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.     

Social suppression of female reproductive maturation and infanticidal behavior in cooperatively breeding Mongolian gerbils

In several cooperatively breeding species, reproductively suppressed, nonbreeding females are attracted to infants and routinely provide alloparental care, while breeding females may attack or kill other females' infants. The mechanisms underlying the transition from alloparental to infanticidal behavior are unknown. In this study, we tested the hypothesis that this transition is associated with cessation of reproductive suppression and onset of ovarian activity in the Mongolian gerbil (Meriones unguiculatus), a cooperatively breeding rodent. Young female gerbils were housed with their natal family (FH), with a female pairmate (PH) or singly (SH). When females were either 11-13 or 16-18 weeks of age, we characterized their behavioral responses to an unfamiliar pup, reproductive development, and plasma progesterone, cortisol, and prolactin concentrations. In both age groups, FH females were significantly less likely to attack pups than PH or SH females and in fact never did so. FH females also had smaller ovaries and uteri, less developed scent glands, and lower progesterone levels, and were more likely to be anovulatory than PH or SH females, especially in the 11- to 13-week-old age group. Prolactin concentrations did not differ with reproductive status but were significantly higher in females that did not attack pups than in those that did. We found no other significant associations, however, between reproductive or endocrine measures and behavioral responses to pups. These results suggest that cohabitation with the natal family inhibits both infanticidal behavior and reproductive maturation in young female gerbils but that these two effects may not be causally related.     

A Comparison of the Maternal Care of Females within Prairie Vole (Microtus ochrogaster) Communal Groups

Communal rearing, the shared rearing of offspring by multiple individuals or mothers, may improve the fitness of individuals in group‐living species. To date, many studies have focused on these potential fitness consequences. Fewer studies have emphasized the relative contributions to care of offspring by mothers and non‐breeding alloparents in singularly breeding groups (i.e., one female breeds) and mothers within plurally breeding groups (i.e., more than one female breeds). We compared the care provided by prairie vole (Microtus ochrogaster) mothers and alloparents in singularly breeding groups and mothers in plurally breeding groups. Subjects were littermate siblings in both types of social groups. Specifically, we quantified the amount of time that mothers and alloparents were away from pups during 6 h observational trials and the amount of time that females tactilely stimulated pups (licking and grooming) during 20 min trials. We also compared the quality of milk, measured as total solids, produced by mothers in plurally breeding groups. In singularly breeding groups, mothers spent significantly more time out of the nest but tactilely stimulated pups more than alloparents. In plurally breeding groups, focal mothers (i.e., the first mother to produce a litter) spent significantly more time out of the nest than second mothers (i.e., the second female to produce a litter) but licked and groomed pups an equal amount as second mothers. In plurally breeding groups, focal and second mothers produced milk with a similar concentration of total solids. These results suggest that communal rearing in groups is more beneficial to focal mothers than to other breeding or non‐breeding adult females. We discuss fitness‐based hypotheses that may explain the observed differences in the amount of care provided by mothers and alloparents.     

Social Behaviour and Cooperative Breeding in Arctic Foxes,Alopex lagopus (L.), in a Semi-natural Environment

Most canid species show cooperative breeding at least occasionally. The helper-at-the-den system, when extra adults serve as helpers by feeding and guarding the cubs of an alpha pair, has been observed but not studied in any detail in wild Arctic foxes (Alopex lagopus). During a 3-months study of arctic foxes in two enclosures of 4 ha each, we measured the social behaviour during the reproductive season. Older foxes dominated younger ones and males dominated females of the same age. A litter with one surviving cub was born in one enclosure. The alpha male increased his rate of urine marking and barking and fed the alpha female both before and after the birth of the litter. However, about 10 days after the birth, the alpha female died. The cub was fed by his putative father, his sister and his brother (both one year old). The one year old female increased her rate of territorial defence, measured as urine marking and barking, when the mother died. The subordinate females were probably suppressed from breeding by the high aggression levels and territorial defence of the dominant females in each enclosure. The dominant female in the second enclosure came into heat after the death of the alpha female (her mother) in the first enclosure. These changes in behaviour can probably be explained by sexual inhibition by the alpha female while she was present. The significance of territorial defence and dominance, inbreeding avoidance, sexual suppression and evolution of helping behaviour are discussed.     

