrence of the behavior. We found that females with surviving litters performed more nest building behavior during the last 24 h before parturition (p = 0.004) and spent less time outside the nest during the entire observation period (p = 0.001). Increased litter survival was also associated with more passive maternal behaviors and the female ignoring still pups less. Females that lost their litters performed more parturition-related behaviors, suggesting prolonged labor. The results indicate that maternal behavior plays a significant role in laboratory mouse pup survival. Complications at parturition also contribute to litter mortality.     

Adult female prairie voles and meadow voles do not suppress reproduction in their daughters

Reproductive suppression of young females by conspecific females has been reported from laboratory studies on several species of rodents, including the prairie vole, Microtus ochrogaster, but not meadow voles, M. pennsylvanicus. We exposed female prairie voles and meadow voles to two treatments: a mother and one 23-26-day-old daughter paired with a strange male and a 23-26-day-old daughter paired with a different strange male. We found no differences in the proportion of daughters breeding or the time to sexual maturation for daughters raised in the two treatments for either species. Thus, we have no indication that mothers had any adverse effect on reproductive efforts of their daughters. These results differ from previous studies that concluded young female prairie voles were reproductively suppressed by female relatives. The difference between our and previous studies on reproductive suppression is that we examined breeding in young females rather than proximate measures of growth and reproductive development. We question the evolutionary significance of reproductive suppression among related female microtine rodents, especially in that it has not been documented from field populations.     

The cost of dominance: suppressing subordinate reproduction affects the reproductive success of dominant female banded mongooses

Social species show considerable variation in the extent to which dominant females suppress subordinate reproduction. Much of this variation may be influenced by the cost of active suppression to dominants, who may be selected to balance the need to maximize the resources available for their own offspring against the costs of interfering with subordinate reproduction. To date, the cost of reproductive suppression has received little attention, despite its potential to influence the outcome of conflict over the distribution of reproduction in social species. Here, we investigate possible costs of reproductive suppression in banded mongooses, where dominant females evict subordinates from their groups, thereby inducing subordinate abortion. We show that evicting subordinate females is associated with substantial costs to dominant females: pups born to females who evicted subordinates while pregnant were lighter than those born after undisturbed gestations; pups whose dependent period was disrupted by an eviction attained a lower weight at independence; and the proportion of a litter that survived to independence was reduced if there was an eviction during the dependent period. To our knowledge, this is the first empirical study indicating a possible cost to dominants in attempting to suppress subordinate breeding, and we argue that much of the variation in reproductive skew both within and between social species may be influenced by adaptive variation in the effort invested in suppression by dominants.     

Effects of feeding endophyte infected tall fescue seed on reproductive performance of female CD-1 mice via competitive breeding

This study was conducted to determine the effects of feeding endophyte-infected (Acremonium coenophialum ) tall fescue (Festuca arundinacea ) seed on the growth and reproductive performance of female CD-1 mice via competitive breeding. One hundred sixty female mice were randomly allocated to groups of ten and fed one of two diets. Diet 1 consisted of 50% mouse chow and 50% noninfected Ky-31 tall fescue seed (w/w). Diet 2 contained 50% chow and 50% tall fescue seed that was 80% infected with A. coenophialum . After 50 d of preconditioning on their respective diets, a single male was introduced into each group of 10 females and allowed to cohabitate for 96 h. The males were removed after the cohabitation period and the females continued through gestation on their respective diets. Body weight of dams and litter weights were recorded at parturition. There were no differences (P>0.05) in pregnancy rates between dietary Treatments 1 and 2 (50% vs 48.8%, respectively). However, the average number of pups born per litter (11.10 pups) and average total litter weight (17.21 g) was greater for those females consuming Diet 1 than for females consuming Diet 2 (9.33 pups per litter and 13.97 g total litter weight). The incidence of dead and cannibalized pups was more frequent with Diet 2 than Diet 1 (0.13 vs 0.0 dead; 0.21 vs 0.03 cannibalized, respectively). The obtained data suggest that although the pregnancy rate was similar between the two dietary treatments, the reproductive capacity (litter size and litter weight) of female CD-1 mice was affected by the consumption of endophyte infected fescue seed.     

