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     

Breeding season, litter size and nestling mortality of the Harvest mouse, Micromys minutus (Rodentia: Muridae), in Britain

Data are presented on the breeding biology of Micromys minutus in Britain. It is shown that although litters are produced over a protracted period (May-December), 74% of the litters are born in August and September. Mean litter size is 5·40±0·16( n = 62), which is a significant reduction on the mean litter size of 6·75±0·40( n = 16) calculated from pre-1917 literature. Litter size was found to be constant throughout the breeding season, and there was no difference in mean litter size between two samples collected close to the northern and southern limits of the known British range. By comparing the mean litter size of samples 1–5, 6–10 and 11+ days old, no significant loss of individual mice within litters could be detected, although 12·3% of all litters died prior to weaning. This loss was predominantly of autumnal litters, cold and wet being important climatic factors that terminate the breeding season. Comparisons are made with data from other parts of the animal's range.     

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.     

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.     

A reproductive study of Weiser-Maples guinea pigs]

The Weiser-Maples (WE) guinea pig strain was introduced by Backshire Co., Ltd. (USA) in 1977. We have been breeding WE strain guinea pigs for skin melanization research. The WE guinea pig colony produced 1271 pups in 417 litters from May 1978 through December 1983. Breeding date are shown below. The mean litter size was 3.05, the stillborn rate was 15.2%, the weaning rate for live-born pups was 93.5% and the sex ratio was 1.01. The average age at first vaginal membrane rupture was 31.4 days at which time body weight was 290.5g. The mean length of the first 7 estrous cycles was about 17 days, with no cyclical variation in length. The mean duration of gestation was 67.9 days. Duration of pregnancy varied with litter size. There was an inverse relationship between litter size and duration of pregnancy. Most of the pups were delivered alive in mid-pregnancy with a parturition range of 56 to 76 days. The probability of pup death depends on gestational length: the lowest incidence of mortality was seen in litters born at 70 days. The mortalities were related to litter size but not to parity. There was an inverse relationship between birth weight and litter size. In WE guinea pigs, the mean weight for a litter of 1 was 120 g; for a litter of 5, the mean body weight was 58g. Male body weights were slightly heavier than female at birth and at weaning age. The mean body weights are shown below, date of birth: female 88.3g, male 93.3g, weaning age (2 weeks): female 181.1g, male 198.8g and 30 weeks: female 758.7g, male 1018.0g. These date for WE guinea pigs are comparable to those of other strains.     

Breeding system can affect the offspring sex ratio in Syrian hamsters

Nulliparous female Syrian hamsters were used to investigate the effect of two different breeding systems on the fertility of the female Syrian hamster. We hypothesized that females submitted to a harem system (HS) would deliver smaller and more female-biased litters than in a monogamic system. Ten female and 10 adult male hamsters housed individually (G1) were kept in a monogamic temporary breeding system, while 10 females and five males (G2) were submitted to HS with two females and a male permanently housed together since female weaning. Females from G1 and G2 delivered, respectively, 47 and 50 litters, and produced 364 (G1) and 383 (G2) weaned pups without any difference in litter size, mean weight of weaned pups and body condition of dams. Interparturition intervals were shorter and the percentage of male pups per litter was higher in the HS possibly as a result of different endocrine conditions provided by different breeding systems. Besides providing evidence that housing conditions can influence the sex of hamster offspring, our findings suggest a mechanism for the non-random distribution of male and female pups in hamster litters.     

Lifespan ontogeny of breeding and reproductive success in Mongolian gerbils

An analysis was made of demographic data collected from a colony of Mongolian gerbils (Meriones unguiculatus). The data on births of over 3800 gerbils provide evidence on several aspects of development and fecundity. Approximately 4% more females than males survived to weaning. Mean number of pups per dam per year was estimated to be 48.3, greater reproductive success than reported previously. The shortest period of gestation resulting in viable pups was 25 days. Implantation was delayed by the presence of suckling pups. When gestation was prolonged, there was a direct relationship between the number of pups being suckled concurrently and the length of the delay. Length of gestation did not affect the size of the subsequent litter. Female gerbils gave birth as early as 72 days of age. Gerbils continued to reproduce until after 2 years of age in some cases. There were fewer pups per litter born to older females, fewer pups per litter with increasing parity, and longer intervals between litters with increasing age.     