Maternal investment during pregnancy in wild meerkats

Maternal investment in offspring development is a major determinant of the survival and future reproductive success of both the mother and her young. Mothers might therefore be expected to adjust their investment according to ecological conditions in order to maximise their lifetime fitness. In cooperatively breeding species, where helpers assist breeders with offspring care, the size of the group may also influence maternal investment strategies because the costs of reproduction are shared between breeders and helpers. Here, we use longitudinal records of body mass and life history traits from a wild population of meerkats (Suricata suricatta) to explore the pattern of growth in pregnant females and investigate how the rate of growth varies with characteristics of the litter, environmental conditions, maternal traits and group size. Gestational growth was slight during the first half of pregnancy but was marked and linear from the midpoint of gestation until birth. The rate of gestational growth in the second half of pregnancy increased with litter size, maternal age and body mass, and was higher for litters conceived during the peak of the breeding season when it is hot and wet. Gestational growth rate was lower in larger groups, especially when litter size was small. These results suggest that there are ecological and physiological constraints on gestational growth in meerkats, and that females may also be able to strategically adjust their prenatal investment in offspring according to the likely fitness costs and benefits of a particular breeding attempt. Mothers in larger groups may benefit from reducing their investment because having more helpers might allow them to lower reproductive costs without decreasing breeding success.     

Optimal allocation of reproductive effort: manipulation of offspring number and size in the bank vole

The number of offspring attaining reproductive age is an important measure of an individual's fitness. However, reproductive success is generally constrained by a trade-off between offspring number and quality. We conducted a factorial experiment in order to study the effects of an artificial enlargement of offspring number and size on the reproductive success of female bank voles (Clethrionomys glareolus). We also studied the effects of the manipulations on growth, survival and reproductive success of the offspring. Potentially confounding effects of varying maternal quality were avoided by cross-fostering. Our results showed that the number of offspring alive in the next breeding season was higher in offspring number manipulation groups, despite their smaller body size at weaning. Offspring size manipulation had no effect on offspring growth or survival. Further, the first litter size of female offspring did not differ between treatments. In conclusion, females may be able to increase the number of offspring reaching reproductive age by producing larger litters, whereas increasing offspring size benefits neither the mother nor the offspring.     

高寒草甸生态系统中高原鼠兔的繁殖特征

2002年4月至8月,在中国科学院海北高寒草甸生态系统定位站附近,采用标志重捕法对高原鼠免的繁殖特征进行了研究。高原鼠兔的繁殖具有明显的季节性差异,4月下旬和5月为繁殖高峰期,雄性的睾丸重而饱满,雌性的怀孕率最大。雄性成体的体重和睾丸重在繁殖期的不同时段具有显的差异,在4月11日至5月10日、6月11日至7月10日体重和睾丸重之间呈显正相关。雌性怀孕早期胚胎数与临产前胚胎数没有显差异,未发现胚胎吸收现象;同时,胚胎数在繁殖期的不同时段存在显差异。采用种群统计学中同生群的划分方法,将5～8月份出生的幼体依次记为L1、L2、L3、L4。在出生后20天内L1、L2幼体存活率明显高于L3、L4;在从出生50天至80天期间L4的存活率显高于L2。当年出生的雌雄幼体在发育上存在不同步现象,当年出生的雌性幼体性成熟早,有的可以直接参加繁殖,但当年出生的雄性幼体却无此现象。结果表明：在海北地区,经过综合治理后,高原鼠兔的生境发生改变,其繁殖策略也随之发生改变,即,减少每次繁殖活动的投入,增加繁殖次数,延长繁殖时间。     

Effect of polygyny on female reproductive success in the mandarin vole, <Emphasis Type="Italic">Microtus mandarinus</Emphasis> (Rodentia,Arvicolinae)

Indices of reproductive success were compared in monogamous and polygynous groups (MGs and PGs) of female mandarin voles kept under different laboratory conditions: in small cages, with frequent handling disturbance (30 MGs and 15 PGs), and in large glass tunnel systems, without disturbance (20 MGs and 16 PGs). MGs consisted of unrelated male-female pairs, and PGs consisted of two female sibs and an unrelated male each. No reproductive skew was observed within PGs; moreover, there was a positive correlation between the sibling females in the presence/absence of offspring, its total size, and the number of litters produced over 90 days. Regardless of keeping conditions, the proportion of parous females recorded over 45 days and the number of successfully reared offspring per female were greater in MGs than in PGs. Among groups kept in cages, reproductive success in PGs was lower because of a delay in breeding, reduced size of the first litter, and increased pup mortality during the first days of life. Observations on voles in tunnel systems were performed to quantify aggressive interactions and reveal the causes of pup mortality. In general, the level of aggression in both types of groups was low, but the frequency of female-female conflicts in PGs drastically increased during several days before and after the birth of the litter. Nevertheless, the sibling females in PGs used the common breeding nest and regularly fed reach other’s offspring. The causes of high pup mortality in PGs and probable advantages of communal breeding in mandarin voles are discussed.     