Comparative studies on the reproductive biology of three species of laboratory bred Australian conilurine rodents (Muridae: Hydromyinae)

The reproductive biological parameters of laboratory bred and maintained individuals from three species of Australian conilurine rodents, Notomys alexis, Pseudomys australis and P. nanus were determined. Considerable' divergence was found in interbirth intervals (indicative of gestation length) in nonsuckling and suckling mothers, litter size, growth rate of pups, age at weaning, and time of sexual maturity in both males and females. It is concluded that selection has been for rapid production and development of young in P. nanus , whereas in P. australis and, especially N. alexis , litter size has been maximized within the constraints of the mammary formula. These data further emphasize the high degree of plasticity of the reproductive system in this assemblage of old endemic murid rodents of Australasia.     

The first reproductive parameters and evidence of multiple paternity in one new spiny dogfish species,Squalus albicaudus (Squaliformes,Squalidae)

Understanding elasmobranch reproductive biology is necessary for species conservation. Multiple paternity (MP) has been reported for elasmobranchs, and this study investigates the reproductive aspects and mating system (paternity genetic analyses) for Squalus albicaudus. Thirteen pregnant females were analysed concerning reproductive parameters, and the mating system was assessed for nine females and their litters. The study found a mean fecundity of 2.84 pups per litter without correlation between total female length and the number of embryos per litter. One litter showed evidence of MP, indicating the presence of polyandrous behaviour of the species.     

Limitation of reproductive success by food availability and litter size in the bank vole,Clethrionomys glareolus

Food limitation has been suggested as one of the most important factors affecting life history evolution in terrestrial vertebrates. However, this inference is based mainly on evidence from birds, and reproductive trade-offs may differ among groups with different forms of parental care. To study whether the costs of enlarged litters (decreased mass of offspring) would appear when food is not limiting, we performed outdoor enclosure experiments in which we manipulated simultaneously the litter size (control versus litter plus two pups) and food availability (control versus food-supplemented) of female bank voles, Clethrionomys glareolus. The weaning success of females increased significantly in response to supplementary food. When females were provided with extra food, no differences were observed in body masses of weanlings of control and enlarged litters. Further, food-supplemented females grew to larger sizes during nursing than unsupplemented females. Our experiment suggests that energetic requirements during nursing constrain the number of offspring that can be raised successfully in a particular breeding attempt. The results also indicate that unlimited food resources may increase future reproductive potential of females because they can use more energy for somatic growth.     

Reproductive effort and costs of reproduction in female European ground squirrels

Reproductive effort, factors affecting reproductive output and costs of reproduction were studied in primiparous yearling compared to multiparous older female European ground squirrels (Spermophilus citellus). Yearling females weaned smaller litters than older ones. Litter size increased with posthibernation body mass at the expense of slightly lighter young for yearling but not for older mothers. In older females, on the other hand, emergence body mass influenced offspring mass, whereas litter size was affected by oestrus date. High reproductive effort entailed reproductive costs in terms of reduced subsequent fecundity but not subsequent survival for both yearling and older females. The production of large litters and long duration of lactation delayed subsequent oestrus, which, in turn, correlated negatively with litter size. During the second half of lactation, oestradiol levels were significantly elevated, indicating the initiation of follicular maturation processes. Oestradiol levels during that time correlated negatively with current, but positively with subsequent litter size. We therefore assume that inhibitory effects of lactation on gonadal development may mediate the negative relationship between reproductive effort and subsequent reproductive timing in adults. This effect is absent in yearlings because they are reproducing for the first time. Reproductive output in yearlings was influenced by interactions between structural growth and puberty. Received: 22 March 1999 / Accepted: 7 June 1999     

Reproductive success of solitarily and communally nesting white-footed mice and deer mice

To determine the fitness consequences of communal nesting inwhite-footed mice, Peromyscus leucopus, and deer mice, P. maniculalus,I compared the reproductive success of field populations offemales nesting solitarily, in communal groups of more thanone female, in extended families of successive litters, andin communal groups with extended families. Mean first littersize of weanlings and juveniles 6 weeks old did not differ significantlyfor pups raised under the four nesting situations. Similarly,for pups born into extended families, litter sizes of pups fromsecond litters did not differ significantly from those of firstlitters or from pups born to solitarily nesting females. Delayeddispersal of juvenile females did not result in resource competitionor inhibition of reproduction. Thus, reproductive success offemales was not significantly affected by additional membersin the nest. At least 26 of 28 communally nesting females wereclose relatives. Solitary nesting is the common breeding patternin Peromyscus, and extended families and communal nesting arealternative reproductive tactics in response to limited space,delayed dispersal, and local grouping among related females.     