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.     

Delayed motherhood decreases life expectancy of mouse offspring

This study analyzes the long-term effects of delayed motherhood on reproductive fitness and life expectancy of offspring in the mouse. Hybrid (C57BL/6JIco x CBA/JIco) first-generation (F1) females, either at the age of 10 or 51 wk, were individually housed with a randomly selected 12- to 14-wk-old hybrid male following a breeding pen system until females reached the end of their reproductive life. Reproductive fitness of second-generation (F2) females was tested from the age of 25 wk until the end of their reproductive life. In F2 males, the testing period ranged from the age of 52 wk until their natural death. Delayed motherhood of hybrid F1 female mice was associated with a decreased percentage of male F3 offspring at birth and lower life expectancy and body weight during adulthood of F2 offspring. There was, however, no evident negative effect of delayed motherhood on several reproductive fitness variables in either male or female F2 offspring. This included between-parturition interval, litter size at birth and at weaning, body weight at weaning and preweaning mortality of F3 pups, percentage of F3 litters with at least one pup cannibalized, and time at which female and male F2 offspring ceased their reproductive life. These data clearly show that delayed motherhood in the mouse is associated with negative long-term effects on offspring survival.     

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.     

The effect of cage size on reproductive performance and behavior of C57BL/6 mice

Scientific research has yet to conclusively determine the optimal cage size for mice. The authors examined the effect of cage size on mouse breeding performance and on offspring behavior, which can serve as indications of overall well-being. They housed breeding trios of C57BL/6Tac mice in standard or large individually ventilated cages and measured four reproductive parameters: litter size; litter survival to weaning age; average pup weight at 7, 14 and 21 days; and the number of days between litter births. They investigated the behavior of a subset of male and female pups from parents housed in cages of each size in the elevated plus maze test, the open field assay and the acoustic startle test. Cage size had no significant effect on any of the reproductive parameters measured and few or inconsistent effects on behavior in weaned pups.     

Seasonal variation in fertility, fecundity and litter sex ratio in laboratory and wild stocks of house mice (Mus domesticus)

Data compilations were made for three parameters pertaining to reproduction in a domestic strain (14 years) and a wild stock (4 years) of commensal house mice: (a) the percentage of females mated that produced litters; (b) the average number of pups per litter; and (c) the sex ratio of the pups in the litters. Fecundity and fertility varied seasonally in both domestic and wild mice. More females become pregnant and litter sizes were larger in the spring, summer, and fall months than during the winter season. Sex ratios also varied seasonally with more male biased litters produced during the 4 winter months. There appear to be seasonal shifts in productivity for both stocks of mice and these seasonal trends have not been altered by domestication under laboratory conditions. In spite of the fact that house mice are generally opportunistic, it is possible that there has been selection in the mice for shifting rates of production in relation to the best seasons of the year in terms of climate and resource availability. The higher production of males during summer months may be geared toward greater success in dispersal at that season and a higher probability that the males can find a territory and mate successfully in summer rather than winter. These results have potential implications for animal breeders and for those who maintain mouse colonies to produce animals for scientific investigations.     