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.     

Trophic egg laying in the spider, Amaurobius ferox: mother-offspring interactions and functional value

Offspring of the spider Amaurobius ferox (Araneae, Amaurobiidae) were provided with trophic eggs of their mother the day after their emergence from the egg sac. This precisely timed egg laying followed after a series of mother-offspring interactions involving specific behaviors. Experiments showed that the trophic egg laying of the mother (providing she is in the appropriate reproductive condition) necessitated not only their presence, but also the stimulating behavior of the spiderlings. By stimulating their mother the spiderlings actually inhibited the normal maturation of the second generation of maternal eggs and prompted the release. Comparing to the trophic egg-deprived clutches, the clutches provided with the trophic eggs developed with higher body mass, earlier moulting and matriphagy. More offspring survived at the matriphagy with the mother normally provisioning the first clutch with trophic eggs rather than with the mother that did not produced the trophic eggs for her first clutch but for her second clutch. By turning her potential second generation into food, the mother increases her reproductive success.     

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.     

Reproductive performance of otters Lutra lutra (Linnaeus, 1758) in Eastern Germany: low reproduction in a long-term strategy

The reproductive status of female otters ( Lutra lutra ) was determined from an examination of 518 carcasses collected from Eastern Germany between 1950 and 2001. In Germany otters mate throughout the year. Significant seasonal differences are evident with a distinct peak in summer. Females were in breeding condition between the ages of three and 15 years, with the majority between six and nine years. The mean litter size at birth was 2.36, which was the lowest when compared with other inland populations. There were no significant differences in litter size for regions, seasons or age. Prenatal losses account for 26.31%. The mortality between birth and first appearance of cubs following their mother is about 29%. An effective reproduction rate of 78.4% was deduced from the known age structure of the sample and the proportion of breeding females. Reproductively active females show a significantly higher body condition than non-reproductive females. Following these investigations into breeding status, suggestions on reproductive output and the life history of the otter are discussed.  © 2002 The Linnean Society of London, Biological Journal of the Linnean Society , 2002, 77 , 329–340.     

Behavioral and physiological suppression of fertility in subordinate marmoset monkeys

In laboratory groups of common marmosets (Callithrix jacchus jacchus), socially induced reproductive suppression among subordinates and offspring effectively maintained a monogamous breeding system. Male subordinates or male offspring were inhibited or restrained from showing sexual behavior, while similarly placed females could also suffer from complete ovarian failure. In well-established families, a familiarity or inbreeding taboo restricted reproduction among otherwise fertile offspring. However, only one daughter ovulated in any family, and in up to 50% of family groups, all daughters were inhibited from ovulating. This differential effect on daughters may have reflected a qualitative shift in the mother-daughter relationship: the ovulating daughter may have represented the next breeding female and may no longer have regarded the mother as an inhibitory influence. In newly established peer groups of pubertal and postpubertal offspring, one male and female dominated all others in each group and overtly inhibited sexual behavior in subordinates of their own sex. Ovulation was suppressed in all subordinate females because of inadequate gonadotrophin secretion. This was not related to increased secretion of cortisol or prolactin, but may have been related to hypothalamic inhibition of luteinizing hormone-releasing hormone (LHRH) secretion.     

北京大兴地区黑线仓鼠种群繁殖生态研究

黑线仓鼠(Cricetulus barabensis)是我国华北地区广泛分布的农田主要害鼠之一。1982年9月到1985年3月,作者在北京、天津及河北省一些地区,调查了它的分布和群落结构并研究其种群生态,本文仅就北京郊区大兴县黑线仓鼠的种群繁殖问题进行讨论。     

Post-conception reproductive competition in cooperatively breeding common marmosets