Sex-specific costs of reproduction in Eastern Bluebirds Sialia sialis

In species with bi-parental care, individuals must partition energy between parental effort and mating effort. Typically, female songbirds invest more than males in reproductive activities such as egg-laying and incubation, but males invest more in secondary sexual traits used in attracting mates. Animals that breed more than once within a season must also allocate time and energy between first and subsequent breeding attempts and between current and future breeding seasons. To investigate strategies of reproductive investment by males and females and the consequences of such strategies, we manipulated the size of broods of Eastern Bluebirds Sialia sialis . Pairs with enlarged first broods were less likely to produce a second clutch or took longer to initiate one than pairs with reduced broods. After rearing enlarged broods, females were less likely than males to survive to the following year. Although plumage coloration is a sexually selected trait in Eastern Bluebirds that is influenced by nutritional stress, we did not detect an effect of brood-size manipulation on female coloration. Past research, however, demonstrates that, in males, plumage colour is negatively affected by increasing brood size. We suggest that there are sex-specific strategies of reproductive investment in Eastern Bluebirds, and that researchers should incorporate measures of residual reproductive value in studies of life-history evolution.     

Influence of maternal mass and condition on energy transfer in Weddell seals

1. Environmental variation influences food abundance and availability, which is reflected in the reproductive success of top predators. We examined maternal expenditure, offspring mass and condition for Weddell seals in 2 years when individuals exhibited marked differences in these traits. 2. For females weighing > or = 355 kg there was a positive relationship between maternal post-partum mass (MPPM) and lactation length, but below this there was no relationship, suggesting that heavier females were able to increase lactation length but lighter females were restricted to a minimum lactation period of 33 days. 3. Overall, females were heavier in 2002, but in 2003 shorter females were lighter than similar-sized females in 2002 suggesting that the effects of environmental variability on foraging success and condition are more pronounced in smaller individuals. 4. There was no relationship between MPPM and pup birth mass, indicating pre-partum investment did not differ between years. However, there was a positive relationship between MPPM and pup mass gain. Mass and energy transfer efficiency were 10.2 and 5.4% higher in 2002 than 2003, which suggests costs associated with a putatively poor-resource year were delayed until lactation. 5. Heavier females lost a higher proportion of mass during lactation in both years, so smaller females may not have been able to provide more to their offspring to wean a pup of similar size to larger females. 6. MPPM had only a small influence on total body lipid; therefore, regardless of mass, females had the same relative body composition. Females with male pups lost a higher percentage of lipid than those with female pups, but by the end of lactation female pups had 4.5% higher lipid content than males. 7. It appears that for Weddell seals the consequences of environmentally induced variation in food availability are manifested in differences in maternal mass and expenditure during lactation. These differences translate to changes in pup mass and condition at weaning with potential consequences for future survival and recruitment.     

Age at puberty and first litter size in early and late paired rats

The rate of sexual maturation among female Sprague-Dawley rats was measured in a variety of intraspecific social environments. It was found that females of this strain differ from at least one other strain of laboratory rat in that neither age at vaginal perforation nor age at first estrus was affected in Sprague-Dawley females by the presence or absence of male, regardless of his age or breeding history. Sizes of first litter among females who mated at their first estrus were compared with those among females who were first inseminated at older ages. On average, females bred at first estrus produced litters that contained more than 3 fewer pups than females mated at older ages. This observation suggests that female Sprague-Dawley rats do not attain full reproductive competence until sometime after the onset of puberty.     

The effects of size, age and a cost of early breeding on reproduction in female mountain hares

Both age and size may influence female reproductive performance in mammals, and successful early reproduction may lead to reduced success at later attempts. The effects of age, size and early reproduction on distribution of reproductive effort throughout a single breeding season was examined in female mountains hares Lepus timidus L. Hind foot length was used as an index of body size, because, unlike body weight, it did not fluctuate with reproductive status. Fifty-six female carcasses were collected from March to October 1984, and their litters were assigned to one of three chronologically equal'litter periods'(1–3) of equal length. Whereas number of ova shed was always independent of age, large females shed more ova than did smaller females in litter periods 1 and 2. Prenatal mortality of ova and embryos was highest during litter period 1, when it was independent of age and size. Although prenatal mortality remained high in first year females in litter period 2, there was an overall decline through to the final litter period when it was negligible. Total number of young produced through the season increased with skeletal size in old females (age > 1), but not significantly in first year females. It is concluded that large size, rather than age, favours early reproduction in mountain hares. Every additional offspring produced in litter periods 1 and 2 reduced that female's production in period 3. After correcting for this cost of early reproduction the number of young produced in the final litter period also increased with maternal size.