The colony structure and reproductive biology of the afrotropical Mashona mole-rat, Cryptomys darlingi

Cryptomys darlingi occurs in the mesic Miombo woodland of north-eastem Zimbabwe. It occurs in colonies of up to nine individuals, in which reproduction is limited to one of the largest males and the largest female in the colony.
Reproduction and details of colony size and number of breeding animals in a colony are described for five complete field-captured colonies.
In captivity, mating is not confined to a particular season, and up to three litters of pups are orn per annum. The reproductive female initiates the pre-copulatory behaviour. The gestation lengti is 56–61 days ( n = 2 ). The new-born pups are altricial and litter size is small = 1.7 ± 0.5 ( n = 6). In this case, the pups first left the nest 10 days after birth, began to eat solids when 14 days old, and were fully weaned at five weeks. They began to spar with each other when 36–40 days old, but did not disperse and were incorporated into the colony. This suggests that the Mashona mole-rat colonies are composed of a founding pair and at least three successive litters of pups.     

Short- and long-term effects of litter size manipulation in a small wild-derived rodent

Iteroparous organisms maximize their overall fitness by optimizing their reproductive effort over multiple reproductive events. Hence, changes in reproductive effort are expected to have both short- and long-term consequences on parents and their offspring. In laboratory rodents, manipulation of reproductive efforts during lactation has however revealed few short-term reproductive adjustments, suggesting that female laboratory rodents express maximal rather than optimal levels of reproductive investment as observed in semelparous organisms. Using a litter size manipulation (LSM) experiment in a small wild-derived rodent (the common vole; Microtus arvalis), we show that females altered their reproductive efforts in response to LSM, with females having higher metabolic rates and showing alternative body mass dynamics when rearing an enlarged rather than reduced litter. Those differences in female reproductive effort were nonetheless insufficient to fully match their pups’ energy demand, pups being lighter at weaning in enlarged litters. Interestingly, female reproductive effort changes had long-term consequences, with females that had previously reared an enlarged litter being lighter at the birth of their subsequent litter and producing lower quality pups. We discuss the significance of using wild-derived animals in studies of reproductive effort optimization.     

Reproductive lifespan and reproductive performance in SPF C3H mice: the onset of reproductive life and production efficiency (author's transl)]

To improve the production system, the onset and the termination of reproductive life of C3Hf/HeMsNrs mice mated immediately after weaning and reared for 400 days of life, were studied. From weaning females mated with a full grown male (group A), the first litter was obtained at a mean age of 47 days, suggesting the first copulation at 26 days of age. The age of males at the first copulation was estimated to be at 44 days of age from the age giving the first litters in weanling males mated with weanling (group B) and full grown (group C) females. The sex ratio of litters delivered by young dams tended to be excess in males. The reproductive performance of dams in later life was not affected by the parturition in earlier age. The production efficiency with weaned youngs per pair during the first 200 days after mating was the highest in group A. It was found from these results that the C3H females attained their sexual maturity at 5 to 6 days after weaning, being available for breeding without any deletion in reproductive performance.     

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.     

Kin Recognition and Maternal Care under Restricted Feeding in House Mice (Mus domesticus)

This study tests the hypothesis that female house mice (F1 generation of wild caught Mus domesticus) should preferentially invest in own offspring if confronted with young of different degrees of relatedness. The maternal behaviour of females with litters of 4 own and 4 unrelated alien young (cross-fostered at day 1 of lactation) was analysed during a lactation period of 22 days both under ad libitum and under restricted feeding (food was restricted by 20%). Cross-fostering and restricted feeding had no effect on the amount of time spent nursing until weaning. Under both feeding conditions the females did not differ in their maternal behaviour towards own and alien young: there were no significant differences either in the amount of time spent nursing own versus alien pups or in the time spent licking own versus alien young. Weight gain of own and alien = wild littermates did not differ significantly in mixed litters and was similar both under ad libitum and under restricted feeding. Such indiscriminate behaviour might be adaptive if female house mice prefer to communally nest with a relative and thus improve their inclusive fitness by investing in own and related offspring in a communal nest. Under moderate restricted feeding females could not wean the entire litter but reduced litter size by cannibalizing on average 2.7 pups (75% of the pups were killed when they were 4–8 days old). Females with cross-fostered litters killed as many own as alien young. This suggests that females cannot discriminate between own and unrelated young if cross-fostering takes place at day 1 of lactation. Besides testing kin recognition abilities, the experiments also allow analysis of the weaning strategy of females under food shortage. Under restricted feeding, body weight of the females was significantly lower during middle lactation than under ad libitum feeding. Weaning weight of young in reduced litters under food restriction (9–10 g) did not differ significantly from weaning weight of young in litters of 7–10 young, but was lower than that of young in similar sized litters (litter size 6), under ad libitum feeding. The maternal behaviour of cannibalizing some young under food shortage can be interpreted as a weaning strategy which results in the largest number of offspring that can be raised to a minimal weaning weight of 9–10 g. Such a weaning strategy might represent a favourable trade-off between number and size of young produced.     