Common marmosets are cooperatively breeding monkeys that exhibit high female reproductive skew. Subordinate females usually fail to breed as a consequence of ovulation suppression and inhibition of sexual behavior, and, even when they do breed, typically rear fewer infants than dominants. We evaluated possible mechanisms of post-conception reproductive competition by comparing hormonal profiles across pregnancy, pregnancy outcomes, infant survivorship, and behavior in laboratory-housed families containing one (N=9) or two (N=7) breeding females. Breeding females in plurally breeding groups did not exhibit well-defined dominance relationships and rarely engaged in escalated aggression with one another. No significant differences were found among singly breeding mothers, plurally breeding mothers, and plurally breeding daughters in urinary chorionic gonadotropin or estradiol sulfate concentrations during pregnancy, fetal biparietal diameter, frequency of spontaneous abortion, frequency of stillbirths, number of live-born infants per litter, or infant mortality rates. When females gave birth while another female in the family was pregnant, however, their infants were highly likely to be killed. The perpetrator was definitively identified in only one family, in which a pregnant female killed her daughter's infant. These results are consistent with observations of free-living common marmosets and suggest that breeding females do not regularly influence one another's pregnancy outcomes, but that they may commonly kill each other's infants, especially during their own pregnancy. Our findings further suggest that infanticide by breeding females may have selected for the evolution of reproductive restraint in subordinate female marmosets.     

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     

Socially controlled growth and size-dependent sex change in the anemonefishAmphiprion frenatus in Okinawa,Japan

Social structure, growth and reproductive experience of a protandrous anemonefish,Amphiprion frenatus, were investigated on a coral reef in Okinawa, Japan. In a 67 m × 334 m study area, 24 breeding groups, 10 nonbreeding groups and 2 groups of unknown breeding experience were found around isolated sea anemones. One group usually consisted of 2 or 3 fish. The female in a breeding group was larger than not only her mate but also all males in other breeding groups. The body size and gonadal state of the largest individual in a nonbreeding group were intermediate between the female and male in a breeding group. In both breeding and nonbreeding groups, the largest fish retarded growth of the second largest. After the disappearance or removal of females, their mates took more than 1.5 years to attain the minimum functional female size (about 75 mm in standard length). This delayed sex change can be attributed to strong growth suppression by the female.     

Reproduction and spacing behaviour of females in a peak density population of Clethrionomys glareolus

A peak density population of Clethrionomys glareolus was studied by snap-trapping to determine by experimentation whether spacing behaviour regulated the breeding density. On control plots onset of reproduction was asynchronous, litter size of overwintered females decreased significantly during the summer and no year-born animals matured during the reproductive period. A removal experiment in the early summer resulted in sexual maturation of year-born females. A second removal in late summer indicated an inhibition of maturation in year-born females despite continued intense reproduction of overwintered females. We conclude that spacing behaviour regulated maturation of females early in the summer but other factors, such as food quality, limited maturation in late summer.     

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.     

Reproductive biology of captive male cottontop tamarin monkeys as a function of social environment

The cottontop tamarin, Saguinus oedipus oedipus, is a cooperatively breeding monkey in which mature male and female offspring serve as helpers to assist in rearing younger siblings. Generally, only one female per social group reproduces; breeding restriction is mediated in postpubertal female offspring through low and acyclic levels of reproductive hormones. We investigated (1) reproductive activity of postpubertal male offspring, and (2) whether aggression towards male offspring and a cortisol-mediated stress response might restrict breeding of male offspring in the natal group. We examined sexual behaviour, olfactory communication and urinary hormone levels (testosterone, dihydrotestosterone, luteinizing hormone, cortisol) of the subject males while we manipulated their social environment from housing in natal groups to pairing with a novel female, and after the production of their own offspring. Mounting and erection rates of the male subjects were as high in the natal group as when paired with a novel female. However, most mounts in the natal group were directed towards other males, and complete copulation sequences did not occur with natal-group females. Social environment had no significant effect on olfactory investigation of breeding females. Although hormone levels increased significantly after the subjects were removed from the natal group, the elevation was transient; the hormone levels of subjects in their natal groups did not differ from the levels shown by the same males when successfully producing their own offspring. Male offspring received more contact aggression in the natal group than when paired with the novel female. However, most of the aggression was received from siblings rather than the breeding pair, and levels of cortisol did not correspond with levels of aggression. Thus, at both a behavioural and endocrine level, mature male offspring in captive natal groups were potentially fertile, but sexual activity with natal-group females appeared to be behaviourally restricted and directed instead towards group males. In wild cottontop tamarin groups, this reproductive potential may allow male helpers flexibility to respond to breeding opportunities. Copyright 2001 The Association for the Study of Animal Behaviour.