Some characteristics of the XO mouse (Mus musculus L.) II. Reproduction: fertility and gametic segregation

A preliminary investigation of reproductive capacity in XO mice showed that they produced smaller litters than normal litter mates. More time elapsed between successive litters when kept in the presence of a male except during pregnancy and weaning. This lower level of reproduction is manifest during the whole reproductive period. Also reproductive capacity in XO mice reaches its maximum and minimum (end of reproductive period) earlier than in normals.Further study also demonstrated an underdevelopment of the ovaries-the whole ovary, as well as the numbers of maturing and mature follicles, are smaller in XO mice than in controls. Since these differences can be corrected by unilateral ovariectomy, they appear to be under control of extra-ovarial factors, e.g. of gonadotropic hormone(s). The data also suggest depression of activity in the oestrogen-producing system, and in general that the lower reproductivity of XO mice may be attributed to a diminished secretion of gonadotropic hormones together with a smaller number of primordial germ cells in XO mice.The segregation from XO parents seems to favor transmission of X-gametes in young mothers, with however the preference for X tending to decrease with parental age. Since the data tend to rule out postzygotic selection effects, the excess of X-bearing gametes may relate to meiotic drive.     

Oral administration of pharmacological doses of vitamins C and E reduces reproductive fitness and impairs the ovarian and uterine functions of female mice

This study aims to ascertain whether oral administration of pharmacological doses of Vitamins C and E has any detrimental effect on reproductive fitness of female mice. We fed hybrid female mice from the first day of weaning a standard diet supplemented or not supplemented with pharmacological doses of Vitamins C and E. At the age of 28 weeks, we individually caged females with a male for the rest of their reproductive life. We performed a series of mating experiments to ascertain the number of oocytes ovulated and the potential for embryo development in vitro to the blastocyst stage and in vivo to Day 12 of gestation. The antioxidant diet decreased the frequency of litters, litter size, total number of offspring born and survival of male pups to weaning. This effect was associated with lower number of corpora lutea in the left ovary, decreased percentage of viable fetuses, and higher number of fetal resorptions in the left uterine horn when compared to the control group. The strategy of supplementing the diet with antioxidant vitamins to prevent the age associated decrease in reproductive potential should not be implemented in human beings until a safe and efficient diet is designed.     

Reproduction of the bank vole, Clethrionomys glareolus, in northern and southern Sweden during several seasons and in different phases of the vole population cycle

The breeding biology of the bank vole was studied in northern and southern populations in Sweden in the years 1973–76. Trapped specimens supplied organ weights and histological data, which were utilized to describe the breeding season, number and size of litters, reproductive losses, spermatogenesis, and sexual maturation. In the north the populations are cyclic. During the increase phase of the cycle the breeding season was long, litter sizes and gonad weights were large, and there was maturation of yearlings in the summer. During the peak phase reproduction was impaired in all these respects. In southern Sweden there was no cyclicity, and the reproductive events varied less, but in 1976 the litters were larger than usual and the season was much extended.
In the south the voles born during the early part of the season regularly became sexually mature during their first summer. The differences in reproductive biology are related to population dynamics and discussed in terms of different hypotheses concerning vole population cyclicity.